Introduction

Pathways used by pests

Pest dispersal occurs through both natural and anthropogenic processes, strongly facilitated during the past decades by the globalization of markets for plants and plant products including food, planting material and wood. Global travel and the trade of agricultural products have moved crops, weeds, pathogens, and insect pests away from their native environments to new ones. Newly introduced crops may expand pest distribution, and the introduction of new pests into a completely new ecosystem may cause extremely serious damage because pests and hosts may not have coevolved together. This coevolution has been especially recognized for plants and their pests (Woolhouse et al., 2002) and has created a stable balance between hosts and pests within their endemic ecosystems. As an example, pine wilt nematode (see case study below), which has coevolved with the host plant species in its native area, North America, does not cause serious damage there. Once introduced into Asia, however, it killed several millions of trees of various Pinus species.

According to Anderson et al. (2004), half of all emerging diseases of plants are spread by global travel and trade, while natural spread, assisted by weather events, is the second most important factor. In addition, there are also likely to be interactions between pest establishment and climatic or weather conditions. For example, global warming may facilitate the establishment of some pests that would otherwise not be able to establish (e.g. during an unusually warm winter under temperate climatic conditions). In fact, the increased market globalization of recent years, coupled with increased temperatures, has led to a situation that is extremely favourable to pest movement and establishment, with concomitant increases in the risk of severe yield losses (Deutsch et al., 2018; Savary et al., 2019). When considering the potential impact of climate change on plant health and hence on plant distribution, it is therefore important to understand not only which conditions allow pests to thrive, but also the pathways by which they move from one place to another.

An understanding of the pathways is also needed when determining what measures should be taken to mitigate and adapt to the changes in pest risk brought about by climate change. Considerable national and international efforts have been made to reduce the risk of international movement of pests (Meurisse et al., 2019), including the publication and implementation of International Standards for Phytosanitary Measures (ISPMs), developed under the auspices of the Commission on Phytosanitary Measures and the Secretariat of the IPPC. These include guidance on how to conduct pest risk analysis (PRA) to determine the risk of introduction (entry and establishment) and spread of pests and to select which measures to apply to prevent this occurring (ISPM 2, 2019; ISPM 11, 2019; ISPM 21, 2019). Such phytosanitary measures are generally applied with reference to pathway risks. As there is a requirement to periodically review the information supporting the PRA (ISPM 11, 2019), this presumably includes re-evaluation of the pathway risks, or at least those that are extremely dependent on changing climatic conditions such as the occurrence of extreme weather events that can spread quarantine pests across great distances.

A summary of the main types of pathways is provided below.

Wood packaging

Historically, wood, including packaging, has played a major role in spreading plant pests. Among the examples that show the significance of such a pathway is the movement of invasive insect species, such as the wood beetle Anoplophora glabripennis (Coleoptera: Cerambycidae), in packaging during international trade (EPPO, 2020a, 2021a). This species is polyphagous (i.e. it feeds on a wide range of foods), feeding on several species of the trees maple (Acer), poplar and aspen (Populus), willow (Salix) and elm (Ulmus) in forests and urban environments. Native to China and the Republic of Korea, it has been introduced into the United States of America and Canada in infested wood packaging and it has also been detected in several European countries. Eradication programmes are underway in these countries, these involving the detection, removal and destruction of infested trees. Careful inspection and treatment of solid wood packaging material, such as pallets and dunnage, is an international requirement to prevent new introductions. Modelling efforts to predict the geographical distribution of the beetle have shown that climate change may alter its distribution and impact (Hu et al., 2009).

Wood packaging has also been indicated as the likely pathway of many bark beetle species, such as Ips grandicollis (Coleoptera: Curculionidae), as well as other serious forest pests such as the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and the Sirex woodwasp, Sirex noctilio (Hymenoptera: Siricidae) (Meurisse et al., 2019). Movement of the pine wilt nematode, B. xylophilus (see case study), or its insect vector, through untreated wood packaging material has also been observed (Sousa et al., 2011).

Seeds, planting material, soil and growing media

Globalization of seed and planting-material markets is one of the main causes of the recent and rapid spread of plant pathogens to new hosts. Moreover, some of the newly introduced pathogens and insect pests that are typical of warm areas are spreading easily in temperate regions, because of increases in temperature. In general, seeds are vectors of pests. Mature plants are also great vectors of live insects including mites, aphids, caterpillars, leaf miners and thrips. For this reason, Australia, for instance, has completed a PRA on cut flowers that lists the main insects associated with them.

Particularly in the vegetable sector, the recent spread of new pathogens in different countries is clearly linked to the fact that, being seed-borne, their diffusion is favoured by market globalization; the effect of global warming on plants and their hosts has also contributed to this spread. This has been shown to be the case, for instance, with Alternaria spp., Fusarium equiseti and Myrothecium spp., which have recently been observed on lettuce, wild and cultivated rocket, lamb’s lettuce, basil and spinach (Gilardi, Garibaldi and Gullino, 2018). Tomato viruses (Tomato brown rugose fruit virus) and viroids (Potato spindle tuber viroid) are classic, recent and topical examples. Tomato brown rugose fruit virus has emerged in the last few years and has spread easily by seed movement. Many of the pathogens that cause severe losses in leafy vegetables, such as those mentioned above, can be seed-transmitted and hence go unnoticed. Thus, even low levels of seed infection can lead to the rapid emergence of new diseases in distant geographical areas (Gitaitis and Walcott, 2007; Gullino, Gilardi and Garibaldi, 2014a, 2019; Munkvold, 2009). Unfortunately, this happens very frequently, as shown by many recent introductions, despite the presence of industry and international standards defined in order to reduce this risk.

