Risks Posed by Exotic Forests Pests-Foliage Feeding Insects

Andrew Leibhold and György Csóka

Many of the world’s most notorious forest pests are foliage feeders that can be categorized into two principal groups: leaf-sucking insects and leaf-eating insects. The leaf-sucking insects are mainly in the order Hemiptera (aphids, adelgids, scales, mealy bugs, etc). The leaf-feeding forest insects are mainly represented by the Lepidoptera (moths and butterflies) and the Hymenoptera (sawflies); this group can be subdivided even further into external feeders and leaf miners, which are small insects that tunnel within the leaf tissue. While there are numerous examples in these groups that are native pest species, many foliage-feeding pests are exotic. There are obviously too many exotic defoliators to cover fully here, so we will illustrate a few selected species below.

Leaf-sucking insects
Within this group, there are many examples of forest pests that have caused considerable damage. Aphids are a large group and are illustrated by the green spruce aphid, Elatobium abietinum, which is native to continental Europe where it is not a major problem. It appears to have been introduced to the British Isles several hundred years ago, but more recently, it has become a major pest on exotic sitka spruce, which was widely planted there over the last 100 years. When populations become high, aphids feeding on needles can cause complete defoliation of trees over large areas. This feeding results in growth loss and ultimately tree mortality. It was accidentally introduced to Iceland from Denmark on cut Norway spruce Christmas trees in the 1950s and it also has had a devastating effect on sitka spruce plantations there. It was also accidentally introduced to New Zealand in the early 1900s and damage was so extensive that spruce is no longer planted there. It has been recognized as a pest in northwestern North America for many years and was originally thought to be native. Recent evidence, however, indicates that it is exotic there also. Lately it has expanded its range in North America into the southern Rocky Mountains where it has caused extensive defoliation of Engleman spruce. The observation that this insect has spread to so many portions of the globe indicates the ease with which it is transported on either live or recently cut plant material.

Figure 1a. Spruce aphids, adult (photo USDA Forest Service).	Figure 1b. Severe foliar browning caused by spruce aphid (photo Canadian Forest Service).
Figure 2a. Hemlock woolly adelgid egg masses produced by overwintering adults (photo USDA Forest Service).	Figure 2b. North American hemlock stand heavily damaged by hemlock woolly adelgid (photo USDA Forest Service).

Adelgids are sucking insects closely related to aphids and despite their small size, there are several examples of exotic adelgids that cause considerable damage. Effects of adelgid feeding are similar to that of aphids. The hemlock woolly adelgid, Adelges tsugae, is native to localized regions of Japan and China, but outbreaks are rare in these areas. The mode by which this insect came to North America is not clear, but it was discovered in 1924 in British Columbia and in 1955 in Virginia. There is some evidence of host resistance in western hemlocks, but outbreaks of this insect are common through much of the native range of eastern hemlock where this insect has been established. There are no parasitoid species associated with this species, and this has greatly limited the ability to use biological control to reduce its impacts.

Mealybugs are another major group of foliage-sucking insects. In China, the pine-feeding mealybug, Oracella acuta, was accidentally introduced from North America on live seedlings in 1988 and has subsequently rapidly expanded its range and caused considerable defoliation and tree mortality in hundreds of thousands of hectares of exotic slash pine plantations. Work currently underway to introduce parasitoids of this species holds some promise of reducing its impact.

Leaf-feeding insects
There are numerous examples of exotic external leaf-eating forest insects. In North America probably the most widely studied forest insect pest is the gypsy moth, Lymantria dispar. This species is native to most of Europe and Asia and was accidentally introduced to North America in the late 1860s by an amateur entomologist from France, E. Leopold Trouvelot. In European populations of this insect, females are incapable of flight, so they have limited dispersal capabilities. However, females prefer to lay their eggs in cryptic locations, and therefore, egg masses may often be found on a variety of man-made objects, such as automobiles, camping equipment, and shipping containers. While the lack of flight in females has resulted in a very gradual rate of range expansion in North America, the association of egg masses with man-made objects has resulted in numerous cases of accidental introduction of new populations in unifested areas. While several gypsy moth predator and parasitoid species have been successfully introduced from Europe and Asia, outbreaks of this insect are still common and intense. Repeated episodes of defoliation may ultimately result in growth loss and tree mortality, but the gypsy moth’s greatest impacts are on the aesthetic value of trees growing in residential areas. Outbreaks are also common through much of the gypsy moth’s native range, and this may explain the lack of complete success in the use of biological control to reduce gypsy moth impacts.

Figure 3a. Gypsy moth larval stages (photo USDA Forest Service).	Figure 3b. Gypsy moth larvae emerging from egg mass (photo USDA Forest Service).

