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Parasites of Harmonia Axyridis: Current Research and Perspectives

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Parasites of Harmonia Axyridis: Current Research and Perspectives BioControl DOI 10.1007/s10526-016-9766-8 REVIEW Parasites of Harmonia axyridis: current research and perspectives Danny Haelewaters . Serena Y. Zhao . Susana Clusella-Trullas . Ted E. Cottrell . Andre´ De Kesel . Luka´sˇ Fiedler . Annette Herz . Helen Hesketh . Cang Hui . Regina G. Kleespies . John E. Losey . Ingrid A. Minnaar . Katie M. Murray . Oldrˇich Nedveˇd . Walter P. Pfliegler . C. Lidwien Raak-van den Berg . Eric W. Riddick . David I. Shapiro-Ilan . Rebecca R. Smyth . Tove Steenberg . Paul S. van Wielink . Sandra Vigla´sˇova´ . Zihua Zhao . Piotr Ceryngier . Helen E. Roy Received: 10 March 2016 / Accepted: 27 September 2016 Ó International Organization for Biological Control (IOBC) 2016 Abstract Harmonia axyridis (Coleoptera: Coccinellidae) study presents a review of the parasites of H. axyridis, has been introduced widely for biological control of discussing their distributions and effects on host populations agricultural pests. Harmonia axyridis has established in four across the host’s native and invasive range. These parasites continents outside of its native range in Asia and it is are: Hesperomyces virescens Thaxt. fungi, Coccipolipus considered an invasive alien species (IAS). Despite a large hippodamiae (McDaniel and Morrill) mites, and Parasity- body of work on invasion ecology, establishment mecha- lenchus bifurcatus Poinar and Steenberg nematodes. nisms of IAS and their interactions with natural enemies remain open questions. Parasites, defined as multicellular Keywords Coccipolipus hippodamiae Á Enemy organisms that do not directly kill the host, could potentially release hypothesis Á Harmonia axyridis Á play an important role in regulating host populations. This Hesperomyces virescens Á Parasites Á Parasitylenchus bifurcatus Electronic supplementary material The online version of this article (doi:10.1007/s10526-016-9766-8) contains supple- mentary material, which is available to authorized users. Handling Editor: Lori-Jayne Lawson Handley. D. Haelewaters (&) A. De Kesel Department of Organismic and Evolutionary Biology, Botanic Garden Meise, Meise, Belgium Harvard University, Cambridge, MA, USA e-mail: [email protected] L. Fiedler Gymna´zium Jı´rovcova and University of South Bohemia, S. Y. Zhao Ceske Budejovice, Czech Republic Department of Integrative Biology, The University of Texas at Austin, Austin, TX, USA A. Herz Á R. G. Kleespies Institute for Biological Control, Federal Research Centre S. Clusella-Trullas Á I. A. Minnaar for Cultivated Plants, Julius Ku¨hn-Institute, Darmstadt, Centre for Invasion Biology, Department of Botany and Germany Zoology, Stellenbosch University, Stellenbosch, South Africa H. Hesketh Á H. E. Roy Centre for Ecology & Hydrology, Wallingford, UK T. E. Cottrell Á D. I. Shapiro-Ilan Southeastern Fruit and Tree Nut Research Laboratory, Agricultural Research Service, United States Department of Agriculture, Byron, GA, USA 123 D. Haelewaters et al. Introduction Wyoming as the only contiguous state without a record (Roy et al. 2016). In Europe, H. axyridis was first The harlequin or multicoloured Asian ladybird Har- recorded in the wild in 1999 in Germany (Brown et al. monia axyridis (Pallas) (Coleoptera: Coccinellidae) is 2008) and is now considered established in over 30 a striking example of a biological introduction with countries (Aysal and Kivan 2014; Havelka et al. 2015; unintended ecological consequences. H. axyridis is Kulijer 2016; reviewed in Roy et al. 2016). The first native to vast areas in temperate and subtropical South American (Argentina) record was made in 2001 (southeastern) Asia, from the Japanese archipelago (Lombaert et al. 2010;Stals2010). In Africa, H. and Kuril Islands in the east to Western Siberia in the axyridis is known to be most widespread in South west, with the southernmost localities reported from Africa where it was first recorded in 2001 (Stals 2010; southern China and Vietnam (Orlova-Bienkowskaja Roy et al. 2016). Larvae of H. axyridis were observed et al. 2015). The most western localities reported by for the first time in New Zealand in 2016 (http:// Orlova-Bienkowskaja et al. (2015) lie in longitudes of naturewatch.org.nz/observations/3175895), marking about 72° E, but some authors (Tyumaseva 1997; the first Oceanian report for this ladybird species. H. Pekin 2007; Khabibullin et al. 2009) report H. axyridis axyridis is highly competitive with native ladybird as far east as the Ural Mountains (approximate species and its strong dispersal capacities allow it to longitude 55° E). It was introduced repeatedly into rapidly expand its range into new regions (Roy et al. the USA beginning in 1916 and in Western Europe 2016). Being a globally