All against one: first results of a newly formed foreign exploration consortium for the biological control of perennial pepperweed
H.L. Hinz,1 E. Gerber,1 M. Cristofaro,2 C. Tronci,3 M. Seier,4 B.A. Korotyaev,5 L. Gültekin,6 L. Williams7 and M. Schwarzländer8
Summary Perennial pepperweed (PPW), Lepidium latifolium L., is a mustard of central Asian origin that is invading natural and cultivated habitats in North America and is difficult to control with conventional means. Biological control of PPW is hampered by the fact that it is relatively uncommon in its native range and that it has more than 30 native North American congeners. In addition, detailed information on phytophagous organisms and diseases associated with PPW in its native range is sparse. In 2005, a foreign exploration consortium was formed, and in 2006, five field trips were conducted: three to Turkey, one to Kazakhstan and one to Romania and Bulgaria. A total of 28 field sites of PPW were sampled. Based on identifications available thus far and combined with data of previous opportunistic surveys, we reared or sampled 67 phytophagous organisms, only seven of which have previously been recorded from PPW. Although plants in Kazakhstan showed more obvious signs of damage than in Turkey, a similar number of phytophagous organisms were collected. Only three species were found in both countries, indicating two distinct herbivore communities. At least six potential biological control agents were found during these first surveys: one root-mining weevil, Melanobaris sp. pr. semistriata Boheman, and an eriophyid mite, Aculops sp., in Turkey; one gall-forming weevil, Ceu- torhynchus marginellus Schultze, a shoot-mining flea beetle, Phyllotreta reitteri Heikertinger, and a fungal leafspot pathogen, Septoria lepidii Desmazières, in Kazakhstan; and a shoot-mining chloropid fly, Lasiosina deviata Nartshuk, in both countries. The shoot-mining flea beetle in particular was found to be very damaging, causing the die-back of shoots. For M. sp. pr semistriata and P. reitteri, we have established a colony in quarantine at CABI and have started to investigate their biology.
Keywords: Lepidium latifolium, Turkey, Kazakhstan, field surveys.
Introduction ceous, semi-woody perennial that typically reaches 0.5 to 1.5 m in height and reproduces vegetatively and by Perennial pepperweed (PPW), Lepidium latifolium L. seed (Renz, 2000). Plants regrow early each year from (syn.: Cardaria latifolium) (Brassicaceae), is a herba- a dense network of creeping, horizontal roots, flower in June/July and set seeds in July/August. PPW is a 1 CABI Europe-Switzerland, Rue des Grillons 1, 2800 Delémont, prolific seed producer, capable of producing more than Switzerland. six billion seeds per acre of infestation (Miller et al., 2 BBCA and ENEA-Casaccia, Via del Bosco 10, 00060 Sacrofano 1986). (Rome), Italy. PPW is native to central Asia and is believed to have 3 BBCA, Via del Bosco 10, 00060 Sacrofano (Rome), Italy. 4 CABI UK Centre, Silwood Park, Buckhurst Road, Ascot, Berkshire been introduced into the United States through Califor- SL5 7TA, UK. nia around 1900 as a contaminant of sugar beet seeds 5 Russian Academy of Sciences, Zoological Institute, 199034 St. Peters- (Renz and DiTomaso, 1998). It is now widespread burg, Russia. across North America but especially prevalent in Ne- 6 Atatürk University, Department of Plant Protection, 25240 Erzurum, Turkey. vada, Oregon, Utah and California. Perennial pepper- 7 USDA, ARS, Exotic and Invasive Weeds Research Unit, 920 Valley weed is declared noxious or prohibited in 14 US states Road, Reno, NV, USA. and Canadian provinces (US Department of Agricul- 8 University of Idaho, Department of Plant, Soil and Entomological ture (USDA)–Natural Resources Conservation Service Sciences, Moscow, ID 83844-2339, USA. Corresponding author: H.L. Hinz
154 All against one: first results of a newly formed foreign exploration consortium
PPW is often associated with mesic habitats, such three field trips to Turkey in April, June and October, as riparian areas, drainage ditches and subirrigated ten PPW sites were found, while in Kazakhstan (14 –31 pastures and hay meadows. However, it can invade a May), 19 sites of PPW were found (Fig. 1). Literature wide range of habitats including pastures, open fields, records indicate that PPW occurs in northeastern Bul- roadsides and residential areas (Young et al., 1998). garia and southern Romania; however, we were unable Downstream movement of seeds and root fragments to find PPW at several locations mainly along the Dan- along waterways and irrigation systems is the primary ube River. mode of spread for this weed. PPW is highly compe- At each field site, adult insects were sampled, plants titive, and invasions result in dense monocultures and were dissected, and eggs and immature larvae were subsequent loss of biodiversity through