Systematic literature review

This systematic review conforms to the guidelines outlined by the Preferred Reporting Items for Systematic Reviews recommendations (PRISMA) [45] and follows the systematic quantitative literature review approach outlined in Pickering and Byrne [46]. We have used the PRISMA Statement to demonstrate how we conducted the review and reported the methods and results used in this review according the requirement of the PRISMA reporting criteria (Checklist S1).

To obtain a comprehensive list of species with seed that can be dispersed on/in passenger vehicles (cars), we conducted a systematic review of the academic literature to identify all original published research studies that: (1) assessed seed dispersed by passenger vehicles, and (2) either directly identified seed collected from vehicles or identified seedlings of seed collected from vehicles, and (3) included the scientific names of the species and (4) were published in English.

To identify eligible studies, we conducted a systematic search of original research studies using the electronic databases: ScienceDirect, Web of Science, Scopus, Google Scholar and Google, from April 2012 to May 2013. A search string using a combination of the following keywords were used; man, human, tourists, visitors, automobile, motor vehicles, vehicles, cars, weeds, seeds, diaspores, spread, transport* and disper*. We used different combinations of search terms based on the requirements or limitations of each database. The search strategy for ScienceDirect, for example, was (man OR human OR tourists OR visitors OR motor vehicle* OR vehicle* cars OR automobile) AND (weeds OR seeds OR alien species OR invasive species OR non-native OR diaspores) AND (spread OR transport* OR disper*). The references cited by each potentially relevant study were reviewed to locate additional potential studies.

To ensure that we only included studies related to the topic, we first screened all the studies obtained after reading the titles and abstracts, and then excluded those that did not mention: 1) automobile or vehicles or humans as dispersal vectors; or 2) dispersal, or spread, or transportation, or 3) dispersal of plants, or weeds or alien species or invasive species. We then obtained the full text for all the original research study that passed this initial screening and reviewed them in detail. A second screening was then employed where a study was excluded if it did not generate empirical data or only reported on seed dispersed by vectors other than vehicles. Also, studies that reported specifically on specialized vehicles such as farm machinery/vehicles, earth moving vehicles, military vehicles, aircraft and boat/ships were excluded. Only studies that reported data about seed dispersed by general types of cars (sedans, two and four-wheel drive, utilities and wagons) were included. The number of studies excluded and those retained were recorded for each of the screening stages according to the PRISMA Statement (Figure 1) [45]. At the end, a total of 13 original research studies fitted all the criteria out of a total of 1,533 potentially relevant studies (Figure 1). For these 13 studies, information about the research in the studies was extracted including the name of author(s), publication year, geographical location of the study (continent and country), details of the sampling design, methods used to identify species (germinated seed and/or direct identification of seed) and the number of taxa listed in the study (Table 1).

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Figure 1. Flow chart using the PRISMA statement for the systematic review.

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Authors of three of the studies [29,31,47] kindly gave us more complete species lists than were included in the original studies. Two studies identified in the electronic searches [31,47] represented different aspects of the results from the same experiment and therefore were treated as one dataset (Table 1).

The studies are concentrated in a few regions, with five studies from Europe and four from Australia (Table 1). They had one of three research designs with 10 natural experiments (Table 1). Across the 13 studies, seeds were most often collected from mud or sludge with some of the studies reporting other methods such as brushing, trapping, vacuuming and/or hand removal from vehicle parts. Nine of the studies identified the species (456) based on seedlings germinated in glasshouses and/or laboratories (Table 1).

List of species with seed dispersed on/in cars

To obtain as complete a list as possible of species with seed dispersed by cars, we created a species database using results from the 13 studies. Due to variation in the methods used, duration and location of study and measurements taken among the studies, it was only possible to compare presence/absence data for species among the studies. To ensure consistency in the results, only data at the level of species was included, not genera, and only if the scientific name was included (e.g. not morphotaxa). The species database included information about all species listed in one or more of the studies, including its scientific name, common name, synonyms, family, growth form and life span. Species names were obtained from the original studies, while other information about those species was obtained from online databases and a weed compendium [43,48,49,50]. Plant nomenclature conforms to United States Department of Agriculture [49] and PlantNET [50]. Synonyms were checked and data consolidated by removing duplicates and retaining only names that conform to the nomenclature authority used (Figure 2).

