Skip to main content
Log in

Prospects for classical biological control of Marchalina hellenica in Australia

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The giant pine scale, Marchalina hellenica Gennadius (Hemiptera: Marchalinidae), is a sap-sucking insect native to South-East Europe that was recently introduced in Australia where it threatens the pine forestry industry. To initiate a classical biological control programme, a literature review and field surveys were carried out in Greece to investigate the natural enemy complex of the scale. While no parasitoids were found, M. hellenica was attacked by several predators, most notably Neoleucopis kartliana Tanasijtshuk (Diptera: Chamaemyiidae). N. kartliana was present at all sites investigated and is presumably specific to Marchalina. This highlights its potential as a biological control agent for M. hellenica. This predatory fly has already been used to control M. hellenica on the Italian island of Ischia. Interestingly, molecular analyses of Greek samples revealed other Chamaemyiidae predatory flies that can be potentially included in the Australian classical biological control programme of M. hellenica.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bacandritsos N, Saitanis K, Papanastasiou I (2004) Morphology and life cycle of Marchalina hellenica (Gennadius) (Hemiptera: Margarodidae) on pine (Parnis Mt.) and fir (Helmos Mt.) forests of Greece. Ann Soc Entomol Fr 40:169–176

    Article  Google Scholar 

  • Downham R, Gavran M (2017) Australian plantation statistics 2017 update. Australian Government Department of Agriculture and Water Resources, Canberra

    Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Gaimari SD, Milonas P, Souliotis C (2007) Notes on the taxonomy, biology and distribution of Neoleucopis kartliana (Diptera: Chamaemyiidae). Folia Heyrovskyana Ser A 15(1):7–16

    Google Scholar 

  • García Morales M, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB (2016) ScaleNet: a literature-based model of scale insect biology and systematics. Database. https://doi.org/10.1093/database/bav118

    Article  PubMed  PubMed Central  Google Scholar 

  • Garonna AP, Viggiani G (2011) The establishment in Italy of Neoleucopis kartliana (Tanasjtshuk) (Diptera: Chamaemyiidae), predator of Marchalina hellenica (Gennadius) (Hemiptera: Margarodidae). XXIII Italian National Congress of Entomology Genoa, p 346 (in Italian)

  • Gounari S (2006) Studies on the phenology of Marchalina hellenica (gen.) (Hemiptera: Coccoidea, Margarodidae) in relation to honeydew flow. J Apic Res 45:8–12

    Article  Google Scholar 

  • Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJ (2016) Exotic biological control agents: a solution or contribution to arthropod invasions? Biol Invasions 18:953–969

    Article  Google Scholar 

  • Harvey JA, van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72(3):520–531

    Article  Google Scholar 

  • Hoddle MS, Ramirez CC, Hoddle CD, Loayza J, Lincango MP, van Driesche RG, Causton CE (2013) Post release evaluation of Rodolia cardinalis (Coleoptera: Coccinellidae) for control of Icerya purchasi (Hemiptera: Monophlebidae) in the Galapagos Islands. Biol Control 67:262–274

    Article  Google Scholar 

  • Hodgson C, Gounari S (2006) Morphology of Marchalina hellenica (Gennadius) (Hemiptera: Cocoidea: Marchalinidae) from Greece, with a discussion on the identity of M. caucasica Hadhjbeyli from the Caucasus. Zootaxa 1196:1–32

    Article  Google Scholar 

  • Jashenko RV (1999) Fauna, natural enemies, agricultural harm and possibility of industrial use of margarodids (Coccinea, Margarodidae) in East Europe and North Asia. Silevinia. pp 43–50

  • Kenis M, Hurley BP, Hajek AE, Cock MJ (2017) Classical biological control of insect pests of trees: facts and figures. Biol Invasions 19:3401–3417

    Article  Google Scholar 

  • Kohler GR, Stiefel VL, Wallin K, Ross DW (2008) Parasitoids reared from predators of hemlock woolly adelgid (Hemiptera: Adelgidae), and the hymenopterous parasitoid community on western hemlock in the Pacific Northwest. Environ Entomol 37:1477–1487

    Article  CAS  Google Scholar 

  • Lubanga U, Lefoe G, Weiss J, Kenis M, Avdzis D, Kwong R (2018) Feasibility of biological control of giant pine scale Marchalina hellenica (Gennadius) (Hemiptera: Marchalinidae) in Australia. Agriculture Victoria, Bundoora

    Google Scholar 

  • Martinez-Sañudo I, Mazzon L, Simonato M, Avtzis D, Pujade-Villar J, Faccoli M (2018) Tracking the origin and dispersal of the Asian chestnut gall wasp Dryocosmus kuriphilus Yasumatsu (Hymenoptera, Cynipidae) in Europe with molecular markers. Bull Entomol Res 109(3):300–308

