Non-native gall-inducing insects on forest trees: a global review

György Csóka1*, Graham N. Stone2 and George Melika3

1National Agricultural Research and Innovation Centre, Forest Research Institute, Hegyalja str. 18, 3232 Mátrafüred, Hungary2The University of Edinburgh, Institute of Evolutionary Biology, The Kings Buildings, West

Mains Road, Edinburgh EH9 3JT, United Kingdom 3National Food Chain Safety Office, Directorate of Plant Protection, Soil Conservation and

Agri-environment, Budaörsi str. 141-145, 1118 Budapest, Hungary

*csokagy@erti.hu; Phone number: +36-30-3050747; Fax number: +36-37-520-047

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Abstract - Gall-inducing insects cause the development of specialised plant tissues (galls)

that provide them with nutrition and some measure of protection from physical and biotic

stresses. Their interaction with the plant is the most intimate metabolically of any herbivore

group and is often associated with high host specificity. We survey the gall inducers that have

become invasive pests of forest trees, most of which belong to just four insect families in

three orders: Hemiptera (Adelgidae), Diptera (Cecidomyiidae) and Hymenoptera (Cynipidae and Eulophidae). Most are associated with introduction of plants on which they are specialists, but some have also shifted from introduced to native plant hosts. No formal comparative analysis of traits associated with success of establishment and subsequent range expansion has yet been made, and it is often hard to identify why one species has become a major range-expanding pest, while closely related and biologically very similar species have not. We provide an overview of biological traits likely to facilitate gall inducer range expansion, and highlight the importance of natural enemies in community impacts and biological control. Increasing global trade is likely to result in further range expansions by economically damaging species. The effects of climate change on the direction, frequency, and impact of gall inducer range expansions are likely to be complex and probably species-specific.

Key words: gall-inducing insects, non-native, invasion, host specificity, range expansion

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Introduction

Biological invasions cause severe economic and ecological impacts worldwide (Simberloff

2001, 2011; Kenis et al. 2009). There are a growing number of examples worldwide where

the natural processes and functioning of forest ecosystems have been radically transformed by

invasive plants, herbivores (both vertebrates and invertebrates), predators and pathogens

(Wardle and Peltzer 2017). Insects are among the most numerous invaders globally (Kenis

and Branco 2010; Brockerhoff and Liebhold 2017), and make up ca. 87% of the alien

arthropods in Europe (Roques 2010). The probability and pathways of introduction, and

potential for establishment and invasion, vary among different guilds and among species

within a given taxonomic group (Liebhold et al. 1995b; Langor et al. 2009; Ripka 2010). The

outcomes of introductions are determined not only by biological charateristics of the potential

invaders, but also by their links to human trade and transport and to ecological characteristics

of the introduced range (vegetation, landscape history, geography, etc.) (Niemelä and Mattson

1996; Mattson et al. 2007; Ripka 2010). Here we present a global overview of alien/invasive

species in one specialised guild of herbivorous insects, the gall inducers.

Galls are abnormal plant growths caused by another organism - the gall inducer (also termed a

gall maker, or galler), and which provide the inducer with food and protection from biotic

stressors and natural enemies (Stone and Schönrogge 2003; Giron et al. 2016). Galls result

from very specific metabolic interactions between the gall inducers and their host plants

(Giron et al. 2016; Oates et al. 2016), and gall inducers are often considered the most highly-

evolved herbivores. Gall induction has evolved independently in many different insect orders

(Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera, Thysanoptera) and other plant

parasitic organisms such as mites and nematodes (Raman et al. 2005) and affects a wide

diversity of host plant taxa including many woody forest plants.

Gall-inducing insects are typically highly host-specific, only galling a single host genus or

specific subgroups (subgenera, sections or single species) within a genus. Most also attack

only specific host plant organs (such as leaves, buds, fruits, flowers, roots). Some groups

show cyclical parthenogenesis, with alternation of morphologically and ecologically different

generations within a year that are also sometimes associated with different host plants. Such

complex lifecycles are typical for some families in the Hemiptera (Adelgidae, Pemphigidae;

Havill and Foottit 2007) and some genera of cynipid gall wasps (Hymenoptera: Cynipidae;

Stone et al. 2002; Csóka et al. 2005). Presence of appropriate host plants is essential for

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successful introduction and establishment of gall-inducing insects. While some gallers, such

as the Chestnut gallwasp (Dryocosmus kuriphilus) discussed below, have proven able to shift

easily from introduced to native plants in the same genus, the metabolic intimacy of gall

induction means that successful shifts to a novel host are typically very rare for gall inducers

(e.g. Stone et al. 2009). There are no gall inducers able to attack a very wide range of host

plants, and hence able to attack a wide diversity of novel hosts in their invaded range. This

stands in sharp contrast to the very wide host range of some successful invaders in other

herbivore guilds, such as the gypsy moth, Lymantria dispar (Lepidoptera: Erebidae), a

Eurasian species that is invasive in North America and which can feed successfully on 650

host plants belonging to 53 families (Liebhold et al. 1995a; McManus and Csóka 2007).

Another example is the citrus flatid planthopper, Metcalfa pruinosa (Hemiptera: Flatidae),

which is native to North America that is invasive in Europe and has been recorded from at

least 330 host plants in 78 families (Csóka et al. 2012; Tuba et al. 2012). Successful

establishment and invasion of new continents and regions by gall-inducing insects is thus

usually preceded by extensive introduction of host plants from their native range, for example

through import and plantation of exotic species. Given this requirement, insect gall inducers

as a group show several traits that might be expected to facilitate accidental introduction,

settlement and successful invasion. We return to these issues, using examples from this

review, in our final synthesis.

(i) Many gall inducers are able to improve the nutritional quality of gall tissues as food,

preventing the accumulation of toxic secondary plant chemicals through physiological

manipulation (Giron et al. 2016; Oates et al 2016). As a result, gall inducers are often

effectively isolated from chemical plant defences. They can be detected and destroyed by

plant R-gene mediated defence, which prevents feeding or leads to apoptosis of nutritive gall

tissues (Zinov’eva et al. 2004; Kaloshian and Walling 2016). To resist attack, plants need to

detect eliciting stimuli in the gall inducer (Kaloshian and Walling 2016). Plants may not be

able to detect such stimuli a novel introduced gall inducer, leading to widespread lack of plant

resistance that can contribute to galler invasiveness.

(ii) All gall-inducing insects as immature stages are concealed within (often cryptic) galls that

are physically part of a host plant, increasing the chances of accidental introduction with the

host plant.

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(iii) Several groups have lifecycles that are completely or partially parthenogenetic (Havill

and Foottit 2007; Csóka et al. 2005), such that a single parthenogenetic female (usually with

high fecundity) can establish an invading population. Taxa where parthenogenesis is common

are regularly considered successful potential invasive insects (Brockerhoff and Liebhold

2017).

(iv) Many gall inducers have one or more small and relatively dispersive winged stages in

their life cycle (though in the case of gall midges and gall wasps these are short-lived). These

are hard to detect and allow long-range wind-borne or vehicle-borne dispersal to previously

unoccupied areas.

