Appl Entomol Zool DOI 10.1007/s13355-016-0459-7

REVIEW

Walnut husk , completa (Diptera: ), invades Europe: invasion potential and control strategies

François Verheggen1 · Agnès Verhaeghe2 · Philippe Giordanengo3,4 · Xavier Tassus5 · Abraham Escobar‑Gutiérrez6

Received: 16 February 2016 / Accepted: 20 October 2016 © The Japanese Society of Applied Entomology and Zoology 2016

Abstract Rhagoletis completa Cresson (Diptera: Teph- distributed in Europe, either as isolated wild trees or in ritidae) is native to North America and invaded Western orchards, favouring the probability of fly establishment in Europe in the late 1980s, causing important damage to its currently fly-free areas. In addition, the European territo- principal host, walnut (Juglans spp.). In this review, we ries where Juglans species are present share biogeographic summarize the important elements of R. completa’s biol- similarities. In orchards where R. completa is present and ogy, phytosanitary status and methods used in Europe for uncontrolled, 100% of walnut trees can be infested, caus- its control, and then present the main conclusions associ- ing losses in walnut yields of up to 80%. The negative ated with a completed risk analysis performed in 2014 to effect is low (<10% yield loss) under phytosanitary control, evaluate the dispersion and establishment potential of R. although additional costs must also be considered to sup- completa in Europe. The walnut husk fly was initially iden- port specific monitoring forR. completa. The information tified in Switzerland (1988) and Italy (1991), from where presented here underlines a strong need for better walnut it spread to at least seven additional countries: France, husk fly monitoring across European countries, as well as Spain, Germany, Austria, Croatia, Slovenia and Hungary. for increasing efforts to develop biological methods to con- R. completa has not reached the limits of its potential dis- trol this emerging pest. tribution. The main dissemination pathways within Europe include: (1) natural adult dissemination; (2) adult hitch- Keywords Plant pest risk analysis · Invasive species · hiker behaviour; and, to a lesser extent, (3) transportation Biological invasion · Tephritidae fruit fly of larvae in fresh fruits. R. completa host plants are widely

* François Verheggen Introduction [email protected] Authorities and policymakers in the agricultural sector are 1 Laboratoire d’Entomologie fonctionnelle et évolutive, continuously facing the risk of epidemics and pest out- Université de Liège, Gembloux Agro-Bio Tech, 2, Passage des Déportés, 5030 Gembloux, Belgium breaks (Peña 2013). At the same time, scientific progress, as well as increasing public concerns for both human and 2 Centre Technique Interprofessionnel des Fruits et Légumes, 38160 Chatte, France environmental health, continuously prompts legislators and policymakers to create and enforce rules for pest control. In 3 INRA, Université Nice Sophia Antipolis, CNRS, UMR 1355-7254, Institut Sophia Agrobiotech, the context of global climate change and global trade, there Sophia Antipolis, France are increasing concerns about the ecological and economic 4 Université de Picardie Jules Verne, 33 Rue St Leu, impacts of non-indigenous invasive species of pathogens 80039 Amiens Cedex, France and parasites on plants. 5 Laboratoire de la santé des végétaux, Agence nationale de Tephritidae is a family of the order Diptera comprising a sécurité sanitaire de l’alimentation, de l’environnement, wide group of economically important fruit pests, with the et du travail (ANSES), 49044 Angers, France Mediterranean fruit fly,Ceratitis capitata (Wiedemann), 6 INRA, UR4, 150 route Le Chêne, Lusignan, France being considered one of the world’s most destructive

