Ecosystem service provision by road verges

This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2019 The Authors. Journal of Applied Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society. 1Environment and Sustainability Institute, University of Exeter, Penryn, Cornwall, UK 2NERC Centre for Ecology and Hydrology, Wallingford, Oxfordshire, UK


| INTRODUC TI ON
Roads form a vast global network and are a ubiquitous and fundamental component of human-dominated landscapes. They have diverse and often profound negative ecological impacts, primarily habitat loss and fragmentation, light and noise pollution, chemical pollution of air and water, and the direct mortality of wildlife due to collisions with vehicles (Forman et al., 2003). These negative impacts affect surrounding landscapes, often up to distances of 1 km, so potentially impacting 20% of all land (Ibisch et al., 2016). However, given how central roads are to the global economy and to everyday life, it is more realistic to look to reduce and mitigate these negative impacts, and to develop opportunities for positive environmental contributions, rather than simply seek to remove the source of the problems altogether.
'Road verges' provide one such set of opportunities. They are the strips of land (known by a variety of terms) in the immediate vicinity of roads that separate them from the surrounding landscape ( Figure 1).
Road verges tend foremost to be written about in the context of more heavily 'constructed' roads. But the concept, and our definition here, extends much more widely as virtually all roads have associated bordering strips of land that are distinctively different, and typically much more heavily and anthropogenically disturbed, from that which lies beyond (Figure 1). Road verges are commonly grassland habitats, but can be shrubland, forest or artificial arrangements of K E Y W O R D S ecosystem services, green infrastructure, highways, natural capital, pollution, road verges, roadside, traffic F I G U R E 1 Road verges and the wide variety of forms that they can take: (a) grassy road verges along the D2 highway in the Czech Republic, (b) road verges with grass, shrubs and trees along a busy expressway near Kuala Lumpur, Malaysia, (c) regularly mown, grassy road verges in a suburban area in Sheffield, UK, (d) a tree-lined urban street in Chittagong, Bangladesh, (e) road verges separating surrounding forest in Northwest Territories, Canada, (f) wide, grassy road verges that have been managed by cutting in Namibia, (g) a small lane with narrow road verges that form vertical habitats with adjacent hedges in Devon, UK and (h) a dirt road in the Namib Desert, Namibia, where the only apparent road verge has been created by vehicles pulling over. trees and horticultural plants (Figure 1), and we use the term also to include bare earth and freshwater bodies (e.g. ditches). On a global scale, verges are hugely variable and can range from a few centimetres of disturbed road edge, to a few metres of regularly mown vegetation, to many metres of unmanaged habitat (Figure 1). Road verges can support biodiversity and there is growing appreciation of their potential value as a conservation resource (Gardiner, Riley, Bommarco, & Öckinger, 2018). This paper goes one step further by proposing that road verges and the species they support have the capacity to provide ecosystem services (ES) on a large scale.
Road verges serve a range of purposes: they can increase visibility and improve aesthetics for road users, provide a route for road drainage or a refuge for pedestrians, and buffer people and the surrounding landscape from adverse impacts of traffic. However, the land itself is largely unutilized and is generally only managed for safety purposes-namely cutting, burning or grazing to reduce vegetation height and improve visibility for road users-or not managed at all. There is thus the potential to design and manage road verges in a way that enhances ES. While roads run like a network of veins across landscapes, causing widespread negative ecological impacts to adjacent areas, road verges form a parallel network and have the potential both partially to mitigate negative impacts of roads and to deliver environmental benefits. However, this must be set against the loss of ES from the habitats that road verges displace, as well as potential ecosystem disservices. The potential for road verges to provide ES may be particularly marked because of the spatial extent of road verges, the breadth of positive environmental contributions that they can make and there being little competition for their use.
There is also debate around how road verges are managed: whether they should be managed primarily for safety, or also as a component of green and conservation infrastructure (e.g. Plantlife, 2019).
In this paper, we examine the actual and potential contributions of road verges to ES provision. First, we provide a conceptual framework and review the literature to identify the extent of current knowledge and evidence. We then use this as the basis for exploring the characteristics of road verges that might influence their capacity to provide ES including their area, connectivity, shape and contextual ES supply and demand. In each case, we consider the current supply of ES from verges, and then how this is likely to change in the future based on projections for growth in road extent, traffic densities and urban populations. Finally, we provide some key considerations for designing and managing road verges for ES and an agenda for future research. Throughout, our focus is on road verges, but many of the general principles might apply equally to the vegetated borders of other linear transport infrastructure such as railways and canals.

| Framework
Across the world, road verges are likely to provide a diverse array of ES that primarily benefit road users (both drivers and pedestrians) and local people ( Figure 2 supporting populations of plants and/or animals that provide crop pollination, pest control and nutrient cycling, and, due to their proximity to roads, filtration of air and water) and cultural services (e.g. health and aesthetic benefits by providing access to nature; Figure 2). However, road verges likely also provide ecosystem disservices ( Figure 2), and the net benefits need to be compared with the loss of ES from the habitats that road verges have displaced.

