Ophelimus maskelli

Introduction

Ophelimus maskelli Ashmead (Hymenoptera: Eulophidae), commonly known as the Eucalyptus gall wasp, is a serious gall-inducing pest of Eucalyptus. Native to New South Wales, Australia, O. maskelli has spread and established itself in Europe, the Mediterranean, Middle East, Africa and has recently been recorded in North America (2014). Originally described as Pteroptrix maskelli in 1900, the gall wasp was reclassified in 1988 as part of the revision of Australasian Chalcidoidae by Boucek (1988).

Oviposition by O. maskelli  induces single-blister like galls on the surface of leaves, holding a single egg. High gall density can lead to severe leaf damage, early leaf drop and in extreme cases complete defoliation of the tree. As with the movement of other Eucalyptus pests, O. maskelli has spread without the presence of any principal parasitoids or other natural enemies that occur naturally in Australia, leaving Eucalyptus spp. open to injury. Ophelimus maskelli is causing extensive damage in Eucalyptus plantations, particularly on E. camaldulensis across the Mediterranean and Middle East.

Description
Adults:

Adults are black bodied and approximately 1 mm in length.The most distinct characteristic of O. maskelli is the presence of a single seta on the submarginal vein of the forewing.

Male O. maskeli

Ophelimus maskelli adult. Image Protasov et al. 2007

Galls:

Oviposition into the leaf epidermis induces a blister like gall that is round and uniform in size and shape (gall diameter 0.9 – 1.2 mm). Gall density can range from 11.5 – 36 galls/cm². Ophelimus maskelli develop in the single-cell galls on the leaf surface. Gall colouring appears as soon as the third instar larva develop (see table below).

O. maskelli galls

O. maskelli galls on Eucalyptus leaves. Image G. Dessi 2008, Agriculture and Environment Vocational Institute “Cettolini”, Villacidro.

Typically, galls exposed to sunlight are a bruised-red colour, whilst those in shaded areas can be a greenish-yellow colour.

gall

Red and green galls. Image D. Mifsud 2012

Biology:

The understanding of the biology and ecology for O. maskelli is still limited in Australia and in many of the newly established countries. Much of the biological data for O. maskelli comes from research from Israel, site of the original introduction.

Females lay on average 109 eggs on both the upper and lower sides of the leaf, however gall density is generally higher on the ventral side. Each oviposition puncture induces a gall, in which a single wasp develops. The females prefer to oviposit on an area of the leaf blade near the petiole, on large, immature green coloured leaves in the lower canopy of the tree. The optimum time for wasp development appears to be on leaves 30 to 40 days old, but can take place from 15 to 90 days after bud break. Development of the pre-imaginal stages within the galls requires 110 ± 19 d at 18 – 25°C after which the adults emerge. Studies have shown that the wasp has three generations per year in Israel. The first generation is in spring, followed by the second in summer and a third through autumn. Larvae overwinter in galls.

There are five wasp development phases that coincide with gall development, consisting of three larval instars, a non-feeding pupal stage and adult (see table below). The adult emerges by cutting a circular hole in the gall wall close to the plane of the leaf. In Israel, heavily galled leaves survived for approximately 70 days, whilst those free of galls had a longevity of around 243 days.

Table 1. Five stages of wasp and gall development

               Gall
       development
     Wasp
development
 Development      period     Total days
Stage one: From oviposition, gall visibly develops on the leaf surface  1st larval instar    30 – 35 days   30
Stage two: Galls develops typical colour (green-yellow or red-purple hue)  2nd larval instar    15 – 25 days   60
Stage three: Gall reaches maximum size First stage of 3rd larval instar    16 – 27 days    87
Stage four: Larva reaches maximum size, pupates, filling entire  gall chamber Pupa    20 – 26 days    113
Stage five:   Adult    10 – 16 days   129

Protasov et al. 2007

Distribution

Ophelimus maskelli has established itself as an invasive species across Europe, Asia, the Middle East, Mediterranean, Africa and North America. The probable cause of introduction into the Euro-Mediterranean areas, and the subsequent movement across the globe, is through trade of its host (Eucalyptus sp.). It is highly likely that O. maskelli will establish itself in new parts of the world via this method.