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(Liquido et al. 1990). The genus Rhagoletis contains surface (Sarles et al. 2015). Each female can infest up to around 60 species, with some of them infesting tree fruits, 20 fruits per season. Males are territorial and attack other including Rhagoletis cerasi Loew, Rhagoletis cingulata males that land on their walnut (Bush 1966). The eggs Loew, Rhagoletis pomonella (Walsh), and Rhagoletis com- hatch in 3–10 days depending on temperature (Duso and pleta Cresson. R. completa, also known as the walnut husk Lago 2006). Young larvae, grouped inside the husk, feed fly, attacks the fruits of English walnut (Juglans regia L.), on the inner husk (fleshy pericarp), making it black, soft, causing heavy damage in the absence of chemical control wet, sticky, causing it to soften and blacken and making it (Van Steenwyk et al. 2010). It may also attack Juglans adhere to the maturing nut (endocarp) and thus difficult to nigra L., Juglans californica Wats and Juglans hindsii Jeps remove. Under very severe attacks, larvae totally destroy fruits (Foote 1981). Empirical evidence suggests that peach the pericarp, leaving only a black and withered exocarp fruits (Prunus persica L.) could also be attacked (Bush around the mature shell. The infestation may be the cause 1966) but the identification was made on the basis of lar- of black spots on the shells and reduces their commercial val stages and the importance of these attacks is not known. value (Samietz et al. 2012). In case of early attacks, the Finally, Yee and Goughnour (2008) reported English haw- development of the seed (kernel) is strongly inhibited and thorn Crataegus monogyna Jacq. as a host in the United the fruit falls. Therefore, the larval stage is the most dam- States. aging. After 2–5 weeks of development, the larvae (Duso Originating from North America, R. completa invaded and Lago 2006) drop to the ground or fall with the fruit, several European countries in the late 1980s [European and pupate in the soil at a depth of a few centimetres. Pupa- and Mediterranean Plant Protection Organization (EPPO) tion allows the to overwinter. The following summer, 2013]. After presenting the current status of R. completa the majority of adults (>80%) emerge from the ground and invasions in Europe, we discuss the potential risks asso- repeat this cycle, while part of the pupae spend another ciated with (1) the introduction of additional individu- season in diapause (<10%) (Duso and Lago 2006). Adult als on the continent, (2) their dissemination, and (3) their often remain on the plant above the ground where establishment in non-invaded European areas. Finally, the they emerge. However, movements of individuals are likely costs associated with monitoring and control efforts are to be more frequent in the event of high population den- discussed. sity. Passive dispersal by other means (wind, cars, etc.) is also likely. Dissemination of R. completa individuals is dis- cussed below. State of the art Origin and distribution in Europe Biology Walnut husk fly originated from North America, where it Like most species of Tephritidae, R. completa is a small- is present in Canada (British Columbia), as well as in the sized fly (4–7 mm in length) with a yellow dot on the pos- western and central states of the USA. The presence of terior base of the thorax, and transparent wings with three R. completa has also been officially documented in West- dark brown stripes, the last being of an extended L shape ern Europe, where this pest was reported for the first time which commences at the front edge of the wing (Bush in Switzerland, in 1988. The fly subsequently spread to 1966). The recommended identification method has been nearby countries, including Italy (1991), Slovenia (1997), extensively described in EPPO (2013) and has to be per- Croatia (2004), France (2007), Germany (2008), Austria formed with a binocular microscope on adult specimens (2008) and Hungary (2011) (Duso 1991; Duso and Lago for better reliability. Larvae and pupae can also be identi- 2006; Merz 1994) (Fig. 1). Some R. completa individu- fied using the spiracular arrangement, assuming specimens als were observed in a Spanish orchard situated near the reared from walnuts are available for comparison. Portuguese border in 2013, but these observations remain Walnut husk fly has one generation per year (Bush unofficial (ANSES2014 ). Aluja et al. (2011) invoked the 1966). Adults emerge from the soil in early July to the phenomenon of global warming to explain the relaxing end of August, with a peak of emergence between late of climatic barriers and the spreading of R. completa in July and early August. Its lifespan can reach up to 40 days Europe. under natural conditions. Mating occurs 6 to 8 days after emergence, and females begin to lay eggs 1 to 2 weeks Monitoring after mating. Each female lays 300 to 400 eggs in groups of about 20 eggs per fruit (Duso and Lago 2006). Usually, R. completa is classified in the European Directive 2000/29 there is a single patch of eggs per fruit because the female EC, Annex I, Part A, Chapter 1. Monitoring of R. com- deposit an oviposition-deterring pheromone on the fruit pleta is necessary to adapt phytosanitary treatments to pest

