GLOBAL WARNING PERMIT

A ROQUES INRA Zoologie Forestière Orléans, France

ESENIAS Training Course, Sofia, 3-4 April 2017 Outlines of the talk

 Invasion rate: plateau or not plateau ?  Relationships with trade  Pathways and donor areas are changing with time; a focus on alien in Europe  Recently established alien species are spreading faster than before in Europe. Why ?  Genetic tracking the origin (donor area) is essential  Complex patterns of invasion and new genetic admixtures  How to forecast the next arrivals ?  Effect of climate change probable but not easy to ascertain  Climate change proved to promote invasion: The example of pine processionary in Europe

ESENIAS Training Course, Sofia, 3-4 April 2017 I- Invasion rate: plateau or not plateau ?

ESENIAS Training Course, Sofia, 3-4 April 2017 Recent progresses in invasion studies A novel, worldwide database of established alien species, including data on first records per country/ continent

45,813 first records for 16,926 species

From Plants to mammals

(Seebens et al., Nat.Comm. 2017)

ESENIAS Training Course, Sofia, 3-4 April 2017 No saturation at world level in the establishment rate of alien species

Global temporal trends in first record rates for all and vegetal species at world level

(Seebens et al., Nat.Comm. 2017)

ESENIAS Training Course, Sofia, 3-4 April 2017 The same trend for most groups but inter-taxonomic variations…

(Seebens et al., Nat.Comm. 2017) ESENIAS Training Course, Sofia, 3-4 April 2017 … as well as inter-continental variations

can be largely attributed to the diaspora of European settlers in the 19th century and to the acceleration in trade in the 20th century

(Seebens et al., Nat.Comm. 2017)

ESENIAS Training Course, Sofia, 3-4 April 2017 II- Relationships with trade

ESENIAS Training Course, Sofia, 3-4 April 2017 Clear relationships with trade increase Values of annually imported commodities vs. first record rates for all taxonomic groups

(Seebens et al., Nat.Comm. 2017) ESENIAS Training Course, Sofia, 3-4 April 2017

Focus on terrestrial invertebrates in Europe Globalization is exponentially accelerating alien establishment

Basic data: EU DAISIE 2005- 2008

Update: EU JCR- EASIN 2014 www.easin.org

Rate increase due to phytophages whilst the other groups decreased during the last period

ca. 11.5 new phytophagous species per year since the Roques, 2010 Biorisks 2000s (4.5 during 1950-75)

ESENIAS Training Course, Sofia, 3-4 April 2017 Establishment rate is increasing significantly more in species related to woody plants than in species linked to herbaceous and crops

Europe

(Roques et al., Biol. Inv. 2016)

ESENIAS Training Course, Sofia, 3-4 April 2017 2-fold more establishments from 2000 on of alien associated to woody plants than during 1950- 1975

465 exotic arthropods related to woody plants established in Europe by 2016

• 405 insects • 60 mites

ca. 8 new species per year since the 2000s 2,1x more Likely related to the recent ‘blooming’ in ornamental trade

(Roques, 2010 NZJF updated)

ESENIAS Training Course, Sofia, 3-4 April 2017 III- Pathways and donor areas are changing with time

ESENIAS Training Course, Sofia, 3-4 April 2017 Accidental introductions largely dominant vs. intentionnal ones in invertebrates

Deliberate Escape Contaminant Stowaway

Plants 17% 51% 20% 13% Mammals 64% 36% 0% 0% Birds 88% 12% 0% 0% Amphibia 70% 21% 5% 4% Marine 7% 30% 30% 33% Freshwater 59% 31% 7% 3% Invertebrates 7% 3% 72% 18%

ESENIAS Training Course, Sofia, 3-4 April 2017 Identify a pathway: not so easy !

