Phytoseiidae in Dutch green space

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1 Phytoseiidae in Dutch green space G. (Bert) Vierbergen & Antoon J.M. Loomans Plant Protection Service, Reference Laboratory, Department of Entomology, PO Box 9102, 6700 HC Wageningen, The Netherlands, Evaluation of risks associated with the release of exotic biocontrol agents is a task of the Plant Protection Service in Wageningen. Several exotic Phytoseiidae have been released in The Netherlands during recent years and migration of these agents, such as Neoseiulus californicus, from (greenhouse) cultures into the green space has already been observed. To increase the knowledge of the presence of species we prepared a checklist of Phytoseiidae of The Netherlands. The taxa are divided into species that live in the open (42), in heated places (1), species released for biological control, but that have not settled (4), species with an unknown status (5) and species that have been found during import inspections (10). A two-year survey has been started to investigate the occurrence and composition of Phytoseiidae in the green space. In 2008 this resulted in 124 samples, 83% of which contained Phytoseiidae. Samples were taken from hedgerows belonging to seven plant species. In the near future the Phytoseiidae and Tetranychidae will be identified and studied on the presence and quantity of exotics. Keywords: faunistics, the Netherlands, Phytoseiidae, checklist, green space, survey, hedgerows The Dutch Flora and Fauna Act of April 1, 2002, prohibits the release of animals or eggs of animals in nature, which conflicts with some current biological control programs. In 2005, the release of 134 species has been authorized by derogation with an Order in Council (Loomans & Sütterlin 2005), 17 of which belong to the Phytoseiidae (Anonymous 2005). The Dutch Plant Protection Service (PPS) evaluates the risks of biocontrol agents after the applicant has submitted an application (Loomans et al. 2007). Since 1968 Phytoseiidae have been released in The Netherlands in mass to control spider mites, thrips and to a lesser extent other phytophagous mites and insects, such as gall mites and whiteflies. Neoseiulus californicus (McGregor), one of the phytoseiids that is released in greenhouses and tunnels, has been found to occur spontaneously outdoors since 1996 (Table 1). PROC. NETH. ENTOMOL. SOC. MEET. - VOLUME

2 PHYTOSEIID MITES FROM DUTCH HEDGEROWS Table 1. Records of Neoseiulus californicus in the (semi-)open in The Netherlands, based on microscopic slide material of the Plant Protection Service, Wageningen. Date Location Plant genus 18-ix-1995 Mortel Fragaria* 24-viii-1996 Ede Pleioblastus 18-ix-1996 Ede Pleioblastus 12-v-1997 Odiliapeel Fragaria 20-x-1997 Eck en Wiel Ribes 25-viii-1998 Waardenburg Fragaria 22-vii-1999 Horst Ulmus 1-viii-2000 Wouw Malus 12-x-2000 Boskoop Buxus 13-viii-2001 Horst Buxus 23-viii-2001 Horst Rosa 27-vii-2005 Venray Fagus 23-xi-2006 Asten Bambusoidea 9-xii-2006 Beesd Bambusoidea 12-v-2007 Ede x Fatshedera 23-vi-2007 Valkenswaard Semiarundinaria 3-vii-2007 Bleiswijk cf. Phyllostachys 25-vii-2007 Arcen Sasa 12-ii-2008 Asten Pseudosasa, Semiarundinaria 20-x-2008 Wassenaar Phyllostachys *Spontaneous in tunnel culture; initially misidentified as Amblyseius reductus (Vierbergen 1996) Initially this species was not recognized as such and confused with the native N. reductus (Wainstein) (Vierbergen 1996; van der Linden 2008). In 2005 the PPS was attended on a hedgerow of Fagus sylvatica with serious damage of the spider mite Eotetranychus fagi (Zacher) at Venray (Vierbergen 2008). In this hedgerow N. californicus and the common Amblyseius andersoni (Chant) were present. The occurrence of N. californicus may have a relation with the spider mite occurring as a pest here. The detection of this species in the Dutch green space, has initiated further research. In this paper we present a checklist of the Dutch Phytoseiidae and an overview of species that have been or are still released in The Netherlands. We also present the method we use for our survey in the Dutch green space and the first results. PHYTOSEIIDAE OF THE NETHERLANDS A checklist is given of the Phytoseiidae species found in The Netherlands (Table 2), divided in several sections: - Section 1: indigenous species, non-exotics - Section 2: established synanthropic exotic species: on cultivated plants in the open 46

