The most frequently cited agricultural pathways of accidental transportation for IAPUC are listed in Table 3, while Figure 1 gives a simplified overview.
Sub-category “4.5 Machinery/equipment” resulted to be the most frequent pathway of accidental transportation of IAPUC as stowaway, followed by the contamination of habitat material (“3.10 Transportation of habitat material (soil, vegetation, wood…)”). Both are quite general pathways (not requiring specific plant adaptations or conditions) that are easy to detect or infer, as are those involving the transport on vehicles (“4.10 Vehicles (car, train, etc.)”) and vessels (“4.4 Hitchhikers on ship/boat (excluding ballast water and hull fouling”), which is particularly relevant for aquatic IAPUC. The role of machinery and equipment was already found to be important for plants by Pergl et al. [
13], especially for their secondary spread rather than their primary introduction in the EU, and the same can be said for pathway related to the transportation of habitat material and contamination of nursery plans. On the contrary, pathways related to the contamination of seeds, foods, and animals were less frequently cited for IAPUC, while, for Pergl et al. [
13], at least seed contamination had a main role in the introduction and spread of alien plants. Such discrepancies are likely related to the different samples of the analysed species with respect to the broad group of alien plants analysed by Pergl et al. [
13]. A few IAPUC are crop weeds, a category which usually includes species that most likely become “contaminants”.
The likelihood of IAPUC being introduced or spread through a new range through one of the considered accidental pathways is generally not very high (Table 3, Figure 1). In particular, this is true for their introduction to a new area, as, for the most part, voluntary IAPUC introduction pathways are more likely (e.g., ornamental plant trade). With respect to the introduction stage, accidental pathways are more likely to act in the spread of IAPUC; however, the likelihood is meanly low or moderate. In few cases there is a high chance that species could be spread via accidental pathways, but it can happen in the case of transportation and spread via habitat materials (mostly soil) (e.g., Acacia saligna, Ailanthus altissima), machinery and equipment (e.g., Pennisetum setaceum), and marginally through animals (e.g., livestock), as seed contaminant and hitchhiker on vessels. More often, pathways related to transportation of habitat material and presence as hitchhikers on machinery and equipment, vehicles and other means of transportation are moderately likely. However, even if the likelihood is not always high, attention on agriculture-related pathways should be maintained. Insights about involuntary pathways are given in following sections.
2.1. Stowaways: Machinery, Equipment, Vehicles and Vessels
The main routes that could lead to the introduction and spread of IAPUC as stowaways are “4.5 Machinery/equipment”, followed by “4.10 Vehicles (car, train, etc.)” and “4.4 Hitchhikers on ship/boat (excluding ballast water and hull fouling)”, which is of key importance for macrophytes; minor pathways for IAPUC are “4.1 Angling/fishing equipment” and “4.6 People and their luggage/equipment (in particular tourism)” (Figure 1, Table 3).
In agriculture, machinery and equipment can refer to a broad selection of items eligible to work as stowaway vectors, both on land and on inland waters. Firstly, this category can include both machinery and powered (e.g., trimmers) or hand tools (e.g., hoes, rakes, spades). Devices can be specific for agriculture or employable also for other activities, such as loaders, excavators on land or weed cutting buckets, dredges in inland waters can also be used, for example, in construction sites, channels cleaning, etc. All these vectors have in common that viable plant propagules can be accidentally transported directly, nested in the machine body or implements (e.g., embedded in cracks, crevices, and components) or with the litter, soil, or mud attached to external or internal parts of the machines and devices (e.g., tire treads, tracks). Because of their structure and size, large-sized machinery is more viable to be an efficient stowaway vector than small-sized powered or hand tools, of which the dimensions and body structure are generally not highly suitable for the attachment of high amounts of viable propagules; despite this, their role as stowaway vectors should not be neglected.