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Figure 2. Flow chart using the PRISMA statement showing the steps involved in screening individual taxa.

This was done to obtain a comprehensive list of species with seed collected from cars.

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We used the Chi-square goodness of fit tests to compare the proportion of seeds of different growth forms and life spans collected on/in cars. The Chi-square test for independence was then used to determine if growth form of the species with seed dispersed by cars were dependent on their life spans. The categories, annual, biennial and those species that are both annual and biennial species were combined and referred to here as ‘annual-biennial’ while those with mixed or intermediate life spans such as biennial/perennial and annual/perennial were combined to form a category called ‘mixed’.

Weed status of species

To determine if a species was considered a weed somewhere in the world, data from the ‘Global Compendium of Weeds’ was used [48]. For international environmental weeds, that is, weeds that invade natural vegetation and adversely affect biodiversity, we used a list of the top 400 international environmental weeds [43]. Our database was also compared with the list of the 100 world's worst invasive alien species [51].

To assess how many species of weeds in Europe have seed that could be dispersed by cars, we compared our database with the ‘European Alien Species Database’ from the Delivering Alien Invasive Species Inventories for Europe (DAISIE) [52]. This database includes 5,970 species classified as alien invasive/naturalized plants in one or more of the 27 European Union member countries [53] including the 150 most widespread alien species in Europe [54]. We also assessed the invasive status of the species according to information on alien and invasive plant species in north and central Europe provided by The European Network on Invasive Alien Species (NOBANIS) [55]. The 52 species on the European and Mediterranean Plant Protection Organization (EPPO) invasive plant species list [56] was also used. To see if car dispersal is common in the weed flora of a specific country in Europe we used the catalogue of invasive species for the Czech Republic, which comprises 1,454 alien taxa of which 61 are considered invasive [57]. Weed status in countries were the studies were carried was also determined.

Data on the weed status in Australia of the species in our database were obtained from the 2,739 species of weeds that are listed as naturalised in Australia [11]. We also compared our database with the 429 plant species declared ‘Noxious Weeds’ by one or more state or territory government [44] and the 32 weeds that are considered of ‘National Significance’ as determined by the Australian Government [58]. To assess how many weed species in North America could be dispersed by cars, we used the 1,596 species that have been documented as invasive or noxious weeds in North America [59] and the 112 plant species declared noxious weeds federally in the United States [60]. As a single comprehensive list of invasive species for Asia and Africa was difficult to obtain, so we focused on weed lists for India, China and South Africa, which have large human populations, many cars and expanding road networks. For India, we used a list of 1,599 species classified as alien plant species, of which 225 species are declared invasive [61], while for China we used a list of 265 invasive plant species [62]. For South Africa, we used the list of 198 species of weeds/invasive plants listed in Regulation 15 of ‘The Conservation of Agricultural Resources Act’, No. 43 of 1983 of South Africa [63].

Which species have seed that can be dispersed by cars?

Seeds of 626 species representing 75 families have been collected from cars (Table 2, Figure 2); with an average of 48 species reported per study (range 2-222). The families with the greatest diversity of species were the Poaceae (grasses) with 178 species (28%), the Asteraceae (daises, 80 species, 13%) and the Fabaceae (peas, 42 species, 7%) (Figure 3).

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Figure 3. The number of species from the most common plant families with seed collected from cars.

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When seeds of species on cars were compared to plants growing in the region, many of the species with seed on cars are also found growing on road verges and/or in the local area [26-28,30,32,34]. However, the frequency and/or abundance of seed on cars compared to  plants in the local area is often quite low, indicating that car floras are a selective mechanisms, favouring the dispersal of seed of a subset of species found on road verge flora [27,28,30,32].

How many of these species are weeds and where are they weeds?

Nearly every species with seed collected from cars has been cited as a weed in some part of the world (599, 96%) [48], with over one-sixth (101 species) are classified as international environmental weeds [43] and some are also among the 100 world's worst invasive species [51] (Table 2).