3 G. VIERBERGEN & A.J.M. LOOMANS Table 2. The Phytoseiidae species of The Netherlands, with reference of first record for The Netherlands Section 1: indigenous (non-exotic) species Amblyseius andersoni (Chant) Van de Vrie 1965 isuki Chant & Hansel Miedema 1987 obtusus (Koch) Ellis & Vierbergen 2002 Anthoseius bakeri (Garman) Van de Vrie 1963 foenilis Oudemans Oudemans 1930b involutus Livshitz & Kuznetsov Wageningen, 19-iv-2002, Juniperus, leg. G. Vierbergen picea (Karg & Edland) Vierbergen 2004 rhenanus (Oudemans) Miedema 1987 richteri Karg Vierbergen 2003 Euseius finlandicus (Oudemans) Nesbitt 1951 Galendromus longipilus (Nesbitt) Bravenboer 1959 Kampimodromus aberrans (Oudemans) Oudemans 1930a, syn. K. vitis (Oudemans) elongatus (Oudemans) Oudemans 1930a Neioseiulella aceri (Collyer) Vught, 24-ix-2008, on Acer campestre, leg. J. Heesters tiliarum (Oudemans) Nesbitt 1951 Neoseiulus agrestis (Karg) Miedema 1987 alpinus (Schweizer) Miedema 1987, syn. Amblyseius aurescens (Athias-Henriot) cucumeris Oudemans Chant 1959; first commercial release in 1985 reductus (Wainstein) Ellis & Vierbergen 2002 reticulatus (Oudemans) Oudemans 1930b umbraticus (Chant) Wageningen, 25-vii-2005, Verbascum thapsus, leg. E. G. M. Dijkstra Paraseiulus soleiger (Ribaga) Nesbitt 1954 talbii (Athias-Henriot) Miedema 1987 triporus (Chant & Yoshida-Shaul) Miedema 1987 Phytoseius macropilis (Banks) Nesbitt 1951, syn. Phytoseius spoofi (Oudemans) Proprioseiopsis okanagensis (Chant) Miedema 1987 Typhlodromips bicaudus (Wainstein) Vierbergen 1997 bryophilus (Karg) Vierbergen 2006 callunae (Willmann) Bennekom, 14-ix-1964, Cladonia impexa, leg. C. F. van de Bund 47

4 PHYTOSEIID MITES FROM DUTCH HEDGEROWS Table 2. Continued [Section 1: indigenous (non-exotic) species] [Typhlodromips] graminis Chant Vierbergen 2003 longulus Berlese Bennekom, 14-ix-1964, Cladonia impexa, leg. C. F. van de Bund masseei (Nesbitt) Van de Vrie 1963 rademacheri (Dosse) Miedema 1987 similis (Koch) subsolidus (Beglyarov) Oudemans 1930b Miedema 1987, syn. Amblyseius canadensis (Chant & Hansell) Typhlodromus bichaetae Karg Vierbergen 2004 ernesti Ragusa & Swirski Vierbergen & Ellis 2007 laurae Arutunjan Chant & Yoshida-Shaul 1987 pyri Scheuten Van de Vrie 1963; first commercial release in 1985 setubali Dosse Vierbergen 1998 tiliae Oudemans Nesbitt 1951 Section 2: settled synanthropic exotic species: on cultivated plants in the open Neoseiulus californicus (McGregor) Vierbergen 1996; first commercial release in 1985 Section 3: settled synanthropic exotic species: restricted to heated places, introduced Neoseiulus barkeri Hughes Van de Vrie 1963; first commercial release in 1981 Section 4: synanthropic exotic species: released for biological control, not introduced Galendromus occidentalis (Nesbitt) first commercial release in 1991* Iphiseius degenerans (Berlese) first commercial release in 1993 Phytoseiulus persimilis Athias-Henriot first commercial release in 1968 Typhlodromips swirskii (Athias-Henriot) first commercial release in 2004 Section 5: species with unknown status in The Netherlands Gamasus vepallidus Koch Oudemans 1902 Phytoseiulus riegeli Dosse Bravenboer & Dosse 1962 Seiulus truncatus Oudemans 1905 Oudemans 1905 Typhlodromus cryptus Athias-Henriot 1960 Vierbergen 2004 (as Neoseiulus zwoelferi (Dosse 1957)) musci Oudemans 1929 Oudemans

