Review Article
Print
Review Article
Traits related to biological invasion: A note on the applicability of risk assessment tools across taxa
expand article infoLisa M. Emiljanowicz, Heather A. Hager, Jonathan A. Newman
‡ University of Guelph, Guelph, Canada
Open Access

Abstract

Biological invasions are occurring frequently and with great impact to agricultural production and other ecosystem services. In response to this, the Australian Weed Risk Assessment (AWRA) was created to assess the potential ‘weediness’ of plants based on answers to questions related to biogeography, undesirable attributes, and biology or ecology. This basic model has been expanded and adapted for use on other taxa, often without adequate validation. Since invasive insect crop pests are a major economic cost to agricultural production, there is interest in using an expanded model for insects. Here, we review traits related to invasiveness of insects based on a systematic review of the literature. We then compare the identified invasive traits of insects with those identified for plants in the AWRA. Using insects as a case study, we illustrate that although there is some overlap in invasive traits, there are many unique traits related to invasion for both insects and plants. For insects, these traits relate largely to social behaviour. This lack of congruence may also be the case for other taxa. To increase predictive power, a taxon-specific risk assessment tool and deliberate verification are required.

Keywords

Australian weed risk assessment, invasion traits, life history traits, risk assessment, systematic review, invasive insects

Introduction

It is now widely accepted that invasive species are a major cause of global biodiversity loss, and as such, public interest in the topic has increased over recent decades (Didham et al. 2005). By way of increased transportation and international trade, biological invasions are occurring more frequently with increasingly undesirable costs to ecosystem services (Mack et al. 2000, Colautti et al. 2006). Although invasive species are defined in a number of ways with a variety of terms (Lockwood et al. 2013), often they are associated with ‘harm’ to the newly invaded environment (Mack et al. 2000). Because this is not always the case, and harm can be defined in many ways (Sagoff 2009), we follow Richardson et al. (2000b) and define ‘invasive species’ as those that have established and spread in a new geographic range.

In the United States alone, it has been estimated that 50 000 non-native species have been introduced, 4 500 of those being arthropods (Pimentel et al. 2005). Narrowed further, about 500 (11%) introduced insect and mite crop pest species have invaded (Pimentel et al. 2005), and the most economically important species of all agricultural pests are non-native (Mack et al. 2000). Approximately 95% of these arthropod introductions are accidental through entrance on plants, soil, ship ballast water, food sources, wood, etc (Pimentel et al. 2005, Rabitsch 2010). These crop pest introductions are estimated to cause US$13.5 billion dollars in damage annually in the United States due to crop loss and additional pesticide use (Pimentel et al. 2005). Economic impacts can also be indirect through restrictions on trade flow and market access changes (Roques et al. 2010). In comparison to the United States, 383 introduced insect species have been documented in the Czech Republic, of which 111 (29%) are considered either greenhouse or storage pests causing economic damage (Sefrova 2014). For just 10 nuisance invasive species (not just insect pests) in Canada, it was estimated that fisheries, forestry, and agriculture suffer a CDN$187 million loss annually (Colautti et al. 2006). In Europe, 1383 alien insects have been introduced and established to date, while the rate of introduction continues to accelerate (Roques et al. 2010). Despite substantial variation, species invasion is a global problem affecting a range of economically important services.

Government regulatory bodies have a legal responsibility to assess the risks of potential biotic invasions that could result in a detriment to plant resources, as dictated by the International Plant Protection Convention treaty (IPPC 1997). Thus, predictive pest risk assessment schemes have been created to assess invasion risks posed by plant species (e.g., Reichard and Hamilton 1997, Pheloung et al. 1999) based on the idea that certain life history traits increase the probability of invasiveness (Baker 1974). Using such schemes, plant species are evaluated for invasion risk according to the number and type of invasive traits they possess. For example, Reichard and Hamilton (1997) created a scheme to predict the invasion of woody plants in North America, yielding ~80% predictive success rate using life history and biogeographical attributes of a plant to predict invasion. In particular, reproductive attributes of the invader were important in predicting the invasive potential of woody plants (Reichard and Hamilton 1997).

Pheloung et al. (1999) expanded the decision tree method employed by Reichard and Hamilton (1997) to produce a computer-based spreadsheet checklist for invasive plants called the Australian Weed Risk Assessment (AWRA). The AWRA comprises 49 equally weighted questions, with sections on biogeography, undesirable attributes, and biology and ecology. The answers to these questions result in a score that informs the user about the potential ‘weediness’ of the plant, and from there a regulatory decision can be made. Pheloung et al. (1999) conclude that the AWRA can serve as a biosecurity tool to identify potentially invasive weeds, and can be modified for use in other locations. Currently the AWRA is used by the Department of Agriculture in Australia as a component of their multi-tiered WRA process (Department of Agriculture and Water Resources 2015). A comparison of the AWRA and other models (such as Reichard and Hamilton [2007]) found the AWRA to be the most accurate (Jefferson et al. 2004). The AWRA has since been modified and tested for invasive plants in New Zealand (Pheloung et al. 1999), the Hawaiian Islands (Daehler and Carino 2000), other Pacific islands (Daehler et al. 2004), Japan (Kato et al. 2006), the Czech Republic, and Florida (Gordon et al. 2008), with fairly consistent results. However, when the AWRA was tested for invasive plants in Canada, it was found to reject a high proportion of non-weedy species (McClay et al. 2010). Since Canada is characterized by cool, short growing seasons, simple alterations to the system that take cold-hardiness into account could increase the predictive power of the AWRA in Canada (McClay et al. 2010). Therefore, this system is generally accepted to function as a template for weed risk assessments across tropical and temperate geographies (Gordon et al. 2008).

Following the success of the AWRA, attempts have been made to create similar models for use with other taxa. Some models have evaluated potential invasive traits based on a priori hypothesized characteristics. For example, Causton et al. (2006) proposed a simple scoring system for identifying insects that are potentially invasive to the Galapagos Islands. However, it is not clear why Causton et al. (2006) chose the traits that they did, as the selection does not appear to be based on any systematic analysis. Similarly, Kolar and Lodge (2002) and Marchetti et al. (2004) do not provide reasoning for their selection of traits that were considered in their models for fish invasion. Additionally, the AWRA has been used as a basis for risk assessment schemes that are generalized for other non-native taxa (Table 1). Although this method might be useful because of its generality, it may not be valid if traits that are relevant to weediness in plants are not applicable to invasiveness in other taxa; its applicability remains unknown because the traits assessed in the AWRA have not been tested for relevance in other taxa.

Examples detailing when the AWRA has been adapted for use on taxa other than plants.

Risk assessment model Taxon Reference
UK risk assessment scheme Freshwater fish, marine fish, marine invertebrates, amphibian Baker et al. 2008
FISK Freshwater fish Copp et al. 2005, Copp et al. 2008
MFISK Marine fish Copp et al. 2008
FI-ISK Freshwater invertebrates Copp et al. 2008
MI-ISK Marine invertebrates Copp et al. 2008
AmphISK Amphibians Copp et al. 2008
Infectious Agent Risk Assessment Module Infectious agents Copp et al. 2008
Generic Pre-screening Module All other taxa Copp et al. 2008

The issue of transferability of invasive traits across taxa was investigated by Hayes and Barry (2008), who tested the significance of 115 invasive characteristics across seven taxonomic groups. Of the 49 studies included in their systematic review of predictors of invasion success, only two pertained to insects. Although they found some consistency in trait differences between native and invasive species, this was mainly only for plants. Overall, climate or habitat match was the only trait related to invasiveness across biological groups (Hayes and Barry 2008). Therefore, it is unclear whether a scheme created for use on plants can be generalized for use with other taxa. Traits that are related to invasiveness in plants may not generalize to other taxa, and if they do, their importance may not be similar across taxa.

Currently, there is no adequately validated, trait-based approach to risk assessment for insects, as there is for plants. Additionally, it remains unclear whether traits that are related to invasiveness in plants are generalizable to other taxa. Formal analyses are needed to determine traits predictive of invasiveness in taxa other than plants to ascertain the validity and generality of using a single risk assessment scheme across taxa. Because the AWRA has been expanded for use on other taxa, without validation, the aim of this paper is to compare questions in the AWRA with traits in the literature that are claimed to be related to insect invasion success.

As a first step in evaluating the generalizability of an invasion risk assessment scheme, we performed a systematic review of the literature for traits that are claimed to affect invasiveness in any insects. We compare these traits with those that are used to assess weediness in plants, and then discuss the potential validity of, and problems with, generalizing the AWRA for assessing the invasion risk of insects. We include all types of insects to gather the most trait data possible. This review, synthesis, and comparison of information is an important precursor to a larger project that will evaluate predictive traits and critical pathways of insect invasion with the overall objective of producing a comprehensive insect pest risk assessment scheme.

Methods

To determine whether there is congruence between traits related to invasion success in both plants and insects, we conducted a literature search that was completed in August 2015 using the Web of Science database (Thomson Reuters, New York, USA) and the following Boolean search adapted from Hayes and Barry (2008) in the “topic” function: (attributes OR correlates OR characteristics) AND (alien OR non-native OR non-indigenous OR exotic OR invasive) AND (invasion OR establishment) AND (success OR predict) AND (insect OR invertebrate). The search resulted in approximately 3 500 results; from this, 125 articles were identified as relevant (i.e. they minimally discussed a biological or environmental trait of an invasive insect) by examining the article abstract. Papers were included in our analysis if they tested or claimed traits that were related to invasion success in insects (i.e. other classes of invertebrates were excluded). Papers that were included were then screened for experimental, observational, or anecdotal information pertaining to traits of invasive or native insects. These data were extracted and compiled into a spreadsheet to highlight whether differences existed between invasive and native insects, and between invasive plants and invasive insects. The data we included were: the trait being tested or claimed, the trait type (life history or environmental), the trait states (invasive vs. native), the reference, and what the significance or application of this result was.

Results and discussion

We identified a total of 79 traits that were claimed to have some relation to invasiveness in insects (Table 2). We grouped the most similar traits together to avoid repetition, and we assigned categorical nomenclature (Table 3 and 4). Traits that related to the same life processes were assigned to the same group. For example, the trait dispersal includes flight speed, flight distance, flight temperature, dispersal type, dispersal habitat, and colonization ability. Consolidation of similar traits resulted in a total of 29 trait groups that are allegedly related to invasion success in insects. These 29 trait groups were divided into life history (Table 3) and environmental traits (Table 4) and compared against plant traits used to assess weediness in the AWRA to determine if there are clear analogues between insect and plant invasiveness traits.

Life history and environmental traits related to invasion, highlighting the suggested differences between invasive and native insects that were found through an extensive literature review.

