First record of the red gum lerp psyllid, Glycaspisbrimblecombei Moore (Hemiptera Psyllidae), in Tunisia

Sarra Ben Attia & Carmelo Rapisarda

Received: 18 September 2013 /Accepted: 3 February 2014# Springer Science+Business Media Dordrecht 2014

Abstract During a survey carried out in August 2013along all coastal areas of north-eastern Tunisia (governor-ships of Bizerte, Ariana, Tunis, Ben Arous, Nabeul,Sousse), eucalyptus treeswere found to be highly infestedby the invasive pest Glycaspis brimblecombei Moore,1964, also known as red gum lerp psyllid. This insect,native to the Australian region and secondarily dispersedalso in the Americas, Mauritius, Madagascar and SouthAfrica, very recently started to invade theMediterraneanregion and in almost 5 years has spread to the IberianPeninsula, Italy, Greece and Morocco. Its presence inTunisia (which is recorded here for the first time) mostprobably dates back to summer 2012, since typicalnecrotic spots caused by the lerp of the psyllid hadalready been noted on leaves during spring 2013. Nopresence of its main parasitoid – Psyllaephagus bliteusRiek – nor of any other natural enemy, was noted up tonow during our survey in Tunisia.

Keywords Eucalyptus trees . Invasive pest . Jumpingplant-lice . New record . North Africa

Introduction

The Mediterranean Basin is considered one of the mainhotspots for biodiversity, climatic changes and, as aconsequence, for biological invasions of alien organisms(Ponti et al. 2013). Extremely important plant pests havebeen introduced and spread rapidly in this area duringthe last decade and are causing much damage to agricul-tural, forest and ornamental plants. The Asiatic red palmweevil, Rhynchophorus ferrugineus (Olivier), and theSouth-American tomato leafminer, Tuta absoluta(Meyrick), both of them first recorded in Spain butinvasive to the entire Mediterranean region (and farther)in less than 5 years, are the most outstanding examples(Suma et al. 2013; Tropea Garzia et al. 2012).

With almost the same pest severity and invasiondynamics, the red gum lerp psyllid, Glycaspisbrimblecombei Moore, 1964, recently started to invadethe Mediterranean Basin, severely infesting plants ofthe genus Eucalyptus (Myrtaceae). Already widelydispersed in the Iberian Peninsula and Italy and foundalso in Morocco and Greece, this insect is recorded herefor the first time from Tunisia, showing an evidentspreading from West to East through the Mediterraneanregion and North Africa, as already predicted by deQueiroz et al. (2013).

Brief notes on the species

Identification Adults of G. brimblecombei are ~3 mmlong, light green-colored on the head, mesothorax andabdomen, with the rest of the body having alternating

PhytoparasiticaDOI 10.1007/s12600-014-0391-8

S. Ben Attia :C. Rapisarda (*)Department of Agri-food and Environmental SystemsManagement (Dipartimento di Gestione dei SistemiAgro-alimentari e Ambientali – DiGeSA), AppliedEntomology Section, University of Catania,Via Santa Sofia n. 100, 95123 Catania, Italye-mail: rapicar@unict.it

S. Ben Attiae-mail: benattia.sarra@yahoo.fr

light yellow and orange bands. Slide-mounted materialfor microscope observation is essential for their positiveidentification, with good diagnostic characters beingfound especially in the dorsal shape of the genal conesand the lateral profile of the male parameres (Burckhardtet al. 2008). Nymphs are yellow-orange to orange-brown, with dark brown wing pads bearing powdery,white waxy production, in the shape of small dots. Theyalso produce a protective dorsal white follicle over theirbody, the so-called ‘lerp’, sub-conical in shape andconsisting of a mixture of wax and crystallized honey-dew, reaching 2.5–3 mm in diameter and height in thefinal instar nymph. On infested Eucalyptus leaves, thewhite lerp follicles can be easily detected, showing thepresence of the psyllid (Fig. 1).

Geographical distribution Like its host plants,G. brimblecombei is native to the Australian regionand has remained strictly limited to this area until a littlemore than a decade ago, when it became an invasivespecies spreading to many countries on different conti-nents. Outside of its native region, it has been reportedfrom the USA (California, Florida, Hawaiian Islands)(Brennan et al. 1999; Nagamine & Heu 2001), Mexico(Castillo 2003) and several countries in South America:Argentina (Bouvet et al. 2005), Brazil (Santana et al.2003), Chile (Sandoval & Rothmann 2002), Colombia(Tayloret al. 2013), Ecuador (Onore&Gara 2007), Peru(Burckhardt et al. 2008) and Venezuela (Rosales et al.

2008). There are almost contemporary records regardingMauritius (Sookar et al. 2003) and Madagascar (DavidOuvrard, pers.comm.). Invasion of Europe started a bitlater, with the red gum lerp psyllid being reported fromthe Iberian Peninsula (Hurtado & Reina 2008; Valente& Hodkinson 2009), Italy (Laudonia & Garonna 2010),France (Cocquempot et al. 2012) and recently Greece(Bella & Rapisarda 2013). In Africa, the psyllid hasbeen recorded recently from Morocco (Bami 2011;Maatouf & Lumaret 2012) and South Africa (Tayloret al. 2013); it is new to Tunisia.

Bio-ecology Glycaspis brimblecombei lives exclusivelyon species and hybrids of the genus Eucalyptus(Brennan et al, 1999, 2001; Paine et al. 2006), whichare infested by the insect with different degrees ofseverity due to a variable susceptibility to the attacksby the pest. In Mediterranean environments, reproduc-tive activity is shown by this psyllid during summer,with two or three generations (Garonna et al. 2011); upto four annual generations are reported from the nativeAustralian region (Moore 1970). The female laysorange-yellow eggs, usually fixed to the underside ofthe leaf and arranged to form an arc. Egg hatchinggenerally occurs 7–10 days after oviposition andpostembryonic development goes through five nymphalstages.