the exclusion transferred into artificial diet for rearing. In addition, of native, riparian vegetation (Trumbo, 1994; Young et plant parts (leaves, shoots and roots) with immature al., 1995; Blank and Young, 1997). In areas that are stages or signs of mite or pathogen attack were collec- not mown annually, semi-woody stems can accumulate ted and transported to the lab. Immature stages were over the years, negatively impacting nesting habitat reared to adult and sent, together with field-collected for birds and hindering the grazing and movement of adults, to taxonomists for identification. Based on iden- livestock and wildlife (Renz, 2000). In addition, like tifications available thus far and combined with data of Tamarix, PPW alters habitat by increasing soil salinity opportunistic surveys during previous years (see Hinz (Blank and Young, 1997), thereby hindering regene- and Cristofaro, 2005), we reared or sampled 65 species, ration of native flora. Conventional control methods 59 of which are probably associated with plants in the are not necessarily cost-effective or environmentally family Brassicaceae. safe and must need to be repeated over several years So far, 28 species have been identified from - Ka to be successful. Therefore, CABI Europe-Switzerland zakhstan and 25 from Turkey. Interestingly, only three (CABI E-CH), Biotechnology and Biological Control insect species, based on identifications available thus Agency (BBCA) and associated collaborators formed far, were recorded from both countries, indicating the a foreign exploration consortium in 2005 to investigate existence of distinct herbivore communities in both ar- the feasibility for biological control of PPW. eas and endorsing the importance of conducting field surveys for PPW over a large geographic area. Similar Literature surveys to results of surveys on other brassica weeds (e.g. hoary cress), two thirds of insects sampled and reared are The native range and area of origin of PPW are not clearly weevils (Curculionidae; n = 30) and leaf beetles (Chrys understood because of high intraspecific variability and omelidae; n = 16). However, not all identifications have the fact that the plant has been cultivated as a spice and been completed. vegetable since the twelfth century (Hegi, 1986). The plant is probably native to central Asia, with a centre of species diversity in Tajikistan, Kazakhstan and western Kazakhstan Mongolia (E. Jäger, personal communication). In terms of potential biological control agents, Kazakh During a literature search for phytophagous organ stan is a very interesting country, presumably because isms associated with PPW, we found 23 insect species it forms part of the area of origin of PPW. Sites were (Hinz et al., 2007). Twelve of these are beetles, and relatively easy to find but never very large. PPW grow- nine are heteropterans. In addition, the list contains one ing along the roadside was usually relatively healthy or mite and eight fungal pathogens. Overall, surprisingly attacked by oligophagous or polyphagous insects, such little information is available on phytophagous organ as heteropterans. Plants with heavy insect and patho- isms and diseases associated with PPW, especially com gen damage were mostly located in natural, relatively pared to the closely related hoary cress, Lepidium draba wet areas, such as the Ili River corridor, where PPW L., another invasive perennial mustard, for which we was often growing in close vicinity or intermixed with found nearly 200 associated phytophagous organisms common reed, saltcedar and/or Russian olive. (Cripps et al., 2006). Lack of detailed investigations Of particular interest are the flea beetle Phyllotreta on PPW in its area of origin may reflect its more reitteri Heikertinger, two weevil species Lixus myagri eastern distribution and relative scarcity. This has been Olivier and Ceutorhynchus marginellus Schultze and confirmed by results of our first field surveys that have the chloropid flyLasiosina deviata Nartshuk (Table 1). already revealed new host associations with PPW (see Plants at several sites in Kazakhstan were attacked by below). a white rust, identified as Albugo candida (Pers.). The species is known to attack several crops in the mus- Field surveys tard family and is already present in several areas in the western USA. Also identified were the pycnial and In 2006, five field trips were conducted, three to cen- aecial stages of an unknown, possibly heteroecious tral and northeastern Turkey, one to southeastern Ka- rust, as well as the coelomycete fungus Septoria lepi- zakhstan and one to Bulgaria and Romania. During the dii Desmazières, reported from several species within
155 XII International Symposium on Biological Control of Weeds , perennial pepperweed, in 2006. Lepidium latifolium Overview of field surveys conducted for potential biological control agents Figure 1.
