Skip to main content
NCBI home page
Journal of Insect Science logoLink to Journal of Insect Science
. 2023 Sep 18;23(5):3. doi: 10.1093/jisesa/iead015

Native natural enemies of plant pests in Slovenia with an emphasis on species suitable for mass rearing

Stanislav Trdan 1, Žiga Laznik 2, Tanja Bohinc 3,✉
Editor: Muhammad Chaudhury
PMCID: PMC10506447  PMID: 37721494

Abstract

In Slovenia, only the native natural enemies of plant pests that are on the EPPO Positive List of biological control agents can be used in agricultural production to control plant pests. The List of native species of organisms for biological control, which is an important part of the Regulations on biological control, currently includes a total of 35 species of beneficial insects and mites and entomopathogenic nematodes. Compared to the number of species on the first list that was established in 2006, the number of beneficial species that Slovenian growers of food and ornamental plants can currently use in everyday practice has doubled. This is the result of intensive professional and research work in the investigation of the occurrence and distribution of natural enemy species in Slovenia, which has been systematically supported by the state for many years. Natural enemy species, which are an integral part of the EPPO Positive List of biological control agents, can be included on the list of native biological control species via a special procedure. However, many natural enemy species that are not yet included on the EPPO Positive List have been identified in the period 2007–2022. In this paper, we list 75 such species and we present 5 candidates (Cotesia glomerata [L.], Diadegma semiclausum [Hellen], Anisopteromalus calandrae [Howard], Neochrysocharis formosa [Westwood] and Kampimodromus aberrans [Oudemans]) that, in our opinion, have high potential as biological controls and will be suitable in the future for mass rearing and use in augmentative biological control.

Keywords: biological control, EPPO Positive List, candidate

Introduction

The production and consumption of safe food are increasingly important to the public not only in the developed world but also in developing countries (Carvalho 2017). As a result, the use of agrochemicals, especially chemical pesticides, herbicides, and fertilizers, is being restricted at various levels, with the desire to reduce their impact on nontarget organisms in the environment and to reduce residues in food, soil, and groundwater (Grant and Blicher-Mathiesen 2004, Klatt et al. 2016). Biological control techniques are therefore gaining importance worldwide and represent one of the most appropriate alternatives to the chemical protection of plants (van Lenteren 2000, Crowder 2007, Trdan et al. 2020).

The European and Mediterranean Plant Protection Organization (EPPO) is an intergovernmental organization responsible for European–Mediterranean regional cooperation in protecting plant health. Its objectives are to protect plants by developing international strategies against the introduction and spread of pests that are a threat to agriculture, forestry, and the environment and by promoting safe and effective pest control methods (EPPO 2023). Among the various activities in the field of biological control, the development and expansion of the EPPO Positive List are probably the most well-known (Orlinski 2016). The EPPO Positive List presents the BCAs used in the EPPO region to support EPPO member countries when making decisions concerning the release of BCAs. The EPPO Positive List currently recognizes 141 species of beneficial organisms. The list is subject to review and may change based on new information whereby a listed BCA may no longer fulfill the criteria to be included in the Positive List (EPPO 2021).

In accordance with the national biological plant protection regulations of countries from the EPPO area, countries may take into account the recommendations of the EPPO. Slovenia, which in 2006 implemented the Regulations on biological control (Official Gazette of the Republic of Slovenia, 2006, no. 45/06), decided to further categorize the organisms from the EPPO Positive List into ‘native’ and ‘nonnative’, with only the use of organisms in the ‘native’ category being allowed in plant production within the territory of Slovenia. The lists of native and nonnative biological control species are therefore very important components of the Regulations on biological control from the start. The expansion (upgrading) of the list of native biological control species directly depends on the scope of research, technical, or scientific articles or other official evidence of the occurrence of beneficial organisms deemed native in the territory of Slovenia (Mavsar and Trdan 2015). Because of this, the practical use of beneficial organisms in the control of plant pests in Slovenia is subject to much stricter criteria than in most EPPO countries.

Currently, the Slovenian list of native biological control species includes 35 species, namely, 23 predators, 8 parasitoids, and 4 entomopathogenic nematodes (Ministry of Agriculture, Forestry and Food RS 2023). With the aim of increasing the number of species on this list, researchers at the Department of Agronomy of Biotechnical Faculty have been systematically studying the distribution of beneficial organisms in Slovenia on various cultivated and wild plants since 2007. When studying the occurrence, in addition to the species from the EPPO Positive List, we found many other species that are not yet an integral part of this list; therefore, their inclusion among the options from the list of native biological control species has not been possible. However, since the EPPO Positive List is a living list and is updated once a year, usually expanding by at least one species, research findings concerning currently ‘uninteresting’ species of natural plant pest enemies in Slovenia may have practical significance in the future.

To that end, in this paper, we present the natural plant pest enemies whose presence in Slovenia we confirmed during the period from 2007 to 2022. Based on the needs of Slovenian and European agriculture, we recommend in this paper which species would be suitable for mass rearing and use in biological control.

Materials and Methods Used in the Different Studies

Sampling Sites and Methods

The occurrence of predators, parasitoids, and entomopathogenic nematodes was investigated during the period from 2007 to 2022 in various parts of Slovenia. Specifically, for a clearer geographical definition of the locations, we focused on five areas (western Slovenia, central Slovenia, SE Slovenia, Štajerska and Koroška, and NE Slovenia) that represent areas of activity of the public plant protection service in Slovenia. Samples of natural enemies on various cultivated and wild-growing plants were not collected according to a pre-prepared program, but several times completely randomly, when we also performed other professional or research activities at the sampling locations. Therefore, the data (species of natural enemies) presented in the tables cannot be analyzed even with a simple statistical analysis, since in all cases they represent the first records of natural enemies in Slovenia.

Sampling of Parasitoid Wasps

Several insects at immature stages (the vast majority were in the parasitized hosts) were collected on cultivated and noncultivated plants across Slovenia and placed in insectariums in the Laboratory for whytomedicine of the Biotechnical Faculty in Ljubljana. Immature stages of insects were transported by using plastic bags and cooling bags. Rearing of insects (we did not feed them additionally) was performed at room temperature (20 ± 2°C) for 10–14 days from the day of sampling in the field. When parasitoids emerged, they were stored in 70% ethanol (Tomanović et al. 2022) for morphological identification and 100% ethanol for molecular identification. Molecular identification was only performed for Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) according to the methods previously described by Ivezić et al. (2020).

Sampling of Predatory Mites

Between 2012 and 2019, plant-inhibiting mites were collected from cultivated and uncultivated areas in all parts of the country. As previously described by Kreiter et al. (2020), mites were directly collected from leaves with a fine brush by using the leaf ‘dipping-shaking-washing-filtering’ method or by tapping the plants and collecting the mites that fell off in a black plastic rectangular tray of 45 × 30 cm dimensions.

Sampling of Predatory Bugs (Anthocoridae and Miridae) and Predatory Beetles

Sampling of predatory bugs and predatory beetles was performed by hand picking with ethanol and brushes in the area of sampling (Musser et al. 2004). As already mentioned by Shipp and Zariffa (1991), blossom sampling was the best sampling method for monitoring the population density of Orius species (Hemiptera: Anthocoridae).

Sampling of Entomopathogenic and Parasitic Nematodes

Isolation of entomopathogenic nematodes from soil was performed by standard extraction techniques, as described by Laznik and Trdan (2011). Each sample was combined from three samples taken at a depth of 3–15 cm/20 m2. After soil samples were prepared, we used a common baiting technique, i.e., the technique of baiting with larvae of Galleria mellonella (L.) (Lepidoptera: Pyralidae), as described by Laznik and Trdan (2011). The greater wax moth larvae were reared in the laboratory. The detailed procedure for the isolation of nematode parasites of mollusks is described by Laznik et al. (2021, 2022). Arion vulgaris Moquin-Tandon (Stylommatophora: Arionidae) specimens were individually dissected alive, and nematodes recovered from the host body cavity were placed into a tube containing ethanol for molecular analysis.