The ornamental industry, due to its international nature, is greatly affected by the introduction of pests through infected material (Daughtrey and Buitenhuis, 2020). Ornamental plants, whether started from seed, from cuttings or from cane section, can easily harbour pests. Only plants micropropagated through tissue culture (generally foliage plants) have a considerably reduced risk of infection by pathogens, provided that they are kept clean, consequently avoiding reinfection (Chen and Henny, 2006). Several of the most damaging insect and mite pests of greenhouse crops have originated through the importation of infested plant material and have established quickly because of the special environmental conditions of greenhouses (Albajes et al., 1999; Wang et al., 2015). Ornamental coffee plants imported from Costa Rica and infected by Xylella fastidiosa subsp. pauca are considered the possible vector of this destructive pathogen in Europe (Bergsma-Viami et al., 2015).

Soil and potting media, often imported, can harbour soil-borne pathogens (e.g. Fusarium spp., nematodes), the larvae of insect pests and weed seeds. This has been well documented in relation to peat and other media used in the ornamental industry and in nurseries. Contamination of growing substrates by soil-borne pathogens (e.g. Fusarium oxysporum, Pythium spp., Rhizoctonia solani) results in incomplete disinfestation and in early attacks of young plants (Garibaldi and Gullino, 1995).

In addition to the pest risk posed by the movement of seed, planting material, soil and growing media described above, a new type of threat has emerged in recent years, with the increasing online market that spreads planting material around the world. The planting material marketed as such is often of low quality and generally not subject to phytosanitary control, and hence it represents a new type of threat. This aspect, not yet considered at the moment, should be taken into account in the future.

Conveyances, cargo and movement of animals

Tractors, cars, trucks, trains, ships, aeroplanes, containers, re-sold used agricultural equipment, and other vehicles are common means for passively moving pests. Indeed, plant pathologists, entomologists and weed scientists often consider the speed of spread of pests as directly related to the speed of conveyances.

Living organisms can also spread pests such as weed seeds located on animal skin or fur. For example, movement of animal herds by pastoral communities into new territories in search of pasture has spread seeds of the invasive alien plant Parthenium hysterophorus in eastern and southern Africa (McConnachie et al., 2011).

The global shipping network is widely recognized as a pathway for vectoring invasive species. One insect species that is known to have spread throughout the world by shipping, including transportation by ships and shipping containers, is the gypsy moth, Lymantria dispar. This species may be introduced into a new area when the port has a suitable climate for the survival and establishment of the species. Two subspecies, with different geographical origins, are known today, and the global distribution threat from the Asian subspecies has been estimated using a CLIMEX model (Paini et al., 2018).

The brown marmorated stink bug heteropteran Halyomorpha halys (Hemiptera: Pentatomidae) is another example of an invasive insect travelling mainly through international trade as a contaminant of non-regulated goods such as machinery, containers and vehicles, but also by passengers and to a lesser extent through movement of plant material. It is highly polyphagous, feeding on more than 300 plant-host species, including food crops, forest trees and ornamentals. This pest has caused serious economic losses in hazelnut crops in Georgia and fruit crops in Italy since its introduction – most likely from North America. A detailed report of a pest risk assessment for the introduction and establishment of H. halys can be found in Burne (2019).

Passengers

People, with their leisure or business travel, are perfect vectors of pests, particularly in the absence of strict controls at points of entry. Leisure travel, in particular, is often associated with people bringing back food, seeds or exotic plants, and these can be infested with pests or can themselves be a pest. To counter this, an increasing number of countries are establishing campaigns at points of entry (airports and harbours), aimed at increasing the public’s understanding of the threat to biosecurity posed by the movement of plants and plant parts. Many countries inspect baggage and mail for food and other biosecurity-risk material and encourage incoming passengers to declare potential biosecurity risks. They screen passengers and their baggage using X-rays, detector dogs and manual inspections. Passengers with risk materials may be fined or even refused entry. In this respect, countries such as Australia, New Zealand and the United States of America (McCullough et al., 2006) have a long history of strict control, as well as of collecting and reporting data on interceptions.

Natural dispersal

There are examples where native and non-native pests have significantly expanded their geographical ranges naturally (i.e. not assisted by humans). These are usually in relation to major changes in host distribution or climate. Of the changes in climate, increasing temperatures have particularly facilitated range expansion in pests, especially at higher latitudes and altitudes. In Europe, for example, higher winter temperatures have increased the larval survival and nocturnal adult dispersal of the pine processionary moth, Thaumetopoea pityocampa, allowing the northern expansion of its range (Battisti et al., 2006). In addition, wind and storms can transport spores of pathogens over long distances, even across continents. For example, changing wind or storm patterns are projected to promote the future distribution of wheat stem rust, caused by Puccinia graminis (Prank et al., 2019). Also, myrtle rust (Austropuccinia psidii), detected for the first time in Australia in 2010 on the central coast of New South Wales, is expanding its distribution and can now be found in a range of native forest ecosystems, with disease impacts ranging from minor leaf spots to severe shoot and stem blight and tree dieback (Pegg et al., 2017). The distribution of several pests, including fruit flies, can be affected through hurricanes in the Caribbean, Central America, and the southern United States of America. For example, Flitters (1963), when following the hurricane “Carla”, observed that several insect species emerged in unusually large numbers in Texas, suggesting that they had been transported there by the hurricane from distant locations.