Role of Insect Vectors in Epidemiology and Invasion Risk of Fusarium Circinatum, and Risk Assessment of Biological Control of Invasive Pinus Contorta Eckehard G

Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum, and risk assessment of biological control of invasive Pinus contorta Eckehard G. Brockerhoff, Margaret Dick, Rebecca Ganley, Alain Roques, Andrew J. Storer

To cite this version:

Eckehard G. Brockerhoff, Margaret Dick, Rebecca Ganley, Alain Roques, Andrew J. Storer. Role of insect vectors in epidemiology and invasion risk of Fusarium circinatum, and risk assessment of biological control of invasive Pinus contorta. Biological Invasions, Springer Verlag, 2016, 18 (4), pp.1177-1190. 10.1007/s10530-016-1059-8. hal-02632311

HAL Id: hal-02632311 https://hal.inrae.fr/hal-02632311 Submitted on 27 May 2020

HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Copyright Version postprint vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Zealand, Eckehard G. Brockerhoff, (New Scion Zealand Forest Research Institute), Christchurch, New Correspondence: h Institute), Researc Rotorua Forest Zealand (New Ganley, Scion Rebecca 2812 Andrew Storer, of School Forest J. R Alain Roques,INRA Zoologie –UR0633, Forestière, 40001,45075 de 2163Av.CS Pomme pin, Rotorua, Institute), Research Forest Zealand (New Scion Dick, Margaret Eckehard G. Brockerhoff, (New Scion Zealand Forest Research Ins F

Biological Invasions Biological to or submission Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect circinatum [email protected] Technological University, 1400Townsend Drive, Houghton, MI 49931,USA,e [email protected] [email protected] Zealand, Orléans, France, e- France, Orléans, Role of insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : e - mail: [email protected] e -

mail: [email protected]: , and risk assessment of biological control of invasive

vectors mail: [email protected]:

Comment citer cedocument: in epidemiology and invasion risk 10.1007/s10530-016-1059-8 esources and Environmental Science, Michigan

contorta

, Tel +64 3642949,Fax+64 364

titute), Christchurch,titute), New New Zealand, New New Zealand , New

Fusarium Fusarium

Pinus Pinus - mail: e , e - mail: - mail: 1 Version postprint 10 11 13 12 15 14 23 22 21 20 19 18 17 16 1 2 9 8 7 6 5 4 3 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Pitch canker Pitch Abstract sp may pines could be introduced as biological control agents of invasiveand contorta Pinus how plantationforestsradiata and urban trees wounding agents or vectors assess and worldwide canker infe from disease, as wounding agents allow across five continents Pinaceae in New Zealand, there are only few pine insects, only are pine there few mainly Zealand, New in accidentalPinaceae introductions risk insect the of there is uncertainty about its ability to act as vector of F. circinatum validirostris Keywords potentialthe impacts F. circinatum of assess to framework ageneric as used be can associates pine of potential vector the and evaluate ecies. . Of potentially six suitable biocontrol candidates affect the affect impact o Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : It a is threat natural to and planted pine forests, and date to it

c ted to healthy trees. to ted Cone and seed insects; invasive alien species; pathogen vectors; pitchcanker species; alien invasive insects; seed and : Cone s is , caused by the pathogen circinatum Fusarium recorded New onpines in Zealandlikely is to be host specificity host the most and promising impact onseed production , but regarding . Pine f a potential F. circinatum - to determine whether feeding insects can play a key role the in epidemiology of the ed W present in New Zealand that Zealand may New in as act present are insects which e review Comment citer cedocument: 10.1007/s10530-016-1059-8 ing pathogen access or as vectors t vectors as or access pathogen . invasion . W ed the role of insectsthe in epidemiology of pitch also evaluated e also

pat . As invasion there are nonative pines or other , the European pine cone weevil Pissodes Pinus Pinus adverselyhogen affect could invasion , is a, is serious disease of pines, Pinus cone or seed or cone whether avector Our methodology. Our review to ransmitting has , suggesting invaded countries the pathogen of of insects low disease disease low

. None this 2 Version postprint 25 24 27 26 28 29 30 35 34 33 32 31 48 47 46 45 44 43 42 41 40 39 38 37 36 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological

Pitch canker Pitch Introduction has emerged as a particularly damaging aparticularly as emerged 2008). Since thehas 1980’s it pines ( some of disease serious Don the in native range pinevarious ofin pa this al. 2008) Italy). forSpain, example), restricted nurseries to (as reported from Chile),or parks and gardens (as in among regions and species, host and symptoms forests commonin be and (as can plantations in et al. 2007; Brazil nt, andnt, consequently prese are Pinaceae native no mainly because insects, associated P where hemisphere 1996; access or as vectors of the pathogen from infected healthy to trees et (Fox al. 1991; an roleallow important pathogen the in infection process, as wounding agents of trees thatmay California in haveStudies shown tha (Ganleydisease et al. 2009) aclimatehave that is suitable for establishmentof the fungus and development of pitchcanker dis plantation disease remained confined nurseries to 2005w until /Central America ( 2001). The America pathogen assumed originate is to /Central from Mexico ease has yet not been recorded, including Zealand New Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect Storer et al. 1998; has invaded the has United it where States from ere pitch canker was first detected in 1990 (Viljoen et al et (Viljoen 1990 in detected first In was canker Africa, South wh pitch ere and Italy and control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : s ( Province Cape the in Western Wingfield et al. 2008; , caused by the pathogen circinatum Fusarium , affecting inus Storer et al. 2004a al. et Storer relatively are there tree, exotic an as widely planted is radiata a range of pine species (Dwinell 1999; . Pinus spp.)Pinus ( Comment citer cedocument: 10.1007/s10530-016-1059-8 Pfenning et al et Pfenning t bark - Coutinho et al. 2007) Coutinho ). In New Zealand and other countries the in southern insects play insects seed and cone as well as insects feeding Dick 1998;

). T . 2014). rts of California (Storer et al.Gordon 1997; et California of rts , Haiti, Japan, South Africa, South , Haiti,Japan, Spain Chile, hen an outbreak was reported young in Gordon et al. 2001; China, and, China, Australia he extent of disease problems varies varies problems disease of extent he (Nirenberg and O’Donnell Several countries where the the where countries . Several Wingfield et al. 2002; D radiata Pinus of disease Wingfield et al. , are thought to Wingfield et al. . 1994), the Hoover et al. et Hoover no are there ) is a , is few few Carlucci Carlucci

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Storer et al. ( al. et Storer potential as Zealand introduced over the years. P their direct impact is mostly pests insect benign. several However, native specialised insect herbivores. Occasionally, some native insects attack pines, although invaded natural or semi act insects are specialised, adapted species that exhibit a high degree of host degree of ahigh exhibit that species adapted specialised, are insects trees of parts other to damage causing or growth affecting and se highly valued plantationforestry in and urban also in amenity plantings assessed (Brockerhoff and Kay 1998; serious invader among the pines (L plantings of P vectors of F. circinatum aformal However, there. established became ever it if plantations, (Turgeon et al. 1994) an informed response the in event of an incursion of F. circinatum Knowledge biological control of wilding for an assessment of the riskof of theintroduction potentialintentional seed- (Gadgilspread et al. 2003; ( considered environmental weeds New in Zealand and other southern hemisphere countries Richardson and Higgins et Rundel al. 1998; 2014 as vectors of the fungus, may and this the spread limit of the fungus impact and onpine its Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect ed a insects is favoured approach as control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : about any potential ). Currently, there appear to be few insects in New Zealand that are likely to likely are to that Zealand New in insects few be to appear there Currently, 2004b). inus contorta were contorta of limited extent, this species is now considered the most vector , therefore limiting risks to non - in New Zealand is not available Zealand New in natural grassland and scrub (Ledgard communities 1998). Although Ganley 2007; s reliminary of F. circinatum of have (invasive) is necessary is associates insect other and vectors disease Comment citer cedocument: 10.1007/s10530-016-1059-8 edgard 1998).for Options biological control have been are are species Brockerhoff pine et several al. 2004). Because review . Several pine species pine Loudon contorta Pinus Several . Fourrier vecto The et al. 2015). such insects may reduce the spread of pines without s of

the role of the been provided by been Gadgil et al. (2003) and ). ). In - target plants some regions of New Zealand New of regions some . . I addition, most cone most n addition, and seed insects associated with pines in New New in pines with associated insects . On the other hand, seed- of pines potential the analysisof and evaluate to the riskof , t plant r issue is also important he potentialuse of cone have become become have feeding insects for for insects feeding specificity are now now are , pines have to enable enable to eating eating 4

