Two invasive alien insect species, Leptoglossus occidentalis (Heteroptera: Coreidae) and Cydalima perspectalis (Lepidoptera: Crambidae), and their distribution and host plants in Istanbul Province, Turkey.
Abstract: Leptoglossus occidentalis (Heidemann, 1910) and Cydalima perspectalis (Walker, 1859) are alien insect species which have invaded Turkey. Leptoglossus occidentalis was recorded for the first time in Istanbul (Turkey) in 2009 and Cydalima perspectalis was recorded there for the first time in 2011. We examined the distribution of these two invasive alien insect species, and their host plants, in Istanbul province of Turkey. Leptoglossus occidentalis was observed in Istanbul Province on Pinus nigra, Pinus pinea, Pinus radiata and Abies concolor. Cydalima perspectalis was recorded only on Buxus sempervirens and B. sempervirens cv 'aureavariegata' in Istanbul Province, and severe damage was inflicted on these cultivars.

Key Words: Leptoglossus occidentalis, Cydalima perspectalis, Buxus sempervirens, Buxus sempervirens cv 'aureavariegata', Pinus nigra, Pinus pinea, Pinus radiata, Abies concolor

Leptoglossus occidentalis (Heidemann, 1910) y Cydalima perspectalis (Walker, 1859) son especies de insectos exoticos invasores en Turquia. Se registro Leptoglossus occidentalis por primera vez en Estambul, Turquia en el 2009 y se registro Cydalima perspectalis por primera vez en Estambul, Turquia en el 2011. Este estudio examino la distribution de estas dos especies de insectos exoticos invasivores y sus plantas hospederas en la Provincia de Estambul en la Turquia. Se observo Leptoglossus occidentalis en la provincia de Estambul sobre Pinus nigra, Pinus pinea, Pinus radiata y Abies concolor. Se registro Cydalima perspectalis sobre Buxus sempervirens y B. sempervirens cv 'aureavariegata, en la Provincia de Estambul, y causando dano grave a estos cultivares.
Article Type: Report
Subject: Entomology (Research)
Lepidoptera (Distribution)
Invasive species (Research)
Author: Hizal, Erdem
Pub Date: 06/01/2012
Publication: Name: Florida Entomologist Publisher: Florida Entomological Society Audience: Academic Format: Magazine/Journal Subject: Biological sciences Copyright: COPYRIGHT 2012 Florida Entomological Society ISSN: 0015-4040
Issue: Date: June, 2012 Source Volume: 95 Source Issue: 2
Topic: Event Code: 310 Science & research; 690 Goods & services distribution Advertising Code: 59 Channels of Distribution Computer Subject: Company distribution practices
Geographic: Geographic Scope: Turkey Geographic Code: 7TURK Turkey
Accession Number: 299988812
Full Text: Globalization of trade and travel on an unprecedented scale, has inadvertently led to the increased transport and introduction of alien species, and the breaking down of natural barriers between countries and continents (Lowe et al. 2000). Invasive alien species are increasingly recognized as one of the major threats to biodiversity (Wittenberg et al. 2006).

The western conifer seed bug, Leptoglossus occidentalis (Heidemann, 1910) (Heteroptera: Coreidae), is an invasive alien species of North American origin (McPherson et al. 1990). In Europe, it was first collected in Italy in 1999 (Tescari 2001). From there, it quickly expanded its range to western and eastern Europe (Bernardinelli & Zandigiacomo 2001; Hradil 2008; Kment & Banar 2008; Lis et al. 2008; Rabitsch 2008; Simov, 2008; Werner 2011). Leptoglossus occidentalis was recorded for the first time in Sariyer, Turkey in 2009 (Arslangundogdu &Hizal 2010).