• Intercepted vs established 1995- 2012: only 7 species over 117 established ! o Anoplophora chinensis (Coleoptera: Cerambycidae) P4P, bonsais o Anoplophora glabripennis (Coleoptera: Cerambycidae), WPM, bonsais o Cydalima perspectalis (: Pyralidae), P4P o Horidiplosis ficifolii (Diptera: Cecidomyiidae), P4P o Paysandisia archon (Lepidoptera: Castniidae), P4P o Singhella citrifolii (Hemiptera: Aleyrodidae), P4P o Leptoglossus occidentalis (Hemiptera: Coreidae), Hitchhiker

(Eschen, Roques & Santini, Div & Dist., 2014)

ESENIAS Training Course, Sofia, 3-4 April 2017

An example: Most likely pathway for alien insects related to woody plants Ornamental trade more important than forest products

% exotic invertebrate species related to woody plants in Europe 0 20 40 60 80 100

437 Plants for planting 80 But based on species’ biology… 48 Seeds/ fruits 0 Europe- Total Actual pathway could be 45 UK largely different Fresh wood 3 e.g. hitchhiking for a

17 number of species ! Wood packaging 0 Europe- Daisie UK- Smith et al., 2007

ESENIAS Training Course, Sofia, 3-4 April 2017 The trend tended to increase during the recent period

100 90 80 70 Plants for planting

Bark Seeds/ Fruits Wood Packaging Source: Daisie, 2008 20 Rounwood/ Sawnwood 16 12 8 4 0 Percentage of arrivals per pathway pathway per arrivals of Percentage 1850-1899 1900-1949 1950-1974 1975-1999 2000-2007

ESENIAS Training Course, Sofia, 3-4 April 2017 Another way to identify the invasive pathways ? Looking at the colonization by exotic insects of tree species growing in Europe

Exotic trees planted in Europe more colonized than native trees

The top 10 spp. includes Citrus, Palms, Eucalypts

A number of insects arrived along with the exotic host

Most did not switch (yet) onto natives (51%) (Eschen, Roques & Santini, 2014, Div & Dist.)

ESENIAS Training Course, Sofia, 3-4 April 2017 Temporal changes in colonization tends to reflect the invasive processes

Looking at large taxonomic groups during the last period

Faster increase in deciduous, shrubs, palms

vs.

decrease in conifers and slowering in fruit trees

(Eschen, Roques & Santini, 2014, Div & Dist.)

ESENIAS Training Course, Sofia, 3-4 April 2017 New trends in colonization of native angiosperms by alien arthropods

Increase in: • Fraxinus • Salix • Castanea

Stable in: • Quercus

ESENIAS Training Course, Sofia, 3-4 April 2017 Large differences between families Fast increase in Myrtaceae (Eucalypts), Fabaceae (exotic legume trees), Rutaceae (Citrus), Arecaceae (palms) but decrease in Pinaceae and Fagaceae

per family

(Eschen, Roques & Santini, 2014, Div & Dist.)

 A link with climate change ?  Most used as plants for planting and not for wood

ESENIAS Training Course, Sofia, 3-4 April 2017 New trends in colonization of native gymnosperms by alien arthropods

Increase in: • Pinus

Decrease in: • All others

ESENIAS Training Course, Sofia, 3-4 April 2017 Temporal changes in origin of the established species New couples: Origin x Donor (imported) tree species

Asia turned dominant as area of primary origin

ESENIAS Training Course, Sofia, 3-4 April 2017 Coherent with the temporal changes in the trade of plants for planting

NA

Origin of the import of live plants in the EU

Eschen et al., 2014 FEM Asia

AUS- NZ

ESENIAS Training Course, Sofia, 3-4 April 2017 Plants for planting but not precluding the trade of wood and derivates as a pathway!

Wrong to consider only this pathway with regard to recent invasions: o Wood packaging still as issue:  Aromia bungii  New outbreaks of A. glabripennis o Wood trade, too:  exotic ambrosia beetles trapped in Italian ports (Ambrosiodmus rubricollis, Cyrtogenius luteus, Xylosandrus crassiusculus; Rassati et al., 2013) o Hitchhikers in commodities:  Leptoglossus bugs

ESENIAS Training Course, Sofia, 3-4 April 2017 IV- Recently established alien species are spreading faster than before in Europe

Why ? Arrivals mostly through continental Italy and France

ESENIAS Training Course, Sofia, 3-4 April 2017 It took a long time for many alien species to colonize the whole Europe

Area colonized in 2015 with regard to the date of first record of each alien

(Roques et al., 2016)

ESENIAS Training Course, Sofia, 3-4 April 2017 Accidentally-introduced species spread faster than intentionnaly- introduced ones

ESENIAS Training Course, Sofia, 3-4 April 2017 No differences in spread speed with regime

ESENIAS Training Course, Sofia, 3-4 April 2017 Since 1989, a much faster spread across Europe of alien insects after the establishment

(Roques et al., 2016 Biol. Inv)