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implications for vectoring F. circinatum biocontrol agent selection preliminary the review also We may Zealand vectors. New as act in present insects which Here we review the role of insectsthe in epidemiology of pitchcanker world- approach. the in interest renewed introduce a cone insect for biocontrol of invasive pines (Lennox e vector of the pitchcanker pathogen . In Africa, South such concerns have circinatum ofintroduction such insectsNew to Zealand wouldgreatly increase the associated risks with F. and Kay 1998; show promise as potentialbiocontrol agents, New in both Zealand Africa and South (Brockerhoff specificity, potentialimpact onseed production and other criteria, some insects are thought to P attack that insects seed and cone of areview on Based es plantspread actually reduc rates effect (e.g., their Rees and Paynter whether determined 1997). insects may be not as effective as other types of biocontrol agents, andremains it be to iii. ii. i.

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : establishment of F. circinatum risk the assess to and Zealand to evaluateto the insects potentially suitable for biocontrol of P vector as acting species ofthe these likelihood reviewto the native and introduced insects found New onpines in Zealand, determine to epidemiology disease canker pitch with associated insects the of overview an provto ide of biocontrol agents against invasive pines and the explore of risks introducing such because the biocontrol agent may act as an additional,and potentially important, Brockerhoff et al. 2004; s to New to Zealand, particularly regard with our to current knowledge about in the countries where the disease occurs to date; to occurs disease the where countries the in Comment citer cedocument:

10.1007/s10530-016-1059-8 of the ; and ; Roqueset al. 2004). However, feared is it thatthe . Our

ir introduction in relation in introduction the to potential specific objectives are: are: objectives specific

s of F. of inus circinatum , considering contorta host t al.t 2009) inus ;

in New in contorta halted plans to and their role in , although there is wide and assess

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th agents, vectors circinatum carriers and Wounding Fusarium of which among is susceptible the species most of pine (Correll et al. 1991; California in studied where of pitchcanker disease has become amajor otherin regions insects appear play to a role. minor insects Associations with have been best In some regions insects have been play shown to an role important the in infection process while the pathogen, and visiting susceptiblean organismplant hosts, met (Leach 1940). These being to state addition thatin associated diseased with carrying plants, have developed. However, order in be to classified as a ‘vector’ ‘carriers’ because they carry from inoculum diseased they plants either or visited onwhich they are insects Some by made beetles. bark those as such tunnels via or cuticle damaged the via Storer et al. 2002). Insects can act as ‘wounding agents’ that example, if they if example, for vectors, successful necessarily are inoculum of carriers all Not by species. caused another wounding agents act concurrently as vectors a but vector can also cause an infection via a wound transmitting with diseasedwith or healthy plants host therefore consider to important the differences involvement of in the various insects associated

iv. e pathogen Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : circinatum to F. F. of vectors with associated risks of assessment the for framework ageneral develop the pathogen thatwere plants to yet not infected

are causing not any wounding thatwouldbe sufficient for It transmission. is or similar or pathogens Comment citer cedocument: 10.1007/s10530-016-1059-8 and thatcan also be used for other countries. t o classify each species accordingly (T species classify each o

allow the pathogen enter to the plant under controlled conditions must be capable of capable be must , Leach’s, postulates and their interactions with the native the Adams et al. 1999; able 1). able P successfully successfully need be to inus

, radiata . Some . Some

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radiatae andradiatae punctulatus Ernobius feedingshoot and the creation of wounds during The cone oviposition. beetles, Conophthorus colonization by the insect (Storer et al 2004a Pityophthorus during exploratory feedi species insect 2004a al. Ips paraconfusus as such beetles feeding have been vector shown to the pitchcanker pathogen California, in especially bark Insects thatfeed subcortically onlivetrees or thatwound livetrees during exploratory host Supplementary Table S1 Table Supplementary are known wounding agents or carriers none but of these are known vectors (Table 1, 1). Several other species, including and shoot foliage feeders, sap suckers and predatory insects the surface of infected tissues when conditions are moist. These are dispersed by water dispersed are These moist. are conditions when tissues infected of surface the (known as sporodochia) containing thousandsof spores asexual (conidia) may be produced on the nature of potentialinteractions between these organisms. Fruit bodies of F. circinatum i it disease, To assess the role of insectsthe in infection of trees by F. circinatum beetle pheromones (Sa weresuspensions sprayed trees onsmall the in field and the branches were then baited twig with ( apparent bark of trees surface even the when fruit from bodies are readily not recovered be also can Spores and can be carried air in currents throughout the year (Blakeslee et al.Correll 1978; et al. 1991). treated and untreated trees. It likely is thatspore loads were very high these in compared studies Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : ; Erbilgin et al 2008; Adams s important to consider to important s the life cycles of the both pathogen and potentialvectors and ). Twig beetles are thought vector to the pitchcanker pathogen pines also into setosus et al et . 1999). Two rounds of have studies been conducted where spore resulted pitchcanker in infections onthose trees despite the lack of kamoto et al. 2007). The results showed nodifference disease in between ng material. find suitable to host Baiting trees pheromones with of ). ). Table 1 Table beetles, Pityophthorus et (Fox al. 1991) and twig beetles, Comment citer cedocument: 10.1007/s10530-016-1059-8 are also confirmed vectors ( vectors confirmed also are ; see Supplementary Table S1 for an alphabetical listing of of listing alphabetical an for S1 Table Supplementary see ; ). Other thatmay habits resultwounding in include

Hoover et al. 1995,1996; and the epidemiology of the spp. (Storer spp. et - splash Table Table

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Fox et al.Fox (1990) reported of the isolation pathogen from galleries P in spp. of Ips of the body and be trapped amongst hairs and other sur sporodochia may readily pick upmany of the sticky spores that while chewing their way though out diseased Insects tissue. coming into contact with the whatwith occurs naturally. It seems likely thattheperhaps insects pick upspores the in tree, propagule loads ontwoIps surface low.The is appears riskof transmission vary to at different of times the year according to spores. By contrast as well as hyphal fragments include can presumably carry that beetles propagules The trees. discoloured or resinous tissues Once infection has occurred the fungus colonises the sapwood and can be readily isolated from considered an factor important of studies the in vector efficiency (Erbilgin et al. 2009). impact ontree growth. Lesions onbranches girdle the branch port the so distal result from infections transmittedby cone and seed insects wouldprobably have relatively little being the result of a separate infection. Although unsightly, the branch and twig death thatwould other or borers leads death to of the branch insects cone beyond the cone, branch with dead each does spread not great distances the wood. within Infection of a cone, or a cone whorl, vectored by down the branch usually oris shoot arrested at the node (Dwinell et al 1985; be extensive due to the multiple infections.be due theT extensive to multiple Individual trees may crown sustain thus infections for many years. However, crown dieback can nce and for tree circumfere deaththe result to (Gordon et al attacks by bark beetles. trunk attacks Multiple are required order in the cambium around kill to and tree death follow girdling will of the from stem a number of separate infections and/or Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : , itis likely that the importance of casually acquiring spores from the tree species (Erbilgin et al. 2008). Spore loads of twi (McCain et al. 1987; Comment citer cedocument: 10.1007/s10530-016-1059-8 runk infections are often by initiated bark beetles,