Insect trait Trait component Differences between invasive and non-invasive insects Type of evidence†
Life history traits
Feeding guild Feeding niche Invasive insects predominantly sap feeders and detritivores (Kenis et al. 2007) C
Feeding guild Herbivores more likely to establish than predators and parasitoids (Engelkes and Mills 2011);
Parasitoids more likely to establish than predators (Kimberling 2004)
A, C
Taxon Diptera and Lepidoptera fastest to disperse, Coleoptera slowest (Paynter and Bellgard 2011)
Invasive species predominantly Hemiptera (56.4 %), Lepidoptera (14.9 %), and Hymenoptera (12.9 %) (Matosevic and Zivkovic 2013);
Invasive species predominantly Homoptera (39 %), Coleoptera (19 %), Lepidoptera (13 %), and Hymenoptera (13 %) (Mattson et al. 2007);
Invasive species predominantly Coleoptera, Sternorrhyncha, and Psocoptera (Kenis et al. 2007);
Homoptera and Lepidoptera most likely to establish (Peacock and Worner 2008)
C
Feeding method Miners, borers, and leaf-rollers disperse faster than external feeders, and root-, rosette-, and seed-feeders (Paynter and Bellgard 2011)
Internal feeders more likely to establish than external feeders (Kimberling 2004)
Insects that use single host species are more likely to establish than those that use multiple hosts (Mondor et al. 2007)
C
Diet breadth Diet breadth or Host specificity Invasive insects have a wide diet breadth (generalist) compared to natives (Moller 1996, Cervo et al. 2000, Kasper et al. 2004, Kimberling 2004, Moeser and Vidal 2005, Snyder and Evans 2006, Mondor et al. 2006, Ward and Masters 2007, Wilson et al. 2009, Orledge et al. 2010, Andersen et al. 2011) A, C, E, O
Generation onset Voltinism (number of generations per year) Dispersal rate increases as number of generations/year increases (Yan et al. 2005, Paynter and Bellgard 2011);
Insects with multiple generations per year more likely to establish than insects with one generation per year (Kimberling 2004)
A, C
Adult emergence Invasive insects emerge earlier than natives (Hack and Lawrence 1995, Pickett and Wenzel 2000, Gamboa et al. 2002, Gamboa et al. 2004, Boivin et al. 2008) A, E, O
Onset of egg laying Invasive insects start laying eggs earlier than natives (Kajita and Evans 2010b, Laugier et al. 2013) E, O
Development Growth rate Invasive insects have rapid growth rates compared to natives (Labrie et al. 2006, Ward and Masters 2007) A, O
Preimaginal (pre-adult) development time Invasive insects have shorter preimaginal development time than natives (Cervo et al. 2000, Gamboa et al. 2004, Boman et al. 2008, Delatte et al. 2009);
Invasive insects have a longer preimaginal development time than natives (Bonato et al. 2007)
A, E, O
Generation time Invasive insects have shorter generation time than natives (Facon et al. 2011);
Short generation times increase colonization success (Yan et al. 2005)
A, E
Intrinsic rate of increase Invasive insects have higher intrinsic rate of increase than natives (Crawley 1987, Duyck et al. 2007, Delatte et al. 2009, Orledge et al. 2010) A, C, E, O
Intrinsic death rate Invasive insects have lower intrinsic death rate than natives (Duyck et al. 2007, Foucaud et al. 2013) A, E, O
Dispersal Flight speed Invasive insects have higher flight speeds than natives (Sun et al. 2013);
Flight speed can enhance invasion (Lombaert et al. 2014)
A, E, O
Flight distance Invasive insects can fly longer distances than natives (Yan et al. 2005) A
Flight temperature Invasive insects can fly within a broader range of temperatures than natives (Yan et al. 2005) A
Dispersal type Insects capable of flight more likely to disperse than wind-dispersed or crawling species (Moller 1996, Paynter and Bellgard 2011);
Macropterous individuals increases dispersal ability (Niemelä and Spence 1991)
A, C, O
Dispersal habitat Aquatic insects disperse faster than terrestrial insects (Paynter and Bellgard 2011);
Permanent stream flow enhances invasion (Holway 1998)
C, O
Colonization ability Invasive insects have better colonization ability than natives (Harcourt et al. 1998, Yan et al. 2005) A, O
Desiccation resistance Desiccation resistance Invasive insects more resistant to desiccation than natives (Parkash et al. 2014) E, O
Mating behaviour Copulatory behaviour Invasive insects faster to copulate than natives (Laugier et al. 2013);
Female invasive insects fertilized by more males than native females (Laugier et al. 2013);
Invasive insects copulate more effectively than natives (Liu et al. 2007, Crowder et al. 2010)
A, E
Thermal resistance Temperature tolerance Invasive insects have lower temperature tolerance than natives (Wuellner and Saunder 2003, Bonato et al. 2007, Peacock and Worner 2008, Delatte et al. 2009, McGrannachan and Lester 2013, Parkash et al. 2014);
Invasive insects have higher temperature tolerance than natives (Michaud 2002, Wuellner and Saunder 2003, Bonato et al. 2007, Delatte et al. 2009, Ju et al. 2013)
Invasive insects have a higher lower developmental threshold than native insects (Jarošík et al. 2015)
C, E, O
Overwintering behaviour Aggregate overwintering Invasive insects overwinter in aggregate, whereas natives do not (Cottrell and Shapiro-Ilan 2003) E, O
Overwintering site Invasive insects overwinter in sheltered habitat, whereas natives do not (Yan et al. 2005) A
Winter survival Invasive insects have higher winter survival than natives (Inoue 2011, Raak-van den Berg et al. 2012) E, O
Body size Body size Invasive insects are smaller than natives (Crawley 1987, McGlynn 1999b, Gamboa et al. 2004, Ness et al. 2004, Cremer et al. 2006, Mondor et al. 2006, Cremer et al. 2008, Wilson-Rich and Starks 2010, Abril et al. 2013);
Small insects more likely to establish than large insects (Lawton et al. 1986, Lester 2005);
Invasive insects are larger than natives (Ings et al. 2006, Delatte et al. 2009, Kajita and Evans 2010a, Kajita and Evans 2010b);
Large body size may promote invasion success (Moller 1996)
A, C, E, O
Offspring mass Invasive insect offspring mass smaller than native offspring mass (Armstrong and Stamp 2003) E
Functional group Functional group Invasive insects predominantly cryptic, generalized Myrmicinae, and opportunists (McGlynn 1999a) C
Fecundity characters Lifetime performance Invasive insects have higher lifetime performance (product of hatching rate, larval survival, and subsequent fecundity) than natives (Facon et al. 2011);
High progeny production increases colonization success (Yan et al. 2005)
A, E
Egg laying behaviour Insects that lay eggs in batches less likely to become invasive (Crawley 1987)
Egg size Invasive insects lay larger eggs than natives (Duyck et al. 2007, Delatte et al. 2009);
Invasive insects lay smaller eggs than natives (Kajita and Evans 2010a)
A, E, O
Fecundity Invasive insects are fecund later than natives (Armstrong and Stamp 2003);
Invasive insects allocate more resources to fecundity than natives (Curtis et al. 2005);
Invasive insects have higher fecundity than natives (Pickett and Wenzel 2000, Michaud 2002, Duyck et al. 2007, Boivin et al. 2008, Delatte et al. 2009, Kajita and Evans 2010a, Kajita and Evans 2010b, Laugier et al. 2013);
Invasive insects have higher net reproductive rate than natives (Duyck et al. 2007, Delatte et al. 2009);
Invasive insects have higher gross reproductive rate than natives (Moller 1996, Duyck et al. 2007);
A, E, O
Egg viability Invasive insects have higher egg viability than natives (Michaud 2002) E, O
Juvenile survival Invasive insects have higher juvenile survival than natives (Duyck et al. 2007, Delatte et al. 2009); A, E, O
Percentage paternity Invasive insects have higher percentage paternity than natives (Laugier et al. 2013); E
Pupal mass Invasive insect pupae are larger than natives (Duyck et al. 2007) A, O
Competitive ability Competitive ability, adaptive ability Invasive insects can outcompete natives (Holway 1999, Thomson 2004, Snyder and Evans 2006, Rowles and O’Dowd 2007, De Barro and Bourne 2010, Wilson and Holway 2010, Sanders and Suarez 2011, Auger-Rozenberg and Roques 2012, Wilder et al. 2013);
Interspecific competition may limit invasion (LeBrun et al. 2007);
Invasive insects can use resources that natives cannot (Orledge et al. 2010);
Invasive insects can use resources in their introduced range that they cannot in their native range (Yan et al. 2005, Sun et al. 2013);
Invasive insects avoid predation through crypsis (Yan et al. 2005)
A, C, E, O
Predation Invasive insects prey upon native insects (Wilson and Holway 2010) E, O
Reproduction Reproductive strategy Invasive insects may be asexual, whereas natives reproduce sexually (Moller 1996, Mondor et al. 2006, Peccoud et al. 2008, Mikheyev et al. 2009, Caron et al. 2013) A, C, E, O
Oviposition site Oviposition site Insects that oviposit internally more likely to establish than insects that oviposit outside of host (Kimberling 2004) C
Sex ratio Sex ratio Invasive insects have female-skewed sex ratio, whereas natives do not (Michaud 2002, Liu et al. 2007) E, O
Intraguild predation Intraguild predation Invasive insects are stronger intraguild predators than natives (Michaud 2002, Snyder et al. 2004, Roy et al. 2008a);
Native insects consume more conspecific eggs than invasive insects (Michaud 2002);
Invasive insects consume more heterospecific eggs than natives (Michaud 2002, Ware et al. 2009)
E, O
Foundress activity Foundress activity Invasive insect foundresses build and repair nests more often than natives (Armstrong and Stamp 2003);
Invasive insect foundresses more aggressive towards offspring than natives (Armstrong and Stamp 2003)
E
Aggression Level of aggression Invasive insects show less intraspecific aggression compared to natives (Holway et al. 1998, Suarez et al. 1999, Le Breton et al. 2004, Errard et al. 2005, Cremer et al. 2008, Fournier et al. 2009, Perdereau et al. 2011, Sanders and Suarez 2011, Suhr et al. 2011, Ugelvig and Cremer 2012, Hoffmann 2014);
Low intraspecific aggression may promote invasion success (Moller 1996);
Invasive insects show more interspecific aggression than natives (Human and Gordon 1999, Cremer et al. 2006, Duyck et al. 2006, Snyder and Evans 2006, Rowles and O’Dowd 2007, Carpintero and Reyes-Lopez 2008, Fournier et al. 2009, Blight et al. 2010, Perdereau et al. 2011)
A, E, O
Usurpation Native insects attempt usurpation more often than invasive insects (Gamboa et al. 2002, Gamboa et al. 2004);
Usurpation may increase establishment success (Moller 1996)
A, O
Colony characteristics Colony productivity Invasive insect nests (combs) contain more cells than natives (Pickett and Wenzel 2000, Gamboa et al. 2002, Gamboa et al. 2004);
Colony budding may increase establishment success (Moller 1996, Tsusui and Suarez 2003)
Invasive insects produce more adults than natives (Gamboa et al. 2004)
A, E, O
Relatedness to queen Invasive insects are less related to their queen than natives (Ross et al. 1996) O
Polygyne social form Invasive insects are polygyne (multiple egg-laying queens per nest) (Yang et al. 2012) O
Unicoloniality Invasive insects are unicolonial, whereas natives are multicolonial (Tsusui and Suarez 2003, Le Breton et al. 2004, Errard et al. 2005, Cremer et al. 2008, Suarez et al. 2008, Fournier et al. 2009, Wilson et al. 2009, Sanders and Suarez 2011, Ugelvig and Cremer 2012, Hoffmann 2014) A, E, O
Sociality Social insects are likely to become invaders (Moller 1996) A
Recognition cues Invasive insects are more chemically similar than natives (Errard et al. 2005, Cremer et al. 2008, Brandt et al. 2009, Fournier et al. 2009, Perdereau et al. 2011);
Invasive insects are more genetically similar than native insects (Tsusui and Suarez 2003, Suarez et al. 2008, Ugelvig and Cremer 2012)
A, E, O
Colony longevity Shift from small, annual colony to large, perennial colony can increase invasion success (Wilson et al. 2009) E, O
Queen characteristics Queen longevity Queen longevity is greater in invasive insects than in natives (Gamboa et al. 2002) O
Queen number Invasive insects have more queens per nest than natives (Ross et al. 1996, Tsusui and Suarez 2003, Abril et al. 2013);
Invasive insects produce more gynes (reproductive female caste) than native insects (Pickett and Wenzel 2000, Ings et al. 2006)
A, E, O
Nesting Nesting habitat Ground nesting ants more likely to establish than arboreal ants (Suarez et al. 2005);
Invasive insects nest in urban areas, whereas natives nest in rural areas (Downing 2012)
C, O
Nest predation Invasive insect nests suffer less predation than native nests (Cervo et al. 2000);
Invasive insects more likely to re-nest after predation than natives (Gamboa et al. 2004)
A, O
Nest reutilization Invasive insects may reuse a nest, whereas natives seldom do (Cervo et al. 2000) A
Environmental traits
Natural enemies present Presence of predators Presence of predators decreases invasive insect abundance and increases native insect development rate (Juliano et al. 2010);
Dispersal increases as presence of parasitoids in native range increases (Paynter and Bellgard 2011);
Absence of predators/parasitoids increases the likelihood of establishment (Lawton et al. 1986, Tsusui and Suarez 2003, Yan et al. 2005, Snyder and Evans 2006, Suarez et al. 2008, Ugelvig and Cremer 2012)
A, C, E
Rate of parasitism Invasive insects parasitized less often than natives (Cervo et al. 2000, Gamboa et al. 2002, Gamboa et al. 2004, Allen et al. 2007, Cremer et al. 2008, Gray et al. 2008, Orledge et al. 2010, Comont et al. 2014);
Invasive insects have higher parasite prevalence than natives (Jones and Brown 2014)
A, C, E, O
Fungal susceptibility Invasive insects less susceptible to fungal infections compared to natives (Cottrell and Shapiro-Ilan 2003) E, O
Immunocompetence
Invasive insects have a lower immune response than natives (Wilson-Rich and Starks 2010, Manfredini et al. 2013) E, O
Antimicrobial defence Invasive insects have an efficient immune system (Vilcinskas et al. 2013) E
Environmental matching Host range Invasive insects have wider host range than natives (Crawley 1987, Peacock and Worner 2008);
Certain mutualistic interactions will enhance invasion success (Wilder et al. 2011);
Presence of suitable host species increases invasion success (Brooks et al. 2012, Graziosi and Rieske 2012, Sun et al. 2013);
Synchronization with host species increases invasion success (Harcourt et al. 1988);
Phenological plasticity increases invasion success (Ward and Masters 2007)
A, C, E, O
Soil type High-moisture soils promote insect invasion (Bolger 2007);
Invasive insects more active at higher soil temperatures than natives (Human et al. 1998)
O
Humidity Invasive insects prefer high humidity, whereas natives do not (Walters and Mackay 2003);
Invasive insects have more extreme high and low humidity tolerances than natives (Wuellner and Saunder 2003)
E, O
Elevation Invasive insects prefer low elevation, whereas natives prefer high elevation (Human et al. 1998, Arndt and Perner 2008, Fitzgerald and Gordon 2012) O
Climate matching Invaded range must be climatically suitable for the invasive insect (Simberloff 1989, Holway 1998, Koch et al. 2006, Gray et al. 2008, Roura-Pascual et al. 2011, Sun et al. 2013) A, C, E, O
Light tolerance Invasive insects have more extreme high and low light tolerances than natives (Wuellner and Saunder 2003) O
Habitat type Invasive insects prefer dry cultivated fields over shrublands and plantations (Roura-Pascual et al. 2011);
Invasive insects more abundant in cool, dry areas, whereas native insects are more abundant in warm, humid areas (Parkash et al. 2014);
Invasive insects prefer open land, whereas natives prefer forests (Ishii et al. 2008);
Invasive insects prefer agricultural lands (56.4 %), followed by parks and gardens (28.7 %), and woodlands and forests (14.9 %) (Matosevic and Zivkovic 2013)
C, E, O
Propagule pressure Propagule pressure Greater numbers of introduced propagules and greater numbers of introductions increase the probability of establishment (Beirne 1975, Simberloff 1989, Hopper et al. 1993, Hight et al. 1995, Memmott et al. 1998, Grevstad 1999, Memmott et al. 2005, Suarez et al. 2005, Walters and Mackay 2005, Ward and Masters 2007, Mikheyev et al. 2008, Tobin et al. 2013);
Propagule size found not to affect establishment (Sagata and Lester 2009)
A, C, E, O
Disturbance Environmental disturbance Environmental disturbance decreases abundance of native species while increasing abundance of invasive species (Human et al. 1998, Zettler et al. 2004, Arndt and Perner 2008, Suarez et al. 2008, Fitzgerald and Gordon 2012);
Environmental disturbance positively associated with invasion success (Simberloff 1989, Snyder and Evans 2006, Roura-Pascual et al. 2011);
Environmental disturbance decreases the abundance of invasive species (Arndt and Perner 2008);
Environmental disturbance negatively associated with invasion success (Yeates et al. 2012)
A, C, E, O
Resistance evolution Resistance to insecticide Invasive insect able to evolve resistance to insecticide, leading to exclusion of native insect (Crowder et al. 2010) A, E
Biotic resistance Biotic resistance Insects able to invade due to lack of biotic resistance in the native assemblage (Niemelä and Spence 1991, Yan et al. 2005);
Areas with high biotic resistance are less prone to invasion (Walters and Mackay 2005, Blight et al. 2010, Roura-Pascual et al. 2011)
A, C, E, O
Foraging Foraging rate Foraging rate is greater in invasive insects than natives (Human and Gordon 1996, Holway et al. 1998, Gamboa et al. 2002, Ings et al. 2006, McGrannachan and Lester 2013) E, O
Predatory efficiency Invasive insects more efficient at capturing prey than native insects (Labrie et al. 2006, Dejean et al. 2007);
Invasive insects consume more prey than native insects (Labrie et al. 2006);
Invasive insects are more efficient at exploiting resources than native insects (Sanders and Suarez 2011)
A, E, O
Foraging distance Invasive insects will travel farther than native insects to forage (Perdereau et al. 2011) E, O
Foraging behaviour Invasive insects show flexible foraging behaviour (Wilson-Rankin 2014);
Invasive insects forage throughout the year, whereas native insects do not forage during winter (Wuellner and Saunder 2003);
Invasive insects start foraging earlier in the day than natives (Gamboa et al. 2004)
E, M, O
Bait recruitment Invasive insects recruit to bait faster than natives (Holway 1999, Dejean et al. 2007, Rowles and O’Dowd 2007, McGrannachan and Lester 2013);
Invasive insects recruit to more bait types than natives (Human and Gordon 1996, Holway 1998, Holway 1999)
E, O