5 G. VIERBERGEN & A.J.M. LOOMANS Alternative section 6: species found during import inspection (with country of origin and year of interception) Amblyseius largoensis (Muma) Thailand, 1998 longicollis Denmark & Evans Costa Rica, 2008 tamatavensis Blommers Ghana, 2005; Surinam, 2007 Kuzinellus querellus (Ueckermann & Loots) South Africa, 2005 Neoseiulus barkeri Hughes Thailand, 1997; South Africa, 2000 californicus (McGregor) Kenya, 2003, 2006; Brazil, 2004; Italy, 2008 longispinosus (Evans) Surinam, 2007 Phytoseiulus persimilis Athias-Henriot Israel, 2000, 2004 Proprioseiopsis peltatus (Van der Merwe) Australia, 1999 Typhlodromips swirskii (Athias-Henriot) Israel, 2002 * Hoying & Croft (1977) refer to an experimental population; spontaneous occurrence has not been established. ** Country of origin. - Section 3: established synanthropic exotic species: species restricted to heated places - Section 4: synanthropic exotic species: released for biological control - Section 5: species with unknown status in The Netherlands - Alternative section 6: species found during import inspection Species from section 1-2 are considered part of the Dutch fauna (occur in the Dutch green space). The nomenclature is mostly according to Karg (1993). SURVEY IN PUBLIC GREEN SPACE In 2008 the Dutch PPS has started a survey on the occurrence of Phytoseiidae in Dutch green space to obtain an overview of the current composition of species, to investigate the extent in which N. californicus has spread and to detect other exotic species. Inspectors of the PPS inspected hedgerows in seven plant genera (Table 3). Samples of twigs and leaves were collected from about 120 locations, widely spread around the country, between September 9 and November 6. During their investigation, inspectors focussed their search on those parts of the hedgerows that were infested with Tetranychidae (spider mites). In Fig. 1 the sites inspected in 2008 are shown. In the laboratory, mites were extracted from the twigs using Berlese traps (Fig. 2) as described by Löser (1983). Prior to their identification, the Phytoseiidae and Tetranychidae were heated at 80 C for 10 minutes in lactic acid between a microscope slide and a coverslip. Identification of the 49

6 PHYTOSEIID MITES FROM DUTCH HEDGEROWS Figure 1. Location of survey sample sites (n = 124) in The Netherlands. Figure 2. Berlese-traps used for extraction of Phytoseiidae and Tetranychidae in the 2008 survey. 50