Co face structures (e.g., Yamoah et al. 2011). rrell et al. 1991) . 2001; are likely to adhere to the surface surface the to adhere likely are to Storer et al et Storer . H owever g beetles were were g beetles Gordon et al. 2001) . 2002). Bark ion diesion , t he fungus inus ; spread spread radiata . 8

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involved in thought to fumigationsoil undertaken is followed by a high level of Although sanitation. insects are not containers (Gadgil et al. 2003) Zealand nursery New in sonable rea confidence with the outcome predict can (Van Wyk et al. 2012) containerised are plants nursery all where However, rigorous procedures sanitation can reduce disease incidence insignificant to a levels in pitch canker disease has been found be to relative application of fungicides generally will reduce the et al. 2007). Unfortunately, contrast in the to majority of pine nursery diseases where diligent for infection of young seedlings. Insect devastating recorded losses (Viljoen et al. 1994). Unlikeolder in trees, wounds are required not fungus has been reported be to capable of spreading through nurseries very rapidly, with Spread of the pitchcanker disease nurseries in different is from what occurs forests. in The although rare is this New Zealand, woundsfrom could also occur ( would be through initiated infection of wounds created I thealso in absence of any other disease agents (e.g., and Wingfield 2011). Six Ips (especially beetles n the absence of insects vectoring F. circinatum vectoring insects of absence the n such as windand hail Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : be important in the disease epidemiology within nurseries, certain insects may spreading the disease from nurseries surrounding to . spp. and spp. Dendroctonus spp.) can cause considerable mortality of pines ), pruning), or cone collection (Dwinell et al.Gordon 1985; et al. 2001) where are plants reared as both bare nursery root in beds and in . Eradication attempts are likely to resultnursery in closure w Comment citer cedocument: 10.1007/s10530-016-1059-8 - vectored apparently is transmission (Hurley ortant imp not bark stripping by native parrots

to the to trunk of the trees, any infections stem ly ineffective Wingfield pers. (M.J. com.) impacts of of an of introduction F. causes including weather events events weather by including other causes pathogens forests. . Based knowledge, onthis we It is more likely that , chemical control of to a circinatum to (Dick 1998) be be , . In . In hile 9

Version postprint 211 210 209 208 207 206 205 204 203 202 201 200 199 198 197 196 195 213 212 219 218 217 216 215 214 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological America, such as a number of bark beetles and longhorned beetles ( introd are Zealand at lowdensities(e.g., Berndt et al. 2004). Thecommoninsects found New most onpines in primarily polyphagous species, have colonised pines growing New in Zealand, usually occurring closely are ass that insects native no are there a result as and Pinaceae, any or native other pines native no includes flora Zealand New The more or lessspecific pines). to weres classed specie as either these monophagousof (ca. 50%) or oligophagous (ca. 30%) (i.e., pines, including about 30introduced insect species (de North America (north of over Mexico) 1100insect species have been recorded as feeding on fauna asubstantial of is associated there insects. naturally For in occur example, pines Where Zealand New in present vectors Potential a nursery from than byseedlings insects. of thetransmission fungus a to plantationwouldoccur viaplanting out of To obtainan indicationof the relative abundance of insects associated Ne pines in with Nevertheless, the res the Nevertheless, although most over 3000records of formally identified insects.provided This of a list Research Institute) (Bulman 1990). Th Forest Health Database the queried we Zealand

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : of these represent incidental observations of species feed thatdonot onpines. uced species from the native range of pines, mainly from Europe and North ults of this database of this - ults query pine which doreflect Comment citer cedocument: 10.1007/s10530-016-1059-8 of forest health surveillancee database reports contains ociated pines. However, with several native insects,

(maintained by Scion/New Zealand Forest Forest Zealand by Scion/New (maintained Groot and Turgeon 1998). The majority Brockerhoff et al. 2006) feeding insects are most most are insects feeding over 500insect species asymptomatic infected w . 10

Version postprint 228 227 226 225 224 223 222 221 220 229 232 231 230 244 243 242 241 240 239 238 237 236 235 234 233 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological commonly found onpines growing New in Z or dead trees) using information from Scion’s during status the host attack regardto (i.e., live with categorised were associates common These Zealand), and predators or parasitoids (of which several were recorded at but lowfrequencies). association pitchcanker, with exceptfor pine cone insects (of which there are none New in regard their to with overseas considered been have that insects of guilds feeding the all represent relationship. Thecommonly New 25most onpines in Zealand species recorded (Table 2) insect found onpines are probably irrelevant, especially if they have nofeeding or other close only are rarely that insects By Zealand. New in contrast, established become it should disease, most are associates common These Timber Insects Timber Currently there are nohigh - their potential to act as a wounding agent, carrier of F. circinatum or inoculum, vector (Table 2). association the with pitchcanker pathogen. No such species a thatis confirmed vector present is s Pityophthoru or thatwound livetrees during exploratory feedingIps and paraconfusus host as (such been recorded in New from radiata Pinus Zealand, itis those that feed subcortically on live trees bySequaiodendron giganteaattacked cone pyralids (Roques, 1983). Of the insects thathave observed Europe in cones colonize Pseudotsuga to menziesii and of brutia, Pinus therefore unlikely be to able vector to the pathogen livetrees to although has occasionally it pathogen the in United E States. the vector to known species acongeneric has that Zealand New in occurs that only the species is elsewhere, none are currently New in Zealand. knownexist to mollis Ernobius circin F. vector to demonstrated been have that species canker pathogen. insect the Of

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : setosus series (e.g., Brockerhoff and Hosking 2001). species All were then assessed for in California) that could that act Zealand as New vector of in the pitch species risk rnobius Comment citer cedocument: 10.1007/s10530-016-1059-8 likely that would represent the greatest concern regarding concern greatest the represent would that mollis colonises and breeds mostly dead in trees andis it to play to a role the in epidemiology of the pitch canker ealand’s plantation forests and as amenity trees. amenity trees. as and forests plantation ealand’s Forest Health Database and from the Forest and

, an alien anobiid, atum

been been 11

Version postprint 245 257 256 255 254 253 252 251 250 249 248 247 246 258 265 264 263 262 261 260 259 267 266 269 268 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological in New Zealand (Table 2). (Table Zealand New in is knowncarry to is the sp Newin Zealand, although of these most are associated not pines. Among with sap feeding Gadgil et al. (2003) list 14sap- Zealand. New in established circinatum became country where pitchcanker occurs. Therefore, unlikely is it become to anortant vector imp if F. Zealand (Bain et al. 2011). Furthermore, knownbe not to a is carrier it of F. circinatum any in New in generally been uncommon has species the decades several for but trees pine live attack based oncurrent thought not be is to information, a it potentialvector knownattack to is seedlingsater attenuatus has been not isolated from H. ater et al. 1998) P be not consideredshould be to signif species these that suggests feeders sap other with pathogen the of association of lack apparent California.in The absence the of aand spittlebug Zealand feeding New in radiata onPinus (Homoptera:insignicola Coccidae), commonly occur native in an forests d planted radiata Pinus A preliminary evaluation of potential bio Zealand was conducted by Brockerhoff and Kay (1998). T