A comparison of life history traits related to insect invasion and traits considered in the Australian weed risk assessment for plants.

Insect trait Invasive trait measures Plant equivalent
Feeding guild Feeding guild, feeding site, feeding niche, taxon, lifestyle category Parasitic, allelopathic
Diet breadth Diet breadth, host specificity Broad climatic suitability (environmental versatility)
Desiccation resistance Desiccation resistance Broad climatic suitability (environmental versatility)
Thermal resistance Temperature tolerance Broad climatic suitability (environmental versatility)
Overwintering behaviour Winter survival, aggregate overwintering, overwintering site Broad climatic suitability (environmental versatility)
Generation onset Generations per year, adult emergence, onset of egg laying Minimum generative time
Development Preimaginal development time, growth rate, generation time, intrinsic rate of increase, intrinsic death rate Minimum generative time
Dispersal Dispersal type, dispersal habitat, colonization ability, flight speed, flight temperature, flight distance Dispersal mechanisms
Body size Body size, offspring mass Seed size
Functional group Functional group Plant type
Mating behaviour Copulatory behaviour Reproduction
Fecundity Fecundity, egg viability, Net Reproductive Rate (NRR), egg size, Gross Reproductive Rate (GRR), percentage paternity, juvenile survival, lifetime performance, egg laying behaviour, pupal mass Reproduction
Reproduction Reproductive strategy Reproduction
Competitive ability Competitive ability, adaptive ability, predation Climbing or smothering growth habit
Oviposition site Oviposition site None
Sex ratio Sex ratio None
Intraguild predation Intraguild predation None
Foundress activity Foundress activity None
Aggression Aggression, usurpation None
Colony characteristics Recongnition cues, sociality, queen relatedness, colony productivity, polygyne social form, unicoloniality, colony longevity None
Queen characteristics Queen number, queen longevity None
Nesting Nesting habitat, nest predation, nest reutilization None
None None Species has weedy races
None None Species has a congeneric weed
None None Produces spines, thorns, or burrs
None None Unpalatable to grazing animals
None None Toxic to animals
None None Causes allergies or is otherwise toxic to humans
None None Prolific seed production
None None Evidence that a persistent propagule bank is formed (>1 yr)

A comparison of environmental traits related to insect invasion and traits considered in the Australian WRA for plants.

Insect trait Invasive trait measures Plant equivalent
Natural enemies present Presence of predators, rate of parasitism, fungal susceptibility, antimicrobial defense, immunocompetence Effective natural enemies present
Environmental matching Host range, climate matching, soil type, humidity, elevation, light tolerance, habitat type Species suited to climate, quality of climate match data, broad climatic suitability (environmental versatility)
Disturbance Environmental disturbance Broad climatic suitability (environmental versatility); tolerates or benefits from mutilation, cultivation, or fire
Propagule pressure Propagule pressure Dispersal mechanisms
Resistance evolution Resistance to insecticide None
Biotic resistance Biotic resistance None
Foraging Foraging rate, foraging behaviour, predatory efficiency, foraging distance, bait recruitment None
None None Species is highly domesticated
None None Species has become naturalized where grown
None None Native or naturalized in regions with extended dry periods
None None Species has a history of introductions outside its natural range
None None Species is naturalized beyond its native range
None None Garden/amenity/disturbance weed
None None Weed of agriculture/horticulture/forestry
None None Environmental weed
None None Creates a fire hazard to natural ecosystems
None None Is a shade tolerant plant at some stage in its life cycle
None None Grows on infertile soils
None None Forms dense thickets
None None Well controlled by herbicides

For insect invasion-related traits, it is noteworthy that some of the evidence is contradictory, i.e., a positive relation with invasiveness in some cases and a negative relation in others, and universal statements may not be accurate. For example, body size can either be positively or negatively associated with invasion (Table 2). It is self-evidently problematic to include contradictory traits in a risk assessment scheme based on universal statements.

Analogous insect and plant invasiveness traits

We identified 18 of 29 claimed invasive trait groups for insects that were represented by clear analogues of weedy traits in plants (Tables 1 and 2). This might lend some validity to a generalization of the AWRA for use on insects. However, whether these analogous traits infer invasiveness in insects in the same way, or to the same degree, as they do in plants has yet to be formally tested. By using decision tree modelling or similar methods to identify traits that are most important to invasion of insects, it would be possible to assess whether these traits hold similar ranks of importance between plants and insects. Furthermore, certain insect trait groups can be measured through numerous proxies. For example, the insect development trait group comprises a number of measures related to development that are potentially indicative of invasion. In contrast, the AWRA has only one question related to plant development, called minimum generative time. The fact that more developmental characteristics were claimed to be related to invasion in insects does not necessarily mean that development is more important in the invasion success of insects than in plants. This discrepancy may mean that more questions could be developed relating to insect development in a modified pest risk assessment. Conversely, if the multiple insect development measures have similar reliability, the one that is easiest to measure (e.g., development time, rather than development plasticity) could be chosen for inclusion in the risk assessment. However, it is possible that some of these trait groups are more predictive than others, and as such, all else being equal, the measures that are most predictive should be included in a risk assessment if multiple traits are correlated. This same issue arises with other insect trait groups, particularly generation onset, overwintering behaviour, fecundity characters, environmental matching, foraging, and colony characteristics.