ESENIAS Training Course, Sofia, 3-4 April 2017 Spread before and after the collapse of the Iron Wall and the EU enlargment

ArrivalArrival duringduring 19501950--19881988 Arrival during 1989- 2004 Arrival during 1989- 2004

ESENIAS Training Course, Sofia, 3-4 April 2017

For a number of important species > 15 years to invade all of Europe vs. dozens of years before

Explosion of ornamental trade combined with collapse of Berlin Wall and release of EU internal border controls (Roques et al., 2016)

ESENIAS Training Course, Sofia, 3-4 April 2017 Examples of very fast spread West to East I- the American Honeysuckle leaf gall-midge (first record 2003)

Honeysuckle leaf gall-midge Obolodiplosis robiniae 2003 (North America) 2004

2006

2007

2008 2009

2010 2011

ESENIAS Training Course, Sofia, 3-4 April 2017 Examples of very fast spread West to East II- The Asian elm zigzag sawfly (first record 2003)

The elm zigzag sawfly 2003 (China) Aproceros leucopoda 2006

2009

2010

2011 2013

ESENIAS Training Course, Sofia, 3-4 April 2017 Faster spread especially obvious for recent aliens associated with eucalypts and palms

 Eucalypts: foliage feeders and gall-makers (Ophelimus maskelli, Leptocybe invasa, Glycaspis brimblecombei, Blastopsylla occidentalis, Thaumastocoris peregrinus) colonized most of the Mediterranean countries in less than 10 years

vs.

a much slower colonization rate by Phoracanta spp. (arrival 1969 and 1992) and Gonipterus spp. (arrival 1975 and 1991)

ESENIAS Training Course, Sofia, 3-4 April 2017 An invasion East to West: Polygraphus proximus, a threat for European fir moving westwards with new fungal association

Introduced from the Russian Far East to Southern Siberia presumably late1980s Beetle’s success related to lack of fir resistance to an associated blue stain fungus Grosmannia aoshimae (Baranchikov, 2013)

ESENIAS Training Course, Sofia, 3-4 April 2017 The invasive pathway: the transsiberian railway

(Baranchikov, 2013)

ESENIAS Training Course, Sofia, 3-4 April 2017 Another East- West highly-threatening dispersal EAB progression westwards from European Russia Human-aided transport from the native Far East First record in Moscow in 2003

wind protection forest belt (near the town of Puschino, 2012) (Photo: Y. Baranchikov)

ESENIAS Training Course, Sofia, 3-4 April 2017 Rapid expansion from Moscow towards West

201 3

(Orlova- Bienkowskaja, 2013) (Baranchikov, Kurteev, 2012)

An accelerating effect of the Ukrainian conflict ?

ESENIAS Training Course, Sofia, 3-4 April 2017 EAB invasion is favoring the expansion of a native species related to ash, A. convexicollis

201 Dark gray: invasive range of A. 3 planipennis

Light gray: native range of A. convexicollis

Triangles: localities where A. convexicollis was found outside its native range in 2007–2013.

Bienkowskaja & Volkovitsh Biol Invasions (2015) ESENIAS Training Course, Sofia, 3-4 April 2017 V- Genetic tracking of the origin (donor area) is essential

ESENIAS Training Course, Sofia, 3-4 April 2017 Example of very fast spread West to East The Asian box tree moth, Cydalima perspectalis

2006 2007 Probably arrived 2008 from China in 2005 2010

2011

2012

2013

2014

ESENIAS Training Course, Sofia, 3-4 April 2017 Rapid spread towards Central Asia along the Black sea, resulting in heavy damage

A north route with the Sotchi games and a south route from Turkey

Krasnodar- 2012 Sotchi- 2013 Chechen Rep- 2013 Abkhazia, Georgia (Adjara, Samegrelo- 2015 but probably 2013) Heavy damage in Adjara in 2015 (M. Kenis courtesy)

ESENIAS Training Course, Sofia, 3-4 April 2017 Genetic analysis revealed the probable routes Multiple introductions followed by human-mediated dispersal with ornamental trade

COI, mtDNA

Spatial genetic structure with 3 geographic regions (West Europe, Central Europe, East Europe and Central Asia) Bras et al, 2016

ESENIAS Training Course, Sofia, 3-4 April 2017 A similar scenario for the highly-threatening Asia long-horned beetle, Anoplophora glabripennis

Several introduction events followed by a spread within Europe (Javal et al., 2016)

