EPP 12045 Dispatch: 13.6.13 Journal: EPP CE: Vinothkumar P. Journal Name Manuscript No. B Author Received: No. of pages: 6 PE: Amudhapriya Bulletin OEPP/EPPO Bulletin (2013) 43 (2), 1–6 ISSN 0250-8052. DOI: 10.1111/epp.12045

1 Distribution and biology of the yellow-spotted longicorn beetle 2 3 Psacothea hilaris hilaris (Pascoe) in Italy 4 5 2 D. Lupi, C. Jucker and M. Colombo 6 3 Department of Food,University of Milan, Environmental and Nutritional Sciences (DeFENS), Via Celoria 2, 20133, Milan, (Italy); 7 e-mail: [email protected] 8 9 10 11 The Asiatic yellow-spotted longicorn beetle, Psacothea hilaris hilaris, was found for the 12 first time in Northern Italy in 2005. As the xylophagous insect is considered one of the most 13 important pests of Morus spp. and Ficus carica in its countries of origin, a multi-year study 14 was carried out to determine the spread of the pest in Northern Italy, to evaluate its estab- 15 lishment potential and to improve knowledge on its biology in the new habitat. The survey 16 confirmed that P. hilaris hilaris has established in Italy and has colonized an area of about 17 60 km2. The species overwinters as eggs or larvae. Adults are present from June to October. 18 Damage has been recorded mostly on Ficus carica plants, and very rarely on Morus alba. 19 Both young and older plants in healthy and stressed phytosanitary condition can be attacked 20 by the pest. Severely attacked plants become weakened and are eventually killed. 21 22 23 (Hanks, 1999). After a first period of feeding under the Introduction 24 bark, the larvae tunnel into the xylem of host trees. This 25 Psacothea hilaris (Pascoe) (Coleoptera Cerambycidae Lamii- results in considerable damage to the tree which is pro- 26 nae Lamiini), commonly known as the yellow spotted longi- gressively weakened. The adults feed on the leaves and on 27 corn beetle, is native to the East Asia where it is widely the tender bark of the smaller branches (Jucker et al., 28 distributed. The species Psacothea hilaris includes 13 sub- 2006). Studies on the biology in the countries of origin 29 species distinguishable by their morphology (Kusama & Ta- indicated that P. hilaris hilaris is generally univoltine, 30 takuwa, 1984). The subspecies present in Europe is although the species can complete its life cycle in two 31 Psacothea hilaris hilaris which occurs in China and Japan. years, or can have two generations per year, depending on 32 In its area of origin P. hilaris is a destructive and eco- the time oviposition occurs (Watari et al., 2002). Two 33 nomically important pest of plants belonging to the Mora- different ecotypes of this subspecies are described in 34 ceae family, including fig trees (Ficus carica) and mulberry Japan: Ecotype E (East Japan type) which does not 35 trees (Morus spp.). In Japan P. hilaris is a serious pest of undergo winter larval diapause and it is thus distinguish- 36 sericulture, as the larvae bore tunnels in the trunks and the able from the ecotype W (West Japan type), which does 37 adults feed on the leaves of mulberry trees, which are the (Iba et al., 1976; Iba, 1980; Makihara, 1986; Sakakibara 38 food source of Bombyx mori. In Europe, where sericulture & Kawakami, 1992; Shintani & Ishikawa, 1999). The two 39 has nearly disappeared, the insect can attack Morus trees ecotypes can also be distinguished by the stripe pattern on 40 grown for ornamental purposes. As the production of figs is the pronotum (broken in the Western ecotype, continuous 41 important around the Mediterranean Basin, and many fig in the Eastern) (Iba, 1980). Depending on the ecotype, 42 trees are grown in private gardens, the establishment of the adults’ emergence peaks in different period over the year. 43 pest in this area could become a threat for fig production. The W-type has its main emergence peak in early summer 44 Psacothea hilaris hilaris adults are easily recognizable: and a smaller one in autumn, while the E-type has an 45 the tegument is black and it is covered by a green-grayish increase in the population in autumn, but does not form a 46 pubescence with yellow spots on the elytra and the abdo- sharp emergence peak (Iba et al., 1976; Sakakibara & 47 men, and yellow stripes on the pronotum (Fig. 1). Variation Kawakami, 1992). 48 in the body size of P. hilaris hilaris is conspicuous, espe- The beetle has been discovered several times in North 49 cially in males: the body length (from the head to the tip of America and Canada in warehouses, on wood and wooden 50 elytra) varies from 13 to 30 mm in males and from 15 to spools imported from Asia. The species was also intercepted 51 31 mm in females (Iba, 1993; Fukaya, 2004). Adults are in the UK in 1997 but it did not establish. Subsequently in 52 characterized by long antennae whose length is longer than 2008 in the United Kingdom one live adult beetle was detected 53 twice the length of the body in males and longer than 1.5 in a public garden in Derbyshire (East Midlands) (EPPO, 54 the length of the body in females. 2008/201), but no information is available about its establish- 55 The larvae are xylophagous and bore tunnels in the ment in the country (http://www.fera.defra.gov.uk). In Italy 5 56 trunks and branches of different diameter under the bark P. hilaris hilaris was first recorded in Lombardy Region