Unique invasiveness trait groups of insects

We identified 11 of 29 trait groups that seem to be uniquely related to insect invasion and have no clear analogue to plant traits. These trait groups involved both life history and the environment. This result suggests that a pest risk assessment developed for plant invasion may not be applicable for insects because traits that are important to insect invasion may be missing from the assessment. We next examine these unique insect life history and environmental trait groups in further detail.

Sex ratio: In sexually reproducing species, the intrinsic rate of population increase is generally limited by the number of females rather than the number of males. For example, sex ratio, specifically female dominance, can increase the successful establishment of biological control agents such as Harmonia axyridis (Asian lady beetle; Michaud 2002, Kimberling 2004). Harmonia axyridis has a female-skewed sex ratio that may give it intrinsic advantages over the native Cycloneda sanguinea (spotless lady beetle; Michaud 2002). A female-skewed sex ratio can compound the effect of high per capita fecundity, leading to explosive population growth, by which such invasive species may outcompete native species, or escape control by natural enemies. Aspects of plant reproduction are considered in the AWRA, such as self-fertilization and viable seed production, which may be distantly analogous to sex ratio in insects.

Oviposition site: According to Kimberling (2004), oviposition site can influence the establishment of alien insects whereby those who oviposit on or inside the host are more likely to establish. Although Kimberling does not discuss the reasoning for this association, we assume that larvae are not required to find a host upon hatching, so that individuals are more likely to achieve their developmental requirements. By contrast, eggs that are deposited elsewhere would be more susceptible to damage and death before finding a suitable host, and individuals would be less likely to complete development. Although seed dispersal mechanisms are considered in the AWRA, oviposition site is not included because it is not relevant to plants.

Intraguild predation: Organisms that kill potential competitors within their feeding guild are referred to as intraguild predators. For example, the invasive H. axyridis is more likely than the native Coccinella septempunctata (seven-spot ladybird) to consume the cadavers of Pandora neoaphidis fungus-infected aphids (Roy et al. 2008a), a form of intraguild predation. Although study of other members of the aphidophagous and coccidophagous guilds is lacking, evidence indicates that H. axyridis may affect the population of P. neoaphidis more negatively than would C. septempunctata, leading to a greater competitive advantage for H. axyridis. In addition, H. axyridis will consume more heterospecific eggs (i.e., Adalia bipunctata eggs) than the native A. bipunctata will consume H. axyridis eggs (Ware et al. 2009). This also indicates a competitive advantage for the invasive insect over the native.

Resistance evolution: Because insecticides are commonly used to control invasive insects, the evolution of pesticide resistance would benefit species that are capable of evolving rapidly (Crowder et al. 2010). This trait has been recognized in the invasive biotype of the cryptic Bemisa tabaci (whitefly) species complex, which was able to displace other whiteflies competitively through adaptation to an insecticide (Crowder et al. 2010). The AWRA does not explicitly consider whether a plant is able to evolve resistance to herbicides; however, the trait well controlled by herbicides is included as a persistence attribute. Although it is possible that a plant will evolve resistance to an herbicide, a plant may resist control by an herbicide due to the specific mode of action; therefore, although these two traits may seem similar (resistance evolution and well controlled by herbicides), we consider them as different.

Biotic resistance: Native species richness can affect the extent to which biological invasions are likely to occur such that environments with greater species richness are often less easily invaded (Byers and Noonburg 2003). Although this may be a scale-dependent effect with multiple contributing factors such as disturbance, propagule pressure, and environmental stress (Byers and Noonburg 2003), environments with high biotic resistance by native fauna (i.e. areas with an abundance of similar species or containing competitors and predators) may provide protection against foreign invaders. For example, certain native ant species provide biotic resistance against the invasion of Linepithema humile (Argentine ant; Blight et al. 2010, Roura-Pascuala et al. 2011). Although there is evidence for biotic resistance against invading plants (Maron and Vila 2001), it is possible that this trait is not included in the AWRA because it could be a difficult parameter to measure. Biotic resistance may also be correlated to plant invasion through other explicit traits and therefore not warranted for inclusion in the AWRA. For example, at large scales, native and exotic plant diversity are positively related because they are driven by factors related to spatial heterogeneity (e.g. differences in soil measures such as soil depth and nitrogen; Davies et al. 2005).

Foraging: There is considerable diversity in the foraging abilities and behaviours of insects that affect their invasive potential. The foraging trait group includes the traits: search efficiency, foraging rate, bait recruitment, foraging behaviour, predatory efficiency, and foraging distance (Table 2). For example, invasive ants are able to dominate native communities with respect to the rate and efficiency with which they forage, which may alter the food web structure in their favour (Human and Gordon 1996, Holway 1998, Holway 1999, Gamboa et al. 2002, Ings et al. 2006, Dejean et al. 2007, Rowles and O’Dowd 2007, McGrannachan and Lester 2013). Invasive ants have been found to forage at times of the year when native ants do not (Wuellner and Saunder 2003), and invasive wasps exhibit flexible foraging behaviour (Wilson-Rankin 2014). Overall, these traits imply dominance over the native community with respect to resource acquisition and may be important in invasion success. Although plants do not actively forage or recruit to bait, the AWRA does consider whether a plant is able to grow on infertile soils or fix nitrogen; these characteristics relate to the ability of the plant to acquire water and nutrients from the soil, which is related to but different from foraging behaviour in insects (but see e.g. Sutherland and Stillman 1988 for an alternative perspective).

Colony characteristics: Invasive ants (Holway et al. 2002), bees (Goulson et al. 2003), and wasps (Beggs et al. 2011) are some of the most widely studied invasive insects, and thus, many characteristics of social insect colonies are claimed to affect invasion potential. Traits included in this category are: greater colony productivity and longevity, decreased relatedness to queen, polygyne social form, sociality, unicoloniality, and recognition cues (Table 2). These traits are associated with colony structure. Certain traits lead to a competitive advantage for invasive insects; in general, large, unicolonial forms confer invasiveness in social insects by increasing the rates of colony growth and spread (Moller 1996, Tsusui and Suarez 2003). Loss of genetic diversity (Tsusui and Suarez 2003, Suarez et al. 2008, Ugelvig and Cremer 2012) and shifts in colony structure (Wilson et al. 2009) are also related to sustained rapid growth and dispersal of invasive social insects. This is thought to be the case because large supercolonies can be formed from many genetically similar individuals, making the colony more successful. It may be the case that plant coloniality (selfing, reproducing by extensive rhizomes) plays a similar role, although the mechanisms differ.

Foundress activity: Female founders (foundresses) can exemplify different behaviours within the colony. Armstrong and Stamp (2003) found that certain foundress activity (higher aggression towards offspring and higher nest repairing tendency) is related to invasiveness in Polistes dominulus (European paper wasp) as compared to the native P. fuscatus (northern paper wasp). It is unclear whether the aggression of P. dominulus foundresses leads to higher colony productivity, but the tendency of P. dominulus to be more opportunistic may increase its success as an invasive species (Armstrong and Stamp 2003). Prior to Armstrong and Stamp’s (2003) work, it was thought that greater foundress activity would increase foraging behaviour of the workers (Reeve and Gamboa 1987), leading to higher productivity, and thus invasive potential.

Aggression: Aggression is thought to be related to insect invasiveness because it may lead to large, ecologically dominating supercolonies (Suhr et al. 2011). Individuals can display inter- and/or intraspecific aggression, which can lead to differences in colony structure between native and invasive insects. For ants and termites, invasive species tend to have lower intraspecific aggression than native species (Holway et al. 1998, Suarez et al. 1999, Le Breton et al. 2004, Errard et al. 2005, Cremer et al. 2008, Fournier et al. 2009, Perdereau et al. 2011, Suhr et al. 2011, Ugelvig and Cremer 2012, Hoffmann 2014), suggesting that multiple invasive colonies may behave as a supercolony (Suhr et al. 2011). Interspecific aggression is also exhibited in invasive ants and Ceratitis catoirii (Mascarenes fruit fly; Human and Gordon 1999, Cremer et al. 2006, Duyck et al. 2006, Snyder and Evans 2006, Rowles and O’Dowd 2007, Carpintero and Reyes-Lopez 2008, Fournier et al. 2009, Blight et al. 2010, Perdereau et al. 2011). Low intraspecific aggression combined with high interspecific aggression can lead to ecological dominance of the invasive species while allowing individuals of the same species to amalgamate, possibly behaving as a supercolony (Suhr et al. 2011). Aggression may therefore be important in evaluating the potential invasiveness of certain insects and is easily measured between individuals (inter- or intraspecific) using a standard 1-1 assay (Holway et al. 1998).

Queen characteristics: Like colony characteristics, this category includes queen traits related to invasiveness: greater queen number and greater queen longevity. For example, an invasive colony of insects likely contains more queens (Ross et al. 1996, Tsusui and Suarez 2003, Abril et al. 2013), and these queens live longer (Gamboa et al. 2002) than do queens of native species. These invasive characteristics can lead to higher sustained progeny production and thus greater colony growth (Tsusui and Suarez 2003).

Nesting: The habitat used by nesting insects (Suarez et al. 2005, Downing et al. 2012), tendency of the nest to be predated (as a result of mimicry or habitat selection; Cervo et al. 2000), re-nesting after predation (Gamboa et al. 2004), and general nest reuse (Cervo et al. 2000) have all been claimed to be related to insect invasion in different ways. Invasive ants tend to be ground nesters rather than arboreal (Suarez et al. 2005), and invasive wasps tend to nest in urban rather than rural or natural habitats (Downing et al. 2012). Invasive ants and wasps may exploit nest resources not used by their native counterparts (Suarez et al. 2005), leading to their successful establishment. Invasive wasps also tend to encounter less nest predation as a result of their nest location choice (Cervo et al. 2000), and in the case of predation, are more likely to re-nest (Gamboa et al. 2004). Reuse of previous nests is also apparent in invasive wasps, conserving resources and saving time for foundresses (Cervo et al. 2000). These factors lead to a greater probability of establishment, and subsequently invasion, of these species by securing their persistence.

Many of the behavioural traits that are unique to insect invasion are also unique to social insects, which tend to dominate the insect invasion literature (e.g., Holway et al. 2002, Goulson et al. 2003, Kenis et al. 2009, Beggs et al. 2011). Social insects generally possess a suite of traits inherent to their lifestyle that also aids in the invasion process. As discussed above, certain ant species form supercolonies with genetically similar individuals, and these colonies may contain many reproductive females. This state, combined with high aggression, could allow the colony to dominate native species, further amplifying other traits that are important to invasion success, such as reproduction and development. It is likely that understanding insect social form is critically important in determining the invasive potential of that insect, and therefore must be included in a risk assessment scheme. Because non-social invasive insects tend to be studied less often, there may be other behavioural traits that are important to invasion that are yet to be identified. These traits could be important for the predictive ability of a risk assessment scheme, but would possibly not be comparable to traits found in the AWRA.

Unique invasiveness traits of plants

Just as there are unique traits relating to invasion of insects, mainly relating to social behaviour, there are also a number of traits that are considered to be indicative of weediness in plants that do not generalize to insects. In total, 21 questions in the AWRA are not applicable to insects (Tables 3 and 4). Much of the discrepancy is found in the first four subsections of the AWRA.

Subsection one (three questions) of the AWRA deals with the domestication or cultivation of introduced plants. These questions refer to cases in which plants that have been introduced for horticultural or agricultural purposes, for example, escape cultivation, become naturalized, and then invasive. By contrast, invasive insects have rarely been introduced intentionally, with the exception of biocontrol agents that have become invasive, and so this would not apply to an insect model.

