Comparative survey of the phytophagous arthropod faunas associated ...

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Correspondence: Michael G. Cripps, Field Service Centre, PO Box 84, Lincoln University, Canterbury, ...... Anthribidae. Bruchela muscula (Daniel). F. R. P ? .... (21 endemic genera with 290 species) (Thellung 1909; Hedge 1976; Rollins 1993).
Biocontrol Science and Technology, 2006; 16(10): 1007 1030

Comparative survey of the phytophagous arthropod faunas associated with Lepidium draba in Europe and the western United States, and the potential for biological weed control

MICHAEL G. CRIPPS1, HARIET L. HINZ2, JESSICA L. MCKENNEY1, BRADLEY L. HARMON1, FRANK W. MERICKEL1, & MARK SCHWARZLAENDER1 1

Division of Entomology, Department of Plant Soil and Entomological Sciences, University of Idaho, Moscow, USA, and 2CABI Bioscience, Switzerland Centre, Dele´mont, Switzerland

(Received 1 December 2005; returned 20 January 2006; accepted 7 March 2006)

Abstract Hoary cress (Lepidium draba L.) is an invasive perennial mustard (Brassicaceae) introduced to North America from Eurasia. In 2001 we initiated a program to investigate the potential for classical biological control of this weed in the US. Literature and field surveys for the arthropods associated with L. draba were conducted on both continents. Field surveys began in Europe in 2001, and in 2002 2003 standardized surveys were conducted in both Europe and the western US. These field surveys resulted in 80 new host records for L. draba in Europe, and 37 new host records in the US. Although total species richness was nearly four times greater in Europe, there were approximately equal proportions of oligophagous and polyphagous species in each range. Monophagous species were only encountered in the European surveys. The literature surveys revealed that the arthropod fauna associated with L. draba is fairly well known in Europe (175 species), but not in the US (eight species), where the literature was virtually derelict of host records. In both the literature and field surveys, the order Coleoptera contained the most species ( /50%) in Europe, whereas the order Hemiptera contained the most species ( /40%) in the US. Nearly one-half of the species found in literature and field surveys are flower or seed feeders and the other half are primarily foliage or stem feeders. Ten potential biological control agents were discovered from the surveys, of which four are currently being investigated at the CABI Bioscience Centre in Switzerland. The phenologies of these four species are briefly described.

Keywords: Biological control, species richness, Ceutorhynchus turbatus, Ceutorhynchus merkli, Ceutorhynchus cardariae, Psylliodes wrasei

Introduction Hoary cress, Lepidium draba L, ( /Cardaria draba (L.) Desv.) is a perennial mustard (Brassicaceae) indigenous to the Caucasus region, central Asia (Caspian Sea region)

Correspondence: Michael G. Cripps, Field Service Centre, PO Box 84, Lincoln University, Canterbury, New Zealand. E-mail: [email protected] ISSN 0958-3157 print/ISSN 1360-0478 online # 2006 Taylor & Francis DOI: 10.1080/09583150600828361

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(Mulligan & Frankton 1962), and the European coastal regions of the Mediterranean and Black Seas (Ball 1964). Lepidium draba now occurs on every continent except Antarctica (Scurfield 1962) and is classified as either adventive or naturalized. Introductions of L. draba into North America in the late 1800s were from seed in shipballast (Bellue 1933) and contaminated alfalfa seed from central Asia (Groh 1940). The first record of L. draba in the United States was in 1862 from Long Island, New York, and the first record from Canada was in 1878, from Ontario (Mulligan & Findley 1974). Other early records in North America report L. draba occurring near seaports in New York and Washington, DC, in 1898 (Bellue 1933) and in California as early as 1876 (Robbins 1940). It is recorded from the east to west coasts of North America, but is considered particularly problematic throughout the west, where it is declared a noxious weed in 16 states and three Canadian provinces (USDA-NRCS 2004; Rice 2005). Lepidium draba commonly occurs in neutral to alkaline soils in a wide range of habitats including cultivated land, rangeland, pastures, roadsides and waste areas. It thrives particularly well in disturbed habitats and riparian or irrigated areas (Scurfield 1962). The deep rhizomatous root system is reported to penetrate 3.6 9 m deep, and single shoots can produce 850 silicles, each containing two seeds (Corns & Frankton 1952). Approximately three-quarters of the biomass of L. draba plants are belowground (Miller et al. 1994), which confers a high capacity for regrowth (McInnis et al. 1990) and a strong competitive ability (Selleck 1964; Sheley & Stivers 1999). This strong competitive ability of L. draba may also be aided by allelopathic glucosinolates that can inhibit growth of competitors (Qasem 1994, 2001, 2004; Kiemnec & McInnis 2002), and are toxic to grazing livestock (Kingsbury 1964). Since the early 1900s control of L. draba has been attempted by chemical and cultural means with limited success due to the large root reserves, which makes the plant difficult to eradicate from a site (Peitersen & Burdick 1920; Hulbert et al. 1934; Rosenfels & Headley 1944; Stougaard et al. 1999). In addition, some biotypes of L. draba have developed resistance against 2,4-D, the most commonly used herbicide for this weed (Lyons 1998). Thus, after nearly a century of control efforts, L. draba remains a serious weed problem, with no satisfactory control methods. This publication is one of a pair of papers comparing the phytophagous communities on L. draba in its native and introduced ranges. The present paper provides comprehensive species lists, while a subsequent paper will more thoroughly quantify and compare species richnes, diversity, and evenness among the surveyed regions. This work is also part of an ongoing effort that began in 2001 to investigate the potential for classical biological control of L. draba. Before introducing biological control agents from the native range of an invasive plant it is important to investigate which herbivores already occur in the introduced range, which niches on the plant are unoccupied, and whether potential agents have already been introduced by chance (Goeden 1971, 1974). Here we report results of literature and field surveys of the phytophagous arthropod faunas associated with L. draba in its native (Europe) and introduced (western United States) ranges. We present data on the feeding niches, host ranges, and distributions of the phytophagous faunas, and note four potential biological control agents currently being investigated at the CABI Bioscience Centre, Switzerland.

