Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-17T14:38:32.253Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic and morphological studies of Trichosirocalus species introduced to North America, Australia and New Zealand for the biological control of thistles

Published online by Cambridge University Press:  09 November 2015

A. De Biase ,
E. Colonnelli ,
S. Belvedere ,
A. La Marca ,
M. Cristofaro  and
L. Smith
A. De Biase*
Affiliation:
Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università di Roma La Sapienza, Viale dell'Università 32, 00185 Rome, Italy
E. Colonnelli
Affiliation:
Via delle Giunchiglie 56, 00172 Rome, Italy
S. Belvedere
Affiliation:
Dipartimento di Biologia e Biotecnologie ‘Charles Darwin’, Università di Roma La Sapienza, Viale dell'Università 32, 00185 Rome, Italy
A. La Marca
Affiliation:
BBCA-onlus, Via Angelo Signorelli 105, 00123 Rome, Italy
M. Cristofaro
Affiliation:
ENEA C.R. Casaccia SSPT-BIOAG-PROBIO, Via Anguillarese 301, 00123 S. Maria di Galeria (Rome), Italy
L. Smith
Affiliation:
USDA-ARS, 810 Avenue du Campus Agropolis, 34980 Montferrier-sur-Lez, France
*
*Author for correspondence A. De Biase Phone: +39 0649914744 Fax: +39 064958259 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Trichosirocalus horridus sensu lato has been used as a biological control agent of several invasive thistles (Carduus spp., Cirsium spp. and Onopordum spp.) since 1974. It has been recognized as a single species until 2002, when it was split into three species based on morphological characters: T. horridus, Trichosirocalus briesei and Trichosirocalus mortadelo, each purported to have different host plants. Because of this taxonomic change, uncertainty exists as to which species were released in various countries; furthermore, there appears to be some exceptions to the purported host plants of some of these species. To resolve these questions, we conducted an integrative taxonomic study of the T. horridus species complex using molecular genetic and morphological analyses of specimens from three continents. Both mitochondrial cytochrome c oxidase subunit I and nuclear elongation factor 1α markers clearly indicate that there are only two distinct species, T. horridus and T. briesei. Molecular evidence, morphological analysis and host plant associations support the synonymy of T. horridus (Panzer, 1801) and T. mortadelo Alonso-Zarazaga & Sánchez-Ruiz, 2002. We determine that T. horridus has been established in Canada, USA, New Zealand and Australia and that T. briesei is established in Australia. The former species was collected from Carduus, Cirsium and Onopordum spp. in the field, whereas the latter appears to be specific to Onopordum.