This pathway has clear affinities with another important pathway for IAPUC, “4.10 Vehicles (car, train, etc.)” (
Figure 1,
Table 3), which is related to the accidental introduction and spread of IAPUC via means of transportation (cars, vans, lorries, trucks, trains) [
59]. Even if not exclusively related to agriculture, vehicles for transportation are commonly used in farming and forestry contexts; furthermore, in the patchwork of cultivated lands that characterize wide regions of the EU, agricultural areas are often crossed by linear infrastructure (from highways to rural or forest roads), with a consequent potential of remarkable propagule pressure from this kind of pathway. The mechanism of transportation of IAPUC as hitchhikers on vehicles is the same as in the “machinery/equipment” pathways (physical attachment to the body or components of the vehicle); seeds can be accumulated differently in different parts of vehicles [
77]. Vehicles can accrue a wide variety of seeds and plant propagules, and driving surface, road conditions, and seasons affect the rate of accrual. The type of vehicle also has relevance; for example, it has been observed that, on unpaved roads (where the risk of gaining propagules is likely to be higher than on paved roads), tracked vehicles accrue more seeds than small and large 4-wheel-drive vehicles and that the rates of accrual dramatically increase under wet conditions, which make surfaces muddy [
78]. These considerations can also be extended to the machinery pathway, whose contribution to propagules dispersal can be affected by machinery types, as well as soil conditions [
79,
80].
It is very important to underline that the risk of transporting viable plant propagules via vehicles, machinery, and equipment (VME) is strictly related to previous “in field” use in invaded sites, condition that would allow the attachment of viable propagules of plants to vehicles, machines, and tools. Consequently, the second-hand VME trade has a predominant role with respect to brand-new articles on the market in introducing and spreading IAPUC [
81]. This pathway has relevance both at small and large scales. Locally, VME can be routinely used at different sites, following operational relocations, with a consequent spread or introduction of propagules in different places at a small scale; Ansong and Pickering [
77] found that seeds can be dispersed over hundreds of kilometres by cars, even if they usually fall off after shorter distances. At a wider scale, the second-hand VME trade can work as vectors of introduction at the international level thanks to the resistance of viable plant propagules (
Table 5).
In France, the spread of
Andropogon virginicus has been assumed to be related to the movement of forest machinery in pinewoods management [
82].
Lygodium japonicum is a climbing fern that is likely to be transported as a stowaway via VME with certain ease. Rhizomes and roots fragments may remain viable for several days if embedded in soil within machinery or equipment, which protects them from desiccation [
83], but spores are viable for longer (up to 5 years;
Table 5), and are likely to be found on the surfaces and crevices of VME, as well as on quite small powered and hand tools. A thorough analysis by Hutchinson and Langeland [
76] revealed the presence of spores (also attached to fern micro-fragments) and gametophytes of
L. microphyllum, especially on chainsaws, sprayers, and machetes, used in controlling exotic ferns in the USA; operators themselves resulted in being active pathways of transportation of viable propagules (
Figure 1,
Table 3). This is also expected to happen with spores of
L. japonicum, due to the similarities in life history, reproductive biology, habitus and living environments between these two congener ferns [
84]. Other successful cases of transportation through VME can be associated with many other plants. For example, seeds of
Impatiens glandulifera Royle, a very prolific annual plant, can be successfully transported as hitchhikers on agricultural machinery (e.g., mowers, tractor wheels) [
85], as well as those of
Asclepias syriaca L. that are not dispersed by wind [
86]; seeds and fragments of plants of
Pueraria montana can be accidentally introduced or spread via VME, both in agricultural and other contexts, including snow removal activities [
87,
88]. Information about the likelihood of being transported as stowaways on VME can come from different sources, and are linked both to scientific investigations and anecdotal and case-specific observations. Furthermore, evidence can also come from data gathered in sectors other than agriculture and forestry, representing valid information as the mechanisms and vectors types are comparable to those employed in farming and silviculture. An exemplificative case is represented by
Microstegium vimineum, of which transportation and spread as a stowaway on machinery and vehicles has been investigated during routine rural road maintenance along a forest road in the USA [
79].
Additionally, vehicles may promote the spread of viable propagules of invasive alien plants thanks to the airflow created by their passage [
88]. This mechanism of human-mediated dispersal is usually relevant, especially for species producing seeds adapted to anemochory (winged or plumed seeds/fruit) (
Table 5). For example, samaras of
A. altissima can be transported for more than 150 m in the slipstream of vehicles along highways [
89]; dried seed-containing pods of
Acacia saligna (as other Fabaceae) have the potential to be moved by vehicle passage and by wind [
90,
91,
92]. The potential of being moved by airflow should not be disregarded for other species producing seeds that are not specialized to anemochorous dispersal, but that can be wind-dispersed, even if more slowly and for smaller distances, as demonstrated for the non-IAPUC
Brassica napus (round and smooth seeds) and
Ambrosia artemisiifolia (hooked cypselae) according to von der Lippe [
88].