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Materials and methods Literature surveys We searched the literature to find known records of phytophagous arthropods associated with L. draba in Europe and North America. Recent taxonomic work has rendered the Desvaux classification of the genus Cardaria (Desvaux 1814) invalid, and the original Linnean name was resurrected (Al-Shehbaz et al. 2002). The reported number of species in the former Cardaria genus varied from one species, C. draba containing two subspecies (Ball 1964), to as many as five species (Mulligan & Frankton 1962). Therefore, arthropod associations were searched for L. draba and Cardaria species. Common regional arthropod faunal catalogues (e.g. Essig 1936; Dieckmann 1972; Tietz 1972; Freud et al. 1983) (see Tables I and II) and the CABPEST† databases were searched for host plant associations. Arthropods known to be associated with plants in families other than Brassicaceae were not included in the literature survey. The distributions of species were found by searching checklist catalogues (e.g. Wheeler & Henry 1992; EIS 1998; Schwartz & Foottit 1998; Maw et al. 2000) and also the CABDirect † database. Species distributions are recorded as Palearctic, Nearctic, or Holarctic. We use the term Holarctic to describe species that are present in both the Palearctic and Nearctic regions regardless of origin. Field surveys In spring of 2001, the first surveys began in Europe, where 133 sites were sampled encompassing 11 countries (Figure 1). Arthropods were collected using sweep-net samples or by aspirating specimens directly from the plants. In addition, about 30 plants were randomly collected per site, dissected, and an effort made to rear any immature stages through to adults. In spring of 2002 and 2003, standardized sampling protocols were used in both Europe and the US. In each continent, nine sites were surveyed in 2002 and 13 sites in 2003. The 2002 2003 surveys encompassed seven European countries and four US states (Figure 1). Field sites were selected on each continent in order to maximize the number of different habitats sampled, and to survey a broad geographical range. The L. draba habitats surveyed included waste areas, roadsides, pastures, meadows, orchards and vineyards. At each field site, the arthropod community on L. draba was surveyed by beating plants into a sweep-net for 30-s intervals. Nine to ten 30-s samples were collected at each site. In 2002, only Hemiptera (sensu latu ) and Coleoptera were collected by aspirating all the Hemipteran and Coleopteran specimens from the sweep-net. In 2003, the entire contents of the sweep-net for each 30-s sample were emptied into sealed plastic bags and later transferred to vials of 70% ethanol. In addition, in both years L. draba plants (ca. 90 180 shoots per site) were excavated from each site: stems and roots were dissected, and an effort made to rear immature insect stages to adult for identification. Only phytophagous species that were identified to genus or species are included in the faunal lists. Many morphospecies (Cripps 2005), were collected but were not identified to the species level due to being immature, or of limited quantity or quality. Phytophagous was broadly defined to encompass all arthropods feeding on pollen and/ or nectar, but excluding parasitic hymenoptera, which as adults, may also occasionally feed on pollen and/or nectar. Phytophagous species collected in the samples that are known not to feed on Brassicaceae are excluded from the faunal lists. However, some

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Table I. Literature records of phytophagous arthropods associated with Lepidium draba in Europe. For each species the primary feeding niche, host range, and distribution are indicated. Orders and families are listed phylogenetically according to Triplehorn and Johnson (2005); genera and species within a family are listed alphabetically.

ORDER/Family Species ACARI Eriophyidae Aceria draba (Nalepa) Tetranychidae Bryobia praetiosa (Koch) (/Bryobia graminis [Oudemans]) Tetranychus atlanticus McGregor Tetranychus urticae Koch

Primary feeding Host rangeb Distributionc nichea

Referenced

S

M

P

1,2,3,4,5

F,S

P

H

6,

F,S F,S

P P

H H

6,7 6,7,8

ORTHOPTERA Acrididae Chorthippus biguttulus (L.)

F

P

P

9

DERMAPTERA Forficulidae Forficula auricularia L.

F

P

H

10

F F F,S F,S F

P P P P P

H P H H

6,7 10 6,7 6,7 6

F F F F F F

P P P O O O

P P P P P P

10 10 7 6,7,9 6,7,9,10 10

F F F

P P P

P P P

9 9 9

S S

P P

P H

10 9

F,S

P

P

9

F

P

F F F F F

P P P P P

P P P P P

9 9 9 9 9

F F F

P P P

H P P

9 12 10

HEMIPTERA Miridae Adelphocoris lineolatus (Goeze) Calocoris sp. Lygus gemellatus (Her.-Sch.) Lygus rugulipennis Poppius Polymerus vulneratus (Wolff) Pentatomidae Carpocoris mediterraneus Tamanini Carpocoris purpureipennis (DeGeer) Dolycoris baccarum (L.) Eurydema oleracea (L.) Eurydema ornata (L.) Eurydema ventralis Kolenati Rhyparochromidae Beosus maritiums (Scopoli) Megalotonus chiragra (F.) Pionosomus opacellus Horva´th Lygaeidae Nysius ericae (Schilling) Nysius thymi (Wolff) Oxycarenidae Metopoplax origani (Kolenati) Alydidae Alydus sp. Coreidae Ceraleptus gracilicornis (Her.-Sch.) Coreus marginatus (L.) Coriomeris denticulatus (Scopoli) Coriomeris scabricornis (Panzer) Syromastus rhombeus (L.) Cercopidae Aphrophora alni (Falle´n) Aphrophora spumaria (L.) Cercopis sanguinolenta (Scopoli)

9

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Table I (Continued ) ORDER/Family Species Lepyronia coleoptrata (L.) Philaenus spumarius (L.) Cicadellidae Allygidius atomarius (F.) Anaceratogalia spp. Aphrodus sp. Cicadella viridis (L.) Circulifer opacipennis (Lethierry) Eupelix cuspidate (F.) Euscelis sp. Graphocraerus ventralis (Falle´n) Psammotettix majusculus Linnavuori Cixiidae Hyalesthes obsoletus Signoret Aphididae Aphis craccivora Koch Aphis fabae Scopoli Aphis nasturtii Kaltenbach Aphis verbasci Schrank Aulacorthum solani (Kaltenbach) Brevicoryne brassicae (L.) Macrosiphum euphorbiae (Thomas) Myzus ornatus Laing Myzus persicae (Sulzer) Phorodon humuli (Schrank) THYSANOPTERA Phlaeothripidae Haplothrips setiger Priesner Thripidae Frankliniella intonsa (Trybom) Taeniothrips atratus (Haliday) Thrips angusticeps Uzel Thrips fuscipennis Haliday Thrips major Uzel Thrips tabaci Lindeman COLEOPTERA Scarabaeidae Amphicoma vulpes (F.) Anomala sp. Cetonia aurata (L.) Oxythyrea cinctella (Schaum) Tropinota hirta (Poda) Valgus hemipterus (L.) Cantharidae Cantharis spp. Malthinus spp. Rhagonycha sp. Dermestidae Anthrenus pimpinellae F. Anthrenus scrophulariae L. Anthrenus verbasci (L.)