(v) Gall inducers often cannot be attacked successfully by generalist predators, but are instead

attacked by specialist natural enemies that possess the sensory traits able to recognise a gall,

and ovipositional anatomy able to penetrate plant tissues to reach their concealed hosts (Stone

and Schönrogge 2003). If gall inducers are introduced without the enemies from their native

range, they may remain undetected by enemies in their invaded range, and experience

‘enemy-free space’, at least initially (Schönrogge et al. 1996, 2006). This can contribute to

rapid population growth, and facilitate establishment and invasiveness (Colautti et al 2004;

Brockerhoff and Liebhold 2017).

In addition to these biological traits, invasiveness is also often associated with introduction to

areas with appropriate and benign weather/climate, and by specific circumstances that aid

natural or anthropogenic dispersal (wind, traffic, plant trade within the introduced range, etc.).

Here we provide examples, by taxonomic group, of alien/invasive gall-inducing insects that

attack woody plants. We introduce their life histories, significance, and possible routes of

introduction, and highlight characteristics and environmental factors likely to have facilitated

successful invasion. While our focus is on major economic pests, not all of our examples fall

into this category; one, included for purposes of illustration, is a biocontrol agent of invasive

trees.

The species by orders

Hemiptera

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Gall-inducing species are present in several families within the Hemiptera, but the most

interesting and important forest invaders are probably the adelgids (family Adelgidae,

Aphidoidea). Adelgids are endemic in the boreal and temperate zones of the Northern

Hemisphere, and all are associated with host trees in the Pinaceae. Fewer than 70 species have

been described, but due to taxonomic uncertainty the exact number of species remains

unknown (Havill and Foottit 2007). Adelgids are cyclically parthenogenetic, and have

complex multigeneration life cycles that can either be holocyclic (a 2-year lifecycle including

a sexual generation and host alternation) or anholocyclic (entirely asexual, without host

alternation) (Havill and Foottit 2007; Havill et al. 2007). Both holocyclic and anholocyclic

adelgids are strictly host specific (Havill and Foottit 2007; Havill et al. 2007). For holocyclic

species the primary host (on which sexual reproduction and gall induction occur) is always

Picea, and the secondary host (on which reproduction is asexual, without gall induction) can

be Abies, Larix, Pseudotsuga, Tsuga, or Pinus (Havill and Foottit 2007). The galls induced on

the primary hosts resemble very small pineapples. Anholocyclic life cycles are either

completed on Picea or another species in Pinaceae. Some adelgids that are considered

anholocyclic may in fact be holocyclic species whose sexual forms on the alternate host have

yet to be discovered or described (Havill and Foottit 2007). From this point of view these

species parallel some oak cynipid gall wasps in which sexual and asexual generations in a

cyclically parthenogenetic lifecycle (originally described as distinct species) have yet to be

linked (Csóka et al. 2005). There are alien and invasive adelgid species, both in North

America and in Europe.

Adelges (Dreyfusia) piceae (Ratzeburg)

Balsam woolly adelgid, Adelges (Dreyfusia) piceae, is native to Central Europe. It was

accidentally introduced to North America (SE Canada and NE USA), reaching the West Coast

(the San Francisco Bay area) in 1929 and the southeast by the mid 1950s. This species

probably spread through dispersal of infested nursery plants within the American continent

(Ragenovich and Mitchell 2006). Adelges piceae causes swellings and thickening of shoots on

Abies species, and heavy infestation may result in crown thinning and dieback. This species

causes major damage both in Christmas tree plantations and also in forest stands. North

American Abies species lack heritable resistance, and while European Abies alba can survive

very high infestation without being severely damaged, North American species (A. fraseri, A.

balsamea) can be seriously damaged (Ragenovich and Mitchell 2006); in some regions Fraser

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fir (A. fraseri) declined by 60% between 1954 and 1988 due to attack by this insect

(McManamay et al. 2011). The extensive mortality caused can have serious negative effects

on native species associated with this tree species, including local extinction (Liebhold et al.

1995b). McManamay et al. (2011) found that Fraser fir stands at higher elevations are

recovering, but stands at lower elevations may be becoming even more susceptible to A.

piceae-induced mortality.

Establishment of this species may have been facilitated by the fact that it reproduces

parthenogenetically. Invading populations have also escaped their natural enemies, and North

American native predators and parasitoids show no significant potential to regulate A. piceae

populations. Several native European enemies, including predatory beetles and flies, have

been introduced to North America, but none have had significant impacts (Ragenovich and

Mitchell 2006).

Adelges (Aphrastasia) tsugae Annand

Hemlock woolly adelgid, Adelges (Aphrastasia) tsugae, is native to Asia and western North America (Havill and Foottit 2007; Day and Salom 2010). It is a holocyclic species in its native range, but its life cycle differs significantly in its native and

invaded ranges. As an invader in the eastern US Adelges tsugae attacks Tsuga species

(secondary hosts) and is obligately parthenogenetic, since there are no suitable Picea

hosts for the sexual generation (Butin et al. 2005). In contrast as a native in Japan it alternates

between Tsuga sieboldii and Picea torano, with P. torano serving as the primary host on which galls are induced (Sato 1999).

In the early 1950s A. tsugae was reported in eastern Virginia, USA, and it has since spread to 19 states, with a distribution centred on the Appalachian part of the eastern US (Day and Salom 2010, Preisser et al. 2014). Birds (at least 10 species), deer and human activity (logging) may have played a significant role in long distance dispersal of A. tsugae (McClure 1990). Spread of this species varies in different directions, and is restricted towards

the south and west by low availability of Tsuga hosts, and to the north by low January

temperatures (Morin et al. 2009). Milder winters in future may facilitate further northwards spread of this species (Paradis et al. 2007).

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Adelges tsugae has minimal effects on its native secondary host plants (i.e. T. chinensis), but has devastating impacts on Tsuga canadensis and Tsuga caroliniana in eastern North America, causing extensive mortality of T. canadensis in the mid-Atlantic states and southern New England (Brockerhoff and Liebhold 2017). The basal area of hemlock fell by 70% between 1982-2002 in hemlock-dominated stands in southeastern Connecticut (Small et al. 2005), triggering an unprecedented change in tree species composition. The canopy basal area of black oaks (Quercus

velutina, Q. coccinea, Q. rubra) increased from 28% (1982) to 41% (2002). Sapling density

of oaks increased from 80 to 5,600/ha, and Sassafras albidum and Acer rubrum also showed

substantial increases in stem density (Small et al. 2005). These altered conditions often help

other alien invasive species (such as tree of heaven, Ailanthus altissima and Japanese

stiltgrass, Microstegium vimineum) to penetrate into the damaged stands (Orwig and Foster

1998).

Loss of hemlock can also alter terrestrial and aquatic wildlife habitats (Spaulding and Rieske

2010). Adelges tsugae-associated damage to hemlock stands has negatively affected 2 of 3

hemlock-dependent songbird species (Swartzentruber and Master 2005). However, hemlock

mortality can have contrasting effects on different bird species (Tingley et al. 2002): while

some species (i.e. warblers, flycatchers) are strongly associated with healthy hemlock stands,

others (tits, nuthatch, woodpeckers) are more abundant in damaged stands. Compositional

changes may have significant long-term impacts on forest stream ecosystems, resulting in

changes to the composition of fish communities and less stable thermal and hydrological regimes (Snyder et al. 2005).

Due to high cost and serious environmental side-effects, chemical control is not a viable option in forests (Havill et al. 2014). However, single hemlock trees can be protected efficiently by stem injection (Doccola et al. 2007). Both Carolina hemlock and eastern hemlock have been crossed with the highly resistant Chinese hemlock (T. chinensis) in an attempt to generate resistant hybrids. While hybrids of Carolina and Chinese hemlock show intermediate resistance, crosses between Chinese and eastern hemlock have been unsuccessful (Havill et al. 2014).