ESENIAS Training Course, Sofia, 3-4 April 2017 Genetic markers proved the horse-chesnut leaf miner, Cameraria ohridella to originate from the Balkans

Photo: D. Lees

COI mtDNA (barcode fragment - 658 bp) Confirmed by analysis of herbarium and sequencing of old samples

(Lees et al., 2011, Frontiers Ecol. & 25 haplotypes Only haplotype “A” is dominant (67–100%). Envir.) Valade et al (2009), Molecular Ecology

ESENIAS Training Course, Sofia, 3-4 April 2017 VI- Complex patterns of invasion and new genetic admixtures

ESENIAS Training Course, Sofia, 3-4 April 2017 Bridgehead effect A particular invasive population serves as a source for subsequent invasions (Lombaert et al. 2010)

• Genetic recombinations from different sources • Adaptative patterns and genetic drift Hybrids more The Harlequin ladybird, Harmonia axyridis • aggressive (Lombaert et al., 2011, PLoSOne)

ESENIAS Training Course, Sofia, 3-4 April 2017 Temporal patterns of invasion by seed bugs, Leptoglossus occidentalis

Western American conifer bug invasion in Europe 2011 (Leptoglossus occidentalis) 2009 from its arrival in Italy in 1999 2009 2008 2011

2007

2007 2007

2006 2006 2005 2009 1999 2004 2002 2003 2006 2006 2008 2010 2009 2008 2003 2004

2008 2003 Lesieur et al., submitted

ESENIAS Training Course, Sofia, 3-4 April 2017 A Western US (bug native range) origin for the European invasion ?

DNA Unsampled population analyses and in eNA Approximate Bayesian Computation (ABC) eNA Italy wNA approach : wNA population admixture eNA-wNA X X Best scenario for the origin of the population of Northern Italy

ESENIAS Training Course, Sofia,X 3-4 April 2017 Multiples introductions and bridgehead effect in bug invasion

DNA Unsampled population analyses and in eNA ABC techniques:

Best scenario Admixtures… for the origin of the population of Barcelona, Spain

X

ESENIAS Training Course, Sofia, 3-4 April 2017 The most reliable scenarios for Leptoglossus European invasion

 Multiple independent introductions : - at least 2 in Italy and Spain - Probably much more : NW France, Spain, …  Source for all: not wNA but eNA= Bridgehead effect  Movements within Europe: flight+ hitchhiking

ESENIAS Training Course, Sofia, 3-4 April 2017 Temporal patterns of invasion by the blue gum gall wasp, Leptocybe invasa, in the Mediterranean basin

Direct trade of Eucalypts with Australia more limited: Exchanges of ornamental plants for planting and/or cut foliage likely responsible for the invasion… from one Mediterranean country to the others

ESENIAS Training Course, Sofia, 3-4 April 2017 Bridgehead effect probably more common than expected in relation with the explosion of ornamental trade

 Significant consequences

 Important to consider systematically the donor area, not only the native range  Necessity to test for behavioral consequences of potential hybridization from different genetic sources and from populations having been submitted to strong bottlenecks

ESENIAS Training Course, Sofia, 3-4 April 2017 Even more complex: Where does come from the Lime leaf miner, Phyllonorycter issikii ? East or West ?

Moscow

*2011 *2009 *2008

*2003 *1992

*2005 Moscow *2004 *1985 *2004 *1999 *1992*1995 *1995 *2006

- Tilia range - P. issikii invasion *2008 *2012 *2010 (Kirichenko et al., Plos One 2017) *1977

ESENIAS Training Course, Sofia, 3-4 April 2017 Contradictory high genetic diversity in the putative invaded area vs the native one !

COI mtDNA (barcode fragment - 658 bp)

6 unique haplotypes in RFE 1 unique haplotypes in Japan

(Kirichenko et al., Plos One 2017)

ESENIAS Training Course, Sofia, 3-4 April 2017 VII- How to forecast the next arrivals ?

ESENIAS Training Course, Sofia, 3-4 April 2017 Relying on interceptions to predict the arrivals ? Large discrepancies with establishments !

Intercepted vs established 1995- 2012: (Eschen, Roques & Santini, 2014, Div & Dist.)