otential biological control agents for invasive pines control invasive agentsotential for biological ecies California, in only spittlebugs have been be shown to associated pitchcanker with (Storer Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : , can , even though other sap feeding species such as the Monterey pine scale, Physokermes be a carrier of the pathogen of acarrier be ( pathogen in the United States (Storer et al 2004b). In F. circinatum Spain, Of the other species other the Of feeding species as potentialvectors of the pitchcanker pathogen (for maturation feeding) Comment citer cedocument: 10.1007/s10530-016-1059-8 , however, another species the in same genus, Hylastes icant associates of F. circinatum of associates icant logical control agents against wilding New pines in Romón et al. 2007,2008).Romón Nevertheless, , Hylastes ater Hylastes ,

and this Pinus Pinus was species target main he of a genus that arepresentative is could raise its risk status in New Zealand. New in . Sirex noctilio is known to is Hylastes Hylastes

but but

Version postprint 279 278 277 276 275 274 273 272 271 270 283 282 281 280 289 288 287 286 285 284 290 294 293 292 291 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological P disease dynamics (see below). The survey focussed oncone the insectsnatural within range of the agent have not should any other unwanted effects such as a tree to potentialcontribution the target species substantially, and be able to disperse to isolate be compatible the with climate the in target region(s) New in Zealand, reduce seed production of and subspe agents including: the candidate agent have should a range host thatincludes the target species (Brockerhoff and Kay 1998). A number of criteria were applied the in selection of potential n against tha a target controversial species less therefore that is economically important commercialin for plantations several decades, and biocontrol using seed- becausecontorta considered is it invader. important pine the has most been this not Also, planted specific or attacked other parts of trees, which could affect tree growth. tree affect could which trees, of parts other attacked or specific worthy of fur (Brockerhoff and Kay species 1998) of were which six considered be to potentially suitable and was introduced, especially parts in of Europe. Based 16species onthis, were assessed other species of Eucosma of genus are species other albicaulis grandis species this but was disregarded onthewider basisof range its host thatcovers firs ( The North American cone Eucosma moth can rescissoriana significantly reduce seed production, both firsboth and pines. Three other species, nigrans the anobiidErnobius Conophthorus ponderosae Conophthorus beetle cone pine the were effectmore limited onseed production, at least their in natural geographic range. promising Most conicola, and the tortricid tore Cydia

inus Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect contorta and contorta also oncone ins control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : ), A. lasiocarpa and pines ( uld be reviewed as all Hedlin; et al., 1980). However,all as range the host reviewed be species of this uld sho cies, be sufficiently specific host attack wouldnot such thatit non- ther consideration and research (Table 3). The other species were insufficiently host Comment citer cedocument: 10.1007/s10530-016-1059-8 , P contorta Pinus - ects that have colonised the species in areas where the tree tree the where areas in species the colonised have that ects specific, unusual thatE andis it , mayuta be sufficiently specific host they but usually have a

inus , a North American species, and Pissodes and species, American aNorth , monticolaand possibly P d tree In populations. addition, ucosma rescissoriana , the cerambycid Paratimia the ,

feeding insects is is insects feeding target tree species, species, tree target inus Abies Abies

attacks 13

Version postprint 295 304 303 302 301 300 299 298 297 296 307 306 305 308 309 319 318 317 316 315 314 313 312 311 310 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological vali the ability reduce to seed production considerably (Brockerhoff and Kay 1998; uesRoq & El Alaoui El Fels basin Mediterranean the O for New to potentialintroduction Zealand. prioritised P havenot developed adaptations against particular this cone insect. Based onthese findings, we on seed production, possibly because the twospecies co not did - 2004). However, P tunnel (RoquesChina validirostris Pinus leucodermis these species parts in of- south of forest planted of areas large of are knownbe not to attackedpresence the or damaged, despite and P. radiata taedapines Pinus ,belonging the to subsection Australes subsection Ponderosae hartwegii Pinus on arboreta French in recentlywas noticed species of the subgenus Pinus Europein such as lodgepole (Annila pine,contorta Pinus Delplanque 1975; et al. 1988), a (Roques, 1983). attacks Weevil are also recorded onsome North American pines widely planted Mediterranean pines of the subsection Pinaster

ut ofut a of total 21insect species knowndevelop to the in cones of Pinus , thedirostris European pine cone weevil. Both these species have a narrow range host and Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect such as Pinus sylvestris as , P. mugo and such ,P. uncinata,P. nigra subspecies, and P. ing through and the tissues destroyinging the seeds. They attack native pines of the subgenus control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : which allbelong the to subsection Pinus all over the Palaearctic region Palaearctic the over all present is issodes 1983). Larvae issodes validirostris as (A , Pissodes validirostris t is appeared to be the most effect most the be validirostris to appeared lain R 2002). Most other 2002). Most species cause only damage. minor Pissodes of P of but from but western Europe where Pissodes generally where validirostris is very Europe western oques Comment citer cedocument: 10.1007/s10530-016-1059-8 issodes the agent of first choice for more detailed consideration and , unpublished data)., unpublished By contrast, the North American the validirostris section Trifoliae , such as P. pinaster

he most damaginghe most cone from Portugal and Scandi (Gernandt as et al. well 2005), as develop exclusively pine in cones, (= P. (= rudis . C P. validirostris from damage one evolve, and P , P. halepensis ive in terms of its effects ), a member of the the of amember ), of the subgenus Pinus spp. in Europe in spp. and in insect (Roques inus Brockerhoff et al. navia northern to , and P. pinea) may may contorta

1983; 1983; , 14

Version postprint 329 328 327 326 325 324 323 322 321 320 330 331 332 333 338 337 336 335 334 339 340 344 343 342 341 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological c ( preferences respectively, plant host in which correspond the to differences ofthe populations the Iberian Central Peninsula, Europe and Northern/ Eastern Europe, evolutionary lineages. Atleast three phylogeographic lineages were identified corresponding to P species Pinaster validirostris and Roques2001). However, host pines1999) of asthe exotic same are subgenus subgenuss Strobu (Roques normal et hosts al.common onits 2004). In native addition, pine species the in Northern European onP populations pines (Roques the original for host these In populations. no- Pissodes Pinus pineaPinus by damage Cone Pissodes validirostris greater than 80% has been reported from natural standsof al. et (Roques cones these from of populations the Pinus sylvestris biotype were capable of completing their development in (Roques Roqueset 1977; al. attacked than P than attacked was nearly twice the damage damage in nearly the was twice of 94% of P

omm. P inus Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect ). P ). control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI :

(Roques et al. 2004). Recent molecular and morphometric confirmed studies thatthe were capable of laying eggs on cones of P laying of of cones eggs capable were on sylvestris issodes inus opulations that opulations which specialize onpines either of the subsectionor Pinus of the subsection in Spain (Bachiller

et al. et contorta inus validirostris suchstone pine as( Swiss (

2004; Annila and Hiltunen 1977) sylvestris cones were damaged by damaged were P cones are more closely associated with Central and and Central with closely associated more are contorta Pinus colonized 2004). Géraldine Roux Géraldine probably incorporates disc

when these two species are planted in pr in planted are species two these when 1983). However, P P. sylvestr P. Comment citer cedocument:

10.1007/s10530-016-1059-8 - 1966) and of P specificity tests revealed that there are different biotypes different are of P. there that revealed tests specificity inus sylvestris than with th , pers. comm.) is Pinus cembraPinus ), are avoided (Dormont and Roques

choice selection biotypes host both experiments, of ( 82.0% 46.3%) vs. , probably due specific to (Dormont volatiles host . In central France, cone damage in P in damage cone France, In. central

inus issodes inus inus

contorta , butonly radiata the larvae originating sylvestris rete taxa, or at least independent independent least at or taxa, rete . This suggests. This thatP

validirostris ose developing onMediterranean

appears to be significantly more more significantly be to appears (

Delplanque et al. et Delplanque and

oximity. In Finland, 42% P compared 1% with - inus Géraldine Roux Géraldine

uncinata inus sylvestris

1988). Larvae inus in France France in

contorta , pers.

