IOBC-WPRS Working Group “Benefits and Risks of Exotic Biological Control Agents”
Proceedings of the fourth meeting
at / à
Ponta Delgada, Azores (Portugal)
September 12 - 14, 2018
Edited by: Danny Haelewaters Jana Collatz
IOBC-WPRS Bulletin Bulletin OILB-SROP Vol. 145, 2019 The content of the contributions is in the responsibility of the authors.
The IOBC-WPRS Bulletin is published by the International Organization for Biological and Integrated Control of Noxious Animals and Plants, West Palearctic Regional Section (IOBC-WPRS).
Le Bulletin OILB-SROP est publié par l‘Organisation Internationale de Lutte Biologique et Intégrée contre les Animaux et les Plantes Nuisibles, section Regionale Ouest Paléarctique (OILB-SROP).
Copyright: IOBC-WPRS 2019
The Publication Commission of the IOBC-WPRS:
Dr. Ute Koch Dr. Annette Herz Schillerstrasse 13 Julius Kühn-Institute D-69509 Moerlenbach (Germany) Federal Research Center of Cultivated Plants Tel +49-6209-1079 Institute for Biological Control e-mail: [email protected] Heinrichstr. 243 D-64287 Darmstadt (Germany) Tel +49-6151-407-236, Fax +49-6151-407-290 e-mail: [email protected]
Address General Secretariat:
Dr. Gerben Messelink Wageningen UR Greenhouse Horticulture Violierenweg 1 P.O. Box 20 NL-2665 ZG Bleiswijk, The Netherlands Tel.: +31 (0) 317-485649 e-mail: [email protected]
ISBN 978-92-9067-330-9 Web: http://www.iobc-wprs.org Darmstadt, 2019
Preface
A 2007 informal meeting in Brussels, Belgium saw the formation of the IOBC-WPRS Working Group “Benefits and Risks of Exotic Biological Control Agents”. Since then, four formal Working Group meetings have been organized: in 2009 in Engelberg, Switzerland; in 2011 in Hluboká, Czech Republic; in 2015 on Bornholm, Denmark; and in 2018 in Ponta Delgada on the island of São Miguel of the Azores Archipelago, Portugal. These meetings have had the following foci: (1) characteristics of exotic natural enemies that are considered to be successful biological control agents, (2) characteristics of exotic natural enemies introduced into a country as biological control agents that subsequently have become invasive alien species, (3) research areas requiring attention and strategies to support priority research, and (4) the development of guidelines assessing environmental benefits and risks of exotic biological control agents. This IOBC-WPRS Bulletin comprises a collection of papers and extended abstracts resulting from the fourth meeting of the Working Group at the Ponta Delgada campus of the University of the Azores. The Bulletin bundles a total of 22 contributions by researchers from 10 countries in Europe but also from North America (USA), South America (Argentina and Chile), and western Asia (Iran). Most of the contributions focus on the harlequin ladybird Harmonia axyridis, flagship species for biological control gone awry. However, it is not surprising that many ladybird researchers submitted (preliminary) results of their work; the Working Group meeting was preceded by the IUCN Red List Training Course for members of the newly formed IUCN SSC Ladybird Specialist Group. The aims of this training were twofold – to offer an introduction to using the IUCN Red List categories and criteria and to provide a forum for discussion of best practices addressing important ladybird conservation issues. On behalf of all attendees, we congratulate the Scientific and Organizing Committees of the Working Group meeting in Ponta Delgada for a stimulating and informative meeting: Dr. Isabel Borges, Enésima P. Mendonça, Dr. António Onofre Soares (University of the Azores, Portugal), Dr. Peter M. J. Brown (Anglia Ruskin University, UK), Dr. Audrey A. Grez (Universidad de Chile, Chile), Dr. Peter G. Mason (Ottawa Research and Development Centre, Canada), and Dr. Helen E. Roy (Centre for Ecology & Hydrology, UK).
Danny Haelewaters Olga M. C. C. Ameixa
I II
Introductory remarks: Benefits and risks of exotic biological control agents
Firstly, I would like to thank the Scientific and Organizing Committees of this Working Group meeting for the invitation to be part of this international meeting about the benefits and risks of the exotic agents of biological control. This event certainly honours the Autonomous Region of the Azores, the University of the Azores and the scientific community that studies this Region. This is evidence that here in the Azores, we have exceptional conditions to welcome more and more such international events, the result of our unique location between the American and European continents, the ease of incoming flight routes from diverse destinations, and the hospitality of the Azorean people. In the last few years, certain pesticides have been removed from the market, in great measure because of the high standards demanded by community legislation. Using biological organisms – such as insects, bacteria, fungi, among many others – is an important and useful alternative to chemical control. Indeed, these are renewable natural resources acting in a way that has been shown to be beneficial in the limitation and control of pests. The use of these organisms is an important and valuable tool for agriculture. However, biological control programs need to be further developed in the Azores Autonomous Region, which is increasingly biological and chemical-free. The international meetings of the IOBC-WPRS Working Group “Benefits and Risks of Exotic Biological Control Agents” therefore are extremely important to discuss a matter of huge relevance to society, with maximum scientific accuracy. These meetings help to disseminate the work done in this area. The connection between scientific studies and society is becoming increasingly important to avoid false alarms in public opinion, which is sometimes based on positions without any technical foundation (so-called “fake news”). The use of plant protection products involves highly regulated criteria, with high safety standards for both applicators and the environment. The Azores Autonomous Region is part of the European Union; European Union law and rules apply to the Azores under the Treaty on the Functioning of the European Union. As we know, any type of border controls has been abolished within the European Union (or to be more precise, within the Schengen Area). In other words, when importing or exporting produce, it is unquestionable that all the rules in terms of food safety have been assured. The government of the Azores has made a strong commitment to the training of farmers, not only to make them more qualified, but also to allow greater awareness of risk factors, such as accidental introductions of new pests and diseases. In the last two years, more than 250 training actions have been promoted especially dedicated to the application of plant protection products, involving 2,600 trainees and over 4,000 hours of training. At the same time, every year, control and inspection actions are promoted, ranging from producers to service providers and municipalities. In this regard, I would like to underline the good work Azorean public administration technicians are doing, particularly those working in the regional laboratories, resulting in the Azores to be regarded as a model case. The results speak for themselves. In the Azores, the number of plant products with pesticides above the legal limits has been residual. In addition, the number of violations detected by analyses of samples collected in products of plant origin has decreased substantially. For example, no violations were detected in 2015, and in both 2016 and 2017, only a single infraction was registered. These indicators reflect the focus of the public entities as well as the efforts that have been made towards supervision and monitoring to guarantee high-quality agricultural production and food security in the Region. III
It is up to politicians to make decisions. However, decisions must be based on theoretical and scientific knowledge; the Azorean Regional Government relies on the research presented here and elsewhere, which provides technical advice to better define regional policies on agriculture. It is necessary to mention that the Azores Autonomous Region has already started projects in the field of organic farming, both in terms of horticulture and organic meat production. The Regional Government of the Azores has sought to do its part in terms of organic farming with all determination. A working group was created to develop a Regional Strategy for the Development of Organic Agriculture of the Azores (see Lopes, 2019 elsewhere in this Bulletin). This working group has already delivered the final document to the Regional Directorate for Agriculture after including the contributions received from the public discussion stage. It is now the stage of appreciation and validation of the document, and the final version of the agriculture development strategy in the Azores should be announced later this year. The strategic document defines five important and strategic objectives: promoting the expansion of biological production areas, increasing the production of and the supply of agricultural and agro-food products from organic production, promoting technical and scientific knowledge, stimulating business innovation, and promoting and enhancing trust and credibility of organic products to consumers. Before concluding, I would like to reinforce that the Regional Government of the Azores relies on the scientific work presented here and is always available to collaborate and be an active partner, within its field of competence. We all share the same goal: finding the best solutions for the sake of our agriculture.
João António Ferreira Ponte Regional Secretary of Agriculture and Forestry
Reference
Lopes, D. J. H. 2019. Strategy for the development of organic agriculture in the Azores Autonomous Region. IOBC-WPRS Bull. 145: 22-28.
List of participants
Catarina Afonso Nicole Aguiar RAIZ Faculty of Sciences and Technology Forest and Paper Research Institute University of the Azores Aveiro, Portugal Ponta Delgada, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
Olga M. C. C. Ameixa Patrícia Arruda Department of Biology and CESAM Faculty of Sciences and Technology University of Aveiro University of the Azores Aveiro, Portugal Ponta Delgada, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
Marek Barta Isabel Borges Institute of Forest Ecology Faculty of Sciences and Technology Slovak Academy of Sciences and cE3c – ABG Zvolen, Slovakia University of the Azores E-mail: [email protected] Ponta Delgada, Azores, Portugal E-mail: [email protected]
Peter M. J. Brown Renato Calado Department of Biology Faculty of Sciences and Technology Anglia Ruskin University University of the Azores Cambridge, UK Ponta Delgada, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
Jana Collatz Patrick de Clercq Biosafety Group Department of Crop Protection Agroscope Ghent University Zürich, Switzerland Ghent, Belgium E-mail: [email protected] E-mail: [email protected]
Ana C. F. S. Durão Rachel A. Farrow Direção Regional da Agricultura School of Life Sciences Governo dos Açores Anglia Ruskin University Ponta Delgada, Azores, Portugal Cambridge, UK E-mail: [email protected] E-mail: [email protected]
Patrícia Garcia Irina Goryacheva Faculty of Sciences and Technology Laboratory of Insect Genetics and cE3c – ABG Vavilov Institute of General Genetics University of the Azores Russian Academy of Sciences Ponta Delgada, Azores, Portugal Moscow, Russia E-mail: [email protected] E-mail: [email protected]
IV V
Audrey Grez Danny Haelewaters Facultad de Ciencias Veterinarias y Pecua Faculty of Science Universidad de Chile University of South Bohemia Santiago, Chile České Budějovice, Czech Republic E-mail: [email protected] E-mail: [email protected]
Dorothy Hayden Tim Haye School of Biology and Environmental Centre for Agriculture and Biosciences Science International (CABI) University College Dublin Egham, UK Belfield, Dublin, Ireland E-mail: [email protected] E-mail: [email protected]
Axel Hochkirch Milada Holecová Trier Centre for Biodiversity Conservation Department of Zoology Universität Trier Comenius University Trier, Germany Bratislava, Slovakia E-mail: [email protected] E-mail: [email protected]
Alois Honěk Pavel Kindlmann Crop Research Institute Department of Biodiversity Research Prague, Czech Republic Czech Academy of Sciences E-mail: [email protected] Brno, Czech Republic E-mail: [email protected]
Johannette Klapwijk Jan Kulfan R & D Entomology Institute of Forest Ecology Koppert B. V. Slovak Academy of Sciences Berkel en Rodenrijs, The Netherlands Zvolen, Slovakia E-mail: [email protected] E-mail: [email protected]
Antoon J. M. Loomans David João Horta Lopes Department of Entomology Departamento de Ciências Agrárias National Plant Protection Organization Universidade dos Açores Wageningen, The Netherlands Terceira, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
John E. Losey Zdenka Martinkova Department of Entomology Crop Research Institute Cornell University Prague, Czech Republic Ithaca, New York, USA E-mail: [email protected] E-mail: [email protected]
Kelly Martinou Enésima Mendonça Joint Service Health Unit Faculty of Sciences and Technology Akrotiri, Cyprus and cE3c – ABG E-mail: [email protected] University of the Azores Ponta Delgada, Azores, Portugal E-mail: [email protected] VI
James Miksanek Oldřich Nedvěd Department of Entomology Department of Zoology University of Minnesota University of South Bohemia St. Paul, Minnesota, USA České Budějovice, Czech Republic E-mail: [email protected] E-mail: [email protected]
Rúben Oliveira Andrei Orlinski Faculty of Sciences European and Mediterranean Plant University of Lisbon Protection Organization (EPPO) Lisboa, Portugal Paris, France E-mail: [email protected] E-mail: [email protected]
Jodey Peyton João António Ferreira Ponte Centre for Ecology & Hydrology Secretaria Regional da Agricultura e Florestas Wallingford, UK Governo dos Açores E-mail: [email protected] Ponta Delgada, Azores, Portugal E-mail: [email protected]
Helen E. Roy Vasco Santos Biological Records Centre Faculty of Sciences and Technology Centre for Ecology & Hydrology University of the Azores Wallingford, UK Ponta Delgada, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
Luis F. D. Silva Jiří Skuhrovec CIBIO-InBIO Group Functional Diversity of Invertebrates Department of Biology and Plants in Agro-Ecosystems University of the Azores Crop Research Institute Ponta Delgada, Azores, Portugal Prague, Czech Republic E-mail: [email protected] E-mail: [email protected]
António Onofre Soares Zuzana Štípková Faculty of Sciences and Technology Global Change Research Institute and cE3c – ABG Czech Academy of Sciences University of the Azores Brno, Czech Republic Ponta Delgada, Azores, Portugal E-mail: [email protected] E-mail: [email protected]
Gudrun Strauß Victoria Werenkraut Austrian Agency for Health and Laboratorio Ecotono Food Safety (AGES) Universidad Nacional del Comahue Graz, Austria San Carlos de Bariloche, Argentina E-mail: [email protected] E-mail: [email protected]
Gill Weyman Peter Zach School of BEES Institute of Forest Ecology University College Cork Slovak Academy of Sciences Cork City, Ireland Bratislava, Slovakia E-mail: [email protected] E-mail: [email protected]
Contents
Preface ...... I
Opening remarks ...... II
List of participants ...... IV
Contents ...... VII
Full articles
Non-target phyllophagous insects in oak forests of central and southeastern Europe as potential hosts of Entomophaga maimaiga Marek Barta, Milan Zúbrik, Jan Kulfan, Peter Zach, Daniela Pilarska, Ann E. Hajek, Tonya D. Bittner, Danail Takov, Andrej Kunca, Slavomír Rell, Anikó Hirka and György Csóka ...... 1-5
Ladybird community change induced by the harlequin ladybird Harmonia axyridis: evidence from a long-term field study in the UK Peter M. J. Brown and Helen E. Roy ...... 6-12
Polymorphism of invasive and native Harmonia axyridis populations on the mitochondrial atp-6 gene Irina Goryacheva, Boris Andrianov and Ilia Zakharov ...... 13-16
Tracking an ectoparasitic fungus of Harmonia axyridis in the USA using literature records and citizen science data Danny Haelewaters, Thomas Hiller, Fred Y. Pan and Jeffrey Y. Pan ...... 17-22
Strategy for the development of organic agriculture in the Azores Autonomous Region David João Horta Lopes ...... 23-29
Evaluating the risks and benefits of Aphelinus certus, an introduced enemy of soybean aphid, in North America James R. Miksanek and George E. Heimpel ...... 30-32
Age and temperature effects on accumulation of carotenoids in ladybirds Oldřich Nedvěd, Aslam Muhammad, Rahim Abdolahi, Samane Sakaki and Antonio O. Soares ...... 33-36
VII VIII
Extended abstracts
Anagonia sp. (Diptera: Tachinidae), potential biocontrol agent of Gonipterus platensis (Coleoptera: Curculionidae) in the Iberian Peninsula Catarina Afonso, Carlos Valente, Catarina I. Gonçalves, Ana Reis, Beatriz Cuenca and Manuela Branco ...... 37-39
Risk and benefit assessment of biological control agents in Switzerland: A case study with Trichopria drosophilae Jana Collatz, Sarah Wolf, Nasim Amiresmaeili and Jörg Romeis ...... 40-41
A rare coccinellid surviving the spread of Harmonia axyridis Rachel A. Farrow, Helen E. Roy and Peter M. J. Brown ...... 42-44
Ecological effects of the invasive coccinellid Harmonia axyridis in East Anglia, UK Rachel A. Farrow, Helen E. Roy and Peter M. J. Brown ...... 45-46
Composition and functional traits of coccinellids in greenspaces vary with landscape urbanization Audrey A. Grez, Tania Zaviezo, M. M. Gardiner and A. Alaniz ...... 47-49
Field and laboratory evidence of mechanisms explaining the dominance of Harmonia axyridis (Pallas) in alfalfa in Chile Audrey A. Grez, Tania Zaviezo, Antonio O. Soares, Violeta Romero and Carlos González ...... 50-52
Hesperomyces “harmoniae” nom. prov. (Laboulbeniales), an ectoparasitic fungus specific to Harmonia axyridis Danny Haelewaters ...... 53-55
Field investigations of the invasive leaf beetle pest Paropsisterna selmani (Chrysomelidae) and laboratory-based evaluation of the parasitoid wasp Enoggera nassaui as a biological control agent Dorothy Hayden, John Finn and Jan-Robert Baars ...... 56-58
Does Harmonia axyridis (Coccinellidae) suppress native ladybirds? Pavel Kindlmann and Zuzana Štípková ...... 59-61
Ecosystem services provided by the native predator Scymnus nubilus Mulsant (Coleoptera: Coccinellidae) against aphids on forestry nurseries Roberto Meseguer, Isabel Borges, Virgílio Vieira, Gemma Pons and António O. Soares ...... 62-63
Engaging people in surveillance and monitoring of non-native species Helen E. Roy, Peter M. J. Brown, Marc Botham and Steph Rorke ...... 64-66
IX
Collaborating to map ladybirds across Europe Helen E. Roy, Jiří Skuhrovec, Tim Adriaens, Peter M. J. Brown, Alois Honěk, Alberto F. Inghilesi, Karolis Kazlauskis, Oldřich Nedved, Gabriele Rondoni, David B. Roy, António O. Soares and Sandra Viglasova ...... 67-68
Structure and dynamics of aphidophagous guilds and aphids in a country on the margin of Harmonia axyridis distribution Zuzana Štípková and Pavel Kindlmann ...... 69-70
Mapping the distribution of Harmonia axyridis (Pallas) in Argentina through citizen science Victoria Werenkraut, Florencia Baudino and Helen E. Roy ...... 71-73
Establishing the pattern of spread of harlequin ladybirds in Cork County, Ireland Gill Weyman, Fidelma Butler, Pádraig Whelan and Sean McKeown ...... 74-76
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 1-5
Non-target phyllophagous insects in oak forests of central and southeastern Europe as potential hosts of Entomophaga maimaiga
Marek Barta1, Milan Zúbrik2, Jan Kulfan1, Peter Zach1, Daniela Pilarska3,4, Ann E. Hajek5, Tonya D. Bittner5, Danail Takov3, Andrej Kunca2, Slavomír Rell2, Anikó Hirka6 and György Csóka6 1Institute of Forest Ecology, Slovak Academy of Sciences, Ľ. Štúra 2, 960 53 Zvolen, Slovakia; 2National Forest Centre, Forest Protection Service, Lesnícka 11, 969 23 Banská Štiavnica, Slovakia; 3Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 2 Gagarin Str., Sofia 1113, Bulgaria; 4New Bulgarian University, Department of Natural Sciences, 21 Montevideo Str., Sofia 1618, Bulgaria; 5Department of Entomology, Cornell University, Ithaca, NY 14853-2601, USA; 6NARIC Forest Research Institute, Department of Forest Protection, Mátrafüred, Hungary *Corresponding author: [email protected]
Abstract: Entomophaga maimaiga is an important host-specific fungal pathogen of gypsy moth larvae in North America. In 1999, this entomopathogenic fungus was successfully introduced into Bulgaria. At present, it is spreading fast in southeastern and central Europe. It has been recorded from Serbia, Greece, Macedonia, Romania, Hungary, Slovakia, and the Czech Republic. European oak forests harbour a very rich and diverse entomofauna, which consists of many uncommon, rare, and protected species. E. maimaiga thus might pose a threat to such insect species. In this study, we evaluated the presence of entomopathogens in non-target phyllophagous larvae in Slovakia (two plots), Hungary (three plots), and Bulgaria (one plot). The surveys were conducted in areas where E. maimaiga had previously been reported and as many as 4045 larvae were collected. In total, 45 (1.13%) collected larvae died because of fungal infections but none of them was infected by E. maimaiga. Pathogens were identified as Beauveria bassiana, B. pseudobassiana, Zoophthora radicans, Aspergillus flavus, and an unidentified species from the family Entomophthoraceae. Mean prevalence of E. maimaiga infection in collected gypsy moth larvae reached 0.84% at the surveyed plots. Our results confirm a high host specificity of E. maimaiga to Lymantria dispar.
Key words: Entomophaga maimaiga, gypsy moth, host specificity, oak forests, non-target species
Introduction
The gypsy moth, Lymantria dispar L. (Lepidoptera: Erebidae), is one of the most damaging forest defoliators in Europe. Repeated gypsy moth outbreaks have been reported mainly in central and southern Europe (Csóka and Hirka, 2009; Zúbrik et al., 2013; Hlásny et al., 2016). Entomophaga maimaiga Humber, Shimazu and Soper (Entomophthorales: Entomophthoraceae) is an important host-specific fungal pathogen of gypsy moth larvae in North America, which was originally described from Japan. The fungus was intentionally introduced into the USA near Boston in 1910, into the state of New York in 1985, and into Virginia in 1986. It was not recovered from natural populations until 1989, when it caused
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extensive epizootics in the northeastern USA (Hajek, 1999). At present, E. maimaiga is the principal pathogen infecting gypsy moth larvae in North America (Hajek et al., 2015; Hajek and van Nouhuys, 2016). In 1999, the fungus was introduced into Europe (Bulgaria) (Pilarska et al., 2000). The introduction was successful and the first epizootics in European gypsy moth populations by this fungus were observed in 2005 (Georgiev et al., 2013). Recent research suggests that E. maimaiga has been spreading fast in central and southeastern Europe (Zúbrik et al., 2016). Both laboratory and field studies in North America have demonstrated that E. maimaiga is highly host specific (Hajek et al., 1995; 1996). European oak forests host a very rich entomofauna, consisting of many species, including some that are uncommon, rare, and protected (Patočka et al., 1999; Csóka and Szabóky, 2005). Since E. maimaiga might pose a threat to such insect species, investigations are needed to evaluate its host specificity in European forests. In this study, we evaluated the presence of entomopathogenic fungi in non-target phytophagous larvae inhabiting ecosystems of oak forests in central and southeastern Europe.
Material and methods
The study was conducted at six plots (Figure 1): two in Slovakia (SK), three in Hungary (HU), and one in Bulgaria (BG) during 2014-2017. The study plots were selected based on the presence of E. maimaiga in L. dispar populations, which had been confirmed in previous years. The forests are dominated by Quercus robur L. and Q. cerris L. (SK and HU) and by Q. petraea (Matt.) Liebl., Q. cerris, and Q. frainetto Ten. (BG). Larvae were collected by beating the foliage and branches with wooden sticks. Collection was mainly focused on the foliage of oak trees, but other trees were also sampled. Collected larvae were transported to the laboratory, sorted by species, and reared in plastic containers (at 20 °C) until death or pupation. Cadavers were investigated with microscopy techniques, and infected ones were analysed using molecular data (by the ITS and LSU regions of the nuclear ribosomal RNA).
Results and discussion
A total of 4045 phyllophagous larvae were collected during this study. They belonged to 104 species from 19 families in the orders Lepidoptera, Hymenoptera, and Coleoptera. The most commonly collected ones were Agriopis leucophaearia Denis & Schiffermüller (n = 466, 11.52%); Orthosia cruda Denis and Schiffermüller (n = 327, 8.08%); Operophtera brumata L. (n = 300, 7.42%); and Orthosia cerasi Fabricius (n = 300, 7.42%). Microscopic and molecular analyses demonstrated that 45 (1.13%) larvae died due to fungal infections (Table 1). The pathogens were identified as Aspergillus flavus Link, Beauveria bassiana (Bals.-Criv.) Vuill., B. pseudobassiana S. A. Rehner and R. A. Humber, Zoophthora radicans (Bref.) A. Batko, and an unidentified species in the subfamily Erynioideae (Entomophthoraceae). Overall, 17 (0.42%) larvae were infected by Aspergillus spp., B. bassiana was found in 10 (0.25%) cadavers, one specimen of O. cerasi was infected by B. pseudobassiana, and Beauveria sp. was identified from three (0.07%) larvae. Zoophthora radicans was found in two geometrid cadavers. Nine larvae of Orthosia spp. were killed by unidentified species in the subfamily Erynioideae (different from the subfamily containing E. maimaiga).