7 G. VIERBERGEN & A.J.M. LOOMANS Table 3. Phytoseiidae and/or Tetranychidae in samples (n) of the 2008 survey. Plant genus n Phytoseiidae (%) Tetranychidae (%) Phytoseiidae & Tetranychidae (%) Acer Carpinus Fagus Malus Prunus Sorbus Tilia Totals Phytoseiidae will be carried out primarily with Karg (1993) and the Tetranychidae primarily with Pritchard & Baker (1955), using phase contrast magnifications up to The result of our identifications will be reported elsewhere. DISCUSSION/CONCLUSIONS The Dutch Flora and Fauna Act is established to prevent introduction of exotic species. During the past decade two exotic Phytoseiidae released for biological control in the Netherlands have settled in green space, and according to the act, new introductions should be prevented by prohibition of release of such species when they are considered a threat to biodiversity. Neoseiulus barkeri occurs spontaneously in bulb cultures (Messelink & Van Holstein-Daj 2006) and in glasshouses since The second species, N. californicus, has established in public green space since 1995 (Table 1). Of the 164 species mentioned in Fauna Europaea ( [20-xi-2008]) 42 are known from the Netherlands (Table 2). Our initial survey in hedges shows that Phytoseiidae are commonly present, but that one of the important preys, the Tetranychidae, is much less common (Table 3). In the near future, identification of the mites can show which exotic species have already settled outdoors, and how common N. californicus is in the investigated hedgerows. Acknowledgements Our thanks are due to inspectors of the PPS, who sampled under all kinds of weather conditions: Piet Boersma, Henk Dekker, Geert Dolfing, Ruud van Donk, Jan Heesters, Ad Langeraar, Peter Mocking, Gerard Prinsen, Aad Ruiter en Jan Schamp. Ir. Tessy Smeets is thanked for preparation of the map with locations of survey sample sites. REFERENCES Anonymous, Vrijstellingenlijst biologische bestrijders en bestuivers Flora en Faunawet. Staatscourant 23:

8 PHYTOSEIID MITES FROM DUTCH HEDGEROWS Bravenboer, L De chemische en biologische bestrijding van de spintmijt Tetranychus urticae Koch. Dissertation Landbouw Hogeschool, Wageningen, Netherlands. Bravenboer, L. & G. Dosse Phytoseiulus riegeli Dosse als Prädator einiger Schadmilben aus der Tetranychus urticae-gruppe. Entomologia Experimentalis & Applicata 5: Chant, D.A Phytoseiid mites (Acarina : Phytoseiidae). Part I. Bionomics of seven species in southeastern England. PART II. A taxonomic review of the family Phytoseiidae, with descriptions of thirty-eight new species. The Canadian Entomologist, Supplement 12, 166 pp. Chant, D.A. & E. Yoshida-Shaul A world review of the pyri species group in the genus Typhlodromus Scheuten (Acari: Phytoseiidae). Canadian Journal of Zoology 65: Ellis, W.N. & G. Vierbergen Entomofauna van Westerwolde. Verslag van de 156e zomerbijeenkomst te Ter Apel. Acari-mijten. Entomologische Berichten, Amsterdam 62: 118. Hoying, S.A. & B.A. Croft Comparisons between populations of Typhlodromus longipilus Nesbitt and T. occidentalis Nesbitt: taxonomy, distribution and hybridization. Annals of the Entomological Society of America 70: Karg, W Acari (Acarina), Milben, Parasitiformes (Anactinochaeta), Cohors Gamasina Leach, Raubmilben. Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise, 2. überarbeitete Auflage: Linden, A. van der Natural occurrence and establishment of predatory mites (Acari: Phytoseiidae) on nurseries for amenity trees. IOBC/wprs Bulletin 32: Loomans, A.J.M Introductie van uitheemse soorten als bestrijders van plagen: ecologische risico-analyse. Entomologische Berichten, Amsterdam 60: Loomans, A.J.M., F. Bigler, G. Sterk & J.S. Bale REBECA Work Package 5 Macrobial (Invertebrate) Biological Control Agents. Loomans, A.J.M. & S. Sütterlin Regulation of invertebrate control agent: international context and situation in The Netherlands. IOBC/wprs Bulletin 28: Löser, F Nutzung des Berlese Apparates zur Untersuchung von Blattproben auf Blattlausbesatz. Nachrichtenblatt für den Pflanzenschutz in der DDR 6: McMurtry, J.A., D.L. Mahr & H.G. Johnson Geographic races in the predaceous mite, Amblyseius potentillae (Acari: Phytoseiidae). International Journal of Acarology 2: Messelink, G.J. & R. van Holstein-Saj Potential for biological control of the bulb scale mite (Acari: Tarsonemidae) by predatory mites in amaryllis. Proceedings of the Netherlands Entomological Society Meeting 17: Miedema, E Survey of phytoseiid mites (Acari: Phytoseiidae) in orchards and surrounding vegetation of northwestern Europe, especially in the Netherlands. Keys, descriptions and figures. Netherlands Journal of Plant Pathology 93 (supplement 2) Nesbitt, H.H.J A taxonomic study of the Phytoseiidae (Family Laelaptidae) predaceous upon Tetranychidae of economic importance. Zoologische Verhandelingen 12, 64 pp., 32 plates. Nesbitt, H.H.J Some random notes on the mite fauna of Limburg with the description of two new species. Natuurhistorisch Maandblad 43:

