Hymenoptera: Eulophidae) Associated with Invasive Pests in Europe and North America: Taxonomic and Ecological Implications

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Hymenoptera: Eulophidae) Associated with Invasive Pests in Europe and North America: Taxonomic and Ecological Implications bs_bs_banner Zoological Journal of the Linnean Society, 2015, 173, 352–423. With 179 figures An integrative study of Necremnus Thomson (Hymenoptera: Eulophidae) associated with invasive pests in Europe and North America: taxonomic and ecological implications MARCO GEBIOLA1,2*, UMBERTO BERNARDO1, ANTONI RIBES3† and GARY A. P. GIBSON4 1CNR – Istituto per la Protezione Sostenibile delle Plante, UOS di Portici – Via Università 133, 80055 Portici (NA), Italy 2Department of Entomology, The University of Arizona, 410 Forbes Bldg., Tucson, AZ 85721, USA 3C/Lleida 36, 25170 Torres de Segre, Lleida, Spain 4Agriculture and Agri-Food Canada, Canadian National Collection of Insects, Arachnids and Nematodes, K. W. Neatby Building, 960 Carling Avenue, Ottawa, Ontario, Canada K1A 0C6 Received 14 June 2014; revised 1 September 2014; accepted for publication 2 September 2014 The species of Necremnus attacking two invasive pests of tomato and canola in Europe and North America, re- spectively, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) and Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae), have been revised using an integrative taxonomy approach. Molecular data from the mitochondrial cytochrome oxidase c subunit I and the nuclear D2 expansion region of the 28S ribosomal subunit and internal transcribed spacer 2, the discovery of new morphological features, and study of type material resulted in the de- lineation of three species groups, the Necremnus artynes, Necremnus cosconius, and Necremnus tidius groups, the discovery of four new species, and the resurrection of three taxa from synonymy. Lectotypes have been designat- ed for 13 species originally described in Eulophus by Walker. Although Necremnus has not been revised, an il- lustrated key is given to differentiate 23 recognized European species. The key, type images, and treatments of the three species groups will enable more accurate identification of the valid species of Necremnus in the future. They will also benefit biological control practitioners of pest species. The ecological consequences of the new taxo- nomic concepts are discussed. © 2015 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 173, 352–423. doi: 10.1111/zoj.12210 ADDITIONAL KEYWORDS: Ceutorhynchus obstrictus – cryptic species – integrative taxonomy – morphol- ogy – parasitoids – phylogenetics – Tuta absoluta. INTRODUCTION species under a single taxonomic entity and the under- estimation of true species diversity. Mounting evi- Closely related species often display only slight, if any, dence, mainly from the use of molecular data, is showing differences in external morphological traits. If slight that some recognized morphospecies are in fact com- differences are misinterpreted as intraspecific vari- plexes of lineages that differ in critical behavioural and ation, this can lead to the lumping of two or more ecological features such as host range (Heraty et al., 2007; Gebiola et al., 2009, 2012; Chesters et al., 2012; *Corresponding author. E-mail: [email protected] Hernandez-Lopez et al., 2012). Cryptic diversity is †Deceased. common amongst hymenopteran parasitoids, in which species confusion can have significant economic con- 352 © 2015 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean Society of London, Zoological Journal of the Linnean Society, 2015, 173, 352–423 This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. AN INTEGRATIVE STUDY OF NECREMNUS 353 sequences because of their wide use as biological control classical biological control (McLeod, 1951). At least 20 agents. Accurate species identification and host- species in five families of Chalcidoidea are recorded range assessment of parasitoids, especially when mor- as associated with Ce. obstrictus in North America (Haye phological variation is slight or absent, are crucial for et al., 2013). This surprisingly diverse fauna includes the success of biological control attempts and to avoid species with both Nearctic and putatively Holarctic dis- undesired, potentially deleterious nontarget effects of tributions, although many of the species appear to have introduced parasitoids on indigenous hosts (Heraty, expanded their host ranges to include Ce. obstrictus 2004). as a host in North America. Some of the species appear Europe and North America are currently strug- to be niche-specific whereas others are more host- gling with major pest problems caused by two inva- specific (Gibson et al., 2005; Dosdall