Leptoglossus occidentalis is specialised to conifers. It has been recorded from about 40 species of conifers, mostly from pines (Pinales: Pina ceae), e.g., Coulter pine (Pinus coulteri D. Don), Aleppo pine (P. halepensis Mill.), Jeffrey pine (P. jeffreyi Balf.), sugar pine (P. lambertiana Douglas), western white pine (P. monticola Douglas ex D. Don), mugo pine (P. mugo Turra), Austrian pine (P. nigra J. F. Arnold), Italian stone pine (P. pinea L.), Ponderosa pine (P. ponderosa P. Lawson & C. Lawson), Monterey pine (P. radiata D. Don), red pine (P. resinosa Alton), California foothill pine (P. sabiniana Douglas), eastern white pine (P. strobus L.), and Scots pine (P. sylvestris L.), but also on Douglas fir (Pseudotsuga menziesii [Mirb.] Franco), big-cone Doulas fir (P. macrocarpa [Vasey] Mayr), eastern hemlock (Tsuga canadensis Carriere), mountain hemlock (T. mertensiana (Bong.) Carriere), incense cedar (Calocedrus [=Libocedrus] decurrens (Torr.) Florin [Pinales: Cupressaceae]), white fir (Abies concolor [Gord. & Glend.] [Pinales: Pinaceae]), California red fir (A. magnifica A. Murray), white spruce (Picea glauca [Moench] Voss; [Pinales: Pinaceae]) and Italian cypress (Cupressus sempervirens L. [Pinales: Cupressaceae]) (e.g., Koerber 1963; McPherson et al. 1990; Gall 1992; Vanin et al. 2005; Kment & Banaf 2008; Protic 2008; Maltese et al. 2009).

Leptoglossus occidentalis feeds on young developing cones and may cause abortion of young conelets, fusion of seeds to cone scales as well as direct damage by depletion of the lipid and protein content of the seed up to its complete emptying (Bates et al. 2000a, b). Tiberi (2007) listed L. occidentalis among pests of Pinus pinea cultivated in Italy. Uyemoto et al. (1986) reported damage caused by L. occidentalis on cultivated pistachio.

Box tree moth Cydalima perspectalis (Walker, 1859) (Lepidoptera: Crambidae) is an invasive alien species of East Asia origin. The natural range of the C. perspectalis is the humid subtropical regions of East Asia, India, China, Japan, Korea and Russian Far East (Mally & Nuss, 2010). In Europe, it was reported for the first time in 2007, in Germany (Billen 2007). In subsequent years, C. perspectalis (Walker 1859) continued to spread in Germany and nearby countries (Straten & Muus 2010). Cydalima perspectalis was recorded for the first time in Sariyer, Turkey in 2011 (Hizal et al. 2012).

Cydalima perspectalis causes damage on Japanese box (Buxus microphylla Siebold & Zucc.; Euphorbiales: Buxaceae), common box (B. sempervirens L.), Chinese boxwood (B. sinica [Rehder & E. H. Wilson] M. Cheng), Japanese spindletree (Euonymus japonicus Thunb.; Celastrales: Celastraceae), Burningbush (E. alata (Thunb.) Siebold), Purple holly (Ilex purpurea Hassk.; Aquifoliales: Aquifoliaceae) (Maruyama 1993; Kawazu et al. 2007, 2010; Straten & Muus 2010; Korycinska & Eyre 2011). The plants lose all of their leaves as a result of the attack of this moth.

Here I report on the distribution and host plants of L. occidentalis and C. perspectalis in the Istanbul Province Turkey.

Materials and Methods

Leptoglossus occidentalis especially prefers coniferous trees and damages young developing cones. For this reason, coniferous tree species distribution areas were marked on forest management plan maps. The marked points included possible areas of damage. The species is much easier to find in the late summer and fall when it is seeking out overwintering locations. Possible areas of damage were visited 4 times each month between the dates Sep-Dec 2009, Aug-Dec 2010, and Aug-Dec 2011. Adults were captured by using an insect net on the needles, cones and insects in flight. Bird nest boxes, the loose bark of trees, and buildings near the possible areas of damage were investigated.

Cydalima perspectalis larvae damage boxwood leaves. Buxus species are widely used for decorative purposes in parks and gardens. European and Asian (Anatolian) sides of the parks and gardens were visited 2 days a week starting on 20 Jun 2011. Leaves were searches for C. perspectalis larvae.

All data concerning the presence of these pests were transferred to tables and maps, and specific mapped locations were sampled to ascertain the distribution of these 2 adventive species.

Results

Leptoglossus occidentalis was first recorded from the Istanbul Province on 14 Sep 2009 in the Fatih Forest at Sariyer-Istanbul. Sampling locations and host plants on which L. occidentalis was observed for all sampling dates are listed in Table 1; and these same locations are displayed on the map of sampling locations, Fig. 1. Consistent with earlier host plant records, L. occidentalis was observed in the Istanbul Province on Pinus nigra, Pinus pinea, Pinus radiata and Abies concolor.

Cydalima perspectalis was recorded for the first time in the European side of Sariyer-Istanbul in Turkey on 15-VI-2011, and the species was particularly abundant in the Sariyer district. Cydalima perspectalis was not detected in the Asian side of Istanbul until 30-VII-2011 (Hizal et al. 2012).