The major problem: only A1 and A2 pests targeted Most new species: unknown as pests in countries of origin (cf EAB)

ESENIAS Training Course, Sofia, 3-4 April 2017 How to forecast and detect precociously the next arrivals ? A number of EU projects to develop novel strategies

 Preventive warning:  Lists based on the pests known in the native range: most newly-arrived species not considered as pests … or Unknowns  Sentinel plantings of European plants in exotic countries  Sentinel nurseries of exotic plants in exotic countries  Survey of arboreta and botanical gardens with European plants Former EU projects PRATIQUE, ISEFOR & PERMIT At present COST ‘GLOBAL WARNING’ and IPSN

 Early detection at arrivals:  Test of multiplex traps and lures with generic attractivity in ports-of entry French PORTRAP project (2015-2016), proposed EUPHRESCO project “Multi-lure and multi-trap surveillance for invasive tree pests”

ESENIAS Training Course, Sofia, 3-4 April 2017 Sentinel plantings: 7 European trees species in China (2008-2011) survey for 3 years for insect and pathogen colonization

Beijing suburban area Continental conditions INRA- CABI

Fuyang, nr. Hangzhou Warm and humid climate INRA- IOZ- ZAF

ESENIAS Training Course, Sofia, 3-4 April 2017 Experiments designed for statistic analysis of colonization by insects and pathogens ….. ….. Abies alba ….. ….. Quercus suber ….. ….. Cupressus sempervirens ….. ….. Quercus petraea ….. ….. ….. ….. 100 seedlings per site Fagus sylvatica ….. ….. and species Quercus ilex ….. ….. ….. ….. Carpinus betulus …..…. ….. ….. ….. ….. ….. Random planting of ….. ….. blocks of 25 seedlings ….. ….. ….. …..…. ….. ….. All seedlings individually tagged ….. …..

ESENIAS Training Course, Sofia, 3-4 April 2017 105 insect species colonized the seedlings in 3 yrs 3 years enough to check species recruitment Top species not incidental> 15 occurrences over several years: A list of 39 threatening species

5 candidates for PRA

Pteroma nr. pendula (positive tests under quarantine conditions)

Same for pathogens

ESENIAS Training Course, Sofia, 3-4 April 2017 Sentinel nurseries taking into account the role of ornamental trade (2012- 2014) 71 insect species in >20 families, most not included in Chinese lists

Selection of the 6 most imported woody plants from China to Europe during 2008- 2011

No treatments to follow the « freely » colonization by insects and pathogens

Large differences among tree species after 3 yrs

Would have allowed to warn about the arrival of the invasive boxmoth, Cydalima perspectalis

Kenis et al., in prep.

ESENIAS Training Course, Sofia, 3-4 April 2017 COST GLOBAL WARNING: An attempt to promote sentinel strategies … but there are limits

• A manual in preparation for assigning observed damage to insects and pathogens in broadleaved and conifer sentinel plants (End 2016)

• Many specimens (larvae, eggs) not identifiable by morphological keys (some may be unknown to Science)

• Necessity of molecular librairies (barcodes) but nothing for some taxa

• Mostly foliage pests, no pests of mature trees (xylophagous, seed/ fruit insects, …)

• Role of travel and plantation stress difficult to assess

ESENIAS Training Course, Sofia, 3-4 April 2017 Arboreta surveys another method for identifying potential invaders and for early detection of invaders

- Inspection of European trees and shrubs in arboreta and other plantations in other continents

- Inspection of arboreta/ gardens in Europe

IPSN Conference, Kew, UK, 24 February 2016 A significant example : Survey of rose seed infestation by seed chalcids in major European botanical gardens

Survey 2014- 2016: Detection of 5 exotic species of Megastimus seed chalcids in MNHN Paris and Kew gardens

No alien chalcids outside these gardens yet: Arboretum= trap for aliens ?... and early warning Pathway= uncontrolled seed exchange (no X-rays) between gardens ?

ESENIAS Training Course, Sofia, 3-4 April 2017 VIII- Faciliting effect of climate change probable but not easy to ascertain

Faster increase in colonization of tropical/ subtropical alien trees vs. natives

Link with • Climate change ? • Change in trade because most exotics used as plants for planting and not for wood ? • Both ?

(Eschen, Roques & Santini, 2014, Div & Dist.)