Primary feeding Host nichea rangeb Distributionc

Referenced

F F

P P

H H

9,10 2,3,9,10

F F F F F F F F F

P P P P P P P P P

P

H P P H P

9 9 9 10 10 10 10 9 10

F

P

P

11,12

F F F F F F F F F F

P P P P P O P P P P

H H H P H H H H H H

6,7 6,7 6,7 7 6,7 2,3,6,7 6,7 6 6,7 7

F,S

P

P

6

F,S F,S F,S F,S F,S F,S

P P P P P P

P H P H P H

6,7 6,7 6 6 6 6,7

S S S S S S

P

P

P P P P

P P P H

10 10 10,13 11,13 9,10,13 9,10,13

S S S

P P P

S S S

P P P

10 10 10 H H H

10 10 10

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Table I (Continued ) ORDER/Family Species Melyridae Axinotarsus sp. Dasytes sp. Malachius bipustulatus (L.) Psilothrix sp. Nitidulidae Meligethes aeneus (F.) Meligethes corvinus Erichson Meligethes lepidii Miller Meligethes nigrescens Stephens Meligethes rotundicollis Brisout Meligethes viridescens (F.) Phalacridae Olibrus sp. Phalacrus sp. Cryptophagidae Cryptophagus sp. Mordellidae Mordellistena sp. Tenebrionidae Omophlus syriacus Mulsant Podonta nigrita (F.) Oedemeridae Oedemera flavipes (F.) Oedemera virescens (L.) Meloidae Alosimus armeniacus (Falderman) Alosimus syriacus (L.) Oenas tenuicornis Abeille Cerambycidae Agapanthia cardui (L.) Agapanthia dahlia (Richter) Agapanthia leucaspis (Stevens) Chrysomelidae Colaphellus hoefti Me´ne´trie´s Colaphellus sophiae (Schaller) Phaedon cochleariae (F.) Phyllotreta aerea Allard Phyllotreta atra (F.) Phyllotreta cruciferae (Goeze) Phyllotreta diademata (F.) Phyllotreta erysimi Weise Phyllotreta foudrasi Weise Phyllotreta nemorum (L.) Phyllotreta nigripes (F.) Phyllotreta nodicornis (Marsham) Phyllotreta ochripes Curtis Phyllotreta ozbeki Gruev & Aslan Phyllotreta parallela Boieldieu Phyllotreta procera (Redtenbacher) Phyllotreta undulata Kutschera Phyllotreta vittula (Redtenbacher) Phyllotreta vittata (F.)

Primary feeding Host nichea rangeb Distributionc

Referenced

S S S S

P P P P

S S S S S S

O O M? O O O

S S

P P

10 10

S

P

10

S

O?

10

S S

P P

P P

10 10

S S

P P

P P

9,13 9,10,13

S S S

P P P

P P P

10 10 10

S S S

P P P

P P P

10,16 10,16 10

F F F F F F F F F F F F F F F F F F F

O O O O O O O O O O O O O O O O O O O

P P P H P H P P P P P P P P P P H P P

10,17,18 6,7,10,16 9 7,16,19 6,7,16,19 6,7,16,19 7,16,19 7 16 6,7,9,16 6,7,10,16 7,9,16 9,16 20 19 7,16 6,7,9,16 7,16 6,9,16

P

H P P H P P

10 10 7,14 10 6,9,10,15 10,15 15 10,15 10,15 10,15

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Table I (Continued ) ORDER/Family Species Psylliodes chrysocephala (L.) Psylliodes thlaspis Foudras Curculionidae Aulacobaris chlorizans (Germar) Aulacobaris coerulescens (Scopoli) Aulacobaris cuprirostris (F.) Aulacobaris janthina (Boheman) Ceutorhynchus atomus Boheman Ceutorhynchus aeneicollis Germar Ceutorhynchus assimilis (Paykull) (/Ceutorhynchus pleurostigma [Marsham]) Ceutorhynchus cardariae Korotyaev Ceutorhynchus chalybaeus Germar Ceutorhynchus coarctatus Gyllenhal Ceutorhynchus cochleariae Gyllenhal Ceutorhynchus constrictus (Marsham) Ceutorhynchus contractus (Marsham) Ceutorhynchus gallorhenanus Hoffman Ceutorhynchus griseus Brisout Ceutorhynchus merkli Korotyaev Ceutorhynchus nanus Gyllenhal Ceutorhynchus napi Gyllenhal Ceutorhynchus obstrictus (Marsham) Ceutorhynchus pallidactylus (Marsham) (/Ceutorhynchus quadridens [Panzer]) Ceutorhynchus pulvinatus (Germar) Ceutorhynchus rapae Gyllenhal Ceutorhynchus rhenanus Schultze Ceutorhynchus scapularis Gyllenhal Ceutorhynchus sulcicollis (Paykull) Ceutorhynchus syrites Germar Ceutorhynchus turbatus Schultze Ceutorhynchus typhae Herbst (/Ceutorhynchus floralis [Paykull] ) Eremobaris picturata Me´ne´trie´s Melanobaris atramentaria (Boheman) Melanobaris laticollis (Marsham) Melanobaris semistriata (Boheman) Mylacus rotundatum (F.) Phyllobius viridearis (Laicharting) Tanymecus dilaticollis Gyllenhal HYMENOPTERA Tenthredinidae Athalia rosea (L.) LEPIDOPTERA Plutellidae Plutella xylostella (L.) Tortricidae Clepis pallidana (F.) Pieridae Pieris brassicae (L.) Pieris napi (L.)

Primary feeding Host nichea rangeb Distributionc

Referenced

F F

O O

H P

9,16 16,19,21

F F F F F F F,R

O O O O O O M?

P P P P P P P

22,23 6,22,23 7,23 22 23,23,25,26 9,23,25,26 9,22,23,25

F F F F F,S F F,S F F F,S F F,S F

M O? O O O P O O M O O O O

P P P P P P P P P P P H H

24 6,23,25,26 23 22,23 22,23 10,22,23,25 22,23,25 23,25,26 27 23,25,26 6,7,22,23,25 6,9,10,23,25 7,9,23,25

F F F F F F,S F,S F,S

O? O O O? O O M O

P H P P H P P H?

6,23,26 6,7,22,23,25,26 23,25,26 22,23 6,23 22,23,25,26 10,22,23,25,26 6,23,25,26

F F F F F F F

O O O M? P P P

P P P P P P P

22 22,23 6,7,22,23 24 9,28 7,28 7,28

F

O

P

9,10

F

O

H

7,9,10,31,32

F

P

P

9

F F

O O

P H

6,7 6,7

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Table I (Continued ) ORDER/Family Species Pieris rapae (L.) Euchloe ausonia Hu¨bner DIPTERA Cecidomyiidae Contarinia cardariae Fedotova Contarinia lepidii Kieffer Contarinia nasturtii (Kieffer) Dasineura cardariae Fedotova Dasineura lepidiiphaga Fedotova Anthomyiidae Delia cinerella (Falle´n) Delia platura (Meigen) Delia variata (Falle´n) Agromyzidae Chromatomyia horticola Goureau Liriomyza brassicae (Riley) Liriomyza lepidii Harrison Liriomyza strigata (Meigen) Phytomyza atricornis Meigen Drosophilidae Scaptomyza flaveola (Meigen) Scaptomyza pallida (Zetterstedt)

Primary feeding Host nichea rangeb Distributionc

Referenced

F F

O O

H P

6,7 33

S S S S S

M? O? O M? O?

