Pests Associated with Seeds, Propagative Materials and Nursery Stocks

Alain Roques

Worldwide exchange and trade of tree reproductive materials is rapidly increasing with the development of plantations and ornamentals using exotic tree species. Such exchanges are highly favorable to the invasion of new pests because no or few phytosanitary regulations exist for importation of such material in a number of countries. Several categories of organisms are concerned, especially insects, mites, and fungi developing within or on seeds because seeds are preferred to cones and fruits for trade of conifers and of most broadleaved tree species.

Seedborne insects and mites
Only the species spending their entire development (egg to pupa) as endophytes within seeds (known as spermatophages) constitute a real invasive threat. Species with lifecycles partly affecting seeds usually drop to the ground as mature larvae prior to seed harvesting. However, early seed collection may prevent larval drop down (essentially in seed midges), and such larvae can then be found within seed lots. Problems in cleaning seeds after harvest may also result in additional invaders, e.g., species pupating within cones, where the cocoons remain attached to the seeds. The Port-Orford cedar seed midge, Janetiella siskyiou, has probably been introduced in that way from North America to Europe.

In conifers, spermatophages represent 62 of the 400 species presently known to attack cones in the world, and nearly 80% of the conifer species host at least one spermatophage. The dominant group is the seed chalcid wasps in the genus Megastigmus (Torymidae- 52 species), to which can be added a few other chalcids of the genus Eurytoma (Eurytomidae- 2 species), seed midges (Cecidomyiidae - genera Plemeliella and Mayetiola- 3 species), and several mites in the genus Trisetacus (Nalepellidae), especially in junipers and cypresses. Seeds of broadleaved trees are infested by the same genera plus several other Torymid chalcids (Bootanellus, Bootania, Torymus) and seed beetles (Bruchidae), especially in Leguminosae. Nearly all of these organisms are associated with particular host genera, i.e., they develop in seed species of a same genus.

Figure 1. Lifecycle of the Douglas-fir seed chalcid, Megastigmus spermotrophus (adapted from Hedlin et al., 1980). Click image for an enlarged view.	Figure 2. Radiograph of Douglas-fir seeds attacked by M. spermotrophus

The lifecycle of all seed chalcids is roughly similar to that of the Douglas fir seed chalcid, Megastigmus spermotrophus (Fig. 1). The female uses its long ovipositor to lay an egg directly into the seed where, after feeding, the mature larva overwinters. The larva cannot be detected by examining the outside of the seeds at harvesting but show up in X-rays (Fig. 2). Thus, the absence of an X-ray survey of seed lots is likely to result in the importation of infested seeds. Three additional biological characteristics allow chalcids to cope with hazards during the process of transferring to new host trees: 1) the capability of extending larval diapause in seeds for up to 4 years in most species, allowing them to escape periods of null seed crop; 2) parthenogenesis, in which the females can reproduce without males; 3) the capability of developing in unfertilized seeds shown in some species, allowing them to escape lack of pollination. As a result, a recent survey of Megastigmus spp. in the West Palearctic showed that about 40% (8/21) of the recorded species were introduced through seed trade. In mites, the lifecycle is synchronized to that of seeds, and the various life stages are present within seeds from initiation to dispersal.

The development of invasion by seed chalcids largely depends on the presence of native trees in the same genera as the original host. When such genera are absent, the introduced chalcid cannot develop except when the original host is introduced simultaneously on a large scale. In that case, the chalcid tends to entirely occupy the seed niche because of the absence of native and introduced competitors as well as that of parasitoids. Therefore, damage to the seed crop is much more important than in native areas, examples being given by M. spermotrophus introduced to Europe and New Zealand (Fig. 3) and the Casuarina seed chalcid, Bootanelleus orientalis, introduced to North America. When suitable tree genera exist in the introduction area, the chalcid usually shifts to these (Fig. 4), although it is not yet known whether such shifts arose from genetically differentiated populations or from the species plasticity. Competition with native cone insects, however, limits the species impact in most cases. The relative length of ovipositor with regard to the cone size may also limit the host range.

Figure 3. Comparison of seed damage by M. spermotrophus in the native range (North America) and the introduction range (Europe). Click image for an enlarged view.	Figure 4. Seed damage by native and introduced species of seed chalcids, Megastigmus spp., on European and Asian firs planted in a French arboretum (1994). Click image for an enlarged view.

Unlike cones, nuts are used for trade of nut-bearing trees such as oaks (acorns), hazels, chestnuts, walnuts, pecans, hickory, and tanoak. Such nuts are normally hosts to weevils in the genera Curculio and Conotrachelus; Tortricidae (moths) in the genus Cydia; and Cynipidae wasps (Eumayria spp., Callirithys glandium.). With the exception of the Cynipidae, most of these species vacate the nuts as mature larvae to pupate into the ground during the autumn, but some remain in nuts as late as December. Thus, nut harvesting may occur before larval drop, and larvae are often observed in collection bags. As was the case for conifer spermatophages, the invasive patterns of these species depend on the presence of the same tree genera as the original host.