Host trees

The most susceptible species to O. maskelli attack are Eucalyptus camaldulensis and E. tereticornis (= umbellate Smith). Host testing of 84 eucalyptus species, determined that 14 were suitable hosts for O. maskelli. Tests revealed that those belonging to the Exsertaria section of the genus are at greater risk of injury from O. maskelli than those in the Latoangulata and Maidenaria sections. Susceptible species include:

  • E. botryoides
  • E. bridgesiana
  • E. camaldulensis
  • E. cinerea
  • E. globulus
  • E. grandis
  • E. gunii
  • E. nicholii
  • E. pulverulenta
  • E. robusta
  • E. rudis
  • E. saligna
  • E. tereticornis
  • E. viminalis

Ophelimus maskelli poses a significant threat to hardwood production in the Mediterranean regions and the Middle East where E. camaldulensis is one of the most economically important trees grown in forestry plantations.

Damage & symptoms

As with other successful eucalyptus pest invaders, O. maskelli has moved unaccompanied by its principal natural enemies. Populations were free from pressure by naturally occurring predators and parasitoids in the newly-established locations that are commonly associated with the gall wasp in Australia. In favourable conditions O. maskelli populations can reach epidemic levels. The entire leaf surface can be covered in small blister like galls ranging from a red-bruised colour to a yellow-green hue. Leaves bearing greater than 50 galls live considerable less in comparison to those without galls.

Heavy galling in Eucalyptus trees causes serious injury in the form of premature leaf drop, occurring soon after wasp emergence. Heavily injured trees are revealed by the desiccation of large parts of their crown and canopy, as a result of leaf shedding. Continual attack by O. maskelli can cause the death of young and newly planted trees. In a severe case from Israel, 80 year old E. camaldulensis trees shed their foliage to near complete defoliation. As a result, E. camaldulensis planting ceased for a period in Israel. There have also been instances where mass emergence of O. maskelli in spring have reached such high densities that ‘clouds’ of wasps cause nuisance to human activities.

Monitoring

The exact distribution of O. maskelli across a range of countries, particularly in countries where the wasps is recently established, is limited. That new recordings have recently been confirmed from North America and South Africa indicates that O. maskelli is continuing to spread. What is unclear is the limit of the Eucalyptus gall wasps establishment potential. Green sticky traps are an effective and affordable way to monitor for the presence and movement of O. maskelli and parasitoids, and the rate and distribution of spread can be measured through annual surveys.

Chemical control

Chemical control of O. maskelli is still limited. In young and small trees, application of  systemic neonicotinoids such as thiacloprid and acetamiprid have proven to provide some protection against attack. In the nursery, application of Kaolin to young trees has provided some protection against O. maskelli attack. Kaolin, (Al2Si2O5 (OH)4), is a white porous, non-swelling, non-abrasive clay product that when applied, causes the treated surface to become hard, making it less suitable for oviposition. The white particle film hides the colour of the leaf, reducing host recognition without an interference to photosynthesis or stomatal conductance.

Biological control

Ophelimus maskelli populations were free from parasitoid pressure In newly established areas of the Mediterranean and the Middle East O. maskelli popultions were free from parasitoid pressure, with no observation’s of attack from native species either.  In 2003 the Volcani Center of Bet Dagan (Israel) and CSIRO (Australia) initiated a biological control program to search for natural enemies of O. maskelli in Australia for possible introduction into Israel. Three parasitic wasps were found Closterocerus chamaeleon (Girault) (Hymenoptera: Eulophidae: Enedontinae), Stethynium ophelimi (Huber) and S. breviovipositer (Huber) (Mymaridae).

Approximately 12,000 C. chamaeleon adults were released in Israel from 2005 to 2006, which lowered O. maskelli population densities within one year of release.  It has demonstrated its extreme mobility by occupying areas 120km away from its original release location one year later. Closterocerus chamaeleon is most active during the winter months when O. maskelli development has slowed. Stethynium ophelimi was reared and released in conjunction with C. chamaeleon, however subsequent surveys post release failed to recover large numbers of the parasitoid. Closterocerus chamaeleon has been released in Israel and Italy, and has been detected in Algeria, Spain, Turkey, Portugal, Tunisia and South Africa.