Published in "BioControl 62(3): 341–354, 2017" which should be cited to refer to this work. Assessing the ecological risk posed by a recently established invasive alien predator: Harmonia axyridis as a case study Marc Kenis . Tim Adriaens . Peter M. J. Brown . Angelos Katsanis . Gilles San Martin . Etienne Branquart . Dirk Maes . Rene´ Eschen . Renate Zindel . Johan Van Vlaenderen . Dirk Babendreier . Helen E. Roy . Louis Hautier . Remy L. Poland Abstract Invasive alien predators are a serious native species encounters H. axyridis in the field, the threat to biodiversity worldwide. However, there is hazard of competition for food, and the IGP hazard. no generic method for assessing which local species Thirty native European ladybird species were assessed are most at risk following the invasion of a new through data obtained from field observations, labo- predator. The harlequin ladybird, Harmonia axyridis ratory experiments and literature reviews. The species (Pallas) (Coleoptera: Coccinellidae), is an alien in that are considered most at risk are found on deciduous Europe and many other parts of the world where it trees, have immature stages which are highly vulner- affects other species of ladybirds through competition able to IGP by H. axyridis, and are primarily for food and intra-guild predation (IGP). Here, we aphidophagous. These species should be the focus of describe a method developed to assess which Euro- specific studies and possibly conservation actions. The pean ladybird species are most at risk following the risk assessment method proposed here could be invasion of H. axyridis. The three components of the applied to other alien predators which are considered risk assessment are: the likelihood that the assessed a threat to native species through competition and predation. M. Kenis (&) Á A. Katsanis Á R. Eschen Á E. Branquart R. Zindel Á J. Van Vlaenderen Á D. Babendreier Invasive Species Unit, De´partement de l’Etude du Milieu http://doc.rero.ch CABI, 2800 Dele´mont, Switzerland Naturel et Agricole (DEMNA), Service Public de e-mail: [email protected] Wallonie, Avenue Mare´chal Juin, 23, 5030 Gembloux, Belgium T. Adriaens Á D. Maes Research Institute for Nature and Forest (INBO), R. Zindel 1070 Brussels, Belgium Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland P. M. J. Brown Animal & Environment Research Group, Department of H. E. Roy Life Sciences, Anglia Ruskin University, NERC Centre for Ecology & Hydrology, Cambridge CB1 1PT, UK Crowmarsh Gifford, Oxfordshire OX10 8BB, UK G. S. Martin Á L. Hautier R. L. Poland De´partement Sciences du Vivant, Centre Wallon de Clifton College, Clifton, Bristol, Avon BS8 3JH, UK Recherches Agronomiques, Unite´ Protection des Plantes et Ecotoxicologie, 5030 Gembloux, Belgium 1 Keywords Biological invasions Á Coccinellidae Á is usually lacking despite its obvious potential use for Ecological impact Á Harmonia axyridis Á Intra-guild prioritising research and conservation actions in the predation Á Risk assessment invaded regions. An example of an introduced arthropod predator that has had undesirable ecological impacts is the harlequin ladybird Harmonia axyridis (Pallas) Introduction (Coleoptera: Coccinellidae). This beetle was intro- duced into North America in 1916 and throughout the Invasive alien species are recognised as one of the 20th century to control aphids and coccids, and main causes of animal biodiversity loss (Bellard et al. became established in the 1980s (Roy et al. 2016). 2016). Associated animal species declines are mainly Since then, although successfully regulating pest due to competitive exclusion, predation, and intro- aphids in a range of crop systems, it has spread and duction of new diseases (Long 2003; Kenis et al. increased in number rapidly across most of North 2009). In particular, alien predatory insects are known America, where it has become the dominant aphi- to displace insects and other animals worldwide dophagous ladybird (e.g. Colunga-Garcia and Gage through competition for resources and predation 1998; Harmon et al. 2007). Harmonia axyridis was (Snyder and Evans 2006; Wagner and van Driesche commercially available in Europe as a pest-control 2010). In most cases, invasive alien insects have been agent from the late 1980s and feral populations were introduced accidentally, either as contaminants or first observed in Germany in 1999 (Brown et al. 2011). stowaways (Hulme et al. 2008). Nevertheless, preda- The beetle then rapidly invaded most European tors and parasitoids have also been released inten- countries and many other regions on all continents tionally in biological control programmes for pest except Antarctica (Roy et al. 2016). control and a small proportion of them have had The threat posed by H. axyridis to