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One of the main reasons for the successful spread and expansion of A. tsugae in the eastern US (in additional to high abundance of suitable hosts lacking resistance) is the lack of specialist native enemies. Much attention has therefore been devoted to finding natural enemies that are both safe to release and capable of regulating A. tsugae populations at low levels. Since no parasitoids are known to attack adelgids, the search has concentrated on pathogens and predators (Brockerhoff et al. 2006; Havill et al. 2014). The coccinellid beetle Sasajiscymnus tsugae, native to Japan, was first

introduced to the US (Connecticut) in 1995. It successfully overwintered and reproduced, but

its impact on the adelgid population was minor (Havill et al. 2014). Several other coccinellids,

Scymnus species, were later introduced from China, but without spectacular success. A

specialist beetle predator of adelgids, Laricobius nigrinus (Derodontidae), which is native to

western North America, has also been introduced to the invaded area. In British Columbia it is

closely associated with A. tsugae (Zilahi-Balogh et al. 2002). Laricobius osakensis, a species

new to science, was discovered in Japan in 2005. It soon became a potential agent of classical

biological control against A. tsugae. After detailed study (Lamb et al. 2011; Vieira et al.

2011) L. osakensis was released in the eastern USA in 2012. The monitoring of this predator

is underway. Despite the serious efforts taken so far, a really safe and efficient biological

control agent has yet to be found.

Adelges cooleyi (Gilette)

Adelges cooleyi is a holocyclic species native to western North America. The primary host, on

which galls are induced, is Picea sitchenis while the secondary hosts are Pseudotsuga species

such as Douglas fir (Pseudotsuga menziesii) (Havill and Foottit 2007). It was accidentally

introduced to Europe, probably with living plants, and was first recorded in Great Britain in

1913. Since then it has been recorded in many European countries, including Austria,

Switzerland, the Czech Republic, Germany, Denmark, France, Italy, the Netherlands, Poland,

Romania, Serbia, Sweden, Slovakia and Ukraine (Mifsud et al. 2010). The primary host Picea

sitchenis is widely planted in Great Britain, Ireland, Denmark, Norway and Iceland, but can

be found in parks and arboreta in many other countries. Wide planting of the primary host has

facilitated Europe-wide range expansion. There are several parthenogenetic generations on the

Pseudotsuga secondary host. Heavy infestation can cause distortion and discolouration of the

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needles and early needle abscission. In general, this species causes less damage to affected

trees than A. piceae and A. tsugae.

Adelges (Dreyfusia) nordmannianae (Eckstein)

Adelges nordmannianae is a holocyclic species, native to the Caucasus Mountains. It has been

introduced to most of the European countries (Austria, Denmark, France, Germany, Hungary,

Ireland, Italy, etc.) and is also recorded from Australia (Anon 2008). It induces cone-like galls

on the primary host (Picea orientalis), and attack on the Abies secondary host results in

curling and thickening of needles, resembling a bottlebrush (Redfern et al. 2002). This species

can cause damage in younger stands and particularly in Christmas tree plantations (Ravn et al.

2013; Zubrik 2013a).

Other Adelgids

Several other alien gall-inducing adelgids of minor importance have been introduced to

Europe, all with Picea primary hosts. These are Adelges merkeri Eichhorn from Asia Minor

(the secondary host is Abies), Adelges prelli Grossmann from the Caucasus Mountains (the

secondary host is Abies), and Pineus orientalis, also from the Caucasus (the secondary host is

Pinus). These species have been recorded from many European countries, without causing

severe forest damage (Zubrik 2013b). DNA sequencing (both mitochondrial and nuclear) of

Adelges nordmannianae, A. piceae and A. prelli collected in Europe and North America has

not provided evidence of differentiation, suggesting that these species have either diverged

recently, or require taxonomic revision (Havill and Foottit 2007; Ravn et al. 2013).

Diptera

Gall-inducing Diptera occur in several families, but by far the most species-rich is the gall

midge family Cecidomyiidae, with 6,203 species in 736 genera (Gagné and Jaschhof 2014).

Gall midges are the most species rich galling insect group in the World, regularly dominating

gall inducer species richness in any geographic region (Yukawa and Rohfritsch 2005). New

species are frequently described, with one estimate predicting a total of 8,000 species

(Skuhravá and Skuhravý 1993). The host plant families most often attacked by gall midges

include Salicaceae, Fagaceae, Lauraceae, Rosaceae, Fabaceae, Caprifoliaceae Asteraceae and

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Poaceae (Yukawa and Rohfritsch 2005). Gall midges are often highly host specific, most are

strictly monophagous or oligophagous, and very few attack host plants in different families

(Yukawa and Rohfritsch 2005; Carneiro et al. 2009). Gall midge life histories are linked to the

phenology of their host plants (Yukawa and Rohfritsch 2005), such that hosts with ongoing

shoot production (mainly herbs) may harbour multivoltine gall midge species, but most of the

species galling woody plants are probably univoltine.

Skuhravá et al. (2010) listed 23 gall midge species alien to Europe, representing

approximately 1.3% of the species richness of the native European gall midge fauna (ca.

1,800 species). Relative to their extremely high species richness, the number of significant

invaders on woody plants is low, with only 4 of these 23 species linked to forest woody

plants. There is little information on alien gall midges outside Europe.

Dasineura gleditchiae Osten Sacken

Honey locust (Gleditsia triacanthos) is native to Atlantic North-America, and is widely

introduced and naturalised in other parts of the US. It has been widely planted in Europe since

the 1700s (Gencsi and Vancsura 1992), and has been introduced to Australia, Argentina,

Chile and some parts of Africa, where it is considered a weed tree (Csurhes and Markula

2016). It is a popular urban and street tree (particularly the thornless variety) in many

European countries. With the exception of a few rather polyphagous scale insects, almost no

native European pest insects have been recorded from it. In the last couple of decades two

bruchid seed beetles from Asia (Wendt 1980; Jermy et al. 2002; György 2007; Martynov and

Nikulina 2014) and a gall midge from North America have appeared on this tree in Europe.

The honey locust gall midge (Dasineura gleditchiae Osten Sacken – Diptera: Cecidomyiidae)

was first recorded in Europe in 1975 in the Netherlands (Nijveldt 1980), and has since been

found in many European countries: in 1983 in the UK (Smith et al. 2007), 1992 in Hungary

(Ripka 1996), 1995 in Slovakia (Hrubik 1999), 1996 in Spain (Del Estal et al. 1998), 2002 in

Denmark (Skuhravá et al. 2005), 2004 in Italy (Skuhravá and Skuhravý 2005), 2005 in

Turkey (Bayram et al. 2005), 2007 in the Czech Republic (Hrubik 2007), and 2008 in Sweden

(Molnár et al. 2009a).

Dasineura gleditchiae induces pod-like galls on the individual leaflets, often galling all

leaflets on leaves and even on whole branches. Each gall contains 1-5 larvae, and fully

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developed larvae pupate in the gall. The galled leaves are distorted, later becoming brown and

dry, and are shed (Ripka 1996). Fully-grown larvae overwinter in cocoons in the topsoil and

pupate in the following spring in the same place. Pupae can show prolonged diapause (Alford

2002). These biological traits in combination mean that the most likely route of long distance

anthropogenic dispersal for this species is transport of topsoil containing pupae. Local and

medium distance spread is probably through wind-assisted dispersal of adults.