ª 2013 The Authors. Journal compilation ª 2013 OEPP/EPPO, EPPO Bulletin 43, 1–6 1 2 D. Lupi et al.

1 investigate whether the insect had established. The sites were 2 checked yearly to evaluate the presence of the species and its 3 distribution. Further sites were randomly chosen in the neigh-

4 COLOR bourhood and in the nearby municipalities. Visual inspections 5 were also carried out following recommendations from people 6 living in the infested area. The position of each site was geo- 7 registered with eTrex VISTA HCx GARMIN. The methods 8 used to detect the insect and/or the symptoms of its presence 9 were dependent on the season and, consequently, the stages of 10 the insect present. 11 Fig. 1 Adult of P. hilaris hilaris. 12 Bio-ethology and dangerousness 13 14 (Northern Italy) in September 2005 when two dead specimens To acquire data on the bio-ethology of the pest in the new 15 (one male and one female) were collected near a wood ware- habitat, from spring 2010 to autumn 2012 two sites (45°49′ 16 house, in the municipality of Almenno San Salvatore (Bergamo 40.06″N, 9°13′07.44″E; 45°46′09.98″ N, 9°11′52.86″E) with 17 province) (45°45′28.6′’N;9°35′53.18′’E).Thesameyear, about 30 infested plants were chosen. 18 in October, another adult was captured in Asso (Como province) Surveys were carried out throughout the year and the pres- 19 (45°51′36.96″N; 9°16′16.71″E), about 30 km away from the first ence of different instars was documented (eggs, preimaginal 20 point of detection, and brought to DeFENS - University of Milan. instars, adults). Presence of adults was ascertained by visual 21 In both cases no infested plant was detected on the site (Jucker inspection in the canopy. When possible the specimens were 22 et al., 2006). P. hilaris hilaris was considered to have probably captured, prepared and stored in entomological boxes. For the 23 been introduced into the area via firewood or import of fig trees. observation of the preimaginal stages, the bark was removed 24 However the exact point of entry and origin is not known. In when sawdust was observed on the outside of the trunks or 25 2008 P. hilaris was added to the EPPO Alert List. In 2012 the branches. In addition some branches were cut from infested 26 species was deleted from the list because it has been included for plants in different localities, transferred to the laboratory of 27 more than 3 years and during this period no particular interna- the University of Milan and kept at room temperature to allow 28 tional action was requested by the EPPO member countries. adult to emerge and to confirm insect species and evaluate its 29 As the species was detected again in 2007 in Anzano del sex ratio. Emergence holes in dead plants were counted and 30 Parco (Como province) (45°46′08.09′’N; 9°12′12.09′’E), their depth into the wood evaluated. 31 a municipality located about 10 km from Asso, and numer- 32 ous live insects and attacked fig plants were found, a multi- Results 33 year study started. This paper reports the information 34 acquired on the establishment potential of the new pest in Geographic distribution of Psacothea hilaris hilaris in 35 Northern Italy and its spread. Data on the bio-ethology and Italy 36 the potential damage that could be caused by this wood 37 borer in Italy were also obtained. The species was observed in 29 sites within 19 municipali- 38 ties (Table 1). The latitude of these sites ranged from 6 39 40 Materials and methods 41 Psacothea hilaris hilaris 42 Geographic distribution of in 43 Italy COLOR 44 The study area is in the south of Como lake, one of the 45 largest hydrographic basins in Northern Italy. This is 46 a highly populated area with fig trees cultivated in many 47 private gardens and plants also growing as ruderal species 48 in undisturbed areas. As this region was one of the most 49 important for sericulture at the beginning of the twentieth 50 century, Morus alba plants are still present as ornamentals, 51 planted in parks and along streets. The climate in the area 52 is subcontinental (Pinna, 1978), and in proximity of the 53 lake the winter is milder. 54 The survey started in Anzano del Parco (CO) where the first 55 live adults of P. hilaris hilaris and symptomatic plants were Fig. 2 Distribution map of P. hilaris hilaris in Italy (in green: point of 56 detected. The localities were initially visited in 2008, to first detection in 2005; in yellow: area of spreading in 2012).

