NARDI and VOMERO: Trogoderma variabile Ballion, 1878: A Possible New Pest of Italian Entomological Collections(Coleoptera: Dermestidae)

Trogoderma variabile Ballion, 1878: A Possible New Pest of Italian Entomological Collections
(Coleoptera: Dermestidae)

Abstract

The first infestation of an entomological collection in Italy by Trogoderma variabile Ballion, 1878 is recorded; it was detected in Rome in 2014. This record and another one from the Molise Region, are herein discussed. Distributional, biological and nomenclatural data on this polyphagous alien pest are summarized, and its possible local establishment is discussed.





Introduction

Trogoderma variabile Ballion, 1878 (Figs 1–2) is a cosmopolitan (Háva 2015) polyphagous species of high economic relevance, since it represents a pest of stored products and of zoological and botanic collections (Hagstrum & Subramanyam 2009; Hagstrum et al. 2013; see also http://www.MuseumPest.net).

Hereunder, captures of this alien species in Italy are discussed in order to alert museum curators handling botanical and zoological collections.

Material and Methods

The specimens were identified following various works (Bousquet 1990; Kingsolver 1991; Peacock 1993; Banks 1994; Háva 2011) and finally, identification was confirmed by Jiří Háva (Praha-západ, Czech Republic).

Acronyms of specimen depositories:

CGN

G. Nardi collection, Cisterna di Latina (Latina), Italy

CJH

J. Háva collection, Praha-západ, Czech Republic (J. Háva, pers. comm., 2017)

CVV

V. Vomero collection, Rome (Italy)

Results

Trogoderma variabile Ballion, 1878

  • Trogoderma variabilis [sic!] Ballion, 1878: 277.

  • Trogoderma (Phradonoma) variabilis [sic!] Ball.: Sumakov 1907: 17.

  • Globicornis 4-guttata [(Reitter, 1878)] ssp. unifasciata Pic, 1908: 41.

  • Globicornis quadriguttata ssp. subfasciata [sic!] Pic, 1908: Dalla Torre 1911: 64.

  • Phradonoma variabile Ballion, 1878: Dalla Torre 1911: 66.

  • Trogoderma persica [sic!] Pic, 1914: 10.

  • Trogoderma parabile Beal, 1954: 53.

Material examined. Italy: Lazio, Roma, Nuovo Salario, 41.57.18.59N, 12.31.6.94E (WGS84), Jun 2014, V. Vomero leg., on dry beetles, many adults and larvae (CGN; CVV); Molise, Campomarino (Campobasso), 25 May 1993, J. Háva sen. & Y. Elznicova leg., at light, 2 adults (CJH).

Chorotype and distribution. Cosmopolitan (Háva 2015). This species, indigenous to Central Asia (cf. Ballion 1878; Mroczkowski 1968; Hagstrum et al. 2013), is currently known from all zoogeographical regions, but is mainly distributed in the Holarctic Region (cf. Hagstrum & Subramanyam 2009; Háva 2015). In Europe, it was firstly recorded from Caucasus (Mroczkowski 1968) and since 1975 in other regions (cf. Šefrová & Laštůvka 2005; Denux & Zagatti 2010). In Europe it is known from: Armenia, Belarus, Czech Republic, Finland, Great Britain, Greece, Italy, Latvia, Lithuania, South European Russia, Sweden and The Netherlands (Barševskis 2001; Hagstrum et al. 2013; Zhantiev 2013; Háva 2015).

This species was also recorded from Belarus (Barševskis 2001), Kyrgyzstan (Ovchinnikov 1996), “Syrie” (Pic 1908, as Globicornis 4-guttata unifasciata; Háva 2007), and The Netherlands (cf. Hagstrum et al. 2013; Zhantiev 2013) and these countries were not included in the distributional data provided by Háva (2015).

Ecology. In synanthropic environments, the larvae of T. variabile feed on grain, seeds, cereals, legumes, cocoa, nuts, milk powder and a wide range of other dried high-protein materials, including specimens of zoological collections and of herbaria (cf. Bousquet 1990; Peacock 1993; Beal 2003; Hagstrum et al. 2013). The adults do not feed (Peacock 1993). The synanthropic association of T. variabile is very old; Chu and Wang (1975, as T. persicum Pic) recorded this species from a Chinese tomb of ca. 100 B.C. In natural habitats, this dermestid develops in bees’ and birds’ nests and these can act as a source of infestation (Peacock 1993; Ikin et al. 1999).

Females of Trogoderma variabile, exhibit a diel pattern of calling behavior, and they produce a potent sexual pheromone to attract males (cf. Tobin & Bell 1986; Wright & Delves 1994); both males and females have four categories of antennal sensilla (Wei et al. 2015), that probably are involved also in the sexual communication.