Honey locust produces new shoots throughout the growing season, and so provides

oviposition sites for multiple overlapping generations of Dasineura gleditchiae, with 5-7 in

the USA (Johnson and Lyon 1976) but only 2-3 in Europe (Fischer and Pivot 1992; Halstead

1992). The number of generations is probably strongly dependent on environmental

conditions (latitude, weather, etc.). While variable in extent, this multivoltinism is likely to

facilitate rapid population growth. Climate change, with milder winters and longer autumns

increase voltinism and lead to more frequent outbreaks.

In Hungary only Gleditsia triacanthos is attacked by Dasineura gleditchiae, while planted

Asian G. caspica and G. ferox seem to be inherently resistant to galling (Ripka 1996). This

again shows the high host fidelity of gall-inducing insects (in contrast to the Asian seed

bruchids, which will accept the seeds of North American G. triacanthos).

There is no information on any parasitoids associated with this species, and low enemy-

imposed mortality may contribute to the success of the species in its introduced range.

Obolodiplosis robiniae (Haldeman)

North American Black locust (Robinia pseudoacacia L.) was first introduced to Europe in

1601, and from the 19th century onwards it has become an increasingly important tree in the

afforestation of warm lowland areas (Gencsi and Vancsura 1992). It is now one of the most

common plantation trees Europe-wide, with plantations exceeding 2.5 million hectares.

Several countries have particularly large and growing areas of black locust plantation,

including Poland (310,000 ha), Italy (377,000 ha), Ukraine (422,000 ha) and Hungary

(465,000 ha) (Hasenauer et al. 2016). Hungarian Black locust plantations cover almost a

quarter of the total forested area of the country (Csóka and Ambrus 2016). Large Robinia

plantations are being established in China (ca.700-800,000 ha in total) and in North and South

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Korea (300-350,000 ha total). Due to its modest demands, fast growth and attractive and

fragrant flowers it is a popular ornamental and urban tree almost everywhere in the temperate

zone.

Obolodiplosis robiniae (Haldeman) (Diptera: Cecidomyiidae) is a gall midge monophagous

on Robinia. In addition to R. pseudoacacia, it is known from R. viscosa, another popular

ornamental tree (Csóka Gy. personal observation). Its native range overlaps with that of R.

pseudoacacia, its main host. Robinia produces new shoots and leaves over the whole

growing season and O. robiniae is multivoltine, with up to 3-4 generations per year, again

facilitating successful spread. The galls of this species are downward-folded swellings of the

leaf margin that may contain 3-8 (Yang et al. 2006) and up to 10 whitish larvae (Csóka 2006).

Larvae of all but the last generation each year pupate in the gall. Larvae of the last generation

pupate in the soil and then overwinter there. Heavy infestations, particularly on young trees,

cause leaf drying and early abscission. Hardly anything is known about its real pest potential,

but historical US records from Pennsylvania (Haldeman 1847) and New York State (Fitch

1859) report considerable damage caused by the species. Several authors (Yang et al. 2006;

Csóka 2006; Kollár et al. 2009; Bakay 2014) consider it a potential pest. Following the

widespread planting of Robinia as an ornamental urban tree, O. robiniae has expanded its

range within North America. By 1999 it was already present in Victoria, Vancouver Island,

Canada, rather far from its native range (Csóka Gy. personal observation). In 2002 it was first

recorded in Northern Italy (Duso and Skuhravá 2003). Soon after the first European records it

started to spread explosively (Duso et al. 2005; Skuhravá et al. 2007). By 2004 it had already

reached the Czech Republic (Skuhravá and Skuhravý 2004), and in autumn 2006 it was found

in Hungary (Csóka 2006), Slovakia (Hrubik 2007; Kollár et al. 2009), Croatia (Pernek and

Matosevic 2009) and Serbia (Mihajlović et al. 2008). Expansion to the north and east was

extremely rapid in Hungary, and was probably significantly facilitated by the highest

concentrations of Robinia in Europe. By the end of 2008 the invaded area spanned the whole

country, 530km from west to east. By 2006 it was already widespread in southern Germany

(Wehrmaker 2007) and in 2007 it was recorded in Switzerland (Wermelinger and Skuhravá

2007), Poland (Skrzypczynska 2007), Austria (Csóka Gy. personal obs.) and Rumania (Bálint

et al. 2010). The first UK record was from summer 2007 at the botanical garden of Oxford

University (Csóka Gy. personal observation; Skuhravá et al. 2007). By 2008 it had reached

Sweden (Molnár et al. 2009b), at least 1,200 km from the location of the first record in

Northern Italy. In 2013 it was found in Spain (Sánchez and Umaran 2013). Several factors are

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likely to have contributed to such extremely rapid range expansion within Europe. One is that

the host plant is widespread and often abundant, providing many suitable ‘stepping stones’

habitat patches for the invasion. As a popular ornamental (and plantation) species, Robinia

plants are frequently transported within Europe and also worldwide, and this is generally

considered a major pathway of accidental pest introductions (Liebhold et al. 2012; Roques

2015). Because Robinia is most often transported as young leafless plants, anthropogenic

dispersal is most likely to have involved hibernating pupae in soil. Transport of plants with

leaves increases the risk of dispersal through galls. Multivoltinism, high infestation rates and

large numbers of larvae per gall (up to 10) all facilitate range expansion. Though specific data

are missing for Obolodiplosis, the small size and weight of the adults may well facilitate long-

range dispersal on air currents (Cusimano et al. 2016).

In 2002 Obolodiplosis robiniae was discovered in South Korea and in 2003 in Fukuoka,

Kyushu, Japan (Kodoi et al. 2003; Uechi et al. 2005). Since then it has expanded its

distribution in both countries. In 2008 the species was recorded from the Russian Far East, in

Vladivostok (Csóka Gy. personal observation) and Sakhalin Island (Gninenko 2013). These

distant records again suggest dispersal with transported host plants, though wind dispersal

could also be involved.

In 2003 a parasitoid of the gall midge was found in Italy. The species, Platygaster robiniae n.

sp. (Hymenoptera: Platygastridae) was new to science (Buhl and Duso 2008) and was

probably introduced to Europe together with Oboloidiplosis (Duso et al. 2011). Later the

parasitoid was found in Switzerland (Wermelinger and Skuhravá 2007), Croatia (Pernek and

Matosevic 2009), Hungary (Csóka pers. obs.), Romania (Bálint et al. 2010), Slovakia (Tóth et

al. 2011), Japan (Buhl and Duso 2008), and South Korea (Kim et al. 2011). Kim et al. (2011)

considered it to be strictly host specific. Tóth et al. (2011) in Slovakia found 8 parasitoid

species (7 of them native) attacking Obolodiplosis, but Platygaster robiniae was dominant.

They found annual larval parasitism rates of 5.4-10.8%, reaching as high as 40% late in the

season. However this parasitism rate, at least currently, does not seem to have restricted rapid

range expansion.

Hymenoptera

The order Hymenoptera includes several families with gall-inducing species (Cynipidae,

Xyalidae, Tenthredinidae, Braconidae, Pteromalidae, Eulophidae, etc.). The most important

14

gall-inducing species, in terms of potential for forest damage, belong to Cynipidae and

Eulophidae.