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Figure 1. Map of central and southeastern Europe displaying sites in Slovakia, Hungary, and Bulgaria, where larvae were collected.
Recently, a preliminary field study regarding the occurrence of E. maimaiga in non- target phyllophagous insects, was conducted in Bulgaria and high host specificity to L. dispar was found (Georgieva et al., 2014). In the USA, extensive laboratory and field studies have been conducted on the host specificity of this fungus (Hajek et al., 1996; 2000; 2004). Inoculation bioassays supported its specificity to Lepidoptera (Hajek et al., 1995). In this country, only nine non-target lepidopteran species have been found to be naturally infected by E. maimaiga: Dasychira basiflava Packard, D. obliquata Grote and Robinson, D. leucophaea J. E. Smith, D. vagans Barnes and McDunnough, Orgyia leucostigma J. E. Smith, Malacosoma disstria Hübner, Catocala ilia Cramer, Agrochola bicolorago Guenée, and an unidentified species from Gelechiidae. However, infection prevalence was always low (Hajek et al., 1995; 1996; 2000, 2004). Our results confirm high specificity of E. maimaiga to L. dispar in central and southeastern European oak forests. In a cohort of 4045 individuals of non-target species collected and reared during this study, we were not able to find any specimen infected by E. maimaiga. We confirmed infection by E. maimaiga in L. dispar larvae at visited sites. Out of 1780 L. dispar specimens collected, 15 individuals (0.84%) were infected. The low population density of the gypsy moth in every collection plot during the entire study period could be a reason for the relatively low prevalence of this specific infection.
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Table 1. List of identified entomopathogenic fungi. Only host species with presence of entomopathogenic fungi are listed.
Host species Entomopathogenic fungi HYMENOPTERA Tenthredinidae Tenthredinidae sp. indet. 9 Aspergillus flavus LEPIDOPTERA Drepanidae Polyploca ridens Fabricius 1 Beauveria bassiana, 1 A. flavus Erebidae Catocala nymphagoga Esper 1 Entomophthorales sp. indet. Euproctis chrysorrhoea L. 1 Beauveria sp. Geometridae Agriopis aurantiaria Hübner 2 Entomophthorales sp. indet. Agriopis leucophaearia Denis and 1 Zoophthora radicans, Schiffermüller 2 B. bassiana Apocheima hispidaria Denis and 1 Z. radicans Schiffermüller Colotois pennaria (L.) 2 B. bassiana Lycia hirtaria Clerck 2 A. flavus Lasiocampidae Malacosoma neustria (L.) 1 Beauveria sp. Noctuidae Jodia croceago Denis and Schiffermüller 1 A. flavus Lithophane ornitopus Hufnagel 1 A. flavus Orthosia cerasi Fabricius 1 Erynioideae sp. indet., 1 Beauveria pseudobassiana, 2 A. flavus Orthosia cruda Denis and Schiffermüller 8 Erynioideae sp. indet., 1 A. flavus Noctuidae sp. indet. 3 B. bassiana Tischeriidae Tischeria ekebladella Bjerkander 1 Beauveria sp. Tortricidae Tortrix viridana L. 2 B. bassiana
Acknowledgements
This work was supported by the Slovak Research and Development Agency via grant no. APVV-15-0348.
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References
Csóka, G. and Hirka, A. 2009. A gyapjaslepke (Lymantria dispar L.) legutóbbi tömegszaporodása Magyarországon. Növényvédelem 45: 196-201. Csóka, G. and Szabóky, C. 2005. Checklist of herbivorous insects of native and exotic oaks in Hungary I (Lepidoptera). Acta Silv. Lign. Hung. 1: 59-72. Georgiev, G., Mirchev, P., Rossnev, B., Petkov, P., Georgieva, M., Pilarska, D., Golemansky, V., Pilarski, P. and Hubenov, Z. 2013: Potential of Entomophaga maimaiga for suppressing Lymantria dispar outbreaks in Bulgaria. Cr. Acad. Bulg. Sci. 66: 1025-1032. Georgieva, M., Takov, D., Georgiev, G., Pilarska, D., Pilarski, P., Mirchev, P. and Humber, R. 2014. Studies on non-target phyllophagous insects in oak forests as potential hosts of Entomophaga maimaiga (Entomophthorales: Entomophthoraceae) in Bulgaria. Acta Zool. Bulg. 66: 115-120. Hajek, A. E. 1999. Pathology and epizootiology of the Lepidoptera-specific mycopathogen Entomophaga maimaiga. Microbiol. Mol. Biol. Rev. 63: 814-835. Hajek, A. E., Butler, L. and Wheeler, M. M. 1995. Laboratory bioassays testing the host range of the gypsy moth fungal pathogen Entomophaga maimaiga. Biol. Control 5: 530-544. Hajek, A. E., Butler, L., Walsh, S. R. A., Silver, J. C., Hain, F. P., Hastings, F. L., O’Dell, T. M. and Smitley, D. R. 1996. Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environ. Entomol. 25: 709-721. Hajek, A. E., Butler, L., Liebherr, J. K. and Wheeler, M. M. 2000. Risk of infection by the fungal pathogen Entomophaga maimaiga among Lepidoptera on the forest floor. Environ. Entomol. 29: 645-650. Hajek, A. E., Strazanac, J. S., Wheeler, M. M., Vermeylen, F. and Butler, L. 2004. Persistence of the fungal pathogen Entomophaga maimaiga and its impact on native Lymantriidae. Biol. Control 30: 466-471. Hajek, A. E., Tobin, P. C. and Haynes, K. J. 2015. Replacement of a dominant viral pathogen by a fungal pathogen does not alter the synchronous collapse of a forest insect outbreak. Oecologia 177: 785-797. Hajek, A. E. and van Nouhuys, S. 2016. Fatal diseases and parasitoids: from competition to facilitation in a shared host. Proc. Roy. Soc. B 283: 20160154. Hlásny, T., Trombik, J., Holuša, J., Lukášová, K., Grendár, M., Turčáni, M., Zúbrik, M., Tabaković-Tošić, M., Hirka, A., Buksha, I., Modlinger, R., Kacprzyk, M. and Csóka, G. 2016. Multi-decade patterns of gypsy moth fluctuations in the Carpathian Mountains and options for outbreak forecasting. J. Pest. Sci. 89: 413-425. Patočka, J., Krištín, A., Kulfan, J. and Zach, P. 1999. Die Eichenschädlinge und ihre Feinde. Institut für Waldökologie, SAW, Zvolen. Pilarska, D., McManus, M., Hajek, A. E., Herard, F., Vega, F., Pilarski, P. and Markova, G. 2000. Introduction of the entomopathogenic fungus Entomophaga maimaiga Hum., Shim. and Sop. (Zygomycetes: Entomophthorales) to a Lymantria dispar (L.) (Lepidoptera: Lymantriidae) population in Bulgaria. J. Pest. Sci. 73: 125-126. Zúbrik, M., Kunca, A. and Csoka, G. 2013. Insects and diseases damaging trees and shrubs of Europe. Napedition, Paris. Zúbrik, M., Hajek, A. E., Pilarska, D., Špilda, I., Georgiev, G., Hrašovec, B., Hirka, A., Goertz, D., Hoch, G., Barta, M., Saniga, M., Kunca, A., Nikolov, C., Vakula, J., Galko, J., Pilarski, P. and Csóka, G. 2016. The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe. J. Appl. Entomol. 140: 565-579. Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 6-12
Ladybird community change induced by the harlequin ladybird Harmonia axyridis: evidence from a long-term field study in the UK
Peter M. J. Brown1* and Helen E. Roy2 1Applied Ecology Research Group, School of Life Sciences, Anglia Ruskin University, Cambridge, UK; 2Biological Records Centre, NERC Centre for Ecology and Hydrology, Wallingford, UK *Corresponding author: [email protected]
Abstract: This study examines changes in ladybird (Coleoptera: Coccinellidae) communities at four sites (two lime tree sites, one pine tree site and one nettle site) in East Anglia, UK, over an 11-year period (2006-2016) following invasion by the non-native ladybird species Harmonia axyridis (Pallas). Overall, H. axyridis represented 41.5% of all ladybirds sampled and was over three times more abundant than the second commonest species, Coccinella septempunctata L. There was a significant negative relationship between H. axyridis and Adalia bipunctata (L.) adults at the lime tree sites, but not between H. axyridis and adults of any of the other main ladybird species sampled. Adalia bipunctata adults and Adalia spp. larvae were the only native ladybirds that significantly declined. Our study shows a clear change in the ladybird community on lime trees over an 11-year period. Intraguild predation is hypothesised to be an important driver of the changes observed.
Key words: Adalia bipunctata, biological control, Coccinellidae, intraguild predation, invasive species, non-target effects
Introduction
Through direct and indirect interactions with native species, invasive non-native species are widely acknowledged as one of the main causes of biodiversity loss globally (Millennium Ecosystem Assessment, 2005), and this pressure on biodiversity has increased over recent decades (Butchart et al., 2010). Competition, predation and disease-vectoring are some of the mechanisms by which invasive non-native species may negatively affect native species. Ladybird (Coleoptera: Coccinellidae) communities in a particular habitat often comprise a small suite of species (typically dominated numerically by one or two species) that co-exist in different niches (Evans, 2004; Honěk et al., 2014; Viglášová et al., 2017). The harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) is a voracious ladybird species that primarily feeds on aphids and was introduced in many countries as a promising biological control agent in a range of glasshouse and field crops (Koch, 2003; Roy et al., 2016). Native to Asia (Orlova-Bienkowskaja et al., 2015), H. axyridis is regarded as an invasive non-native species in Europe, where it has been spreading rapidly since the early years of the 21st century (Brown et al., 2011 b). In the UK, H. axyridis arrived primarily by spread from mainland Europe (Majerus et al., 2006) and was established in East Anglia (a region of south-east UK) by 2005 (Brown et al., 2008).
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In an earlier study we reported declines in three native species over a three-year period following the arrival of H. axyridis in East Anglia (Brown et al., 2011 a). However, like many insects, ladybird abundance varies substantially from one year to another (Heathcote, 1978; Honěk et al., 2016), so long-term monitoring of their populations is essential in order to provide rigorous temporal trends (Day and Tatman, 2006). The aim of the present study was to examine changes in ladybird communities at four sites in East Anglia, UK, over an 11-year period following invasion by H. axyridis.
Material and methods
Ladybird sampling was carried out at four sites in East Anglia, UK. The sites were of three habitat types: mature lime trees Tilia × europea L. (Malvaceae) (sites A and B), pine trees Pinus sylvestris L. (Pinaceae) (site C) and stinging nettle Urtica dioica L. (Urticaceae) (site D). The sampling protocol of Brown et al. (2011 a) was used. In short, the sites were each sampled for twenty minutes in a standardised way on nine occasions per year (April- October) during 2006-2016 (site A was only sampled since 2008). Thus, a total of 378 surveys were completed. The three sites (A to C) comprising trees were sampled by tree beating whilst the fourth site (D) was sampled by sweep netting. Conspicuous ladybird (sensu Majerus, 1994) (i. e., Coccinellidae subfamilies Epilachninae, Coccinellinae, and Chilocorinae) adults and late instar larvae were recorded to species. Sampling was generally carried out between 10:00 and 16:00 h (and occasionally between 10:00 and 18:00 h) on dry days with air temperature of at least 14 °C. Weather data and aphid data (limited to an abundance scale) were also recorded. At the lime tree sites individually, species abundance (total adults and larvae) for the most abundant species was compared between early [site A: 2008-2011; site B: 2006-2011 (excluding 2008*)] and late years [sites A & B: 2012-2016 (excluding 2013*)] (i. e., 7 species × 2 sites = 14 t-tests conducted). (*Excluded years because of low ladybird counts due to tree pollarding.) For details of methods and analyses, please refer to Brown and Roy (2018).
Results and discussion
The total number of ladybirds recorded in a year varied significantly, from a low of 320 2 (in 2013) to a high of 1,567 (in 2011) (one-way classification chi-square: X 8 = 1332.856, N = 9301, P < 0.01) (Table 1). Of all ladybirds sampled, H. axyridis represented 41.5% [varying from a low of 0.2% (1 of 521 ladybirds) in 2006 to a high of 70.7% (724 of 1,024) in 2015] and overall was more than three times more abundant than C. septempunctata, the second commonest species. The proportion of native ladybirds declined from 99.8% (520 of 521) in 2006 to 30.7% (383 of 1,248) in 2016 (Table 1). The change in community structure was thus numerical, not just proportional. Our study shows a clear change in the ladybird community on lime trees over an 11-year period in which H. axyridis invaded the UK, with an association between ladybird native status (H. axyridis or native) and year (2008-2016) (two-way classification chi-square: 2 X 8 = 1002.352, N = 9,301, P < 0.001). Sites A and B (lime trees) were dominated by H. axyridis, which had an overall H. axyridis component of: site A: 50.9% (range between years = 25.7% to 85.3%); and site B: 57.6% (range between years = 0.3% to 87.9%) (Table 1).
8
2016, 2016,
-
2006
in
D) in East Anglia, UK,
-
(A
separated from those of native ladybirds (all native species combined). Reproduced from Brown
Harmonia axyridis
Roy(2018).
Table Table 1. Summary of ladybird abundance (and percentages of totals) at each of four sites with counts of and
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Across all years, 12, 15, 13 and 10 species were recorded at sites A, B, C and D, respectively. Across all sites mean annual species richness was 8.0 (range = 5 to 11). Mean species diversity was higher in early than in late years, with a significant difference between early and late years at site B only (Shannon’s: paired t-test: t8 = 2.461, P = 0.039; Simpson’s: paired t-test: t8 = 2.864, P = 0.021). Comparisons of species abundances between early and late years at the lime tree sites for the main ladybird species resulted in only two (of 14) tests showing significance: adult Adalia bipunctata (L.) (t-test: t6 = 3.292, P = 0.017) and Adalia spp. larvae (t-test: t6 = 2.462, P = 0.049) varied between early and late periods at site A only, with lower abundance in the late period. The abundance of H. axyridis did not differ significantly between early and late years. A significant negative relationship was observed between H. axyridis and A. bipunctata adults at the lime tree sites, with A. bipunctata abundance in 2016 reduced to approximately 16% of the total from the first surveys in 2006. The relationship between H. axyridis and Adalia decempunctata (L.) was much less clear and not significant, with great variability in A. decempunctata numbers between years. There is high H. axyridis niche overlap with both A. bipunctata and A. decempunctata (Kenis et al., 2017). The ladybird community structure on lime trees has changed dramatically since the arrival of H. axyridis, the only non-native species recorded, but the species that now dominates on lime, at the expense of A. bipunctata. The small number of similar long-term studies from North America suggest negative effects on native ladybirds of invasive non- native ladybirds (Turnock et al., 2003; Alyokhin and Sewell, 2004); or show no detectable effects (Day and Tatman, 2006). It is possible that A. bipunctata was already declining for reasons unconnected to H. axyridis (Honěk et al., 2016). However, after a period of apparent increase in the UK, Roy et al. (2012) demonstrated declines of A. bipunctata following the arrival of H. axyridis; and in Belgium, where A. bipunctata was already declining, this decline was accelerated by the invasion of H. axyridis (Roy et al., 2012). Whilst H. axyridis rapidly dominated at the lime tree sites, it comprised a relatively small proportion of the ladybird assemblage at the pine tree site and the nettle site. Dominance of H. axyridis at the nettle site was expected (Alhmedi et al., 2009) but not observed, with the species only representing 11.4% of total ladybirds there, compared to 50.2% by Coccinella septempunctata L. Harmonia axyridis was only the fourth most abundant species on the nettles. Despite early indications of a negative effect of H. axyridis on C. septempunctata (Brown et al., 2011 a) the present longer-term study suggests that there has been little effect on this species. The two species are similar in size and have a medium niche overlap (Kenis et al., 2017), with C. septempunctata preferring herbaceous vegetation to trees. Similarly, in this study there was no discernible negative effect on Propylea quattuordecimpunctata (L.). Harmonia axyridis had low abundance on the pine trees (representing 5.3% of total ladybirds – the fifth most abundant species), a result similar to that found by Brown et al. (2011 a) and in line with Purse et al. (2015). The pine tree site had the lowest overall abundance of ladybirds and the community here was less dominated by a single species. On pines in the UK H. axyridis may be out-competed by specialist species such as Myrrha octodecimguttata (L.) and Harmonia quadripunctata (Pontoppidan) that are better adapted to the prey and/or micro habitats. Alternatively, it could be that pine trees represent a less favourable habitat for H. axyridis for abiotic reasons, and further fieldwork to establish this is necessary. The mechanisms behind the declines in A. bipunctata and Adalia spp. larvae on lime trees seem to be most likely a consequence of intraguild predation (IGP) (Pell et al., 2008; Hautier et al., 2011), which can be an important influence on community structure (Polis and
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Holt, 1992). Indeed, through molecular analyses (PCR), Thomas et al. (2013) showed that IGP by H. axyridis on both Adalia species took place (at least in 2009-2010) at both of the lime tree sites used in the present study. Like the results reported by Brown et al. (2011 a), there was substantial overlap (69.8%, N = 53) in the timing of Harmonia and Adalia larvae on the same lime trees, thus facilitating the potential for IGP to occur. Only very limited relationships were found between aphid abundance and either total natives, total H. axyridis, or total adult A. bipunctata. In conclusion, this study shows a marked change in the ladybird community on lime trees (but not on pine trees or nettles) following the arrival of H. axyridis, with evidence that significant declines in A. bipunctata were caused by the invasive species. At the least, H. axyridis is now one of the dominant species on deciduous trees in southern UK, and there is no indication that this situation will change in the short-medium term. Further research on the possible negative effects of H. axyridis on other insect groups is needed, some of which may be rather subtle, e. g., via resource competition (Howe et al., 2015). For a completer version of this paper please refer to Brown and Roy (2018).
Acknowledgements
We are very grateful to the following people and organisations for permission to carry out the site surveys: Don MacBean and Worlington Parish Council (site A), Fordham Parish Council (site B), Michael Taylor and Natural England (site C), and R. and A. Martin (site D). Thanks to Dawn Hawkins (Anglia Ruskin University) for advice on statistics. This study was funded by Anglia Ruskin University. H. E Roy receives co-funding from the Natural Environment Research Council (NERC) and the Joint Nature Conservation Committee (JNCC).
References
Alhmedi, A., Haubruge, E. and Francis, F. 2009. Effect of stinging nettle habitats on aphidophagous predators and parasitoids in wheat and green pea fields with special attention to the invader Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Entomol. Sci. 12: 349-358. Alyokhin, A. and Sewell, G. 2004. Changes in a lady beetle community following the establishment of three alien species. Biol. Invasions 6: 463-471. Brown, P. M. J., Roy, H. E., Rothery, P., Roy, D. B., Ware, R. L. and Majerus, M. E. 2008: Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non- native coccinellid. BioControl 53: 55-67. Brown, P. M. J. and Roy, H. E. 2018. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv. Divers. 11: 230-239. Brown, P. M. J., Frost, R., Doberski, J., Sparks, T., Harrington, R. and Roy, H. E. 2011 a. Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol. Entomol. 36: 231-240. Brown, P. M. J., Thomas, C. E., Lombaert, E., Jeffries, D. L., Estoup, A. and Lawson Handley, L.-J. 2011 b: The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56: 623-641.
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Butchart, S. H., Walpole, M., Collen, B., Van Strien, A., Scharlemann, J. P., Almond, R. E., Baillie, J. E., Bomhard, B., Brown, C. and Bruno, J. 2010. Global biodiversity: indicators of recent declines. Science 328: 1164-1168. Day, W. H. and Tatman, K. M. 2006. Changes in abundance of native and adventive Coccinellidae (Coleoptera) in alfalfa fields, in northern New Jersey (1993-2004) and Delaware (1999-2004), USA. Entomol. News 117: 491-502. Evans, E. W. 2004. Habitat displacement of North American ladybirds by an introduced species. Ecology 85: 637-647. Hautier, L., San Martin y Gomez, Gilles, Callier, P., de Biseau, J. and Gregoire, J. 2011. Alkaloids provide evidence of intraguild predation on native coccinellids by Harmonia axyridis in the field. Biol. Invasions 13: 1805-1814. Heathcote, G. D. 1978. Coccinellid beetles on sugar beet in eastern England, 1961-75. Plant Pathol. 27: 103-109. Honěk, A., Martinkova, Z., Kindlmann, P., Ameixa, O. M. and Dixon, A. F. 2014. Long‐term trends in the composition of aphidophagous coccinellid communities in Central Europe. Insect Conserv. Divers. 7: 55-63. Honěk, A., Martinkova, Z., Dixon, A. F. G., Roy, H. E. and Pekar, S. 2016. Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from an invasive non-native species. Insect Conserv. Divers. 9: 202-209. Howe, A. G., Ransijn, J. and Ravn, H. P. 2015. A sublethal effect on native Anthocoris nemoralis through competitive interactions with invasive Harmonia axyridis. Ecol. Entomol. 40: 639-649. Kenis, M., Adriaens, T., Brown, P. M., Katsanis, A., San Martin, G., Branquart, E., Maes, D., Eschen, R., Zindel, R. and van Vlaenderen, J. 2017. Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study. BioControl 62: 314-354. Koch, R. L. 2003. The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J. Insect Sci. 3: 1-16. Majerus, M. E. N. 1994. Ladybirds. New Naturalist series no. 81. HarperCollins, London, UK. Majerus, M. E. N., Strawson, V. and Roy, H. E. 2006. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol. Entomol. 31: 207-215. Millennium Ecosystem Assessment 2005. Ecosystems and Human Well-Being: Biodiversity Synthesis, Volume 86. World Resources Institute, Washington D.C., USA. Orlova-Bienkowskaja, M. J., Ukrainsky, A. S. and Brown, P. M. J. 2015. Harmonia axyridis (Coleoptera: Coccinellidae) in Asia: a re-examination of the native range and invasion to southeastern Kazakhstan and Kyrgyzstan. Biol. Invasions 17: 1941-1948. Pell, J. K., Baverstock, J., Roy, H. E., Ware, R. L. and Majerus, M. E. N. 2008. Intraguild predation involving Harmonia axyridis: a review of current knowledge and future perspectives. BioControl 53: 147-168. Polis, G. A. and Holt, R. D. 1992. Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol. Evol.: 151-154. Purse, B. V., Comont, R., Butler, A., Brown, P. M. J., Kessel, C. and Roy, H. E. 2015. Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. J. Biogeogr. 42: 575-588.