Identification of Beneficial Species

The identification of several detected beneficial species was performed by scientists listed in Trdan and Bohinc (2016), and the identification of other natural plant pest enemies was performed by experts from different foreign laboratories. For the identification of Ichneumonidae family parasitoids, Dr. Kees Zwakhals (Dr. Dreeslaan, CM Arkel, The Netherlands) participated, and Dr. Peter Neerup Buhl (Tärsvej 33, DK-4990, Saskøbibg, Denmark) participated in the identification of the parasitoids from the family Platygastridae, while Dr. Volker Assing (Gabelsbergerstrasse 2, Hannover, Germany) participated in the identification of the predatory beetles from the family Staphylinidae. Prof. Željko Tomanović (Biological Faculty in Belgrade) performed the identification of aphid parasitoids, Dr. Stefan Schmidt (Zoologishe Staatssamlung, München, Germany) participated in the identification of parasitoids from the family Figitidae, and Dr. Andrej Gogala from the Slovenian Museum of Natural History and Aleksandar Stojanović from the Natural History Museum in Belgrade participated in the identification of predatory bug (Anthocoridae and Miridae) species. The identification of predatory mites was carried out at the Centre for Biology and Management of Populations in Montpellier, France under the guidance of Dr. Serge Kreiter. Dr. Mark R. Shaw (Natural Museums of Scotland) participated in the identification of the parasitoid wasp of the cabbage butterfly (Cotesia glomerata [L.] [Hymenoptera: Braconidae]). Dr. Paul Rugman-Jones (the University of California, United States of America) participated in the identification of Trichogramma brassicae. Mite species from the family Parasitidae were performed by Maria Lourdes Moraza Zorilla from the University of Navarra, Pamplona, Spain. Molecular characterization of entomopathogenic nematodes was sequenced in the Laboratory of the Agricultural Biotechnology Centre in Gődőllo, Hungary. For morphological characterization of parasitic nematodes, the nematodes were mounted on temporary microscope slides, covered with coverslips, and viewed using a compound microscope (Leica DM200, Leica Microsystem, Wetzlar, Germany). For DNA extraction, individual nematodes were added to 0.2 ml PCR tubes containing a mix of Chelex/Proteinase and underwent polymerase chain reaction of the small subunit rRNA gene, the D2-D3 large subunit rRNA gene, the Internal Transcriber Spacer rRNA gene, and the mitochondrial cytochrome c oxidase subunit I gene. Identification of Oligota oviformis Casey (Coleoptera: Staphylinidae) was performed by using identification keys (Kos and Celar 2018).

Results From the Different Studies

Table 1 lists 35 species of natural plant pest enemies, namely, 23 predators, 8 parasitoids, and 4 entomopathogenic nematodes, whose occurrence in Slovenia has been confirmed by research or professional work (Trdan et al. 2020). The target pests (prey/hosts of the natural enemies) and the place of use of the natural enemies are summarized according to the standard PM 6/3 (5) Biological control agents safely used in the EPPO region (EPPO 2021).

Table 1.

List of native biological control species (last change 29 August 2022) – Regulations on biological control (Official Gazette of the Republic of Slovenia, no. 45/06)

Beneficial organism Target pest(s) Use (greenhouse/Open field)
Adalia bipunctata (L.) Aphididae Greenhouse
Aeolothrips intermedius Bagnall Acarina, Thysanoptera Open field
Amblyseius andersoni (Chant) Tetranychus urticae Koch, Aculus schlechtendali (Nalepa), Panonychus ulmi (Koch), Aculops lycopersici (Tryon), Thysanoptera Greenhouse/Open field
Amblyseius barkeri (Hughes) Thysanoptera (Thrips tabaci) Lindeman, Frankliniella occidentalis (Pergande), Tarsonemidae Greenhouse
Anastatus bifasciatus (Geoffroy) Heteroptera (Halyomorpha halys [Stål]) Open field
Anthocoris nemoralis (Fabricius) Psyllidae Open field (orchards)
Anthocoris nemorum (L.) Caccopsylla pyri (L.), Thysanoptera Open field
Aphelinus mali (Haldeman) Eriosoma lanigerum (Hausmann) Open field
Aphidius ervi Haliday Aulacorthum solani Kaltenbach, Macrosiphum euphorbiae (Thomas), and other Aphididae species Greenhouse/Open field
Aphidius matricariae Haliday Myzus persicae Sulzer Greenhouse/Open field
Aphidoletes aphidimyza (Rondani) Aphididae (Aphis gossypii Glover, Myzus persicae, Macrosiphum sp., Aulacorthum sp.) Greenhouse/Open field
Chrysoperla carnea (Stephens) Aphididae Greenhouse/Open field
Coccinella septempunctata L. Aphididae Open field
Diglyphus isaea (Walker) Agromyzidae (Liriomyza spp.) Greenhouse/Open field
Encarsia formosa Gahan Aleyrodidae (Trialeurodes vaporariorum [Westwood]), Bemisia tabaci (Gennadius) Greenhouse
Episyrphus balteatus (De Geer) Aphididae Greenhouse/Open field
Eupeodes corollae (Fabricius) Aphididae, Aleyrodidae, Thysanoptera, Pseudococcidae, Arachnida Greenhouse/Open field
Euseius gallicus Kreiter & Tixier whiteflies (Aleyrodidae) and thrips (Thysanoptera) Greenhouse
Exochomus quadripustulatus L. Adelgidae, Coccoidea, Aphididae Greenhouse/Open field
Feltiella acarisuga (Vallot) Tetranychus urticae Greenhouse
Heterorhabditis bacteriophora Poinar Coleoptera, Diptera, Lepidoptera Greenhouse/Open field
Macrolophus pygmaeus (Rambur) Aleyrodidae Greenhouse
Micromus angulatus (Stephens) Aphididae Greenhouse/Open field
Neoseiulus californicus (McGregor) Tetranychidae Greenhouse/Open field
Neoseiulus cucumeris (Oudemans) Thysanoptera (Thrips tabaci, Frankliniella occidentalis) Greenhouse/Open field
Orius majusculus (Reuter) Thripidae (Frankliniella occidentalis, Thrips tabaci) Greenhouse/Open field
Picromerus bidens (L.) Lepidoptera Greenhouse/Open field
Praon volucre (Haliday) Aphididae Greenhouse
Propylea quatuordecimpunctata (L.) Aphididae Greenhouse/Open field
Sphaerophoria rueppellii (Wiedemann) Aphididae, Thripidae, Acarina, Aleyrodidae Greenhouse/Open field
Steinernema carpocapsae (Weiser) Otiorhynchus spp., Sciaridae, soil insects Greenhouse/Open field
Steinernema feltiae (Filipjev) Melolonthidae, Sciaridae etc. Greenhouse/Open field
Steinernema kraussei (Steiner) Otiorhynchus sulcatus (F.) and other Otiorhynchus and Coleoptera species Greenhouse/Open field
Trissolcus basalis (Wollaston) Heteroptera (Nezara viridula [L.], Halyomorpha halys) Greenhouse/Open field
Typhlodromus pyri Scheuten Epitrimerus vitis (Nalepa), Panonychus ulmi, Tetranychus urticae, Eriophyes vitis (Pagenstecher) Open field
Open in a new tab

Table 2 presents predatory species recorded on different vegetable species. In terms of species, this is the fourth largest group of natural enemies in the contribution. Eight predatory species were sampled from vegetables in the greenhouses, while 3 species originated from plants in the open field. Among the 11 species, we found 3 species from the family Anthocoridae, order Hemiptera (Orius minutus [L.], Orius niger [Wolff], Orius horvathi [Reuter]) and one species from the family Miridae. Four species belonged to the family Phytoseiidae and two belonged to the family Staphylinidae, while Parasitus fimetorum (Berlese) (Acarida: Parasitidae) was the only representative of the family Macrochelidae. The majority of the novel beneficial organisms fed on two-spotted spider mites as prey.

Table 2.

