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Review of the Species of Trichomalus (Chalcidoidea: Pteromalidae) Associated with Ceutorhynchus (Coleoptera: Curculionidae) Host Species of European Origin

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Review of the Species of Trichomalus (Chalcidoidea: Pteromalidae) Associated with Ceutorhynchus (Coleoptera: Curculionidae) Host Species of European Origin 643 Review of the species of Trichomalus (Chalcidoidea: Pteromalidae) associated with Ceutorhynchus (Coleoptera: Curculionidae) host species of European origin Franck J. Muller CABI Europe—Switzerland, Rue des Grillons 1, 2800 Delémont, Switzerland Hannes Baur Department of Invertebrates, Natural History Museum, Bernastrasse 15, CH-3005 Bern, Switzerland Gary A.P. Gibson, Peter G. Mason Agriculture and Agri-Food Canada, Biodiversity and Integrated Pest Management, Research Centre, 960 Carling Avenue, Ottawa, Canada Ulrich Kuhlmann1 CABI Europe—Switzerland, Rue des Grillons 1, 2800 Delémont, Switzerland Abstract—Six species of Trichomalus Thomson were reared as parasitoids of Ceutorhynchinae hosts in Europe during surveys in 2000–2004. Trichomalus rusticus (Walker) is treated as a valid species, resurrected from synonymy under T. lucidus (Walker), and T. lyttus (Walker) is trans- ferred from synonymy under T. lucidus and newly placed in synonymy with T. rusticus. Illus- trated keys to females and males are given to differentiate the six species (T. bracteatus (Walker), T. campestris (Walker), T. gynetelus (Walker), T. lucidus, T. perfectus (Walker), and T. rusticus) except for males of T. bracteatus and T. gynetelus. A lectotype female is designated for T. rusticus. Trichomalus campestris is newly recorded as a parasitoid of Ceutorhynchus cardariae Korotyaev. Implications of the host–parasitoid associations recovered by the surveys are dis- cussed relative to introduction of species to North America for classical biological control. Résumé—Six espèces de Trichomalus Thomson ont été élevées en tant que parasitoïdes de Ceu- torhynchinae en Europe lors de périodes d’échantillonnage entre 2000 et 2004. Trichomalus rus- ticus (Walker) est traité comme espèce valide et non plus comme synonyme de T. lucidus (Walker), et T. lyttus (Walker) est transféré de sa synonymie avec T. lucidus et nouvellement placé en tant que synonyme de T. rusticus. Une clé illustrée est fournie afin de différencier les mâles et les femelles des six espèces (T. bracteatus (Walker), T. campestris (Walker), T. gynetelus (Walker), T. lucidus, T. perfectus (Walker) et T. rusticus) à l’exception des mâles de T. bracteatus et T. gynetelus. Un lectotype femelle est décrit pour T. rusticus. Trichomalus campestris est trouvé pour la première fois parasitant Ceutorhynchus cardariae Korotyaev. Les associations hôte–parasitoïdes déterminées lors des échantillonnages sont discutées, et en particulier ce que ces résultats impliquent pour l’introduction d’espèces en Amérique du Nord en tant qu’auxiliaires de lutte biologique. Muller657 et al. Curculionidae, itself the most speciose family of Introduction Coleoptera. Some species of Ceutorhynchinae are Colonnelli (2004) stated that Ceutorhynchinae used worldwide as natural enemies for classical bi- (Coleoptera: Curculionidae) contains 1316 species, ological control of weeds to reduce their impact in making it one of the most speciose subfamilies of crop and non-crop habitats (Julien and Griffiths Received 28 June 2006. Accepted 27 March 2007. 1Corresponding author (e-mail: [email protected]). Can. Entomol. 139: 643–657 (2007) © 2007 Entomological Society of Canada 644 Can. Entomol. Vol. 139, 2007 1998), but several species are known to be herbiv- taxonomic status of closely related Trichomalus orous pests of high economic importance in agri- species to (i) accurately document ecological cultural crops (Dieckmann 1972; Mason and data on the species associated with Ceutorhyn- Huber 2002). One such species, the cabbage seed- chinae hosts in Europe, the area of origin of pod weevil, Ceutorhynchus obstrictus (Marsham) C. obstrictus, and (ii) address safety issues in [= Ceutorhynchus assimilis (Paykull); see classical biological control initiatives. Colonnelli 2004], is a pest of oilseed rape, Bras- In this paper we provide (i) illustrated keys to sica napus L. (Brassicaceae), in Europe and was differentiate females and most males of Tricho- accidentally introduced into western North Amer- malus species known from Ceutorhynchinae ica in the early 1930s (McLeod 1953). It is now hosts in Europe; (ii) a list of type material ex- widespread in North America (Kuhlmann et al. amined, together with notes on concordance 2002), though it was only recently found in the with specific characters of voucher specimens; Canadian provinces of Alberta (Cárcamo et al. (iii) a complete list of all voucher specimens 2001), Saskatchewan (Dosdall et al. 2002), Que- examined; (iv) short diagnoses of females and bec (Brodeur et al. 2001), and Ontario (Mason