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Roy, H. E., Adriaens, T., Isaac, N. J. B., Kenis, M., Onkelinx, T., San Martin, G., Brown, P. M. J., Hautier, L., Poland, R., Roy, D. B., Comont, R., Eschen, R., Frost, R., Zindel, R., van Vlaenderen, J., Nedved, O., Ravn, H. P., Gregoire, J., de Biseau, J. and Maes, D. 2012. Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18: 717-725. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honěk, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L-J., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Thomas, A. P., Trotman, J., Wheatley, A., Aebi, A., Zindel, R. and Brown, P. M. J. 2013. Predation of native coccinellids by the invasive alien Harmonia axyridis (Coleoptera: Coccinellidae): detection in Britain by PCR-based gut analysis. Insect Conserv. Divers. 6: 20-27. Turnock, W. J., Wise, I. L. and Matheson, F. O. 2003. Abundance of some native coccinellines (Coleoptera: Coccinellidae) before and after the appearance of Coccinella septempunctata. Can. Entomol. 135: 391-404. Viglášová, S., Nedvěd, O., Zach, P., Kulfan, J., Parák, M., Honěk, A., Martinková, Z. and Roy, H. E. 2017. Species assemblages of ladybirds including the harlequin ladybird Harmonia axyridis: a comparison at large spatial scale in urban habitats. BioControl 62: 409-421.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 13-16
Polymorphism of invasive and native Harmonia axyridis populations on the mitochondrial atp-6 gene
Irina Goryacheva*, Boris Andrianov and Ilia Zakharov Institute of General Genetics of Russian Academy of Sciences, Laboratory of Insect Genetics, 3 Goubkin str., 119333 Moscow, Russia *Corresponding author: [email protected]
Abstract: A study of 11 populations (3 native, 8 invasive) of Harmonia axyridis was carried out to assess the genetic structure of native versus invasive H. axyridis. The populations of the eastern and western parts of the native range differ in the frequencies of the two haplotypes. In all invasive populations, haplotype diversity is reduced when compared with populations of the native part of the range. The ratio of the main atp-6 haplotypes persists in the invasive populations of Europe as the range extends from west to east. In the H. axyridis genome, an ancient form of the atp-6 gene was transferred to the nuclear genome, which is represented with a high frequency in the mitochondrial genome of H. axyridis from the western population group.
Key words: Harmonia axyridis, genetic structure, haplotypes diversity, atp-6
Introduction
Harmonia axyridis (Pallas, 1773) (Coleoptera: Coccinellidae) is one of the best-studied invasive insect species (e. g., Roy et al., 2016; Camacho-Cervantes et al., 2017). In Europe, the first record of H. axyridis in the wild was reported from Frankfurt am Main (Germany) in 2000 (Klausnitzer, 2002). In 18 years, H. axyridis has dispersed about 2,500 kilometers to the east. The most eastern finding of this species was made in the city of Nalchik (Russia). Local populations at the periphery of the invasion are susceptible to genetic stochastic processes, such as the founder effect and the bottleneck effect, which may adversely affect the integrity of their genetic structure and, as a result, fitness (Laugier et al., 2016). The aim of our work was to study the genetic structure of H. axyridis populations to identify the genetic features inherent of invasive populations. For this purpose, data on the structure of the mitochondrial atp-6 gene and its nuclear copy were used.
Material and methods
DNA sampling and amplification To characterize the H. axyridis atp-6 haplotype diversity, we used DNA samples of beetles from native and invasive populations. Samples from native locations include the western Siberian population from Novosibirsk (sampling in 2014) and two eastern Asia populations include Birobidjan (2014) and Russikiy Island (2009). Samples from West and East European invasive populations include Paris (2006), Berlin (2008), Munich (2006), Turin (2006), Prague (2011), Kaliningrad (2010), the Black Sea coast of the Caucasus (Greater Sochi)
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(2013), and Crimea (multiple localities) (2016). Amplification of variable mitochondrial fragment was carried out with primers a6H-2f (5’-TTTTCTTCTTTTGATCCTTCATCTT-3’) and c3H-2r (5’-GCTCCTAAAATTGGTCAAGGA-3’) in a final PCR volume of 25 μl using the EncycloPlus PCR kit (Evrogen, Russia, Moscow) following the manufacturer’s protocol.
Sequencing and bioinformatics analysis PCR fragments were sequenced after elution from forward and reverse primers on an ABI PRISM 3500 sequencer using the BigDye®Terminator v.3.1 Cycle Sequencing Kit (Applied Biosystems, United States) following the manufacturer’s protocol. The determined sequences were aligned with database sequences using NCBI resources (http://www.ncbi.nlm.nih.gov) and MEGA7 software (Kumar et al., 2016).
Results and discussion
Seven mitochondrial haplotypes were identified for the atp-6 gene (GenBank accession numbers MG559722-MG559728), of which three were major – H2-S1 (MG559726), H2-S2 (MG559727), and H2-n1 (MG559724). Haplotype diversity was higher in the eastern population cluster than in the western cluster, with H = 0.53 and 0.24, respectively. The western population cluster is characterized by (1) the absence of haplotype Ha-S2 and (2) the high frequency of carriers of the haplotype Ha-N1 (more than half of the sampling). We think that minor haplotypes Ha-Bi1 and Ha-R4 with haplotype frequencies less than 10% are specific for the eastern population cluster. In invasive populations, the haplotype diversity was reduced in the easternmost sample on the Black Sea coast of the Caucasus owing to the decrease in the frequency of haplotype Ha-S2 (Figure 1).
Figure 1. Haplotype diversity in populations of H. axyridis on data from the gene atp-6.
Amplification under conditions of low or high DNA concentration made it possible to identify two forms of mitochondrial DNA (mtDNA) in H. axyridis since some nucleotides were ambiguously read at phylogenetically informative sites of haplotypes Ha-S1 and Ha-S2 15
(Table 1). In case of PCR with low DNA template concentration, the chromatograms were read unambiguously, whereas in the PCR with high DNA concentration, two forms of mtDNA were detected. Both reading variants were haplotype-specific and did not depend on the H. axyridis sampling localities. Double chromatogram peaks were never detected in beetles with haplotype Ha-N1 (Table 1).
Table 1. Polymorphic nucleotide sites within the H. axyridis gene atp-6.
Haplotype DNA Number of site in the reference H. axyridis name concentration mitochondrial genome (KJ778886) 4014 4050 4350 high A + G A + G Ha-S2 A low A A high G + A G Ha-S1 G low G Ha-N1 high/low A G G NUMT A
These data may be interpreted alternatively. Either H. axyridis mtDNA is represented by two forms with different copy numbers, or there are fragments of the mitochondrial atp6 gene in the nuclear genome. Herewith the sequence of a mitochondrial fragment copy in the nuclear genome coincides with the haplotype Ha-N1 within the studied region. The second assumption is more probable. In the literature, mitochondrial sequences in nuclear genome are called NUMT, the acronym for “nuclear mitochondrial DNA segment”. Since this NUMT was detected together with mitochondrial sequences in all samples (both from native and invasive ranges), it may be concluded that this atp-6 NUMT was acquired by the H. axyridis ancestral genome. In this case the haplotype Ha-N1 may be considered ancestral. At present, mitochondrial haplotype Ha-N1 is often found only in the western population cluster, where it is close to fixation. It is rare in the eastern population cluster and was not found in invasive populations. In the late Pleistocene, sharp changes in vegetation and landscapes occurred. At this time, there were only two large regions in which H. axyridis could survive the glaciation. First, the Far Eastern region, including the northeastern and eastern regions of modern China, where the forest zone remained throughout the Pleistocene. The second region was the Altai, where isolated isles of forest vegetation were preserved even at the peak of the glaciation. With the onset of warming, the range of the species again began to expand from two refugia, with the restoration of the integrity of the area about 8,000-10,000 years ago. Obviously, the isolation time was sufficient to accumulate differences in molecular-genetic and morphological features in the western and eastern groups of populations. At present, considerable geographic variation is described for three morphological traits of H. axyridis: the pattern of the elytra, the pattern of the pronotum, and the presence/absence of an elytral ridge. Geographic variations in these traits allow to identify two large zones of the H. axyridis area: Western (Western Siberia, Altai, Sayans) and Eastern (Amur Region, Far East). Inter-population differences within these zones are minimal and have no relation to geographic location. The complex of the differences between populations from the Far East and from Siberia by morphological traits and by mtDNA polymorphism allows the identification of two subspecies – eastern and western (Blekhman et al., 2010). 16
Since the beginning of the area expansion, the eastern subspecies has captured a significantly larger area than the western one. This subspecies is better acclimatized in new habitats. According to our observations, it survives better after overwintering and is less predisposed to cannibalism compared with the western subspecies. Our data and data obtained using microsatellites loci from Lombaert et al. (2010; 2014) confirm that invasive populations are descended from the eastern subspecies. To date, all studied by us European invasive populations retain the genetic division characteristic for the species H. axyridis. Persisting genetic diversity suggests a persisting genetic plasticity and therefore an ability of H. axyridis to adapt to new conditions during further invasive range expansion despite multiple genetic stochastic processes that the species overcomes on the front of invasion.
Acknowledgements
The study was supported by the Russian Science Foundation (Project No. 16-16-00079).
References
Blekhman, A. V., Goryacheva, I. I. and Zakharov, I. A. 2010. Differentiation of Harmonia axyridis Pall. according to polymorphic morphological traits and variability of the mitochondrial COI gene. Moscow Uni. Biol. Sci. Bull. 65: 174-176. Camacho-Cervantes, M., Ortega-Iturriaga, A. and del-Val, E. 2017. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ 5: e3296. Kumar, S., Stecher, G. and Tamura, K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874. Laugier, G. J. M., Le Moguédec, G., Su, W., Tayeh, A., Soldati, L., Serrate, B. and Estoup, A. 2016. Reduced population size can induce quick evolution of inbreeding depression in the invasive ladybird Harmonia axyridis. Biol. Invasions 18: 2871. Lombaert, E., Guillemaud, T., Cornuet, J. M., Malausa T., Facon, B. and Estoup, A. 2010. Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. Plos One 5: e9743. Lombaert, E., Estoup, A., Facon, B., Joubard, B., Grégoire, J. C., Jannin, A., Blin, A. and Guillemaud, T. 2014. Rapid increase in dispersal during range expansion in the invasive ladybird Harmonia axyridis. J. Evol. Biol. 27: 508-517. Roy, H. E., Brown P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A.G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A.O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 17-22
Tracking an ectoparasitic fungus of Harmonia axyridis in the USA using literature records and citizen science data
Danny Haelewaters1,2,3*, Thomas Hiller4, Fred Y. Pan5,6# and Jeffrey Y. Pan7# 1Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts 02138, USA; 2Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic; 3Current address: Department of Botany and Plant Pathology, Purdue University, 915 West State Street, West Lafayette, Indiana 47907, USA; 4Institute of Evolutionary Ecology and Conservation Genomics, University of Ulm, Albert-Einstein Allee 11, 89081 Ulm, Germany; 5Phillips Academy Andover, 180 Main Street, Andover, Massachusetts 01810, USA; 6Current address: Boston College, 140 Commonwealth Avenue, Chestnut Hill, Massachusetts 02467, USA; 7Reading Memorial High School, 62 Oakland Road, Reading, Massachusetts 01867, USA *Corresponding author: [email protected] #These authors contributed equally.
Abstract: Hesperomyces harmoniae nom. prov. (Ascomycota: Laboulbeniales) is a common fungal ectoparasite of Harmonia axyridis (Coleoptera: Coccinellidae), a globally invasive pest species. We launched an initiative to create a dataset encompassing all available records of the H. axyridis – H. harmoniae nom. prov. association in the USA. Reports have been gathered from the literature and from online citizen science platforms such as Bugguide and iNaturalist. A total of 163 curated records were downloaded from Bugguide and iNaturalist. Using these records, we built a distribution map available at http://beetlehangers.org. All occurrences are shown, each with location information, collection date, collector(s), and source – Bugguide, iNaturalist or literature. In time, the map will become searchable by date, as to be able to determine where in the USA the ladybirds–parasite association originated and track its distributional expansion over the years.
Key words: citizen science, distribution, Harmonia axyridis, Hesperomyces, Laboulbeniales
Introduction
Hesperomyces virescens is a fungal ectoparasite (Ascomycota: Laboulbeniales) that infects adult ladybirds (Coleoptera: Coccinellidae). We recently discovered that H. virescens is a complex consisting of multiple species, each specialized to a single host species or host species within a single genus (Haelewaters et al., 2018). One of these, H. harmoniae nom. prov., is only known from Harmonia axyridis from many countries around the world (Haelewaters et al., 2019). We do not know the place this fungus originated. Is it native to North America (Roy et al., 2011)? Was it imported into North America with H. axyridis upon introduction of the latter? Or did a host shift occur from a North American native ladybird to H. axyridis, after which the fungus became more successful on the invader?
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From studies in the Netherlands and the USA, we know there is a significant gap between establishment of H. axyridis in the wild and the first observations of the fungus on this ladybird (Haelewaters et al., 2017). Supposedly, the ladybird acquired the fungus after a certain time lag, providing some support for the hypothesis that H. harmoniae nom. prov. is a North American native fungus. Here, we report preliminary results of our initiative to create a dataset encompassing all available reports of the H. axyridis–H. harmoniae nom. prov. association in North America.
Material and methods
We extracted information from Bugguide.net and the citizen-science initiative iNaturalist by searching for the following queries: “Hesperomyces virescens”, “green beetle hanger”, and “Laboulbeniales fungus”. We downloaded data from 2002 (Garcés and Williams, 2004) up to 2018. All records were subject to manual quality control; photographs of records were checked for correct host species identification and whether Hesperomyces fruiting bodies were indeed present. Duplicate records were filtered out based on date, locality, collector, and photographs. Bugguide records were not associated with geographic coordinates (contrary to records downloaded from iNaturalist), hence we used coordinates of the city or on county level from where records were made. All data were combined into a single database, which served as basis for a distribution map of the H. axyridis – H. harmoniae nom. prov. association in the USA. The data from online sources were complemented by reports from the literature (Garcés and Williams, 2004; Riddick and Schaefer, 2005; Harwood et al., 2006 a; 2006 b; Riddick, 2006; 2010; Nalepa and Weir, 2007). We constructed a map showing all gathered occurrences of H. harmoniae nom. prov. associated with H. axyridis ladybirds, each with location information, collection date, name(s) of collector(s), and source (Bugguide / iNaturalist / literature). The distribution map is available at http://beetlehangers.org.
Results and discussion
We report a total of curated (= post-quality control) 163 records from the USA between 2002 and 2018. July-August 2002 marks the first published report of H. harmoniae nom. prov. on H. axyridis, from Ohio (Garcés and Williams, 2004). The number of records downloaded from Bugguide was 59, whereas the number of records from iNaturalist was 104 (Table 1). Early data are patchy; between 2002 and 2010 not enough records are available to make meaningful statements about targeted distributional spread of this association. It is likely that the association was present but that it has not been spotted or reported because not too many people – including researchers – are familiar with this laboulbenialean fungus. Second, citizen science initiatives are only recently gaining more traction with the wide public, slowly accumulating publicly available species records. Indeed, citizen science projects are increasingly important for the detection of easily recognizable species, such as the harlequin ladybird, H. axyridis. Examples are the Lost Ladybug Project (http://www.lostladybug.org/) and the UK Ladybird Survey (http://www.ladybird-survey.org/). To date, 1,000s and 1,000s of people have contributed observations of ladybirds through this UK initiative (Roy et al., 2015; Brown et al., 2018) aiding us to better understand post-invasion effects of H. axyridis. However, the next step – citizen scientists providing photographs of natural enemies of ladybirds – comes with 19
difficulties, as it becomes more than simply taking a photograph and uploading it to a website. There is a need to actively screen the observed specimen for fungal growth and take close-up photographs for good documentation. Much less citizen scientists will be willing to go that far. Those who will contribute, however, are expected to provide high-quality data.
Table 1: Number of records extracted from Bugguide & iNaturalist, by year and post-quality control.
Year Bugguide iNaturalist 2002 2003 2004 2 2005 3 2006 4 2007 2 2008 1 2009 6 2010 13 2011 4 1 2012 3 2013 6 4 2014 5 5 2015 2 7 2016 3 19 2017 3 22 2018 2 46
What we did in this study was making use of already available photographs from online sources to screen ladybirds for Hesperomyces. Fruiting bodies may not be observed if photographs are of poor quality or if fruiting bodies are only present ventrally whereas the photograph only shows the elytra (or vice versa). In other words, there are limitations to this approach, but we have been able to gather over 100 records of H. hamoniae nom. prov. from H. axyridis, accounting for some first state-wide records in the USA (Haelewaters et al., 2017). In 2018 alone, data downloaded from iNaturalist included new state records of H. axyridis – H. harmoniae nom. prov. for Indiana, Missouri, and Wisconsin. As a next step, we aim to incorporate records submitted to the photo-sharing website Flickr.com. When searching for “ladybug” + “fungus”, the number of observations is 757, but following quality control this number is likely to be much decreased. In addition, we will add data from personal collections in North America and from screening dried ladybirds in natural history collections. We further aim to transform this into citizen science project, through which users can submit sightings of H. harmoniae nom. prov. on H. axyridis. In the future, the map will be searchable by date, as to be able to determine where in North America the association originated and track its distributional expansion over the years. 20
Figure 1. Harmonia axyridis – Hesperomyces harmoniae nom. prov. in North America. Top panel: data from 2002, only from the literature. Middle panel: data from 2003-2017, taken from Bugguide and iNaturalist. Lower panel: data from 2018 alone, taken from Bugguide and iNaturalist. 21
Acknowledgements
A massive thank you to all people who submit photographs of specimens they observe to Bugguide and iNaturalist. Research would be a lot more limited without the data provided by citizen scientists.
References
Brown, P. M. J., Roy, D. B., Harrower, C., Dean, H. J., Rorke, S. L. and Roy, H. E. 2018. Spread of a model invasive alien species, the harlequin ladybird Harmonia axyridis in Britain and Ireland. Sci. Data 5: 180239. Garcés, S. and Williams, R. 2004. First record of Hesperomyces virescens Thaxter (Laboulbeniales: ascomycetes) on Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). J. Kansas Entomol. Soc. 77: 156-158. Haelewaters, D. 2019. Hesperomyces “harmoniae” nom. prov. (Laboulbeniales), an ectoparasitic fungus specific to Harmonia axyridis. IOBC-WPRS Bull. 145: 53-55. Haelewaters, D., de Kesel, A. and Pfister, D. H. 2018. Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci. Rep. 8: 15966. Haelewaters, D., Zhao, S. Y., Clusella-Trullas, S., Cottrell, T. E., De Kesel, A., Fiedler, L., Herz, A., Hesketh, H., Hui, C., Kleespies, R. G., Losey, J. E., Minnaar, I. A., Murray, K. M., Nedvěd, O., Pfliegler, W. P., Raak-van den Berg, C. L., Riddick, E. W., Shapiro-Ilan, D. I., Smyth, R. R., Steenberg, T., van Wielink, P. S., Viglášová, S., Zhao, Z., Ceryngier, P. and Roy H. E. 2017. Parasites of Harmonia axyridis: current research and perspectives. BioControl 62: 355-371. Harwood, J. D., Ricci, C., Romani, R., Pitz, K. M., Weir, A. and Obrycki, J. J. 2006 a. Prevalence and association of the laboulbenialean fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on coccinellid hosts (Coleoptera: Coccinellidae) in Kentucky, USA. Eur. J. Entomol. 103: 799-804. Harwood, J. D., Ricci, C., Romani, R. and Obrycki, J. J. 2006 b. Historic prevalence of a laboulbenialean fungus infecting introduced coccinellids in the United States. Antenna 30: 74-79. Nalepa, C. A. and Weir, A. 2007. Infection of Harmonia axyridis (Coleoptera: Coccinellidae) by Hesperomyces virescens (Ascomycetes: Laboulbeniales): Role of mating status and aggregation behavior. J. Invert. Pathol. 94: 196-203. Riddick, E. W. 2006. Influence of host gender on infection rate, density and distribution of the parasitic fungus, Hesperomyces virescens, on the multicolored Asian lady beetle, Harmonia axyridis. J. Insect Sci. 6: 42, doi:10.1673/031.006.4201. Riddick, E. W. 2010. Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull. Insectol. 63: 13-20. Riddick, E. W. and Schaefer, P. W. 2005. Occurrence, density, and distribution of parasitic fungus Hesperomyces virescens (Laboulbeniales: Laboulbeniaceae) on multicolored Asian lady beetle (Coleoptera: Coccinellidae). Ann. Entomol. Soc. Am. 98: 615-624. Roy, H. E., Rhule, E., Harding, S., Lawson Handley, L.-J., Poland, R. L., Riddick, E. W. and Steenberg, T. 2011. Living with the enemy: parasites and pathogens of the ladybird Harmonia axyridis. Biocontrol 56: 663-679. Roy, H. E., Rorke, S. L., Beckmann, B., Booy, O., Botham, M. S., Brown, P. M. J., Harrower, C., Noble, D., Sewell, J. and Walker, K. 2015. The contribution of volunteer recorders to our understanding of biological invasions. Biol. J. Linn. Soc. 115: 678-689. 22
Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 23-29
Strategy for the development of organic agriculture in the Azores Autonomous Region
David João Horta Lopes Azorean Biodiversity Group (GBA, CITA-A) and Platform for Enhancing Ecological Research & Sustainability (PEERS), Universidade dos Açores, Faculdade de Ciências Agrárias e Ambiente, Departamento de Ciências e Engenharia do Ambiente, Rua Capitão João D’Ávila, 9700-042 Angra do Heroísmo, Terceira, Azores, Portugal E-mail: [email protected]
Abstract: Following the publication in the Diário da República of the Resolution approving, the National Strategy for Organic Agriculture and the Plan of Action, it was imperative to develop a strategic plan for the development of organic agriculture in the Azores. To achieve this, a protocol was signed with the Cooperativa de Produtores de Agricultura Biológica-CRL (BioAzórica) and a working group was created specifically for this task. The Regional Strategy for the Development of Organic Agriculture and the Plan of Action for the Production and Promotion of Organic Agricultural Products of the Azores Region will not be far from the concepts and actions defined at national level. This document results from the detailed analysis of the actions of the national strategy and its adaptation to the specific characteristics of the Region. This approach is reflected in its structure and content by defining a specific strategic plan and with some own and exclusive measures of the Region based on the current knowledge of the state of development of organic production. This document has already been presented and discussed publicly and is now for approval by the Regional Government of the Azores. This strategic document consists of two parts: (I) Characterizing Agriculture and Organic Production and (II) Strategic Objectives and Axes for the Development of Organic Agriculture in the Azores Autonomous Region. On this part the strategic objectives and the axes of the action plan, operational objectives and actions to be developed, short, medium and long term, are presented. Finally, a set of tables with all actions of the action plan is presented for each of the operational objectives to be developed. In its final part, an assessment based on surveys on the development potential of Organic Agriculture in the different islands of the Azores Autonomous Region is presented.
Key words: Organic agriculture, strategic, development, promotion, Azores
A strategic plan for the development of organic farming in the Azores
In the Autonomous Region of the Azores, the Regional Secretariat for Agriculture and Forestry is responsible for collaborating, defining and guiding measures for the benefit of organic production in the field of agrarian activities in cooperation and partnership with proven associative and cooperative entities that assume a relevant role in the matter. Following the publication of the Resolution of the Council of Ministers nº 110/2017 of July 27 approving the National Strategy for Organic Agriculture (ENAB, 2016) and the Action Plan for the production and promotion of agricultural products and organic foods, it was imperative that the Azores Region should also have a strategic plan for the development
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of organic farming – just like the Autonomous Region of Madeira (DSDA, 2016). To this end, a protocol was signed with the Cooperativa de Productores de Agricultura Biológica-CRL (BioAzórica) and a specific working group was created to define a strategic plan and action plan for the development and implementation of organic agriculture in the Region. This Regional Strategy for the Development of Organic Agriculture and the Plan of Action for the Production and Promotion of Organic Agricultural Production in the Azores will be expected not to be far from the national concepts and actions. This document results from the detailed analysis of the actions of the national strategy and its adaptation to the specific characteristics of the Region. This approach is reflected on its structure and content by defining a specific strategic plan and with some own and exclusive measures of the Region based on the current knowledge of the state of development of organic production, or modo de produção biológica in Portuguese (from here on abbreviated as MPB).