P P P P P

34 35 2,3,7 34 36

R R R

O ? ?

P H P

10 6,10 10

F F F F F

P P O? P P

P H P P P

6,7,9 31,38 37 6,31,38 31,38

F F

O O?

P H

6,31,38 10

a

S/sexual reproductive plant parts (flowers and seeds); F/foliage (stems and leaves); R /roots. bM/ monophagous (restricted to Lepidium draba and closely related species); O/oligophagous (restricted to Brassicaceae); P/polyphagous (feeds on several plant families). cP/Palearctic; H/Holarctic. Introduced or indigenous status is not distinguished. d1 (Houard 1908); 2 (Buhr 1964); 3 (Buhr 1965); 4 (Lipa 1976); 5 (Lipa 1978); 6 (Lipa 1977); 7 (Manojlovie´ et al. 1994); 8 (Meagher & Meyer 1990); 9 (Tosic et al. 1996); 10 (Campobasso et al. 1999); 11 (Sforza et al. 1998); 12 (Sforza et al. 1999); 13 (Freude et al. 1969); 14 (Freude et al. 1979); 15 (Freude et al. 1967); 16 (Freude et al. 1966); 17 (Sobian 1975); 18 (Sobian 1976); 19 (Douget 1994); 20 (Gruev & Aslan 1998); 21 (Krzhizhanovsky 1974); 22 (Guryeva & Kryzhanovsky 1965); 23 (Freude et al. 1983); 24 (Korotyaev 1993); 25 (Diekmann 1972); 26 (Hoffmann 1954); 27 (Korotyaev 2000); 28 (Freude et al. 1981); 29 (Dieckmann 1980); 30 (Emmet 1996); 31 (Hering 1957); 32 (Idris & Grafius 1996); 33 (Kuznetzov 1994, 1999); 34 (Fedotova 2000); 35 (Ru¨bsaamen 1895); 36 (Fedotova 1994); 37 (Spencer 1990); 38 (Se´guy 1934).

species whose host ranges are uncertain were included in the faunal lists, but were not included in any of the graphical presentations summarizing species feeding on L. draba . Each identified species from the field surveys was also searched in the CABDirect † database to determine if it has economic pest status. The distribution and host association of each species from the field surveys were determined in the same manner as species from the literature records. Voucher specimens of identified material from the field surveys are deposited in the W.F. Barr Entomological Museum, University of Idaho, Moscow, Idaho. Results Literature and field surveys From the European literature, 175 phytophagous arthropod species were recorded associated with L. draba, representing nine orders (Figure 2) and 51 families (Table I).

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Table II. Literature records of phytophagous arthropods associated with Lepidium draba in North America. For each species the primary feeding niche, host range, and distribution are indicated. Orders and families are listed phylogenetically according to Triplehorn and Johnson (2005); genera and species within a family are listed alphabetically. ORDER/ Family Species

Primary feeding nichea

Distributionc

Referencesd

HEMIPTERA Miridae Lygus elisus Van Duzee Lygus hesperus Knight Aphididae Aphis armoraciae Cowen Myzus persicae (Sulzer)

F,S F,S

N N

1,2,3 1,2

F F

H H

4 5

THYSANOPTERA Thripidae Thrips tabaci Lindeman Frankliniella occidentalis (Pergande)

F,S F,S

H H

6 6

COLEOPTERA Curculionidae Ceutorhynchus obstrictus (Marsham)

S

H

7,8

LEPIDOPTERA Pieridae Pontia protodice (Boisd. & Lec.)

F

H

9

a S/sexual reproductive plant parts (flowers and seeds); F/foliage (stems and leaves). bO/oligophagous (restricted to Brassicaceae); P /polyphagous (feeds on several plant families). cN/Nearctic; H/Holarctic. Introduced or indigenous status is not distinguished. d1 (Fye 1980); 2 (Fye 1982); 3 (Schwartz & Foottit 1992); 4 (Sobhian 1978); 5 (Tamaki & Olsen 1979); 6 (Hammon 2002); 7 (Fox & Dosdall 2003); 8 (Dosdall & Moisey 2004); 9 (Robinson et al. 2002).

In contrast, only eight species were recorded from L. draba in the US literature, which are represented by four orders (Figure 2) and five families (Table II). The European field surveys resulted in 162 phytophagous species collected from L. draba , of which 22 species were reared from plants (Table III). Of the 162 species, 47 were only

Figure 1. Survey regions for phytophagous arthropods on Lepidium draba in Europe and the western US. Triangles indicate areas surveyed only in 2001. Stars indicate areas surveyed in 2001 (for Europe) 2002 and 2003. Squares indicate areas surveyed only in 2003.

M.G. Cripps et al.

Species

1016

100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0%

OTHER LEPIDOPTERA THYSANOPTERA HEMIPTERA COLEOPTERA

Europe U.S. literature literature

Europe samples

U.S. samples

Figure 2. Comparison of the taxonomic composition of the phytophagous species recorded in the literature and collected in the field (2002 and 2003 samples) on Lepidium draba in its native (European) and introduced (western US) ranges. Other/Acari, Orthoptera, Dermaptera, Hymenoptera, and Diptera.

collected in the 2001 surveys, and for another 23 species the host ranges were uncertain (Table III). Therefore, 92 species were identified from the 2002 2003 European field surveys that feed on L. draba, and are represented by seven orders (Figure 2) and 41 families. The US field survey resulted in 45 phytophagous species collected from L. draba, of which two species were reared from plants (Table IV). Of the 45 species, the host ranges of two species are uncertain. Therefore, 43 species were identified from the US field surveys that feed on L. draba, and are represented by seven orders (Figure 2) and 24 families. In both the literature and field surveys, the order Coleoptera contained the most species (/50%) in Europe, whereas the order Hemiptera contained the most species (/40%) in the US (Figure 2). From the European field surveys, 61 species collected were previously recorded on L. draba in the literature, and six species from the US field surveys were previously reported. Therefore, 80 new arthropod host records (does not include species with uncertain host ranges) are reported for L. draba in Europe (20012003 surveys), and 37 new arthropod host records are reported for L. draba in the US From the literature and field surveys, 10 species were common to both the US and Europe. The combined literature and field surveys for both Europe and the US report 290 different species from L. draba , of which 59 are Holarctic in distribution. In the European field surveys, 14% of the species were common, 21% were occasional, and 65% were rare (Table III). In the US field surveys, 24% of the species were common, 16% were occasional, and 60% were rare (Table IV). In both literature and field surveys, polyphagous species represented the majority, followed by oligophagous species (Figure 3). Monophagous species only occurred in the European surveys and represented less than 10% of the total phytophagous species (Figure 3). Nearly one-half of the species in each literature and field survey are flower or seed feeders and the other half are primarily foliage feeders (Figure 4). The European literature survey lists five species that feed on the roots, of which two were collected in the field survey. The US literature survey found one species (Aphis armoraciae Cowen) that feeds on the roots; however, this species was not found in this field survey. From the field surveys, 57 (35%) of the species in Europe, and 23 (51%) of the species in the US have some economic pest status (Tables III and IV).