List of predators recorded on vegetable crops during the period from 2013 to 2020

Beneficial Family Prey Host plant 1st record (location/GPS) Greenhouse (G)/Open field (OF) SI region 1st record (yr) Reference
Cydnodromus californicus Athias-Henriot 1977 Phytoseiidae Tetranychus urticae Koch, 1836 Solanum melongena Bukovica -Volčja Draga (45.901359, 13.658493) G Western 2018 Kreiter et al. 2020
Holobus flavicornis (Boisduval & Lacordarie, 1835) Staphylinidae Tetranychus urticae Koch, 1836 Solanum melongena Ljubljana (46.047840, 14.473996) G Central 2014 Trdan and Bohinc 2016
Macrolophus rubi Woodroffe, 1957 Miridae Tetranychus urticae Koch, 1836, Tuta absoluta (Meyrick, 1917) Solanum lycopersicum Dragonja (45.467969, 13.610327) G Western 2013 Trdan and Bohinc 2016
Oligota oviformis Casey, 1893 Staphylinidae Tetranychus urticae Koch, 1836 Solanum melongena Ljubljana (46.047840, 14.473995) G Central 2017 Kos and Celar 2018
Orius minutus (Linnaeus, 1758) Anthocoridae Thrips, mites, and aphids Solanum melongena Ljubljana (46.047840, 14.473995) G Central 2014 Trdan et al. 2015
Orius niger (Wolff, 1811) Anthocoridae Tetranychus urticae Koch, 1836 Capsicum annum Korte (45.486948, 13.656318) OF Western 2016 Trdan et al. 2017
Orius horvathi (Reuter, 1884) Anthocoridae Tetranychus urticae Koch, 1836 Cucumis sativus Grabrovec (45.681514, 15.306066) OF South-Eastern 2018 Trdan et al. 2019
Parasitus fimetorum (Berlese, 1904) Parasitidae Root knot nematode Dactuca sativa Zgornja Lipnica (46.322055, 14.185942) OF Central 2020 Trdan et al. 2021
Phytoseiulus persimilis Athias-Henriot, 1957 Phytoseiidae Tetranychus urticae Koch, 1836 Cucumis saticus Sečovlje (45.471054, 13.599258) G Western 2018 Kreiter et al. 2020
Proprioseiopsis bordjelaini Athias-Henriot Phytoseiidae Tetranychus urticae Koch, 1836 Cucumis sativus Straža (45.917733, 15.416631) G South-Eastern 2018 Kreiter et al. 2020
Typhlodromips driggeri Phytoseiidae Tetranychus urticae Koch, 1836 Cucumis sativus Straža (45.917733, 15.416631) G South-Eastern 2018 Kreiter et al. 2020
Open in a new tab

Among 9 newly recorded species of parasitoids found on vegetable crops, 3 species were from the family Scelionidae, which is a commonly known family of parasitoids that attack stink bugs (Saunders et al. 2022). Almost 80% of the parasitoid species were found on cabbage plants. Only two species were found in greenhouses. Details are presented in Table 3.

Table 3.

List of parasitoids recorded on vegetable crops during the period from 2012 to 2022

Beneficial Family Prey Host plant 1st record (location/GPS) Greenhouse (G)/open field (OF) SI region 1st record (yr) Reference
Copidosoma floridanum (Ashmead, 1900) Encyrtidae Autographa gamma (Linnaeus, 1758) Brassica oleracea Logatec (45.930939, 14.221625) OF Central 2021 Trdan et al. 2022
Cotesia glomerata (Linnaeus,1758) Braconidae Pieris brassicae (Linnaeus, 1758) Brassica oleracea Zgornja Lipnica (46.322055, 14.185942), Ljubljana (46.322055, 14.185942) OF Central 2014 Trdan and Bohinc 2016
Diadema semiclausum (Hellen, 1949) Ichneumonidae Plutella xylostella (Linnaeus, 1758) Brassica oleracea Zgornja Lipnica (46.322055, 14.185942) OF Central 2014 Trdan and Bohinc 2016
Hyposoter ebeninus (Gravenhorst, 1829) Ichneumonidae Plutella xylostella (Linnaeus, 1758) Brassica oleracea Ljubljana Savlje (46.096175, 14.505316) OF Central 2020 Trdan et al. 2021
Neochrysocharis formosa (Westwood, 1833) Eulophidae Liriomyza sp. Mik, 1894 Solanum lycopersicum Sečovlje (45.474196, 13.621523) G Western 2012 Trdan and Bohinc 2016
Pnigalio spp. Schrank, 1802 Eulophidae Tuta absoluta (Meyrick, 1917) Solanum lycopersicum Dragonja (45.462872, 13.630877) G Western 2013 Trdan and Bohinc 2016
Trissolcus festivae (Viktorov, 1964) Scelionidae Eurydema ventralis Kolenati, 1846 Brassica oleracea Zgornja Lipnica (46.322055, 14.185942) OF Central 2014 Trdan and Bohinc 2016
Trissolcus scutellaris (Thomson, 1861) Scelionidae Eurydema ventralis Kolenati, 1846 Brassica oleracea Škocjan (45.539396, 13.764718) OF Western 2021 Trdan et al. 2022
Trissolcus viktorovi Kozlov, 1968 Scelionidae Eurydema ventralis Kolenati, 1846 Brassica oleracea Orehovlje (45.89264, 13.61065), Vrtojba (45.9072040, 13.6172590) OF Western 2022 Trdan et al. 2023
Open in a new tab

Among the parasitoids recorded, 2 species were recorded in storage facilities, 2 species were recorded in fields with Brassica napus L. (Brassicales: Brassicaceae), and one egg parasitoid was recorded on maize plants. Details are presented in Table 4.

Table 4.

List of parasitoids recorded on field crops/grains during the period from 2012 to 2021

Beneficial Family Prey Host plant 1st record (location/GPS) Storage facility (SF)/Open field (OF) SI region 1st record (yr) Reference
Anisopteromalus calandrae (Howard, 1881) Pteromalidae Sitophilus spp. Wheat grain Ljubljana (46.047840, 14.473995) SF Central 2014 Trdan and Bohinc 2016
Dibrachys microgastri (Bouché, 1834) Pteromalidae Sitophilus spp. Wheat grain Ljubljana (46.047840, 14.473995) SF Central 2012 Trdan and Bohinc 2016
Mesopolobus morys (Walker, 1848) Pteromalidae Ceutorhynchus spp. Brassica napus Lenart (46.581479, 15.817844) OF North-Eastern 2016 Trdan et al. 2017
Tersilochus heterocerus (Thompon, 1889) Ichneumonidae Meligethes aeneus Brassica napus Komenda (46.203327, 14.533564) OF Central 2014 Trdan and Bohinc 2016
Trichogramma brassicae Bezdenko, 1968 Trichogrammatidae Ostrinia nubilalis Zea mays Cerklje ob Krki (45.88279, 15.50805) OF South-Eastern 2021 Trdan et al. 2022
Open in a new tab

Seventeen predatory mite species that were recorded in orchards during the period from 2003 to 2019 are presented in Table 5. According to the number of species, this is the largest group of natural enemies in the contribution. Sampling was mainly performed on Malus domestica Borkh. (Rosales: Rosaceae) trees but also on Prunus cerasus L. (Rosales: Rosaceae), Fragaria sp. (Rosales: Rosaceae) and Rubus fruticosus L. (Rosales: Rosaceae) plants. The majority of the species were recorded in open fields, with only two species originating from the greenhouse.

Table 5.