Overview of the strategic plan
This strategic document consists of two parts. The first part (I), Characterizing Agriculture and Organic Production, begins with the definition of organic agriculture, the characterization of organic production in the world (Agence BIO, 2017; INFOAM EU Group, 2016; Willer and Lernoud, 2017), the European community (DGAGRI, 2013), Portugal (DGADR, 2016; INE 2002; 2013), and the Azores Autonomous Region (SREA, 2015; 2016). The legislation and the support measures for organic production are referred and the organic farming teaching and professional formation is also discussed, involving also the investigation and experimentation and demonstration procedures made until now in the country and in the Azores region. This part ends with a swot analysis of the situation of Biological Agriculture in the Azores Region. The second part (II), Strategic Objectives and Axes for the Development of Organic Agriculture in the Azores Autonomous Region, presents the strategic objectives and the axes of the action plan, operational objectives, and actions to be developed on the short-term (1 to 2 years), medium-term (3 to 5 years) and long-term (6 to 10 years) (Table 1). Finally, there is a set of tables with all actions of the action plan for each of the operational objectives to be developed. In its final part, based on surveys carried out an assessment is also presented on the development potential of Organic Agriculture in the different islands of the Azorean Autonomous Region.
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Table 1. Short-term, medium-term, and long-term measures for the development of the Strategic Plan in the Autonomous Region of the Azores.
Short-term measures - Elaborate a proposal to create new support and increase existing support for MPB - Raise awareness for producers, operators and technicians - Increase the organic milk production in the Azores - Increase number of organic meat producers in the Azores - Market studies to define priority sectors to be developed in MPB - Establish an applied research network for the promotion of organic farming - Elaborate technical specifications, specific in the various aspects, to support technicians and producers in MPB - Increase the number of producers in MPB of horticultural crops with special interest - Stimulate the creation of professional and higher education training in organic farming - Public awareness campaigns in MPB in schools - Elaborate advertising and marketing campaigns focused on organic products and MPB - Promote visits by technicians and producers to organic farms outside of the Azores - Create an online portal on organic farming - Establish an operational group to monitor the implementation of the organic agriculture development strategy in the Azores - Create a Regional Observatory for Organic Agriculture Medium-term measures - Ensure the creation/inclusion of measures to increase support for organic farming in the next Rural Development Program (PRORURAL+ and POSEI) - Create technical centers with the associations of producers of all islands of the Azores - Implement demonstration plots based on the results of applied research on priority crops - Prepare technical manuals in MPB - Make progress in the production of dairy products in MPB - Implement school gardens in MPB - Create biological seed banks and biological vegetative propagation material on some islands in the Azores - Maintain and update the portal on organic farming in the Azores - Evaluate the implementation of the proposed actions and possible adjustments to be included in the defined strategy - Encourage the adhesion of the municipalities of the Azores to join the international network of bioregions Long-term measures - Implement the measures and actions proposed by the medium-term evaluation in the defined strategy - Create a competence center for organic farming - Define a strategy for the definition and development of a BIO island
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Part II
In the definition of the Regional Strategy for the Development of Organic Agriculture of the Azores, for a time horizon of 10 years, five strategic objectives were defined: o Strategic Objective 1: To promote the expansion of biological production areas in the Agriculture, Livestock and Aquaculture sectors, by improving technical support and strengthening its economic importance; o Strategic Objective 2: To increase production and consequently the supply of agricultural and agri-food products from organic production, promoting its competitiveness and commercial profitability in domestic and foreign markets; o Strategic Objective 3: To promote technical-scientific knowledge and to raise the level of competences on organic production under regional specific soil and climatic conditions; o Strategic Objective 4: To stimulate business innovation and the availability of statistical information on the Biological Products market with a focus on future generations and strengthening partnerships through the development of dissemination, information and awareness raising actions; o Strategic Objective 5: Increase the demand for organic products by effectively creating different ranks, opening new markets, promoting them and enhancing the trust and credibility of these products with the consumer.
These five specific strategic objectives for organic farming are in line with those defined and included in the Program of the XII Government of the Autonomous Region of the Azores for Agriculture, Livestock and Forestry. In order to achieve these strategic objectives, four Axes of the Plan of Action were defined: o Axis 1: Production; o Axis 2: Research, training and technical support; o Axis 3: Innovation, knowledge transfer and information dissemination; o Axis 4: Promotion of products and Markets. The Regional Strategy for the Development of Organic Agriculture in Azores was defined with a time horizon of 10 years, and its evaluation and mid-term review is scheduled at the end of its 5th year of validity or application (2023), coinciding also with the evaluation implementation of the Plan of Action for the production and promotion of organic products. At the end of 2023, together with the mid-term review of this Regional Strategy for the Development of Organic Agriculture of the Azores, a second Action Plan should be defined for the period 2024-2029, already in force in the new framework and a new regional development program, which are expected to reflect the measures proposed here. In this sense, the strategic axes, strategic and operational objectives of this Strategy, as well as some financial measures involving the increase of support necessarily integrate the principles and guidelines that should serve as a basis for the definition of the next Regional Development Program. Thus, 15 strategic goals were defined: o Duplicate the current MPB area of the Autonomous Region of the Azores; o Duplicate areas of fruit and vegetable crops intended for direct consumption or processing; o Doubling the livestock production and beekeeping in MPB of the Azores; o Ensure that products of animal origin in MPB are marketed as biological products; o Creation of aquaculture production units in MPB; o Increase the internal processing capacity of agricultural biological products, animals and aquaculture; 27
o Increase consumption of organic products; o Duplicate the availability of regional biological products in the market; o Triple the specific training offer for producers and operators in AB; o Strengthen the specific technical capacity in MPB, by doubling the number of accredited technicians; o Promote the specific training offered in AB in vocational and higher education in the Azores; o Increase the applied Research in MPB with the creation of an experimentation network, with at least one certified experimental unit, in 4 islands of the Azores; o Elaborate at least 5 technical manuals and specific dissemination material in strategic areas of activity in MPB; o Create a portal on organic farming; o Create and operationalize of a Regional Observatory for Organic Agriculture;
The assumption of these goals is even more relevant when combined with the objectives adopted for increases in production and supply of regional products of excellence intended for direct consumption in detriment of pasture and forage areas that are currently supported in MPB without any production and placement markets for organic products. This is followed by a policy of diversification of regional production to the market, contrary to the current trend of increasing imports, aiming at increasing the degree of self-provision in organic products and organizing the commercialization of organic products and encouraging the appearance and presence of these products on local, national and European markets. At the same time, it is intended to effectively strengthen consumer knowledge and trust in organic products, with consumer awareness and information in order to develop consumption in a sustainable way, allowing capture of value and market for this production. There is also a need to continue a significant effort in production and especially in the technical assistance to producers by recreating a real system of rural extension as a way of guaranteeing the diffusion of knowledge, without which it will be difficult to achieve the objectives outlined here. Given the industry's lower economic attractiveness to industry, applied research and support for innovation in agriculture and organic production, it cannot fail to be considered as a particularly important area for public investment by strengthening research, demonstration and experimentation (I & DE). In this sense, through targeted public support, efforts will be made to fill gaps in knowledge production, training and education, as well as the dissemination of information. Promotion of the consumption of regional organic products will be strengthened by the integration of these products into school curricula of the various levels of education in the Region. The measures to be undertaken for the development of this strategy in the short-, medium- and long-term are presented above in Table 1.
As an example, a detailed plan of actions table is presented (Table 2).
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Table 2. Table with plan of actions for Axis 1: Production. Shown are all actions of the action plan for all strategic and operational objectives as well the entities involved in the development of these actions.
Operational Entities involved in Strategic objectives Actions to be developed objectives development of actions Encourage the expansion of 1.1 - Increase 1.1.1 - Discriminate Regional Government of production areas in the organic production positively investment support the Azores and Producer Organic Production Mode in for organic farming, Organizations the Agriculture, Livestock particularly in the most and Aquaculture sectors, by important ones for the market improving their technical (horticulture, fruit growing) viability and enhancing their economic importance 1.1.2 - Give priority to crops Regional Government of that can contribute to lower the Azores, Azores imports in order to meet the University and Producer needs of own consumption, Organizations especially in horticulture and fruit crops from the MPB
1.1.4 - Institute the possibility Regional Government of of conversion to MPB of the Azores, Azores other Agro-environmental University and Producer systems without loss of Organizations support
1.1.5 - Create new Regional Governement of mechanisms for the Azores differentiating the monetary support provided for in the conversion period by area of farms devoted to horticultural and fruit production, compensating producers for production losses during this period. 1.2.1 - Discriminate Regional Governement of positively the promotion of the Azores organic livestock production
Regional Government of 1.2.2 - Encourage the the Azores, Chambers of production of milk and dairy Commerce and Industry and products, their export and Producer Organizations placement in national and international markets
Regional Government of 1.2.3 - Encourage the the Azores and Producer production of organic meat Organizations 1.2.4 - Encourage and Regional Governement of guarantee the exit of products the Azores of plant and animal origin and their derivatives from pastures in MPB, object of support
29
Acknowledgements
We thank to all the working group members: Beatriz Medeiros, Adelaide Mendes – Instituto Alimentação e Mercados Agrícolas, Secretaria Regional de Agricultura e Florestas (SRAF); Ana Branco – Serviço de Desenvolvimento Agrário do Faial, SRAF; Ana Mendonça – Direção Regional das Pescas, Secretaria Regional do Mar, Ciência e Tecnologia (SRCMT); Diogo Araújo, Ricardina Barbosa, Vânia Coelho, José Adriano Mota, Carlos Santos – Direção Regional da Agricultura, SRAF; Jorge Tiago T. S. O. Martins – Serviço de Desenvolvimento Agrário da Terceira, SRAF; Susana Lima, Mónica Rocha – BioAzórica, Produtos de Agricultura Biológica-CRL; Susana Sebastião – Gabinete de Planeamento, SRAF. We also thank the following people for contributing to this strategy document: Prof. José Estevam de Matos, Prof. João Pedro Barreiros, Prof. Paulo Borges, Prof. Rosalina Gabriel, and technicians: Maria Clara Cogumbreiro Estrela Rego, Cristina Márcia Gonçalves Saramago Roque, Maria José Aranda e Silva
References
Agence BIO 2017. La BIO dans le monde. Edition 2017. Les carnets de l’Agence BIO. Observatoire National de L’Agriculture Biologique, Montreuil, France. DGADR 2016. Portugal Continental: produtores agrícolas (1994-2005). [WW document] http://www.dgadr.mamaot.pt/sustentavel/modo-de-producao-biologico. Cited 30 Apr. 2019. DGAGRI 2013. Facts and figures on organic agriculture in the European Agriculture. [WWW document] http://ec.europa.eu/agriculture/rural-area-economics/ index_en.htm. Cited 30 Apr. 2019. DSDA 2016. Plano Estratégico para a Agricultura Biológica 2016-2020. Direção de Serviços de Desenvolvimento da Agricultura, Secretaria Regional de Agricultura e Pescas, Região Autónoma da Madeira, Portugal. ENAB 2016. Resolução de Conselho de Ministros nº 110/2017, de 27 de julho: Aprova a Estratégia Nacional para a Agricultura Biológica (ENAB) e o Plano de Ação (PA) para a produção e promoção de produtos agrícolas e géneros alimentícios biológicos. IFOAM EU Group 2016. Organic in Europe. Prospects and development 2016. [WWW document] https://shop.fibl.org/CHen/mwdownloads/download/link/id/767/?ref=1. Cited 30 Apr. 2019. INE 2002. Inquérito à Floricultura. Instituto Nacional de Estatística, Lisboa, Portugal. INE 2013. Floricultura e plantas ornamentais 2012, Edição de 2013. Instituto Nacional de Estatística, Lisboa, Portugal. SREA 2015. Inquérito à Horticultura 2014. Informação Estatística, Serviço Regional de Estatística dos Açores, Portugal. SREA 2016. Inquérito à Fruticultura 2015. Informação Estatística, Serviço Regional de Estatística dos Açores, Portugal. Willer, H. and Lernoud, J. 2017. The World of Organic Agriculture Statistics and Emerging Trends. Research Institute of Organic Agriculture (FIBL), Frick, and IFOAM – Organics International, Bonn, Germany.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 30-32
Evaluating the risks and benefits of Aphelinus certus, an introduced enemy of soybean aphid, in North America
James R. Miksanek* and George E. Heimpel University of Minnesota Department of Entomology, St. Paul, Minnesota, USA *Corresponding author: [email protected]
Abstract: Exotic biological control agents under consideration for importation and release are evaluated for risk through the sole use of laboratory-based studies of host range, but ecosystem- and landscape-level effects should be incorporated into the decision-making process as well. The recent invasion of Aphelinus certus (Hymenoptera: Aphelinidae), a generalist Asian parasitoid attacking soybean aphid and native Aphis spp., provides a rare opportunity to investigate the role of a natural enemy in a complex network of interactions – both positive and negative, direct and indirect – throughout the ecological landscape. To address this, we (a) surveyed the distribution and population dynamics of A. certus in agricultural and native habitats and (b) used population models and field studies to determine the potential and actual effect of A. certus on soybean aphid. We found that A. certus readily colonizes or has successfully established in prairies, although the magnitude of its impact on native aphid populations has yet to be quantified. We also show that A. certus has the potential to be a key natural enemy of soybean aphid, although its effectiveness in the field has been more variable. Finally, we discuss the overall impact of A. certus within a risk – benefit framework incorporating its direct effects on soybean aphid and native aphid species as well as potential indirect effects in reducing insecticide applications, which, by extension, aids in conservation of pollinators and other vulnerable insect species. This perspective promotes an environment-based decision-making approach to classical biological control.
Key words: biological control, parasitoid, Aphelinus certus, soybean aphid, North America, matrix model, risk – benefit, non-target effects
Introduction
While management of soybean aphid (Aphis glycines) in North America tends to rely on neonicotinoid seed treatments and seasonal applications of broad spectrum foliar insecticides, biological control offers an alternative or complementary management strategy that may reduce risk to beneficial non-target organisms such as natural enemies, pollinators, or other species of conservation interest (Heimpel et al., 2004; Ragsdale et al., 2011; Tilmon et al., 2011). Predatory insect residents of North America – including the coccinellids Harmonia axyridis and Coccinella septempunctata, the anthocorid bug Orius insidiosus, the predatory midge Aphidoletes aphidimyza, as well as various chrysopid and syrphid species – offer some protection against soybean aphid, but damaging outbreaks still occur (Ragsdale et al., 2011; Heimpel et al., 2013). To increase the impact of the natural enemy community, exotic agents have been considered for importation and release (Heimpel et al., 2004). One such agent, Aphelinus certus (Hymenoptera: Aphelinidae), was evaluated for release against soybean aphid, but failed laboratory-conducted host-specificity tests because it readily parasitized a
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broad range of non-targets in the genera Aphis, Diuraphis, Rhopalosiphum, Schizaphis, and Myzus (Hopper et al., 2017). As a result, A. certus was not further considered for biological control; however, as an aphid specialist, there may be an argument for its use in classical biological control if the benefits (pest population suppression and indirect reduction in insecticide applications) outweigh the risks (attack of native aphid species). Thus, the accidental introduction of A. certus in North America in 2005 provides a rare opportunity to investigate the effects of a generalist natural enemy of aphids, allowing for a retrospective assessment of the process involving exotic enemy selection in classical biological control.
Material and methods
Lab-parameterized population models and field experiments were used to determine the potential and actual impact of A. certus on soybean aphid, and field surveys were used to document the distribution and dynamics of A. certus in paired agricultural and native prairie sites. Bioassays estimating host and parasitoid developmental times as well as parasitoid host- stage preference, longevity, and fecundity were used to parameterize a coupled host-parasitoid stage-structured matrix model. Supplemental life history parameters were obtained from the literature (Lin and Ives, 2003; McCornack et al., 2004; Costamagna et al., 2007; Frewin et al., 2010). Simulations were run for 90 days using starting population densities estimated from 2017 field surveys (described below). Field experiments consisted of 202 whole-plant exclusion cages set up at six sites in central and western Minnesota during 2017 and 2018. Three experimental treatments were used: (1) an open cage that allowed all natural enemies access to aphids; (2) a predator exclusion cage with a wide mesh that allowed only A. certus, the smallest natural enemy, access to aphids; and (3) a total exclusion cage with a very fine mesh that prevented all enemies from accessing aphids. Additionally, sham cages were used to control for microclimate, and the production of alate aphid morphs was carefully monitored. Finally, field surveys of four pairs of soybean and prairie sites spanning western Minnesota occurred during 2017 and 2018; depending on site and relative abundance of host plants, 50–200 individual Monarda fistulosa, Asclepias spp., and/or soybean were sampled from the interior of each site every 2-3 weeks.
Results and discussion
Model analysis showed that A. certus suppressed peak soybean aphid population densities, keeping soybean aphid populations below the economic injury level (674 aphids per plant) in 30.2% of simulations and below the economic action threshold (250 aphids per plant) in 9.5% of simulations. In all cases, a 21% daily level of parasitism was required to maintain aphid population growth at or below replacement level. However, manipulative field experiments did not identify A. certus as a factor in reducing the growth rate of soybean aphid populations, although the natural enemy community in general did reduce aphid population growth at two of the six sites studied. Field surveys of paired soybean-prairie sites identified A. certus attacking the native aphids Aphis asclepiadis and Aphis monardae, and the colonization timelines of A. certus in soybean and prairies were similar. When present, A. certus parasitized native aphid species at equal or greater rates compared to soybean aphid. The lab-parameterized population model identified A. certus as a potentially key natural enemy of soybean aphid, suggesting that this parasitoid reduces soybean aphid densities at a relevant economic level. This reduction in densities would result in an indirect decrease in 32
insecticide applications and, by extension, aid in protection of pollinators and other species of conservation interest. However, contrary to the predictions of the model, A. certus was not found to be effective in the field. These results are in contrast with a previous experiment conducted in Minnesota (Kaser and Heimpel, 2018) but are consistent with a study in Quebec (Leblanc and Brodeur, 2018). Additionally, sampling in prairie habitats revealed that A. certus has successfully established in (or readily colonizes) prairies and attacks native aphid species, although the magnitude of its impact on native species has yet to be quantified. Whereas some degree of risk to native aphids may have been acceptable in a risk-benefit analysis, there is limited field-based evidence that identifies a benefit of A. certus in reducing pest populations. Overall, this paradigm of incorporating broader (and often indirect) environmental variables in the decision-making process for classical biological control agents is worth further investigation (Heimpel and Mills, 2017).
References
Costamagna, A. C., Landis, D. A. and Difonzo, C. D. 2007. Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans. Ecol. Appl. 17: 441-451. Frewin, A. J., Xue, Y., Welsman, J. A., Broadbent, A. B., Schaafsma, A. W. and Hallett, R. H. 2010. Development and parasitism by Aphelinus certus (Hymenoptera: Aphelinidae), a parasitoid of Aphis glycines (Hemiptera: Aphididae). Environ. Entomol. 39: 1570-1578. Heimpel, G. E., Ragsdale, D. W., Venette, R., Hopper, K. R., O’Neil, R. J., Rutledge, C. E. and Wu, Z. 2004. Prospects for importation biological control of the soybean aphid: Anticipating potential costs and benefits. Ann. Entomol. Soc. Am. 97: 249-258. Heimpel, G. E., Yang, Y., Hill, J. D. and Ragsdale, D. W. 2013. Environmental consequences of invasive species: Greenhouse gas emissions of insecticide use and the role of biological control in reducing emissions. Plos One 8: e72293, doi:10.1371/journal.pone.0072293. Heimpel, G. E. and Mills, N. J. 2017. Biological Control: Ecology and Applications. Cambridge University Press, Cambridge, UK. Hopper, K. R., Lanier, K., Rhoades, J. H., Hoelmer, K. A., Meikle, W. G., Heimpel, G. E., O’Neil, R. J., Voegtlin, D. G. and Woolley, J. B. 2017. Host specificity of Aphelinus species collected from soybean aphid in Asia. Biol. Control 115: 55-73. Kaser, J. M. and Heimpel, G. E. 2018. Impact of the parasitoid Aphelinus certus on soybean aphid populations. Biol. Control 127: 17-24. Leblanc, A. and Brodeur, J. 2018. Estimating parasitoid impact on aphid populations in the field. Biol. Control 119: 33-42. Lin, L. A. and Ives, A. R. 2003. The effect of parasitoid host-size preference on host population growth rates: An example of Aphidius colemani and Aphis glycines. Ecol. Entomol. 28: 542-550. McCornack, B. P., Ragsdale, D. W. and Venette, R. C. 2004. Demography of soybean aphid (Homoptera: Aphididae) at summer temperatures. J. Econ. Entomol. 97: 854-861. Ragsdale, D. W., Landis, D. A., Brodeur, J., Heimpel, G. E. and Desneux, N. 2011. Ecology and management of the soybean aphid in North America. Ann. Rev. Entomol. 56: 375-399. Tilmon, K. J., Hodgson, E. W., O’Neal, M. E. and Ragsdale, D. W. 2011. Biology of the soybean aphid, Aphis glycines (Hemiptera: Aphididae) in the United States. J. Integr. Pest Manag. 2: 1-7. Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 33-36
Age and temperature effects on accumulation of carotenoids in ladybirds
Oldřich Nedvěd1,2*, Aslam Muhammad1,2, Rahim Abdolahi3, Samane Sakaki4 and Antonio O. Soares5 1Faculty of Science, University of South Bohemia, Branišovská 31, 37005 České Budějovice, Czech Republic; 2Institute of Entomology, Biology Center, Branišovská 31, 37005 České Budějovice, Czech Republic; 3Department of Plant Protection, College of Agriculture and Natural Resources, University of Tehran, Karaj, P.O. Box 31587-77871, Iran; 4Department of Plant Protection, College of Agriculture, Vali-e-Asr University of Rafsanjan, Rafsanjan, Iran; 5cE3c - ABG - Centre for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Azores, Portugal *Corresponding author: [email protected]
Abstract: Carotenoids are important pigments of ladybirds providing bright red colouration. We measured the rate of deposition of carotenoids with age in elytra of two ladybird species in ethanol extracts, as well effects of sex and temperature. In Coccinella undecimpunctata, content of carotenoids continued to increase after 60 days of adult age at both 20 and 25 °C. Males had slightly higher pigment concentration than females. Carotenoid content in adult Harmonia axyridis (forma succinea) increased up to four months of the adult stage. No difference was found between individuals with contrasting extent of melanic pattern or between sexes. The trend of increase was between Holling functional types 1, 2, and 3. In a later experiment, the carotenoid content increased up to three months of the adult stage similarly for three levels of melanisation. There was no decrease of carotenoids in individuals with large melanic patterns. This means that carotenoids are not deposited under black spots. After four months, there was little decrease in carotenoid content. Thus, the trend was between functional types 2, 3, and 4. Slower rate of carotenoid deposition during adult stage after 1 week and 1 month was observed at higher temperatures (25, 30 °C) than at lower ones (15, 20 °C).
Key words: colouration, ladybirds, pattern, pigment, time
Introduction
Carotenoid pigments are important compounds in the epidermis of ladybird beetles (Coleoptera: Coccinellidae) providing bright red colouration of elytra and other body parts. Together with melanin pattern in the cucticle, they provide aposematic signalling to potential predators (Průchová et al., 2014; Ceryngier et al., 2018), they moderate thermal properties of the body surface (heating by basking; DeJong et al., 1996), and there is assortative mating among colour morphs of the same species (Odonald et al., 1984). Animals are not able to synthesize carotenoids and they ingest them with food. Thus, some ladybirds gradually develop their colour background from yellow through orange to red during the adult stage, according to the rate of deposition of carotenoids in their elytra (Bezzerides et al., 2007).
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We investigated the rate of this deposition in two ladybird species depending on age, sex, extent of melanic pattern, and temperature by extracting carotenoids in ethanol and subsequent spectrophotometric measurements.