was was 55% 15

Version postprint 346 345 356 347 358 357 348 361 360 359 349 366 365 364 363 362 351 350 368 367 354 353 352 355 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological opening (Roques (Roques of Based onthe available information about potentialeffectiveness and non- cone completely (Roques thorus ponderosae thorus Conoph beetle, cone pine promising potentialbiocontrol agents against wilding New pines in Zealand are the ponderosa than greater four be must larvae of number T rescissoriana (Brockerhoff and Kay 1998,above). In the addition, lodgepole pine cone Eucosma moth, P 2004a al. et Storer (e.g. States United Western brancheswounds to and may stems also act as vectors as has been shown for twig beetles the in have a high act potentialto as vectors of the pitchcanker pathogen. In those thatcause addition, planted forest becoming vectors of the pitchcanker pathogen and thereby causing unwanted damage of pines in (Annila al. et (Delplanque R

her inus isks associated with introducing biocontrol agents against P Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect e are thatneed issues important be to addressed concerning the riskof these insects issodes

seed content larvaeachweevil responsible is for, contorta aofcontent 60% 40to loss of the seed control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : 1975).

1976)

validirostris , could be considered can if it be determined sufficiently is thatit specific. host s . B . Resin bleeding. Resin

iocontrol agents thatenter tissues the host 1976)

1988) whilst the1988) presence whilst of 2larvae per cone increas . In P

1976) by yield seed by affect inus , Comment citer cedocument:

10.1007/s10530-016-1059-8 but in pine in speciesbut large with sylvestris reduces seed dispersal by dispersal seed reduces , 3- , a

to getsametothe result. In the small - ). ). nd the pine cone weevil, Pissodes validirostris larvae 4

direct feeding and by inducing resin bleeding of

P. validirostris (as opposed t

prevent invasive r

cones (e.g., P ing pines o feeding externally) feeding o

target impacts, the most

es seed to loss ca. 80% are enough to de one scales from from scales cone the

inus si

zed coneszed of pinaster stroy a a stroy ) the the )

Version postprint 386 385 384 383 382 381 380 379 378 377 376 375 374 373 372 371 370 369 392 391 390 389 388 387 393 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological adult P. validirostria by seedlings carry any F. circinatum fungal trans species. Suchdamage appear not did affect to different biotypes of P al. et (Roques trees the of feeding onleader observed is shoots autumnbefore in theoverwinter settle adults to the in bark of laying capable and mature eggs sexually become oncones (Roques adult weevils require maturation feeding, typically onthe pine leader shoots Although larval and pupal development of Pissodes validirostris occur of any association the with pathogen. significance the feedingshoot by increase habitexhibited also other members could ofe genus th canker pathogen as a vector or as a wounding agent. habitby Ain shift species this include to the pitch the The with lodgepole pine cone Eucosma may moth, , rescissoriana associated become speciesknown host (Storer et al. 2004b) may it therefore and California ponderosae Conophthorus there. The behavior The there. F. circinatumthepathogen should of established become avector as act could Zealand, New Based onthese findings, cannot it be ruled thatP out of the fungus plant(Lennox the host into et al. 2009). show any of conidia. transmission However, its

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : mission. Freshmission. washed adults immediately after emergence from the cones not did several types wouldallow several species of association the with pitchcanker this of issodes conidia (Lennox et al. 2009). In an e 2004). In cont species acongeneric has validirostris be a vector in New Zealand. A Zealand. New in avector be Comment citer cedocument: 10.1007/s10530-016-1059-8 that had been artificially infected with F. rast to egg to rast , a host switch could host occur can feed of onthe a shoots large number of pine plant health feeding damage appeared to facilitate the ingress ingress the facilitate to appeared damage feeding

- laying, behavioral showed tests thatthe that is a confirmed vector of the pathogen in issodes (Roques et al. et (Roques validirostris xperiment is not a not is lthough radiata Pinus . 1976). Another period of , feeding radiata onPinus s entirely in seed cones, cones, seed entirely in 2004) , if i if , circinatum , in spring, in order in to t weret introduced to , but itmay help did not not did

Version postprint 400 399 398 397 396 395 394 406 401 408 407 405 404 403 402 411 410 409 418 417 416 415 414 413 412 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological cones of P new environments cannot be ruled If out. P insect anew represents validirostris responsible mechanism the maturation is feeding behaviour weevil. of this Furthermore, P egg laying, adultand larval feeding, and during invasion larval feeding. Thelikely most pathogen, inoculationof the pathogen during egg laying and adultfeeding, ingression through pathogen including spreading the pathogen by through dissemination emerging adults the with The pitch canker disease caused to by disease threat canker amajor the pathogen pitch The F. circinatum represents nurseries. for in plantedin forestsZealand New in forests one worldwide.is ofsusceptible radiata the Pinus pines most Conclusions the disease in New Zealand, as wounding agents or car or agents wounding as Zealand, New in disease the present.are O occur. I 83% providing partial or complete control spread of wilding the success pines. While of pasthas biocontrol introductions been high, with Furthermore, certain not is it how effective a biocontrol agent wouldbe terms in of reducing the risky,too mainly because ofintroduction biocontrol agents against invasive P beto present thatcould act as effective vectors. Against background, this the proposed

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : n New Zealand New n inus has ademonstrated has ability to colonise new

ur review identified several species thatcould play a role the in epidemiology of , then it could, thenalso affect it radiata breeding programmes and the production of seed , t - host use host plantassociation.host The in potentialfor additionalchanges his risk is moderated riskis his by the fact thatnoknown vectors of F. circinatum of the pitchcanker pathogen vectoring issue(Dick and Bain 2004). Comment citer cedocument: 10.1007/s10530-016-1059-8 and several other countries where F. circinatum where countries other several and of target plants issodes

were to colonise and damage damage and validirostris colonise to were inus riers appear of the pathogen noinsects , but such as such hosts, contorta or contorta other pines has been deemed , seed eating agents have perhaps been been perhaps have agents eating seed , , and itis an important tree P inus , and contorta this does not yet not issodes pine in in

Version postprint 429 428 427 426 425 424 423 422 421 420 419 430 431 432 443 442 441 440 439 438 437 436 435 434 433 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Acknowledgements assessments and future possible incursion responses. S F. also circinatum presentis where (e.g., and occur species these where regions in conducted research oninsects present New in Zealand and onpotentialbiocontrol agents could be effectiveness of biocont canker Africa South in where the disease already is present, and because of about questions the 2011). Recently has been it decided pursue further to not this due associated risks to pitch with insects for the control of invasive pines has been considered Africa South in (Hoffmann et al. 2000 al. et (Fowler effective less We thank John Bain thank forWe John reviewing an earlier version of the manuscript. Funding for re this was obtained from the New Zealand Government ( Biosecurity). C04X1104 core funding contract , Scion to via MBIE Annila E ( DH, FrankelTidwell TE Adams SJ, References

pain Africa and South for some of the European further insects).with wouldassist This risk Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect harmfulness, especially pine seed Scots in orchards. Inst Commun For Fenn– 85:1 Canb Nov , pine radiata ME, control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : . Matheson erra,

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. AC, AC, 1998, rol relying solely oncone and seed insects (Lennox et al. 2009). Further Gordon CSIRO Forestry and Forest ProductsReport No. 112,CSIRO, ; Suckling 2013). Aproposal similar introduce to seed eating Comment citer cedocument: 10.1007/s10530-016-1059-8 TR ( TR Pissodes validirostris

( 1999) e ds.) Current and potentialimpactsCurrent of pitchcanker ds.) in

Chronicle of pitchcanker California. in In:

and Better Border Border FRST contract Better and C04X0302 Gyll. Curculionidae) (Col. and its

95.