et males or, if required, a more comprehensive de- al. 2004). In the major canola (oilseed rape) pro- scription of the species whose taxonomic status duction areas in Alberta and Saskatchewan, crop is being changed. losses due to C. obstrictus have been reduced through registration of broad-spectrum insecticides Material and methods (Mason and Huber 2002). As an invasive alien species for North Amer- Our study is based primarily on surveys car- ica, C. obstrictus was considered for classical ried out during 2000–2004 in Switzerland, Ger- biological control after its establishment, and in many, France, Austria, Hungary, Romania, and 1949 three species of larval ectoparasitoids Ukraine, to obtain specimens of relevant spe- were introduced from Europe to British Colum- cies of Trichomalus associated with Ceutorhyn- bia, Canada (McLeod 1962). McLeod (1953) chinae. “Lab ex.” indicates that the specimens reported one of these species as Trichomalus were obtained by dissecting Ceutorhynchinae perfectus (Walker) (Hymenoptera: Pteromali- host plants bearing a larval ectoparasitoid and dae). Trichomalus perfectus is the most impor- then rearing the latter individually to the adult tant parasitoid responsible for reducing stage. “Mass collected” specimens were ob- C. obstrictus populations in Europe (Williams tained by collecting and placing host plants in 2003) and is one of several species of Tricho- emergence boxes. Adult parasitoids emerged malus Thomson known to be important mem- into glass vials and were collected, killed, air- bers of parasitoid complexes associated with dried, pinned, and labelled for later identifica- some species of Ceutorhynchinae (Murchie and tion. All voucher specimens identified as Williams 1998). Although follow-up studies to collected by F. Muller, B. Klander, prove establishment were not carried out, M. Grossrieder, and M. Cripps were obtained T. perfectus was considered established in during the 2000–2004 field surveys and are de- North America until very recently. Gibson et al. posited in the Natural History Museum in Bern, (2005) verified from voucher material that Switzerland (NMBE). Additional material, in- T. perfectus was indeed introduced into British cluding type specimens of relevant species, was Columbia in 1949, but showed that all subse- obtained from either NMBE or the Natural His- quent reports of T. perfectus in North America tory Museum in London, United Kingdom were based on misidentifications of another Eu- (BMNH). A detailed list of hosts and host ropean species, Trichomalus lucidus (Walker). plants from which the various Trichomalus spe- Classical biological control of C. obstrictus cies were obtained is given in Table 1. is again being considered for North America to Descriptions are based on observations made provide a reduced-risk alternative to insecticide using a Leica MZ16 binocular microscope cou- applications. Accurate identification of natural pled to a Leica CLS 150× incandescent light enemies is the cornerstone of biological control source and a light diffuser placed over the speci- and is essential when exotic species are intro- men to reduce glare. Several images of a speci- duced, especially when morphological differen- men were taken through the binocular microscope tiation among species is slight, such as for the at different focal planes using a JVC KY-F70BU species of Trichomalus associated with Ceutor- triple CCD digital camera and processed using hynchinae hosts. It is crucial to clarify the the Syncroscopy Auto-Montage™ software suite. © 2007 Entomological Society of Canada Muller et al. 645 Table 1. List of hosts and host plants (all Brassicaceae except T. perforatum (Asteraceae)) from which the various Trichomalus species were obtained. Trichomalus species Host(s) Host plant Trichomalus bracteatus Collected only from sweeping Trichomalus campestris Ceutorhynchus cardariae Korotyaev Cardaria draba (L.) Desv. and collected from sweeping (Lepidium draba L.) (root crown galls) Trichomalus gynetelus Microplontus edentulus Schultze and Tripleurospermum perforatum collected from sweeping (Mérat) Laínz (stems) Trichomalus lucidus Ceutorhynchus roberti Gyllenhal Alliaria petiolata (Bieb.) Cavara & Grande (stems) Ceutorhynchus alliariae Gyllenhal Alliaria petiolata (Bieb.) Cavara & Grande (stems) Ceutorhynchus scrobicollis Alliaria petiolata (Bieb.) Cavara & Nerensheimen and Wagner Grande (stems) Ceutorhynchus quadridens Panzer Brassica oleracea L. Trichomalus perfectus Ceutorhynchus obstrictus (Marsham) Brassica napus L. (pods) Trichomalus rusticus Ceutorhynchus quadridens Panzer Brassica oleracea L. This enabled production of a single, composite, (1993). Terms for colours of various body parts focused image, which allowed us to overcome the are taken from Graham (1969). Measurements of problems historically associated with inadequate each species were taken from about 6–10 air- depth of field for three-dimensional imaging of dried
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