Keywords

biological controlmolecular taxonomysynonymythistlesTrichosirocalus horridus species complexweevils
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 106 , Issue 1 , February 2016 , pp. 99 - 113
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alonso-Zarazaga, M.A. & Sánchez-Ruiz, M. (2002) Revision of the Trichosirocalus horridus (Panzer) species complex, with description of two new species infesting thistles (Coleoptera: Curculionidae, Ceutorhynchinae). Australian Journal of Entomology 41, 199–208.Google Scholar
Alonso-Zarazaga, M.A., Sánchez-Ruiz, M. & Domingo-Quero, T. (2006) Lista preliminar de los Curculionidea (Coleoptera) de la Comunidad de Madrid (España). Graellsia 62 (número extraordinario), 43–52.Google Scholar
Alziar, G. & Lemaire, J.-M. (2012) Les missions entomologiques du Muséum d'Histoire Naturelle de Nice (France) 2004–2010. Biocosme Mésogéen 29, 57–104.Google Scholar
Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M.T., Balke, M., Hendrich, L., Geijer, J., Herrmann, J., Foster, G.N., Ribera, I., Nilsson, A., Barraclough, T.G. & Vogler, A.P. (2012) The effect of geographical scale of sampling on DNA barcoding. Systematic Biology 61, 851–869.Google Scholar
Blaxter, M.L. (2004) The promise of a DNA taxonomy. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 359, 669–679.Google Scholar
Boldt, P.E. & Campobasso, G. (1978) Phytophagous insects on Carduus macrocephalus in Italy. Environmental Entomology 7, 904–909.Google Scholar
Boldt, P.E. & Campobasso, G. (1981) Biology of two weevils, Ceutorrhynchus trimaculatus and Trichosirocalus horridus, on Carduus spp. in Europe. Environmental Entomology 10, 691–696.Google Scholar
Boldt, P.E., Campobasso, G. & Colonnelli, E. (1980) Palearctic distribution and host plants of Ceutorhynchus trimaculatus and Trichosirocalus horridus (Coleoptera: Curculionidae). Annals of the Entomological Society of America 73, 694–698.Google Scholar
Briese, D.T. (2012) Onopordum acanthium L. – Scotch thistle Onopordum illyricum L. – Illyrian thistle hybrids. pp. 416–424 in Julien, M.H., McFadyen, R. & Cullen, J. (Eds) Biological Control of Weeds in Australia. Collingwood, Victoria, CSIRO Publishing.Google Scholar
Briese, D.T., Sheppard, A.W., Zwölfer, H. & Boldt, P.E. (1994) Structure of the phytophagous insect fauna of Onopordum thistles in the northern Mediterranean basin. Biological Journal of the Linnean Society 53, 231–253.Google Scholar
Briese, D.T., Pettit, W.J., Swirepik, A. & Walker, A. (2002 a) A strategy for the biological control of Onopordum spp. thistles in south-eastern Australia. Biocontrol Science and Technology 12, 121–136.Google Scholar
Briese, D.T., Thomann, T. & Vitou, J. (2002 b) Impact of the rosette crown weevil Trichosirocalus briesei on the growth and reproduction of Onopordum thistles. Journal of Applied Ecology 39, 688–698.Google Scholar
Briese, D.T., Walker, A., Pettit, W.J. & Sagliocco, J.L. (2002 c) Host-specificity of candidate agents for the biological control of Onopordum spp. thistles in Australia: an assessment of testing procedures. Biocontrol Science and Technology 12, 149–163.Google Scholar
Colonnelli, E. (2004) Catalogue of Ceutorhynchinae of the World, With a Key to Genera (Insecta: Coleoptera: Curculionidae). pp. 1–124. Barcelona, Spain, Argania editio.Google Scholar
Colonnelli, E. (2013) Subfamily Ceutorhynchinae Gistel, 1848. pp. 176–214 in Löbl, I. & Smetana, A. (Eds) Catalogue of Palaeartic Coleoptera, Curculionoidea II. Leiden, Netherlands, Brill.Google Scholar
Cristofaro, M., De Biase, A. & Smith, L. (2013) Field release of a prospective biological control agent of weeds, Ceratapion basicorne, to evaluate potential risk to a nontarget crop. Biological Control 64, 305–314.Google Scholar
Cullen, J.M. & Sheppard, A.W. (2012) Carduus nutans L. – nodding thistle. pp. 118–130 in Julien, M.H., McFadyen, R.E.C. & Cullen, J.M. (Eds) Biological Control of Weeds in Australia. Collingwood, Victoria, CSIRO Publishing.Google Scholar
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.Google Scholar
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.Google Scholar
De Clerck-Floate, R. & Cárcamo, H. (2011) Biocontrol arthropods: new denizens of Canada's grassland agroecosystems. pp. 291–321 in Floate, K.D. (Ed.) Arthropods of Canadian Grasslands (Volume 2): Inhabitants of a Changing Landscape. Ottawa, Canada, Biological Survey of Canada.Google Scholar
DeSalle, R. (2006) Species discovery versus species identification in DNA barcoding efforts: response to Rubinoff. Conservation Biology, 20, 1545–1547.Google Scholar