Subsection two (five questions) outlines climate and distribution. Environmental matching was identified as important for insect invasion (Table 2); however, the five questions in the AWRA are specific to Australian climatic conditions and should be modified for the specific region of interest (for example, Pheloung et al. 1999 modified the AWRA for use in New Zealand). Also, more environmental matching traits relating to abiotic factors were identified for insects than are included in the AWRA. This subsection would likely have to be expanded to apply appropriately to insects.

Subsection three (five questions) contains questions about the weediness of the plant elsewhere. This relates to the notion that success elsewhere can be a predictor of future invasiveness in areas with similar environmental conditions (Panetta and Mitchell 1991). It could also mean that the plant may have an increased probability of escape and spread because it is already naturalized. Whether an insect has been naturalized elsewhere may help to predict future invasiveness as certain species have been found to invade multiple areas (Samways 1999), but this was not identified as important for insect invasiveness in our search of the literature.

Subsection four (12 questions) lists undesirable physical and chemical traits of plants such as whether they produce thorns, spines, burrs, or toxic compounds. Many of these traits do not apply to insects because of their biology. Although it may be possible for an insect to possess mechanical/chemical defenses such as stinging or venom, these are not traits that are currently thought to be important for their invasion success, although they may be related to the ecological impact of the species, and thus would likely not be useful to include in an insect pest risk assessment.

Conclusion

Our systematic review of the invasion literature demonstrates that there are a number of differences in the traits that are claimed to be important for invasion in plants and insects. Species invasion is a complex process that involves both the invading species and its interaction with the biological and physical environment (Hayes and Barry 2008). Using insects as a case study, we have illustrated that expanding a pest risk assessment scheme originally developed for plants (such as the AWRA) may not appropriately capture the potential for invasiveness in other taxa because there are likely to be key differences in both the traits related to invasive behaviour and the importance of these traits. Given that this is the case for insects, it may also be the case for other important invasive taxa such as fish and mammals. Although invasive traits have been identified for plants and validated for a variety of regions (Gordon et al. 2008), consistent correlates of invasion success have yet to be comprehensively assessed across taxa (Hayes and Barry 2008).

Although our analysis identified a number of similar invasion traits for plants and insects, these traits may not carry the same importance in both taxa. For example, we identified many developmental traits that were claimed to be important to the invasion success of insects, while in the AWRA, few questions relate to the development of plants. Whether development, or any other trait, is more predictive of invasion in insects compared to plants would therefore have to be tested.

Furthermore, there are also traits that are unique to plants, as well as traits that are unique to insects. Therefore, the strength and predictive ability of an assessment scheme may be compromised by adapting an assessment for plants to other taxa without comprehensive validation and verification. For example, Coop et al. (2009) were required to further calibrate an invasion screening tool that was adapted from the AWRA to be used on fish. Many of the unique insect invasion-related traits identified were behavioural and were examined in social insects only. Many of these behavioural traits do not transfer directly to plants, but more importantly, non-social insects are largely absent from the insect invasion literature. It is unclear if additional or different traits might also be important to the invasion of non-social insects. The inclusion of behavioural traits may add to the predictive power of an insect risk assessment scheme, and more generally, this highlights a need for further research into invasion-related traits of non-social insects.

A reliable risk assessment scheme must reflect which traits are most strongly indicative of invasiveness for a given taxon. For a rapid risk assessment tool to be useful, consideration must also be given to understanding which traits are easily measured or commonly available in the scientific literature. For example, many of the suggested insect traits (Table 2) may be related to invasiveness but may be difficult to evaluate, especially for insects that are not well studied. The presence of many unanswered questions in any rapid risk assessment tool can compromise its validity and usefulness. Thus, the trade-off between simplicity and accuracy would also require assessment.

Future research development should aim to rate the importance and weight of specific traits related to invasion in taxonomic groups other than plants to develop comprehensive pest risk assessment tools for other taxa. Currently, we are evaluating which traits are predictive of invasiveness in insects as a first step towards the development of such a tool for insects. Although in this analysis we found that 29 traits are related to invasion in insects, further analysis will inform which of these traits are most important in insect invasion. This approach will consolidate the trade-off between the most indicative and readily available trait information to produce a rapid and efficient design. From this we will know whether differences in invasive traits between taxa require that new risk assessment tools be created for other taxa, or if the approach taken thus far (i.e. making general risk assessments for all non-native taxa) is sufficient.

Acknowledgements

The authors thank the Editor (Alain Roques), and Robert Haack, Marc Kenis, and an anonymous third referee for helpful comments and suggestions. Funding for this research was provided by the Ontario Ministry of Agriculture, Food and Rural Affairs through a grant to HAH and JAN and a HQP scholarship to LME.