In freshwater environments, seeds, but more than often fragments of macrophytes, with highly regenerative capacity and resistance to desiccation, can be successfully transported as hitchhikers to new sites on VME [
71]. Obviously, together with VME, the transport of hitchhikers on vessels is a highly relevant pathway for aquatic or amphibious IAPUC (“4.4 Hitchhikers on ship/boat (excluding ballast water and hull fouling)”); in fact, for all of them, this is a potential pathway (
Figure 1;
Table 3). Pathways related to VME and vessels can operate both in aquatic and terrestrial (riparian) environments; transportation can occur entirely along watercourses (natural and artificial) or banks, but it can also include overland routes as well, both at local and international scales (e.g., international trade, second-hand market). Among aquatic IAPUC,
Elodea nuttallii,
Lagarosiphon major, and also
Myriophyllum aquaticum, can be accidentally transported on vessels, boat trailers, and aquatic weed machinery, which can be moved from site to site along the same watercourse or changing water systems if transported to sites that are not interconnected. It is likely that the helophyte
Gymnocoronis spilanthoides takes advantage of hitchhiking on cleaning machines, which seasonally mow the vegetation along channels in rice fields in Italy [
49]. For amphibious IAPUC living on the shores of waterbodies, such as
Alternanthera philoxeroides (Mart.) Griseb. or
Ludwigia sp.pl., the contribution of terrestrial VME accessing banks should not be overlooked in their accidental transportation to new sites.
Obviously not all IAPUC have the same likelihood to be transported thanks to VME and vessels. These pathways are not considered highly likely for all IAPUC where it is considered possible. For example, the EPPO [
93] indicated that the transportation of viable propagules of
Lysichiton americanus (Hultén and St. John) (pieces of rhizome) through machinery and vehicles is a remote possibility due to depth of the rhizomes of the plant, and the few management measures in the habitats where it occurs (wet or waterlogged forests). Another case regards seed-containing pods and seeds of
Prosopis juliflora that are not considered highly prone to adhere to machinery and vehicles by experts [
94]. Among macrophytes, for
Eichhornia crassipes, it is less likely to be transported as hitchhikers on machinery and boats than other macrophytes, due to the conspicuous nature of its propagules (which usually are not small, undetectable ramets) [
75].
2.3. Contaminants: Habitat and Nursery Material
The category “3.10 Transportation of habitat material (soil, vegetation, wood, etc.)” is one of the most frequently cited pathways of introduction and spread for IAPUC (
Figure 1,
Table 3). Specifically, for this pathway, the main role is played by the transport of soils contaminated with viable propagules of plants. and only in few cases does the contamination regard different materials (e.g., hay). Soil has already been cited as a media facilitating the accrual of propagules on VME, or it can represent the mean of contamination in nursery plants (“3.1 Contaminant nursery material”). In this case, soil has to be considered a commodity itself (
Table 2), which is traded and/or transported as growing media (not a relatively small amount associated with plants) [
59], waste, and also for restoration activities (e.g., backfilling material in quarry restoration) [
98]. It can be a relevant pathway, especially for terrestrial and amphibious IAPUC, while it is usually not cited for aquatic species, even if it cannot be excluded that short-distance transport of wet soil (ensuring the right conditions to maintain propagules viable against desiccation) could actively contribute to spread. Viable propagules eligible to be transported as soil contaminants are seeds or spores and fragments of plants with regenerative capacity (mostly fragments of rhizomes and roots). Regarding seeds, their viability and quantity/density in soil are determinant variables for successful dispersal along this pathway. As reported in
Table 5, all IAPUC likely to be accidentally transported in soil can produce quite long-lasting soil seed banks with seed viability generally spanning from a few years to decades. In addition to a persistent soil seed bank, prolific viable seed production is another trait usually common to these IAPUC. For
Acacia saligna seeds, density in soil is variable, but can exceed 15,000 seeds m
−2 [
68,
99] and a density of 10,000–100,000 seedlings m
−2 has been found for
Gunnera tinctoria [
100]. Seeds of
A. saligna have a funicle and aril (elaiosome) and are suited to myrmecochorous dispersal; ants can also contribute to their accumulation in the first soil layer [
68]. The soil seed bank of
Impatiens glandulifera can reach exceptionally high densities (32,000 seeds m
−2) and even if most seeds germinate during the spring following their dispersal, according tothe annual plant strategy, a small part of these can maintain viability for 4 years [
101,
102].