DeSalle, R., Egan, M.G. & Siddall, M. (2005) The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society of London B: Biological Sciences 360, 1905–1916.Google Scholar
Dieckmann, L. (1972) Beiträge zur Insektenfauna der DDR: Coleoptera – Curculionidae: Ceutorhynchinae. Beiträge zur Entomologie 22, 3–128.Google Scholar
Drummond, A.J., Suchard, M.A., Xie, D. & Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.Google Scholar
Ence, D.D. & Carstens, B.C. (2011) SpedeSTEM: a rapid and accurate method for species delimitation. Molecular Ecology Resources 11, 473–480.Google Scholar
Ezard, T., Fujisawa, T. & Barraclough, T.G. (2009) SPLITS: SPecies’ LImits by Threshold Statistics. R package. Version 1.0–18/r45. Available online at http://R-Forge.R-project.org/projects/splits/ (accessed June 2013).Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fontaneto, D., Herniou, E.A., Boschetti, C., Caprioli, M., Melone, G., Ricci, C. & Barraclough, T.G. (2007) Independently evolving species in asexual bdelloid rotifers. PLoS Biology 5, e87.Google Scholar
Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent (GMYC) approach: a revised method and evaluation on simulated datasets. Systematic Biology 62, 707–724.Google Scholar
Fujita, M.K., Leaché, A.D., Burbrink, F.T., McGuire, J.A. & Moritz, C. (2012) Coalescent-based species delimitation in an integrative taxonomy. Trends in Ecology and Evolution 27, 480–488.Google Scholar
Fumanal, B., Martin, J.-F. and Bon, M.C. (2005) High through-put characterization of insect morphocryptic entities by a non-invasive method using direct-PCR of fecal DNA. Journal of Biotechnology 119, 15–19.Google Scholar
Gaskin, J.F., Bon, M.C., Cock, M.J., Cristofaro, M., De Biase, A., De Clerck-Floate, R., Ellison, C.A., Hinz, H.L., Hufbauer, R.A., Julien, M.H. & Sforza, R. (2011) Applying molecular-based approaches to classical biological control of weeds. Biological Control 58, 1–21.Google Scholar
Groenteman, R., Kelly, D., Fowler, S.W. & Bourdôt, G.V. (2008) Which species of the thistle biocontrol agent Trichosirocalus are present in New Zealand?. pp. 145–149 in Julien, M.H., Sforza, R., Bon, M.C., Evans, H.C., Hatcher, P.E., Hinz, H.L. & Rector, B.G. (Eds) Proceedings of the XIIth International Symposium on Biological Control of Weeds, La Grande Motte, France, 22–27 April 2007. UK, CAB International Wallingford.Google Scholar
Harris, P. (1984) Carduus nutans L., nodding thistle and C. acanthoides L., plumeless thistle (Compositae). pp. 115–126 in Kelleher, J.S. & Hulme, M.A. (Eds) Biological Control Programs against Insects and Weeds in Canada, 1969–1980. Slough, UK, CAB.Google Scholar
Hebert, P.D., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biology 2, e312.Google Scholar
Hernández-Vera, G., Mitrović, M., Jović, J., Toševski, I., Caldara, R., Gassmann, A. & Emerson, B.C. (2010) Host-associated genetic differentiation in a seed parasitic weevil Rhinusa antirrhini (Coleptera: Curculionidae) revealed by mitochondrial and nuclear sequence data. Molecular Ecology 19, 2286–2300.Google Scholar
Hoffmann, A. (1955) Faune de France. 59. Coléoptères curculionides (Deuxième partie). pp. 487–1207. Paris, France, Lechevalier.Google Scholar
Hudson, R.R. 1991. Gene genealogies and coalescent process. pp. 1–44 in Futuyma, D.J. & Antonivics, J. (Eds) Oxford Surveys in Evolutionary Biology. Oxford, UK, Oxford University Press.Google Scholar
Janzen, D.H. (2004) Now is the time. Philosophical Transactions of the Royal Society B: Biological Sciences 359, 731.Google Scholar
Jessep, C.T. (1989) Introduction of the crown weevil (Trichosirocalus horridus) as an additional biocontrol agent against nodding thistle. Proceedings of New Zealand Weed and Pest Control Conference, vol 42, 52–54.Google Scholar
Kingman, J.F. (1982) The coalescent. Stochastic Processes and their Applications 13, 235–248.Google Scholar
Kleine, R. (1910) Die Lariiden und Rhynchophoren und ihre Nahrungspflanzen (Fortsetzung.). Entomologische Blätter 6, 231–244.Google Scholar
Kok, L.T. (1975) Host specificity studies on Ceuthorhynchidius horridus (Panzer) (Coleoptera: Curculionidae) for the biological control of musk and plumeless thistle. Weed Research 15, 21–25.Google Scholar
Kok, L.T. (1978) Biological control of Carduus thistles in northeastern USA. pp. 101–104 in Freeman, T.E. (Ed.) Proceedings of the IVth International Symposium on Biological Control of Weeds. Center for Environmental Programs, Institute of Food and Agricultural Sciences, Florida University. 30 August–2 September 1976, Gainesville, Florida.Google Scholar