An example of a species transported in the opposite direction (from North America to Europe) is the fall webworm (Hyphantria cunea). It was first recorded in Europe in 1940 in the port of Csepel (Budapest), Hungary, near the River Danube. It was probably accidentally transported during the shipping process, but the identity of the infested commodity and the associated developmental phase remain unknown. During the following six decades it spread to many countries in Central and Eastern Europe. The species is extremely polyphagous and causes damage to many shrub and tree species, including fruit and forest trees. As is the case with most defoliators, feeding diminishes host resistance to secondary agents, which may ultimately lead to tree mortality. In Central Europe it produces two generations a year and overwinters as a pupa. Since both males and females are relatively good fliers, adult dispersal can, at least partially, explain the expansion of its range through Europe.

Figure 4a. Larva of the introduced pine sawfly (photo USDA Forest Service).	Figure 4b. Defoliation caused by the introduced pine sawfly (photo USDA Forest Service).

The introduced pine sawfly, Diprion similis, is an example of a foliage-feeding exotic hymenopteran. This species was introduced to North America from Europe in the early 1900s probably in the cocoon stage on nursery stock from Holland. It has expanded its range through most of eastern North America, and during outbreaks, it can defoliate many different species of pines, both native and exotic. These outbreaks can occur in natural forests but are most problematic in plantations and Christmas trees, on which cosmetic damage is unacceptable. Several parasitoid species were introduced from Europe, and they seem to contribute to natural control, but they have not totally eliminated outbreaks. In Europe, natural control appears to be more effective, as outbreaks are relatively uncommon.

The habit of leaf-mining is a common life history in several insect orders, but most common among Lepidoptera, Diptera (flies), and Hymenoptera. The leaf-mining insects are generally much more host-specific than most of the free living leaf feeders. Therefore, their establishment and spread in new regions is strongly determined by the presence of their original host plant or closely related tree species. A good example is provided by black locust (Robinia pseudoacacia) and its two monophagous leaf-mining moths, Parectopa robiniella and Phyllonorycter robiniella. Black locust is native to North America and was introduced to Europe in the early 17th century as an ornamental tree and two centuries later became an important tree in forest plantations in France, Italy, Hungary, Rumania, Moldavia, and Ukraine.

Figure 5. Leaf mine of Phyllonoryter robiniella (photo by G. Csóka).	Figure 6. Leaf mine of Parectopa robiniella (photo by G. Csóka).

Two leaf miners feeding on black locust were recently discovered in Europe and have caused extensive damage. Parectopa was first found in Italy in 1970, and Phyllonoryter was found in Switzerland in 1983. The rate of spread for both species is strongly related to the regional abundance of their host plant. Both species spread (and are still spreading) slowly in parts of Europe where their host trees are not abundant. But in Hungary, where black locust is one of the most common tree species (more than 20% of the total forested area is covered by it), the rate of spread accelerated considerably, reaching at least 100 km/year in the case of Phyllonoryter robiniella. Due to the recent appearance of these species, there is not much information on their impact; early leaf drop may occur during outbreaks, and this likely affects tree growth and resistance to secondary agents. The precise identity of the developmental phase that first arrived in Europe is still unknown. Grafts and seedlings carried from North America to Europe for plant- breeding purpose were probably transferred without leaves and, therefore are unlikely carriers of the leaf miners. A more likely but unproven mechanism for the introduction could have been seed trade. Locust seeds remain intact on the ground for a long time and can be collected easily in bulk. Seeds collected along with some soil fragments could easily become contaminated by the tiny pupae of both species. The spread of these two species within Europe has probably been facilitated by the windborne dispersal of the tiny moths.

Figure 7. Horse chestnuts in Hungary heavily infested by Cameraria  ohridella (photo by G. Csóka).	Figure 8. Adults of Cameraria ohridella (photo by G. Csóka).

Another recent example of invasion of a host-specific leaf miner is the case of Cameraria ohridella, a leaf-mining moth on horse chestnut (Aesculus hippocastaneum). It was discovered as an undescribed species in 1986 from a collection near Lake Ohrid, Macedonia (very close to the Albanian border), but its origin is still unknown. The most likely explanation is that Chinese settlers accidentally introduced it to Albania. There are several species of Aesculus both in Asia and North America. This leaf miner was deliberately carried to Linz, Austria, by an amateur entomologist. The species escaped and started to spread in many directions making impressive progress within a decade. Spread appears to be facilitated both by passive windborne flight and by accidental movement on vehicles. Its spread appears to be enhanced by the abundance of horse chestnut, which is a very popular ornamental tree throughout Europe. Defoliated trees are unsightly, but there are no reports to date of this insect causing extensive mortality. However, leaf-miner feeding does appear to increase the vulnerability of trees to the leaf fungus, Guignardia aesculi.

Conclusions
In summary, foliage-feeding forest insects represent a diverse group of which there are many example of species introductions that have had devastating effects. In most cases the risk of transporting feeding life stages may be low, but many of these species have resting stages that may be easily transported accidentally. This risk seems particularly great for transportation of live or recently cut plant material. While lack of suitable hosts may represent a significant barrier to establishment of certain species, many other defoliators have fairly broad host ranges, and there are many cases where introduced populations are more problematic than are populations of the same species in their native habitat.