References

  • Allen GR, Seeman OD, Schmid-Hempel P, Buttermore RE (2007) Low parasite loads accompany the invading population of the bumblebee, Bombus terrestris in Tasmania. Insectes Sociaux 54: 56–63. doi: 10.1007/s00040-007-0908-y
  • Andersen HF, Jordal BH, Kambestad M, Kirkendall LR (2012) Improbable but true: the invasive inbreeding ambrosia beetle Xylosandrus morigerus has generalist genotypes. Ecology and Evolution 2: 247–257. doi: 10.1002/ece3.58
  • Armstrong TR, Stamp NE (2003) Colony productivity and foundress behaviour of a native wasp versus an invasive social wasp. Ecological Entomology 28: 635–644. doi: 10.1111/j.1365-2311.2003.00564.x
  • Arndt E, Perner J (2008) Invasion patterns of ground-dwelling arthropods in Canadian laurel forests. Acta Oecologica 34: 202–213. doi: 10.1016/j.actao.2008.05.005
  • Baker RH, Black A, Copp R, Haysom GH, Hulme KA, Thomas PE, Brown MB, Brown A, Cannon M, Ellis RJC, Ellis J, Ferris M, Glaves R, Gozlan P, Holt RE, Howe J, Knight L, MacLeod JD, Moore A, Mumford NP, Murphy JD, Parrott ST, Sansford D, Smith CE, St-Hilaire S, Ward NL (2008) The UK risk assessment scheme for all non-native species. Neobiota 7: 46–57.
  • Beggs JR, Brockerhoff EG, Corley JC, Kenis M, Masciocchi M, Muller F, Rome Q, Villemant C (2011) Ecological effects and management of invasive alien Vespidae. BioControl 56: 505–526. doi: 10.1007/s10526-011-9389-z
  • Beilhe LB, Arnoux S, Delatte H, Lajoie G, Fontenille D (2012) Spread of invasive Aedes albopictus and decline of resident Aedes aegypti in urban areas of Mayotte 2007–2010. Biological Invasions 14: 1623–1633. doi: 10.1007/s10530-012-0177-1
  • Beilhe LB, Delatte H, Juliano SA, Fontenille D, Quilici S (2013) Ecological interactions in Aedes species on Reunion Island. Medical and Veterinary Entomology 27: 387–397. doi: 10.1111/j.1365-2915.2012.01062.x
  • Beirne BP (1975) Biological control attempts by introductions against pest insects in the field in Canada. The Canadian Entomologist 107: 225–236. doi: 10.4039/Ent107225-3
  • Blight O, Provost E, Renucci M, Tirard A, Orgeas J (2010) A native ant armed to limit the spread of the Argentine ant. Biological Invasions 12: 3785–3793. doi: 10.1007/s10530-010-9770-3
  • Boivin T, Rouault G, Chalon A, Candau JN (2008) Differences in life history strategies between an invasive and a competing resident seed predator. Biological Invasions 10: 1013–1025. doi: 10.1007/s10530-007-9180-3
  • Bolger DT (2007) Spatial and temporal variation in the Argentine ant edge effect: implications for the mechanism of edge limitation. Biological Conservation 136: 295–305. doi: 10.1016/j.biocon.2006.12.002
  • Boman S, Grapputo A, Lindström L, Lyytinen A, Mappes J (2008) Quantitative genetic approach for assessing invasiveness: Geographic and genetic variation in life-history traits. Biological Invasions 10: 1135–1145. doi: 10.1007/s10530-007-9191-0
  • Bonato O, Lurette A, Vidal C, Fargues J (2007) Modelling temperature‐dependent bionomics of Bemisia tabaci (Q‐biotype). Physiological Entomology 32: 50–55. doi: 10.1111/j.1365-3032.2006.00540.x
  • Brandt M, Van Wilgenburg E, Tsutsui ND (2009) Global‐scale analyses of chemical ecology and population genetics in the invasive Argentine ant. Molecular Ecology 18: 997–1005. doi: 10.1111/j.1365-294X.2008.04056.x
  • Brooks CP, Ervin GN, Varone L, Logarzo GA (2012) Native ecotypic variation and the role of host identity in the spread of an invasive herbivore, Cactoblastis cactorum. Ecology 93: 402–410. doi: 10.1890/11-0541.1
  • Byers JE (2003) Scale dependent effects of biotic resistance to biological invasion. Ecology 84: 1428–1433. doi: 10.1890/02-3131
  • Caron V, Norgate M, Ede FJ, Nyman T, Sunnucks P (2013) Novel microsatellite DNA markers indicate strict parthenogenesis and few genotypes in the invasive willow sawfly Nematus oligospilus. Bulletin of Entomological Research 103: 74–88. doi: 10.1017/S0007485312000429
  • Carpintero S, Reyes-López J (2008) The role of competitive dominance in the invasive ability of the Argentine ant (Linepithema humile). Biological Invasions 10: 25–35. doi: 10.1007/s10530-007-9103-3
  • Causton CE, Peck SB, Sinclair BJ, Roque-Albelo L, Hodgson CJ, Landry B (2006) Alien Insects: Threats and implications for conservation of Galápagos Islands. Annals of the Entomological Society of America 99: 121–143. doi: 10.1603/0013-8746(2006)099[0121:AITAIF]2.0.CO;2
  • Cervo R, Zacchi F, Turillazzi S (2000) Polistes dominulus (Hymenoptera, Vespidae) invading North America: some hypotheses for its rapid spread. Insectes Sociaux 47: 155–157. doi: 10.1007/PL00001694
  • Colautti RI, Bailey SA, van Overdijk CDA, Amundsen K, MacIsaac HJ (2006) Characterised and projected costs of nonindigenous species in Canada. Biological Invasions 8: 45–59. doi: 10.1007/s10530-005-0236-y
  • Comont RF, Purse BV, Phillips W, Kunin WE, Hanson M, Lewis OT, Harrington R, Shortall CR, Rondoni G, Roy HE (2014) Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conservation and Diversity 7: 334–342. doi: 10.1111/icad.12060
  • Copp GH, Britton JR, Cowx IG, Jeney G, Joly JP, Gherardi F, Gollasch S, Gozlan RE, Jones G, MacLeod A, Midtlyng PJ, Miossec L, Nunn AD, Occhipinti-Ambrogi A, Oidtmann B, Olenin S, Peeler E, Russell IC, Savini D, Tricarico C, Thrush M (2008) Risk assessment protocols and decision making tools for use of alien species in aquaculture and stock enhancement. EU Co-ordination Action Project: IMPASSE Environmental impacts of alien species in aquaculture, Deliverable report, 3.
  • Copp GH, Garthwaite R, Gozlan RE (2005) Risk identification and assessment of non-native freshwater fishes: a summary of concepts and perspectives on protocols for the UK. Journal of Applied Ichthyology 21: 371–373. doi: 10.1111/j.1439-0426.2005.00692.x
  • Cottrell TE, Shapiro-Ilan DI (2003) Susceptibility of a native and an exotic lady beetle (Coleoptera: Coccinellidae) to Beauveria bassiana. Journal of Invertebrate Pathology 84: 137–144. doi: 10.1016/j.jip.2003.09.003
  • Crawley MJ (1987) What makes a community invasible? In: Gray AJ, Crawley MJ, Edwards PJ (Eds) Colonization, Succession and Stability. Blackwell Scientific Publications, Oxford, 429–453.
  • Cremer S, Ugelvig LV, Drijfhout FP, Schlick-Steiner BC, Steiner FM, Seifert B, Hughes DP, Schulz A, Petersen KS, Konrad H, Stauffer C, Kiran K, Espadaler X, d’Ettorre P, Aktac N, Eilenberg J, Jones GR, Nash DR, Pedersen JS, Boomsma JJ (2008) The evolution of invasiveness in garden ants. PLoS ONE 3: e3838. doi: 10.1371/journal.pone.0003838
  • Cremer S, Ugelvig LV, Lommen STE, Petersen KS, Pedersen JS (2006) Attack of the invasive garden ant: aggression behaviour of Lasius neglectus (Hymenoptera: Formicidae) against native Lasius species in Spain. Myrmecologische Nachrichten 9: 13–19.
  • Crowder DW, Horowitz AR, De Barro PJ, Liu SS, Showalter AM, Kontsedalov S, Khasdan V, Shargal A, Liu J, Carrière Y (2010) Mating behaviour, life history and adaptation to insecticides determine species exclusion between whiteflies. Journal of Animal Ecology 79: 563–570. doi: 10.1111/j.1365-2656.2010.01666.x
  • Curtis TR, Aponte Y, Stamp NE (2005) Nest paper absorbency, toughness, and protein concentration of a native vs. an invasive social wasp. Journal of Chemical Ecology 31: 1089–1100. doi: 10.1007/s10886-005-4249-x
  • Daehler CC, Carino DA (2000) Predicting invasive plants: prospects for a general screening system based on current regional models. Biological Invasions 2: 93–102. doi: 10.1023/A:1010002005024
  • Davies KF, Chesson P, Harrison S, Inouye BD, Melbourne BA (2005) Spatial heterogeneity explains the scale dependence of the native-exotic diversity relationship. Ecology 86: 1602–1610. doi: 10.1890/04-1196
  • De Barro P, Bourne A (2010) Ovipositional host choice by an invader accelerates displacement of its indigenous competitor. Biological Invasions 12: 3013–3023. doi: 10.1007/s10530-010-9691-1
  • Dejean A, Kenne M, Moreau CS (2007) Predatory abilities favour the success of the invasive ant Pheidole megacephala in an introduced area. Journal of Applied Entomology 131: 625–629. doi: 10.1111/j.1439-0418.2007.01223.x
  • Delatte H, Duyck PF, Triboire A, David P, Becker N, Bonato O, Reynaud B (2009) Differential invasion success among biotypes: case of Bemisia tabaci. Biological Invasions 11: 1059–1070. doi: 10.1007/s10530-008-9328-9
  • Didham RK, Tylianakis JM, Hutchinson MA, Ewers RM, Gemmell NJ (2005) Are invasive species the drivers of ecological change? Trends in Ecology and Evolution 20: 470–474. doi: 10.1016/j.tree.2005.07.006
  • Downing H (2012) Nest parameters of Polistes and Mischocyttarus species (Hymenoptera: Vespidae) before and after detection of the invasive wasp, Polistes dominula in western South Dakota and Wyoming. Journal of the Kansas Entomological Society 85: 23–31. doi: 10.2317/JKES111011.1
  • Duyck PF, David P, Junod G, Brunel C, Dupont R, Quilici S (2006) Importance of competition mechanisms in successive invasions by poluphagous tephritids in La Reunion. Ecology 87: 1770–1780. doi: 10.1890/0012-9658(2006)87[1770:IOCMIS]2.0.CO;2
  • Duyck PF, David P, Quilici S (2007) Can more K‐selected species be better invaders? A case study of fruit flies in La Réunion. Diversity and Distributions 13: 535–543. doi: 10.1111/j.1472-4642.2007.00360.x
  • Engelkes T, Mills NJ (2011) A conceptual framework for understanding arthropod predator and parasitoid invasions. BioControl 56: 383–393. doi: 10.1007/s10526-011-9377-3
  • Errard C, Delabie J, Jourdan H, Hefetz A (2005) Intercontinental chemical variation in the invasive ant Wasmannia auropunctata (Roger) (Hymenoptera Formicidae): a key to the invasive success of a tramp species. Naturwissenschaften 92: 319–323. doi: 10.1007/s00114-005-0628-y
  • Facon B, Hufbauer RA, Tayeh A, Loiseau A, Lombaert E, Vitalis R, Guillemaud T, Lundgren JG, Estoup A (2011) Inbreeding depression is purged in the invasive insect Harmonia axyridis. Current Biology 21: 424–427. doi: 10.1016/j.cub.2011.01.068
  • Fitzgerald K, Gordon DM (2012) Effects of vegetation cover, presence of a native ant species, and human disturbance on colonization by Argentine ants. Conservation Biology 26: 525–538. doi: 10.1111/j.1523-1739.2012.01836.x
  • Foucaud J, Rey O, Robert S, Crespin L, Orivel J, Facon B, Loiseau A, Jourdan H, Kenne M, Masse PSM, Tindo M, Vonshak M, Estoup A (2013) Thermotolerance adaptation to human‐modified habitats occurs in the native range of the invasive ant Wasmannia auropunctata before long‐distance dispersal. Evolutionary Applications 6: 721–734. doi: 10.1111/eva.12058
  • Fournier D, de Biseau JC, Aron S (2009) Genetics, behaviour and chemical recognition of the invading ant Pheidole megacephala. Molecular Ecology 18: 186–199. doi: 10.1111/j.1365-294X.2008.04018.x
  • Gamboa GJ, Greig EI, Thom MC (2002) The comparative biology of two sympatric paper wasps, the native Polistes fuscatus and the invasive Polistes dominulus (Hymenoptera, Vespidae). Insectes Sociaux 49: 45–49. doi: 10.1007/s00040-002-8278-y
  • Gamboa GJ, Noble MA, Thom MC, Togal JL, Srinivasan R, Murphy BD (2004) The comparative biology of two sympatric paper wasps in Michigan, the native Polistes fuscatus and the invasive Polistes dominulus (Hymenoptera, Vespidae). Insectes Sociaux 51: 153–157. doi: 10.1007/s00040-003-0721-1
  • Gordon DR, Onderdonk DA, Fox AM, Stocker RK (2008) Consistent accuracy of the Australian weed risk assessment system across varied geographies. Diversity and Distributions 14: 234–242. doi: 10.1111/j.1472-4642.2007.00460.x
  • Gray RH, Lorimer CG, Tobin PC, Raffa KF (2008) Preoutbreak dynamics of a recently established invasive herbivore: roles of natural enemies and habitat structure in stage-specific performance of gypsy moth (Lepidoptera: Lymantriidae) populations in northeastern Wisconsin. Environmental Entomology 37: 1174–1184. doi: 10.1093/ee/37.5.1174
  • Graziosi I, Rieske LK (2012) Local spread of an exotic invader: using remote sensing and spatial analysis to document proliferation of the invasive Asian chestnut gall wasp. In V International Chestnut Symposium 1019: 113–118. doi: 10.3832/ifor0633-005
  • Grevstad FS (1999) Experimental invasions using biological control introductions: the influence of release size on the chance of population establishment. Biological Invasions 1: 313–323. doi: 10.1023/A:1010037912369
  • Haack RA, Lawrence RK (1995) Attack densities of Tomicus piniperda and Ips pini (Coleoptera: Scolytidae) on Scotch pine logs in Michigan in relation to felling date. Journal of Entomological Science 30: 18–28.