I. glandulifera frequently colonizes riparian habitats, so its seeds can be mostly found in riverine top soil and gravel, which\ can be vectors of transport, even if they are moved in small amounts due to the high density of seeds [
85,
102].
Together with seeds, highly-regenerative fragments of IAPUC can be transported, embedded in soils, ready to sprout when solicited. Beyond prolific seed production, the key of success of
Asclepias syriaca is in its rhizome, thanks to its below-ground modified stem, is due to the plants forming a viable “bud bank” in soil and, in case of disturbance (e.g., soil excavation), fragmentation of the rhizome produces viable units able to generate new plants (clones), thanks to sprouting from buds [
86]. Another interesting case is the highly invasive
Ailanthus altissima. In addition to an amazing production of seeds, this IAPUC can also be effectively transported with soils thanks to its highly regenerative dispersal units; fragments of stem or root with adventive buds, even small-sized ones (<1 cm), can maintain viability, even after environmental stress (e.g., submersion), generating new clones and boosting the dispersal of the plant [
51,
52,
103].
The movement of contaminated soil can contribute to IAPUC dispersal, both at local and international scales. It is quite easy to figure out how this pathway works at a local scale, thinking about the excavation of soil and its re-use or disposal at other sites during a wide array of agricultural activities. At the international scale, soil trade volume and characteristics are not easy to trace, even at the EU level. It is relevant to notice that within the EU there are no particular restrictions or requirements for the inspection of soils moving from one Member State to another and only a small proportion of soil entering the EU is inspected at points of entry for the transportation of associated harmful organisms, and inspection intensity largely varies between EU Member States [
104]. Consequently, the contribution of this pathway can be relevant in introducing and spreading IAPUC from other countries, inside or outside the EU.
Beyond soil, some IAPUC can be accidentally transported with other types of habitat material, even if other vectors seem to be less relevant in the EU. The most frequently cited vector is hay and, among IAPUC, it especially is noteworthy in the context of Poaceae (
Table 3). For
Andropogon virginicus,
Pennisetum setaceum, Ehrharta calycina, and
Microstegium vimineum the accidental introduction through import of contaminated hay has been cited, even if evidence about the real role of this pathways is lacking. For example, even if transport of hay (and livestock) is observed for
A. virginicus in Australia (secondary spread), on the other hand, its introduction through contaminated hay from USA to Europe has to be inferred; there is no published evidence of
A. virginicus being transported as part of hay material from the USA, while there is evidence that hay is imported into the EU and that seed material of
A. virginicus can potentially be included [
105]. The same can be said for
E. calycina [
24]. For
M. vimineum, this pathway is simply cited [
30] and, for
P. setaceum, hay contamination is only supposed to have a role in the primary introduction to Australia [
106]. A peculiar case is represented by the fern
Lygodium japonicum, of which spores can be contaminants of pine straw. Clear evidence of contamination has been observed in the USA where the fern is invasive in pine plantations related to specific pine straw production; even if pine straw is not imported from the USA to the EU and this has to be considered a minor pathway [
83], this information gives a measure of the high dispersal potential of the fern.
The contamination of nursery material is another relevant involuntary pathway of introduction and spread for several IAPUC. Responsible for this contamination are usually seeds, spores, or fragments of contaminant plants that “accidentally colonize” soils or water where terrestrial or aquatic nursery plants are grown. This is possible if contaminant plant propagules occur in the nursery, conditions that today are likely to happen mostly outside of EU borders, where there are no restrictions on trade and the possession of IAPUC. For example, both
Alternanthera philoxeroides and
L. japonicum have been found to be contaminants in bonsai imported from China [
107,
108].