156 All against one: first results of a newly formed foreign exploration consortium
Table 1. Potential biological control agents for Lepidium latifolium, perennial pepperweed. Species Family Plant part attacked Country found in Ceutorhynchus marginellus Curculionidae Petioles, leaves, stems Kazakhstan (gall inducer) Melanobaris sp.n. semistriata Curculionidae Root, root crown Turkey Phyllotreta reitteri Chrysomelidae Stem Kazakhstan Lasiosina deviata Chloropidae Stem Turkey, Kazakhstan Aculops sp. Eriophyidae Inflorescences and leaves (?) Turkey Septoria lepidii Coelomycete leaf Kazakhstan the genus Lepidium (Cardaria). Identification of other Weevils were either released onto potted plants of disease symptoms is still under way. Small flea bee- PPW or transferred into cylinders and offered cut plant tles occurring in large numbers on PPW were also material inserted in wet florist foam blocks. Oviposi- collected. However, most of these were identified as tion occurred in the foam material, which may suggest oligophagous or polyphagous species. In addition, two that in the field,M. sp. pr. semistriata females lay eggs, weevil larvae were found mining in the root crown of not as most other weevil species into the plant tissue PPW at one site, and leaf-mining flies were collected but into the soil close to the root crown. Host-specific- at several sites. Unfortunately, none of these could be ity tests will start in 2007. reared through to adult. The weevil is very close to M. semistriata Boheman, normally developing on L. draba (hoary cress), another Turkey invasive Brassicaceae studied at CABI, but may well represent a distinct undescribed species (Korotyaev, We concentrated our surveys in eastern Turkey and unpublished data). in Central Anatolia and the Ankara region. As in Ka- zakhstan, most sites were in relatively wet areas, i.e. Ceutorhynchus marginellus along rivers, irrigation channels and sewage ditches, in both natural and urban areas. (Coleoptera: Curculionidae) Compared to Kazakhstan, plants in Turkey showed During the field trip to Kazakhstan in May 2006, less obvious signs of damage. Nevertheless, a similar we found several sites, at which PPW plants were at- number of phytophagous organisms was collected (see tacked by this gall-inducing weevil. Not much infor- above). Three potential biological control agents were mation is available on the species, except that it has found: the weevil M. sp. near semistriata Boheman, been collected previously on PPW in Russia (Isaev, the chloropid fly L. deviata and an eryophyid mite, 1994) and also occurs in Kazakhstan. Galls are formed preliminarily identified as Aculops sp. near lepidii. on leaf midribs, leaf stalks and stems, and weevil lar- Two additional species of potential interest are an as vae were mining inside. Gall induction appears to stunt yet unidentified flea beetle, Psylliodes sp., that prob- shoot growth. At one site, we also found adults of ably mines in the shoots of PPW, and the root-mining C. marginellus. Infested material and adult weevils weevil L. myagri. However, the latter is reported to be were returned to CABI’s quarantine facility in Swit- oligophagous (Dieckmann, 1983). zerland. Mature larvae left the material to pupate in the soil, and adults emerged between 12 and 27 June. Potential biological control agents Weevils were artificially overwintered in an incubator at 3°C and started to lay eggs in March 2007. Melanobaris. sp. pr. semistriata (Coleoptera: Curculionidae) Phyllotreta reitteri (Coleoptera: This root-mining weevil is recorded from several Chrysomelidae) PPW sites in Turkey, and data on its biology and phe- At two field sites in Kazakhstan in May, we found nology have been collected since 2002 (Gültekin et PPW plants that were heavily attacked by larvae of P. al., unpublished data). Adults usually become active reitteri. The species is also recorded from Uzbekistan in mid-May and feed on young petioles and the base and the Crimea Peninsula (Lopatin, 1977). No infor- of stems. In mid-June, the first larvae were found fee- mation is available on the biology of this species. We ding in the petioles. Larvae then move down to the root observed larvae mining in the stems of PPW. At one crown, where they also pupate. New generation adults site, nearly 100% of plants were attacked, and heavy emerge in the autumn. During the field trip to Turkey at attack caused the die-back of shoots. We took infested the beginning of April 2006, 28 adults were collected material back to CABI’s quarantine facility in Switzer- and taken back to Switzerland to establish a colony in land, and between 16 June and 7 July, adults emerged. quarantine and develop methods for host-specificity tests. Beetles were successfully overwintered and started to