Material and methods
We reared larvae of Coccinella undecimpunctata, a population originating from Azores Islands, Portugal, under laboratory conditions (25 °C, 16 L:8 D) until adult stage. Then we reared the adults at two temperatures: 20 and 25 °C, feeding them by Aphis fabae raised on Vicia faba. For Harmonia axyridis, forma succinea, in the first experiment, we reared pupae at two constant temperatures affecting the size of melanic spots: 17 °C – large, 26 °C – small, and under long day photoperiod (18L:6D). We subsequently reared these adults at thermofotoperiod (15 °C, 6 h, D / 20 °C, 6 h, L / 25 °C, 6 h, L / 20 °C, 6 h, L), feeding them by Acyrthosiphon pisum raised on Vicia faba. In the second experiment, we reared H. axyridis pupae at three constant temperatures affecting the size of melanic spots: 15 °C – large, 22 °C – small, and 30 °C – missing. In the third experiment, we reared adults of H. axyridis that hatched at constant 20 °C at four subsequent constant temperatures (15, 20, 25, 30 °C). We sampled adults from the stock, 10 males and 10 females, at diverse ages. We killed the beetles, cut both elytra, deposited them in 500 μl of 96% ethanol in a sealed Eppendorf vial at 4 °C under darkness for one month. We measured absorbance of the extracts at 450 nm in 96-well plates, volume 200 μl.
Results and discussion
In C. undecimpunctata, content of carotenoids was still increasing after 60 days of adult age at both 20 °C and 25 °C, according to trend being something between Holling functional types 1 and 2. Males had slightly higher pigment concentration than females (Figure 1). The content of carotenoids in adults of H. axyridis, forma succinea, increased up to four months of the adult stage similarly for both small and large extent of the melanic pattern (achieved by rearing pupae at 17 and 26 °C, respectively) and for both sexes. The trend was something between Holling functional types 1, 2, and 3 (Figure 2). Carotenoids contents in adults of H. axyridis, when pupae developed at three temperatures affecting the size of melanic spots (15, 22, and 30 °C), increased up to three months of the adult stage similarly for all colour patterns. There was no clear decrease of carotenoids in individuals with large melanic pattern. This means that under black spots, carotenoids are not deposited. They are either deposited in the entire elytra surface or in the smaller visible part of epidermis with higher intensity. After four months, there was little decrease in carotenoid content. Thus, the trend was something between functional types 2, 3, and 4.
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Figure 1. Deposition of carotenoids of Coccinella undecimpunctata at 20 °C. Blue curve: males. Red curve: females.
1,2
1,0
0,8
0,6
Absorbance
0,4
0,2
0,0 0 20 40 60 80 100 120 140 160 180 Time [days] Figure 2. Deposition of carotenoids of Harmonia axyridis at thermophotoperiod with average 20 °C. 36
Lower amount of carotenoids after 1 week and 1 month of adult life was observed at higher temperatures (25, 30 °C) than at low ones (15, 20 °C). This difference somewhat complicates use of the concentration as universal measure of age of ladybirds. There was mostly negligible difference between sexes. The provided knowledge about the gradual increase of carotenoid contents in elytra of ladybirds with adult age is important for estimation of the age of individuals and number of co-occurring generations in the field populations of ladybirds (L. Fiedler and O. Nedvěd, unpublished data).
Acknowledgements
We thank Selgen A.s. company in Stupice, Czech Republic, for providing seeds of Vicia faba for free.
References
Bezzerides, A. L., McGraw, K. J., Parker, R. S. and Husseini, J. 2007. Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav. Ecol. Sociobiol. 61: 1401-1408. Ceryngier, P., Nedvěd, O., Grez, A. A., Riddick, E. W., Roy, H. E., San Martin, G., Steenberg, T., Veselý, P., Zaviezo, T., Zúñiga-Reinoso, Á. and Haelewaters, D. 2018. Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biol. Invasions 20: 1009-1031. DeJong, P. W., Gussekloo, S. W. S. and Brakefield, P. M. 1996. Differences in thermal balance, body temperature and activity between non-melanic and melanic two-spot ladybird beetles (Adalia bipunctata) under controlled conditions. J. Exp. Biol. 199: 2655-2666. Odonald, P., Derrick, M., Majerus, M. and Weir, J. 1984. Population genetic theory of the assortative mating, sexual selection and natural-selection of the 2-spot ladybird, Adalia bipunctata. Heredity 52: 43-61. Průchová, A., Nedvěd, O., Veselý, P. and Fuchs, R. 2014. Visual warning signals of the ladybird Harmonia axyridis (Pallas, 1773): the avian predators’ point of view. Entomol. Exp. Appl. 151: 128-134.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 37-39
Anagonia sp. (Diptera: Tachinidae), potential biocontrol agent of Gonipterus platensis (Coleoptera: Curculionidae) in the Iberian Peninsula
Catarina Afonso1*, Carlos Valente1, Catarina I. Gonçalves1, Ana Reis2, Beatriz Cuenca3 and Manuela Branco4 1RAIZ, Forest and Paper Research Institute, Quinta de S. Francisco, Rua José Estevão (EN 230-1), 3800-783 Eixo, Aveiro, Portugal; 2Altri Florestal, S.A., Quinta do Furadouro, 2510-582 Olho Marinho, Portugal; 3Vivero Maceda, Grupo Tragsa – SEPI, Carretera Maceda, Baldrei, Km 2, 32700 Maceda, Spain; 4CEF – Forest Research Centre – Instituto Superior de Agronomia, Tapada da Ajuda, 1349-017 Lisboa, Portugal *Corresponding author: [email protected]
Extended abstract: Eucalyptus-feeding weevils from the “Gonipterus scutellatus” complex (Coleoptera: Curculionidae) are a group of species native to Australia. Some of these insects have accidentally spread from their native range into various parts of the world where they have become major pests of eucalypt plantations, as both larvae and adult feed on leaves of Eucalyptus trees. From these, the Tasmanian Gonipterus platensis (Marelli) is considered to be the most detrimental and widely distributed species (Mapondera et al., 2012). First introduced in South Africa (Tooke, 1955), the egg-parasitic wasp Anaphes nitens (Girault) (Hymenoptera: Mymaridae) has been the key parasitoid in all classical biological control programs implemented against these weevils worldwide. However, this egg parasitoid has failed to prevent economically relevant attacks of G. platensis in eucalypt plantations in several regions, namely in the Iberian Peninsula (Cordero Rivera et al., 1999; Reis et al., 2012; Valente et al., 2018). The partial success of Gonipterus spp. control by A. nitens has traditionally been explained as a consequence of the parasitoid maladaptation to environmental factors, in particular low temperatures during winter and at higher altitudes (Reis et al., 2012). Today, however, it is clear that host-parasitoid mismatch has also contributed to this ineffective control of the pest (Barratt et al., 2018). Therefore, new or better host and/or climate-matched natural enemies of this insect pest are currently being studied. Additional natural enemies of G. platensis have been recently identified and imported from Tasmania, Australia, including the Tasmanian egg-parasitoid Anaphes inexpectatus Huber and Prinsloo (Hymenoptera: Mymaridae), which has been studied and already released in Portuguese mainland (Valente et al., 2017 a; Valente et al., 2017 b). Nevertheless, as eucalypt pests around the globe are rapidly increasing their rate of spread (Hurley et al., 2016), the use of supplementary parasitoids might be valuable to increase pest control. Introducing multiple natural enemy species is a strategy that might lead to greatest reduction of pest densities, especially if they present some degree of niche separation (Pedersen and Mills, 2004). As such, recent efforts have been made in order to identify and study parasitoids attacking different life stages of G. platensis (Valente et al., 2017 b). Field surveys undertaken in Tasmania in 2017 followed by the import of Gonipterus spp. larvae allowed the establishment of larval parasitoid populations from the genus Anagonia (Diptera: Tachinidae) under quarantine conditions in Portugal, since December 2017.
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Available information about tachinids and especially Anagonia species related to Gonipterus species is scarce. Field surveys in Tasmania indicate 2 to 12% parasitism rates by at least two Anagonia species on Gonipterus spp. larvae and the revision of the genus Anagonia by Donald Colless (2012) indicates that six Anagonia species parasitise Gonipterus spp. and the remaining species are mainly associated with chrysomelids. Rearing of Anagonia sp. under quarantine conditions has allowed the study of its basic life cycle and to determine its mode of attack (direct oviposition on L3/L4 instars of G. platensis). Furthermore, observations throughout its rearing show that chemosensory cues from hosts and cues from the host plant (Eucalyptus globulus) seem to play an important role for parasitism behavior and rates by this species. Although tachinids are not very popular as biological control agents, as many exhibit unusually wide host ranges, a few species have been successfully used in biological control programs (Stireman et al., 2006; Dindo and Grenier, 2014). Anagonia sp. has shown to be relatively easy to rear, with parasitism rates up to 50% on the target host in the laboratory, and available literature indicates that it might have a narrow host range (Colless, 2012). Once it attacks the host larvae, Anagonia sp. might be a very good candidate to apply in biological control programs against G. platensis in order to complement the activity of already established egg-parasitoids. This parasitoid will be further studied, and a complete environmental risk assessment will be performed prior to its putative release in the field in the Iberian Peninsula.
References
Barratt, B. I. P., Cock, M. J. W. and Oberprieler, R. G. 2018. Weevils as targets for biological control, and the importance of taxonomy and phylogeny for efficacy and biosafety. Divers. 10(3): 73-82. Colless, D. H. 2012. The Froggattimyia-Anagonia genus group (Diptera: Tachinidae). Rec. Aust. Mus. 64(3): 167-211. Cordero Rivera, A., Santolamazza Carbone, S. and Andres, J. A. 1999. Life cycle and biological control of the Eucalyptus snout beetle (Coleoptera, Curculionidae) by Anaphes nitens (Hymenoptera, Mymaridae) in north-west Spain. Agric. For. Entomol. 1: 103-109. Dindo, M. L. and Grenier, S. 2014. Production of dipteran parasitoids. In: Mass Production of Beneficial Organisms: Invertebrates and Entomopathogens (eds. Morales-Ramos, J. A.; Rojas, M. G. and Shapiro-Ilan, D. I.): 101-143. Academic Press, London, UK. Hurley, B. P., Garnas, J., Wingfield, M. J., Branco, M., Richardson, D. M. and Slippers, B. 2016. Increasing numbers and intercontinental spread of invasive insects on eucalypts. Biolog. Invasions. 18: 921-933. Mapondera, T. S., Burgess, T., Matsuki, M. and Oberprieler, R. G. 2012. Identification and molecular phylogenetics of the cryptic species of the Gonipterus scutellatus complex (Coleoptera: Curculionidae: Gonipterini). Aust. J. Entomol. 51: 175-188. Pedersen, B. S. and Mills, N. J. 2004. Single vs. multiple introduction in biological control: the roles of parasitoid efficiency, antagonism and niche overlap. J. Appl. Ecol. 41: 973-984. Reis, A. R., Ferreira, L., Tomé, M., Araújo, C. and Branco, M. 2012. Efficiency of biological control of Gonipterus platensis (Coleoptera: Curculionidae) by Anaphes nitens (Hymenoptera: Mymaridae) in cold areas of the Iberian Peninsula: implications for defoliation and wood production in Eucalyptus globulus. For. Ecol. Manag. 270: 216-222. 39
Stireman, J. O. III, O’Hara, J. E. & Wood, D. M. 2006. Behavior, ecology and evolution of tachinid parasitoids. Annu. Rev. Entomol. 51: 525-555. Tooke, F. 1955. The Eucalyptus Snout Beetle, Gonipterus scutellatus Gyll. A study of its ecology and control by biological means. Entomol. Mem. Union S. Af. 3: 1-282. Valente, C., Afonso, C., Gonçalves, C. I., Alonso-Zarazaga, M. A., Reis, A. and Branco, M. 2017 a. Environmental risk assessment of the egg parasitoid Anaphes inexpectatus for classical biological control of the Eucalyptus snout beetle, Gonipterus platensis. BioControl 62(4): 457-468. Valente, C., Gonçalves, C. I., Reis, A. and Branco, M. 2017 b. Pre-selection and biological potential of the egg parasitoid Anaphes inexpectatus for the control of the Eucalyptus snout beetle, Gonipterus platensis. J. Pest Sci. 90(3): 911-923. Valente, C., Gonçalves, C. I., Monteiro, F., Gaspar, J., Silva, M., Sottomayor, M., Paiva, M. R. and Branco, M. 2018. Economic outcome of classical biological control: a case study on the Eucalyptus snout beetle, Gonipterus platensis, and the parasitoid Anaphes nitens. Ecol. Econ. 149: 40-47.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 40-41
Risk and benefit assessment of biological control agents in Switzerland: A case study with Trichopria drosophilae
Jana Collatz*, Sarah Wolf, Nasim Amiresmaeili and Jörg Romeis Agroscope, Research Division Agroecology and Environment, Reckenholzstrasse 191, 8046 Zürich, Switzerland *Corresponding author: [email protected]
Extended abstract: In Switzerland, licensing for the use of invertebrates as plant protection products or as classical biological control agents in agriculture is carried out by the Federal Office for Agriculture based on the Ordinance on Plant Protection Products, whereas the Federal Office for the Environment regulates the release of organisms outside the agricultural context. Among other aspects, information on the organism’s natural distribution, its biology and efficacy are required during the application process of a plant protection agent to allow the assessment of benefits and risks by scientific experts (Mason et al., 2017). The latter requires extensive knowledge about the agent and its environment. We selected the hymenopteran parasitoid Trichopria drosophilae Perkins (Hymenoptera: Diapriidae) as a case study. This pupal endoparasitoid can parasitize the invasive Drosophila suzukii Matsumura (Diptera: Drosophilidae), a major pest in fruit and berry crops, and is currently considered for use in several European countries (Knoll et al., 2017; Rossi Stacconi et al., 2018). To determine whether T. drosophilae is a native species, we infested fruits by several native Drosophila species, and exposed them in the field to allow parasitoids to lay eggs on. Subsequent emergence of parasitoids from samples that had been exposed in Northern and Southern Switzerland revealed that T. drosophilae is common in the southern parts of the country and only occasionally found in the north where the closely related Trichopria modesta (Ratzeburg) is common. To evaluate the parasitoid’s potential for winter survival in Northern Switzerland, adults provided with honey and water as well as immatures inside their host were exposed for 1 month to low temperatures in the laboratory. Prior to exposure, all samples were subjected to a three-week period of gradual reduction of daylight and temperature to initiate potential adaptations to winter conditions. After exposure to 0 °C or -5 °C for 1 month, samples were again incubated at 22 °C. We recorded survival of adults, as well as emergence of T. drosophilae from parasitized pupae. Eggs, larvae, and pupae of T. drosophila survived well at 0 °C. At -5 °C, on the other hand, survival was strongly reduced and only a few eggs and larvae developed into adults. None of the adults survived the cold treatment. No-choice and choice experiments, in which adult T. drosophilae females were offered pupae of Drosophila melanogaster Meigen, D. suzukii, and the larger Drosophila immigrans Sturtevant, demonstrated that D. suzukii is a well suitable and preferred host. However, also other Drosophila hosts are accepted, even in a choice situation. Finally, a semi-field experiment was conducted, to assess the efficacy of T. drosophilae in a quantitative manner. Fruits were infested with pupae of D. melanogaster, D. subobscura Collin or D. suzukii, and exposed either at ground level or at 1m height in field cages. Parasitoids were released into the field cages for three to four days, after which samples were re-collected and kept in a climate chamber until emergence of flies or parasitoids. Trichopria drosophilae were released either alone or in combination with one of the two other native parasitoid species Pachycrepoideus vindemmiae Rondani (Hymenoptera: Pteromalidae) and
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Spalangia erythromera Förster (Hymenoptera: Pteromalidae). Numbers of emerged D. suzukii were significantly reduced when samples had been exposed to T. drosophilae together with one of the pteromalids at both heights. Trichopria drosophilae alone had a weak effect on D. suzukii emergence when presented at the ground, and no effect was observed when the samples were presented at 1m height. Overall, the effects of the parasitoids were limited, although experiments had been conducted in a relatively small, closed system. As T. drosophilae is native to Switzerland and shows a preference for D. suzukii, we conclude that augmentative releases are unlikely to pose an unacceptable environmental threat, however its efficacy to control D. suzukii still needs to be validated.
References
Knoll, V., Ellenbroek, T., Romeis, J. and Collatz, J. 2017. Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci. Rep. 7: 40697. Mason, P. G., Everatt, M. J., Loomans, A. J. M. and Collatz, J. 2017. Harmonizing the regulation of invertebrate biological control agents in the EPPO region: using the NAPPO region as a model. EPPO Bull. 47: 79-90. Rossi Stacconi, M. V., Amiresmaeili, N., Biondi, A., Carli, C., Caruso, S., Dindo, M. L., Francato, S., Gottardello, A., Grassi, A., Lupi, D., Marchetti, E., Mazzetto, F., Mori, N., Pantezzi, T., Tavella, L., Tropea Garzia, G., Tonina, L., Vaccari, G., Anfora, G. and Ioriatti, C. 2018. Host location and dispersal ability of the cosmopolitan parasitoid Trichopria drosophilae released to control the invasive spotted wing Drosophila. Biol. Control 117: 188-196.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 42-44
A rare coccinellid surviving the spread of Harmonia axyridis
Rachel A. Farrow1*, Helen E. Roy2 and Peter M. J. Brown1 1Applied Ecology Research Group, School of Life Sciences, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, UK; 2Centre for Ecology and Hydrology, Maclean Building, Crowmarsh Gifford, Wallingford OX10 8BB, UK *Corresponding author: [email protected]
Extended abstract: Coccinella quinquepunctata (5-spot ladybird) is a small conspicuous ladybird, typically 5 mm in length and red with black spots. In mainland Europe this species is a generalist found in a wide range of habitats such as arable agricultural land, hedgerows, woodlands and grasslands (Majerus et al., 2016). In the UK, C. quinquepunctata is usually recorded in a more restricted habitat of unstable river shingle (Roy et al., 2011). Due to only a handful of records since 1913, the 5-spot ladybird was considered extinct in the UK until 1987 (Majerus and Fowles, 1988). The UK Red Data Book Category 3 (RDB3) classification is described as taxa that are not yet endangered or vulnerable but are at risk due to restrictions in their habitat or geographical area (Hyman, 1992). In Scotland, there were previous records of C. quinquepunctata in the early 1900s (Majerus and Fowles, 1988) and upon the rediscovery in Wales, surveys were subsequently undertaken at previously recorded sites in Scotland resulting in further observations of this species (Littlewood, 2015). Exposed riverine sediment (ERS) is the term used to describe river banks that are in a constant state of alteration due to the nature of the river systems. Several rivers that traverse Wales possess such characteristics. As a result, the invertebrate communities in these habitats are well adapted to the unpredictability of these shingle banks (Sadler et al., 2004). However, due to anthropogenic disturbances such as extraction and livestock access, the quality of habitat is being degraded to the point that specialised invertebrate species are at risk (Hewitt et al., 2010). Bates and Sadler (2004) have described C. quinquepunctata as having an ERS fidelity grade of 1. Essentially this means that the coccinellid species is dependent on unstable river shingle for at least one stage of its life cycle. Aside from these short studies, few details are known about one of the UKs rarest and most specialist ladybird species. Given the RDB3 classification of C. quinquepunctata, and the negative effects of the invasive harlequin ladybird, Harmonia axyridis, on native coccinellids (Brown et al., 2011; Brown and Roy, 2018), it is essential to discover what effect the presence of H. axyridis may be having on this specialist coccinellid. Discovering how this species co-occurs with H. axyridis, would prove insightful in an effort to fully understand how this invasive species affects vulnerable native ladybirds in rural habitats (Roy et al., 2016). It was expected that the invasive alien species would co-occur in high numbers with C. quinquepunctata. Additionally, it was expected that other native coccinellids would occur in the same habitat as C. quinquepunctata but in lower numbers compared to H. axyridis. Twelve Welsh river bank sites were surveyed for the presence of C. quinquepunctata, H. axyridis and other coccinellids. Plant species were recorded and vegetation density was assessed in broad categories. Field locations were identified based on where C. quinquepunctata had previously been recorded and 12 sites were identified on the Rivers Severn, Towy, Usk and Wye in Wales for surveys to be carried out. Direct searching was used on shingle banks to assess C. quinquepunctata numbers in their specialised habitat. Direct searching is a useful method when the target species is conspicuous and unlikely to
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move away quickly if disturbed (Ausden and Drake, 2006) and can be standardised to allow for meaningful interpretation of the results. Searching of shingle bank was carried out for one hour and started at either the water’s edge or where the shingle met with grassland and moved laterally over and back across the shingle. All identified shingle sites had vegetation adjacent and these grass margin areas were also sampled for coccinellids by sweep-netting 100 metres of vegetation. All coccinellids encountered were recorded and identified. Data collection took place between 10:00 and 16:00, when the temperature was greater than 14 °C, weather conditions were dry and wind speeds were below 5 on the Beaufort scale (Met Office, 2010). Nine coccinellid species were recorded at 12 river shingle sites in Wales with 715 individuals being recorded in total. Coccinella quinquepunctata was observed at all 12 sites. A third of the sites had no records of H. axyridis. The majority of coccinellids (86%) were recorded from the direct searching (DS) method with the remaining 14% of observations coming from sweep-netting. In total, over 600 coccinellids were observed by DS with the majority (78%) being C. quinquepunctata. Only six percent of the observed coccinellids were H. axyridis. The remaining 15% of observed coccinellids comprised of Adalia bipunctata. A greater number of coccinellids were recorded during the first visit and as the season progressed the numbers recorded significantly decreased. Combining numbers from all sites, however, C. quinquepunctata was consistently the most recorded species during each visit. Coccinella quinquepunctata was once common in central Europe but recent reports indicate a significant decline over 40 years (Honěk et al., 2016). Climatic conditions in the UK are considered suboptimal for C. quinquepunctata, and the UK is considered as being the edge of the acceptable range for this species (Brown and Roy, 2015). This makes C. quinquepunctata particularly susceptible to negative impacts of H. axyridis through competition for prey and intraguild predation (Roy et al., 2016). However, results here indicate that in the UK, H. axyridis may not be having such a negative impact on C. quinquepunctata. The greater concern is the instability of this species habitat, which leaves this species at risk of sudden decline. At some sites, a large proportion of the vegetation comprised of another invasive species, Himalayan balsam (Impatiens glandulifera) which is known to de-stabilise river banks (GB Non-Native Species Secretariat, 2018). Future analysis of the vegetation of the shingle banks is expected to yield more information about the vegetation requirements of C. quinquepunctata.