ª 2013 The Authors. Journal compilation ª 2013 OEPP/EPPO, EPPO Bulletin 43, 1–6 Distribution and biology of longicorn beetle 3 1

1 45°52′48″Nto45°45′10″N and the longitude from 9°18′11″ were removed immediately after the insect detection, in the 2 E and 9°05′41″E, with an altitudinal range from 227 m to subsequent year it was no longer possible to follow the 3 626 m above sea level. Over seven years P. hilaris hilaris infestation of P. hilaris hilaris. 4 spread to an area of about 60 km2. Infested areas were con- 5 tiguous with the exception of the finding in Como city Bioethology and dangerousness 6 (Fig. 2). Establishing the precise distribution of the insect 7 is difficult as the fig plants are mostly found inside private The insect was principally detected in association with fig 8 gardens or in ruderal areas which can be difficult to access. trees. There was only one site (45°49′40.06″N, 9°13′07.44″E) 9 In 8 of the 29 localities adults were collected but the host where mulberry trees were attacked. 10 plants could not be localized. Although in Table 1 the year Adults were observed from mid- June until the end of 11 of detection was reported in different localities, the year is October. Adults did not show a peak of emergence, but 12 not always indicative of the arrival of the insect, which emerged gradually during the observation period. They 13 may have taken place some years before. In many cases the were observed both in the canopy and on the trunks, feed- 14 plants were already in a very poor condition at the first visit ing on the tender bark, on foliage, shoots and occasionally 15 and covered with emergence holes. In some localities plants on fig fruits (Figs 3a,b). Approximately 20–30 days after 16 17 18 19 AB 20 21

22 COLOR 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 C D 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 Fig. 3 Adult feeding (A, B); sawdust (C); 56 exit hole (D).

ª 2013 The Authors. Journal compilation ª 2013 OEPP/EPPO, EPPO Bulletin 43, 1–6 4 D. Lupi et al.

1 emergence, females were observed laying eggs on trunks and larvae to begin their activity under the bark. This infor- 2 and branches. A few days after egg-laying a small amount mation is in line with the results of Shitani and Ishikava 3 of sawdust was visible outside the bark (Fig. 3c). (1999), that established that the minimum temperature at 4 Winter surveys showed the simultaneous presence of which the eggs can survive is À27°C while that of neonate 5 eggs and larvae. Observations in spring in 2011 and 2012 larvae is À18°C. In the study area temperatures never 6 established the capability of overwintering eggs to hatch reached these values as the lowest temperatures recorded in 7 winter were À5.3°C and À11.5°C respectively in 2011 and 8 2012 (data provided by ‘Servizio Meteorologico Regionale 9 – ARPA Lombardia’, www.arpalombardia.it). 10 During the surveys many subcortical larvae, with a maxi- 11 mum head capsule width of 3.5 mm (n = 58), were found. 12 Then the larvae migrate into the xylem and develop until 13 they reach a maximum head capsule width of 4.99 mm 14 (n = 37) before pupation. The depth of the gallery into the 15 trunk, calculated from emergence holes, varied from 16 18.0 mm to 55.0 mm with a mean value of 33.2 Æ 7.7 mm 17 (n = 77) and was not related to the diameter of the infested 18 part of the plant (Fig. 4). 19 Adults emerged by chewing an exit hole through the bark 20 (Fig. 3d). The emergence holes were observed mostly on 21 trunks, on principal and secondary branches but also on 22 exposed roots. The sex ratio obtained in a sample of 289 23 specimens was 0.89 females/males. In 4 sites many plants 24 were observed to have died following infestation with 25 P. hilaris hilaris (Fig. 5). 26 Two dead fig trees (girth at 1 m: 40 cm; 55 cm; height 27 ground-first branches: 2.2 m; 2.3 m) detected respectively 28 in 2010 and 2011, had nearly 250 emergence holes on the 29 two plants. The variability of the dimension of the body of 30 the adults was confirmed by the diameter of the circular 31 exit holes which varied from 3.0 to 12.0 mm with a mean 32 value of 7.86 Æ 1.30 mm (n = 240) on fig trees (Fig. 6). 33 Fig. 4 Frequency histogram of gallery depth in fig plants. 34 35 36 37 38 39 40 COLOR 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 Fig. 5 Decaying fig plants.