De view view vey vey 19

Version postprint 459 458 457 455 454 453 452 451 450 449 448 447 446 445 444 462 461 460 456 467 466 465 464 463 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Brockerhoff JL Foltz GM, Blakeslee GM Blakeslee Berndt LA, Brockerhoff T EG,H, Weis Jactel Bai ( P Bachiller Annila Brockerhoff EG, Hosking ( GP Brockerhoff EG, H

n J, Sopow SL, Sopow n J, Bulman LS Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect Entomol FennEntomol relation in studied the to monoterpene pine and Scots in composition Lodgepole pine. pitch canker of slashpine. Phytopathology canker pitch 71: outbreaks conifers. onexotic N Pseudocoremia suavis pp. 167–173. symbiont. Research and management of a worldwideasive inv pest. Springer, Dordre Instatus. : For Plagas Serv New Zealand Protection Society, Plant pp.216–223. New in contorta Zealand. Proceedings, New 51st Zealand Protection Conference Plant moniliforme management of wilding pines ( Zealand New Rotorua, (Scion), Institute Research pine longhorn beetle. Forest and Timber Inse

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E ,

Hiltunen E 1966) G , Oak SW, Gregory, Oak SW, Moses CS W, Slippers B, Slippers ( de Wingfield Groot P, MJ , Kay M ( M Kay , var. subglutinans Estudio sobre la biologia y tratamientos del Pissodes validirostris Gyll. Boll offmann J, Roques A ( offmann J, 43:

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2001) The deodar weevil, a vector and wounding agent associated with Prospects and of risks biological control of wilding Pinus Damage byDamage Pissodes validirostris 2011) Comment citer cedocument: 10.1007/s10530-016-1059-8 with Pissodesnemorensis Arhopalus tristis Arhopalus Pinus ew Z ew The sirex woodwasp The New sirex in Zealand: history and current 2004) eal spp.)New in Zealand? In: Entomol 27: Entomol , B Is biological control anfor option the

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Curculionidae) Forest : 208.

Ann cht, , ,

Version postprint 469 468 474 473 472 471 470 481 480 479 478 477 476 475 485 484 483 482 486 487 491 490 489 488 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Brockerhoff Kimberley DC, EG, Jones MO, Suckling DM, Donaldson T Carlucci A, Colatruglio L, Frisullo S Bulman LS ( Dallara PL ( Dallara TA, Steenkamp(2007)Coutinho ET, MongwaketsiFirst Wingfield M, outbreak MJ K, Wilmot DL Koehler Wood CS, Gordon McCain TR, AH,JW, Fox Correll JC, de Delplanque A, Giovanini Dick MA ( MA Dick

Groot P, Turgeon JJ ( Turgeon Groot P, JJ Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect Zealand Plant Protection Plant Zealand Bezar (eds.) Future, CM and Managing Present wilding conifers Zealand: New in new Forest in Research No. 197.Forest Research Institute, Rotorua, New Zealand. pheromones and kairomones. For survey for invasive wood boring and bark beetles (Coleoptera) using traps baited with of pitchcanker African a in South pine plantation.Australas Plant Path ( canker California: in pathogenicity, and canker distribution devel circinatum Cal f. pini sp. subglutinans Fusarium with associations their and associates, ecology Pityophthorus of chemical biogeography Pinus of 16: consecutivos a la introduccion de Dougla contorta Pinus ). radiata Pinus Plant Dis control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : 123–132. ifornia. Dissertation 1998) 1997) 1990) Pinus halepensis onPinus Pine pitch canker - canker pitch Pine Studies on the distribution, interspecific onthe distribution, Studies range, relationships, host and BUGS and HEALTH and BUGS —integral part of forest protection strategy. What’s 1998) ques Ro A, Augustin S JP, . Cambridge University Press, Cambridge ersity of California, Berkeley. , University California, of Insect Society, Christchurch, pp.65–78 –682. 75:676 Comment citer cedocument: 10.1007/s10530-016-1059-8 the threat to New Zealand. New Zeal J For 42:30 For Zeal J New Zealand. New to threat the ( - and P. Apulia pinea in (Southern Italy). 91 : Dis Plant pine interactions 2007) est Ecol Manag Ecol est spp. (Coleoptera: Scolytidae) and selected insect selected and Scolytidae) (Coleoptera: spp. First report Fusarium of pitchcanker caused by

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Version postprint 493 492 495 494 498 497 496 504 503 502 501 500 499 515 513 510 509 508 507 506 505 514 512 511 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Dormont L, RoquesA Bai M, Dick Dormont L, RoquesA Dwinell LD,Dwinell Barrows Erbilgin N, Storer AJ, Wood DL,Erbilgin Wood N, Storer AJ, Gordon ( TR Dwinell C, Antoine S, Piou D, Ioos Piou Antoine S, C, Fourrier R Erbilgin N, Gordon TR Erbilgin DL, G, N, Gordon Ritokova Wood TR, Storer AJ

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect 25(1) Alps, theAlps, Pyrenee selection vs. host suitability. host of case A Pissodes validirostris ? weevil, cone pine by specialized attacked the 1998, CSIRO Forestry and Forest ProductsReport No. 112,CSIRO, Canberra Proceedings of the IMPACT Monterey workshop, California, USA,30Nov.3Dec. to Gordon ( TR southern Dis pines. Plant forest cont central,in coastal California. Canadian Entomologist137: coniferous of the hosts pitchcanker fungus by Pityophthorus propagules a dos mediated fungal infections of suscepti control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : LD ( LD amination of pine engraver beetles circinatum Fusarium with e dependent manner. Agric : s in California. Plant Path 32. n J ( n J 1999) 2004) ontrapped pine beetles. For e Global distribution of the pitchcanker Global distribution fungus. In f pitch canker i canker ds.) Current and potentialimpactspitch of - (1999). A survey of insects attacking seed cones of cembra Pinus the in ( Broa Biocontrol of wildings - DL, Storer DL, , Wood s and Massif Central. J Appl Entomol 123: ApplEntomol ands Massif Central. J 2001) ddus J, Kuhlman EG J, ddus Why are seed cones stone pine of( Swiss 69: Comment citer cedocument: 10.1007/s10530-016-1059-8 Entomol 270–276. 57: (2015) For 255–263. 11: Entomol 1103–1108. AJ Exp Appl Exp ble trees induce resistance subsequent to infections in Rapid detection Rapid of circinatum Fusarium est ( 2005) 2009) could it be trouble? New Zeal Tree Grower Grower Zeal Tree New trouble? be it could

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- 22 ,

Version postprint 523 522 521 520 519 517 516 532 531 530 529 528 527 526 525 524 518 534 533 540 539 538 537 536 535 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Fowler SV, Syrett P Ga DL, Wood JW, KoehlerFox O’Keefe CS, ST DL, Wood JW, KoehlerFox CS Gordon Storer TR, AJ Ger Ganley Manning MS, Watt L, RJ, Iturritxa Ganley ( R Hedlin AF, Yates III AF, Yates Hedlin Cibrian HO, Hoffmann Moran Van VC, JH, Wilgen BW (

dgil P, Dick M, Simpson J, Bejakovich Wylie J, Bain M, dgil D, DickRoss Simpson J, P, M, Horgan R, G nandt López DS, GG, García Liston SO, A (2005) Phylogeny and classification of Pinus. Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect 1367. as vectors of the pitchcanker fungus, subglutinans Fusarium 122: environmental weeds New in Zealand. Austral Ecology 25: –42. 54:29 Taxon Can disease. canker perspective. New Zeal For 52(2) J arch, Rotorua, Rese New Unpublished report, Zealand. Forest Zealand. New plan Management (Scolytidae: Ips –1139. 85:1128 invasive Pinus 1–122. Ottawa seed insects of North Am control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : 1157–1166. 2007) ; USDA Forest USDA ; Pitch canker Pitch , Hill RL ( species (Pi species species Wood DL, Wood ( for response an to incursion of pine pitchcanker for Australia and for J For J Serv ) onMonterey pines inf - 2000) riskof New establishmentin Zealand based ona global erican conifers. Environment est naceae) in South Africa. Afr Africa. South in naceae) ( Comment citer cedocument: ice, - 10.1007/s10530-016-1059-8 1990) –2256. Res39:2246 Tovar D, Ebel BH, K 2001) Success and safety the in biological control of DC; Secr. Washington Agric. DC; Recur. Hidraul.,pp. Mexico, Distribution and abundance Distribution of engraver beetles : 26–30. The pitchcanker epidemic California. Dis in Plant E( 2011) ( 2009) 1991)