List of predatory mites recorded on fruit crops during the period from 2003 to 2018

Beneficial Family Prey Host plant 1st record (location/GPS) Greenhouse/Open field SI region 1st record (yr) Reference
Amblyseius rademacheri Dosse, 1958 Phytoseiidae Prostigmata Malus domestica Jastebci (46.448587, 16.256746) OF North-Eastern 2003 Miklavc 2006
Euseius finlandicus (Oudemans, 1915) Phytoseiidae Prostigmata Prunus domestica Bresternica (46.568964, 15.584302) OF North-Eastern 2003 Miklavc 2006
Kampimodromus aberrans (Oudemans, 1930) Phytoseiidae Prostigmata Malus domestica Pohorski dvor (46.505708, 15.624032) OF North-Eastern 2003 Miklavc 2006
Neoseiulella tiliarum (Oudemans, 1930) Phytoseiidae Prostigmata Malus domestica Vučja Gomila (46.704941, 16.293238) OF North-Eastern 2003 Miklavc 2006
Neoseiulus umbraticus (Chant, 1956) Phytoseiidae Prostigmata Rubus fruticosus Kranj (46.268400, 14.338999) OF Central 2019 Kreiter et al. 2020
Neoseiulus reductus (Wainstein, 1962) Phytoseiidae Prostigmata Malus domestica Pohorski dvor (46.505708, 15.624032) OF North-Eastern 2003 Miklavc 2006
Paraseiulus soleiger (Ribaga, 1904) Phytoseiidae Prostigmata Malus domestica Pohorski dvor (46.505708, 15.624032) OF North-Eastern 2003 Miklavc 2006
Paraseiulus talbii (Athias-Henriot, 1960) Phytoseiidae Prostigmata Malus domestica Fokovci (46.732883, 16.264145) OF North-Eastern 2003 Miklavc 2006
Paraseiulus triporus (Chant and Yoshida-Shaul, 1982) Phytoseiidae Prostigmata Malus domestica Pohorski dvor (46.505708, 15.624032) OF North-Eastern 2003 Miklavc 2006
Phytoseius horridus Ribaga, 1904 Phytoseiidae Prostigmata Malus domestica Rakitnica (45.690610, 14.758315) OF Central 2014 Bohinc and Trdan 2015
Phytoseius juvenis Wainstein & Arutunjan, 1970 Phytoseiidae Prostigmata Malus domestica Arnovo Selo (45.963219, 15.561836) OF South-Eastern 2018 Kreiter et al. 2020
Phytoseius macropilis (Banks, 1909) Phytoseiidae Prostigmata Malus domestica Maribor (46.567954, 15.638252) OF North-Eastern 2003 Miklavc 2006
Proprioseiopsis okanagensis (Chant, 1957) Phytoseiidae Prostigmata Prunus cerasus Juršinci (46.42504, 15.963838) OF North-Eastern 2019 Kreiter et al. 2020
Typhlodromus (Anthoseius) bakeri (Garman, 1948) Phytoseiidae Prostigmata Malus domestica Marles (46.562719, 15.592627) OF North-Eastern 2003 Miklavc 2006
Typhlodromus (Anthoseius) recki Wainstein, 1958 Phytoseiidae Prostigmata Fragaria sp. Parecag (45.484937, 13.612742) G Western 2018 Kreiter et al. 2020
Typhlodromus (Anthoseius) rhenanus (Oudemans, 1905) Phytoseiidae Prostigmata Malus domestica Trčova (46.544366, 15.721492) OF North-Eastern 2003 Miklavc, 2006
Transeius fragilis (Kolodochka & Bondarenko, 1993) Phytoseiidae Prostigmata Fragaria sp. Parecag (45.484937, 13.612742) G Western 2018 Kreiter et al. 2020
Open in a new tab

Two parasitoid species, which were recorded in apple orchards, and present the smallest group of natural enemies in the contribution, belonged to different families, i.e., Platygastridae and Scelionidae (Table 6).

Table 6.

List of parasitoids recorded in orchards during the period from 2014 to 2021

Beneficial Family Prey Host plant 1st record (location/GPS) SI region 1st record (yr) Reference
Synopeas sosis (Walker, 1935) Platygastridae Dasineura mali Malus domestica Ljubljana (46.047840, 14.473995) Central 2014 Trdan and Bohinc 2016
Telenomus chlorophus (Thompson 1861) Scelionidae Halyomorpha halys Malus domestica Lesno Brdo (46.003205, 14.327141) Central 2021 Trdan et al. 2022
Open in a new tab

Twelve of 13 species recorded on different woody and herbaceous plants were from the Phytoseiidae family. Only one species, recorded on Calendula officinalis L. (Asterales: Asteraceae), was representative of the Anthocoridae family (Table 7). All 13 species were found in open fields.

Table 7.

List of predators recorded on different plants (woody and herbaceous plants) during the period from 2018 to 2019

Beneficial Family Prey Host plant 1st record (location/GPS) SI region 1st record (yr) Reference
Amblyseius microorientalis Wainstein & Beglyarov, 1971 Phytoseiidae Prostigmata Fraxinus excelsior Veržej (46.579061, 16.172184) North-Eastern 2019 Kreiter et al. 2020
Euseius stipulatus (Athias-Henriot, 1960) Phytoseiidae Prostigmata Ulmus procera Izola (45.529051, 13.669176) Western 2018 Kreiter et al. 2020
Kampimodromus corylosus Kolodochka, 2003 Phytoseiidae Prostigmata Tilia platyphyllos Kočevska Reka (45.577965, 14.810683) Central 2019 Kreiter et al. 2020
Neoseiulella aceri (Collyer, 1957) Phytoseiidae Prostigmata Acer pseudoplatanus Veržej (46.579061, 16.172184) North-Eastern 2019 Kreiter et al. 2020
Neoseiulella tiliarum (Oudemans, 1930) Phytoseiidae Prostigmata Tilia cordata Veržej (46.579061, 16.172184) North-Eastern 2019 Kreiter et al. 2020
Neoseiulus umbraticus (Chant, 1956) Phytoseiidae Prostigmata Carpinus betulus Škofljica (45.969481, 14.573839) Central 2019 Kreiter et al. 2020
Oriuss minutus (Linnaeus, 1758) Anthocoridae Thrips, mites, and aphids Calendula officinalis Krasinec (45.585704, 15.288861) South-Eastern 2018 Report on… 2019
Phytoseius finitimus Ribaga, 1904 Phytoseiidae Prostigmata Cornus sanguinea Sečovlje (45.471054, 13.599258) Western 2019 Kreiter et al. 2020
Typhlodromalus spinosus (Meyer & Rodrigues, 1966 Phytoseiidae Prostigmata Carpinus betulus Škofljica (45.969481, 14.573839) Central 2019 Kreiter et al. 2020
Typhlodromus (Typhlodromus) ernesti Ragusa & Swirki, 1978) Phytoseiidae Prostigmata Picea abies Rakitnica (45.690610, 14.758315) Central 2019 Kreiter et al. 2020
Typhlodromus (Anthoseius) foenilis Oudemans, 1930 Phytoseiidae Prostigmata Quercus robur Ankaran (45.579709, 13.743847) Western 2019 Kreiter et al. 2020
Typhlodromus (Anthoseius) recki Wainstein, 1958 Phytoseiidae Prostigmata Carpinus betulus Škofljica (45.969481, 14.573839) Central 2019 Kreiter et al. 2020
Typhloseiulus calabriae (Ragusa & Swirski, 1976) Phytoseiidae Prostigmata Acer pseudoplatanus Ljubljana (46.052007, 14.483290) Central 2018 Kreiter et al. 2020
Open in a new tab

The entomopathogenic and parasitic nematodes that were recorded for the first time are presented in Table 8. Over a period of 14 yr, we detected one species of entomopathogenic nematode and two species of parasitic nematodes.

Table 8.

List of beneficial nematodes recorded during the period from 2007 to 2021.

Beneficial Family Prey Environment 1st record (location/GPS) SI region 1st record (yr) Reference
Steinernema affine (Bovien, 1937) Steinernematidae Agriotes sp. Soil (meadow) Staro Selo pri Kobaridu (46.245806, 13.523395) Western 2007 Laznik et al. 2008
Phasmarhabditis papillosa (A. Schneider, 1866) Rhabditidae Arion vulgaris Meadow (near the lake Žeje) Podbrezje (46.292343, 14.287174) Central 2018 Laznik et al. 2021
Oscheius myriophilus (Poinar, 1986) Rhabditidae Arion vulgaris Meadow (near the Glinščica stream) Ljubljana (46.048448, 14.471914) Central 2021 Trdan et al. 2022
Open in a new tab

Extensive research was carried out in 2008 and 2011, when aphids on various cultivated/uncultivated plants were monitored (Table 9). As part of this investigation at the Laboratory Field of Biotechnical Faculty in Ljubljana (46.048568, 14.474391), 15 native aphid parasitoids were recorded, the practical use of which is still not possible in Slovenian agriculture for the reasons presented in the introduction.