At least 439 of the 5,970 alien invasive/naturalized species recorded in one or more European countries [52] have seed that can be dispersed by cars (Table 2). These include one-third of the 150 most widespread alien species in Europe [54] and 13% of the alien flora of the Czech Republic (Table 2). Many are considered particularly threatening including Buddleja davidii, Heracleum mantegazzianum, Paspalum distichum and Solidago canadensis which are considered highly invasive and threaten plant health and/or biodiversity (Table 2) [56].

Almost half (206) of the 439 invasive/naturalized species in Europe had seed collected in one or more of the five studies conducted in Europe. Across the three studies in Germany [27,31,47], there was a total of 213 species with seed from cars, of which 65 (31%) are invasive/naturalised in Germany. Of the 49 species with seed on cars from the one study in Sweden [34], 29 (59%) are naturalized alien species in Sweden, two of which, Stellaria media and Urtica dioica are declared invasive in Sweden [55]. For the one British study [30], 9 (25%) of the 36 species found with seed on cars was invasive/naturalized in Britain, while for the one study from Belgium [28], three (11%) of the 28 species were invasive/naturalized in Belgium [52]. These results demonstrate that a wide diversity of weed species in Europe is dispersed by cars in Europe.

Many non-native plants in Australia have seed that can be dispersed by cars. This includes, 14% of the 2,739 naturalised plants in Australia, ~15% of the 249 declared noxious weeds and 28% of the 32 species of weeds considered of national significance in Australia (Table 2). Across the four studies conducted in Australian, 256 species were recorded that are not native to Australia, including the international invasive weeds Andropogon gayanus, Chrysanthemoides monilifera, Genista linifolia, Nassella neesiana, Nassella trichotoma, Rubus fruticosus and Ulex europaeus (Table 2) (Species List S1).

Although only two of the studies were from North America [33,64]; 16% of the 1,596 species listed as invasive/noxious in North America [59] can be dispersed by cars. This included 15% of the nationally listed noxious weeds of the United States [60]. The two American studies, however, recorded only seven species that are considered invasive/noxious weeds in North America, but this included the international environmental weeds Salsola kali, Poa pratensis and Verbascum thapsus [33,43,64].

Although no original research studies from India, China and South Africa were found in the systematic search of the literature, the database included many species considered to be weeds in these countries. One tenth of the 1,599 alien species in India, including a quarter of the 225 invasive species have seed that has been collected from cars (Table 2). Almost a third of the 265 invasive species in China [62] have seed that has been collected from cars. About 12% of the 198 plant species declared as weeds or invaders under Regulation 15 of The Conservation of Agricultural Resources Act, No. 43 of 1983, of South Africa [63] can also be dispersed by cars.

Which plant and seed traits favour dispersal by cars?

Among the 625 species with seed dispersed by cars, most were forbs (58%) or graminoids (32%) with few shrub or tree species (χ² = 210.3, d.f. = 2, P < 0.001) (Table 2). There were nearly equal numbers of perennial species as annual/biennial but few mixed species with seed (χ² = 167.7, d.f. = 2, P < 0.001) (Table 2). When life span and growth form were examined together, there were significant differences; with 19% more perennial graminoids than annual graminoids, 26% more annual forbs than perennial forbs dispersed by cars (χ² = 105.2, d.f. = 4, P < 0.001).

Although there was considerable variation in the species recorded among the studies, with 487 species recorded once (Species List S1), there were some common species (Table 3 and Table 4). For example, there were 16 species recorded in five or more studies, which had some traits in common (Table 3 and Table 4). All 16 species, for instance, are considered widespread species that benefit from disturbance (Table 4), have very high seed output, release seed around ≤ 1 m from the ground, and have small/light seed (mostly ≤ 1 mg) (Table 3). Most can also reproduce vegetatively (Table 4). They were all forbs (nine) or graminoids (seven), with no shrubs or trees, and 50% each annuals and perennials (Table 3). Nearly all of them grow in open habitats and have a low tolerance for shade (Table 4).

Some similar results were reported in individual studies. Species that have seed transported over long distances by cars often produced a lot of seeds [34] that are mostly small in size and lighter in weight [27,28,30,32], and have a persistent seed bank [28,30,34]. Seeds dispersed on cars have also been found to be from low-growing (releasing) plants [34] and from species with shorter seeds [28].

How much seed and how far can they be dispersed by cars?