Prospects for the biological control of A global climatic risk assessment o Engraver beetles (Scolytidae: Ips (Scolytidae: beetles Engraver ected pitchcanker. with Can Entomol oerber TW, Merkel EP ( EP Merkel TW, oerber Entomol 19(2) Entomol Can , Can , ada 553–562. . Can . Entomol 123: Entomol adian : 393–401. For 1980) ( 2003) est Cone and Serv species) species) 1355– f pitch

, ice 23

Version postprint 556 555 554 553 552 551 550 549 558 557 548 547 546 545 544 543 542 541 561 560 559 564 563 562 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Keen FP ( FP Keen Iturritxa E, Ganley Heppe Wright E, J, Steenkamp ( ET, Gordon Wingfield RJ, TR, MJ Hurley BP, B,TA, Slippers Wingfield Coutinho BD, Govender 2007. Wingfield P, MJ. Hoover DL, Bros K, Wood ( WE JW, Fox Leach ( JB borer. tree lemon Cerambycidae), (Coleoptera: Hosking 1978.Oemona GP. (Fabricius) hirta Hoover Bros DL,of 1996.Transmission the K, pitchcanker Wood WE. JW, Fox Storer AJ, Lennox ( Ledgard NJ

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect in the in Basqueradiata Countr genetically homogenous of population circinatum Fusarium forestryAfrican nurs Molecular detection of fungi carried by Bradysia difformis Zealand, pp.1–4. 1169: Forest and T twig fungus, F –91. 127:79 . Can Entomol radiata Pinus punctulatus Ernobius and Scolytidae) (Coleoptera: pitch canker fungus, subglutinans Fusarium For biological control Africa. of invasive South pines in Biol Control of pitchcanker precludes further consideration of a cone weevil, Pissodes for validirostris, control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI :

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Quantitative and seasonal association of the f. s f. , Dougl.) contorta Pinus New in Zealand. J 69(2) J p. pini ( 2009) 115(3):288–295. (Coleoptera: Anobiidae) which infest : Conophthorus radiatae Conophthorus , with 103–109.

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A 24

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Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect . Can Entomol radiata Pinus affecting canker pitch of vectors ecosystemprocesses and Canberra, pp.315–321. of WeedsControl Morin L i suitability of a Pissodes European validirostris, for cone biological weevil, control of challenge to the classic p classic the to challenge de montagne des et Alpes des duSud Pyrénées Orientales. sur la régénération naturelle à duPin ecosystems forest Mediterrannean In Basin. Mediterranean the in Versailles Publications, des Service pitch canker disease. Can disease. canker pitch (Homoptera: Cercopidae future impacts. JForest nvasive pines in South Africa.nvasive South pines in In: JM, Cullen control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : 1983) , Scott ( JK - Morabito G,Gourov M, Hoffmann Kleinhentz A ( JH,

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Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect Protection Society, Christchurch, pp.97–111 (eds.) Managing wilding conifers New in Zealand: Present and Future. New Zealand Plant potent 693. Scolytidae), as vectors of the pitch canker pathogen California. in Can California. Forest 48: Sci negligible to massive: A retrospective analysis. Biol 66: Control on seedling –880. reduction 96:875 specific Dis Plant potentials. oxidation forestry nursery contaminated circinatum Fusarium with plant interactions, and management contemporary review. S pine and plantations forests worldwide TA ( Coutinho pitch canker fungus, circinatum Fusarium AJ, Wood DL, Wood AJ, control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : A, Wingfield MJ, Marasas A, WingfieldTA (1997)tinho MJ, WFO,canker Cou Pitch a ofes: pin Wood DL , Wood ial for damage by the pitchcanker pathogen? In: , Boutigny A 2013) s in South Africa. South in s Dis Plant Groot P ( Groot P de A, 2008) , Gordon ( TR Benefits from biological control of weeds New in Zealand range from Gordon TR Pitch canker caused by caused circinatum canker Fusarium Pitch - L Coutinho TA , Coutinho : 93(9) Sci J Afr 694–700. Comment citer cedocument: 10.1007/s10530-016-1059-8 ( 2004a 2004b) 2002) 1994) The epidemiology of pitchcanker of Monterey pine in ( ) . Annu R Insect fauna of coniferous seed cones: diversity, host Twig beetles, Pityophthorus beetles, Twig Could biological Could control of wilding pines increase the 1994) , Viljoen . Australas Plant Path 78: 411–413.

in Chile. Plant Pathol Plant Chile. , onpines in Fusarium subglutinans Fusarium of report First 309–312. ev E ev A ( –212. 39:179 ntomol 2012) Hill RL, Hill Zydenbos Bezar SM, CM Sanit using hydrogen at peroxide 37,319–334. ( ation of African a South 2002) 27–32. spp. (Coleoptera: spp. - a growi a First report of the the of report First – 136:685 Entomol 51: ng threat to 397. sp. pini sp. f. 27

Version postprint 641 640 vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Yamoah EE, Suckling E, Jones DM, Bourdôt WalterStewart M, GW, A. 2011.Using insects as

Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect potential vectors of tumidum Fusarium control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : Comment citer cedocument: 10.1007/s10530-016-1059-8 to control to gorse. New Zeal 34: Entomol

5–11. 28

Version postprint vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Non insects Predatory Cone insects Shoot and foliage Sapsuckers Bark borers beetles and wood USA (CALIFORNIA) Cone insects Shoot and foliage Bark borers beetles and wood USA (SOUTH S circinatum Fusarium regions in where with pitchcanker occurs associated Insects 1. Table Snails and Pillbugs/Sowbugs and Snails Medetera Lasconotus Enocler Ernobius punctulatus Conophthorus radiatae (none) Aphrophora canadensis Pissodes radiatae Dendroctonus valens Hylurgops Hylastes Pityophtho Pityophthorus setosus Ips I Ips paraconfusus Leptoglossus corculus Cydia Contarinia Rhyacionia nemorensis Pissodes ps ee Supplementary Table S1 for an alphabetical listing of insect species insect of listing alphabetical an for S1 Table ee Supplementary Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect

plastographus mexicanus, - insect taxa control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : (* non (*

spp. us sphegeus spp.

spp.

rus carmeli rus spp.

spp.

spp. spp. -

indigenous sp.) indigenous Species

EAST)

- -

maritimus feede feeders

rs rs

Comment citer cedocument: 10.1007/s10530-016-1059-8 Moll Dipt: Dolychopodidae Colydiidae Col., Cleridae Col., Col., Anobiidae Scolytinae Curculionidae, Col., Homoptera, Cercopidae Molytinae? Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Cor Heteroptera, Lepidoptera, Tortricidae Cecidomyiidae Diptera, Lepidoptera, Tortricidae Curculionidae, Col., usca and Crustacea (Isopoda) Order, family (subf

eidae Molytinae

amily)