invasive alien species (IAS) its since the 1980s where it was used as a biocontrol agent impacts are considered ‘‘immense, insidious, and usu- against aphids and scale insects. ally irreversible’’ (Invasive Species Specialist Group Multiple introductions of H. axyridis to the USA 2000). H. axyridis has negative effects not only on non- occurred, with distinct founding populations in eastern target insect species (including a decline of native and western states (Lombaert et al. 2010). Expansion of ladybird populations), but also on the food industry and H. axyridis populations across regions in the USA human health (Koch and Galvan 2008). Therefore, it is occurred fastest in states with a preponderance of relevant to determine which natural enemies could have biomes similar to its native habitats in Asia (Koch et al. a role in regulating its populations. 2006). H. axyridis was first reported as established in the Despite a few studies focusing on the suite of USA in 1988 in southeastern Louisiana and in 1990 in natural enemies of H. axyridis (Roy and Cottrell eastern Mississippi (Chapin and Brou 1991). H. axyridis 2008; Riddick et al. 2009; Roy et al. 2011;Ceryngier has been found in 47 of the 48 contiguous states, leaving C. Hui C. L. Raak-van den Berg Centre for Invasion Biology, Department of Mathematical Laboratory of Entomology, Wageningen University, Sciences, Stellenbosch University, and African Institute Utrecht, The Netherlands for Mathematical Sciences, Stellenbosch, South Africa C. L. Raak-van den Berg J. E. Losey Á R. R. Smyth Netherlands Food and Consumer Product Safety Department of Entomology, Cornell University, Ithaca, Authority, Utrecht, The Netherlands NY, USA E. W. Riddick K. M. Murray Agricultural Research Service, National Biological Biological and Environmental Sciences, Stirling Control Laboratory, United States Department of University, Stirling, UK Agriculture, Stoneville, MS, USA O. Nedveˇd T. Steenberg University of South Bohemia and Institute of Department of Agroecology, University of Aarhus, Entomology, Ceske Budejovice, Czech Republic Aarhus, Denmark W. P. Pfliegler P. S. van Wielink Department of Biotechnology and Microbiology, Tobias Asserlaan 126, 5056 VD Berkel-Enschot, The University of Debrecen, and Postdoctoral Fellowship Netherlands Programme of the Hungarian Academy of Sciences (MTA), Debrecen, Hungary 123 Parasites of Harmonia axyridis: current research and perspectives et al. 2012; Ceryngier and Twardowska 2013), there Hesperomyces virescens (Ascomycota: is a need for a global overview that includes all Laboulbeniales: Laboulbeniaceae) reported localities and consideration of biological control potential. Here we present an overview of the Hesperomyces virescens is an obligate ectoparasite parasites of H. axyridis and their known global that has been reported to infect adults of over 30 distribution. ladybird species (Coleoptera: Coccinellidae). In addition to the hosts reported by Santamarı´a et al. (1991) and Ceryngier et al. (2012), the ladybird Definitions genera Azya, Epilachna, and Halyzia were recently observed to be hosts of H. virescens (Haelewaters We restrict usage of the term ‘‘parasites’’ to those and van Wielink 2016; Haelewaters unpublished). organisms living at the expense of a single host, which H. virescens completes its entire life cycle on the are multicellular (in contrast to pathogenic microor- integument of a living host where individual ganisms) and do not directly cause death of the host (in yellowish-greenish thalli are formed directly from contrast to parasitoids) (Vinson and Iwantsch 1980; ascospores (detailed morphology in De Kesel 2011). van den Bosch et al. 1982; Godfray 1994; Federici These thalli can be formed on any part of the body 2009). Of the parasites so defined, three species are of the insect (Haelewaters et al. 2012) and penetrate known to attack H. axyridis: the fungus Hesperomyces the insect cuticle by formation of a haustorium virescens Thaxt., the mite Coccipolipus hippodamiae consisting of rhizoids of about 3 lm in diameter (McDaniel and Morrill), and the nematode Parasity- (Weir and Beakes 1996). The development from lenchus bifurcatus Poinar & Steenberg. ascospore into mature thallus can take place at Under this definition, P. bifurcatus (Nematoda: temperatures ranging from 10–30 °C. Under labora- Allantonematidae) is a typical member of parasitic tory conditions at 25 °C this requires 13–26 days nematodes, unlike entomopathogenic nematodes depending on the host species (Cottrell and Riddick (Heterorhabitidae and Steinernematidae), which form 2012). The sticky spores of H. virescens have a associations with mutualistic bacteria in the genera short life span and are exclusively spread by Photorhabdus and Xenorhabdus (Grewal et al. 2005). activities of the host (De Kesel 1995; Cottrell and Entomopathogenic nematodes
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