The Cynipid gall wasp family Cynipidae, with 1,400 described species, is the second largest

gall-inducing family after the gall midges (Diptera, Cecidomyiidae) (Liljeblad and Ronquist

1998; Ronquist 1999). Over 70% cynipid species belong to the tribe Cynipini, which gall

hosts in the family Fagaceae (Quercus, Castanea, Castanopsis, Chrysolepis, Lithocarpus and

Notholithocarpus). Cynipid galls in the tribes Cynipini and Pediaspidini (sycamore gall

wasps) typically have cyclically parthenogenetic life cycles (though some species are known

to lack sexual generations, and the pairing of generations for many species remains to be

demonstrated), and some Cynipini show alternation between hosts in different sections of the

oak genus Quercus (Stone et al. 2009). Oak gallwasps induce the most visually striking and

structurally complex galls, which support complex and species-rich communities of inquilines

(including other gallwasps) and parasitoids (primarily chalcids) (Stone and Cook 1998; Stone

et al. 2002; Csóka et al. 2005). Some (primarily oak) cynipid galls have historically been

important resources over the centuries as sources of tanning for production of leather, dying

of textiles and ink production) and traditional medicines (disinfectants, astringents), and have

a long history of international trade extending back to the Roman empire and before (Csóka et

al. 2005). The consequences of this transport are discussed below. Most cynipid gallwasps are

not considered serious pests (Stone et al. 2002), but some notable exceptions have

considerable economic and/or ecological effects on host trees and ecosystems.

Neuroterus saltatorius (Edwards)

Neuroterus saltatorius is native to the West Coast of the USA, and has two alternate

generations per year. The sexual generation induces clusters of integral leaf galls (formed

within the leaf lamina, and non-dehiscent), while the asexual generation develops in tiny

(1mm) spherical galls on the underside of the leaves. Once fallen from the plant, the asexual

generation gall is able to jump through sudden movements of the larva inside, hence its

common name of jumping gall (Russo 1979). Both generations develop on white oaks

(Quercus, section Quercus), including Garry oak (Quercus garryana). Neuroterus saltatorius

appeared near Victoria, on Vancouver Island in British Columbia in the early 1980s, probably

though vehicle traffic from Washington State (Hellmann et al. 2012). It has become far more

abundant there than in its native range, probably through escape from parasitoids and other

natural causes of mortality (Prior and Hellmann 2013). Heavy infestation can cause severe

15

defoliation on Garry oak (Humble and Allen 2001), which is the only native oak to British

Columbia, and alters the quality of its leaves with negative effects on a native specialist

butterfly, Erynnis propertius (Prior and Hellmann 2010).

Plagiotrochus amenti Kieffer

Cork oak (Quercus suber) is an evergreen oak native to southwest Europe and northwest

Africa. Its natural stands harbour diverse ecosytems including endangered species (Bugalho et

al. 2016). Its bark has long been used to provide corks for wine. Plagiotrochus amenti can be

a dangerous pest of Q. suber in Europe, particularly in northeastern Spain (Garbin et al.

2008), and in California (Weld 1926) and Argentina (Díaz 1973) where large cork oak

plantations were established to provide corks for the wine industry (Bailey & Stange 1966,

Zuparko 1996). Although alternating sexual and asexual generations each year are known in

Spain (with P. suberi identified as the alternating generation; Garbin et al. 2008; Pujade-Villar

et al. 2008), introduced American populations are purely parthenogenetic (Bailey and Stange

1966; Zuparko 1996), and as a result these two forms have been regarded as separate species

pending proof of their relationship (Pujade-Villar & Ros-Farré 1998). It has been argued

(Pujade-Villar 1998; Pujade-Villar and Díaz 2001) that even if P. amenti is confirmed to be

the sexual form of P. suberi, there could be two effective biological species – an ancestral

species with cyclical parthenogenesis, and a derived species with wholly parthenogenetic

reproduction. Ability of the species to reproduce purely parthenogenetically is certainly an

advantage in terms of invasiveness, as a single asexual female can successfully establish a

new population. Introduction is also facilitated by the fact that while the sexual generation

galls are visible on catkins and shoots, the asexual galls develop cryptically under the bark of

2-3 year old twigs, without visible external signs (Nieves-Aldrey 2001). This makes it easy to

accidentally introduce this species since even careful inspection may fail to detect infested

plants. Asexual generation larvae pupate by the end of the summer and the adults emerge the

following March–May or after a year of diapause (Nieves-Aldrey 2001).

Plagiotrochus australis (Mayr) and Plagiotrochus coriaceus (Mayr)

The gallwasp genus Plagiotrochus is primarily associated with Mediterranean sclerophyllous

oaks such as Quercus ilex and Q. suber, particularly in the Iberian Peninsula. Quercus ilex is

grown widely as an ornamental tree across much of northern Europe, and is naturalised in

16

some regions. Two species have recently become established in the UK on Quercus ilex and

were first recorded in 2006 (Schönrogge et al. 2011), most probably through transport of

galled plants from Spain. Plagiotrochus coriaceus is known only from an asexual generation

and induces galls that are small circular swellings within the leaf blade. Plagiotrochus

australis has alternating sexual and asexual generations, which induce galls in the leaf blade

and beneath the bark of twigs, respectively. The asexual generation galls of P. australis are

extremely cryptic, facilitating unintentional dispersal of infested plants. Neither invading

Plagiotrochus species is known to cause significant damage to its host tree.

Callirhytis tumifica (Osten Sacken)

Some North American red oaks (Quercus rubra, Q. palustris, Q. coccinea, Q. schumardi,

etc.) are popular urban plants across Europe. Quercus rubra in particular is widely planted in

some countries, either in pure plantations or in mixtures with other species. Red oaks are

taxonomically distant from native European oaks, and very few native oak herbivores

(including several free feeding lepidopteran larvae and some leaf mining Lepidoptera and

Hymenoptera) feed on them in Europe (Connor et al. 1980; Welch 1981; Csóka and Hirka

2001; Gossner et al. 2007, 2009). Almost all surveys have found no native gall inducers (gall

midges, gall wasps) on introduced red oaks (Welch 1981, 1987, 1993, 1995; Pinkess 1990;

Csóka and Hirka 2001). Though there are a few literature references to gall wasps on red oaks

in Europe (Ionescu 1973; Ambrus 1974; Kelbel 1994, 1996), we consider these records

extremely unlikely.

In autumn 2011, unidentified galls were discovered on leaves and later on acorns of Q. rubra

near Heidelberg, Germany (Beiderbeck 2012). None of the European Callirhytis species have

been found in acorns of Quercus rubra (Hirka 2003; Csóka and Hirka 2006). DNA from the

adults emerging from the leaf galls and the larvae found in the acorns was sequenced and

found to be practically identical to sequence for a native North-American gall wasp,

Callirhytis tumifica (Beiderbeck and Nicholls 2014). This is the first North-American oak

galling cynipid recorded in Europe. In 2014, the typical leaf galls were found in Berlin (H.

Buhr personal communication). As it is likely rather unusual to transport young leaf-bearing

red oaks between continents, the most likely route of introduction is through transport of

infested acorns. Only a single asexual female (and many can develop in a single acorn) is

required to found an introduced population by parthenogenesis. Quercus rubra is already

widespread in Europe, and windborne dispersal of the small adults of the sexual generation

17

and perhaps also further human dispersal of infested acorns are likely to result in considerable

future European range expansion. Since the species is already present in Berlin (latitude 52.3o

North), climate is unlikely to restrict further spread toward South and East of the continent.