Findings in Tunisia

In April 2013, rare but typical necrotic spots caused onEucalyptus leaves by the lerp of G. brimblecombei werenoted in Port El Kantaoui and in Sousse, clearly indicat-ing the presence of the psyllid since the previous summerof 2012, although at very low density. Subsequently, asurvey carried out duringAugust 2013 enabled us to noteserious infestations by the red gum lerp psyllid in manycoastal areas of north-eastern Tunisia, in the governor-ships of Ariana, Ben Arous, Bizerte, Nabeul, Sousse andTunis. A complete list of the localities in which it wasfound is given in Table 1 and reported also in Figure 2.G. brimblecombei has been found in Tunisia over a widearea between 37°15'N and 35°50'N latitude, and between9°54'E and 11°3'E longitude.

The large number of sites where the psyllid has beensought and the fact that no Eucalyptus plants inspectedduring the survey were free of its presence indicate howG. brimblecombei is probably widespread throughout

Fig. 1 Typical lerps of Glycaspis brimblecombei Moore oneucalyptus leaves

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Tunisia. Similar rapidity in spreading all over a newlyinvaded region in just a few months has been shownby the red gum lerp psyllid in Sicily (Italy) during 2011(Lo Verde et al. 2011).

In all Tunisian sites where G. brimblecombei hasbeen detected, the infested plants of Eucalyptus(especially E. camaldulensis Dehnh.) were heavilyattacked, with contemporary presence of all develop-mental stages of the insect.

Pest importance and control possibilities

The red gum lerp psyllid lives exclusively on leaves,which are covered with significant amounts of honey-dew and consequent further development of sooty mold,covering the entire canopy. From the first field observa-tions carried out in Tunisia, infested plants do not seemto show major deteriorations or weakening; however,according to previous experience in arid regions of theU.S.A., the actual harmfulness of this species must beassessed over a 2–4-year period (Daane et al. 2005; Gill1998). In countries where the pest has occurred for alonger time, severe leaf drop and twig dieback are report-ed; death of trees are reported from South America(de Queiroz et al. 2012).

As with other exotic invasive pests, short-term strat-egies to control G. brimblecombei infestations may bebased on chemical control. In any case, to achieve a

Table 1 Sampling sites of the red gum lerp psyllid Glycaspisbrimblecombei in Tunisia (year 2013)

Locality Latitude Longitude

1. Bizerte 37°15'25.21"N 9°54'4.67"E

2. Aousja 37°9'19.09"N 10°7'5.05"E

3. Zouaouine 37°7'50.19"N 10°4'41.58"E

4. Zana 37°3'35.38"N 10°1'5.63"E

5. Pont de Bizerte 37°0'17.68"N 10°3'15.39"E

6. Sidi Thabet 36°56'45.93"N 10°5'15.13"E

7. Ariana 36°53'27.91"N 10°7'0.91"E

8. Gammarth 36°55'13.90"N 10°17'9.50"E

9. Mornag 36°41'23.07"N 10°18'22.77"E

10. Kélibia 36°49'46.03"N 11°3'22.62"E

11. Korba 36°34'41.24"N 10°51'11.27"E

12. Hammamet 1 36°25'23.41"N 10°35'39.90"E

13. Hammamet 2 36°25'2.55"N 10°33'53.79"E

14. Kantaoui 35°53'47.47"N 10°35'19.52"E

15. Sousse 35°50'45.92"N 10°37'21.69"E

Fig. 2 Collecting sites of Glycaspis brimblecombei Moore in Tunisia during 2013

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long-term and large-scale control it is essential to re-establish the balance between the pest and its naturalenemies. In order to do so it is important to perform athorough monitoring of the pest dispersal, of the inten-sity of its attacks and of the indigenous natural enemiesadapting to the invasive species in the newly invadedregion, as it has been done with other exotic pestsspreading over the Mediterranean Basin (Zappalà et al.2013). Native generalist natural enemies occurring inrecently colonized areas do not ensure adequate controleven when present in large numbers (Caleca et al. 2011;Dahlsten et al. 2005; Garonna et al. 2011; Valente &Hodkinson 2009). Thus there is extreme importance totry to introduce efficient natural enemies from the nativearea of the psyllid. In California, a classical biologicalcontrol program of the red gum lerp psyllid has beenrealized through the introduction of its koinobiont endo-parasitoid Psyllaephagus bliteus Riek (HymenopteraEncyrtidae) from South Australia and its subsequentreleases in newly colonized areas by the psyllid(Dahlsten et al. 2005; Paine et al. 2000). Both inCalifornia and in other countries (such as Chile andMexico), where it was artificially introduced later,P. bliteus proved to be an efficient bio-control agent,halving the population of the red gum lerp psyllid in lessthan one year, under appropriate climatic conditions.

Psyllaephagus bliteus has been found on Glycaspisspp. in New Zealand (Withers 2001), Brazil (Berti-Filhoet al. 2003), Spain (Perez-Otero et al. 2011), Italy andMorocco (Caleca et al. 2011), Greece (Bella & Rapisarda2013) without any previous artificial release. No presenceof this parasitoid has been noted in Tunisia in our survey,but a more thorough investigation is needed to ascertainthis aspect.

Acknowledgment The research was supported by the project“Insects and globalization: sustainable control of exotic species inagro-forestry ecosystems (GEISCA)”, financed by the ItalianMin-istry for Education, University and Research (PRIN 2010/2011project 2010CXXHJE_004).

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