Host plants on which C. perspectalis specimens were recorded and their locations are listed in the Table 2, and shown in Fig. 2. Only Buxus sempervirens, common boxwood, and B. sempervirens cv 'aureavariegata', golden variegated boxwood, were noted as host plants in Istanbul Province. I observed severe damage to Buxus spp. in the parks and gardens of Istanbul Province, where these boxwoods are used extensively in topiary plantings.

Discussion

In 2009 L. occidentalis was observed only on the European side of Istanbul, but in 2010, it was recorded for the first time from the Asian (Anatolian) side. At a minimum, the water barrier to dispersal in Istanbul is 700 m wide between Kandilli point and Asiyan. This may have slowed down, but clearly did not stop, the spread of this very strong flier. It may be that the presence of large plantation areas in Istanbul Province contributed to ease with which this species has spread in Turkey. Because L. occidentalis is known as a pest of cultivated pistachio (Uyemoto et al. 1986), it's presence in Turkey potentially threatens cultivated Pistacia vera L. (Sapindales: Anacardiaceae) in Turkey.

There are 2 natural Buxus species (Balearic box-Buxus balearica Lam., and Common Box-B. sempervirens L.) in Turkey (Yaltirik and Efe 2000). Cydalima perspectalis is a new harmful species that poses a great threat to both natural Buxus species and also the ones used in parks and gardens.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Our understanding of the biology, distribution, host plants, chemical and biological control methods of Leptoglossus occidentalis and Cydalima perspectalis in Turkey is far from adequate. Additional studies are needed to assess the extent of the threat posed by these 2 invaders, and to develop appropriate preventive or response strategies.

References Cited

Arslangundogdu, A. and Hizal, E. 2010. The western conifer seed bug, Leptoglossus occidentalis (Heidemann, 1910), recorded in Turkey (Heteroptera: Core idae). Zool. Middle East 50: 138-139.

Bates, S. L., Borden, J. H., Kermode, A. R., and Bennett, R. G. 2000a. Impact of Leptoglossus occidentalis (Hemiptera: Coreidae) on Douglas-fir seed production. J. Econ. Entomol. 93: 1444-1451.

Bates, S. L., Borden, J. H., Savoie, A., Blatt, S. E., Lait, G. C., Kermode, A. R., and Bennett, R. G. 2000b. Impact of feeding by Leptoglossus occidentalis (Hemiptera: Coreidae) on the major storage reserves of mature Douglas-fir (Pinaceae) seeds. Canadian En tomol. 132: 91-102.

Bernardinelli, I., and P. Zandigiacomo, 2001. Leptoglossus occidentalis Heidemann (Heteroptera, Coreidae): a conifer seed bug recently found in northern Italy. J. For. Sci. 47 (Special Issue No. 2): 56-58.

Billen, W. 2007. Diaphania perspectalis (Lepidoptera: Pyralidae) - a new moth in Europe. Mitt. Entomol. Ges. Basel 57: 135-137.

Gall, W. K. 1992. Further eastern range extension and host records for Leptoglossus occidentalis (Heteroptera: Coreidae): well documented dispersal of a household nuisance. Gt. Lakes Entomol. 25: 159-171.

Hizal, E., Kose, M., Yesil, C., and Kaynar, D. 2012. The new pest Cydalima perspectalis (Walker, 1859) (Lepidoptera: Crambidae) in Turkey. J. Animal Veter. Adv. 11 (3): 400-403.

Hradil, K. 2008. Leptoglossus occidentalis (Heteroptera: Coreidae), A new alien species in Montenegro. Acta Entomol. Serbica 13(1/2): 77-79.

Kawazu, K., Honda, H., Nakamura, S., and Adati, T. 2007. Identification of sex pheromone components of the box tree pyralid, Glyphodes perspectalis. J. Chem. Ecol. 33: 1978-1985.

Kawazu, K., Nakamura, S., and Adati, T. 2010. Rearing of the box tree pyralid, Glypodes perspectalis, larvae using an artificial diet. Appl. Entomol. Zool. 45 (1): 163-168.

Kment, P., and Bauar, P. 2008. Additional records of the invasive Nearctic bug Leptoglossus occidentalis (Heteroptera: Coreidae) in Croatia. Natura Croatica 17: 141-147.