Considering the extreme host conservatism of the oak galling cynipids (Csóka and Hirka

2001; Csóka et al. 2005; Stone et al. 2009), a host shift to native European oaks is very

unlikely, but harmfully abundant occurrence on planted North-American red oaks in Europe is

possible. There are as yet no records of native European natural enemies attacking Callirhytis

tumifica in Europe. Native Western Palaearctic Callirhytis species are attacked by a range of

generalist chalcid parasitoid species (Askew et al. 2013), some of which may recruit to C.

tumescens, particularly in areas where native oaks grow together with the introduced red oak.

Host-alternating Andricus species in Europe

The Western Palaearctic is home to a species-rich clade of Andricus gallwasps whose

lifecycles involve obligate alternation between a sexual generation on oaks in the section

Cerris, and an asexual generation on oaks in the section Quercus. These species thus can only

survive where both oak sections are present. Both are native only in southern Europe,

extending eastwards across Asia Minor to the Caucasus and Iran, and south into Lebanon,

Israel and Jordan. Several hundred years ago, Quercus cerris (section Cerris) was introduced

from Central and Eastern Europe to areas in northern and western Europe previously occupied

only by section Quercus oaks, triggering invasion of these regions by at least eight host-

alternating Andricus species (Schönrogge et al. 2013). For most of these species, the asexual

generation galls on native Quercus robur and Q. petraea are larger and more dramatic than

those of the sexual generation on Quercus cerris, but there is little evidence that either

generation of these species causes significant damage to host trees.

The earliest range expansion was by Andricus kollari (Hartig), which was deliberately

introduced to southern Britain in the 1840s as a source of tannin for the local dyeing industry.

This gallwasp spread rapidly across Britain (Walker et al. 2002), and heavy infestations of its

large asexual generation ‘marble galls’ on the buds of native oaks (Q. robur and Q. petraea)

caused public concern but very little economic damage, although growth of young trees in

nurseries can be stunted. As far as is known, all other invading host-alternating Andricus

species have spread without intentional human assistance. However, the sexual generation

galls of several of these species (Andricus aries (Giraud), A. corruptrix (Schlechtendal), A.

kollari, A. lignicolus (Hartig) and A. quercuscalicis (Burgsdorf)) are tiny (1-2mm) ‘pip’-like

18

galls on buds or catkins of Quercus cerris, and could be easily missed during shipment of

trees across Europe.

The best-known recently invading species is the knopper gallwasp, Andricus quercuscalicis,

whose asexual generation galls destroy the acorns of section Quercus oaks (almost

exclusively Quercus robur in Europe) (Hails and Crawley 1992; Hirka 2003). Range

expansion by this species is well documented across Europe from the 17th century (Stone and

Sunnucks 1993). Another species whose asexual generation gall destroys acorns is Andricus

grossulariae Giraud, 1859. Though dramatic, these asexual generation Andricus galls are not

thought to impose significant damage on oak regeneration. The most notable impact of these

invading gallwasps may have been on populations of parasitoid natural enemies. The invaders

provide many new hosts for these enemies, raising the possibility of apparent competition

between invading and native gallwasps (Schönrogge et al. 1996, 1998, 2000, 2011). Some

parasitoids were introduced with Andricus kollari from the eastern mediterranean and became

established in Britain (Nicholls et al. 2010), while arrival of host alternating Andricus species

in France has also allowed Spanish parasitoids to invade northwards over the Pyrenees

(Hayward and Stone 2006). The sexual generation galls in particular are also important early

spring food for native north-western European birds (Schönrogge et al. 2013).

Pseudoneuroterus saliens (Kollár) and Aphelonyx cerricola (Giraud)

Human introduction of Quercus cerris into northern Europe also allowed invasion of this

region from southern and central Europe by at least two gallwasp species that are wholly

dependent on this oak – Aphelonyx cerricola (first recorded from the UK in 1997) and

Pseudoneuroterus saliens (first recorded from the UK in 2006) (Schönrogge et al. 2011).

Aphelonyx cerricola is only known from an asexual generation, which forms aggregated ball-

like galls on shoots. Though shoots can be stunted by this species, it is not considered an

economic pest. Pseudoneuroterus saliens has a sexual generation that induces galls in the cup

of acorns in their second year of development, and an asexual generation that develops in

small ovoid galls on the exterior of shoots, leaf petioles, and occasionally leaf midribs. Both

generations are on Quercus cerris or closely related section Cerris oaks. Since the attack rates

on acorns can be high, this gallwasp is now considered to be a pest of increasing significance,

at least in some countries (e.g. Hungary), particularly where Turkey oak populations are

maintained by natural regeneration.

19

Dryocosmus kuriphilus Yasumatsu

Chestnuts (Fagaceae: Castanea spp.) are important components of native forests in North

America, Europe and Asia. They are planted widely both within and outside their native

ranges for their valuable fruit crop. Dryocosmus kuriphilus (Hymenoptera, Cynipidae), native

to China, is an important pest of Castanea species (Murakami et al. 1995; Payne et al. 1983).

In its native range it attacks Castanea mollissima and C. seguinii. In introduced areas it is also

known to attack several other chestnut species including C. crenata in Korea and Japan, C.

sativa in Europe, and C. dentata in North America. Castanea pumila and C. alnifolia growing

wild in North American seem to show inherited resistance, since attack of these species has

yet to be recorded. Hybrids of the attacked species are also suitable hosts for D. kuriphilus

(EPPO 2005). It is univoltine, with parthenogenetic females laying eggs in the leaf buds of the

host during summer. The tiny first instar larvae overwinter in the bud, with gall development

starting in the following spring (Brussino et al. 2002). These cryptic eggs and overwintering

larvae make it very easy to spread infested trees without detecting any presence of the

gallwasp. Heavy galling by D. kuriphilus prevents or inhibits shoot development and

flowering, and may stress trees enough to contribute to mortality (Kato and Hijii 1997; Aebi

et al. 2006; Cooper and Rieske 2010). The loss of fruit yield can be 80% or more (Quacchia et

al. 2008; Matošević et al. 2015).

From the 1940s onwards, this species spread from China to Japan, then Korea and the USA. It

reached Europe around the turn of the millennium (Brussino et al. 2002): though the first

record was in 2002 from Piedmont in northwest Italy, its introduction can be traced back to 2–

3 years earlier with the import of nursery chestnut material from China (Quacchia et al. 2008).

Since 2002 to the present it has spread rapidly throughout Europe where chestnuts grow

(Matošević et al. 2015) and is now recorded from Turkey. No control methods (mechanical,

chemical, resistance breeding) are known that provide long-term protection against this pest.

In its native range in China D. kuriphilus populations are kept at low, non-damaging levels, it

is thought (though there have not been detailed studies) by natural enemies (Aebi et al. 2006;

2007, Gibbs et al. 2011). This is not the case in the invaded territories (Japan, South Korea,

the USA, Europe) where D. kuriphilus (at least currently) experiences very low mortality

through attack by native natural enemies. Despite rapid shifts of native parasitoids onto the

new host, parasitism rates remain low (usually 2-4%) and have little influence on host

20

population density (Aebi et al. 2006, 2007; Santi and Maini 2012; Quacchia et al. 2012;

Matošević and Melika 2013, Francati et al. 2015; Kos et al. 2015). Around 30 species of

native chalcid parasitoids that normally attack galls induced by related cynipid gallwasps on

oaks (Fagaceae, Quercus spp.) have colonised D. kuriphilus galls throughout their introduced

range (Aebi et al. 2006, 2007).