The females of this species, as those of other congeners, are known to develop through a higher number of larval instars than males: on average, female larvae pupate after six larval instars, whereas males pupate after five. Under optimal conditions the life cycle of Trogoderma variable from egg to adult is completed in 30 to 37 days. Nevertheless, if conditions are unfavorable larvae can enter diapause during which period they can survive more than a year without food (cf. Esperk et al. 2007; Hagstrum & Subramanyam 2009; see also http://www.MuseumPest.net). The larvae (Fig. 3), have numerous hastisetae on the dorsal surfaces of all segments (Peacock 1993). Hastisetae are easily pulled from the larva when setae of another arthropod become wedged in the slots, so their function is defensive, incapacitating possible arthropods predators by entangling their appendages (cf. Hagstrum & Subramanyam 2006). Anyway, the larvae and pupae of this species are the host of some ectoparasitic wasps of the genus Laelius Ashmead, 1893 (Hymenoptera, Bethylidae) (cf. Hagstrum & Subramanyam 2009), moreover, some nematode species are endoparasites of this dermestid (Rumbos & Athanassiou 2017), and a coccidian Protist can infect larvae, pupae, and adults of this species (Loschiavo 1969, as T. parabile Beal).

Unlike many Trogoderma species, the adult of T. variabile can fly and, at least, the males have a high degree of mobility, with individual beetles moving vertically and horizontally (cf. Hagstrum & Subramanyam 2006).

This species, as other congeners, can produce allergic reactions in humans (cf. Ikin et al. 1999; Bernstein et al. 2009).

In the U.S.A., T. variabile is the most economically serious dermestid pest of stored products (Beal 2003), and in Australia it was target of an eradication campaign (cf. Hagstrum & Subramanyam 2009; Castalanelli et al. 2011), while in Canada it is only considered as a minor pest (Bousquet 1990).

Notes. Trogoderma variabile is similar to T. versicolor (Creutzer, 1799), but differs by the morphology of the antennae, elytral maculation and male genitalia (cf. Bousquet 1990; Kingsolver 1991; Peacock 1993; Banks 1994; Háva 2011).

Trogoderma variabile (excluding some generic citations – “Italy” and “mainland Italy”) was recorded with certainty from three Italian regions: Piedmont, Emilia-Romagna and Sardinia (cf. Nardi & Háva 2013 and references herein). According to Nicoli Aldini (2014), it seems established in the Emilia-Romagna Region. It is possible that prior to this study, this species was overlooked or misidentified owing to its similarity to other closely related species (Peacock 1993; Bank 1994).

The above-mentioned records of T. variabile are the first from peninsular Italy. The record from the Molise region is two years older than the previous records from other Italian regions (cf. Nardi & Háva 2013 and references herein). The above-mentioned record from Rome is based on several adults and larvae (Figs 1–3) infesting dry beetles housed in the entomological collection of V. Vomero, collected from Laos and Italy. This Italian material was collected by V. Vomero, while the Asian beetles have been borrowed directly from local collectors and later sent for preparation in Czech Republic, where the dermestid infestation began, in fact T. variabile occurs in this country (cf. Háva 2011).

The potential establishment of this species is high, since it can breed on a variety of stored foodstuffs and it is also capable of establishing in the natural environment, moreover, larvae often conceal themselves in cracks and crevices and can be difficult to detect (Ikin et al. 1999). In this framework, the above infested collection underwent a fumigation treatment with insecticide containing permethrin 25/75, tetramethrin and piperonyl butoxide, and, the species seems to be eradicated in these premises.

The damage produced by larvae of this species in beetle collections is different from those of Anthrenus spp. (V. Vomero, unpublished data). The infested specimens by T. variabile are heavily damaged but sclerotized parts (e.g. male genitalia, and female styles) remain intact. Examination of the droppings of T. variabile revealed that only the soft tissue of dead beetles is consumed by this pest.

Discussion. Seven species of Trogoderma Dejean, 1821 occur in Italy, and five of them are now known from peninsular regions (cf. Nardi & Háva 2013).

The above new records show that to avoid the spreading in Italy of T. variabile, it is, obviously, necessary to survey imported foodstuffs, using also pheromone-baited traps and to disinfest dry insect collection (cf. Peacock 2003; Hagstrum & Subramanyam 2006, 2009; Hagstrum et al. 2013). In both cases, it is important to check the possible signs of infestation (live or dead beetles, larval exuviae, a fine dust, emergence holes in whole grains), and to remember that during diapause the larvae may be unresponsive to many common pest control treatments (see http://www.MuseumPest.net).

Finally, from a nomenclatorial point of view, this species was described as Trogoderma variabilis Ballion, 1878. According to ICZN (1985, art. 34b), the species name must agree in gender with the generic name (neuter), so this termination is incorrect and was changed accordingly by Mroczkowski (1968) to T. variabile. The same is valid also for T. persica Pic, 1914 (cf. Háva 2015).