Koerber, T. W. 1963. Leptoglossus occidentalis (Hemiptera, Coreidae), a newly discovered pest of coniferous seed. Ann. Entomol. Soc. Am. 56: 229-234.

Korycinska, A., and Eyre, D. 2011. Box tree caterpillar, Cydalima perspectalis. The Food and Environ. Res. Agency (FERA). http://www.fera.defra.gov.uk/plants/publications/documents/ factsheets/boxTreeCaterpillar2011.pdf

Lis, J. A., Lis, B., and Gubernator, J. 2008. Will the invasive western conifer seed bug, Leptoglossus occidentalis Heidemann (Hemiptera: Heteroptera: Coreidae), seize all of Europe? Zootaxa 1740: 66-68.

Lowe, S., Browne, M., Boudjelas, S., and De Poorter, M. 2000. 100 of the world's worst invasive alien species. A selection from the Global Invasive Species Database. Publ. Invasive Species Specialist Group (ISSG), a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN). 12 pp. First publ. special lift-out in Aliens 12 Dec. 2000. Updated and reprinted version: Nov. 2004.

Mally, R., and Nuss, M. 2010. Phylogeny and nomenclature of the box tree moth, Cydalima perspectalis (Walker, 1859) comb. n., which was recently introduced into Europe (Lepidoptera: Pyraloidea: Crambidae: Spilomelinae). European J. Entomol. 107: 393-400.

Maltese, M., Caleca, v., and Carapezza, A. 2009. Primi reperti in Sicilia su diffusione e biologia di Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae), cimice americana dei semi delle conifere, pp. 1413-1418 In Atti del Terzo Congresso Nazionale di Selvicoltura. Taormina (ME), 16-19 ottobre 2008. Accademia Italiana di Scienze Forestali, Firenze.

Maruyama, T., 1993. Life cycle of the box-tree pyralid, Glyphodes perspectalis (Walker) (Lepidoptera: Pyralidae). IV. Effect of various host plants on larval growth and food utilization. Japanese J. Appl. Ento mol. Zool. 7(3): 117-122 (abstract).

McPherson, J. E., Packauskas, R. J., Taylor, S. J., and O'brien, M. F. 1990. Eastern range extension of Leptoglossus occidentalis with a key to Leptoglossus species of America north of Mexico (Heteroptera: Core idae). Gt. Lakes Entomol. 23: 99-104.

Protic, L. 2008. Leptoglossus occidentalis Heidemann (Heteroptera: Coreidae) in Serbia. Acta Entomol. Serbica 13: 81-84.

Rabitsch, w. 2008. Alien true bugs of Europe (Insecta: Hemiptera: Heteroptera). Zootaxa 1827: 1-44.

Simov, N. 2008. Western conifer seed bug Leptoglossus occidentalis Heidemann, 1910 (Heteroptera: Coreidae) already in Bulgaria. Historia Naturalis Bul garica: 19: 179-180.

Tescari, G., 2001. Leptoglossus occidentalis, coreide neartico rinvenuto in Italia - (Heteroptera,Coreidae). Societa Veneziana di Scienze Naturali, Lavori 26: 3-5.

Tiberi, R., 2007. Progetto territoriale: Danni alla fruttificazione del pino domestico: indagine sulle cause e sulle perdite di produzione. Arsia, Regione Toscana & Universitas Florentina. 19 pp.

Uyemoto, J. K., Ogawa, J. M., Rice, R. E., Teranishi, H. R., Bostock, R. M., and Pemberton, w. M. 1986. Role of several true bugs (Hemiptera) on incidence and seasonal development of pistachio fruit epicarp lesion disorder. J. Econ. Entomol. 79: 395-399.

Van Der Straten, M. J., and Muus, T. S. T. 2010 The box tree pyralid, Glyphodes perspectalis (Lepidoptera: Crambidae), an invasive alien moth ruining box trees. Proc. Netherlands Entomol. Soc. 21: 107111. http://www.nev.nl/sete/sete-2010/107-112-vdStratenMuus-2010.pdf

Vanin, S., Uliana, M., Bonato, L., and Maistrello, L. 2005. Nuove segnalazioni di Leptoglossus occidentalis (Heteroptera, Coreidae) nell'Italia nord-orientale. Societa Veneziana di Scienze Naturali, Lavori 30: 149.