Classical biological control using a Chinese parasitoid Torymus sinensis Kamijo

(Hymenoptera: Torymidae) has proven to be the only effective method of controlling

populations of D. kuriphilus, and this species has been released, generally with success, in

Japan, South Korea, the USA, Italy, France, Slovenia, Croatia and Hungary (Gibbs et al.

2011; Cooper and Rieske 2007; Moriya et al. 2002, Quacchia et al. 2008; Bosio et al. 2013;

Matošević et al. 2014). After multiple releases, the parasitism rate of D. kuriphilus by T.

sinensis can be up to 85% (Matošević et al. 2014). The impact of T. sinensis on native

gallwasps anywhere it has been released remains largely unknown (Gibbs et al. 2011).

Galling eulophids on Eucalyptus

Eucalyptus is an extremely species-rich tree genus with approximately 700 described species,

centred on Australia and Tasmania. Some species are evergreen, while others are deciduous.

Eucalypt plantations – major sources of pulp wood in many countries – have been established

all around the world where suitable climates exist. These plantations often cover large areas

and their biological diversity is rather low, increasing the risk of outbreaks of herbivorous

insects through lack of natural enemies, and making them particularly vulnerable to invasive

organisms.

Leptocybe invasa Fisher & La Salle (Hymenoptera, Eulophidae) is a recently described

species in a new genus (Mendel et al. 2004). Probably native to Australia, it has spread to

almost all regions (continents and countries) where eucalypts are grown on a significant scale

(countries in Africa, Asia and the Pacific, Europe, North America and the Near East, Asia

including Cambodia, Thailand, Taiwan, Vietnam and India, and New Zealand). The main

route of accidental intercontinental introduction probably involves transport of infested

eucalypt seedlings, and the large global trade of eucalypt propagation material is almost

certainly a major contributor to the rapid worldwide spread of Leptocybe invasa. Only

parthenogenetically reproducing females are known. These are small and are not strong flyers,

so active dispersal is considered secondary to long range anthropogenic dispersal, with wind

21

dispersal perhaps contributing to spread in areas where the species has been introduced.

Depending on the local climate Leptocybe invasa may have 1-3 generations per year (Mendel

et al. 2004). In Israel, ten Eucalyptus species have been found to be suitable hosts (E.

botryoides, E. bridgesiana, E. camaldulensis, E. globulus, E. gunii, E. grandis, E. robusta, E.

saligna, E. tereticornis, and E.viminalis) (Mendel et al. 2004). It causes bump-like galls on

young shoots and leaves (petioles, midribs), which can be very abundant (up to 50 galls/ leaf).

Heavy infestation may cause early leaf abscission, decreased vigour, and shoot and crown

dieback, and young seedlings may be killed by severe attack. Eucalypts generally resprout

vegetatively very well, so plantations can easily be coppiced for 2-3 cycles. The coppiced

shoots provide excellent food sources for L. invasa, helping to build up abundant populations

(Jacob and Ramesh 2009). This species causes major economic loss, and is likely to cause

even more severe damage in the future. In India alone, L. invasa potentially threatens ca. 8

million hectares of eucalypt plantations (Ramanagouda et al. 2010). In Israel, planting of E.

camaldulensis was stopped because of extensive attacks by the wasp. Leptocybe invasa shows

sensitivity to host variation within Eucalyptus species (Branco et al. 2009; Ramanagouda et

al. 2010; Durand et al. 2011), suggesting the possibility of selective breeding for resistance.

Finding efficient biological agents (both introduced and native) has recently become a major

focus of L. invasa-related research worldwide (Protasov et al. 2008; Kim et al. 2008; Kelly et

al. 2012; Doğanlar et al. 2013; Dittrich-Schröder et al. 2014; Yang et al. 2014; Udagedara and

Karunaratne 2014; Nugnes et al. 2016)

Ophelimus maskelli (Ashmead) is another eulophid wasp harmful to eucalypts that occurs

naturally in New South Wales (Australia) but has also recently been recorded from several

south European countries (Sánchez 2003; Pujade-Villar and Riba-Flinch 2004; EPPO 2006;

Protasov et al. 2007a; Doganlar and Mendel 2007; Branco et al. 2009). In 2014 its galls were

also found in California, representing the first record from the Americas (Burks et al. 2015).

The species induces small pimple-like galls on the leaf blade that can often cover the whole

leaf. Heavy infestation causes early leaf abscission (Protasov et al. 2007b). As for L. invasa,

O. maskelli is also highly sensitive to intraspecific variation in its host plants (Branco et al.

2009; Ramanagouda et al. 2010; Durand et al. 2011). A parasitoid of O. maskelli,

Closterocerus chamaeleon (Hymenoptera: Eulophidae), was found in Portugal in 2006 and

2007 (Branco et al. 2009), and together with three other species has been released in Israel in

an attempt at biological control of the pest (Mendel et al. 2007; Protasov et al. 2007a).

22

Quadrastichus erythrinae on Coral Trees (Erythrina spp.)

Many species of the originally pantropical and species-rich genus Erythrina (Fabaceae

family) are popular ornamental trees all over the World and/or important elements of native

ecosystems. Quadrastichus erythrinae is a tiny eulophid wasp described in 2004 from

specimens from Singapore, Mauritius and Reunion Islands, and later reported form Taiwan,

China, Japan (Okinawa), India, the Philippines, Hawaii, and the USA (Florida) (Howard et al

2008). Its native range is still unknown, but it is thought to have originated from Africa (Li et

al 2006). The female wasp oviposits into young leaf and stem tissues. The developing larvae

induce galls that cause swellings and distortions on the leaves and the petioles. The final

instar larvae pupate in the gall. Heavily infested trees show reduced leaf growth and vigour. In

extremes cases heavy attack can cause severe defoliation and even tree death (Yang et al

2004). The rapid global spread of Quadrastichus erythrinae, predicted by Li et al (2006), was

probably facilitated by several factors. Global trade in the host plant was almost certainly

responsible for many independent accidental introductions. Establishment and spread within

the new range were helped by the presence of the suitable congeneric host plants and lack of

efficient native enemies. Only Aprostocetus felix La Salle, Yang & Lin from Taiwan has been

reported so far as a native parasitoid of Quadrastichus erythrinae (Yang et al 2014).

Trichilogaster gallers on Acacia

Trichilogaster wasps are chalcids in the family Pteromalidae that are native to Australia and

induce a diversity of galls on native Acacia species. Several Australian Acacia species are

widely planted as ornamental and plantation trees wherever suitable climates exist worldwide,

and at least ten species have become serious invasive pests, particularly in South Africa

(Impson et al. 2011). Trichilogaster species that gall the flowers of invasive acacias have been

released as control agents in South Africa, where their large galls impose metabolic costs on

the tree and also directly reduce seed set, and hence propagule pressure, of invading acacia

populations (Hoffmann et al. 2002; Impson et al. 2011). We mention Trichilogaster here

because the (helpful) damage they cause through specialist gall induction on an introduced

tree species parallels the pattern seen in many forestry pests.