References
Ausden, M. and Drake, M. 2006. Invertebrates. In: Ecological census techniques: a handbook. 2nd edition (ed. Sutherland, W. J.): 214-249. Cambridge University Press, UK. Bates, A. and Sadler, J. 2004. Records of rare and notable species of beetle from exposed riverine sediments (ERS) on the rivers Tywi and Upper Severn. Coleopterist 13: 125-132. Brown, P. M. J., Frost, R., Doberski, J., Sparks, T., Harrington, R. and Roy, H. E. 2011. Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol. Entomol. 36: 231-240. Brown, P. M. J. and Roy, H. E. 2015. Reflection on the long-term assessment of ladybird (Coleoptera: Coccinellidae) populations in the Czech Republic and the United Kingdom. Acta Soc. Zool. Bohem. 79: 19-27. Brown, P. M. J. and Roy, H. E. 2018. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv. Divers 11: 230-239. 44
GB Non-Native Species Secretariat 2018. Impacts: Impatiens glandulifera, Himalayan Balsam. [WWW document] http://www.nonnativespecies.org/factsheet/factsheet.cfm? speciesId=1810. Accessed 4 Nov. 2018. Hewitt, S. M., Parker, J. and Kindemba, V. 2010. ERS invertebrate habitat survey of the rivers Afon Ystwyth and Afon Rheidol in Ceredigion. Buglife and Countryside Council for Wales. Honěk, A., Martinokova, Z., Dixon, A. F. G., Roy, H. E. and Pekár, S. 2016. Long-term changes in communities of native coccinellids: population fluctuations and the effect of competition from and invasive non-native species. Insect Conserv. Divers. 9: 202-209. Hyman, P. S. 1992. UK Nature Conservation Series No. 3: a review of the scarce and threatened Coleoptera of Great Britain (Pt. 1). Joint Nature Conservation Committee, Peterborough, England, UK. Littlewood, N. A. 2015. Discovery of 5-spot ladybird Coccinella quinquepunctata (L.) (Col.: Coccinellidae) along the River Dee, Aberdeenshire. Br. J. Entomol. Nat. Hist. 28: 55-57. Majerus, M. E. N. and Fowles, A. P. 1988. The rediscovery of the 5-spot ladybird (Coccinella 5-punctata L.) (Col. Coccinellidae) in Britain. Entomol. Monthly Mag. 125: 177-181. Majerus, M. E. N., Roy, H. E. and Brown, P. M. J. 2016. A natural history of ladybird beetles. Cambridge University Press, UK. Met Office 2010. Beaufort: National Meteorological Library and Archive Fact sheet 6 – The Beaufort scale. Met Office, Exeter, UK. Roy, H. E., Brown, P. M. J., Frost, R. and Poland, R. 2011. Ladybirds (Coccinellidae) of Britain and Ireland: an atlas of the ladybird of Britain, Ireland, the Isle of Man and the Channel Islands. FSC Publications, Shrewsbury, England, UK. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglasova, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Sadler, J. P., Bell, D. and Fowles, A. 2004. The hydroecological controls and conservation value of beetles on exposed riverine sediments in England and Wales. Biol. Conserv. 118: 41-56.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 45-46
Ecological effects of the invasive coccinellid Harmonia axyridis in East Anglia, UK
Rachel A. Farrow1*, Helen E. Roy2 and Peter M. J. Brown1 1Applied Ecology Research Group, School of Life Sciences, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, UK; 2Centre for Ecology and Hydrology, Maclean Building, Crowmarsh Gifford, Wallingford OX10 8BB, UK *Corresponding author: [email protected]
Extended abstract: The invasive non-native species Harmonia axyridis (Coleoptera: Coccinellidae) has been present in the UK since 2004 (Brown et al., 2008). In the UK, Brown et al. (2011) found that H. axyridis was the only species to increase in number over a three- year period while C. septempunctata and A. bipunctata were initially abundant but decreased in the two proceeding years while P. quattuordecimpunctata decreased in number over three years following the arrival of H. axyridis. However, after continued surveying and fresh analysis of the increased data set Brown and Roy (2017) reported a decrease in A. bipunctata only. Whilst distribution of H. axyridis is well known in the UK within urban and other anthropogenic habitats, much less is known on its detailed habitat use in the wider countryside (Brown et al., 2011). The field data presented here came from rural woodland habitats in an effort to determine whether or not H. axyridis dominates coccinellid communities in such habitats. Additionally, the relationship between coccinellid numbers and aphid numbers was explored. All field sites were in Cambridgeshire, Suffolk or Lincolnshire, East Anglia, UK. Three deciduous sites and three coniferous sites were included. As urban areas have previously been shown to have high numbers of the invasive alien species, H. axyridis, two urban sites were included to enable meaningful comparison with the rural sites. Sweep-netting was carried out on the grass margins and beating was used to collect ladybirds from trees. All captured coccinellids were identified to species level. In order to standardise data collection, sampling took place between 10:00 and 16:00h, when the temperature was greater than 14 °C, weather conditions were dry and wind speeds were below 5 on the Beaufort scale (Met Office, 2010). Eighteen species of coccinellid and over 2,200 individuals were recorded during the study period from three distinct site types (deciduous, coniferous, urban). Species richness was lower at urban sites (n = 10) than deciduous (n = 12) and coniferous (n = 16) sites and 58% of all coccinellids recorded were at rural sites. Harmonia axyridis was recorded in significantly greater numbers in urban areas than rural areas, however, abundance of native ladybirds did not differ significantly between urban and rural sites. Harmonia axyridis seems to prefer habitats altered by human activity and it has been suggested that some native coccinellids tend to be more abundant in more rural habitats with less anthropogenic disturbance (Roy et al., 2016). These findings indicate this to be likely, with H. axyridis being less prolific in rural woodlands and appearing not to dominate the coccinellid community as it does in urban areas. Furthermore, deciduous woodland appears to be a lesser preferred habitat of H. axyridis than coniferous woodland but further investigation in why this is the case is necessary. Analysis on these data using GIS software, will investigate how land-use adjacent to survey sites may have an effect on coccinellid abundance and assemblage. Additional analysis into coccinellid assemblage in rural areas will reveal more in-depth knowledge of the relationship between H. axyridis and native coccinellids.
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References
Brown, P. M. J., Roy, H. E., Rothery, P., Roy, D. B., Ware, R. L. and Majerus, M. E. N. 2008. Harmonia axyridis in Great Britain: analysis of the spread and distribution of a non- native coccinellid. In: From biological control to invasion: the ladybird Harmonia axyridis as a model species (eds. Roy, H. and Wajnberg, E.): 55-67. Brown, P. M. J., Frost, R., Doberski, J., Sparks, T., Harrington, R. and Roy, H. E. 2011. Decline in native ladybirds in response to the arrival of Harmonia axyridis: early evidence from England. Ecol. Entomol. 36: 231-240. Brown, P. M. J. and Roy, H. E. 2017. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv. Divers. 11(3), doi:10.1111/icad.12266. Met Office 2010. Beaufort: National Meteorological Library and Archive Fact sheet 6 – The Beaufort scale. Met Office, Exeter, United Kingdom. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E.W., Facon, B., Gardiner, M. M., Gil, A., Grez, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglasova, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 47-49
Composition and functional traits of coccinellids in greenspaces vary with landscape urbanization
Audrey A. Grez1*, Tania Zaviezo2, M. M. Gardiner3 and A. Alaniz1 1Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Casilla 2-15, La Granja, Santiago, Chile; 2Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Santiago, Chile; 3Department of Entomology, Ohio State University, Wooster, Ohio, USA *Corresponding author: [email protected]
Extended abstract: Greenspaces within urban and suburban areas provide many ecosystem services and may be of great value for biodiversity conservation (Goddard et al., 2010). Usually, urbanization leads to a decline in native species abundance and richness. Nevertheless, responses might also depend on trait-based local habitat and landscape-scale filters. Species trophic level, dietary breath, body size, dispersal capacity, and/or habitat specialization influence species occurrence within an urban greenspace and can be mediated by landscape characteristics like composition and heterogeneity (Delgado de la Flor et al., 2017). Rich communities of ladybirds (Coleoptera: Coccinellidae), including native and alien species, occur in urban greenspaces (Egerer et al., 2017; 2018). In Chile, most coccinellid species are concentrated in the central part of the country, a region considered a “hotspot” for biodiversity (Alaniz et al., 2018), and where Santiago, the capital city, is located. In this work, we studied how local characteristics of greenspaces and landscape context at 1000 m influence taxonomic and functional traits composition of native and alien coccinellids across an urbanization gradient. In autumn and spring 2016 and 2017, we sampled ladybirds using five unbaited yellow sticky traps, deployed for four weeks in 82 greenspaces (i. e., city parks and gardens) that varied from 2% to 98% urbanization of the surrounding landscape (1000 m radius). Coccinellids were counted and classified by origin (native or alien), primary diet (e. g., aphids, scales, mildew fungi, white flies or mites) and body size, estimating with the latter the community-weighted mean size. Additionally, habitat specialization for each species was calculated following Grez et al. (2013), with data from coccinellids surveyed in 10 replicate sites of the nine most common habitats in the region. With this information, taxonomic and functional diversity were calculated for each greenspace. Landscapes surrounding greenspaces were characterized using Google Earth satellite images (e. g., Worldview, Geoeye, Ikonos, and Spot 5), estimating Shannon diversity index and the area of different cover types, and also calculating configurational variables. Local characterization of greenspaces was also done, estimating several vegetation variables and aphid abundance. In total, we found 3,337 individuals and 23 species in the greenspaces, including native and endemic species, which account for 43% of the total species described for this region (González, 2017). These species varied in body size (from 1 mm to 7.3 mm), habitat specialization and primary diet. Abundance and richness of native coccinellids were negatively affected by landscape urbanization and positively associated with landscape diversity and the proportion of agricultural area. Aliens were not strongly affected by landscape variables. Coccinellids responded differentially according to their diet. In greenspaces, fungivorous species were associated with larger proportion of agricultural areas, acariphagous species with larger proportion of bare ground and irregular patches in the
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landscape, while aleyrophagous species were associated with urban landscapes. Larger coccinellids dominated in greenspaces in rural landscapes, and smaller in urban landscapes. Contrary to expected, habitat specialists dominated in greenspaces in urban landscapes, and generalists in rural landscapes. Local characteristics of greenspaces were not important predictors of coccinellid richness, abundance or functional traits. Our results show that greenspaces across the Great Santiago support a rich community of coccinellids, including many native species, with different functions, representing an opportunity to conserve these important insects and the ecological services they provide. Nevertheless, the degree to which greenspaces conserve coccinellid communities is strongly dependent on the characteristics of the surrounding landscape. In particular, urbanization has a negative effect on coccinellid abundance and richness in greenspaces, especially natives, while agricultural covers favor them. Other studies also have found that urbanization negatively affects the abundance of coccinellids and other predators (Egerer et al., 2018; Rocha et al., 2018). Landscape composition and configuration also affect the distribution of functional traits of coccinellid communities in greenspaces, depending on body size, habitat specialization and feeding habits. Therefore, surrounding landscape filters coccinellids composition and functional trait distributions in greenspaces, something that should be considered when designing management strategies to conserve coccinellids and the services they provide in urban and rural environments.
Acknowledgements
This work was funded by FONDECYT 1140662 and 1180533. A full paper with the data is in review in Urban Forestry & Urban Greening.
References
Alaniz, A. J., Grez, A. A. and Zaviezo, T. 2018. Potential spatial interaction of the invasive species Harmonia axyridis (Pallas) with native and endemic coccinellids. J. Appl. Entomol. 142: 513-524. Delgado de la Flor, Y. A., Burkman, C. E., Eldredge, T. K. and Gardiner, M. M. 2017. Patch and landscape-scale variables influence the taxonomic and functional composition of beetles in urban greenspaces. Ecosphere 8: e02007. Egerer, M. H., Bichier, P. and Philpott, S. M. 2017. Landscape and local habitat correlates of lady beetle abundance and species richness in urban agriculture. Ann. Entomol. Soc. Am. 110: 97-103. Egerer, M., Li, K. and Ong, T. W. Y. 2018. Context matters: Contrasting ladybird beetle responses to urban environments across two US regions. Sustainability 10(6), doi:10.3390/su10061829. Goddard, M. A., Dougill, A. J. and Benton, T. G. 2010. Scaling up from gardens: biodiversity conservation in urban environments. Trends Ecol. Evol. 25: 90-98. González, G. 2017. Lista actualizada de especies de Coccinellidae (Insecta: Coleoptera) presentes en Chile. [WWW document] www.coccinellidae.cl. Cited 30 Apr. 2019. Grez, A. A., Rand, T. A., Zaviezo, T. and Castillo-Serey, F. 2013. Land use intensification differentially benefits alien over native predators in agricultural landscape mosaics. Divers. Distrib. 19: 749-759. 49
Rocha, E. A., Souza, E. N. F., Bleakley, L. A. D., Burley, C., Mott, J. L., Rue-Glutting, G. and Fellowes, M. D. E. 2018. Influence of urbanisation and plants on the diversity and abundance of aphids and their ladybird and hoverfly predators in domestic gardens. Eur. J. Entomol. 115: 140-149.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 50-52
Field and laboratory evidence of mechanisms explaining the dominance of Harmonia axyridis (Pallas) in alfalfa in Chile
Audrey A. Grez1*, Tania Zaviezo2, Antonio O. Soares3, Violeta Romero1 and Carlos González1 1Facultad de Ciencias Veterinarias y Pecuarias, Universidad de Chile, Casilla 2-15, La Granja, Santiago, Chile; 2Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, Casilla 306-22, Santiago, Chile; 3cE3c – ABG – Centre for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal *Corresponding author: [email protected]
Extended abstract: Harmonia axyridis Pallas is native to Asia, and it was introduced to many regions of the world for biological control of aphids. Then, an invasive strain was generated in eastern North America and this expanded to almost all continents, including Chile where it has rapidly spread along the country (Lombaert et al., 2014; Roy et al., 2016). One of the main negative consequences of the arrival of H. axyridis in these parts of the world has been the decline of native species (Roy et al., 2012; Brown and Roy, 2018). In alfalfa fields in Central Chile, coccinellids assemblages used to be very diverse and dominated by native species, which accounted for most of aphid predation (Ximenez-Embun et al., 2014). But, after the invasion of H. axyridis, coccinellids declined in abundance and diversity, possibly due to antagonistic interactions (Grez et al., 2016). Harmonia axyridis today dominates coccinellid assemblages in alfalfa fields. As possible mechanisms explaining the success of this species in Chile, we studied intraguild predation (IGP), interspecific competition and the scape from parasitism in the most common coccinellids in this crop: the native Eriopis chilensis Hofmann and the aliens H. axyridis and Hippodamia variegata (Goeze) (Figure 1). IGP was studied both in the laboratory and in the field. In the laboratory, we exposed adults of each coccinellid species to eggs of the other two species separately and counted the number of eggs predated. In the field, we used sentinel eggs of the three species glued to transparent cards and observed the number of cards with predation. Also, in the field we collected adults and evaluated IGP through molecular gut content analyses (Singleplex PCR for COI). Interspecific competition was studied in the laboratory. The daily per capita voracity and the proportional weight gain of coccinellid species were estimated when individuals were alone or in conspecific and heterospecific groups of three individuals, under a limited amount of aphids. To determine whether H. axyridis was less susceptible to parasitism by Dinocampus coccinellae (Schrank) compared to the other two species, we collected at least 100 individuals from each species from different alfalfa fields, kept them for 35 days until the appearance of the parasitoid pupa or dissected them to detect larvae inside their bodies. To determine oviposition in the laboratory, all three species were exposed to the parasitoid for 1 hour, and then dissected to detect eggs.
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ESCAPE FROM PARASITISM BY DINOCAMPUS COCCINELLAE
Hippodamia Harmonia Eriopis variegata axyridis chilensis
IGP COMPETITION
Figure 1. Interspecific interactions as possible mechanisms explaining the successful invasion of H. axyridis and the decline of other coccinellids.
Experiments with sentinel eggs showed that E. chilensis and H. variegata were more predated than H. axyridis. Molecular gut content analysis indicated that H. axyridis was the most frequent intraguild predator, and most of its predation was on E. chilensis. In the laboratory, H. axyridis was twice as voracious and gained more weight than the other two species. Finally, successful parasitism by D. coccinellae in the field was lower in H. axyridis. In the laboratory., there was no oviposition by D. coccinellae in H. axyridis, while it reached ~ 40% in the other two species. IGP, voracity and weight gain results suggest that H. axyridis is a superior competitor than the other two species. These interactions, along with the escape from parasitism, may explain the success of this invasive species in Central Chile and the decline of other coccinellids. Furthermore, the positive relation between native coccinellids and biological control observed prior to the arrival of H. axyridis could be disrupted by this invasion.
Acknowledgements
We thank FONDECYT 1140662 and 1180533 for supporting this study.
References
Brown, P. M. J. and Roy, H. E. 2018. Native ladybird decline caused by the invasive harlequin ladybird Harmonia axyridis: evidence from a long-term field study. Insect Conserv. Diver. 11: 230-239. 52
Grez, A. A., Zaviezo, T., Roy, H., Brown, P. M. J. and Bizama, G. 2016. Rapid spread of Harmonia axyridis in Chile and its effects on ladybeetle biodiversity. Divers. Distrib. 22: 982-994. Lombaert, E., Estoup, A., Facon, B., Joubard, B., Grégoire, J.-C., Jannin, A., Blin, A. and Guillemaud, T. 2014. Rapid increase in dispersal during range expansion in the invasive ladybird Harmonia axyridis. J. Evol. Biol. 27: 508-517. Roy, H. E., Adriaens, T., Isaac, N. J. B., Kenis, M., Onkelinx, T., Martin, G. S., Brown, P. M. J., Hautier, L., Poland, R., Roy, D. B., Comont, R., Eschen, R., Frost, R., Zindel, R., van Vlaenderen, J., Nedvěd, O., Ravn, H. P., Gregoire, J. C., de Biseau, J. C. and Maes, D. 2012. Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18: 717-725. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Handley, L. L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M. G., Sloggett, T. T., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglasova, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. H. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Ximenez-Embun, M. G., Zaviezo, T. and Grez, A. A. 2014. Seasonal, spatial and diel partitioning of Acyrthosiphon pisum (Hemiptera: Aphididae) predators and predation in alfalfa fields. Biol. Control 69: 1-7.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 53-55
Hesperomyces “harmoniae” nom. prov. (Laboulbeniales), an ectoparasitic fungus specific to Harmonia axyridis
Danny Haelewaters1,2,3 1Farlow Reference Library and Herbarium of Cryptogamic Botany, Harvard University, 22 Divinity Avenue, Cambridge, Massachusetts 02138, USA; 2Faculty of Science, University of South Bohemia, Branišovská 1760, 370 05 České Budějovice, Czech Republic; 3Current address: Department of Botany and Plant Pathology, Purdue University, 915 West State Street, West Lafayette, Indiana 47907, USA E-mail: [email protected]
Extended abstract: Many fungal species have been described based on morphology alone. Hesperomyces virescens (Ascomycota: Laboulbeniales) is no exception. This is a microscopic ectoparasite of ladybirds (Coleoptera: Coccinellidae); it has been considered a species with a wide host range and geographic distribution spanning all continents except Antarctica. Since its description in the 19th century (Thaxter, 1891), H. virescens has been found on 30 ladybird species, in 20 genera and 5 subfamilies (Haelewaters and de Kesel, 2017). However, species hypotheses for microscopic organisms should be treated with caution (Pringle et al., 2005). Many fungi form associations with other organisms, meaning that they may be circumscribed based on these associations. We hypothesized that H. virescens in reality is a complex consisting of many different species, each adapted to individual host species. DNA was isolated from H. virescens fruitbodies originating from different host species. Next, we amplified nuclear small and large ribosomal subunits (SSU and LSU) and the internal transcribed spacer region of the ribosomal DNA (ITS). Based on generated sequence data, distinct phylogenetic clades within H. virescens were found, each clade consisting of isolates from a single host species (Table 1). The only exception was the clade consisting of isolates from two species of Adalia (A. bipunctata and A. decempunctata). Several species delimitation methods confirm that these lineages represent separate species (details in Haelewaters et al., 2018). What follows is that H. virescens is not a fungus with wide host range but instead a complex of multiple species, each with strict host specificity, apparently limited to the genus level. After the publication of Haelewaters et al. (2018), we were fortunate to have been provided with Hesperomyces-infected individuals of Chilocorus stigma. This ladybird is the original host species from which the type of H. virescens was described by Thaxter (1891). If H. virescens is indeed a species complex, then a distinction must be made between H. virescens sensu lato (the complex of species) and H. virescens sensu stricto. We can only start to describe the different species in the complex when we exactly know what is H. virescens s.s. Our new material of C. stigma allowed us to elaborate on our previous phylogenetic results. We found that the isolates removed from C. stigma form a clade separate from the other previously circumscribed clades. We know now that this clade represents H. virescens s.s. and we can start the process of formally naming the other clades in the complex. Harmonia axyridis is an invasive alien species listed as ‘one of the worst’ in Europe (DAISIE, 2017). It was introduced as a biocontrol agent in several countries but also arrived unintentionally in many other countries (Roy et al., 2016; Camacho-Cervantes et al., 2017). Harmonia axyridis is often reported as host to H. virescens (see Haelewaters et al., 2019
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elsewhere in this Bulletin). Based on our molecular phylogenetic work and sequence-based species delimitation analyses, Hesperomyces isolates from different populations of H. axyridis form a separate species, regardless of geographic origin. This species will be formally described in a future publication as Hesperomyces harmoniae nom. prov.
Table 1. Overview of host species from which H. virescens fruitbodies were removed for DNA isolation and subsequent molecular work.
Host species Country Adalia bipunctata Denmark, Italy, Sweden Adalia decempunctata Italy Azya orbigera Panama Cheilomenes propinqua South Africa Chilocorus stigma USA Cycloneda sanguinea Panama Halyzia sedecimguttata Netherlands Harmonia axyridis Germany, Japan, Netherlands, South Africa, USA Olla v-nigrum USA Psyllobora vigintimaculata USA
Interestingly, Hesperomyces-infected populations of H. axyridis overlap with Olla v-nigrum in the USA (Riddick and Cottrell, 2010), and with Cheilomenes propinqua in South Africa (Haelewaters et al., 2016). Nonetheless, isolates of Hesperomyces removed from these ladybirds are retrieved in distinct clades, always segregated by host species. Hesperomyces harmoniae nom. prov. causes mortality of H. axyridis in laboratory conditions (D. Haelewaters et al., unpublished data) and does not seem to transmit to other ladybirds (Cottrell and Riddick, 2012). This combination of molecular phylogenetic and experimental work has important implications in the potential use of H. harmoniae nom. prov. as a biological control against H. axyridis.
Acknowledgements
This work was supported by the following funding sources: David Rockefeller Center for Latin American Studies, Smithsonian Tropical Research Institute, Torrey Botanical Society. Panama’s Secretaria Nacional de Ciencia, Tecnología e Innovacion (SENACYT). We thank Mr. Arthur Grupe (University of Florida-Gainesville) for looking for and providing us with infected C. stigma ladybirds.