Kok, L.T. (2001) Classical biological control of nodding and plumeless thistles. Biological Control 21, 206–213.Google Scholar
Kok, L.T. & Mays, W.T. (1989) Comparison of the seasonal occurrence of Trichosirocalus horridus (Panzer) (Coleoptera: Curculionidae) in Virginia between 1981–83 and 1979. Journal of Entomological Science 24, 465–471.Google Scholar
Kok, L.T. & Trumble, J.T. (1979) Establishment of Ceuthorhynchidius horridus (Coleoptera: Curculionidae), an imported thistle-feeding weevil, in Virginia. Environmental Entomology 8, 221–223.Google Scholar
Madeira, P.T., Tipping, P.W., Gandolfo, D.E., Center, T.D., Van, T.K. & O'Brien, C.W. (2006) Molecular and morphological examination of Cyrtobagous spp. collected from Argentina, Paraguay, Brazil, Australia, and Florida. BioControl 51, 679–701.Google Scholar
May, B.M. (1993) Larvae of Curculionoidea (Insecta: Coleoptera): a Systematic Overview. Fauna of New Zealand Number 28. Lincoln, Canterbury, Manaaki Whenua Press.Google Scholar
McAvoy, T.J., Kok, L.T. & Mays, W.T. (1987) Dispersal of Trichosirocalus horridus (Panzer) (Coleoptera: Curculionidae) in Southwest Virginia. Journal of Entomological Science 22, 324–329.Google Scholar
Monaghan, M.T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D.J., Lees, D.C., Ranaivosolo, R., Eggleton, P., Barraclough, T.G. & Vogler, A.P. (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.Google Scholar
Moritz, C. & Cicero, C. (2004) DNA barcoding: promise and pitfalls. PLoS Biology 2, e354.Google Scholar
Mound, L.A., Wheeler, G.S. & Williams, D.A. (2010) Resolving cryptic species with morphology and DNA; thrips as a potential biocontrol agent of Brazilian peppertree, with a new species and overview of Pseudophilothrips (Thysanoptera). Zootaxa 2432, 59–68.Google Scholar
Mullis, K.B., Faloona, F.A., Scharf, S.J., Saiki, R.K., Horn, G.T. & Erlich, H. (1986) Specific enzymatic amplification of DNA in vitro: the polymerase chain reaction. Cold Spring Harbor Symposia on Quantitative Biology 51, 263–273.Google Scholar
Nee, S. (1994) Extinction rates can be estimated from molecular phylogenies. Philosophical Transactions of the Royal Society B: Biological Sciences 344, 77–82.Google Scholar
Nee, S. (2001) Inferring speciation rates from phylogenies. Evolution 55, 661–668.Google Scholar
Nee, S., May, R.M. & Harvey, P.H. (1994) The reconstructed evolutionary process. Philosophical Transactions of the Royal Society B: Biological Sciences 344, 305–311.Google Scholar
Padial, J.M., Miralles, A., De la Riva, I. & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology 7, 1–14.Google Scholar
Pelletier, J. (2012) Les Curculionidae du Maroc: addition et correction au catalogue de Kocher (5e note). L'Entomologiste 67, 217–225.Google Scholar
Perris, É. (1877) Larves des coléoptères. Annales de la Société linnéenne de Lyon 23, 1–430.Google Scholar
Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595–609.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, Automatic Barcode Gap Discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.Google Scholar
Pullen, K.R., Jennings, D. & Oberprieler, R.G. (2014) Annotated catalogue of Australian weevils (Coleoptera: Curculionoidea). Zootaxa 3896, 1–481.Google Scholar
Rambaut, A., Suchard, M. & Drummond, A. (2013) Tracer v1.6. Available online at http://tree.bio.ed.ac.uk/software/tracer/ Google Scholar
Rector, B.G., De Biase, A., Cristofaro, M., Primerano, S., Belvedere, S., Antonini, G. & Sobhian, R. (2010) DNA fingerprinting to improve data collection efficiency and yield in an open-field host-specificity test of a weed biological control candidate. Invasive Plant Science and Management 3, 429–439.Google Scholar
Rheinheimer, J. & Hassler, M. (2010) Die Rüsselkäfer Baden-Württembergs. Heidelberg, Germany, Verlag Regionalkultur.Google Scholar
Rizza, A. & Spencer, N.R. (1981) Field tests with the musk thistle insects, Trichosirocalus (Ceuthorrhynchidius) horridus and Ceutorrhynchus trimaculatus to determine their impact on artichoke. Environmental Entomology 10, 332–334.Google Scholar
Sagliocco, J.L., Kwong, R.M. & Morley, T. (2012) Cirsium vulgare (Savi) Tenore–spear thistle. pp. 184–189 in Julien, M., McFadyen, R. & Cullen, J. (Eds) Biological control of weeds in Australia. Clayton, Australia, CSIRO Publishing.Google Scholar
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Scherf, H. (1964) Die Entwicklungsstadien der mitteleuropäischen Curculioniden (Morphologie, Bionomie, Ökologie). Abhandlungen der Senckenbergischen Naturforschenden Gesellschaft 506, 1–335.Google Scholar