biodiversity and undesirable ecological effects on non-target species ecosystem functions in invaded regions may be through competition for resources, predation or considerable. Impacts on native species can occur parasitism on native species (Hajek et al. 2016). both through direct predation and competition for Pre-release risk assessment protocols have the poten- resources. Harmonia axyridis has a broad diet, tial to limit the risk of non-target effects but these risk putting many non-target species at risk from preda- assessments are not yet carried out systematically in tion. Whilst preferring aphid and coccid prey, H. all countries (van Lenteren et al. 2006; Hajek et al. axyridis will also accept the immature stages of many 2016). Other risk and impact assessment protocols insects, including butterflies and other aphid preda- exist for alien species beyond biological control tors (Koch et al. 2003, 2006; Pell et al. 2008). Intra- introductions, many of which are appropriate for guild predation (IGP), i.e. the killing and eating of assessing predators (e.g. D’hondt et al. 2015; Kum- species eating similar, often limiting, resources (Polis schick et al. 2015) and some protocols have been et al. 1989), is widespread amongst aphidophagous http://doc.rero.ch developed for specific groups of predators, such as insects, and H. axyridis is known to attack the ants (Harris et al. 2005). However, these protocols immature stages of many ladybird guild members aim at assessing the risk or impact of specific invasive (Ware and Majerus 2008; Ware et al. 2008a; Rondoni alien species, taking into account their general impact et al. 2012a, b; Katsanis et al. 2013). Recent in the invaded habitat (Kumschick and Richardson observations have demonstrated that H. axyridis also 2013). In contrast, there is no generic method to feeds on European ladybirds in the field (Hautier assess which particular native species are most at risk et al. 2011; Thomas et al. 2013; Rondoni et al. 2014; following the invasion of a predator. Such knowledge Brown et al. 2015). Negative effects of H. axyridis on native Coccinel- lidae have already been documented in North Amer- ica. For example, H. axyridis was reported to be Present Address: A. Katsanis displacing Cycloneda sanguinea (L.), in Florida citrus Department of Ecology and Evolutionary Biology, University orchards (Michaud 2002). Similarly, within four years of California – Irvine, Irvine, CA 92697-2525, USA of its arrival in Michigan, H. axyridis had taken over 2 the status of Coleomegilla maculata (DeGeer) as the Materials and methods dominant aphid predator, and a decrease in popula- tions of three other species of ladybird was reported: A risk assessment involves identifying and quantify- Brachiacantha ursina (F.), Cycloneda munda (Say) ing the hazards, and determining the probabilities that and Chilocorus stigma (Say) (Colunga-Garcia and these hazards will materialise. The risk is then the Gage 1998). However, in an analysis of a 26-years product of a likelihood (probability) and a magnitude dataset in the same region, Bahlai et al. (2015) of hazard (consequence). In this study, the risk posed confirmed the long term decline of two species only, by H. axyridis on 30 native ladybirds (see list in C. maculata and Adalia bipunctata (L.). Table 1) was considered as the product of the likeli- In Europe, field studies have been undertaken in hood that a given ladybird species encounters H. several countries to monitor changes in populations of axyridis in the field, and the consequence of this native ladybird species following the arrival of H. encounter, through competition for food and direct axyridis (e.g. Eschen et al. 2007;Adriaensetal.2008; predation. Therefore, the risk assessment was carried Brown et al. 2011). A first assessment of the impact of out in three steps: (1) likelihood of encounter with H. H. axyridis on native species of ladybird in Belgium, axyridis in the field, (2) competition for food, (3) intra- Britain and Switzerland showed that some historically guild predation. widespread and common species are declining (Roy et al. 2012). For A. bipunctata in Belgium, the rate of Likelihood of encounter with H. axyridis decline warrants red listing as a vulnerable species in the field (Adriaens et al. 2015). However, ladybird populations are known to fluctuate naturally and, thus, it may take The likelihood that a native ladybird species encoun- several years before a long-term impact can be ters H. axyridis in the field was measured using field ascertained. Also, some species were already in data in Switzerland, Belgium and Britain. Datasets decline before the arrival of H. axyridis,suggesting comprising field observations were used to assess that the invasion acted as an additional