Table 9.

List of aphid parasitoids recorded on plants from different botanical families

Parasitoid Subfamily Prey Host Plant Family Reference
Aphidius absinthii Marshall, 1896 Aphidiinae Macrosiphoniella millefolii (DeGeer) Asteraceae Kos et al. 2008
Aphidius funebris Mackauer, 1961 Aphidiinae Uroleucon cichorii (Koch) Asteraceae Kos et al. 2008
Aphidius salicis Haliday, 1834 Aphidiiinae Cavariella aegopodii (Scopoli) Polygonaceae and Amaranthaceae Kos et al. 2008
Aphidius rhopalosiphi de Stefani-Perez, 1902 Aphidiinae Sitobion avenae Poaceae Kos et al. 2011
Aphidius uzbekistanicus Luzhetzki, 1960 Aphidiinae Sitobion avenae Poaceae Kos et al. 2011
Binodoxys acalephae (Marshall, 1896) Aphidiinae Aphis fabae cirsiiacanthoides Scopoli Asteraceae Kos et al. 2008
Binodoxys angelicae (Haliday, 1833) Aphidiinae Genus Aphis, Aphis fabae cirsiiacanthoides Scopoli
Brachycaudus cardui (L.)		 Fabaceae, Asteraceae
Boraginaceae		 Kos et al. 2008
Binodoxys centaureae (Haliday, 1833) Aphidiinae Macrosiphoniella millefolii (DeGeer) Asteraceae Kos et al. 2008
Binodoxys heraclei (Haliday, 1833) Aphidiiinae Cavariella aegopodii (Scopoli) Polygonaceae and Amaranthaceae Kos et al. 2008
Diaretiella rapae (McIntosh, 1855) Aphidiiinae Myzus persicae (Sultzer)
Brevicoryne brassicae (L.)		 Brassicaceae Kos et al. 2008
Ephedrus plagiator (Nees, 1811) Aphidiinae Myzus persicae (Sultzer)
Aulacorthum solani (Kaltenbach)		 Apiaceae, Brassicaceae Kos et al. 2008
Lipolexis gracilis Főrster, 1862 Aphidiinae Aphis fabae cirsiiacanthoides Scopoli Asteraceae Kos et al. 2008
Lysiphlebus fabarum (Marshal, 1896) Aphidiinae Aphis fabae Scopoli
Brachycaudus cardui (L.)		 Fabaceae
Boraginaceae		 Kos et al. 2008
Praon abjectum (Haliday, 1833) Aphidiinae Myzus persicae (Sultzer)
Aulacorthum solani (Kaltenbach)		 Apiaceae Kos et al. 2008
Praon barbatum Mackauer, 1967 Aphidiinae Acyrthospihon pisum [Harris] Fabaceae Kos et al. 2008
Praon yomenae Takada, 1968 Aphidiinae Uroleucon cichorii (Koch), Uroleucon hypochoeridis (Fabricius) Asteraceae Kos et al. 2008
Open in a new tab

Discussion

The result of our systematic investigation on the occurrence of native natural plant pest enemies in Slovenia during the period from 2007 to 2022 is the confirmation of 41 predators, 32 parasitoids, and 3 nematodes that have not yet been placed on the EPPO Positive List. Due to the Slovenian biological control legislation, which only allows the use of native natural enemies, these species cannot currently be used in agricultural production to control plant insect pests. The main reason for this limitation is the understanding of the importance of native status, as the drafters of the regulations on biological control informally agreed years ago that they would consider native species to be those that are present in the territory of Slovenia. Among the 35 species on the List of native biological control species for biological control, there are also two species widely distributed in Europe, which otherwise originate from the USA. These are the parasitoids Aphelinus mali (Haldeman) (Hymenoptera: Aphelinidae) and Encarsia formosa (Gahan) (Hymenoptera: Aphelinidae), which were introduced to Europe in the 1920s (Burger et al. 2004, Dedryver et al. 2010).

However, only a species that has been used for at least 5 yr for the control of plant insect pests in at least 5 EPPO countries can be included in the EPPO Positive List (EPPO 2021). This means that the Regulations on biological control (Official Gazette of the Republic of Slovenia, no. 45/06) have as many as two security criteria—the first being the requirement of native status and the second being prior placement on the EPPO Positive List—that prevent, or at least make difficult, an ‘inappropriate’ natural enemy species entering Slovenia.

Many of the 141 native beneficial species on the EPPO Positive List (EPPO 2021) originated from Palearctic, Northern Europe or Europe, Mediterranean, Asia, North Americaa, Australia, or from other areas. The criteria for the use of natural enemies in most other EPPO countries are much milder in regard to native status than are the criteria that Slovenia consciously decided on years ago. Due to the growing importance of biological controls (Brabbs et al. 2015), it is especially the desire of some stakeholders that are suppliers of biological control agents to permit the use of some other species from the EPPO Positive List, especially those of commercial interest; that is, those that are widely used in other EPPO countries, as they have proven to be effective against the most important pests in greenhouses, such as the western flower thrips (Frankliniella occidentalis [Pergande] [Thysanoptera: Thripidae]), the two-spotted spider mite (Tetranychus urticae Koch [Acarida: Tetranychidae]) and the greenhouse whitefly (Trialeurodes vaporariorum [Westwood] [Hemiptera: Aleyrodidae]) (Escudero and Ferragut 2005, Calvo et al. 2011). In light of this, we think it is crucial to define the term ‘native’ because if we define as native all those species whose area of origin is found to be the Mediterranean, of which Slovenia is also an integral part, the list of native species useful in biological plant protection would expand to include 8 species (Cryptolaemus montrouzeri Mulsant [Coleoptera: Coccinellidae], Orius albidipennis [Reuter] [Hemiptera: Anthocoridae], Anagyrus vladimiri Triapitsyn [Hymenoptera: Encyrtidae], Trichogramma cordubensis Vargas & Cabello [Hymenoptera: Trichogrammatidae], Trichopria drosophilae Perkins [Hymenoptera: Diapriidae], Amblyseius degenerans [Berlese] [Mesostigmata: Phytoseiidae], Amblyseius swirskii Athias-Henriot [Mesostigmata: Phytoseiidae] and Phytoseiulus persimilis Athias-Henriot [Mesostigmata: Phytoseiidae]). If we define as native those species whose area of origin has been determined to be Europe, the list of native species useful for biological plant protection would increase by 15 species (Aleochara bilineata Gyllenhal [Coleoptera: Staphylinidae], Atheta coriaria [Kraatz] [Coleoptera: Staphylinidae], Scymnus rubromaculatus [Goeze] [Coleoptera: Coccinellidae], Aphelinus abdominalis [Dalman] [Hymenoptera: Aphelinidae], Dacnusa sibirica Telenga [Hymenoptera: Braconidae], Ephedrus cerasicola Stary [Hymenoptera: Braconidae], Eretmocerus mundus Mercet [Hymenoptera: Aphelinidae], Trichogramma cacaeciae Marchal [Hymenoptera: Trichogrammatidae], Trichogramma dendrolimi Matsumura [Hymenoptera: Trichogrammatidae], Trichogramma evanescens Westwood [Hymenoptera: Trichogrammatidae], Hypoaspis aculeifer [Canestrini] [Mesostigmata: Laelapidae], Heterorhabditis downesi Stock, Griffin & Burnell [Rhabditida: Heterorhabditidae], Heterorhabditis megidis Poinar, Jackson & Klein [Rhabditida: Heterorhabditidae], Phasmarhabditis hermaphrotita [A. Schneider] [Rhabditida: Rhabditidae] and Steinernema glasseri [Steiner] [Rhabditidae: Steinernematidae]), and if we accept the Palaearctic area as the acceptable source area, the list would immediately be enriched by 11 additional species (Chilocorus bipustulatus [L.] [Coleoptera: Coccinellidae], Stethorus punctillum [Weise] [Coleoptera: Coccinellidae], Orius laevigatus [Fieber] [Hemiptera: Anthocoridae], Acerophagus maculipennis [Mercet] [Hymenoptera: Encyrtidae], Anagrus atomus [L.] [Hymenoptera: Mymaridae], Encyrtus aurantia [Geoffroy] [Hymenoptera: Encyrtidae], Leptomastidea abnormis [Girault] [Hymenoptera: Encyrtidae], Leptomastix epona [Walker] [Hymenoptera: Encyrtidae], Opius pallipes Wesmael [Hymenoptera: Braconidae], Trichogramma pintoi Voegele [Hymenoptera: Trichogrammatidae] and Stratiolaelaps scimitus Berlese [Mesostigmata: Laelapidae]) (EPPO 2021). It should be taken into account that, in addition to the eight listed species, expanding the area of origin to be Europe would actually also mean the inclusion of some Mediterranean species on the list of native biological control species, while expanding the area of origin to be the Palearctic would mean the inclusion of all European and Mediterranean species. In addition, the List of native species for biological control would be expanded if we took into account many species from Appendix 2 (Classical BCAs successfully established in the EPPO region), since the set of species listed above is only linked to Appendix 1 (commercially or officially used biological control agents) of standard PM 6/3 (5) (EPPO 2021).