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Table III. Phytophagous arthropods collected and/or reared from Lepidium draba in Europe 2001 2003. For each species the primary feeding niche, relative frequency, distribution, host range, and economic pest status is indicated. Orders and families are listed phylogenetically according to Triplehorn and Johnson (2005); genera and species within a family are listed alphabetically.

ORDER/Family Species ACARI Eriophyidae Aceria draba (Nalepa)R Tetranychidae Bryobia praetiosa (Koch) HEMIPTERA Miridae Lygus rugulipennis Poppius Polymerus cognatus (Fieber) Stenodema calcarata (Falle´n) Tingidae Tingis auriculata (Costa) Pentatomidae Dolycoris baccarum (L.) Eurydema oleracea (L.) Eurydema ventralis KolenatiR Nezara viridula (L.) Sciocoris sulcatus Fieber Berytidae Neides tipularius (L.) Oxycarenidae Metopoplax origani (Kolenati) Platyplax salviae (Schilling) Rhopalidae Rhopalus tigrinus (Schilling) Cercopidae Cercopis sanguinolenta (Scopoli) Philaenus spumaris (L.) Cicadellidae Eupteryx aurata (L.) Euscelis sp. Evacanthus acuminatus (F.) Tettigometridae Tettigometra obliqua (Panzer) Aphididae Brevicoryne brassicae (L.)R Lipaphis lepidii (Nevsky) Macrosiphum euphorbiae (Thomas) Myzus persicae (Sulzer) THYSANOPTERA Phlaeothripidae Haplothrips leucanthemi (Schrank) Haplothrips reuteri (Karny) Melanthripidae Melanothrips fuscus Sulzer Thripidae Frankliniella occidentalis (Pergand) Mycterothrips consociatus (Tar.-Toz.) Rubiothrips ferrugineus (Uzel) Thrips tabaci Lindeman

Primary feeding nichea

Relative Host Pest frequencyb Distributionc ranged statuse

S

C

P

M

F,S

O

H

P

X

F,S F,S F,S

C R R

H H P

P P P

X X

F

R

H

P

F F F F F

R R O R R

P P P H P

P O O P P

F

R

P

P

F,S F,S

O R

P P

P? P?

F

R

H

O

X

F F

O O

P H

P P

X X

F F F

O R R

H

P

X

P

P

F

R

P

P?

F F F

O O C

H P H H

O P P

F,S F,S

C R

H P

P P

F,S

R

P

P?

F,S F,S F,S F,S

C R R C

H P P H

P P? P? P

X X X

X X X X

X

X

X

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M.G. Cripps et al.

Table III (Continued ) ORDER/Family Species COLEOPTERA Scarabaeidae Cetonia aurata (L.) Epicometis hirta (Poda) Oxythyrea funesta (Poda) Valgus hemipterus (L.) Elateridae Dicronychus rubripes (Germar) Melanotus niger (F.) Cantharidae Cantharis rustica Falle´n Malthodes sp. Dermestidae Anthrenus pimpinellae F. Anthrenus scrophulariae L. Anthrenus verbasci (L.) Melyridae Dasytes flavipes (Oliver) Psilothix cyaneus (Oliver) Malachius geniculatus Germar Nitidulidae Meligethes aeneus (F.) Meligethes coracinus Sturm Meligethes kraatzi Reitter Meligethes lepidii Miller Phalacridae Olibrus aeneus (F.) Olibrus bicolor (F.) Phalacrus coruscus (Panzer) Cryptophagidae Telmatophilus sparganii Ahrens Mordellidae Mordellistena brevicauda (Boheman) Mordellistena pumila (Gyllenhal) Oedemeridae Oedemera virescens (L.) Oedemera lurida (Marsham) Meloidae Alosimus syriacus (L.) Anthicidae Formicomus pedestris Rossi Aderidae Aderus pruinosus (Kiesenwetter) Scraptiidae Anaspis viennensis Schilsky Chrysomelidae Colaphellus hoefti Me´ne´trie´s Colaphellus sophiae (Schaller)R Galeruca tanaceti (L.)R Gonioctena fornicata (Bru¨ggemann) Luperus luperus (Sulzer) Pachnephorus villosus (Duftschmid) Phaedon cochleariae (F.) Phyllotreta aerea Allard

Primary feeding nichea

Relative Host Pest frequencyb Distributionc ranged statuse

S S S S

R O R R

P P P H

P P P P

S S

O R

P P

P? P?

S S

C R

P

P

S S S

R O R

H H H

P P P

S S S

R R R

P P P

P? P? P?

S S S S

C R R C

H P P P

O O O? M

S S S

R R O

P P P

P P P

S

R

P

P?

S S

C R

P P

? ?

S S

O R

P P

P? P?

S

R

P

P?

S

R

P

P

S

R

P

P

S

R

P

?

F F F F F

C R R R R

P P P P P P P P

O P ? ? P

X X X X

X X

X

X

X X X

X X

Lepidium draba arthropod comparison

1019

Table III (Continued ) ORDER/Family Species Phyllotreta astrachanica Lopatin Phyllotreta atra (F.) Phyllotreta diademata (F.) Phyllotreta erysimi Weise Phyllotreta nemorum (L.) Phyllotreta nigripes (F.) Phyllotreta undulata Kutschera Phyllotreta vittula (Redtenbacher) Phyllotreta weiseana Jacobs Psylliodes cuprea (Koch) Psylliodes isatidis HeikertingerR Psylliodes persica Allard Psylliodes sophiae Heikertinger Psylliodes thlaspis Foudras Psylliodes wrasei Leonardi et ArnoldR Anthribidae Bruchela muscula (Daniel) Bruchela suturalis (F.) Brentidae Ceratapion onopordi (Kirby) Eutrichapion facetum (Gyllenhal) Eutrichapion punctigerum (Paykull) Eutrichapion viciae (Paykull) Holotrichapion pisi (F.) Holotrichapion pullum (Gyllenhal) Malvapion malvae (F.) Rhopalapion longirostre (Oliver) Protapion fulvipes (Geoffroy) Pseudapion fulvirostre (Gyllenhal) Curculionidae Aulacobaris coerculescens (Scopoli) Aulacobaris lepidii (Germar) Aulacobaris picicornis (Marsham) Baris artemisiae (Herbst) Ceutorhynchus assimilis (Paykull)R ( /Ceutorhynchus pleurostigma [Marsham]) Ceutorhynchus biseriatus (Faust) Ceutorhynchus cardariae KorotyaevR Ceutorhynchus carinatus Gyllenhal Ceutorhynchus chalybaeus Germar Ceutorhynchus coarctatus Gyllenhal Ceutorhynchus contractus (Marsham) Ceutorhynchus difficilis Schultze Ceutorhynchus ericanus Schultze Ceutorhynchus erysimi (F.)R Ceutorhynchus fallax Boheman Ceutorhynchus gerhardti Schultze Ceutorhynchus gottwaldi Dieck. et Smrec. Ceutorhynchus griseus Brisout Ceutorhynchus hirtulus Germar Ceutorhynchus humeralis Gyllenhal Ceutorhynchus inaffectatus Gyllenhal

Primary feeding nichea

Relative Host Pest frequencyb Distributionc ranged statuse P P P P P P P P P P P P P P P

F

C

F

C

F

C

F

R

F

R

F

R

P P

?