9 G. VIERBERGEN & A.J.M. LOOMANS Oudemans, A.C New list of Dutch Acari. Second Part. With remarks on known and descriptions of a new subfamily, new genera and species. Tijdschrift voor Entomologie 45: Oudemans, A.C Acarologische Aanteekeningen. XIX. Entomologische Berichten, Amsterdam 2: Oudemans, A.C Acarologische Aanteekeningen. C. Entomologische Berichten, Amsterdam 8: Oudemans, A.C. 1930a. Acarologische Aanteekeningen. CI. Entomologische Berichten, Amsterdam 8: Oudemans, A.C. 1930b. Acarologische Aanteekeningen. CII. Entomologische Berichten, Amsterdam 8: Pritchard, A.E. & E.W. Baker, A revision of the spider mite family Tetranychidae. The Pacific Coast Entomological Society. Memoirs Series 2: Swirski, E. & S. Amitai Further phytoseiid mites (Acarina: Phytoseiidae) of Israel, with a description of one new species. The Israel Journal of Agricultural Research 16: Vierbergen, G Entomology. Species account. Acari: mites. Phytoseiidae. Amblyseius reductus attacking thrips on strawberry. Verslagen en Mededelingen 179 (Annual Report 1995, Plant Protection Service): Vierbergen, G Verslag van de 151e zomervergadering van de Nederlandse Entomologische Vereniging, 29 mei t/m 2 juni 1996, te Formerum op Terschelling. Acari-mijten. Entomologische Berichten, Amsterdam 57: xxxv. Vierbergen, G Verslag van de 152e zomervergadering van de Nederlandse Entomologische Vereniging, 30 mei t/m 1 juni 1997, te Ommen (Overijssel). Acarimijten. Entomologische Berichten, Amsterdam 58: xxxiv. Vierbergen, G Entomofauna van Meinweg en Roerdal. Verslag van de 157e zomerbijeenkomst te Herkenbosch. Acari-mijten. Entomologische Berichten, Amsterdam 63: 73. Vierbergen, G Entomofauna van Noordoost-Twente. Verslag van de 158e zomerbijeenkomst te Ootmarsum (eds. J.G.M. Cuppen & O. Vorst). Acari-mijten. Entomologische Berichten, Amsterdam 64: 206. Vierbergen, G Entomofauna van Noord-Drenthe. Verslag van de 160e zomerbijeenkomst te Schipborg (eds. B. Drost & J.G.M. Cuppen). Acari-mijten. Entomologische Berichten, Amsterdam 66: 89. Vierbergen, G. & W.N. Ellis, Entomofauna van De Kempen, Noord-Brabant. Verslag van de 161e zomerbijeenkomst te Baarschot (eds. J.G.M. Cuppen & B. Drost). Acari-mijten. Entomologische Berichten, Amsterdam 67: Vierbergen, G Entomofauna van Zuid-Limburg. Verslag van de 162e zomerbijeenkomst te Mechelen (eds. B. Drost & J.G.M. Cuppen). Acari-mijten. Entomologische Berichten, Amsterdam 68: Vrie, M. van de Observations on the ecology of predatory mites (Phytoseiidae) on fruit trees. Mitteilungen der Schweizerischen Entomologischen Gesellschaft 36: Vrie, M. van de Relaties tussen de prooi Metatetranychus ulmi Koch en de predator Typhlodromus potentillae Garman (Acari). Entomologische Berichten, Amsterdam 25:

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