Acknowledgements

Thanks are due to Vincenzo Andriani (Ufficio Territoriale Carabinieri per la Biodiversità di Verona, Verona, Italy), Paolo Audisio (Sapienza Università di Roma, Roma, Italy), Paolo Cornacchia (Porto Mantovano, Mantova, Italy), Franco Mason (Centro Nazionale Biodiversità Carabinieri Bosco della Fontana, Verona, Italy), Gianluca Scaglioni (Porto Mantovano, Mantova, Italy), and Laura Spada (Valeggio sul Mincio, Verona, Italy), for their help; Maurizio Gigli (Roma, Italy) for the photographs of Trogoderma variabile adults; Jiří Háva (Praha-západ, Czech Republic) for the control of our taxonomic identification and for the record from Molise, David Mifsud (University of Malta, Msida, Malta) for the linguistic revision of the manuscript.

References

1 

E Ballion. 1878. Verzeichnis der im Kreise von Kuldscha gesammelten Käfer. Bulletin de la Société impériale des Naturalistes de Moscou, 53: 253–389.

2 

H.J. Banks 1994. Illustrated identification keys for Trogoderma granarium, T. glabrum, T. inclusum and T. variabile (Coleoptera: Dermestidae) and other Trogoderma associated with stored products. CSIRO Australia Division of Entomology Technical Paper 32, iv + 66 pp.

3 

A Barševskis. 2001. New and rare species of beetles (Insecta: Coleoptera) in the Baltic states and Belarus. Baltic Journal of Coleopterology, 1(1–2): 3–18.

4 

R.S. Beal Jr. 1954. Biology and taxonomy of the Nearctic species of Trogoderma (Coleoptera: Dermestidae). University of California Publications in Entomology, 10(2): 35–102.

5 

R.S. Beal Jr. 2003. Annotated Checklist of Nearctic Dermestidae with Revised Key to the Genera. The Coleopterists Bulletin, 57(4): 391–404. doi: http://dx.doi.org/10.1649/573

6 

J.A. Bernstein, M.S. Morgan, D. Ghosh, L. Arlian 2009. Respiratory sensitization of a worker to the warehouse beetle Trogoderma variabile: An index case report. Journal of Allergy and Clinical Immunology, 123(6): 1413–1416. doi: 10.1016/j.jaci.2009.04.006

7 

Y Bousquet. 1990. Beetles associated with stored product in Canada: An identification guide. Agriculture and Agri-Food Canada Publication 1837, 214 pp.

8 

M.A. Castalanelli, K.M. Mikac, A.M. Baker, K. Munyard, M. Grimm, D.M. Groth 2011. Multiple incursions and putative species revealed using a mitochondrial and nuclear phylogenetic approach to the Trogoderma variabile (Coleoptera: Dermestidae) trapping program in Australia. Bulletin of Entomological Research, 101(3): 333–343.

9 

H.F. Chu, L-Y Wang. 1975. Insect carcasses unearthed from Chinese antique tombs [in Chinese]. Acta Entomologica Sinica, 18: 333–337.

10 

O. Denux, P. Zagatti 2010. Coleoptera families other than Cerambycidae, Curculionidae sensu lato, Chrysomelidae sensu lato and Coccinelidae. Chapter 8.5, pp. 315–406. In: A. Roques, M. Kenis, D. Lees, C. Lopez-Vaamonde, W. Rabitsch, J.-Y. Rasplus, D.B. Roy (eds), Alien terrestrial arthropods of Europe. BioRisk, 4(1). doi: 10.3897/biorisk.4.61

11 

T. Esperk, T. Tammaru, S. Nylin, T. Teder 2007. Achieving high sexual size dimorphism in insects: females add instars. Ecological entomology, 32(3): 243–256.

12 

D.W. Hagstrum, B. Subramanyam 2006. Fundamentals of storedproduct entomology. AACC International, St. Paul, Minnesota, USA, v + 324 pp.

13 

D.W. Hagstrum, B. Subramanyam 2009. Stored-Product Insect Resource. AACC International, St. Paul, Minnesota, USA, 509 pp.

14 

D.W. Hagstrum, T. Klejdysz, B. Subramanyam, J. Nawrot 2013. Atlas of Stored-Product Insects and Mites. AACC International Press, St. Paul, Minnesota, USA, 600 pp.

15 

J Háva. 2007. Systematic and synonymic notes upon certain species of Dermestidae (Coleoptera). Studies and Reports of District Museum Prague-East. Taxonomical Series, 3(1–2): 47–49.

16 

J Háva. 2011. Brouci čeledi kožojedovití (Dermestidae) České a Slovenské republiky. Beetles of the family Dermestidae of the Czech and Slovak Republics. Nakladatelství Academia, Praha, 104 pp. [in Czech and English].