A synthesis23

The most important alien/invasive gall-inducing insects belong to just five families (if we include Trichilogaster biocontrol agents) in three orders: Hemiptera (Adelgidae), Diptera (Cecidomyiidae) and Hymenoptera (Cynipidae, Eulophidae and Pteromalidae). There has been no systematic analysis of the traits of gall inducers that might identify ‘rules of thumb’ predisposing particular taxa to successful introduction and subsequent rapid range expansion. Wider taxonomic analyses of invasion success show that, for a range of animals, higher numbers of introduction events and higher fecundity are associated with increased success in establishment, and species with a wider distribution and from similar climatic regions are more likely to expand their range (Hayes and Barry 2008; Capellini et al. 2015). Though reproductive mode – and in particular the ability to start a population from a single parthenogenetic female – is an important correlate of establishment success and subsequent invasiveness in plants, there is no overall correlation for animal datasets (Hayes and Barry 2008). A striking feature of some gall-inducing groups that contain range-expanding species is that they contain biologically very similar taxa that have not expanded their range. For example, though human dispersal of Quercus cerris has led to westwards range expansion across Europe by a suite of gallwasp species, many close relatives of these taxa remain restricted to their natural distributions in southern and eastern Europe (Stone et al. 2009; Schönrogge et al. 2011). There are no obvious differences between invaders and non-invaders in physiology, native range distribution size, life history traits such as longevity or fecundity, or inherent dispersal ability. Thus while the traits we highlight below may facilitate range expansion, they are not always sufficient to guarantee it. Other factors – such as fortuitous anthropogenic dispersal, may determine which species expand their distributions, and which do not. The following patterns should thus be regarded as hypotheses to be tested in an appropriate comparative framework (Capellini et al. 2015).

Gall inducers are among the most host specific herbivores, with very low rates of host shifts over time in some groups (Stone et al. 2009), and even

24

those taxa showing higher rates generally shift between closely related plant species (e.g. Nyman et al. 2010). Successful establishment of introduced gall inducers thus requires the presence of familiar or very closely related host plants in a novel range. This is epitomised by pests associated with large-scale non-native planting of species such as Robinia pseudoacacia, Quercus suber and Quercus cerris. Planting of exotic species in large-scale monocultures may also increase the risk of co-introduction of larger populations of associated specialist herbivores, and (by exposure) facilitate shifts by these herbivores to novel hosts native to the introduction site (Liebhold 2012). Other gall-inducers have proved able to shift to closely related but novel (and usually congeneric) hosts in a new distribution – as observed in Dryocosmus kuriphilus shifting between Castanea species, and Adelges tsugae shifting between Tsuga species.

Trade in living plants (including seeds and grafts) is often considered the main route of introduction for alien/invasive insects. This is particularly true for those gall inducers whose life cycles involve cryptic galls or dormant eggs laid within plant tissues, which are unlikely to be detected on inspection, and which may outlast quarantine periods. Long distance trade will almost certainly continue to grow, resulting in intercontinental exchange of tree species and increasing numbers of insect introductions (including gall inducers) (Rasplus 2010). Range expansion may be facilitated where multiple congeneric tree species are involved in human trade and are attacked by the same pest – as for Leptocybe invasa on Eucalyptus. Because of their cryptic nature and often-complex lifecycles, the diversity and biology of gall inducers is relatively less known than other insect trophic groups. It is likely that many more species remain to be described in their native distributions – for example of gall inducers on Eucalyptus in Australia. Some may well be noticed only for the first time when they appear in large numbers in an exotic plantation in a different part of the world.

Once introduced, a combination of further anthropogenic dispersal and passive dispersal through air currents are likely to have been important for most species. Parthenogenetic life stages in some species may have

25

facilitated establishment from very small population sizes – as thought to be the case for chestnut gallwasp Dryocosmus kuriphilus.

The impact of range expansions by gall inducers is highly variable. Some, such as most cynipid gallwasps, cause little more than aesthetic damage to plant health even at relatively high densities. Because gallers are static on their host plant (rather than destroying many plant units, such as chewing herbivores do), their potential for causing damage tends to be determined by the organ galled. Those species that restrict growth (by destroying shoot tips or large numbers of buds) or reduce fruit set (by destroying flowers or fruits) are more likely to be damaging economically than those that cause galls on leaves. Thus the chestnut gallwasp is more damaging than most of its relatives on oak because it has a major impact on tree growth and health (through attacking shoots), and massively reduces the production of a valuable seed crop (Battisti et al. 2014). Heavy infestation by this species thus threatens both chestnut-associated biodiversity and a traditional source of income. In contrast, oak gallwasps that can destroy acorns in equivalent numbers – such as Andricus quercuscalicis (Hails and Crawley 1992) are not considered serious pests because (except in seed nurseries) acorns are a less valuable crop.

Gall-inducers are inherently hard to control using externally applied chemicals or biopesticides because they are protected within plant tissues. Considerable interest has therefore focussed on biological control using natural enemies. Gall-inducers tend to be attacked in their native range by specialist natural enemies that are able to recognise, and successfully attack, gall tissues (Stone and Schönrogge 2003). Range expansion by gall inducers often results in escape from these natural enemies – at least for a while (e.g. Aebi et al. 2006, Schönrogge et al. 2006) – allowing the introduced species to rapidly expand its populations and become established. There are relatively few examples of simultaneous co-introduction of gallers and associated natural enemies (for a human-mediated example, see Nicholls et al. 2010). Though enemies native to their site of introduction eventually attack many alien gall inducers, these tend not to impose adequate mortality to regulate galler populations (as

26

shown by the examples of Dryocosmus kuriphilus and Adelges tsugae). In most cases classical biological control seems to be the only viable option. In some cases it has proved relatively easy to find an effective control agent (e.g. Torymus sinensis control of Dryocosmus kuriphilus), while other cases are proving more challenging (e.g. Adelges tsugae).

Most introductions and invasive spread of alien gall-inducing insects have been recorded from the temperate zone of the northern Hemisphere, with the obvious exception of eucalypts and Trichilogaster biocontrol agents on Acacia species in South Africa. There is no apparent trend in the directions of introductions, with exchanges in both directions known for introductions between each of America, Asia and Europe. This in principle could alter as ongoing climate change shifts the match in climatic conditions between different regions of the world. Climate change may also alter the plant landscape available to gall inducers. In areas that are becoming warmer and drier, populations of some plants are showing signs of stress that increases their susceptibility to attack by herbivores and pathogens (e.g. Seidl 2011; Logan et al. 2010). The impact on tree-galler interactions is likely to be complex. Some gall inducers do better on healthy hosts, and so may do less well on unhealthy trees (Csóka et al. 2005; Cornelissen et al. 2008). Restricted gall growth (which we might expect on less healthy plants) can make the inducer more vulnerable to attack by natural enemies and potential biocontrol agents (Egan and Ott 2007). Changes in the timing of budburst can have major consequences for the availability of suitable galling sites, and has significant impacts on oak gallwasp abundance (Sinclair et al. 2015). On the other hand, milder winters may increase galler survival rate, resulting in more damaging outbreaks in the following year. The complex biologies of many gall inducers mean that each interaction may well respond in an esoteric way that makes identification of overall patterns challenging.

Acknowledgements

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GC was supported by funding Agrárklíma.2 VKSZ_12-1-2013-0034 from the Hungarian State and the National Research, Development and Innovation Fund.GNS was supported by a UK NERC grant NE/J010499. GM was supported by Hungarian funding council OTKA K101192 grant.

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