Collectively cars can transport a large number of seeds with estimates of 67,500 ± 7,300 seedlings per ton of dry sludge from car washes in Australia [65], 6,252 seedlings germinating in glasshouses from seed traps located inside long motorway tunnels in Germany [31] and 3,926 seedlings germinating from mud collected from cars driven in Germany [27]. Estimates of the number of seed per car, however, tend to be low with estimates of 3-6 seeds per tourist car in a National Park in northern Australia [66], 1-2 seeds per vehicle in University of the Sheffield car parks in England [30] and three seeds per vehicle in a car park at the University of Ghent in Belgium [28].

When the results of the studies that estimated number of seed per car [28,30,66] are combined we estimate an average of only 2-4 seeds could be carried by each car. Multiplying these numbers by the current number of cars in a country or region it is possible to estimate the average number of seeds that could be transported by this vector. For example, cars could be moving around ~490-980 million seeds in the United States, 480-960 million seeds within the European Union, 248-496 million seeds in India, 240-480 million seeds in China, 25.4-50.8 million seeds in Australia, and 12.6-25.2 million seeds in South Africa [36,37,38,39,40,41].

Only one study [33] has quantified the actual distance seed can be transported by a car. This was done using a manipulative experimental design to assess the dispersal potential of Bread wheat (Triticum aestivum), Rapeseed (Brassica napus) and Wild rye (Elymus trachycaulus) which found that some seeds were transported over 250 km. Some other studies have estimated the distance seed could be dispersed by cars, with Hodkinson and Thompson [30] indicating that while seed may be dispersed over hundreds of kilometres they were most likely to be dispersed between 3-40 km. Other studies indicated shorter distances, with von der Lippe and Kowarik [31] estimating that seeds of at least 32 species could be dispersed over 250 m while Veldman and Putz [68] estimated that seed had travelled at least 500 m on cars.

Where can seed collect on/in cars?

Seeds have been collected from different parts of cars including under the chassis, front and rear bumpers, wheel wells and rims, front and back mudguards, wheel arches, tyres and the interior floor mats. Considerable variation in the amount/diversity of seed among different parts of a car has been recorded [29,33,67]. In an Australia study, more seeds were found attached to the underside of the cars, followed by back mudguards, front mudguards and cabins than on engines, radiators, tyres and rims [67]. In terms of the diversity of seed, cabins and engine bays have been found to contain a greater diversity of viable seed than other parts of cars in another study in Australia [29]. In a study determining whether long distance dispersal by vehicles contributes to grass invasion in Bolivian forests [68], most seeds were found on the tires and wheel wells and on interior floor mats. This was related to the amount of mud attached to, or deposited in, the car and how often that part of the car was exposed to air movement and/or wet conditions [29,33,67]. Some studies indicate that seeds are dispersed over shorter distances when attached to more exposed parts of a car such as wheel wells, undersides and the front and rear bumpers, especially in wet conditions [28,33,64,67].

Do driving conditions influence type and amount of seeds dispersed?

Based on the results of the studies, the potential for seed to be dispersed by cars is affected by several factors including where cars are driven [33,64]. Variation in the amount and type of seed among cars used for different purposes and at different times was observed in some of the studies [64,66]. Cars traveling on unpaved/untarred roads and off-road for instance, often collected more seed in mud/soil than those driven on paved roads, particularly if conditions are wet [32,33,64]. As a result, cars used by more adventurous tourists/drivers were reported to collect/disperse more seed because they were mostly driven on unpaved roads and/or off-road with lots of mud that contains seeds [33,64,66].

Climatic conditions can affect seed dispersal by cars. For example, more seeds were found on cars driven under dry conditions either on paved and unpaved roads than driven under wet conditions, irrespective of the location of seed on the car [28,33,64]. Although in wetter conditions, mud on the road increased the risk of seeds attaching to cars, particularly on unpaved roads, it was thought to also increase the potential for mud and seed to be washed off cars [33], while dry conditions facilitated longer distance dispersal [28,33,64].

According to some of the studies [28,30,32,65], seasonality can also affect seed dispersal by cars. More seeds were found on cars when plants are seeding, including more seed on cars autumn in Australia [67] or in the dry season in Nigeria [32] than at other times of year when fewer species were seeding.