17 

J Háva. 2015. World Catalogue of Insects, Volume 13. Coleoptera Dermestidae. Brill, Leiden/Boston, xxvi + 419 pp.

18 

ICZN (International Commission on Zoological Nomenclature) 1999. International Code of Zoological Nomenclature. Fourth edition. International Trust for Zoological Nomenclature, London, xxiv + 306 pp.

19 

B. Ikin, A. Roach, D. Rees, J. Banks 1999. Pest Risk analysis of a proposal for the importation of feed grain Maize (Zea mays) from the USA – Arthropod pest risk analysis. Australian Government, Department of Agriculture and Water Resources, Canberra, 90 pp., available at: http://www.agriculture.gov.au/90

20 

J.M. Kingsolver 1991. Dermestid beetles (Dermestidae, Coleoptera), pp. 115–136. In: J.R. Gorham (ed.), Insect and Mite Pests in Food: An illustrated key. Volume 1. U.S.D.A., Agriculture Handbook number, 655: iv + 767 pp.

21 

S.R. Loschiavo 1969. A coccidian pathogen of the dermestid Trogoderma parabile. Journal of Invertebrate Pathology, 14: 89–92.

22 

M Mroczkowski. 1968. Distribution of the Dermestidae (Coleoptera) of the world with a catalogue of all known species. Annales Zoologici, 26: 15–191.

23 

G. Nardi, J. Háva 2013. Italian Dermestidae: notes on some species and an updated checklist (Coleoptera). ZooKeys, 360: 45–81. doi: 10.3897/zookeys.360.6023

24 

Aldini R Nicoli. 2014. Note sulla presenza nel Piacentino di insetti esotici di recente ingresso in Italia. Parva Naturalia, 10 (2012–2014): 155–170.

25 

S.V. Ovchinnikov 1996. Dermestidae, pp. 136-137. In: Y.S. Tarbinsky (ed.), Genetical fund cadastre of Kyrgyzstan, Volume III. Superclassis Hexapoda (Entognatha and Insecta) [in Russian]. Bishkek, 406 pp.

26 

E.R. Peacock 1993. Adults and larvae of Hide, Larder and Carpet Beetles and their relatives (Coleoptera: Dermestidae) and of Derodontid Beetles (Coleoptera: Derodontidae). Handbooks for the Identifications of British Insects, 5(3), 144 pp.

27 

M Pic. 1908. Descriptions ou diagnoses et notes diverses – Suite –. L′Échange, Revue Linnéenne, 24(282): 41–46.

28 

M Pic. 1914. Notes diverses, descriptions et diagnoses (Suite.). L’Échange, Revue Linnéenne, 30(350): 10–13.

29 

E Reitter. 1878. Hadrotoma quadriguttata n.sp. Deutsche entomologische Zeitschrift, 22: 95.

30 

C.I. Rumbos, C.G. Athanassiou 2017. The use of entomopathogenic nematodes in the control of stored-product insects. Journal of Pest Science, 90: 39. doi: 10.1007/s10340-016-0795-y

31 

H. Šefrová, Z. Laštůvka 2005. Catalogue of alien animal species in the Czech Republic. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis, 53(18): 151–170.

32 

G.G. Sumakov 1907. Novyj vid iz roda Trogoderma Latr. (Coleoptera, Dermestidae) i obzor vidov etogo roda [in Russian]. Russkoe Entomologicheskoe Obozreniye, 7: 15–19.

33 

T.R. Tobin, W.J. Bell 1986. Chemo-orientation of male Trogoderma variabile (Coleoptera, Dermestidae) in a simulated corridor of female sex pheromone. Journal of Comparative Physiology. A: Sensory, Neural and Behavioral Physiology, 158(5): 729–739.

34 

C. Wei, B. Ren, X. Chen, X. Zhou, W. Wang, Z. Wang 2015. Scanning electron microscope observations on the antennal sensilla of two stored grain pests Trogoderma granarium and Trogoderma variabile (Coleoptera: Dermestidae). Florida Entomologist, 98(1): 140–148. doi: http://dx.doi.org/10.1653/024.098.0124

35 

R.D. Zhantiev 2013. Fauna Europaea: Dermestidae. In: P. Audisio (ed.), Fauna Europaea: Coleoptera 2. Fauna Europaea version 2.6, available at http://www.fauna-eu.org [accessed6 February 2017].

Figs 1-2

Trogoderma variabile, adults from Italy, Rome. 1, dorsal view of a (body length: 3.15 mm); 2, dorsal view of a ♀ (body length: 3.1 mm) (photos by M. Gigli).

fe-49-1-235-g001.jpg
Fig. 3

Trogoderma variabile last instar larva (body length: 5.0 mm) from Rome (photo by V. Vomero).

fe-49-1-235-g002.jpg
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