ª 2013 The Authors. Journal compilation ª 2013 OEPP/EPPO, EPPO Bulletin 43, 1–6 Distribution and biology of longicorn beetle 5 1

1 mostly in private gardens, could become invasive if it Discussion 2 spreads to regions of Italy and of the Mediterranean Basin 3 The survey confirmed that P. hilaris hilaris has established where F. carica orchards are economically important. 4 in Italy; it represents one of the numerous examples of 5 recently introduced exotic species into the country which Acknowledgements 6 have been able to establish (Jucker & Lupi, 2011). 7 Until a few years ago, phytophagous pests caused little The authors are very grateful to all the researchers and 8 damage to fig plants in Italy. At present F. carica is threa- colleagues that have been involved in the research over the 9 tened by two exotic pests: P. hilaris hilaris and Aclees sp. years. This research was financially supported by the 10 (Coleoptera Curculionidae) (Ciampolini et al., 2005), caus- project ‘New associations between indigenous parasitoids 11 ing serious damage and plant death. In 2012 another Lamii- and exotic insects recently introduced in Italy (PRIN)’ and 12 nae was detected in Central Italy, Batocera rubus the project ‘Insects and globalization: sustainable control of 13 albofasciata Degeer (http://www.ersa.fvg.it), but no infor- exotic species in agro-forestry ecosystems (GEISCA)’, both 14 mation is currently available on its possible establishment. financed by Ministry of Instruction, University and 15 Psacothea hilaris hilaris has spread over the last seven Research. 16 years, but it is still confined to a relatively small territory 17 in the north of Italy. The species was able to survive and 18 Distribution and biology of the yellow- complete its development not only on healthy and vigorous Psacothea hilaris 19 spotted longicorn beetle trees, but also on stressed and weakened hosts. Insects can hilaris (Pascoe) in Italy 20 emerge from decaying or dry plants. Moreover, the yellow- 21 spotted longicorn is able to develop on small branches The Asiatic yellow-spotted longicorn beetle, Psacothea 22 removed from the plant of approximately 1 cm diameter. hilaris hilaris, was found for the first time in Northern Italy 23 This increases the survival of the species and therefore con- in 2005. As the xylophagous insect is considered one of the 24 trol is more difficult. In the period of study, numerous fig most important pests of Morus spp. and Ficus carica in its 25 plants attacked by the beetle were weakened and died. The countries of origin, a multi-year study was carried out to 26 above observations are in contrast with those reported by determine the spread of the pest in Northern Italy, to 27 Hanks (1999) in his review on Cerambycid reproductive evaluate its establishment potential and to improve 28 behavior which stated that P. hilaris is incapable of killing knowledge on its biology in the new habitat. The survey 29 the host. confirmed that P. hilaris hilaris has established in Italy and 30 The information presented in this paper underlines the has colonized an area of about 60 km2. The species 31 damage that P. hilaris may cause and hence the necessity to overwinters as eggs or larvae. Adults are present from June 32 study the biology and proper control measures. The species, to October. Damage has been recorded mostly on Ficus 33 currently present only in a small area where fig is cultivated carica plants, and very rarely on Morus alba. Both young 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 Fig. 6 Frequency histogram of exit holes 56 diameter in fig plants..

ª 2013 The Authors. Journal compilation ª 2013 OEPP/EPPO, EPPO Bulletin 43, 1–6 6 D. Lupi et al.