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651–701.Google Scholar
Staden, R., Beal, K.F. & Bonfield, J.K. (1999) The Staden Package. 1998. pp. 115–130 in Misener, S. & Krawetz, S.A. (Eds), Bioinformatics Methods and Protocols, Methods in Molecular Biology, Vol. 132. Totowa, NJ, The Humana Press Inc.Google Scholar
Stephens, M., Smith, N. & Donnelly, P. (2001) A new statistical method for haplotype reconstruction from population data. American Journal of Human Genetics 68, 978–989.Google Scholar
Takahashi, M., Louda, S.M., Miller, T.E.X. & O'Brien, C.W. (2009) Occurrence of Trichosirocalus horridus (Coleoptera: Curculionidae) on native Cirsium altissimus versus exotic C. vulgare in North American tallgrass prairie. Environmental Entomology 38, 731–740.Google Scholar
Talavera, G., Dincă, V. & Vila, R. (2013) Factors affecting species delimitations with the GMYC model: insights from a butterfly survey. Methods in Ecology and Evolution 4, 1101–1110.Google Scholar
Tamura, K., Dudley, J., Nei, M. & Kumar, S. (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599.Google Scholar
Tautz, D., Arctander, P., Minelli, A., Thomas, R.H. & Vogler, A.P. (2003) A plea for DNA taxonomy. Trends in Ecology and Evolution 18, 70–74.Google Scholar
Trumble, J.T. & Kok, L.T. (1979) Ceuthorhynchidius horridus (Coleoptera: Curculionidae): life cycle and development on Carduus thistles in Virginia. Annals of the Entomological Society of America 72, 563–564.Google Scholar
Villesen, P. (2007) FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes 7, 965–968.Google Scholar
Wagner, H. (1944) Über das Sammeln von Ceuthorrhynchinen. Koleopterologische Rundschau 30, 125–142.Google Scholar
Wakeley, J. (2008) Coalescent Theory: An Introduction. Greenwood Village, Colorado, Roberts & Company Publishers.Google Scholar
Ward, R.H., Pienkowski, R.L. & Kok, L.T. (1974) Host specificity of the first-instar of Ceuthorhynchidius horridus, a weevil for biological control of thistles. Journal of Economic Entomology 67, 735–737.Google Scholar
Wheeler, D.L., Barrett, T., Benson, D.A., Bryant, S.H., Canese, K., Chetvernin, V., Church, D.M., Dicuccio, M., Edgar, R., Federhen, S., Geer, L.Y., Kapustin, Y., Khovayko, O., Landsman, D., Lipman, D.J., Madden, T.L., Maglott, D.R., Ostell, J., Miller, V., Pruitt, K.D., Schuler, G.D., Sequeira, E., Sherry, S.T., Sirotkin, K., Souvorov, A., Starchenko, G., Tatusov, R.L., Tatusova, T.A., Wagner, L. & Yaschenko, E. (2007) Database resources of the National Center for Biotechnology Information. Nucleic Acids Research 35, D5–D12.Google Scholar
Wiens, J.J. (2007) Species delimitation: new approaches for discovering diversity. Systematic Biology 56, 875–878.Google Scholar
Wiggins, G.J., Grant, J.F., Lambdin, P.L., Ranney, J.W. & Wilkerson, J.B. (2009) First documentation of adult Trichosirocalus horridus on several non-target native Cirsium species in Tennessee. Biocontrol Science and Technology 19, 993–998.Google Scholar
Woodburn, T. & Swirepik, A. (2002) Establishment of the crown weevil Trichosirocalus horridus on a novel host, Cirsium vulgare in Western Australia. p. 430 in Spafford Jacob, H., Dodd, J. & Moore, J.H. (Eds) Proceedings of the 13th Australian Weeds Conference, 8–13 September 2002, Perth, Western Australia. Plant Protection Society of Western Australia.Google Scholar
Woodburn, T.L. (1997) Establishment in Australia of Trichosirocalus horridus a biological control agent for Carduus nutans, and preliminary assessment of its impact on plant growth and reproductive potential. Biocontrol Science and Technology 7, 645–656.Google Scholar
Yule, G.U. (1925) A mathematical theory of evolution, based on the conclusions of Dr JC Willis, FRS. Philosophical Transactions of the Royal Society of London. Series B, Containing Papers of a Biological Character 213, 21–87.Google Scholar
Zwölfer, H. (1965) Preliminary list of phytophagous insects attacking wild Cynareae (Compositae) in Europe. Technical Bulletin Commonwealth Institute of Biological Control 6, 81–154.Google Scholar
Supplementary material: File

De Biase supplementary material

Table S1

Download De Biase supplementary material(File)
File 12 KB
Supplementary material: File

De Biase supplementary material

Table S2

Download De Biase supplementary material(File)
File 15.9 KB
Supplementary material: File

De Biase supplementary material

Table S3

Download De Biase supplementary material(File)
File 15.2 KB