  • Harcourt DG, Guppy JC, Meloche F (1988) Population dynamics of the Alfalfa blotch leafminer Agromyza frontella (Diptera: Agromyzidae) in eastern Ontario: Impact of the exotic parasite Dacnusa dryas (Hymenoptera: Braconidae). Environmental Entomology 17: 337–343. doi: 10.1093/ee/17.2.337
  • Hayes KR, Barry SC (2008) Are there any consistent predictors of invasion success? Biological Invasions 10: 483–506. doi: 10.1007/s10530-007-9146-5
  • Hight SD, Blossey B, Laing J, Declerck-Floate R (1995) Establishment of insect biological control agents from Europe against Lythrum salicaria in North America. Environmental Entomology 24: 967–977. doi: 10.1093/ee/24.4.967
  • Hill MP, Chown SL, Hoffmann AA (2013) A predicted niche shift corresponds with increased thermal resistance in an invasive mite, Halotydeus destructor. Global Ecology and Biogeography 22: 942–951. doi: 10.1111/geb.12059
  • Hoffmann BD (2014) Quantification of supercolonial traits in the yellow crazy ant, Anoplolepis gracilipes. Journal of Insect Science 14: 1–21. doi: 10.1673/031.014.25
  • Hogg BN, Daane KM (2013) Contrasting landscape effects on species diversity and invasion success within a predator community. Diversity and Distributions 19: 281–293. doi: 10.1111/j.1472-4642.2012.00935.x
  • Holway DA (1998) Factors governing rate of invasion: A natural experiment using Argentine ants. Oecologia 115: 206–212. doi: 10.1007/s004420050509
  • Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282: 949–952. doi: 10.1126/science.282.5390.949
  • Hopper KR, Roush RT (1993) Mate finding, dispersal, number released, and the success of biological control introductions. Ecological Entomology 18: 321–331. doi: 10.1111/j.1365-2311.1993.tb01108.x
  • Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105: 405–412. doi: 10.1007/BF00328744
  • Human KG, Gordon DM (1999) Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Sociaux 46: 159–163. doi: 10.1007/s000400050127
  • Human KG, Weiss S, Weiss A, Sandler B, Gordon DM (1998) Effects of abiotic factors on the distribution and activity of the invasive Argentine ant (Hymenoptera: Formicidae). Environmental Entomology 27: 822–833. doi: 10.1093/ee/27.4.822
  • Ings TC, Ward NL, Chittka L (2006) Can commercially imported bumble bees out‐compete their native conspecifics? Journal of Applied Ecology 43: 940–948. doi: 10.1111/j.1365-2664.2006.01199.x
  • Inoue MN (2011) Size‐dependent selection against small queens of the invasive bumblebee Bombus terrestris in Japan. Entomologia Experimentalis et Applicata 138: 65–70. doi: 10.1111/j.1570-7458.2010.01075.x
  • Ishii HS, Kadoya T, Kikuchi R, Suda SI, Washitani I (2008) Habitat and flower resource partitioning by an exotic and three native bumble bees in central Hokkaido, Japan. Biological Conservation 141: 2597–2607. doi: 10.1016/j.biocon.2008.07.029
  • Janion C, Leinaas HP, Terblanche JS, Chown SL (2010) Trait means and reaction norms: the consequences of climate change/invasion interactions at the organism level. Evolutionary Ecology 24: 1365–1380. doi: 10.1007/s10682-010-9405-2
  • Jarošík V, Kenis M, Honěk A, Skuhrovec J, Pyšek P (2015) Invasive insects differ from non-invasive in their thermal requirements. PLoS ONE 10(6): e0131072. doi: 10.1371/journal.pone.0131072
  • Jones CM, Brown MJ (2014) Parasites and genetic diversity in an invasive bumblebee. Journal of Animal Ecology 83: 1428–1440. doi: 10.1111/1365-2656.12235
  • Ju RT, Gao L, Zhou XH, Li B (2013) Tolerance to high temperature extremes in an invasive lace bug, Corythucha ciliata (Hemiptera: Tingidae), in subtropical China. PLoS ONE 8: e54372. doi: 10.1371/journal.pone.0054372
  • Juliano SA, Lounibos LP, Nishimura N, Greene K (2010) Your worst enemy could be your best friend: predator contributions to invasion resistance and persistence of natives. Oecologia 162: 709–718. doi: 10.1007/s00442-009-1475-x
  • Kajita Y, Evans EW (2010) Relationships of body size, fecundity, and invasion success among predatory lady beetles (Coleoptera: Coccinellidae) inhabiting alfalfa fields. Annals of the Entomological Society of America 103: 750–756. doi: 10.1603/AN10071
  • Kajita Y, Evans EW (2010b) Alfalfa fields promote high reproductive rate of an invasive predatory lady beetle. Biological Invasions 12: 2293–2302. doi: 10.1007/s10530-009-9644-8
  • Kasper ML, Reeson AF, Cooper SJ, Perry KD, Austin AD (2004) Assessment of prey overlap between a native (Polistes humilis) and an introduced (Vespula germanica) social wasp using morphology and phylogenetic analyses of 16S rDNA. Molecular Ecology 13: 2037–2048. doi: 10.1111/j.1365-294X.2004.02193.x
  • Kato H, Hata K, Yamamoto H, Yoshioka T (2006) Effectiveness of the weed risk assessment system for the Bonin Islands. In: Koike F, Clout MN, Kawamichi M, De Poorter M, Iwatsuki K (Eds) Assessment and Control of Biological Invasion Risk. Shoukadoh Book Sellers, Kyoto, 65–72.
  • Kenis M, Rabitsch W, Auger-Rozenberg MA, Roques A (2007) How can alien species inventories and interception data help us prevent insect invasions? Bulletin of Entomological Research 97: 489–502. doi: 10.1017/S0007485307005184
  • Kimberling DN (2004) Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control. Biological Invasions 6: 301–318. doi: 10.1023/B:BINV.0000034599.09281.58
  • Kleinteich A, Schneider JM (2011) Developmental strategies in an invasive spider: constraints and plasticity. Ecological Entomology 36: 82–93. doi: 10.1111/j.1365-2311.2010.01249.x
  • Kobelt M, Nentwig W (2008) Alien spider introductions to Europe supported by global trade. Diversity and Distributions 14: 273–280. doi: 10.1111/j.1472-4642.2007.00426.x
  • Koch RL, Venette RC, Hutchison WD (2006) Invasions by Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in the western hemisphere: Implications for South America. Neotropical Entomology 35: 421–434. doi: 10.1590/S1519-566X2006000400001
  • Kolar CS, Lodge DM (2002) Ecological predictions and risk assessment for alien fishes in North America. Science 298: 1233–1236. doi: 10.1126/science.1075753
  • Labrie G, Lucas E, Coderre D (2006) Can developmental and behavioral characteristics of the multicolored Asian lady beetle Harmonia axyridis explain its invasive success? Biological Invasions 8: 743–754. doi: 10.1007/s10530-005-3428-6
  • Laugier GJ, Le Moguédec G, Tayeh A, Loiseau A, Osawa N, Estoup A, Facon B (2013) Increase in male reproductive success and female reproductive investment in invasive populations of the harlequin ladybird Harmonia axyridis. PLoS ONE 8: e77083. doi: 10.1371/journal.pone.0077083
  • Lawton JH, Brown KC, Crawley MJ, Way MJ, Holdgate MW, May RM, Southwood R, O’Connor RJ (1986) The population and community ecology of invading insects [and discussion]. Philosophical Transactions of the Royal Society B: Biological Sciences 314: 607–617. doi: 10.1098/rstb.1986.0076
  • Le Breton J, Delabie JH, Chazeau J, Dejean A, Jourdan H (2004) Experimental evidence of large-scale unicoloniality in the tramp ant Wasmannia auropunctata (Roger). Journal of Insect Behavior 17: 263–271. doi: 10.1023/B:JOIR.0000028575.28700.71
  • LeBrun EG, Tillberg CV, Suarez AV, Folgarait PJ, Smith CR, Holway DA (2007) An experimental study of competition between fire ants and Argentine ants in their native range. Ecology 88: 63–75. doi: 10.1890/0012-9658(2007)88[63:AESOCB]2.0.CO;2
  • Lester PJ (2005) Determinants for the successful establishment of exotic ants in New Zealand. Diversity and Distributions 11: 279–288. doi: 10.1111/j.1366-9516.2005.00169.x
  • Liu SS, De Barro PJ, Jing X, Jun-Bo L, Zang LS, Yong-Ming R, Fang-Hao W (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318: 1769–1772. doi: 10.1126/science.1149887
  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. John Wiley & Sons.
  • Lombaert E, Estoup A, Facon B, Joubard B, Grégoire JC, Jannin A, Blin A, Guillemaud T (2014) Rapid increase in dispersal during range expansion in the invasive ladybird Harmonia axyridis. Journal of Evolutionary Biology 27: 508–517. doi: 10.1111/jeb.12316
  • Mack RN, Simberloff D, Londsale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: Causes, epidemiology, global consequences, and control. Ecological Applications 10: 689–710. doi: 10.1890/1051-0761(2000)010[0689:BICEGC]2.0.CO;2
  • Manfredini F, Grozinger CM, Beani L (2013) Examining the “evolution of increased competitive ability” hypothesis in response to parasites and pathogens in the invasive paper wasp Polistes dominula. Naturwissenschaften 100: 219–228. doi: 10.1007/s00114-013-1014-9
  • Marchetti MP, Moyle PB, Levine R (2004) Invasive species profiling? Exploring the characteristics of non‐native fishes across invasion stages in California. Freshwater Biology 49: 646–661. doi: 10.1111/j.1365-2427.2004.01202.x
  • Maron JL, Vila M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95: 361–373. doi: 10.1034/j.1600-0706.2001.950301.x
  • Matosevic D, Pajač Zivkovic I (2013) Foreign phytophagous species of insects and mites on woody plants in Croatia. Forestry 137: 191–203.
  • Mattson W, Vanhanen H, Veteli T, Sivonen S, Niemelä P (2007) Few immigrant phytophagous insects on woody plants in Europe: legacy of the European crucible? Biological Invasions 9: 957–974. doi: 10.1007/s10530-007-9096-y
  • McClay A, Sissons A, Wilson C, Davis S (2010) Evaluation of the Australian weed risk assessment system for the prediction of plant invasiveness in Canada. Biological Invasions 12: 4085–4098. doi: 10.1007/s10530-010-9819-3
  • McGlynn TP (1999) Non‐native ants are smaller than related native ants. The American Naturalist 154: 690–699. doi: 10.1086/303270
  • McGlynn TP (1999) The worldwide transfer of ants: geographical distribution and ecological invasions. Journal of Biogeography 26: 535–548. doi: 10.1046/j.1365-2699.1999.00310.x
  • McGrannachan CM, Lester PJ (2013) Temperature and starvation effects on food exploitation by Argentine ants and native ants in New Zealand. Journal of Applied Entomology 137: 550–559. doi: 10.1111/jen.12032
  • Memmott J, Craze PG, Harman HM, Syrett P, Fowler SV (2005) The effect of propagule size on the invasion of an alien insect. Journal of Animal Ecology 74: 50–62. doi: 10.1111/j.1365-2656.2004.00896.x
  • Memmott J, Fowler SV, Hill RL (1998) The effect of release size on the probability of establishment of biological control agents: Gorse thrips (Sericothrips staphylinus) released against gorse (Ulex europaeus) in New Zealand. Biocontrol Science and Technology 8: 103–115. doi: 10.1080/09583159830478
  • Michaud JP (2002) Invasion of the Florida citrus ecosystem by Harmonia axyridis (Coleoptera: Coccinellidae) and asymmetric competition with a native species, Cycloneda sanguinea. Environmental Entomology 31: 827–835. doi: 10.1603/0046-225X-31.5.827
  • Mikheyev AS, Bresson S, Conant P (2009) Single‐queen introductions characterize regional and local invasions by the facultatively clonal little fire ant Wasmannia auropunctata. Molecular Ecology 18: 2937–2944. doi: 10.1111/j.1365-294X.2009.04213.x
  • Mikheyev AS, Tchingnoumba L, Henderson A, Alonso A (2008) Effect of propagule pressure on the establishment and spread of the little fire ant Wasmannia auropunctata in a Gabonese oilfield. Diversity and Distributions 14: 301–306. doi: 10.1111/j.1472-4642.2007.00463.x
  • Moeser J, Vidal S (2005) Nutritional resources used by the invasive maize pest Diabrotica virgifera virgifera in its new south‐east‐European distribution range. Entomologia Experimentalis et Applicata 114: 55–63. doi: 10.1111/j.0013-8703.2005.00228.x
  • Mondor EB, Tremblay MN, Messing RH (2007) Morphological and ecological traits promoting aphid colonization of the Hawaiian Islands. Biological Invasions 9: 87–100. doi: 10.1007/s10530-006-9010-z
  • Myburgh M, Chown SL, Daniels SR, Van Vuuren BJ (2007) Population structure, propagule pressure, and conservation biogeography in the sub‐Antarctic: Lessons from indigenous and invasive springtails. Diversity and Distributions 13: 143–154. doi: 10.1111/j.1472-4642.2007.00319.x
  • Ness JH, Bronstein JL, Andersen AN, Holland JN (2004) Ant body size predicts dispersal distance of ant-adapted seeds: Implications of small-ant invasions. Ecology 85: 1244–1250. doi: 10.1890/03-0364
  • Niemelä J, Spence JR (1991) Distribution and abundance of an exotic ground-beetle (Carabidae): a test of community impact. Oikos 62: 351–359. doi: 10.2307/3545500
  • Orledge GM, Smith PA, Reynolds SE (2010) The non-pest Australasian fungivore Cis bilamellatus Wood (Coleoptera: Ciidae) in northern Europe: Spread dynamics, invasion success and ecological impact. Biological Invasions 12: 515–530. doi: 10.1007/s10530-009-9455-y