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Fig. 1 Invasion history of the walnut husk fly in Europe (according to the first reports of its presence) pressure. In an orchard, R. completa is commonly detected calculations for French conditions, we estimate the cost 1 based on trapping adults, but larvae can also be detected. of monitoring associated with R. completa at 75 € ha− Detection of adults is conducted with chromatic sticky (including labour and materials). traps, suspended in the canopy: the higher in the tree, the better the efficiency, according to field observations (F. Control methods Verhaeghe, personal observation). Typically, they are visu- ally monitored twice a week. Attraction to traps can be Following the detection of the first R. completa adults, increased by adding ammonium carbonate (Riedl and Hoy- walnut producers need to chemically control the pest. Phy- ing 1981; Sarles et al. 2015). To detect larvae, it is neces- tosanitary products containing thiacloprid have a broad sary to visually inspect the fruit surface where damage is spectrum allowing control of R. completa, but also Cydia first caused by adult females through egg-laying puncture pomonella (Miklavc et al. 2013). Because periods of pres- holes. Then, as a result of larvae feeding activity, the black- ence of adult C. pomonella and R. completa partly over- ening of the husk allows easy detection. Based on our own lap, some phytosanitary treatments against C. pomonella

1 3 Appl Entomol Zool also control R. completa, at least partially. No studies have temperatures; and finally, the husk (and then the contained focused on the resistance of R. completa to insecticides. larvae) is removed before commercialization. In organic orchards, calcined kaolinite (clay) that pro- Pupae could be displaced along with the soil present on vides a physical protection of the fruit has some efficiency the roots of uprooted trees. They can also be transported (ANSES 2014). Its use requires three to four additional locally by motorized vehicles leaving infested orchards. applications per year. However, its application is not Although not impossible, these possibilities seem highly suitable for large trees that make up the majority of the unlikely. orchards. This inefficiency will result in a sharp increase in Adult dissemination likely starts from first adult emer- R. completa populations from one year to the next. Alterna- gence. The dissemination period ends at the date of the tive approaches have been evaluated, including the use of last emergence, to which adult life expectancy should be entomopathogenic nematodes for the control of R. cerasi added (ca. 40 days). In the south-east regions of France, (Kepenekci et al. 2015). Applied on the soil after harvest- adult emergence usually starts in early July and ends in ing, these nematodes are likely to control R. completa mid-September (F. Verhaeghe, personal observation). pupae, but this remains to be tested in the field. Moreover, Adult dissemination is therefore likely to last from early recent work has shown that entomopathogenic nematodes July to late October. However, this period may vary are compatible with insecticides (Laznik and Trdan 2014), according to the bioclimatic area. Male territorial behav- allowing the combination of both methods. iour and the use of marking pheromones during egg lay- Forecasting the demographic dynamics of R. completa ing by females are likely to favour the dispersal of eggs using a classic approach of demographic modelling could and hence the establishment of the species on a new host be useful for better targeting peaks of adult emergence. (Nufio and Papaj 2004; Tadeo et al. 2013; Sarles et al. This should favour a more efficient control of the pest. 2015). The combination of large R. completa populations and a large number of vehicles in an infested area will likely promote the risk of dissemination to a non-infested Invasion potential in Europe nearby area. Although hosts are limited mostly to Juglans spp., their abundance over Europe should allow any fly- Likelihood of dissemination within Europe ing individuals to encounter a host (see below). Like most Tephritidae , R. completa is likely to be able to local- Listing the possible pathways allowing R. completa to ize its host at a distance using kairomones (Sarles et al. spread from an infested area to a non-infested one is an 2015). important step in evaluating the risk of dissemination. One Adults are able to fly over long distances (Aluja et al. could then estimate the probability that the pest is associ- 2011). Evaluating the dissemination speed is a hard task ated with these pathways and the probability that it will because of the lack of available data in the literature. In survive transit from the area of origin to the non-infested France, monitoring efforts have been made since 2009, area. but have not been published. Based on data recorded from As a univoltine fly strictly associated with Juglans spp., 2009 to 2013, two key factors appear to promote spa- the biology of R. completa does not favour its dissemina- tial and temporal dispersal of infestations: the highways tion. However, as presented below, several factors should and valleys of major rivers (ANSES 2014). However, in favour dissemination within Europe. Dissemination is most cases, highways and valleys are juxtaposed, so it is likely to start from an infested orchard. Within an infested difficult to determine the major means of natural disper- orchard, R. completa location differs according to its devel- sal. Adults can also be transported passively by vehicles, opment stage: eggs and larvae are situated in the husk, especially from areas where fruit flies are not controlled. pupation occurs in the soil, and adults fly above ground. Dispersal of R. completa in Clermont-Ferrand (France) Eggs and larvae could be transported along with fresh can be explained by hitchhiker behaviour; we estimate the fruits (nut within its husk) or with empty husks (some- maximum hitchhiker-associated dispersal distance at about 1 times used as a soil amendment). In Europe, no inspec- 326 km year− (distance by road between Bergerac and tion is being conducted on commercialized fresh fruits, Clermont-Ferrand). making the larvae unlikely to be detected. However, this pathway seems unlikely for several reasons. First, infested Likelihood of establishment in non‑invaded areas walnuts often fall to the ground before harvesting, limiting the number of infested fruits being commercialized; sec- After a pest has survived along one of the introduction ond, harvesting occurs at a period during which very few pathways and has entered a new area, several conditions larvae are still present in the husk; third, larvae are sensi- have to be met to allow its settlement, including a favour- tive to transportation conditions such as storage at freezing able climate and host availability.