As the fate of the geographical aspect of what constitutes ‘native’ is still unknown, we also do not know whether the requirement of native status will be removed in the near future from the regulations on biological control (and whether, as is the case in many EPPO countries, the use of all beneficial organisms from the EPPO Positive List will be enabled). Thus, we will continue to strive to investigate the occurrence of beneficial organisms in the territory of Slovenia. Among the 75 species listed in this article, we would like to highlight those that we believe would be suitable for mass rearing and use in agricultural production as soon as possible.

Among the more interesting beneficial species suitable for this purpose, we highlight Cotesia glomerata, a larval parasitoid of Pieris brassicae (L.) (Lepidoptera: Pieridae), which is an important pest of different Brassicaceae family vegetables (Cartea et al. 2009, Trdan et al. 2014). Lee and Heimpel (2008) describe the influence of the type of food on the length of development cycle of this interesting parasitoid. Notably, a large number of harmful insects appear on cabbage plants, especially in southern and central Europe (Bohinc et al. 2014). This requires the very frequent use of synthetic insecticides (Bommarco et al. 2011), which is not in line with the sustainable food production toward which the European Union (EU) is increasingly inclined (Hahn et al. 2015). Therefore, we believe that mass rearing of Diadegma semiclausum (Hellen) (Hymenoptera: Ichneumonidae), a parasitoid of diamondback moth (Plutella xylostella [L.] [Lepidoptera: Plutellidae]) larvae, out in the open could effectively reduce the economic importance of this increasingly important cabbage pest (Kwon et al. 2003, Wang et al. 2004). Among the rare scientific records on the rearing of this parasitoid, the work of Dosdall et al. (2012) should be highlighted. They studied the influence of temperature and different plant species on the development of this interesting species.

With the increase in the world’s human population, the need for storage capacity for food is also increasing. Storage pests represent one of the most serious groups of harmful organisms. In a large part of the world, control of these pests with insecticides has inadvertently caused them to become insecticide resistant (Opit et al. 2012); therefore, the use of natural enemies of storage pests represents an important pest management tactic for the future. We believe that the use of Anisopteromalus calandrae (Howard) (Hymenoptera: Pteromalidae), a larval and pupal parasitoid of beetles that infest stored agricultural products (Solá et al. 2020, Riudavets et al. 2021) that is a commonly observed natural enemy species in warehouses in Slovenia, is one of the more suitable alternatives for reducing the damage potential of these beetle pests. Anisopteromalus calandrae is a parasitoid that was only recently available on the market (Swiss company Andermatt Biocontrol), and there are also some records available of its rearing (Yang et al. 2022).

Leaf miners (Liriomyza spp. [Diptera: Agromyzidae]) impose considerable problems on vegetable growers in greenhouses in some areas of Europe. In southern Europe, which also includes Slovenia, Liriomyza bryoniae (Kaltenbach) (Diptera: Agromyzidae) is the dominant species (Bragard et al. 2020). Fortunately, in Europe this pest is not yet among the three most economically harmful species in greenhouses; however, to limit its spread in the future, we propose the mass rearing and introduction of Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae), a parasitoid of leaf miner larvae and other harmful insects (Saleh et al. 2010). The suitability of this species for practical use is also confirmed by the fact that it is not very sensitive to insecticides (Hernandez et al. 2011).

Among the predatory mites that are active in permanent plantations (orchards, vineyards) in Slovenia and other European countries are Typhlodromus pyri Scheuten (Mesostigmata: Phytoseiidae) and Amblyseius andersoni (Chant) (Mesostigmata: Phytoseiidae) (Solomon et al. 2000). In orchards, especially on apple trees, we found several species of other predatory mites, but for mass rearing, we suggest the species Kampimodromus aberrans (Oudemans) (Mesostigmata: Phytoseiidae), whose suitability for controlling phytophagous mites was proven in Italy in organic production (Duso et al. 2009, Ahmad et al. 2013). Among the more important records, which can be helpful in the future in the mass rearing of this species, we highlight the work of Lorenzon et al. (2012), who investigated the effects of potential food sources on its biological and demographic parameters.

As previously mentioned, the future use of natural enemies of plant pests in Europe and Slovenia will continue to be largely determined by legislation, but we still believe that the results presented in this paper are at least a stone in the mosaic of this important method of plant protection, which can ensure the production of safer food.

Acknowledgments

The preparation of this paper was conducted within the Professional Tasks from the Field of Plant Protection, a program funded by the Ministry of Agriculture and the Environment, Administration of The Republic of Slovenia for Food Safety, Veterinary and Plant Protection. The preparation was partly funded within Horticulture No. P4-0013-0481, a program funded by the Slovenian Research Agency. Special thanks for help with organism identification are given to Kees Zwakhals, Peter Neerup Buhl, Volker Assing, Željko Tomanović, Stefan Schmidt, Andrej Gogala, Aleksandar Stojanović, Serge Kreiter, Mark Shaw, Paul Rugman-Jones and Maria Lourdes Moraza Zorilla.

Contributor Information

Stanislav Trdan, University of Ljubljana, Biotechnical Faculty, Dept. of Agronomy, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia.

Žiga Laznik, University of Ljubljana, Biotechnical Faculty, Dept. of Agronomy, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia.

Tanja Bohinc, University of Ljubljana, Biotechnical Faculty, Dept. of Agronomy, Jamnikarjeva 101, SI-1000 Ljubljana, Slovenia.

Author Contributions

Stanislav Trdan Conceptualization-Equal, Investigation-Equal, Methodology-Equal, Project administration-Equal, Validation-Equal, Writing – original draft-Equal), Žiga Laznik (Investigation-Equal), Tanja Bohinc (Data curation-Equal, Investigation-Equal, Methodology-Equal, Validation-Equal, Writing – original draft-Equal)