  • Panetta FD, Mitchell ND (1991) Bioclimatic prediction of the potential distributions of some weed species prohibited entry to New Zealand. New Zealand Journal of Agricultural Research 34: 341–350. doi: 10.1080/00288233.1991.10417674
  • Parkash R, Singh D, Lambhod C (2013) Divergent strategies for adaptations to stress resistance in two tropical Drosophila species: Effects of developmental acclimation for D. bipectinata and the invasive species D. malerkotliana. The Journal of Experimental Biology 217: 924–934. doi: 10.1242/jeb.096818
  • Paynter Q, Bellgard S (2011) Understanding dispersal rates of invading weed biocontrol agents. Journal of Applied Ecology 48: 407–414. doi: 10.1111/j.1365-2664.2010.01930.x
  • Peacock L, Worner SP (2008) Biological and ecological traits that assist establishment of alien invasive insects. New Zealand Plant Protection 61: 1–7. doi: 10.1111/j.1365-294X.2008.03949.x
  • Peccoud J, Figueroa CC, Silva AX, Ramirez CC, Mieuzet L, Bonhomme J, Stoeckel A, Plantegenest M, Simon JC (2008) Host range expansion of an introduced insect pest through multiple colonizations of specialized clones. Molecular Ecology 17: 4608–4618.
  • Perdereau E, Dedeine F, Christides JP, Dupont S, Bagneres AG (2011) Competition between invasive and indigenous species: an insular case study of subterranean termites. Biological Invasions 13: 1457–1470. doi: 10.1007/s10530-010-9906-5
  • Pheloung PC, Williams PA, Halloy SR (1999) A weed risk assessment model for use as a biosecurity tool evaluating plant introductions. Journal of Environmental Management 57: 239–251. doi: 10.1006/jema.1999.0297
  • Pickett KM, Wenzel JW (2000) High productivity in haplometrotic colonies of the introduced paper wasp Polistes dominulus (Hymenoptera: Vespidae; Polistinae). Journal of the New York Entomological Society 108: 314–325. doi: 10.1664/0028-7199(2000)108[0314:HPIHCO]2.0.CO;2
  • Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecological Economics 52: 273–288. doi: 10.1016/j.ecolecon.2004.10.002
  • Raak-van den Berg CL, Stam JM, De Jong PW, Hemerik L, Van Lenteren JC (2012) Winter survival of Harmonia axyridis in the Netherlands. Biological Control 60: 68–76. doi: 10.1016/j.biocontrol.2011.10.001
  • Rabitsch W (2010) Pathways and vectors of alien arthropods in Europe. Chapter 3. BioRisk 4: 27–43. doi: 10.3897/biorisk.4.60
  • Reeve HK, Gamboa GJ (1987) Queen regulation of worker foraging in paper wasps: a social feedback control system (Polistes fuscatus, Hymenoptera: Vespidae). Behaviour 102: 147–167. doi: 10.1163/156853986X00090
  • Reichard S, Hamilton W (1997) Predicting invasions of woody plants introduced into North America. Conservation Biology 11: 193–203. doi: 10.1046/j.1523-1739.1997.95473.x
  • Richardson DM, Pysek P, Rejmanek M, Barbour MG, Panetta FD, West CJ (2000b) Naturalization and invasion of alien plants: Concepts and definitions. Diversity and Distributions 6: 93–107. doi: 10.1046/j.1472-4642.2000.00083.x
  • Roques A, Kenis M, Lees D, Lopez-Vaamonde C, Rabitsch W, Rasplus J, Roy DB (2010) Alien terrestrial arthropods of Europe. BioRisk 4: 1–1028.
  • Ross KG, Vargo EL, Keller L (1996) Social evolution in a new environment: the case of introduced fire ants. Proceedings of the National Academy of Sciences Proceedings of the National Academy of Sciences of the United States of America 93: 3021–3025. doi: 10.1073/pnas.93.7.3021
  • Roura-Pascual N, Bas JM, Hui C (2010) The spread of the Argentine ant: environmental determinants and impacts on native ant communities. Biological Invasions 12: 2399–2412. doi: 10.1007/s10530-009-9650-x
  • Roura-Pascual N, Hui C, Ikeda T, Leday G, Richardson DM, Carpintero S, Espadaler X, Gómez C, Guénard B, Hartley S, Krushelnycky P, Lester PJ, McGeoch MA, Menke SB, Pedersen JS, Pitt JPW, Reyese J, Sanders JJ, Suarez AV, Touyama Y, Ward D, Ward PS, Worner SP (2011) Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader. Proceedings of the National Academy of Sciences of the United States of America 108: 220–225. doi: 10.1073/pnas.1011723108
  • Rowles AD, O’Dowd DJ (2007) Interference competition by Argentine ants displaces native ants: implications for biotic resistance to invasion. Biological Invasions 9: 73–85. doi: 10.1007/s10530-006-9009-5
  • Roy HE, Baverstock J, Ware RL, Clark SJ, Majerus MEN, Baverstock KE, Pell JK (2008a) Intraguild predation of the aphid pathogenic fungus Pandora neoaphidis by the invasive coccinellid Harmonia axyridis. Ecological Entomology 33: 175–182. doi: 10.1111/j.1365-2311.2007.00954.x
  • Roy HE, Brown PM, Rothery P, Ware RL, Majerus ME (2008b) Interactions between the fungal pathogen Beauveria bassiana and three species of coccinellid: Harmonia axyridis, Coccinella septempunctata and Adalia bipunctata. BioControl 53: 265–276. doi: 10.1007/s10526-007-9122-0
  • Sagata K, Lester PJ (2009) Behavioural plasticity associated with propagule size, resources, and the invasion success of the Argentine ant Linepithema humile. Journal of Applied Ecology 46: 19–27. doi: 10.1111/j.1365-2664.2008.01523.x
  • Sagoff M (2009) Environmental harm: Political not biological. Journal of Agricultural and Environmental Ethics 22: 81–88. doi: 10.1007/s10806-008-9127-4
  • Samways MJ (1999) Managing insect invasions by watching other countries. In: Sandlund OT, Schei PJ, Viken A (Eds) Invasive Species and Biodiversity Management. Kluwer Dordrecht, 295–304. doi: 10.1007/978-94-011-4523-7_20
  • Sanders NJ, Suarez AV (2011) Elton’s insights into the ecology of ant invasions: lessons learned and lessons still to be learned. In: Richardson DM (Ed.) Fifty Years of Invasion Ecology: The Legacy of Charles Elton. Wiley-Blackwell, Oxford, 239–251.
  • Sefrova H (2014) Introduced and invasive insect species in the Czech Republic and their economic and ecological impact (Insecta). Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 53: 151–158. doi: 10.11118/actaun200553050151
  • Simberloff D (1989) Which insect introductions succeed and which fail? In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M, Williamson M (Eds) Biological Invasions: a Global Perspective. John Wiley & Sons, New York, 61–75.
  • Slabber S, Worland MR, Leinaas HP, Chown SL (2007) Acclimation effects on thermal tolerances of springtails from sub-Antarctic Marion Island: Indigenous and invasive species. Journal of Insect Physiology 53: 113–125. doi: 10.1016/j.jinsphys.2006.10.010
  • Snyder WE, Clevenger GM, Eigenbrode SD (2004) Intraguild predation and successful invasion by introduced ladybird beetles. Oecologia 140: 559–565. doi: 10.1007/s00442-004-1612-5
  • Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annual Review of Ecology, Evolution, and Systematics 37: 95–122. doi: 10.1146/annurev.ecolsys.37.091305.110107
  • Suarez AV, Holway DA, Tsutsui ND (2008) Genetics and behavior of a colonizing species: The invasive Argentine ant. The American Naturalist 172: S72–S84. doi: 10.1086/588638
  • Suarez AV, Holway DA, Ward PS (2005) The role of opportunity in the unintentional introduction of nonnative ants. Proceedings of the National Academy of Sciences of the United States of America 102: 17032–17035. doi: 10.1073/pnas.0506119102
  • Suarez AV, Tsutsui ND, Holway DA (1999) Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biological Invasions 1: 43–53. doi: 10.1023/A:1010038413690
  • Suhr EL, O’Dowd DJ, McKechnie SW, Mackay DA (2011) Genetic structure, behaviour and invasion history of the Argentine ant supercolony in Australia. Evolutionary Applications 4: 471–484. doi: 10.1111/j.1752-4571.2010.00161.x
  • Sun J, Lu M, Gillette NE, Wingfield MJ (2013) Red turpentine beetle: innocuous native becomes invasive tree killer in China. Annual Review of Entomology 58: 293–311. doi: 10.1146/annurev-ento-120811-153624
  • Sutherland WJ, Stillman RA (1988) The foraging tactics of plants. Oikos 52: 239–244. doi: 10.2307/3565196
  • Thomson D (2004) Competitive interactions between the invasive European honey bee and native bumble bees. Ecology 85: 458–470. doi: 10.1890/02-0626
  • Tobin PC, Turcotte RM, Snider DA (2013) When one is not necessarily a lonely number: initial colonization dynamics of Adelges tsugae on eastern hemlock, Tsuga canadensis. Biological Invasions 15: 1925–1932. doi: 10.1007/s10530-013-0421-3
  • Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conservation Biology 17: 48–58. doi: 10.1046/j.1523-1739.2003.02018.x
  • Ugelvig LV, Cremer S (2012) Effects of social immunity and unicoloniality on host–parasite interactions in invasive insect societies. Functional Ecology 26: 1300–1312. doi: 10.1111/1365-2435.12013
  • Vilcinskas A, Mukherjee K, Vogel H (2013) Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proceedings of the Royal Society of London B: Biological Sciences 280: 20122113. doi: 10.1098/rspb.2012.2113
  • Walters AC, Mackay DA (2003) An experimental study of the relative humidity preference and survival of the Argentine ant, Linepithema humile (Hymenoptera, Formicidae): Comparisons with a native Iridomyrmex species in south Australia. Insectes Sociaux 50: 355–360. doi: 10.1007/s00040-003-0685-1
  • Walters AC, Mackay DA (2005) Importance of large colony size for successful invasion by Argentine ants (Hymenoptera: Formicidae): Evidence for biotic resistance by native ants. Austral Ecology 30: 395–406. doi: 10.1111/j.1442-9993.2005.01481.x
  • Ward NL, Masters GJ (2007) Linking climate change and species invasion: An illustration using insect herbivores. Global Change Biology 13: 1605–1615. doi: 10.1111/j.1365-2486.2007.01399.x
  • Ware R, Yguel B, 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. Ecological Entomology 34: 12–19. doi: 10.1111/j.1365-2311.2008.01036.x
  • Wilder SM, Barnum TR, Holway DA, Suarez AV, Eubanks MD (2013) Introduced fire ants can exclude native ants from critical mutualist-provided resources. Oecologia 172: 197–205. doi: 10.1007/s00442-012-2477-7
  • Wilder SM, Holway DA, Suarez AV, LeBrun EG, Eubanks MD (2011) Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions. Proceedings of the National Academy of Sciences of the United States of America 108: 20639–20644. doi: 10.1073/pnas.1115263108
  • Wilson EE, Holway DA (2010) Multiple mechanisms underlie displacement of solitary Hawaiian Hymenoptera by an invasive social wasp. Ecology 91: 3294–3302. doi: 10.1890/09-1187.1
  • Wilson EE, Mullen LM, Holway DA (2009) Life history plasticity magnifies the ecological effects of a social wasp invasion. Proceedings of the National Academy of Sciences of the United States of America 106: 12809–12813. doi: 10.1073/pnas.0902979106
  • Wilson-Rankin EE (2014) Social context influences cue-mediated recruitment in an invasive social wasp. Behavioral Ecology and Sociobiology 68: 1151–1161. doi: 10.1007/s00265-014-1726-7
  • Wilson-Rich N, Starks PT (2010) The Polistes war: weak immune function in the invasive P. dominulus relative to the native P. fuscatus. Insectes Sociaux 57: 47–52. doi: 10.1007/s00040-009-0049-6
  • Wuellner CT, Saunders JB (2003) Circadian and circannual patterns of activity and territory shifts: Comparing a native ant (Solenopsis geminata, Hymenoptera: Formicidae) with its exotic, invasive congener (S. invicta) and its parasitoids (Pseudacteon spp., Diptera: Phoridae) at a central Texas site. Annals of the Entomological Society of America 96: 54–60. doi: 10.1603/0013-8746(2003)096[0054:CACPOA]2.0.CO;2
  • Yan Z, Sun J, Don O, Zhang Z (2005) The red turpentine beetle, Dendroctonus valens LeConte (Scolytidae): An exotic invasive pest of pine in China. Biodiversity & Conservation 14: 1735–1760. doi: 10.1007/s10531-004-0697-9
  • Yang CC, Ascunce MS, Lou LZ, Shao JG, Shih CJ, Shoemaker D (2012) Propagule pressure and colony social organization are associated with the successful invasion and rapid range expansion of fire ants in China. Molecular Ecology 21: 817–833. doi: 10.1111/j.1365-294X.2011.05393.x
  • Yeates AG, Schooler SS, Garono RJ, Buckley YM (2012) Biological control as an invasion process: Disturbance and propagule pressure affect the invasion success of Lythrum salicaria biological control agents. Biological Invasions 14: 255–271. doi: 10.1007/s10530-011-0060-5
  • Zettler JA, Taylor MD, Allen CR, Spira TP (2004) Consequences of forest clear-cuts for native and nonindigenous ants (Hymenoptera: Formicidae). Annals of the Entomological Society of America 97: 513–518. doi: 10.1603/0013-8746(2004)097[0513:COFCFN]2.0.CO;2