Persicaria perfoliata can be a contaminant of nursery plants through growing media (e.g.,
Rhododendron L. stock, forestry trees) [
109]. Among aquatic IAPUC,
Hydrocotyle ranunculoides has been found to be a contaminant of cultivated
H. vulgaris in Europe, but before entry into force of Regulation 1143/2014 [
110]. Due to the scarce detectability of propagules and their large use, aquatic plants, such as
Elodea nuttallii and
Lagarosiphon major, are often cited as contaminant of other aquarium plants, even if direct observations are missing for both species [
111,
112]. Especially for IAPUC of which identification can be criticized (e.g., macrophytes), the contamination of nursery plants can be related also to the “accidental” use of mislabeled species [
113], especially for species whose congeners are regularly traded (e.g.,
Cenchrus L. or
Pennisetum Rich.,
Ludwigia L.,
Myriophyllum L.).
A non-negligible number of IAPUC is likely to be accidentally transported with livestock; species can be attached to fur, with soil to clogs, and they can be found in dung. As already said, seeds of
A. virginicus may have been spread in Australia through livestock and possibly through hay used for animals [
105]. Seeds of
E. calycina are likely to be transported attached to fur, but can also be found in the dung of animals grazing contaminated hay [
114]. Livestock eating its pods could also contribute to the spread of
Prosopis juliflora, even if this has not been observed in the EU [
42]. On the other hand, propagules of
Gymnocoronis spilanthoides can be transported attached to animal hooves [
115].
2.4. Contaminants: Minor Pathways
IAPUC are not frequently cited as contaminant of seeds or foods (
Figure 1,
Table 3), probably because few of them are weeds of crops and are rarely used as plant for food or in food-making processes. Anyway for several IAPUC these pathways can be key in their introduction and spread in new ranges. One of these is
Parthenium hysterophorus L., forb devoid of any economic interest (
Table 4), and was primarily introduced as contaminant outside its native range [
116]. Seeds of
P. hysteorphorus have been found to be contaminants of seeds for planting (cereals, vegetables, field crops, pasture seed, seeds for animal consumption—“3.8 Seed contaminant”) and seeds for human consumption (grains—“3.3 Food contaminant”), especially introduced by shipments coming from the USA [
116]. In this case, these pathways are likely to be very effective in the primary introduction of
P. hysteorphorus in its invasive range. In fact, in the EU, even if the plant is not yet naturalized but has been recorded as a casual occurrence,
P. hysteorphorus has been found, especially near entry points of grains and other seeds or mills [
116], supporting the relevance of the introduction of the species as a contaminant of seeds for planting or food and the risk of its establishment. Among IAPUC not yet naturalized in the EU, this species is one of the most worrying as it could be introduced and spread following a wide array of pathways (
Table 3) and it would probably find suitable conditions in Europe [
117]. Other IAPUC can be contaminant of birdseed (
Alternanthera philoxeroides, Microstegium vimineum) or seeds for planting (
Persicaria perfoliata has been introduced, most likely with the importation of
Ilex sp. seeds to Pennsylvania, USA) [
109]. Even if it has to be considered as a pathway of secondary importance,
Heracleum mantegazzianum has been found to be a contaminant of seeds of other Apiaceae for food use (
Carum carvi L., source of cumin) and its seeds have been transported as spice (golpar), probably due to misidentification [
118].
Cortaderia jubata and
Myriophyllum aquaticum use different mechanism of contamination: basing on evidences regarding
C. selloana (Schult. & Schult.f.) Asch. & Graebn., seeds of
C. jubata could be transported as food contaminant due to attachment to the hairy surface of kiwi fruits (
Actinidia deliciosa (A. Chev.) C.F. Liang & A.R. Ferguson) [
117,
119], while fragments of
M. aquaticum could be accidentally transported as contaminants of stocked fish [
120].
Misidentification of plants or their parts can be also the basis for accidental transportation as food contaminant. As example, viable roots of
Pueraria montana, can be wrongly attributed to other plants with similar roots (e.g.,
Dioscorea sp.,
Manihot esculenta Crantz
, Maranta arundinacea L.); furthermore, seeds of the plant can be transported as contaminant of seeds for planting [
88].
Alternanthera philoxeroides can be confused with
A. sessilis (L.) R.Br. ex DC., which is consumed as a vegetable in Asia (Sri Lanka) and can be traded as food, even if this should be not a highly relevant pathway to the EU [
121].
Lygodium japonicum is the only IAPUC that can be transported via the timber trade, even if this pathway is not considered highly likely (Figure 1; Table 3).