F F

R R

? ?

F F F F F F

R R R R R R

P P P P P P P P P P

F

R

F F,S,R

R O

F,S

O

F,S F,S

R O

F,S

R

P H P P P

P P P P P P P P H P P P P P P P

O

X

O O O

X X X X

M?

? ? ? ? ? ? O X ? M?

M

? O

?

X

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M.G. Cripps et al.

Table III (Continued ) ORDER/Family Species Ceutorhynchus merkli KorotyaevR Ceutorhynchus nanus Gyllenhal Ceutorhynchus napi Gyllenhal Ceutorhynchus niyazii Hoffmann Ceutorhynchus obstrictus (Marsham) Ceutorhynchus pallidactylus (Marsham)R ( /Ceutorhynchus quadridens [Panzer]) Ceutorhynchus picitarsis Gyllenhal Ceutorhynchus pulvinatus Gyllenhal Ceutorhynchus rapae GyllenhalR Ceutorhynchus sisybrii (Diekmann) Ceutorhynchus sophiae Gyllenhal Ceutorhynchus sulcicollis PaykullR Ceutorhynchus syrites Germar Ceutorhynchus turbatus SchultzeR Ceutorhynchus typhae (Herbst) ( /Ceutorhynchus floralis [Paykull]) Ceutorhynchus varius Mulsant Eremobaris picturata Me´ne´trie´sR Euidosomus acuminatus Boheman Eusomus ovulum (Germar) Foucartia squamulata (Herbst) Melanobaris atramentaria (Boheman) Melanobaris semistriata (Boheman) Peritelus sphaeroides (Germar) Phyllobius betulae (L.) Phyllobius virideaeris (Laicharting) Rhinusa tetrum (F.) Sibinia pellucens (Scopoli) Tanymecus dilaticollis Gyllenhal Tanymecus palliatus (F.) Thamiocolus nubeculosus (Gyllenhal) HYMENOPTERA Tenthridinidae Athalia rosae (L.)R Athalia cordata Lepeletier LEPIDOPTERA Psychidae Apterona helix (Siebold) Plutellidae Eidophasia messingiella (Fischer von Ro¨s.) Plutella xylostella (L.)R Pieridae Pieris brassicae (L.)R Pieris napi (L.)R Pieris rapae (L.)R DIPTERA Scatopsidae Swammerdamella brevicornis Meigen

Primary feeding nichea

Relative Host Pest frequencyb Distributionc ranged statuse

F,S

O

F,S F,S F,S

R O O

F,S F,S

R R

P P P P H H

M X ? O O

P P H P P H P P H?

O ?

O

X X

X X

F,S F,S F,S F,S

R R C O

O O M O

F,S

R

F,S

R R

F,S

R

F,S

R

F,S F,S F,S

R R R

F,S F

R R

P P P P P P P P P P P P P P P

F F

R R

P P

P P

X X

F

O

H

P

X

O

X

? P? O M? P

X

X

X

P? ? P P P

X X

P F

C

H H H H

S

O

P

X X X

P

Lepidium draba arthropod comparison

1021

Table III (Continued ) ORDER/Family Species Sepsidae Sepsis fulgens Meigen Agromyzidae Chromatomyia horticola (Goureau)R Chromatomyia syngenesiae HardyR Ephydridae Limnellia quadrata Falle´n Philigria interstincta Falle´n

Primary feeding nichea

S

Relative Host Pest frequencyb Distributionc ranged statuse

O

P

P

P H S S

O R

P P

X X X

? ?

a S/sexual reproductive plant parts (flowers and seeds); F/foliage (stems and leaves); R/roots. bR/rare (collected at one or two of 13 sites); O/occasional (collected at 3 to 6 of 13 sites); C /common (collected at seven or more of 13 sites). cP/Palearctic; H/Holarctic. Introduced or indigenous status is not distinguished. dM/monophagous (restricted to Lepidium draba and closely related species); O/ oligophagous (restricted to Brassicaceae); P/polyphagous (feeds on several plant families). eX/economic pest status determined from literature; major versus minor pest status not distinguished. R Indicates the species was reared on Lepidium draba .

Discussion From the combined literature and field surveys, nearly four times as many species are recorded from L. draba in Europe compared to the US. This is partly due to a better knowledge of the fauna associated with L. draba in Europe, compared to the US, where until now relatively little was know about the fauna associated with L. draba. More importantly, the greater species richness in Europe is a result of long coevolutionary relationships between arthoprods and Brassicaceae (Ehrlich & Raven 1964; Thompson 1994). The primary center of diversification of Brassicaceae is in the region of eastern Europe to central Asia (62 endemic genera with 530 species); and the Mediterranean region is considered a secondary center of diversification (21 endemic genera with 290 species) (Thellung 1909; Hedge 1976; Rollins 1993). Therefore, it is not surprising that a large number of oligophagous species occur in its area of origin (Frenzel & Brandl 1998). In North America there are 39 endemic genera with 677 species, mostly occurring in the west with limited distributions (Rollins 1993). In the US, L. draba is fed upon by some highly polyphagous species, and some species oligophagous on Brassicaceae. This could be explained by the widespread distribution, perennial biology, and taxonomic affinity of L. draba to a number of native Brassicaceae species in North America (Lawton & Schro¨der 1977; Strong et al. 1984). In Europe most arthropod species on L. draba belong to the order Coleoptera, whereas in the US, most species on L. draba belong to the order Hemiptera (sensu latu ). This is because most specialized monophagous and oligophagous species that only occur in the native range are beetles, compared to the generalist herbivores in the introduced range, which are mostly Hemipterans. This trend has also been found in other similar comparisons of phytophagous arthropods on plants in their native and introduced ranges (Goeden 1974; Wilson et al. 1990; Memmott et al. 2000; Imura 2003). Only 10 species occurred in both Europe and the US. Given the large number of species from the surveys that are Holarctic, it is somewhat surprising that not more of these species were recorded on L. draba from the US. However, most of the species that are listed as Holarctic were introduced to North America, and may not be widely

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M.G. Cripps et al.