1 and older plants in healthy and stressed phytosanitary Hanks LM (1999) Influence of the larval host plant on reproductive 2 condition can be attacked by the pest. Severely attacked strategies of cerambycid beetles. Annual Review of Entomology 44, – 3 4 plants become weakened and are eventually killed. 483 505. 4 Iba M (1980) Ecological studies on the yellow-spotted longicorn beetle, Psacothea hilaris Pascoe. IV. The geographic difference of the 5 pattern on the pronotum of adult. Journal of Sericultural Science of 6 Distribution and biology of the yellow- Psacothea hilaris Japan 49, 429–433 (in Japanese). 7 spotted longicorn beetle hilaris Iba M, Inoue S & Kikuchi M (1976) Ecological studies on the yellow- 8 (Pascoe) in Italy spotted longicorn beetle, Psacothea hilaris Pascoe. I. The local 9 The Asiatic yellow-spotted longicorn beetle, Psacothea difference in the seasonal prevalence of the adult insect. Journal of – 10 hilaris hilaris, was found for the first time in Northern Italy Sericultural Science of Japan 45, 156 160 (in Japanese). 11 Iba M (1993) Studies on the ecology and control of the yellow-spotted in 2005. As the xylophagous insect is considered one of the longicorn beetle, Psacothea hilaris Pascoe (Coleoptera: Cerambycidae), 12 most important pests of Morus spp. and Ficus carica in its in the mulberry fields. Bulletin of National Institute of Sericultural and 13 countries of origin, a multi-year study was carried out to Entomological Society of Japan 8,1–119 (in Japanese). 14 determine the spread of the pest in Northern Italy, to Jucker C, Tantardini A & Colombo M (2006) First record of Psacothea 15 evaluate its establishment potential and to improve hilaris (Pascoe) in Europe (Coleoptera Cerambycidae Lamiinae 16 knowledge on its biology in the new habitat. The survey Lamiini). Bollettino di Zoologia Agraria e Bachicoltura, Serie II 38(2), 187–191. 17 confirmed that P. hilaris hilaris has established in Italy and Exotic Insects in Italy: An Overview on 18 2 Jucker C & Lupi D (2011) has colonized an area of about 60 km . The species Their Environmental Impact, The Importance of Biological 19 overwinters as eggs or larvae. Adults are present from June Interactions in the Study of Biodiversity, (Ed. Lopez Pujol J), ISBN: 20 to October. Damage has been recorded mostly on Ficus 978-953-307-751-2, InTech, http://www.intechopen.com/articles/show/ 21 carica plants, and very rarely on Morus alba. Both young title/exotic-insects-in-italy-an-overview-on-their environmental-impact 22 and older plants in healthy and stressed phytosanitary [accessed on xx xxxxx xxxx]. 8; 9 23 condition can be attacked by the pest. Severely attacked Kusama K & Tatakuwa M (1984) Lamiinae. In: The Longicorn-Beetles of Japan in Color. (Ed. Japanese Society of Coleopterology) , pp. 24 plants become weakened and are eventually killed. 374–493. Kodansha Inc., Tokyo (JP) (in Japanese). 25 Makihara H (1986) Longicorn beetle. Expansion of the distribution and 26 References geographic variation. In: Japanese Insect. Ecology of Invasion and 27 Disturbance (Ed.Kiritani K), pp. 99–106. Tokai Univ. Press, Tokyo 28 Ciampolini M, Regalin R & Peerin H (2005) Aclees cribratus, nuovo (JP) (in Japanese). 29 per l’Italia nocivo al fico allevato in vivaio. L’Informatore agrario Pinna M (1978) L’atmosfera e il climaUtet, ?????, Torino (IT), pp. 478 10 30 61(47), 69–71 (in Italian). (in Italian). 31 EPPO (2008) Psacothea hilaris detected in the United Kingdom: addition Sakakibara M & Kawakami K (1992) Larval diapauses inheritance mode in two ecotypes of the yellow-spotted longicorn beetle, 32 to the EPPO Alert List/201. EPPO Reporting Sevice, no10, 10-11. http://archives.eppo.int/EPPOReporting/2008/Rse-0810.pdf [accessed Psacothea hilaris (Pascoe) (Coleoptera: Cerambycidae). Applied 33 – on 8 January 2013] Entomology and Zoology 27,47 56. 34 FERA (2010) Psacothea hilaris (Coleoptera: Cerambycidae) and Other Shintani Y & Ishikawa Y (1999) Geographic variation in cold 35 Exotic Longhorn Beetles. http://www.fera.defra.gov.uk/showNews. hardiness of eggs and neonate larvae of the yellow-spotted longicorn – 36 7 cfm?id=454 [accessed on 8 January 2013]. beetle, Psacothea hilaris. Physiological Entomology 24, 158 164. 37 Fukaya M (2004) Effects of male body size on mating activity and Watari Y, Yamanaka T, Asano W & Ishikawa Y (2002) Prediction of 38 female mate refusal in the yellow-spotted longicorn beetle, the life cycle of the west Japan type yellow-spotted longicorn beetle, Psacothea hilaris (Pascoe) (Coleoptera: cerambycidae): are small Psacothea hilaris hilaris (Coleoptera: Cerambycidae) by numerical 39 – males inferior in mating? Applied Entomology and Zoology 39(4), simulation. Applied Entomology and Zoology 37(4), 559 569. 40 603–609. 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56

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‚ C

d r a w t h e s e l e c t e d s h a p e w i t h t h e c u r s o r .

o a d d a c o m m e n t t o t h e d r a w n s h a p e ,

‚ T

m o v e t h e c u r s o r o v e r t h e s h a p e u n t i l a n

a r r o w h e a d a p p e a r s .

o u b l e c l i c k o n t h e s h a p e a n d t y p e a n y

‚ D

t e x t i n t h e r e d b o x t h a t a p p e a r s .