et al., 2006, 2009; sive species (stage V sensu Colautti & MacIsaac, 2004), Gibson, Gates & Buntin, 2006). Most of the parasit- the tomato pinworm, Tuta absoluta (Meyrick) ism has been attributed to Necremnus tidius (Walker) (Lepidoptera: Gelechiidae), and the cabbage seedpod plus three species of Pteromalidae (Chalcidoidea), weevil, Ceutorhynchus obstrictus (Marsham) (Coleoptera: Trichomalus lucidus (Walker), Chlorocytus sp., and Curculionidae). The tomato pinworm is one of the most Pteromalus sp. (Dosdall et al., 2009; Haye et al., 2013). devastating pests of tomato in South America Within North America, N. tidius was identified as (Barrientos et al., 1998; Lietti, Botto & Alzogaray, 2005). Necremnus duplicatus Gahan, 1941 prior to 2005 when It was first reported from Europe in Spain in 2006, Gibson et al. (2005) concluded that the two names were and has subsequently spread throughout the Medi- synonymous, as first suggested by Boucˇek (1959). The terranean Basin, including parts of North Africa and former name was originally described from Europe the Middle East. The pest has caused serious damage and the latter from material reared from Ce. obstrictus to tomato crops in invaded areas since its first detec- in North America (Gahan, 1941). However, although tion and it is currently considered a key agricultural N. tidius has occasionally been reported as a parasitoid threat to European and North African tomato produc- of Ce. obstrictus in Europe (see references in Gibson tion (Desneux et al., 2010; Chailleux et al., 2012). A et al., 2005), it has never been reported as a princi- complex of indigenous natural enemies has been re- pal parasitoid there (Williams, 2003). In North ported since the arrival of T. absoluta in the Mediter- America, Gibson et al. (2005) and Dosdall et al. (2007) ranean Basin and their suitability for biological control reported N. tidius as associated with species of is currently being evaluated (Ferracini et al., 2012; Brassicaceae and Chenopodiaceae. Noyes (2013) Chailleux et al., 2013). A parasitoid identified as listed species of Apionidae, Chrysomelidae, and Necremnus artynes (Walker) (Hymenoptera: Eulophidae) Curculionidae (Coleoptera), Agromyzidae and is one of the most abundant in the field in Italy, Spain, Chloropidae (Diptera), Cephidae (Hymenoptera), France, and Tunisia (Desneux et al., 2010; Ferracini and Gelechiidae, Scythrididae, and Ypnomeutidae et al., 2012; Zappalà et al., 2012, 2013; Abbes et al., 2014; (Lepidoptera) as putative hosts of N. tidius, but Dosdall Gabarra et al., 2014). Necremnus artynes and/or a species et al. (2006) suggested that the noncoleopteran host close to it (see Ferracini et al., 2012) has high poten- associations probably result from incorrect identifica- tial as a biocontrol agent in Mediterranean green- tions of the parasitoid. house tomato production and represents an interesting Within North America, any biological control measure example of adaptation of an indigenous parasitoid to of Ce. obstrictus is inextricably linked to the control an invasive pest (Calvo et al., 2013). Inoculative re- of hoary cress, Cardaria draba (L.) (= Lepidium draba) leases conducted in south-eastern Spain have been suc- (Brassicaceae). This invasive species was accidental- cessful in significantly reducing populations of ly introduced from Europe and in North America is T. absoluta, and some biocontrol companies are already an economically important weed, mainly in canola, involved in the mass rearing and commercial distri- wheat, and barley, although it is also spreading to bution of N. artynes (Urbaneja et al., 2012). Further- natural habitats (Hinz, 2013). Ceutorhynchus obstrictus more, Ferracini et al. (2012) showed that the and T. absoluta are currently controlled through the effectiveness of a Necremnus species near N. artynes use of broad-spectrum chemical pesticides (Cárcamo is even greater than that estimated by parasitization et al., 2001; Roditakis et al., 2012). Alternative control rate alone because its destructive host-feeding behav- strategies such as introduced biological control agents iour kills additional hosts. are urgently needed to reduce pesticide use and to over- The cabbage seedpod weevil is a pest of canola (oilseed come difficulties in current management strategies rape), Brassica napus L. It was accidentally intro- (Hinz, 2013). However, introduction of parasitoids for duced to North America from Europe by the early 1930s control of Ce. obstrictus necessitates these to be host and is now widespread throughout Canada and the USA specific so that they do not negatively impact other (Baur et al., 2007; Dosdall et al., 2009). As an exotic ceutorhynchine weevils
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