References

  1. Ahmad S, Pozzebon A, Duso C.. Augmentative releases of the predatory mite Kampimodromus aberrans in organic and conventional apple orchards. Crop Prot. 2013:52:47–56. 10.1016/j.cropro.2013.05.008. [DOI] [Google Scholar]
  2. Bohinc T, Marković D, Trdan S.. Leaf epicuticular wax as a factor of antixenotic resistance of cabbage to cabbage flea beetles and cabbage stink bugs attack. Acta Agric Scand Sect B Soil Plant Sci. 2014:64(6):493–500. 10.1080/09064710.2014.926978. [DOI] [Google Scholar]
  3. Bohinc T, Trdan S.. New records of biological control agents in Slovenia in the period 2013-2014. In: TRDAN, Stanislav (ed.). Lectures and papers presented at the 12th Slovenian Conference on Plant Protection with International Participation, Ptuj, March 3-42015. Ljubljana: Plant Protection Society of Slovenia. 2015. p. 289–294 [in Slovenian]. [Google Scholar]
  4. Bommarco R, Miranda F, Bylund H, Bjorkman C.. Insecticides suppress natural enemies and increase pest damage in cabbage. J Econ Entomol. 2011:104(3):782–91. 10.1603/ec10444. [DOI] [PubMed] [Google Scholar]
  5. Brabbs T, Collins D, Herard F, Maspero M, Eyre D.. Prospects for the use of biological control agents against Anoplophora in Europe. Pest Manag Sci. 2015:71(1):7–14. 10.1002/ps.3907. [DOI] [PubMed] [Google Scholar]
  6. Bragard C, Dehnen-Schmutz K, Di Serio F, Gonthier P, Jacques MA, Miret JAJ, Justesen AF, Magnusson CS, Milonas P, Navas-Cortes JA, et al. Pest categorisation of Liriomyza bryoniae. EFSA J. 2020:18(3):6038. 10.2903/j.efsa.2020.6038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Burger JMS, Gort G, Van Lenteren JC, Vet LEM.. Natural history of whitefly in Costa Rica: an evolutionary starting point. Ecol Entomol. 2004:29(2):150–163. 10.1111/j.1365-2311.2004.00586.x. [DOI] [Google Scholar]
  8. Calvo FJ, Bolckmans K, Belda JE.. Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. BioControl. 2011:56(2):185–192. 10.1007/s10526-010-9319-5. [DOI] [Google Scholar]
  9. Cartea ME, Padilla G, Vilar M, Velasco P.. Incidence of the major brassica pests in Northwestern Spain. J Econ Entomol. 2009:102(2):767–73. 10.1603/029.102.0238. [DOI] [PubMed] [Google Scholar]
  10. Carvalho FP. Pesticides, environment, and food safety. Food Energy Secur. 2017:6(2):48–60. 10.1002/fes3.108. [DOI] [Google Scholar]
  11. Crowder DW. Impact of release rates on the effectiveness of augmentative biological control agents. J Insect Sci. 2007:7(15):1–11. 10.1673/031.007.1501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dedryver C-A, Le Ralec A, Fabre F.. The conflicting relationships between aphids and men: a review of aphid damage and control strategies. CR Biol. 2010:333(6–7):539–53. 10.1016/j.crvi.2010.03.009. [DOI] [PubMed] [Google Scholar]
  13. Dosdall LM, Zalucki MP, Tansey JA, Furlong MJ.. Developmental responses of the diamondback moth parasitoid Diadegma semiclausum (Hellen) (Hymenoptera: Ichneumonidae) to temperature and host plant species. Bull Entomol Res. 2012:102(4):373–84. 10.1017/S0007485311000708. [DOI] [PubMed] [Google Scholar]
  14. Duso C, Fanti M, Pozzebon A, Angeli G.. Is the predatory mite Kampimodromus aberrans a candidate for the control of phytophagous mites in European apple orchards? BioControl. 2009:54(3):369–382. 10.1007/s10526-008-9177-6. [DOI] [Google Scholar]
  15. EPPO. PM 6/3 (5) Biological control agents safely used in the EPPO region. EPPO standard – safe use of biological control. EPPO Bull. 2021:1:452–454. 10.1111/epp.12801. [DOI] [Google Scholar]
  16. EPPO. European and Mediterranean Plant Protection Organization. 2023. [accessed 2023 Jan 17]. https://www.eppo.int/ABOUT_EPPO/about_eppo.
  17. Escudero LA, Ferragut F.. Life-history of predatory mites Neoseiulus californicus and Phytoseiulus persimilis (Acari: Phytoseiidae) on four spider mite species as prey, with special reference to Tetranychus evansi (Acari: Tetranychidae). Biol Control. 2005:32(3):378–384. 10.1016/j.biocontrol.2004.12.010. [DOI] [Google Scholar]
  18. Grant R, Blicher-Mathiesen G.. Danish policy measures to reduce diffuse nitrogen emissions from agriculture to the aquatic environment. Water Sci Technol. 2004:49(3):91–9. 10.2166/wst.2004.0170. [DOI] [PubMed] [Google Scholar]
  19. Hahn M, Schotthöfer, A, Schmitz J, Franke LA, Brühl CA.. The effects of agrochemicals on Lepidoptera, with a focus on moths, and their pollination service in field margin habitats. Agric Ecosyst Environ 2015:207:153–162. 10.1016/j.agee.2015.04.002. [DOI] [Google Scholar]
  20. Hernandez R, Guo K, Harris M, Liu TX.. Effects of selected insecticides on adults of two parasitoid species of Liriomyza trifolii: Ganaspidium nigrimanus (Figitidae) and Neochrysocharis formosa (Eulophidae). Insect Sci. 2011:18(5):512–520. 10.1111/j.1744-7917.2010.01391.x. [DOI] [Google Scholar]
  21. Ivezić A, Rugman-Jones P, Malausa T, Ris N, Ignjatović-Ćupina A.. Molecular identification of Trichogramma species parasitizing Ostrinia nubilalis in corn and pepper in south-east border of Europe. Int J Pest Manag. 2020:67(4):346–357. 10.1080/09670874.2020.1779383. [DOI] [Google Scholar]
  22. Klatt BK, Rundlof M, Smith HG.. Maintaining the restriction on neonicotinoids in the European Union – benefits and risks to bees and pollination services. Front Ecol Evol. 2016:4(4):1–4. 10.3389/fevo.2016.00004. [DOI] [Google Scholar]
  23. Kos K, Celar FA.. Confirmation of presence of a predatory gall midge, Feltiella acarisuga(Vallot, 1827) and staphylinid predatorOligota oviformisCasey, 1893 of a two spotted spider mite (Tetranychus urticae, Koch, 1836) in Slovenia. Acta Agric Slov. 2018:111(1):137–141. 10.14720/aas.2018.111.1.13. [DOI] [Google Scholar]
  24. Kos K, Petrović A, Stary P, Kavallieratos NG, Ivanović A, Toševski I, Jakše J, Trdan S, Tomanović Z.. On the identity of cereal aphid parasitoid wasps Aphidius uzbekistanus, Aphidius rhopalosiphi, and Aphidius avenaphis (Hymenoptera, Braconidae, Aphidiinae) by examination of COI mitochondrial gene, geometric morphometrics and morphology. Ann Entomol Soc Am. 2011:104(6):1221–1232. 10.1603/an11055. [DOI] [Google Scholar]
  25. Kos K, Tomanović Z, Petrović-Obradović O, Laznik Z, Vidrih M, Trdan S.. Aphids (Aphididae) and their parasitoids in selected vegetable ecosystems in Slovenia. Acta Agric Slov. 2008:91(1):15–22. 10.2478/v10014-008-0002-9. [DOI] [Google Scholar]
  26. Kreiter S, Amiri K, Douin M, Bohinc T, Trdan S, Tixier M-S.. Phytoseiid mites of Slovenia (Acari: Mesostigmata): new records and first description of the male of Amblyseius microorientalis. Acarologia. 2020:60(2):203–242. 10.24349/acarologia/20204364. [DOI] [Google Scholar]
  27. Kwon M, Park K-R, Kwon K-J.. Developmental characteristics of Diadegma semiclausum Hellen (Hymenoptera: Ichneumonidae), a larval parasitoid of Plutella xylostella L. (Lepidoptera: Yponomeutidae). Biol Control. 2003:6(1):105–110. 10.1016/S1226-8615(08)60175-2. [DOI] [Google Scholar]
  28. Laznik Z, Franin K, Trdan S, Vidrih M, Majič I.. Chemotactic response and motility of the mollusc parasitic nematode Phasmarhabditis papillosa towards mucus from different mollusc species. BioControl. 2022:67(3):345–356. 10.1007/s10526-022-10134-w. [DOI] [Google Scholar]
  29. Laznik Z, Majić I, Trdan S, Malan A, Pieterse A, Ross JL.. Is Phasmarhabditis papillosa (Nematoda: Rhabditidae) a possible biological control agent against the Spanish slug, Arion vulgaris (Gastropoda: Arionidae)?. Nematology. 2021:23(5):577–585. 10.1163/15685411-bja10063. [DOI] [Google Scholar]