157 XII International Symposium on Biological Control of Weeds lay eggs in March 2007. We are currently transferring from a number of Lepidium species in Europe and Asia, larvae onto potted PPW plants to establish a colony and specific host strains might exist.Septoria species, consti conduct preliminary host specificity tests. tuting the asexual stage of Mycosphaerella sp., have previously been used successfully as biological control Lasiosina deviata (Diptera: Chloropidae) agents, i.e. Septoria passifloraSyd. against the alien in- vasive Passiflora tripartita (Juss.) Poir. (Banana Poka) This chloropid stem-mining fly was reared for the in Hawaii (Julien and Griffiths, 1998). We are planning first time from PPW in June 2005 (Gültekin, unpub to collect more material in 2007 and start preliminary lished data) and later described by Nartshuk (2006). pathogenicity and host-specificity tests. During surveys in 2006, we mainly found it in central Turkey but presumably also at one field site in Kazakh stan. However, whether the flies from Kazakhstan are Conclusions and outlook exactly the same species as the ones collected in Tur- Results of these first field surveys are very promising key still needs to be confirmed. The fly can be quite and have revealed several insects and one fungal patho- frequent; for example, at one site 60% of shoots were gen with potential for biological control of perennial attacked, and up to 11 larvae were found mining in one pepperweed. We have already established colonies of stem (mean ± SE: 3.8 ± 1.1). In June, mature larvae and two species, one root-mining weevil and one stem-mining pupae were found. Unfortunately, most adults emerged flea beetle and started preliminary host-specificity tests. during the field trip and died, so no further studies In 2007, we will collect material of at least two addi could be initiated. tional species. The identification of all remaining mate- The genus Lasiosina comprises 34 species in the Pa- rial collected in 2006 will be concluded, and depending laearctic (Nartshuk, 2006). This is the first record of a on results, a revised list of potential agents prepared. In Lasiosina species from a dicotyledon plant. The flies addition, we will continue and extend field surveys to usually develop on cereals and grasses (Poaceae). We regions not yet covered, such as western China, Mon- are therefore planning to check monocot plants grow- golia, southern Russia, and southern Ukraine. Finally, ing intermixed with PPW at L. deviata field sites for at- we will collect herbarium specimens and material for tack and conduct preliminary host-specificity tests con- molecular analysis to better understand the genetic vari centrating on one or two important cereals (e.g. wheat) ability of PPW in Eurasia and the origin of invasive and grass species. Depending on results, we will make populations in North America. a decision whether L. deviata can truly be regarded as a potential biocontrol agent for PPW. Acknowledgements Aculops sp. (Aceria: Eriophyidae) We thank Ghislaine Cortat, Bethany Muffley and Cris- This eriophyid mite was only found at one field tobal Tostado for additional technical assistance in site in Central Turkey in June 2006. Plants attacked by the lab; Florence Willemin and Christian Leschenne the mites appeared to have stunted inflorescences and for plant propagation; Dr Roman V. Jashenko and showed discoloration. The species resembles A. lepidii Dr Anna Ivashenko for facilitating our field trip to Roivainen, which was originally described from a sin- Kazakhstan and providing access to the herbarium col- gle location within the Sierra Nevada, Spain (Roivai- lection in Almaty; and the following taxonomists for nen, 1953). It was only found associated with Lepidium species identifications: Prof Paolo Audisio (Nitidulidae), stylatum (Lag. et Rodr.) and is reported to attack leaves, Dr Enrico De Lillo (Acari), Dr Alexander S. Konstanti- causing abnormal pilosity, leaf margin rolling and curl nov (Alticinae) and Prof. Vera A. Richter (Syrphidae). ing. The differences in symptoms, host plant and habi- The following people kindly provided additional infor- tat conditions between A. lepidii and the mite found in mation on the distribution of L. latifolium: Dr Roman V. Turkey indicate that it is most probably a new species Jashenko, Dr Ilhan Kaya and colleagues, Prof. Sergey or subspecies. During a field trip in April to Turkey, Mosyakin, Dr Rumen Tomov, Margarita