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Fig. 2 Juglans spp. potential distribution in Europe

To predict the potential areas of R. completa establish- that Juglans spp. distribution area corresponds to the poten- ment, a map of host plant potential distributions was built tial establishment area of R. completa. on the basis of two climatic requirements of J. regia, J. The impact of winter temperatures on R. completa sur- nigra and Juglans intermedia Carr var. vilmoreana, vival is poorly documented. Thus, in the present state of × namely: (1) an average monthly temperature above 10 °C knowledge, and considering its biology and dispersal abil- for the period May–September (5 months), and (2) annual ity, we believe that this species will come to occupy all of precipitation above 700 mm (Masson 2005). To build the its host plant range in Europe and beyond, that is to say, map, a geographic information system (ArcGIS version up to the natural range of J. regia in Central Asia (Hem- 9.3.1) was used to treat a global database (Bioclim by ery et al. 2005). Geographic barriers such as mountains WorldClim.org) including the climatic norms (built on 30 (the Alps and the Pyrenees) or seas (the English Chan- years of climate records) on an extrapolated grid of 30 arc nel, the Irish Sea and the Baltic Sea) could only delay its seconds. The map is presented in Fig. 2, and is consistent dispersion. with the Food and Agriculture Organization of the United Natural enemies are unlikely to reduce the establishment Nations’ (FAO, http://faostat.fao.org/) data and empirical of R. completa in non-infested European areas. Indeed, par- evidence, except for an area including Romania and Mol- asitoids (e.g. braconid wasps) have only limited ability to dova. J. regia trees have been reported to produce nuts as control R. completa infestations (Laznik and Trdan 2013). far north as Northern Scotland and Southern Norway. Potential competitors include Rhagoletis suavis. However, Moreover, the density and proximity of walnut orchards because both species are exclusively associated with Jug- (J. regia and hybrids) and wood production areas (J. nigra lans spp., an equilibrium should quickly be established and hybrids) in Europe are additional factors that would between their respective populations. likely increase the settlement risk. Given the absence of We conclude that the potential establishment area of R. treatments applied to Juglans trees outside the orchards, it completa in Europe will likely consist of the entire Juglans is very likely that R. completa can survive eradication pro- spp. distribution area of the continent. There is no apparent grams in newly invaded areas. barrier to the settlement of R. completa if compatible hosts are European areas where R. completa has already estab- available (Yee and Goughnour 2008). Seven countries have lished (e.g. France, Italy, Slovenia and Switzerland) present officially announced the presence of R. completa on their terri- climatic conditions similar to those of many non-invaded tory, and this number should increase rapidly (ANSES 2014). areas. The main factor limiting the development of R. com- As observed within the USA (Bush 1966), the geograph- pleta is the presence of Juglans spp. A second factor limit- ical dispersion of R. completa is very likely to occur within ing the establishment of R. completa is the sum of spring Europe. The most probable way of dissemination is through temperatures: monthly mean temperature should be above adult movement. Three to five years should be needed for 7 °C (Aluja et al. 2011). So, it seems, with few exceptions, R. completa to reach its maximum extent in Europe. This