ESENIAS Training Course, Sofia, 3-4 April 2017 The rate of colonization of exotic Eucalypts much faster than that of native deciduous

Since 2000:

2000: Ophelimus maskelli 2002: Ctenarytaina spatulata 2003: Leptocybe invasa 2006: Blastopsylla occidentalis 2006: Ctenarytaina peregrina 2007: Glycaspis brimblecombei 2011: Thaumastocoris peregrinus

A further analysis at the tree species level necessary

ESENIAS Training Course, Sofia, 3-4 April 2017 The rate of colonization of exotic Citrus much faster than that of native fruit trees

Since 1998: 1998- Brevipalpus californicus 1998- Brevipalpus phoenicis 1998- acuta 1998- Singhiella citrifolii 2000- Acaudaleyrodes rachipora 2000- Anoplophora chinensis 2001- Eutetranychus banksi 2001- Icerya formicarum 2007- Acharia stimulea 2007- Aleuroclava aucubae 2008- Aleurocanthus spiniferus 2009- Lopholeucaspis japonica

ESENIAS Training Course, Sofia, 3-4 April 2017 The same story for alien insects on palms

Palm weevil, Rhynchophorus ferrugineus, palm moth, Paysandisia archon, leaf beetles, …

The invasive moth and weevil recorded from the Canary islands or continental Spain from the late 1990s… but without spreading elsewhere 2004- 2007: Colonization of the whole southern Europe

One certainty: the role of Athens’ Olympic games in 2004 with large imports of Spanish palms

Warming up: release of thermal barriers for expansion ?

ESENIAS Training Course, Sofia, 3-4 April 2017 IX- Climate change proved to promote invasion:

The example of pine processionary moth

ESENIAS Training Course, Sofia, 3-4 April 2017 Pine processionary moth (PPM), a model for climate change (IPCC) An insect native of the Mediterranean Basin, with a winter larval development

5 larval instars

Possible prolonged diapause

ESENIAS Training Course, Sofia, 3-4 April 2017 Winter warming up= release of thermal constraints constraining PPM range

TEMPERATURE >-16°C +

(Battisti et al. 2005) IMMEDIATE T nest > 9°C T air > 0°C Realized Feeding SURVIVAL (day) (following night) Threshold (RFT) Activation T Potential feeding T

FEEDING

(Buffo et al. 2007) LONG-TERM SURVIVAL

ESENIAS Training Course, Sofia, 3-4 April 2017 A latitudinal expansion northwards (and in altitude) A 100 km latitudinal shift in the Paris basin since 1972 with a significant acceleration since 1992

Northwards shift - by 2.6 km/yr from 1972 to 2011 Robinet et al. 2010 - by 5.5 km/yr from 1996 to 2011 1996197120112005 Unpubl. data 1992 whilst mean winter temperature increased by 1°C

Mean minimum temperature from October to March in Orléans (moving mean 5 yrs) 3.55 C+/-0.68 (SD) 4 °

3

2 2.46°C +/- 0.86°C (SD) 1 1972 1980 1990 2000

ESENIAS Training Course, Sofia, 3-4 April 2017 Map of PPM expansion all over Southern Europe The 2012 front edge

PCLIM Project

INRA, with the help of A. Battisti (Italy) P. Mirchev (Bulgaria) G. Georgiev (Bulgaria) M. Dautbasic (Bosnia) D. Matosevic (Croatia) K. Ipekdhal (Turkey) M. Glavendekic (Serbia) I. Papazova (Macedonia) S. Naceski (Macedonia) D. Avtzis (Greece) E. Cota (Albania) T. Manole (Romania) J. Garcia (France, Switzerland) F. Goussard (France, Switzerland) (Roques et al, 2015)

ESENIAS Training Course, Sofia, 3-4 April 2017 Only expanding ? No ! Also a man-mediated invader …. although seems crazy to translocate an urticating pest !

A number of colonies 2003- 2008- 14-60km 2012- 90km appeared far beyond 2008- 190km 2015 the expansion front since the early 2000s

Were do they come from ? The expanding area or far beyond ?

How can they survive far beyond the natural front ?

ESENIAS Training Course, Sofia, 3-4 April 2017 The example of invasion of Paris Basin

« Invasive » colonies recently detected largely beyond the natural front (Roques et al., 2014)

ESENIAS Training Course, Sofia, 3-4 April 2017 Limited female flight capabilities and particular population genetic structure Colonies = long-distance jumps from southern areas !