Table IV. Phytophagous arthropods collected and/or reared from Lepidium draba in the United States 2002 2003. For each species the primary feeding niche, relative frequency, distribution, host range, and economic pest status is indicated. Order and families are listed phylogenetically according to Triplehorn and Johnson (2005); genera and species within a family are listed alphabetically.

ORDER/Family Species

Host Pest Primary feeding Relative frequencyb Distributionc ranged Statuse nichea

ACARI Tetranychidae Bryobia praetiosa (Koch)

F,S

C

H

P

X

DERMAPTERA Forficulidae Forficula auricularia L.

F

R

H

P

X

F,S F,S F,S F,S F,S F,S

C R R R C R

N N N N N N

P P P P P P

X X

F F

R R

N N

P P

X X

S

C

N

O

X

F F F F F

C C R R R

N N H N N

P P P P P

HEMIPTERA Miridae Lygus elisus Van Duzee Lygus hesperus Knight Lygus robustus (Uhler) Lygus shulli Knight Melanotrichus albocostatus (Van Duzee) Polymerus basivittis (Reuter) Pentatomidae Holcostethus limbolarius (Sta˚l) Thyanta pallidovirens (Sta˚l) Lygaeidae Nysius niger Baker Cicadellidae Ceratagallia curvata (Oman) Ceratagallia viator Hamilton Neoaliturus tenellus (Baker) Texananus latipex DeLong Xerophloea peltata (Uhler) Cixiidae Cixus cultus Ball Cixus praecox Van Duzee Aphididae Lipaphis erysimi (Kaltenbach) Macrosiphum euphorbiae (Thomas) Myzus persicae (Sulzer)

F F

R R

N N

? ?

F F F

O O C

H H H

O P P

X X X

THYSANOPTERA Thripidae Frankliniella occidentalis (Pergande) Thrips tabaci Lindeman

F,S F,S

C C

H H

P P

X X

S

R

N

P

S S

R R

N N

P P

S

R

P

S

O

P

S

R

COLEOPTERA Scarabaeidae Dichelanyx truncate (LeConte) Elateridae Ctenicera glauca (Germar) Limonius ectypus (Say) Cantharidae Malthodes sp. Melyridae Amecocerus sp. Nitidulidae Meligethes nigrescens Stephens

H

O

X

X X

X X

X

Lepidium draba arthropod comparison

1023

Table IV (Continued ) ORDER/Family Species Latridiidae Melanophthalma sp. Anthicidae Notoxus sp. Cerambycidae Brachysomida atra (LeConte) Cortodera subpilosa (LeConte) Chrysomelidae Orsodacne atra (Ahrens) Phyllotreta sp. Curculionidae Ceutorhynchus americanus BuchananR Ceutorhynchus obstrictus (Marsham) Ceutorhynchus subpubescens LeConte LEPIDOPTERA Psychidae Apterona helix (Siebold) Plutellidae Plutella xylostella (L.)R DIPTERA Heliomyzidae Neossus sp. Drosophilidae Drosophila sp. Scaptomyza sp. Ephidryidae Limnellia sp. Psilopa sp.

Primary feeding Relative Host Pest nichea frequencyb Distributionc ranged Statuse

S

O

P

S

R

P

S S

R R

N N

P P

S S

R C

N

P O

X X

F F,S F

O O R

N H N

O O O?

X

F

O

H

P

X

F

C

H

O

X

S

R

S S

R R

S S

R R

a

S/sexual reproductive plant parts (flowers and seeds); F/foliage (stems and leaves); R/roots. bR/rare (collected at one or two of 13 sites); O/occasional (collected at three to six of 13 sites); C/common (collected at seven or more of 13 sites). cN/Nearctic; H/Holarctic. Introduced or indigenous status is not distinguished. dO/oligophagous (restricted to Brassicaceae); P/polyphagous (feeds on several plant families). eX /economic pest status determined from literature; major versus minor pest status not distinguished. RIndicates the species was reared on Lepidium draba .

distributed. For instance, the introduced species, Meligethes nigrescens Stephens (Hatch 1957), was only found at one field site in Idaho, but is a recent new state record for Idaho (A. Cline, pers. comm.). It is likely that given more time and broader Nearctic surveys, many of these introduced species will be found on L. draba. Some researchers have noted that L. draba is a reservoir for economic pests in the US, such as the cabbage seedpod weevil, Ceutorhynchus obstrictus (Marsham) (Fox & Dosdall 2003) and Lygus species (Fye 1980). However, our surveys show that 23 (51%) of the species collected from L. draba in the US have economic pest status, indicating that L. draba is a far greater reservoir for crop pests than previously known. In Europe the proportion of economic species is less (34%); however, it is evident that L. draba is also a reservoir for Brassica crop pests in Europe. Other species that were not collected in the US field surveys, but are introduced to North America such as

M.G. Cripps et al.

Species

1024

100% 90% 80% 70% 60% 50% 40% 30% 20% 10% 0%

Polyphagous Oligophagous Monophagous

Europe literature

U.S. literature

Europe sampled

U.S. sampled

Figure 3. Comparison of the host specificity of phytophagous species recorded in the literature and collected in the field (2002 and 2003 samples) on Lepidium draba in its native (European) and introduced (western US) ranges.

Number of species

Meligethes aenus (F.), Ceutorhynchus pallidactylus (Marsham) ( /Ceutorhynchus quadridens [Panzer]), and Ceutorhynchus sulcicollis (Paykull), are known Brassica pests (Hayn 1970; Lamb 1989), and have all been reared from L. draba in Europe. The future implication of the likely spread of these introduced species to L. draba reinforces the status of L. draba as a pest reservoir for economically important Brassica crops. These results also emphasize the need to initiate a biological control program for L. draba in North America and so reduce its role in sustaining populations of pest species. A primary premise of classical biological control of weeds is that specialized herbivores exist in the native range of the plant, and that release from these herbivores may contribute to the invasive nature of the plant (Elton 1958; DeBach & Rosen 1991). Many introduced Brassicaceae weeds exist in North America; however, classical biological control has not yet been attempted on any of the species due to their close taxonomic affinity with economically important Brassica crops and native Brassicaceae. From the literature, 10 species on L. draba are recorded to have a restricted host range, and therefore have potential as biological control agents. The two gall midge 225 200 175 150 125 100 75

Flowers/Seeds Foliage (Stems and leaves) Roots

50 25 0 Europe literature

U.S. literature

Europe sampled

U.S. sampled

Figure 4. Comparison of the primary feeding niches of phytophagous species recorded in the literature and collected in the field (2002 and 2003 samples) on Lepidium draba in its native (European) and introduced (western US) ranges.