1 3 Appl Entomol Zool estimate is based on (1) the current distribution of R. com- Walnut production can also be an ancillary activity. In pleta in Europe, (2) R. completa dissemination chronology the absence of a quarantine treatment approved for R. com- within Europe (see Fig. 1), (3) the estimate of the maximal pleta, the latter can lead to total production loss. speed of dissemination (see above), (4) the factors limiting the spread of R. completa (host plant and temperature), (5) Conclusion the host plant distribution area within Europe (Fig. 2). Because of biogeographic similarities across Europe, and because its host plants are widely distributed, R. completa Economic, environmental and societal has not reached the limits of its potential distribution. Most consequences conventional insecticides used to control fruit flies have been banned, leading fruit producers to seek more econom- Although invasive alien species are usually associated with ical and practical options to control walnut husk flies. There biodiversity loss and ecosystem service changes, the direct is a strong need for better fly monitoring across European environmental impacts of R. completa are rather limited, countries, as well as for increased efforts to develop biolog- although economic losses to growers may be substantial. ical methods to control this emerging pest. Ammonium car- In the areas where R. completa is established, all trees of bonate bait traps could allow an earlier detection of initial an orchard are infested in the absence of phytosanitary treat- emergences in orchards. Use of natural enemies (including ments. In the absence of R. completa, a walnut orchard typi- parasitoids) as well as semiochemical-based formulations 1 cally reaches a yield of 2 t fruit ha− . This yield can drop by are two options that should be developed. 80% in the presence of R. completa and in the absence of specific phytosanitary treatment. The exportation of walnut (shell nuts and kernels) outside the territory of the 28 coun- References tries of the EU amounted to about 24,000 t in the period Aluja M, Guilln´n L, Rull J, Höhn H, Frey J, Graf B, Samietz J (2011) 2011–2012 (FAO data, http://faostat.fao.org/). Taking into Is the alpine divide becoming more permeable to biological inva- 1 account the walnut market price (3,300 € t− for export in sions? Insights on the invasion and establishment of the walnut 2012), the total loss in international trade is estimated at 79 husk fly, Rhagoletis completa (Diptera: Tephritidae) in Switzer- million euros. Compared to the world production of walnut, land. B Entomol Res 101(4):451–465 ANSES (2014) Analyse de risque phytosanitaire portant sur European production represents less than 10%. Thus, pro- Rhagoletis completa. https://www.anses.fr/fr/system/files/ duction losses due to R. completa in Europe will likely not SVEG2013sa0094Ra.pdf. Accessed 8 Nov 2016 affect the world market and consequently the international Bush GL (1966) The , cytology, and evolution of the genus price of walnut. Under such circumstances, European grow- Rhagoletis in north America (Diptera, Tephritidae). Bull Mus Comp Zool 134(11):431–562 ers will have to pay the full costs induced by R. completa Duso C (1991) Sulla comparsa in Italia di un Tefritide neartico del infestations. Walnut producers usually apply phytosanitary noce: Rhagoletis completa Cresson (Diptera: Tephritidae). Boll treatments against Cydia pomonella, at an estimated cost of Zool Agric Bachic 23:203–209 159 ha 1. However, in the presence of R. completa, addi- Duso C, Lago GD (2006) Life cycle, phenology and economic € − importance of the walnut husk fly Rhagoletis completa Cres- tional phytosanitary treatments are needed, increasing the son (Diptera: Tephritidae) in northern Italy. Ann Soc Entomol Fr global cost associated with insect control by about 13% in 42(2):245–254 1 Ekesi S, Billah MK, Nderitu PW, Lux SA, Rwomushana I (2009) Evi- conventional culture (180 € ha− ). In organic orchards, this costs increases by 430%, reaching 688 ha 1. dence for competitive displacement of Ceratitis cosyra by the € − invasive fruit fly Bactrocera invadens (Diptera: Tephritidae) on In addition to the huge economic impact, and its appar- mango and mechanisms contributing to the displacement. J Econ ent social effects, R. completa could have some effects on Entomol 102:981–991 the ecology of native species by displacing and outcom- EPPO (2013) PQR database. EPPO, Paris. http://www.eppo.org peting indigenous tephritids (Ekesi et al. 2009), but this Foote RH (1981) The genus Rhagoletis Loew south of the United States (Diptera: Tephritidae). Technical bulletin, Science and remains to be studied in detail. Education Administration, US Department of Agriculture, no. Regarding R. completa invasions, no direct environmen- 1607 tal impact has been described in the literature. However, Hemery GE, Savill PS, Thakur A (2005) Height growth and flushing neonicotinoids and organophosphates used to control R. in common walnut (Juglans regia L.): 5-year results from prov- enance trials in Great Britain. Forestry 78:121–133 completa are highly toxic to aquatic organisms, birds, pol- Kasana A, AliNiazee MT (1994) Effect of constant temperatures on linators and additional beneficial predators and development of the walnut husk fly, Rhagoletis completa. Ento- parasitoids (Vidau et al. 2011). 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