Figure 5. Disease cycle for the cold fungus, Caloscypha fulgens (from Sutherland et al., 1987). Click image for an enlarged view.

Seedborne pathogens
A variety of fungi, some being pathogenic, are associated with the seeds of forest trees. Several grow in forest litter and invade seeds when cones fall down on infested soil and contact mycelium, as is the case for the cold fungus, Caloscypha fulgens, which causes abnormal preemergence losses in conifer nurseries and has been introduced to the U.K. via infested conifer seeds from North America (Fig. 5). Ground-collected cones, especially from squirrel caches, most often contain diseased seeds, whereas the fungus should not be present in seed lots from cones picked directly from trees. The pathogen spreads among seeds during cold periods such as stratification, poststratification storage, or in cold seedbeds or containers. A similar process is involved in the development of the Sirococcus blight, as a result of Sirococcus strobilinus, which affects numerous conifer species in nurseries. Seeds become infected when the pathogen invades old cones, and cross contamination occurs when these are inadvertently included in cone collections. Secondary spread occurs via pycnidiospores produced on diseased tissues and disseminated in rain and irrigation water. Some other seed pathogens are either air- or rainborne (Fusarium, Diplodia) or disseminated by insects (Seiridium cardinale, Pestalotia). Like seed insects, seedborne fungi cannot be detected by examining the outside of the seeds, with some exceptions such as molds.

Potential pest invaders associated with other reproductive materials
Potential pests in this category are much more numerous and it is not possible to consider all types in this paper. In contrast to a number of seedborne pests, most others are nonspecialized organisms. Soilborne pests include insects whose egg, larval, or pupal stages are likely to occur in soil of nursery containers. Several species of root weevils (Curculionidae) such as the black vine weevil (Otiorhynchus sulcatus) and the strawberry root weevil (O. ovatus) have probably been introduced in that way to North America. Adults of these species, both parthenogenetic, flightless, nocturnal, and polyphagous, feed on foliage and lay eggs on the ground, after which larvae develop in the soil through the summer and following spring, feeding first on rootlets and then on large roots. Finally they pupate in cells down to 15 to 20 centimeters below the soil surface. Often, the injury is not apparent until the plant is transplanted. A similar lifecycle, with a few variants, has been noticed for other root weevils introduced to the United States (Brachyderes incanus; Arborvitae Japanese weevil, Phyllobius intrusus; white fringed beetles, Graphognathus spp.; two-banded Japanese weevil, Callirhopalus bifasciatus [in this case by eggs on leaf]; and Asiatic oak weevil, Cyrtepistomus castaneus). This route of transfer may also apply to May and June beetles (white grubs-Scarabaeidae) and to cutworms (moths-Noctuidae), allowing species to overwinter as larvae or eggs in the soil. Springtails (Collembolla) affecting seedlings also overwinter as eggs in soil containers. By contrast, bareroot seedlings host fewer and usually more visible potential insect invaders, e.g., giant conifer aphids (Cinara spp.), gall aphids (Adelges spp.), and also spider mites (Acarina; e.g., the spruce spider mite, Oligonychus ununguis). In the latter species, overwintering occurs in the egg stage under loose bud scales and bases of needles.

Bareroot and container seedlings are also affected by damping-off fungi (Fusarium, Pythium, Rhizoctonia, Phytophthora, Cylindrocladium). Most are unspecialized, soilborne pathogens with similar life histories, and are capable of surviving environmental extremes by developing resistant dormant spores in the soil in small root pieces or in dead organic matter rather than on seeds and seedlings. When seedling roots grow near these spores, germination occurs and the pathogen enters the root. The principal environmental factors influencing disease development are soil pH, moisture, and temperature but the effects vary with both the pathogen and host species. Plant-parasitic nematodes also have to be surveyed in soil of nursery containers and on bareroot seedlings.

Suggested readings:

Cordell C.E., Anderson R.L., Hoffard W.H., Landis T.D., Smith R.S. Jr., Toko H.V., 1989. Forest Nursery Pests. USDA Forest Service, Agriculture Handbook No. 680, 184 pp.

Hedlin, A. F., Yates, H.O. III, Cibrian-Tovar, D., Ebel, B.H., Koerber, T. W. and Merkel, E.P., 1980. Cone and seed insects of North American conifers. Ottawa: Environment Canada/Canadian Forestry Service, Washington D.C.: US Forest Service, México: Secretaría de Agricultura y Recursos Hidráulicos), 122 pp.

Sutherland J.R., Miller T., Quinard R.S., 1987. Cone and seed diseases of North American Conifers. North American Forestry Commission, Victoria B.C., Canada, 77 pp.

Turgeon J., Roques A. , De Groot P., 1994. Insect fauna of coniferous seed cones: Diversity, host plant interactions, impact and management. Annu. Rev. of Entomol. 175-208.