Wounding Wounding agent (+) (+) (+) (+) (+) (+) + + + + + + + + + +

. Carrier + + + + + + + + + + + + + + + +

Confirmed vector (+) (+) (+) + + + +

and the nature of their association. a

Storer et al., 2004b Storer et al., 2004b et Storer al. Dallara 1997, et Storer al. Dallara 1997, Hoover et al. 1995, 1996 Hoover et al. 1995, 1996 Storer et al. 1998 al. et Storer al. et Storer a et Storer al. et Storer Hoover et al. 1995, Storer et al. 2004a, Erbilgin et al. 2005 Hoover et al. 1995, Storer et al. 2004a, Erbilgin et al. 2005 Fox et al. 1991, Erbilgin et al. 2008 Fox et al. 1991, Erbilgin et Fox et al. 1991 Dwinell 1985 al. et Dwinell 1985 al. et Dwinell 1985 al. et Matthews 1962 Blakeslee Blakeslee et and al. 1978, Foltz 1981 l. l. 2004b 2004b 2004b 2004b

References

2004b 2004b

al. 2008

Mis Mis Mis Mis

en en en en

forme forme forme forme

: : : :

Français Français Français Français

(France) (France) (France) (France) Version postprint vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological

a borers Root Cone insects Bark borers beetles and wood SPAIN JAPAN Bark borers beetles and wood CHILE Shoot and foliage AFRICASOUTH Brachyderes incanus P Tomicus piniperda Pityophthorus pubescens Pissodes castaneus Orthotomicus erosus Ips sexdentatu Hypothenemus eruditus Hylurgops palliatus Hylastes attenuatus (? None ater* Hylastes difformis Bradysia nemorensis Pissodes

Nature of association: confirmed +, association; presumed (+), association not yet verified; suspected but (?), less likely issodes Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI :

, see, text)

validirostris

feeders

Comment citer cedocument: 10.1007/s10530-016-1059-8 Curculionidae, Col., Molytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Curcu Col., Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., Scolytinae Curculionidae, Col., SciaridaeDiptera, Curculionidae, Col., lionidae, Scolytinae lionidae,

Molytinae Entiminae Molytinae

(+) (+) (+) (+) (+) (+) (+) (+) (+) (+) (+) (?) +

(?) (?) + + + + + + + + +

(?)

Coutinho et al. 2007 Romón et al. 2007 Roques et al. 2004 al. et Iturritxa Romón al. et Iturritxa Romón et al. 2007 Romón et al. 2007 Romón et al. 2007 Romón et al. 2007 Romón et al. 2007 1997 al. et Viljoen 2008 al. et Wingfield Hurley 2 al. et

or unknown or

et al. 2007, Iturritxa et al. al. et Iturritxa 2007, al. et 007 2011 2011

association (for details see text) see details (for association

Lenn

ox et al. 2009 2011

Version postprint vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological

b a Cone insects Sapsuckers fo and Shoot Bark borers beetles and wood Table 2.I

Erechthias fulguritella Erechthias Heliothrips haemo Eulachnus brevipilosus* californica* Essigella P. Pineus boerneri* Planotortrix notophaea Epiphyas postvittana* Ctenopseustis obliquana Hierodoris atychioides Pseudocoremia suavis Pycnomerus sophorae Mitrastethus baridioides noctilio* Sirex Ernobius mollis* Prion Oemona hirta Hexatricha pulverulenta Calliprason pallidus Arhopalus ferus* Platy Pachycotes peregrinus Hylurgus ligniperda* ater* Hylastes

Hylates ater sometimes ater maturationHylates seedlings for pine attacks feeding; A Possible association in case of establishment of in case association F. of Possible Oemona hirta inbreeds pines, always trees, but dead occasionally it feeds on green twigs of pine (Bain and Hosking 1988); carrier; V, vector;carrier; values in brackets indicate uncertainty of association; ( attacking live trees

pini (* non (* Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect pus apicalis oplus reticularis oplus *

control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI :

- nsects present in New Zealand that may act as associates with may associates as that act Zealand New in present nsects

indigenous sp.) indigenous Species

liage

is normally with trees associated and hardwood attacks of softwoods very are (Hosking rare 1978).

- rrhoidalis* feeders

probably limited to probably and thisbut is rare

Tineidae Thripidae Aphididae Aphididae Adelgidae Adelgidae To Tortricidae Tortricidae Oecophoridae Geometridae Colydiidae Curculionidae Siricidae Anobiidae Cerambycidae Cerambycidae Cerambycidae Cerambycidae Cerambycidae Platypodinae Curculionidae, Scolytinae Curculionidae, Scolytinae Curculionidae, Scolytinae Curculionidae, rtricidae Comment citer cedocument: 10.1007/s10530-016-1059-8 Family (subfamily)

Cryptorhynchinae

circinatum

fire

in New Zealand: W, wounding agent of live trees; C, C, trees; live of agent wounding W, New Zealand: in - damaged trees; H

NZ NZ NZ Europe Cosmopolitan NZ NZ NZ NZ Europe NZ NZ Europe Europe NZ Cosmopolitan? Europe USA Europe USA NZ Australia NZ NZ (native region) (native

rhopalus Origin Origin

s ee text details) for

exatricha ferus

Fusarium

Attacks live (L) or dead plants has as been recorded (L) (L) (L) (L) (?) L L L L L L L L L L L

pulverulenta

(D)

a a a a

D D D D D D D D D D D D a

circinatum

Potential pi Potential sometimes sometimes association (W), (C)(W), (W), (C)(W), (C)(W), (C)(W), (C)(W), (C)(W), W, (C) W, C (W), W, (C) W, (C) W, (C) W, (C) W, canker W, C W, (C) (C) (?) . C C C C C C C C

tch tch

Version postprint vectors in epidemiology andinvasion riskofFusarium circinatum,and riskassessment ofbiological Kay (1998) b c e d a Lepidoptera Coleoptera their characteristics, and potentialfor the involvementwith pitchcanker disease Table promising 3.Most candidate agents for New Zealand biocontrol ofin contorta Pinus

trees; C, V, vector; carrier; values in brackets indicate uncertainty of association; (for details see text) Eucosma rescissoriana Eucosma Cydia toreuta validirostris Pissodes Paratimi Ernobius nigrans Conophthorus ponderosae

Possible association in case of establishment of in case association Fusarium of Possible circinatum Depending on the subspecies / host validirostris of race P. Preliminary of selection Maturation feeding, apparently causing text). little (see damage, may shoots on cur oc range Host Brockerhoff, E.G.,Dick, M.,Ganley,R., Roques,A., Storer,A.J. (2016). Roleof insect control ofinvasive Pinus contorta. Biological Invasions, 18(4), 1177-1190. ,DOI : a conicola Species .

information based on Keen ( al. et (1958), Hedlin

potential

Tortricidae Tortricidae Curculionidae Cerambycidae Anobiidae Curculionidae Family (subfamily) agents according Brockerhoff to and Kay (1998) and Brockerhoff et al. (2004)

Comment citer cedocument: 10.1007/s10530-016-1059-8

P. radiata Pinus Pinus Pinus Pinus Pinus Pinus

(see text). Brockerhoff and and in Brockerhoff listed publications other and 1980)

and and spp., not spp., not spp., not spp., not spp., not Host range Host

Abies Abies

in New Zealand: W, wounding agent of live live of agent wounding W, New Zealand: in P. radiata P. radiata P. radiata P. radiata P. radiata spp., b

not not c

cones Only seed cones Only cones M cones Only seed cones Only seed cones Only seed structu Host

ainly attacked

seed d

seed .

res

canker association Potential pitch pitch Potential W, C,W, (V?) C,W, (V?) W, C,W, (V) C,W, (V) C,W, (V) C,W, (V) a ,