    Article  Google Scholar 

  • Mendel Z, Assael F, Zeidan S, Zehavi A (1998) Classical biological control of Palaeococcus fuscipennis (Burmeister) (Homoptera: Margarodidae) in Israel. Biol Control 12:151–157

    Article  Google Scholar 

  • Mendel Z, Branco M, Battisti A (2016) Invasive sap-sucker insects in the mediterranean basin. In: Payne TD, Lieutier F (eds) Insects and diseases of mediterranean forest systems. Springer, pp 261–291

  • Mills NJ (1990) Biological control of forest aphid pests in Africa. Bull Entomol Res 80:31–36

    Article  Google Scholar 

  • Nicolopoulos CN (1965) Morphology and biology of the species Marchalina hellenica (Gennadius) (Hemiptera Margarodidae - Coelostomidiinae). École de Hautes Etudes Agron., Lab. Zool. Agr/Séri Athens, Athens

    Google Scholar 

  • Petrakis PV, Spanos K, Feest A (2011) Insect biodiversity reduction of pinewoods in southern Greece caused by the pine scale (Marchalina hellenica). For Syst 20:27–41

    Google Scholar 

  • Priore R, Marotta S, Sollino G (1996) The life cycle of Marchalina hellenica (Genadius) (Homoptera, Coccidae: Marchalinidae) on Pinus spp. in the island of Ischia. Boll Lab Entomol Agrar Filip Silv 52:35–41 (in Italian)

    Google Scholar 

  • Pujade-Villar J, Vanegas-Rico JM (2015) Descripción de una especie nueva de Melanips Walker (Hymenoptera: Figitidae), primer registro del género para la región neotropical. Acta Zool Mex 31:48–54

    Google Scholar 

  • Ravn HP, Havill NP, Akbulut S, Foottit RG, Serin M, Erdem M, Mutun S, Kenis M (2013) Dreyfusia nordmannianae in Northern and Central Europe: potential for biological control and comments on its taxonomy. J Appl Entomol 137:401–417

    Article  Google Scholar 

  • Tanasijtsiiuk VN (1986) [Silver-flies (Chamaemyiidae)]. Fauna of the USSR, new series 134. Dipterans, vol 14. Zoological Institute of the Russian Academy of Sciences, Nauka Publishers, St. Petersburg (in Russian)

    Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeankougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid Res 25:4876–4882

    Article  CAS  Google Scholar 

  • Thrasyvoulou A, Manikis I (1996) Some physicochemicals and microscopic characteristics of Greek unifloral honeys. Apidologie 26:441–452

    Article  Google Scholar 

  • Tsagkarakis AE, Emmanouel NG (2016) A note on the natural relocation of Marchalina hellenica (Gennadius) from pine to fir trees. Adv Entomol 4:163–166

    Article  Google Scholar 

  • Ülgentürk S, Szentkirályi F, Uygun N, Fent M, Gaimari SD, Civelek H, Ayhan B (2013) Predators of Marchalina hellenica (Hemiptera: Marchalinidae) on pine forests in Turkey. Phytoparasitica 41:529–537

    Article  Google Scholar 

  • Viggiani G, Mustica L (2008) Notizie sul controllo biologico di insetti dannosi nell'isola d'Ischia. Boll Lab Entomol Agrar Filip Silv 62:79–82

    Google Scholar 

  • Wingfield MJ, Slippers B, Roux J, Wingfield BA (2001) Worldwide movement of exotic forest fungi, especially in the tropics and the southern hemisphere. BioScience 51:134–140

    Article  Google Scholar 

  • Yeşil A, Gürkan B, Saraçoğlu Ö, Zengin H (2005) Effect of the pest Marchalina hellenica Gennadius (Homoptera, Margarodidae) on the growth parameters of Pinus brutia Ten. in Muğla Region (Turkey). Pol J Ecol 53:451–458

    Google Scholar 

Download references

Acknowledgements

This research was funded by Agriculture Victoria, the Australian Government and pine plantation growers represented by the Australian Forest Products Association through the Giant Pine Scale Emergency Response—Transition to Management program. The authors would like to thank the Forest Research Institute (Hellenic Agricultural Organization Demeter), Andrea Battisti (Universita di Padova), Glykeria Chronopoulou (Msc forester and GIS specialist), Paul Cunningham and Linda Semeraro (Agriculture Victoria) and industry stakeholders, for their valuable contributions and advice.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dimitrios N. Avtzis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Handling editor: Marta Montserrat.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1226 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Avtzis, D.N., Lubanga, U.K., Lefoe, G.K. et al. Prospects for classical biological control of Marchalina hellenica in Australia. BioControl 65, 413–423 (2020). https://doi.org/10.1007/s10526-020-10012-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-020-10012-3

Keywords

Navigation