Females fly at more 11km (a few)

DNA microsatellites assigned colonies to southern populations, not to front

Robinet et al. Biol. Inv. 2012

ESENIAS Training Course, Sofia, 3-4 April 2017 Convergent genetic and biological data: Populations not coming from the front edge but from very long distances

The likely pathway: Many PPM nests

The trade of mature trees moving processionary pupae with soil from southern France (> 800 km) (Robinet et al., 2012 Biol Inv)

The same pathway for the invasion of UK by the oak processionary moth (Evans, 2008)

ESENIAS Training Course, Sofia, 3-4 April 2017 The northwards/upwards shift of isotherms allows survival where it was impossible before

Obernai (French- German border):

49.2 49.2 0.5 Saarebrücken 49 Metz 49 0.45 Karlsruhe 0.4 48.8 48.8 Nancy 0.35 48.6 48.6 Strasbourg 0.3 48.4 48.4 Obernai 0.25 48.2 48.2 0.2 48 48 0.15 47.8 47.8 0.1 Basel 47.6 47.6 0.05 6.2 6.4 6.6 6.8 7 7.2 7.4 7.6 7.8 8 8.2 6.2 6.4 6.6 6.8 7 7.2 7.4 7.6 7.8 8 8.2 période 1988-1997 période 1998-2007 Establishment impossible in the early 1990s; colonies established since 2007 from accidental transportation with black pines used for runabouts

ESENIAS Training Course, Sofia, 3-4 April 2017 Most invading colonies proceed from management using ornamental plantations of mature pines

Ornamental pines along as corridors and relays for PPM dispersal (Rossi et al., 2015)

ESENIAS Training Course, Sofia, 3-4 April 2017 Urban heated islands: PPM survival is even favoured in large cities once colonized

Pontoise Severe 15-day cold period in the 75.8% 75.9% Paris basin during January 2009 81.7% PARIS 79.1% -13 2009 -12.5 -12 2004 75.1% 74.0% -13 1996 -14

1992 70.5% Nb hours where T<0 1972 Orléans 71.6% Absolute minimum T % larval survival

Robinet et al. Biol. Inv. 2011

ESENIAS Training Course, Sofia, 3-4 April 2017 A changing parasitoid complex: Expanding PPM populations escape from egg parasitoids Colonies beyond front with only pupal parasitoids

Significant decrease in parasitism from endemic areas to front edge

High frequency of c egg parasitoids

hole of c parasitoid c

bc hole of b bc b b caterpillar a a a a a a a a b No parasitoids or only pupal ones (Imbert, 2012) Less egg mortality may allow larger PPM colonies at the front edge and in isolated colonies, ie better winter survival in colder places

ESENIAS Training Course, Sofia, 3-4 April 2017 All of Europe and Minor Asia likely to become favorable for PPM invasion in the near future

Probability of PPM establishment under different temperature increase scenarios

Any long-range transport with potted pines from the native range is likely to generate colony establishment

(Robinet et al., 2015)

ESENIAS Training Course, Sofia, 3-4 April 2017

An important question remains: PPM adaptations at the front edge and in colonies beyond front ?

Different genetic markers show that the front population is a mosaic of new, unexpected genetic combinations

Possible adaptations at the front edge - Larger flight capabilities and adapted morphology and carbohydrate content ? - Better cold resistance ? - Advanced phenology ? - Fertility (Egg load) - Nest size - Lower urticating capabilities (no. setae and allergen content) in relation to escape from natural enemies - Increased man/ animal sensitivity in

Paris Basin 2015- 2016 newly-colonized zones ?

ESENIAS Training Course, Sofia, 3-4 April 2017 Conclusions and take- home messages

 Invasions are accelerating with globalization without any saturation  Insect invaders mostly arrive with plants for planting but wood and derivates are still to be considered  Hitchhiking is a serious problem difficult to be adressed  Present EU inspections simply focusing on quarantine pests are not efficient  New combinations origin * commodity have to be focused on  Possible bridgehead effects have to be systematically considered as well as the donor area and not only the native area of the species  Possible new associations (insect* fungus*nematode) between invaders and natives to be systematically checked  The release of barriers in EU accelerate the invasive spread  Relationships between invasions and climate change are still a black box in most cases although recent establishement of species related to subtropical hosts suggest a facilitation.  Such facilitation is proved for the pine processionay moth whose actual expansion results from the combination of global warming, the development of ornamental pine plantations, and the increasing trade of mature trees

ESENIAS Training Course, Sofia, 3-4 April 2017

Thank your for your attention !