Werner, D. J. 2011. Die Amerikanische Koniferen-Samen-Wanze Leptoglossus occidentalis (Heteroptera: Coreidae) als Neozoon in Europa und in Deutschland: Ausbreitung un Biologie. Entomologie heute 23:31-68

Wittenberg, R., Kenis, M., Hanggi, A., and Weber, E. 2006. Invasive alien species in Switzerland (An inventory of alien species and their threat to biodiversity and economy in Switzerland), Publ. Federal Office Environ. (FOEN). www.bafu.admin.ch/publikationen/publikation/00028/index.html?lang=...

Yaltirik, F. and Efe, A. 2000. Dendroloji, Istanbul Universitesi Orman Fakultesi Yayinlari No: 4265/465, ISBN: 975-404-594-1.

Erdem Hizal

Department of Forest Entomology and Protection, Istanbul University, Faculty of Forestry, 34473 Sariyer Istanbul, Turkey
Table 1. Leptoglossus occidentalis distribution and host plants, each
number in parentheses is a point on the map shown in Fig. 1.

Periods When Systematic Sampling Was Conducted

                     Between 14 Sep 2009 and 30 Dec 2009

                        European          Asian (Anatolian)
Host Plant                Side                   Side

Pinus nigra      Fatih Forest (1)         Anadolu Feneri (8)
                                          (Not detected)

                 Rumeli Feneri Road (2)   Polonezkoy (9)
                                          (Not detected)

                 Koc University           Kanlica (10)
                 Campus (3)               (Not detected)

                 Istanbul University      Beykoz (11)
                 Forestry Faculty         (Not detected)
                 Campus (4)

                                          Alemdag (13)
                                          (Not detected)

Pinus pinea      Fatih Forest (1)         Alemdag (13)
                                          (Not detected)

                 Ataturk Arboretum (5)    Anadolu Feneri (8)
                                          (Not detected)

Pinus radiata    Feneryolu (6)

Abies concolor   Ataturk Arboretum (5)    (Not detected)

                       Between 10 Aug 2010 and 30 Dec 2010

                        European          Asian (Anatolian)
Host Plant                Side                   Side

Pinus nigra      Fatih Forest (1)         Anadolu Feneri (8)

                 Rumeli Feneri Road (2)   Polonezkoy (9)

                 Koc University           Kanlica (10)
                 Campus (3)

                 Istanbul University      Beykoz (11)
                 Forestry Faculty
                 Campus (4)

Pinus pinea      Fatih Forest (1)         Beykoz (11)

                 Ataturk Arboretum (5)
                 Demircikoy (7)

Pinus radiata    Feneryolu(6)

Abies concolor   (Not detected)           (Not detected)

                      Between 15 Aug 2011 and 30 Dec 2011

                       European          Asian (Anatolian)
Host Plant               Side                   Side

Pinus nigra      Fatih Forest (1)        Anadolu Feneri (8)

                 Rumeli                  Polonezkoy (9)
                 Feneri Road (2)

                 Koc University          Kanlica (10)
                 Campus (3)

                 Istanbul University     Beykoz (11)
                 Forestry Faculty
                 Campus (4)

                 Tayakadin (12)          Alemdag (13)

Pinus pinea      Fatih Forest (1)        Alemdag (13)

                 Ataturk Arboretum (5)

Pinus radiata    Feneryolu(6)

Abies concolor   (Not detected)          (Not detected)

Table 2. Cydalima perspectalis distribution and host plants, each
number in parentheses is a point on the map shown in Fig. 2.

Periods When Systematic Sampling Was Conducted

                            Between 20 Jun 2011 and 30 Jul 2011

Host Plant              European Side         Asian (Anatolian) Side

Buxus              Istanbul Univ. Forestry   Uskudar (7) Not detected
sempervirens       Faculty Campus (1)

                   Fatih Forest (2)          Beykoz (8) Not detected

                   Yenikoy (3)

                   Emirgan (4)

                   Zekeriyakoy (5)

Buxus              Istanbul Univ. Forestry
                   Faculty Campus (1)
sempervirens cv.
'aureavariegata'

                                  Later than 30 Jul 2011

Host Plant              European Side        Asian (Anatolian) Side

Buxus              Istanbul Univ. Forestry   Near woods, Fethipasa
sempervirens       Faculty Campus (1)        -Uskudar (7)

                   Fatih Forest (2)          Beykoz (8)

                   Yenikoy (3)

                   Emirgan (4)

                   Zekeriyakoy (5)

                   Kemerburgaz (6)

Buxus

sempervirens cv.
'aureavariegata'
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