References
Camacho-Cervantes, M., Ortega-Iturriaga, A. and del Val, E. 2017. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ 5: e3296. 55
Cottrell, T. E. and Riddick, E. W. 2012. Limited transmission of the ectoparasitic fungus Hesperomyces virescens between ladybeetles. Psyche 2012, doi: 10.1155/2012/814378. DAISIE (Delivering Alien Invasive Species Inventories for Europe) 2017. Harmonia axyridis. [WWW document] http://www.europe-aliens.org/pdf/Harmonia_axyridis.pdf. Cited 1 May 2019. Haelewaters, D., Minnaar, I. A. and Clusella-Trullas, S. 2016. First finding of the parasitic fungus Hesperomyces virescens (Laboulbeniales) on native and invasive ladybirds (Coleoptera, Coccinellidae) in South Africa. Parasite 23: 5, doi:10.1051/ parasite/2016005. Haelewaters, D. and de Kesel, A. 2017. De schimmel Hesperomyces virescens, een natuurlijke vijand van lieveheersbeestjes. Entomol. Ber. 77: 106-118. Haelewaters, D., de Kesel, A. and Pfister, D. H. 2018. Integrative taxonomy reveals hidden species within a common fungal parasite of ladybirds. Sci. Rep. 8: 15966. Haelewaters, D., Pan, F. Y. and Pan, J. Y. 2019. Tracking an ectoparasitic fungus of Harmonia axyridis in North America using literature records and citizen science data. IOBC-WPRS Bull. 145: 17-22. Pringle, A., Baker, D. M., Platt, J. L., Wares, J. P., Latgé, J. P. and Taylor, J. W. 2005. Cryptic speciation in the cosmopolitan and clonal human pathogenic fungus Aspergillus fumigatus. Evolution 59: 1886-1899. Riddick, E. W. and Cottrell, T. E. 2010. Is the prevalence and intensity of the ectoparasitic fungus Hesperomyces virescens related to the abundance of entomophagous coccinellids? Bull. Insectol. 63: 71-78. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A.G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A.O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016: The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Thaxter, R. 1891. Supplementary note on North American Laboulbeniaceae. Proc. Am. Acad. Arts Sci. 25: 261-270.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 56-58
Field investigations of the invasive leaf beetle pest Paropsisterna selmani (Chrysomelidae) and laboratory-based evaluation of the parasitoid wasp Enoggera nassaui as a biological control agent
Dorothy Hayden1,2*, John Finn2 and Jan-Robert Baars1 1University College Dublin, Belfield, Dublin, Ireland; 2Teagasc, Johnstown Castle, Wexford, Ireland *Corresponding author: [email protected]
Extended abstract: The Eucalyptus leaf beetle pest, Paropsisterna selmani Reid and de Little (Chrysomelidae: Paropsini) was accidentally introduced into Ireland from Australasia and seriously threatens national commercial Eucalyptus plantations in Ireland (Horgan, 2011; Hayden et al., 2013). As the first paropsine leaf beetle to become established in Europe (Fanning and Baars, 2014), this species was initially discovered damaging foliage crops in south west Ireland in 2007 (Horgan, 2011). It was subsequently found causing severe defoliation to a number of species of Eucalyptus in Surrey, UK in 2015 (Malumphy and Redstone, 2015). In the absence of natural enemies, insecticidal control is frequently chosen by growers to avert losses, disrupting the already established biological control agent of another Eucalyptus pest Ctenarytaina eucalypti (Maskell) (Hemiptera: Aphalaridae) (Hayden et al., 2014). The parasitoid wasp, Enoggera nassaui “Girault” (Hymenoptera: Pteromalidae), which has been used as a biocontrol agent of a similar leaf beetle in New Zealand (Kay, 1990; Murray et al., 2008), was imported into the quarantine insectary of University College Dublin (UCD) for further study. Classical biological control potentially offers a cost-efficient and sustainable solution to reducing the damaging effects of this defoliator. Pre-release testing of this biological control agent is required to ensure its effectiveness and host specificity. The use of biocontrol agents for the control of phytophagous pests has a proven track record of success and safety in Eucalyptus producing areas of the world (Wingfield et al., 2013). This study aimed, for the first time, to quantify the threat to commercial Eucalyptus forestry from P. selmani and to investigate the phenology of this invasive beetle in cut foliage plantations in order to establish whether its activity on the foliage synchronised with that of the egg parasitoid, E. nassaui. Observations were made during 4 growing seasons in a young E. nitens forestry plantation to investigate the capacity of the beetle to establish and the way it manifests within the plantation and the subsequent impact on flush foliage. Coinciding with a switch from juvenile to adult foliage, the beetle established throughout the plantation causing significant damage to foliage throughout the plantation. The level of damage increased significantly each year between 2012 and 2014 and was recorded at 37% canopy loss in 2015. The rapidity of colonisation of the study site to utilize available resources reflects the threat that this defoliator presents to the industry. A novel aspect of this investigation is that a correlation was found between damage levels and relative growth rate (RGR). For the first time, phenology studies indicated that adults emerge in early summer (April to May), with 2 generations per year, exhibiting 3 peaks of abundance of adults and larvae, quickly followed by deaths of overwintered and 1st generation adults, with the 2nd generation entering diapause in autumn without any evidence of egg laying. This demonstrates that there are 2 periods when beetle eggs are unavailable, the first for 4 weeks from mid-June to mid-July, when they are only available for just over a month, and unavailable again from the latter part
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of August until the following April. This may present challenges to the wasp, and it is unknown how the wasp will bridge these gaps and whether it will affect the parasitoid’s ability to establish in Irish plantations. Prior to this study, it was known that there were different beetle cohorts during the growing season, but it was not known that there were periods of egg unavailability. The monitoring of the foliage plantation also indicated that over 50% of the E. parvula foliage was consumed by the beetle and significant levels of disbudding occurred. Enoggera nassaui was investigated to determine how it performed on the target pest and to establish the development relative to temperature in order to predict its potential to establish in the Irish climate and areas in Europe where the wasp might establish. Laboratory cultures demonstrated that the parasitoid does develop on the eggs of P. selmani and that it possesses positive life history traits with high fecundity, eggs laid throughout life at moderate temperatures, relatively long adult life, and high larva-to-adult survival rates. For the first time, the viability of the wasp was estimated between May to September, the most likely period of host availability. Life table results predict that it can sustain itself when three or more generations are produced in this period. The predictive models indicate that E. nassaui can produce at least seven generations at this time in Ireland and many more at most locations in Europe. Taking into consideration the projected generational turnover, and the predicted net reproductive rate (Ro) values for these locations, a permanent population is expected to establish in all but a few regions of Europe, assuming host availability. The wasp was exposed to 22 native coleopteran species to determine the risk of parasitoidism of non-target native species. The species selected included the blue willow beetle, Phratora vulgatissima (Linnaeus, 1758), and green dock beetle, Gastrophysa viridula De Geer, 1775, on the basis of belonging to the same subfamily as the target pest and with similar egg morphology, whereas others such as the eyed ladybird, Anatis ocellata (Linnaeus, 1758), and 7-spot ladybird, Coccinella septempunctata Linnaeus, 1758, were chosen due to their larger size and likely sharing the same habitat as the pest. Using no-choice and choice laboratory trials, there is no predicted threat to non-target species. Observations conducted showed the wasp had no significant interest in the eggs of native Chrysomelidae and Coccinellidae. A comparison of hatch rates between exposed and non-exposed eggs of the native beetle species in both choice and no-choice tests showed no significant differences, with the exception of one species in choice trials, the eggs of which were not inspected or oviposited by the wasp during the observational periods, and is suspected to be a false positive. Significantly, no parasitoid development took place in any of the native species eggs tested. This novel finding, together with observed lack of interest in native species eggs in small testing arenas, where maximum host range is likely to be expressed (Withers and Brown, 2004), suggests that non-target species are unlikely to be utilized as hosts in the field. This suggests that the parasitoid is highly specific and potentially a safe candidate biocontrol agent. In the event of a successful release application, E. nassaui is expected to be of immediate economic benefit to the Eucalyptus forestry sector, provided predicted efficacy, spread, and establishment occurs in the field. Commercial management operations in cut foliage and biomass plantations, which could impact parasitoid survival are explored to highlight aspects requiring further research. While there are many challenges facing cut foliage producers, given the requirement for blemish free produce, the introduction of 2 additional psyllid pests (Hodkinson, 2007), further complicates the pest complex. This highlights the need for biocontrol research in Ireland to facilitate successful integrated pest management and an ecological approach to pest control on Eucalyptus crops.
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Acknowledgements
This research was supported by a Walsh Fellowship from Teagasc – The Agriculture and Food Development Authority, Ireland.
References
Fanning, P. and Baars, J.-R. 2014. Biology of the Eucalyptus leaf beetle Paropsisterna selmani (Chrysomelidae: Paropsini): a new pest of Eucalyptus species (Myrtaceae) in Ireland. Agr. Forest Entomol. 16: 45-53. Hayden, D., Whelton, A., Stout, J., Finn, J. and Baars, J.-R. 2013. Biodiversity and integrated pest management of foliage and forestry plantations. In: Ireland's Rural Environment. Research Highlights from Johnstown Castle (eds. Ó hUallacháin, D., Fenton, O. and Foley, M.): 63-64. Teagasc/NDP, Ireland. Hayden, D., Finn, J. and Baars, J.-R. 2014. Beetle threat to horticultural Eucalyptus crops in Ireland. TResearch 9(2): 9. Hodkinson, I. D. 2007. A new introduced species of Ctenarytaina (Hemiptera, Psylloidea) damaging cultivated Eucalyptus parvula (= parvifolia) in Europe. Deut. Entomol. Z. 54: 27-33. Horgan, F. G. 2011. Outbreak of an invasive paropsine beetle in south-west Ireland: Preference, performance and damage to Eucalyptus. J. Appl. Entomol. 135: 621-633. Kay, M. K. 1990. Success with biological control of the eucalyptus tortoise beetle, Paropsis charybdis. What's New Forest Res. 184: 4. Malumphy, C. and Redstone, S. 2015. First incursion of Tasmanian Eucalyptus beetle Paropsisterna selmani in Britain, with a review of Paropsisterna species recorded in Britain (Coleoptera: Chrysomelidae). Brit. J. Entomol. Nat. Hist. 28: 205-212. Murray, T. J., Mansfield, S. and Withers, T. M. 2008. Comparing the behavioural strategies of two parasitoid wasps: is aggressive resource defending good for biological control? In: Proceedings of ISBCA 3 (eds. Mason, G., Gillespie, D. R. and Vincent, C.): 416-420. Withers, T. M. and Browne, L. B. 2004. Behavioral and Physiological Processes Affecting Outcomes of Host Range Testing. In: Assessing host ranges for parasitoids and predators used for classical Biological control: A guide to best practice (eds. van Driesche, R. G. and Reardon, R.): 40-55. Forest Health Technology Team, United States Department of Agriculture & Forest Service, Morgantown, West Virginia, USA. Wingfield, M. J., Roux, J., Slippers, B., Hurley, B. P., Garnas, J., Myburg, A. A. and Wingfield, B. D. 2013. Established and new technologies reduce increasing pest and pathogen threats to Eucalypt plantations. Forest Ecol. Manag. 301: 35-42.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 59-61
Does Harmonia axyridis (Coccinellidae) suppress native ladybirds?
Pavel Kindlmann1,2* and Zuzana Štípková1,2 1Global Change Research Institute, Bělidla 986/4a, 60300 Brno, Czech Republic; 2Institute for Environmental Studies, Faculty of Science, Charles University, Benátská 2, 12801 Prague, Czech Republic *Corresponding author: [email protected]
Extended abstract: The efficacy of biocontrol agents in aphid – ladybird systems is an important issue to determine the success of biological control. Therefore, it has been subject to ample discussion as well as empirical studies, which have attempted to evaluate to which extent predators are able to suppress their aphid prey. A very interesting case occurs, when a guild of native ladybirds is invaded by an alien species. Because of strong cannibalism among ladybirds, the numbers of natives may be diminished by the invader, which lowers the biocontrol potential of the former. However, the new invader also eats aphids, by which it increases the biocontrol efficiency of the ladybird guild here. The question then is what prevails: is the final biocontrol efficiency larger or lower after the invasion, compared to the situation prior to the invasion? The situation is illustrated in Figure 1.
Figure 1. Illustration of the situation when a native ladybird guild is invaded by an alien ladybird.
A nice example is the pan-European invasion of Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), as recently observed in many countries (Roy et al., 2016). It is tempting to state that the invader reduces numbers of native ladybirds and therefore lowers the biocontrol potential of the whole guild in this case (Brown et al., 2011; Roy et al., 2012). However, do
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we really have sufficient data to prove this? We express the fear that in many cases, in attempts to prove this reduction of biocontrol potential, the statistical analyses are insufficient and not correct. Here we raise a series of concerns and warn against improper use of statistics and overemphasis of seemingly persuasive data in this respect. In this extended abstract, we give only an account of individual points. Their full analysis, together with examples of lack or misuse of statistics, will be published elsewhere. We propose that for proper proof of the influence of the invading H. axyridis on local ladybird species, the following items must be satisfied: o The duration of the time series used for the analysis must be sufficiently long. This sufficiency must be checked by proper statistical tests of the numbers of individuals of native ladybirds before and after the invasion (e. g., t test). o The decline of percentage abundance of the native species after the invasion is not a sign of the negative effect of the invader on numbers of local species. It is straightforward that the percentage of abundance of the native species must decline, when a new species is added to the system and total percentage remains 100. o Sometimes, a declining trend in numbers of individuals of local species is presented as a ‘proof’ of negative effect of H. axyridis on abundance of local species. Again, a statistical test of whether this decline is significant must accompany such conclusions. o In addition, one has to keep in mind that correlation does not necessarily mean causation. In other words, a decline in abundances of local species may be a consequence of other factors than invasion of H. axyridis – the real reason may be, e.g., decline of acreage of the host habitat, climate change, or other phenomena. o If intraguild predation (IGP) is assumed to be the reason for decline of native species abundance, then IGP must be common in the system – but is it? Proofs of this are often missing and many data indicate that due to relatively low percentage of aphid colonies attacked by ladybirds, the likelihood of a native species individual meeting an invader is very low and therefore IGP is virtually non-existent, at least in herbs (Kindlmann and Houdkova, 2006). This casts doubts on whether H. axyridis is able to suppress the native ladybird species after its invasion.
When thinking of the resulting effect of the ladybird guild on the aphids before and after invasion, another question appears and is discussed here: how much are ladybirds able to suppress the abundance of aphids in the field? We show examples that the original idea of a large efficiency of ladybirds in controlling aphids (e. g., Schmidt et al., 2003) should be reconsidered (Kindlmann et al., 2015). If the biocontrol potential of the ladybird guild will be shown to be low, then the discussion on whether it will increase or decline after the invasion becomes irrelevant. We conclude that, still, a lot of empirical data must be collected before these interesting questions about the dynamics of the ladybird guild–aphid systems before and after the invasion of an alien species will be finally resolved. It is evident that Harmonia axyridis is now spreading all over Europe. However, the question whether this will affect the biocontrol potential of the whole ladybird guild in the countries invaded remains unanswered.
Acknowledgements
This project was supported by the grant no. 17-06763S of the Grant Agency of the Czech Republic. 61
References
Brown, P. M. J., Frost, R., Doberski, J., Sparks, T., Harrington, R. and Roy, H. E. 2011. Decline in native ladybirds in response to the arrival of Harmonia axyridis: Early evidence from England. Ecol. Entomol. 36: 231-240. Kindlmann, P. and Houdkova, K. 2006. Intraguild predation: fiction or reality? Popul. Ecol. 48: 317-322. Kindlmann, P., Yasuda, H., Kajita, Y., Sato, S. and Dixon, A. F. G. 2015. Predator efficiency reconsidered for a ladybird-aphid system. Front. Ecol. Evol., doi:10.3389/fevo.2015. 00027. Roy, H. E., Adriaens, T., Isaac, N. J. B., Kenis, M., Onkelinx, T., Martin, G. S., Brown, P. M. J., Hautier, L., Poland, R., Roy, D. B., Comont, R., Eschen, R., Frost, R., Zindel, R., van Vlaenderen, J., Nedved, O., Ravn, H. P., Gregoire, J. C., de Biseau, J. C. and Maes, D. 2012. Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18: 717-725. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grezz, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Handley, L. L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M. G., Sloggett, T. T., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglasova, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. H. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Schmidt, M. H., Lauer, A., Purtauf, T., Thies, C., Schaefer, M. and Tscharntke, T. 2003. Relative importance of predators and parasitoids for cereal aphid control. Proc. R. Soc. Lond. B 270: 1905-1909.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 62-63
Ecosystem services provided by the native predator Scymnus nubilus Mulsant (Coleoptera: Coccinellidae) against aphids on forestry nurseries
Roberto Meseguer1, Isabel Borges2*, Virgílio Vieira2, Gemma Pons1 and António O. Soares2 1Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal; 2cE3c – ABG – Centre for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Azores, Portugal *Corresponding author: [email protected]
Extended abstract: Considering the potential negative impacts of invasive alien biological control agents (Soares et al., 2008; Roy et al., 2016), it is commendable to search for candidates in the local natural enemy community. In this study, we assessed the potential of Scymnus nubilus Mulsant (Coleoptera: Coccinellidae), an abundant ladybird species in the Azores (Portugal) (Soares et al., 2003; 2006), as a biological control agent of aphid species (Hemiptera: Aphididae) infesting endemic/protected Azorean plants reared in forestry nurseries. Due to certification requirements, chemical pest control is limited and so an alternative is required. In a preliminary visit to the forestry nurseries it was found that aphid infestation was more generalized than initially expected. Aphis frangulae Kaltenbach, A. spiraecola Patch, Cinara juniperi (De Geer), and Toxoptera aurantii (Boyer de Fonscolombe) were the most abundant aphid species and were associated with the host plants Frangula azorica V. Grubow (Rosales: Rhamnaceae), Viburnum treleasei Gand. (Dipsacales: Adoxaceae), Juniperus brevifolia (Seub.) Antoine (Pinales: Cupressaceae), and Ilex perado Aiton subsp. azorica (Loes.) Tutin (Aquifoliales: Aquifoliaceae), respectively. To study aphid abundance patterns, 50 plants of each host plant species were observed and the number of aphids were recorded. Records were made twice a month from March/April to September for two years, 2014 and 2015, in two nurseries in distinct locations, Furnas and Nordeste. Furthermore, to study the aphid colony dynamics, 10 colonies of the selected aphid species were tagged and followed until collapse for determining the colony lifespan. Aphid abundance and colony lifespan was variable among years, nursery location, and aphid species. Aphis spiraecola was the most abundant aphid species (46%) but J. brevifolia was the host plant with a higher proportion of infested plants (~ 30%). Cinara juniperi colonies persisted for longer, approximately 8 weeks on average. The biological performance of S. nubilus was tested in the laboratory on the main aphid pests found in the nurseries. To assess the effect of prey species on the development and adult weight of the predator, the 4th larval stage was fed on single diets of A. frangulae, A. spiraecola, C. juniperi, and T. aurantii. From hatching to the 4th larval stage, the ladybird larvae were fed with A. fabae Scopoli, the aphid available in the laboratory. The 4th larval instar and pupal developmental times were determined, as well as the weight of the adults. To assess the voracity of the predator on the different prey species, the feeding parameters were studied (Borges, 2008; Sebastião et al., 2015). Laboratorial results showed that all aphid species tested allowed S. nubilus 4th instar larvae and pupae to complete development but
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heavier adults were obtained with T. aurantii. Voracity was significantly higher when S. nubilus fed on A. frangulae but more C. juniperi biomass was consumed. After knowing the consumption capacity of the predator, the biological control potential of the ladybird was assessed in field conditions. Three prey colony size levels were established ranging from the food quantity required for one day to the quantity of food required to complete the 4th larval stage development. Additionally, four treatments were defined: i) aphid colony + predator larva (open system), ii) aphid colony + predator larva + sleeve cage (closed system), iii) aphid colony + sleeve cage (closed system), and iv) aphid colony (open system). Field experiments with the aphid species A. spiraecola and C. juniperi indicated that S. nubilus can contribute to the decrease of pest population densities, more significantly in the case of the former. However, these tests also highlighted the role of other natural enemies occurring naturally in the forestry nurseries, such as Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae), syrphids, and aphid parasitoids, such as Aphidius colemani Viereck (Hymenoptera: Braconidae).
References
Borges, I. 2008. Life history evolution in aphidophagous and coccidophagous Coccinellidae (Coleoptera). Ph. D. Thesis, University of the Azores, Ponta Delgada. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A.O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Sebastião, D., Borges, I. and Soares, A. O. 2015. Effect of temperature and prey in the biology of Scymnus subvillosus. BioControl 60: 241-249. Soares, A. O., Elias, R. B., Resendes, R. and Figueiredo, H. 2003. Contribution to the knowledge of the Coccinellidae (Coleoptera) fauna from the Azores islands. Arquipél. Life Mar. Sci. 20A: 47-53. Soares, A. O., Borges, I., Cabral, S., Figueiredo, H. and Resendes, R. 2006. New records of Coccinellidae (Coleoptera) to the Azores islands. Reports and Communications of the Department of Biology. XII Scientific Expedition of the Department of Biology, Pico 2005, 34: 87-91. Soares, A. O., Borges, I., Borges, P. A. V., Labrie, G. and Lucas, É. 2008. Harmonia axyridis: What will stop the invader? Biocontrol 53: 127-145. Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 64-66
Engaging people in surveillance and monitoring of non-native species
Helen E. Roy1*, Peter M. J. Brown2, Marc Botham1 and Steph Rorke1 1Centre for Ecology & Hydrology, Benson Lane, Crowmarsh Gifford, Oxfordshire, OX10 8BB, UK; 2Applied Ecology Research Group, Department of Biology, Anglia Ruskin University, East Road, Cambridge, CB1 1PT, UK *Corresponding author: [email protected]
Extended abstract: People have been contributing their wildlife observations from across the UK for centuries. Simple biological records (what, where, and when a species was seen) can be made by anyone, anywhere. Technological developments such as smart phone apps are increasing the number of people participating in such citizen science initiatives. The information accruing from them is enabling us to track changes in wildlife over time and address many ecological questions including those on non-native species ecology. The Coccinellidae Recording Scheme is one of more than 80 biological recording schemes within the UK. It was established in the early 1970s and launched as an on-line survey in 2005 as the UK Ladybird Survey (Pocock et al., 2015). The Harlequin Ladybird Survey was initiated as part of the UK Ladybird Survey, at that time, in response to the arrival of the non-native species Harmonia axyridis (Coleoptera, Coccinellidae) in the UK. Harmonia axyridis is a charismatic species that has been instrumental in engaging people in non-native species ecology and encouraging public participation in surveillance and monitoring (e. g., Roy et al., 2015; Brown et al., 2018). The success of this citizen science initiative inspired the development of an alert system for non-native species in Britain. The alert system has been widely publicised through the media but also talks and articles particularly in wildlife magazines. There has been a huge response from people across Britain in reporting sightings of concern particularly for one species: the Asian hornet, Vespa velutina (Hymenoptera, Vespidae) (Figure 1). Vespa velutina is thought to have been accidentally introduced into France in 2004 from China, where it is native (Villemant et al., 2006 a; 2006 b). The species has swiftly spread to Spain, Belgium, Portugal, Italy, Germany, and Switzerland (von Orlow, 2014; Meldelaselva, 2017). One photo-observation is known from the Netherlands (Meldelaselva, 2017). The Asian hornet poses an additional threat to already declining populations of the European honeybee, Apis mellifera – V. velutina feeds on A. mellifera and other insects including other pollinators (Arca et al., 2014). Vespa velutina observations in the UK can be submitted through an online recording form at http://www.brc.ac.uk/risc/alert.php?species=asian_hornet and using the Asian Hornet Watch app (for iPhone or android). Although thousands of people have contributed records, there have been very few confirmed sightings of V. velutina in the UK since 2015 (Budge et al., 2017; Keeling et al., 2017; GOV.UK, 2018). Most of the reports are of a close relative the native European hornet Vespa crabro. Science communication and public engagement has been an important component of the alert system not only to encourage reporting (surveillance) but also to raise awareness around invasive non-native species. There is a need to embrace the complexity of such issues and the importance of evidence-based decision-making to underpin societal perspectives.
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Figure 1. Reports to the alert system since 2011. Noting from 2014 most are of suspected Asian hornets V. velutina which are generally confirmed as V. crabro.
Acknowledgements
We are grateful to all contributors of the UK Ladybird Survey. We thank the following organizations for continuous support: Department for Environment Food and Rural Affairs, National Biodiversity Network Trust, Joint Nature Conservation Committee, Natural Environment Research Council, Centre for Ecology & Hydrology, Anglia Ruskin University, and University of Cambridge.