Yu Dolgov we found PPW plants with curled leaves, symptoms re- skaya and her group and Prof. Vladimir I. Dorofeyev. sembling those described for A. lepidii. More material Margarita Dolgovskaya and her group conducted a sur- will be collected and sent to taxonomists in 2007 to vey of the Russian literature on insects associated with resolve the taxonomic position of the mites found and PPW, and Prof. Dr Eckehart Jäger provided valuable to make a complete morphological description. information on the distribution and taxonomy of PPW. Dr John Gaskin volunteered to investigate the genetics Septoria lepidii of L. latifolium. Financial support for this project was provided by the Wyoming Biological Control Steering (Mycosphaerellaceae: Dothideales) Committee, the Idaho State Department of Agriculture The coelomycete Septoria lepdii was also only and the Bureau of Indian Affairs through the Univer- found at one PPW site in Kazakhstan, causing leaf- sity of Idaho, the Californian Department of Food and spots on infected host plants. Although it is reported Agriculture and the USDA-ARS Western Region Re-
158 All against one: first results of a newly formed foreign exploration consortium search Center, Reno, NV, and would not have been latifolium. A joint report prepared by CABI Europe- possible without the continuing effort and dedication Switzerland and BBCA, Rome, Italy, 23 pp. of Nancy Webber (PPW Consortium chair, WY), Mike Isaev, A.Yu. (1994) Ecological-faunistic review of weevils Pitcairn (CDFA), and Lincoln Smith and Ray Carru- (Coleoptera: Apionidae, Rhynchophoridae, Curculioni- thers (both USDA, ARS, Albany, CA). The study by dae) of Ulyanovsk Province. Priroda Ulyanovskoi Oblasti (Nature of Ulyanovsk Province) 4, 77 pp. (in Russian). B. Korotyaev was supported by the Russian Founda- Julien, M.H. and Griffiths, M.W. (1998) Biological Control tion for Basic Research (07-04-00482-a and 04-04- of Weeds. A World Catalogue of Agents and their Target 81026 Bel2004a). Weeds. Fourth Edition. CABI Publishing, Wallingford, UK, 223 pp. References Lopatin, I.K. (1977) Zhuki-listoyedy Srednei Azii i Kazakh stana: (Opredelitel’) (Leaf beetles of Middle Asia and Ka- Blank, R. and Young, J.A. (1997) Influence of invasion of pe- zakhstan: (A key)) Leningrad, 270 pp. (in Russian). rennial pepperweed on soil properties. USDA Agricultural Miller, G.K., Young, J.A. and Evans, R.A. (1986) Germina- Experiment Station, Oregon State University, Special Re- tion of seeds of perennial pepperweed (Lepidium latifo- port 972, 11–13. lium). Weed Science 34, 252–255. Cripps, M.G., Hinz, L.H., McKenney, J.L., Bradley, L., Nartshuk, E.P. (2006) A new species of grassflies of the genus Harmon, B.L., Merickel, F.W. and Schwarzlaender, M. Lasiosina Becker from Turkey (Diptera: Chloropidae). (2006) Comparative survey of the phytophagous arthro- Zoosystematica Rossica 14, 289–291. pod faunas associated with Lepidium draba in Europe and Renz, M.J. (2000) Element Stewardship abstract for Lepi- the western United States, and the potential for biologi- dium latifolium L. perennial pepperweed, tall whitetop. cal weed control. Biocontrol Science and Technology 16, The Nature Conservancy, Arlington, VA, 22 pp. 1007–1030. Renz, M.J. and DiTomaso, J.M. (1998) The effectiveness Dieckmann, L. (1983) Beiträge zur Insektenfauna der DDR. of mowing and herbicides to control perennial pepper- Coleoptera-Curculionidae (Tanymecinae, Raymondiony- weed in rangeland and roadside habitats. Proceedings minae, Bagoinae, Tanysphyrinae). Beiträge zur Entomo- from the 1998 California Weed Science Conference 50, logie 33, 128 pp. 178. Hegi, G. (1986) Illustrierte Flora von Mitteleuropa. Sperma- Roivainen, H. (1953) Some gall mites (Eriophyidae) from tophyta, Band IV Teil 1. Angiospermae, Dicotyledones 2. Spain. Archivos do Instituto de Aclimatacion 1, 9– 41. Paul Parey, Berlin, Germany, pp. 126–131. Trumbo, J. (1994) Perennial pepperweed: a threat to wildland Hinz, H.L., and Cristofaro, M. (2005) Prospects for the Bio- areas. CalEPPC Newsletter 2, 4–5. logical Control of Perennial Pepperweed, Lepidium lati- Young, J.A., Turner, C.E. and James, L.F. (1995) Perennial folium. A joint report prepared by CABI Bioscience Swit- pepperweed. Rangelands 17, 121–123. zerland Centre and BBCA, Rome, Italy, 23 pp. Young, J.A., Palmquist, D.E. and Blank, R. (1998) The ecol- Hinz, H.L., Gerber, E., Cristofaro, M. and Tronci, C. (2007) ogy and control of perennial pepperweed (Lepidium lati- Biological Control of Perennial Pepperweed, Lepidium folium L.). Weed Technology 12, 402–405.
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