Lepidium draba arthropod comparison

1025

species, Contarinia cardariae Fedotova and Dasyneura cardariae Fedotova, that develop on the flowers and fruits respectively of L. draba (Fedotova 2000), have so far only been found in southern Kazachstan, and were not encountered during our field surveys. The root crown-feeding weevil Melanobaris (Baris ) semistriata (Boheman), attacked cabbage (Brassica oleracea capitata ) under no-choice conditions (Dolgovskaya 2002), and was therefore given low priority. The flower-feeding nitulidid, Meligethes lepidii Miller, is only recorded from L. draba (Freude et al. 1967); however, it is not likely that this feeding mode would be effective in controlling L. draba. Of the remaining six species, the root galling weevil, Ceutorhynchus assimilis (Paykull), and the gall forming eriophyid mite, Aceria draba (Nalepa), are being investigated by other researchers, and therefore will not be reported on here (Fumanal et al. 2004; J. Littlefield, unpublished data). Phenologies of the four species currently being studied at the CABI Bioscience Switzerland Centre are briefly described. Ceutorhynchus cardariae Korotyaev was described in 1992 from the Taman Peninsula to the Dagestan region of the Caucasus, only in association with L. draba (Korotyaev 1993). During our field surveys, C. cardariae was found in the Caucasus, Romania, Hungary and the Crimean Peninsula. Little was known about the biology and host plant associations when work began with this species in 2001. At the CABI Bioscience Centre, females laid eggs from early spring onwards into newly developing shoots of L. draba (Hinz et al. 2004). Feeding by the adult females induced superficial gall formation on stems, petioles, leaf midribs, and shoot-tips, into which eggs were inserted. Gall formation could stunt or kill developing shoots (M. Cripps, pers. observation). Larvae progressed through three instars before leaving the gall to pupate in the soil. Adult weevils emerged in early summer and fed for two to three weeks before entering an aestivation period. Adults recommenced feeding in mid-August on newly developing rosettes. A small proportion of adult females oviposited during this time, the progeny of which emerged the same year. Therefore, C. cardariae has the potential to be bivoltine. This species has shown potential for rapid population increase, and has proven easy to rear. Host specificity tests are well advanced, and thus far show a high degree of specificity. Ceutorhynchus merkli Korotyaev was described in 2000 from Hungary, Moldova, Ukraine and the Caucuses, only in association with L. draba (Korotyaev 2000). During our field surveys we collected C. merkli in Hungary, Bulgaria, Ukraine and the Caucasus. Little was known about the biology and host plant associations when work began with this species in 2001. It has a life cycle similar to C. cardariae. Females oviposited in early spring until about mid-May (Hinz et al. 2003). Larvae mined shoots of L. draba during April and May and developed through three instars before leaving the plant to pupate in the soil. The next generation emerged about 4 weeks later, and adults fed for 23 weeks and then aestivated. Feeding recommenced in late summer on new rosettes before overwintering. Host specificity tests for this species are ongoing. The third weevil species, Ceutorhynchus turbatus Schultz, is widespread and abundant, and occurred at nearly all field sites sampled during our surveys (Hinz et al. 2003). To our knowledge, it is the only specialist on L. draba that has expanded its range together with its host plant west of Hungary (Morris 1982; van den Berg & van de Sande 1999). Females of C. turbatus oviposited into the silicles of L. draba and larvae fed on the developing seeds. Mature larvae exited pods to pupate in the soil, and adults emerged in the following spring. Females did not readily lay eggs under

1026

M.G. Cripps et al.

confined conditions. Thus far, C. turbatus only developed on the closely related Lepidium campestre (L.), which has also been characterized as a field host (Hoffmann 1958). Because L. draba mainly reproduces vegetatively once established at a site, seed feeders are unlikely to have an impact on existing stands, but may reduce spread. The flea beetle, Psylliodes wrasei Leonardi et Arnold, was described from the Caucases, Ukraine, Bulgaria, and Macedonia in 1995 (Leonardi & Arnold 1995). During our surveys, this species was collected in Bulgaria, Romania, and eastern Hungary. Little was known of its biology and host plant associations when work began with this species in 2003. At the CABI Bioscience Centre, females laid eggs from late summer throughout autumn. Larvae hatched in early spring and mined developing shoots of L. draba , which could kill or stunt shoot growth. Adults emerged during June, aestivated after a short feeding period, and re-commenced feeding in late summer. This species has also shown potential for rapid population increase, and has proven easy to rear. Host specificity tests are currently ongoing. Of the four potential biological control agents being investigated at the CABI Bioscience Centre, C. cardariae, and P. wrasei currently seem the most promising. From the US surveys, Ceutorhynchus americanus Buchanan was discovered mining in the stems of L. draba (Table IV), which occupies the analogous niche of C. merkli Korotyeav in Europe. Therefore, C. merkli is of lower priority as a potential biological control agent. Because L. draba is a clonal plant, the seed feeding weevil, C. turbatus , will not likely have a substantial impact on reducing plant populations, and is therefore given lower priority as a potential biological control agent. Ultimately results of host specificity tests will show whether any of the potential biological control agents are suitable for release.

Acknowledgements We are greatly indebted to A. Diaconu, A. Gumovsky, V. Fursov, R. Tomov and S. To¨pfer for their assistance and hospitality during European field surveys. Collections in 2001 were carried out by B. Korotyeav (Caucuses), A. Gassmann (Armenia), U. Schaffner (Turkey), H. Recher (Swizterland, Germany, Denmark), I. Tosevski (Serbia). We thank B. Korotyaev (Curculionoidea) and his colleagues for providing the bulk of the European species determinations. Other species determinations were provide by A. Cline (Nearctic Nitidulidae), B. Gerdeman (Tetranychidae), A. Hamilton (Nearctic Cicadellidae), J. Jelinek (Palearctic Nitidulidae), A. Konstantinov (Chrysomelidae), L. Mound (Thysanoptera), J. Na´poles (Bruchinae), K. Pike (Aphididae), M. Schwartz (Miridae), and W. Turner (Nearctic Diptera) for which we are extremely grateful. We also thank J. McCaffrey and M. Klowden for helpful comments on the manuscript. References Al-Shehbaz IA, Mummenhoff K, Appel O. 2002. Cardaria , Coronopus and Stroganowia are united with Lepidium . Novon 12:5 11. Ball PW. 1964. Cardaria Desv. In: Tutin TG, Heywood VH, Burges NA, Valentine DH, Walters SM, Webb dA, editors. Flora Europaea Vol. 1. Cambridge: Cambridge University Press. p 333. Bellue MK. 1933. Hoary cress. Monthly Bulletin, Deptpartment of Agriculture, State of California 22:287. Buhr H. 1964 Bestimmungstabellen der Gallen (Zoo-und Phytocecidien) an Pflanzen Mittel und Nordeuropas. Band 1. Jena: Veb Gustav Fischer Verlag.

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