References
Arca, M., Papachristoforou, A., Mougel, F., Rortais, A., Monceau, K., Bonnard, O., Tardy, P., Thiéry, D., Silvain, J. F. and Arnold, G. 2014. Defensive behaviour of Apis mellifera against Vespa velutina in France: testing whether European honeybees can develop an effective collective defence against a new predator. Behav. Processes 106: 122-129. Brown, P. M. J., Roy, D. B., Harrower, C., Dean, H. J., Rorke, S. L. and Roy, H. E. 2018. Spread of a model invasive alien species, the harlequin ladybird Harmonia axyridis in Britain and Ireland. Sci. Data. 5: 180239. Budge, G. E., Hodgetts, J., Jones, E. P., Ostojá-Starzewski, J. C., Hall, J., Tomkies, V., Semmence, N., Brown, M., Wakefield, M., Stainton, K. 2017. The invasion, provenance and diversity of Vespa velutina Lepeletier (Hymenoptera: Vespidae) in Great Britain. Plos One 12: e0185172. GOV.UK. 2018. Asian hornet: UK sightings in 2018. [WWW document] https://www.gov.uk/government/news/asian-hornet-uk-sightings-in-2018. Accessed 8 May 2019. 66
Keeling, M. J., Franklin, D. N., Datta, S., Brown, M. A. and Budge, G. E. 2017. Predicting the spread of the Asian hornet (Vespa velutina) following its incursion into Great Britain. Sci. Rep. 7: 6240. Meldelaselva 2017. Vespa velutina in Europe (2017). [WWW document] https://www. google.com/maps/d/embed?mid=1jRfoi4oF6GmiGRgbXuD71Qpbw8s. Accessed 8 May 2019. Pocock, M. J., Roy, H. E., Preston, C. D. and Roy, D. B. 2015. The Biological Records Centre: a pioneer of citizen science. Biol. J. Linn. Soc. 115: 475-493. Roy, H. E., Rorke, S. L., Beckmann, B., Booy, O., Botham, M. S., Brown, P. M. J., Harrower, C., Noble, D., Sewell, J. and Walker, K. 2015. The contribution of volunteer recorders to our understanding of biological invasions. Biol. J. Linn. Soc. 115: 678-689. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A.O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Villemant, C., Haxaire, J. and Streito, J.-C. 2006 a. Premier bilan de l’invasion de Vespa velutina Lepeletier en France (Hymenoptera, Vespidae). Bull. Soc. entomol. France 111: 535-538. Villemant, C., Haxaire, J. and Streito, J. C. 2006 b. The discovery of the Asian hornet Vespa velutina in France. Insectes 143: 3-7. von Orlow, M. 2014. Blog. 9.9.2014. [WWW document] http://www.hymenoptera.de/ Jahr%202014. Accessed 8 May 2019.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 67-68
Collaborating to map ladybirds across Europe
Helen E. Roy1, Jiří Skuhrovec2, Tim Adriaens3, Peter M. J. Brown4, Alois Honěk2, Alberto F. Inghilesi5, Karolis Kazlauskis1, Oldřich Nedved6,7, Gabriele Rondoni8, David B. Roy1, António O. Soares9 and Sandra Viglasova10 1Centre for Ecology & Hydrology, Oxfordshire, OX10 8BB 2, UK; 2Crop Research Institute, Prague 6, Ruzynĕ, Czech Republic; 3Research Institute for Nature & Forest (INBO), Brussels, Belgium; 4Anglia Ruskin University, Cambridge, CB1 5PT, UK; 5Department of Biology, University of Florence, via Romana 17, 50125 Firenze, Italy University of Perugia, Italy; 6Faculty of Science, University of South Bohemia České Budějovice, Czech Republic; 7Institute of Entomology, Biology Centre, České Budějovice, Czech Republic; 8University of Perugia, Italy; 9cE3c – ABG – Centre for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal; 10Institute of Forest Ecology, Slovak Academy of Sciences, Zvolen, Slovakia *Corresponding author: [email protected]
Extended abstract: Recording of ladybirds by volunteers has a long history in a number of countries in Europe and other continents (Losey et al., 2007; Brown et al., 2008; Sæthre et al., 2010; Gardiner et al., 2012; Grez and Zaviezo, 2015; Pocock et al., 2015; Roy and Brown, 2015; Roy et al., 2015). However, there are inherent spatial, temporal and taxonomic biases within the data collated. Many European countries have not had involvement of volunteers through citizen science in recording. There are opportunities to increase the scope of ladybird recording across Europe. Here we present a new smartphone app for recording conspicuous ladybird across Europe which will ultimately underpin large-scale and long-term analysis of ladybird trends (simulated summer droughts). Through this app, we aim to answer the following questions: (1) How do these changes affect the distribution of species? (2) Is the distribution of ladybird species changing differentially across biogeographic zones? (3) Is there a replacement of key species and functional guilds of native ladybirds?
Acknowledgements
We thank the Biological Records Centre for supporting the development of this app.
References
Brown, P. M. J., Adriaens, T., Bathon, H., Cuppen, J., Goldarazena, A., Hägg, T. Kenis, M., Klausnitzer, B. E. M., Kovář, I., Loomans, A. J. M., Majerus, M. E. N., Nedvěd, O., Pedersen, J., Rabitsch, W., Roy, H. E., Ternois, V., Zakharov, I. A. and Roy, D. B. 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. Biocontrol 53: 5-21. Gardiner, M. M., Allee, L. L., Brown, P. M. J., Losey, J. E., Roy, H. E. and Smyth, R. R. 2012. Lessons from lady beetles: accuracy of monitoring data from US and UK citizen- science programs. Front. Ecol. Environ. 10: 471-476.
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Grez, A. A. and Zaviezo, T. 2015. Chinita arlequín: Harmonia axyridis en Chile. [WWW document] http://www.chinita-arlequin.uchile.cl. Accessed 26 Feb. 2019. Losey, J. E., Perlman, J. E. and Hoebeke, E. R. 2007. Citizen scientist rediscovers rare nine- spotted lady beetle, Coccinella novemnotata, in eastern North America. J. Insect Conserv. 11: 415-417. Pocock, M. J., Roy, H. E., Preston, C. D. and Roy, D. B. 2015. The Biological Records Centre: a pioneer of citizen science. Biol. J. Linn. Soc. 115: 475-493. Roy, H. E. and Brown, P. M. J. 2015. Ten years of invasion: Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Britain. Ecol. Entomol. 40: 336-348. Roy, H. E., Rorke, S. L., Beckmann, B., Booy, O., Botham, M. S., Brown, P. M. J., Harrower, C., Noble, D., Sewell, J. and Walker, K. 2015. The contribution of volunteer recorders to our understanding of biological invasions. Biol. J. Linn. Soc. 115: 678-689. Sæthre, M.-G., Staverløkk, A. and Hofsvang, T. 2010. The history of Harmonia axyridis (Pallas, 1773) in Norway. IOBC-WPRS Bull. 58: 97-104.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 69-70
Structure and dynamics of aphidophagous guilds and aphids in a country on the margin of Harmonia axyridis distribution
Zuzana Štípková1,2* and Pavel Kindlmann1,2 1Global Change Research Institute, Bělidla 986/4a, 60300 Brno, Czech Republic; 2Institute for Environmental Studies, Faculty of Science, Charles University, Benátská 2, 12801 Prague, Czech Republic *Corresponding author: [email protected]
Extended abstract: Invasive alien species belong to the major drivers of biodiversity loss (Hilton-Taylor, 2000). The harlequin ladybird (Harmonia axyridis) is an invasive alien species, which has probably escaped from glasshouses in the Netherlands, the country of its initial wild occurrence in Europe, and is now quickly spreading all across Europe (Brown et al., 2011; Roy et al., 2012). During the last decades, its distribution was reported from some countries very far from the place of its initial spread like Ukraine, Turkey or Georgia (Roy et al., 2016). It is therefore interesting to see the distribution and dynamics of aphidophagous guilds and aphids in these “distant” countries. Here we present results of a pilot study performed at one site in Greece as an example of a destination at the margin of H. axyridis distribution, where this species is still absent or is present only in small numbers. We looked at the structure and dynamics of aphidophagous guilds and aphids here, with a special focus on the dynamics and distribution of H. axyridis. We monitored 50 aphid colonies in 2017 and another 50 colonies in 2018. The monitoring was performed twice a week during the whole season. We observed frequent fluctuations in aphid population dynamics: both natural and human-caused ones. Natural fluctuations were mainly due to the effect of aphid enemies (ladybirds in most cases), and by winged aphids leaving the colony. Fluctuations (and often destruction of the whole colony) due to human influence were caused by mowing or animal (goat) grazing. We were not able to explain the reasons for fluctuations in some colonies, however. Vast majority of aphid natural enemies consisted of ladybird larvae or adults, followed by hoverfly larvae and parasitoid wasps from the subfamily Aphidiinae. During our observations, we determined the following ladybird species visiting aphid colonies: Adalia sp., Coccinella septempunctata, Harmonia axyridis (conspicua, spectabilis and succinea forms), Hippodamia variegata and Thea 22-punctata. When trees were sampled in 2017, ladybirds (both larvae and adults) were dominated by H. axyridis (larvae 86.4%; adults 70.6%), followed by some individuals of C. septempunctata (larvae 13.6%; adults 27.6%). In 2018, however, when we excluded trees from the sampling, the aphidophagous guilds were dominated by C. septempunctata (larvae 93.8%; adults 64.7%) followed by some individuals of Hippodamia variegata (23.5%). We did not observe any adults of Harmonia axyridis in 2018. In 2017, H. axyridis larvae were mainly present on tree species (like apple, peach and Prunus trees) while C. septempunctata larvae were present also on herbaceous plants. Regarding adults, the pattern was almost the same in the case of H. axyridis but we found C. septempunctata adults on trees, as well as on herbaceous plants at a higher rate.
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In 2018, the highest abundance of ladybird larvae and adults was observed on Rumex sp. and partly also on Sonchus sp. (mainly C. septempunctata); we also found some adults of Hippodamia variegata, Thea 22-punctata and Adalia sp. When only herbaceous plants in both years are considered, ladybirds were present mainly on Rumex and partly also on Sonchus. We also looked at how much the presence of natural enemies shortens the duration of an aphid colony. According to the theory we tested, this may be one of the reasons, why Harmonia axyridis is not very successful in the Mediterranean: the aphid colony may exist for a too short period in the Mediterranean conditions to enable successful development of H. axyridis. The results of this analysis are not ready yet, however.
Acknowledgements
This project was supported by grant no. 17-06763S of the Grant Agency of the Czech Republic. We would like to thank all collaborators who helped us in the field and with determination of insects, mainly A. Honěk, S. Tsiftsis, M. Pultr and M. Habinová.
References
Brown, P. M. J., Frost, R., Doberski, J., Sparks, T., Harrington, R. and Roy, H. E. 2011. Decline in native ladybirds in response to the arrival of Harmonia axyridis: Early evidence from England. Ecol. Entomol. 36: 231-240. Hilton-Taylor, C. 2000. 2000 IUCN red list of threatened species. [WWW document] https://portals.iucn.org/library/sites/library/files/documents/RL-2000-001.pdf. Accessed 25 Nov. 2018. Roy, H. E., Adriaens, T., Isaac, N. J. B., Kenis, M., Onkelinx, T., Martin, G. S., Brown, P. M. J., Hautier, L., Poland, R., Roy, D. B., Comont, R., Eschen, R., Frost, R., Zindel, R., van Vlaenderen, J., Nedved, O., Ravn, H. P., Gregoire, J. C., de Biseau, J. C. and Maes, D. 2012. Invasive alien predator causes rapid declines of native European ladybirds. Divers. Distrib. 18: 717-725. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A. A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Handley, L. L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M. G., Sloggett, T. T., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglasova, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. H. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 71-73
Mapping the distribution of Harmonia axyridis (Pallas) in Argentina through citizen science
Victoria Werenkraut1*, Florencia Baudino1 and Helen E. Roy2 1Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue, CONICET, Quintral 1250, Bariloche (8400), Argentina; 2Centre for Ecology and Hydrology, Benson Lane, Crowmarsh Gifford, Oxfordshire, OX10 8BB, UK *Corresponding author: [email protected]
Extended abstract: Sometimes species used as biological control agents have become successful invaders; this is the case for the harlequin ladybird, Harmonia axyridis (Pallas). This species is native to Asia and has been introduced intentionally as a biological control of pest insects in many countries, but also unintentionally in many others (Roy et al., 2016). By 2016, H. axyridis was established populations in at least 59 countries outside its native range (Camacho-Cervantes et al., 2017) becoming one of the world’s most widely distributed ladybirds, found on all continents except Antarctica. Indeed, it is listed among the ‘100 of the worst’ alien invasive species in Europe (DAISIE, 2017). The distribution, rate of spread, and effects of this species have been intensively studied in Europe and North America (e. g., Koch and Galván, 2008; Brown et al., 2011; Purse et al., 2015). In South America, detailed information only exists for Chile where the species has shown an extremely fast rate of spread (Grez et al., 2016). Studies on the distribution, spread, and impacts of this species in Argentina are surprisingly scarce, despite the relevance of this species in neighbouring Chile, and that predictions based on climatic models show that the H. axyridis potential distribution includes almost the entire Argentine territory (Poutsma et al., 2008). Harmonia axyridis had been introduced into Argentina in Mendoza Povince in 1986 (García et al., 1999). By 2001, it was detected in Buenos Aires – around 1,000 km away from the introduction area (Saini, 2004). By 2018 it was established in at least five provinces in the centre of Argentina (Buenos Aires, Mendoza, Córdoba, Santa Fe, Entre Ríos), and in NW Patagonia (Neuquén and Río Negro provinces). Unfortunately, these data are mainly from grey literature or records are only anecdotic (e. g., Monteiro and Vignaroli, 2008; Olave et al., 2018). Given the lack of knowledge and uncertainty about the distribution of H. axyridis in Argentina, our aim was to fill this gap, mapping its distribution through a citizen science approach. In June 2018, we developed a website with information about H. axyridis and how to identify it: https://sites.google.com/a/comahue-conicet.gob.ar/vam. There are three ways for records to be reported: (1) submitting photographs through an iNaturalist project (https://www.inaturalist.org/projects/vaquita-asiatica-multicolor), (2) submitting records using a Google Form, and (3) sending an institutional e-mail. We sent over 100 e-mails with a brief description of the project and link to the website to people and e-mail lists from the scientific community and national agencies all over the country, and we specifically asked to spread the message to all their communities (not only to the academic ones). By September 2018, we received 70 records from 45 observers. We confirm the presence of the species in the provinces mentioned above and add new records for the species from the North-West, North- East, Centre, and South of the country, suggesting that the species is widespread in Argentina.
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The number of records we obtained was low, and this could be due to the fact that our request did not reach many people, but it could also be due to the lack of tradition for Argentinean people to be involved in biodiversity reporting. It remains a challenge to capture the attention of people. We are planning to continue our project by increasing engagement through other media such as social networks, radio, television, etc. This work has provided a baseline to continue the study of H. axyridis and its impacts in Argentina.
References
Brown, P. M. J., Thomas, C. E., Lombaert, E., Jeffries, D. L., Estoup, A. and Lawson Handley, L.-J. 2011. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56: 623-641. Camacho-Cervantes, M., Ortega-Iturriaga, A. and del-Val, E. 2017. From effective biocontrol agent to successful invader: the harlequin ladybird (Harmonia axyridis) as an example of good ideas that could go wrong. PeerJ 5: e3296. DAISIE (Delivering Alien Invasive Species Inventories for Europe) 2017. Harmonia axyridis. [WWW document] http://www.europe-aliens.org/pdf/Harmonia_axyridis.pdf. Accessed 30 Apr. 2019. García, M. F., Becerra, V. C. and Reising, C. E. 1999. Harmonia axyridis Pallas (Coleoptera, Coccinellidae). Estudio biológico. Rev. Fac. Cienc. Agrar. 31: 85-91. Grez, A. A., Zaviezo, T., Roy, H. E., Brown, P. M. J. and Bizama, G. 2016. Rapid spread of Harmonia axyridis in Chile and its effects on local coccinellid biodiversity. Divers. Distrib. 22: 982-994. Koch, R. L. and Galvan, T. L. 2008. Bad side of a good beetle: the North American experience with Harmonia axyridis. BioControl 53: 23-35. Monteiro, G. and Vignaroli, L. 2008. Un Coccinelído exótico (Harmonia axyridis) invade los agroecosistema del sudeste de Santa Fé. Rev. Agromensajes 10: 3-4. Olave, A., Dapoto, G. L. and d’Hervé, F. E. 2018. Ingresos de Artrópodos registrados durante una década en la región de los valles irrigados de Río Negro y Neuquén (Argentina). X Congreso Argentino de Entomología. Mendoza, Argentina. Poutsma, J., Loomans, A., Aukema, B. and Heijerman, T. 2008: Predicting the potential geographical distribution of the harlequin ladybird, Harmonia axyridis, using the CLIMEX model. BioControl 53: 103-125. Purse, B. V., Comont, R., Butler, A., Brown, P. M., Kessel, C. and Roy, H. E. 2015. Landscape and climate determine patterns of spread for all colour morphs of the alien ladybird Harmonia axyridis. J. Biogeogr. 42: 575-588. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A. O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016. The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. 73
Saini, E. D. 2004. Presencia de Harmonia axyridis (Pallas) (Coleoptera: Coccinelidae) en la provincia de Buenos Aires. Aspectos biológicos y morfológicos. Rev. Investig. Agropecu. 33: 151-160.
Benefits and Risks of Exotic Biological Control Agents IOBC-WPRS Bulletin Vol. 145, 2019 pp. 74-76
Establishing the pattern of spread of harlequin ladybirds in Cork County, Ireland
Gill Weyman1,2*, Fidelma Butler2, Pádraig Whelan2 and Sean McKeown1 1Fota Wildlife Park, Carrigtwohill, County Cork, Ireland; 2University College Cork, School of Biological, Earth and Environmental Sciences, Distillery Field, North Mall, Cork City, Ireland *Corresponding author: [email protected]
Extended abstract: Harmonia axyridis (Coleoptera: Coccinellidae) is an invasive ladybird that was first recorded in Ireland in 2007. The first record from Northern Ireland (Murchie et al., 2008) was that of a ladybird being transported with vegetables from England. This was followed by subsequent records in Carlow and Cork City in 2010, in Carlow and Cork City (O’Sullivan, 2015). In order to understand the future pattern of its dispersal, it is important to determine the current baseline distribution. It has been demonstrated (Snyder et al., 2004, Yasuda et al., 2004; Ware et al., 2009; Vilcinskas et al., 2013; Roy et al., 2016) that the presence of H. axyridis can negatively impact on native ladybird species in terms of competition for food and other characteristics such as having two or more broods of offspring per year. During June and July 2018, surveys were undertaken at 18 urban locations across an area which extended between 15 to 20 kilometres from Cork city centre. This area was chosen as H. axyridis was already established in Cork City. At each of the 18 locations, 2-6 sites were visited according to the size of the area. At each site twenty minutes was spent searching for ladybirds in addition to tree beating or sweeping, dependant on habitat. It was found that species richness ranged from 3 to 6 species and abundance of native species ranged from 0 to 38 across the 18 sites. To determine the extent of the spread of H. axyridis in Cork, past records were taken from citizen science recording platforms (National Biodiversity Data Centre and www.Biology.ie), and added to the records from the 2018 survey. Harmonia axyridis was found in two urban areas of the survey: Ballincollig and Glanmire. Table 1 lists all native species recorded and shows that 140 individual H. axyridis ladybirds were recorded at 6 of the 9 survey sites in Glanmire. Past records from citizen science surveys such as the Irish Wildlife Trust and this research project show that H. axyridis has spread north, south, east and west since the first record in Cork City in 2010. Dispersal of H. axyrids from past records and this survey found distances of movement from the city centre from up to 124 km to the east, 7.4 km to the west, 1 km to the north and 3.5 km to the south of Cork City. In England, within 6 years, H. axyridis had dispersed across most of the country (Brown et al., 2008). In Cork the current patterns of disperal spread has occurred over 8 years (Figure 1). In 2010 only one record was known from Cork City. In 2017, 19 records were submitted (NBDC, 2017) followed by a number of reports of hibernation sites to the author (personal e-mail). Harmonia axyridis is now established in Cork City. The spread of H. axyridis has been found to be slow in comparison to other European countries where dispersal has been rapid (Brown et al., 2008; Majerus et al., 2009; Brown et al., 2008). Brown et al. (2008) predicted that H. axyridis in time would be found in Ireland.
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Table 1. Number of species and abundance of ladybirds in the 2018 survey, including distance of the survey location from the city centre in km.
Site No. individuals No. species Distance to city centre Ballincollig 27 7 7.38 Glanmire 140 5 6.77 Ballinhassig 10 4 10.4 Cobh 27 3 13.9 Ringaskiddy 15 3 1301 Carrigaline 14 3 11.25 Carrignavar 39 2 9.92 Innishannon 11 2 19.16 Blarney 5 2 6.7 Carrigtwohill 4 2 15.22 Crossbarry 4 2 15.4 Watergrasshill 2 2 15.36 Leamlara 3 1 17.01 Whitechurch 3 1 9.31 Knockraha 1 1 11.69 Riverstick 1 1 14.15 Grenagh 0 0 15.17 Monkstown 0 0 11.6 TOTAL 306 41
Figure 1. Location of H. axyridis ladybirds in Cork City and adjacent areas from the 2018 survey and past records. 76
The results of this survey provide a baseline for future study on the distribution and impact of H. axyridis in Ireland. There are currently isolated records in Dublin, Limerick, Waterford, Carlow and Louth. It is hoped that further records and study will provide the information necessary to establish a management plan for this invasive species.
References
Brown, P. M. J., Adriaens, T., Bathon, H., Cuppen, J. Goldarazena, A., Hágg, T., Kenis, M., Klausnitzer, B. E. M., Kovar, I., Loomans, A. J. M., Majerus, M. E. N., Nedvěd, O., Pedersen, J., Rabitsch, W., Roy, H. E., Ternois, V., Zakharov, I. A. and Roy, D. B. 2008. Harmonia axyridis in Europe: spread and distribution of a non-native coccinellid. BioControl 53: 5-21. Majerus, M., Strawson, V. and Roy, H. 2009. The potential impacts of the arrival of the harlequin ladybird, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), in Britain. Ecol. Entomol. 34: 12-19. Murchie, A. J., Moore, P., Moore, G. A. and Roy, H. E. 2008. The harlequin ladybird (Harmonia axyridis (Pallas)) (Coleoptera: Coccinelidae), found in Ireland. Ir. Nat. J. 29: 25-26. O’Sullivan, J. 2015. A breeding site for the harlequin ladybird [Harmonia axyridis (Pallas)] (Coleoptera: Coccinellidae) in Co. Cork. Ir. Nat. J. 34: 72-77. Roy, H. E., Brown, P. M. J., Adriaens, T., Berkvens, N., Borges, I., Clusella-Trullas, S., Comont, R. F., de Clercq, P., Eschen, R., Estoup, A., Evans, E. W., Facon, B., Gardiner, M. M., Gil, A., Grez, A., Guillemaud, T., Haelewaters, D., Herz, A., Honek, A., Howe, A. G., Hui, C., Hutchison, W. D., Kenis, M., Koch, R. L., Kulfan, J., Lawson Handley, L., Lombaert, E., Loomans, A., Losey, J., Lukashuk, A.O., Maes, D., Magro, A., Murray, K. M., San Martin, G., Martinkova, Z., Minnaar, I. A., Nedved, O., Orlova-Bienkowskaja, M. J., Osawa, N., Rabitsch, W., Ravn, H. P., Rondoni, G., Rorke, S. L., Ryndevich, S. K., Saethre, M.-G., Sloggett, J. J., Soares, A. O., Stals, R., Tinsley, M. C., Vandereycken, A., van Wielink, P., Viglášová, S., Zach, P., Zakharov, I. A., Zaviezo, T. and Zhao, Z. 2016: The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol. Invasions 18: 997-1044. Snyder, W. E., Clevenger, G. M. and Eigenbrode, S. D. 2004. Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140: 559-565. Vilcinskas, A., Stoecker, K., Schmidtberg, H., Rohrich, C. R. and Vogel, H. 2013. Invasive harlequin ladybird carries biological weapons against native competitors. Science 340: 862-863. Ware, R., Yguel, B. and Majerus, M. 2009. Effects of competition, cannibalism and intra- guild predation on larval development of the European coccinellid Adalia bipunctata and the invasive species Harmonia axyridis. Ecol. Entomol. 1: 12-19. Yasuda, H., Evans, E. W., Kajita, Y., Urakawa, K. and Takizawa, T. 2004. Asymmetric larval interactions between introduced and indigenous ladybirds in North America. Oecologia 141: 722-731.