  30. Laznik Z, Toth T, Lakatos T, Trdan S.. Entomopathogenic nematode Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) recorded for the first time in Slovenia. Acta Agric Slov. 2008:91:37–45. 10.2478/v10014-008-0004-7. [DOI] [Google Scholar]
  31. Laznik Ž, Trdan S.. Entomopathogenic nematodes (Nematoda: Rhabditida) in Slovenia: from tabula rasa to implementation into crop production systems. In: F Perveen, editorr. Insecticides - advances in integrated pest management. Rijeka: InTech; 2011. p. 627–656. 10.5772/29540. [DOI] [Google Scholar]
  32. Lee JC, Heimpel GE.. Effect of floral nectar, water, and feeding frequency on Cotesia glomerata longevity. BioControl 2008:53(2):289–294. 10.1007/s10526-007-9070-8. [DOI] [Google Scholar]
  33. Lorenzon M, Pozzebon A, Duso, C.. Effects of potential food sources on biological and demographic parameters of the predatory mites Kampimodromus aberrans, Typhlodromus pyri and Amblyseius andersoni. Exp Appl Acarol. 2012:58(3):259–278. 10.1007/s10493-012-9580-7. [DOI] [PubMed] [Google Scholar]
  34. Mavsar S, Trdan S.. Legislation in the field of biological control of plant pests: lists of beneficial organisms. In: Lectures and papers presented at the 12th Slovenian Conference on Plant Protection with International Participation, Ptuj, March 3-4 2015. Ljubljana: Plant Protection Society of Slovenia; 2015. p. 90–93 [in Slovenian]. [Google Scholar]
  35. Miklavc J. Distribution of predatory mites in apple orchards in Podravje and Prekmurje region and diet needs of the species Typhlodromus pyri Scheuten [M. Sc. Thesis]. [Ljubljana]: Biotehniška fakulteta;: 2006. p. 112 [in Slovenian]. [Google Scholar]
  36. Ministry of Agriculture, Forestry and Food RS. Biological control - List of native species for biological control.2023. https://www.gov.si/teme/bioticno-varstvo-rastlin/ [in Slovenian].
  37. Musser FR, Nyrop JP, Shelton AM.. Survey of predators and sampling method comparison in sweet corn. J Econ Entomol. 2004:97(1):136–44. 10.1093/jee/97.1.136. [DOI] [PubMed] [Google Scholar]
  38. Official Gazette of the Republic of Slovenia. Regulations on biological control (no. 45/06).2006. [accessed on 2023 Jan 17]. http://pisrs.si/Pis.web/pregledPredpisa?id=PRAV6800.
  39. Opit GP, Phillips TW, Aikins MJ, Hasan MM.. Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from stored wheat in Oklahoma. J Econ Entomol. 2012:105(4):1107–14. 10.1603/ec12064. [DOI] [PubMed] [Google Scholar]
  40. Orlinski AD. Work of the EPPO/IOBC panel on biological control agents. Bull OEPP/EPPO Bull. 2016:46(2):243–248. 10.1111/epp.12309. [DOI] [Google Scholar]
  41. Riudavets J, Martínez-Ferrer M-T, Campos-Rivela JM, Agustí N, Castañé C.. Releases of the parasitoid Anisopteromalus calandrae (Hymenoptera: Pteromalidae) can control Sitophilus zeamais (Coleoptera: Curculionidae) in big bags of paddy rice. Biol Control. 2021:163:104752. 10.1016/j.biocontrol.2021.104752. [DOI] [Google Scholar]
  42. Saleh A, Allawi TF, Ghabeish I.. Mass rearing of Neochrysocharis formosa (Westwood) (Eulophidae: Hymenoptera), a parazitoid of leafminers (Agromyzidae: Diptera). J Pest Sci. 2010:83:59–67. 10.1007/s10340-009-0269-6. [DOI] [Google Scholar]
  43. Saunders TE, Avila GA, Holwell GI.. Retrospective host-specificity testing shows Trissolcus basalis (Wollaston) and the native Trissolcus oenone (Dodd) (Hymenoptera: Scelionidae) have overlapping physiological host ranges in New Zealand. Biol Control. 2022:170:104926. 10.1016/j.biocontrol.2022.104926. [DOI] [Google Scholar]
  44. Shipp JL, Zariffa N.. Spatial patterns of and sampling methods for western flower thrips (Thysanoptera: Thripidae) on greenhouse sweet pepper. Can Entomol. 1991:123(5):989–1000. 10.4039/ent123989-5. [DOI] [Google Scholar]
  45. Solá M, Riudavets J, Castañé C.. Control of Rhyzopertha dominica and Sitophilus zeamais in stored rice with different release rates of the larval parasitoid Anisopteromalus calandrae. Entomol Gen. 2020:40(3):323–330. 10.1127/entomologia/2020/0899. [DOI] [Google Scholar]
  46. Solomon MG, Cross JV, Fitz Gerald JD, Campbell CAM, Jolly RL, Olszak RW, Niemczyk E, Vogt H.. Biocontrol of pests of apples and pears in northern and central Europe – 3. Predators. Biocontrol Sci Technol. 2000:10(2):91–128. 10.1080/09583150029260. [DOI] [Google Scholar]
  47. Tomanović Z, Kavallieratos NG, Ye ZP, Nika EP, Petrović A, Vollhardt IMG, Vorburger C.. Cereal aphid parasitoids in Europe (Hymenoptera: Braconidae: Aphidiinae): taxonomy, biodiversity, and ecology. Insects. 2022:13(12):Art. No. 1142. 10.3390/insects13121142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Trdan S, Bohinc T, Vidrih M.. Parasitoid wasp Cotesia glomerata (L.) (Hymenoptera, Braconidae) in Slovenia. Acta Biol Slov. 2014:57(2):37–43. [Google Scholar]
  49. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in 2014. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2015. p. 169 [in Slovenian]. [Google Scholar]
  50. Trdan S, Bohinc T.. New records of biological control agents in Slovenia in the period 2012–2014. In: Boeckx P, editor. Proceedings of the 68th international symposium on crop protection, Gent. Commun Agric Appl Biol Sci. 2016:81(3):375–380. [Google Scholar]
  51. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in year 2016. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2017. p. 135 [in Slovenian]. [Google Scholar]
  52. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in year 2018. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2019. p. 164 [in Slovenian]. [Google Scholar]
  53. Trdan S, Laznik Z, Bohinc T.. Thirty years of research and professional work in the field of biological control (predators, parasitoids, entomopathogenic and parasitic nematodes) in Slovenia: a review. Appl Sci. 2020:10(21):74681. 10.3390/app10217468. [DOI] [Google Scholar]
  54. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in year 2020. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2021. p. 182 [in Slovenian]. [Google Scholar]
  55. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in year 2021. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2022. p. 283 [in Slovenian]. [Google Scholar]
  56. Trdan S, Celar FA, Laznik Ž, Bohinc T, Kos K.. Report on the implemented program of professional tasks in the field of plant protection in year 2022. Ljubljana: Biotechnical Faculty, Department of Agronomy; 2023. p. 233 [in Slovenian]. [Google Scholar]
  57. van Lenteren JC. A greenhouse without pesticides: fact or fantasy?. Crop Prot. 2000:19(6):375–384. 10.1016/s0261-2194(00)00038-7. [DOI] [Google Scholar]
  58. Yang JP, Zhang Y, Yu F, Dai RH, Yang H, Hu DM, Zhang XM, Wang Y.. Biological quality of Anisopteromalus calandrae (Hymenoptera: Pteromalidae) reared with cold-stored larvae of Lasioderma serricorne (Coleoptera: Anobiidae). J Stored Prod Res. 2022:97:Art. No.101974. 10.1016/j.jspr.2022.101974. [DOI] [Google Scholar]
  59. Wang XG, Duff J, Keller MA, Zalucki MP, Liu SS, Bailey P.. Role of Diadegma semiclausum (Hymenoptera: Ichneumonidae) in controlling Plutella xylostella (Lepidoptera: Plutellidae): cage exclusion experiments and direct observation. Biocontrol Sci Technol. 2004:14(6):571–586. 10.1080/09583150410001682304. [DOI] [Google Scholar]

Articles from Journal of Insect Science are provided here courtesy of University of Wisconsin Libraries

RESOURCES