| Literature search
We carried out a formal literature search using Web of Science to identify scientific publications (up to 1 June 2019) addressing ES provision by road verges. This literature is varied and covers a broad range of subjects. Thus, we aimed for a comprehensive, but not necessarily complete review. We used a search string to identify studies on road verges (covering names and forms that road verges take across the world), combined with the phrase 'ecosystem service*' or one of 13 search strings relating to the main ES that road verges might provide (see Appendix S1). We screened the search results using titles and abstracts, or where necessary, the main text. Relevant studies were those that measured or inferred ES provision from road verges or similar roadside areas. When a recent literature review was available for an ES, we did not retrieve empirical studies. The key details and findings of relevant studies were recorded in a spreadsheet (Appendix S1). America and Asia; Appendix S1). Furthermore, few studies compare ES provision by road verges to that from the habitats they have displaced, especially in natural landscapes (probably resulting from the geographical limit of the studies), making it difficult to assess the net impact of road verge construction. Rather than focusing our review on these limited contexts, we provide a holistic framework for ES provision by road verges in all contexts, on a global scale, and use this as the basis for exploring the current and future potential of road verges for ES provision. We direct readers to recent reviews where available, or otherwise describe some of the most relevant empirical studies. We provide the full list of studies in Appendix S1.

| Biodiversity
Road verges support populations of some plants and animals (reviewed in Gardiner et al., 2018).

| Carbon sequestration and storage
Road verge soils and vegetation can provide a substantial carbon sink.
A study in the United States found that roadside filter strips had similar carbon storage and sequestration to grasslands (Bouchard, Osmond, Winston, & Hunt, 2013). Urban roadsides can provide even greater carbon stocks: urban soils have 3-5 times greater carbon stocks than natural soils (because anthropogenic processes provide carbon sources and the upward growth of soil over long periods, resulting in both faster and deeper carbon accumulation), of which urban roadsides have some F I G U R E 2 The ecological impacts of roads and the ecosystem services (ES) and disservices that may be provided by road verges. Road verge ES might address some of the environmental problems caused by roads (e.g. pollution) and provide further benefits to surrounding landscapes. Each broad landscape type (agricultural, urban and natural areas) demands a different suites of ES, which should be the target of management to enhance ES provision by road verges of the greatest stocks of black carbon (produced from burning fossil fuels; reviewed in Vasenev & Kuzyakov, 2018 2002). Many studies demonstrate that roadside vegetation, filter strips and swales (shallow, vegetated channels) provide water filtration, bioremediation and flow regulation (Appendix S1), for example reducing water flow by 75%-90% during storm events (Henderson, Smith, & Fitch, 2016), and swales reducing total suspended soils by

| Pollination and pest control
Many studies in Europe and North America demonstrate that road verges are important semi-natural habitats for insect pollinators (reviewed in Hopwood et al., 2015) and natural enemies of pests (Appendix S1), which are known to spill over from areas of high-density into surrounding landscapes (reviewed in Blitzer et al., 2012). However, few studies have tried to measure spill-over from road verges, or the resulting impact on pollination or pest control services. Three studies provide some evidence: length of road verge in the surrounding landscape was positively related to the activity density of predatory spiders in oilseed rape fields in two studies in Austria (

| Ecosystem disservices
Nature in road verges can also have negative consequences for people. For example, plants can reduce air quality, produce allergens, and damage and disrupt infrastructure (e.g. falling trees, tree roots and leaf fall), and there can be negative social perceptions of infrequent management as neglect (Säumel et al., 2016). However, these effects have received much less attention in the literature than have the ES provided by road verges.

| Large-scale ES multi-functionality
Currently, there are few empirical studies on road verges that consider multiple ES or ES provision beyond the local scale (Appendix S1). However, the overall potential of road verges for ES provision is also determined by their broader-scale characteristics, namely their extent, their impact on connectivity, and the supply of and demand for ES in the surrounding landscape. In the following sections, we discuss the current situation and future projections relating to these characteristics to explore the potential of road verges for providing ES.

| G LOBAL E X TENT OF ROAD VERG E S
The global road network is estimated to be 36 million km in length

F I G U R E 3
The spatial extent of road verges is illustrated by the high density of roads in a small area of the United Kingdom, and by the ubiquity of road verges in a 36 km 2 subarea (near Truro, Cornwall; 50.2759N, −5.1586E). In the map, road verges include areas of grassland, scrub and trees, but exclude roadside hedges. The histogram of road verge widths shows that the size and shape of road verges varies dramatically: most road verges in this area are less than 2 m wide, but a number of road verges are between 20 and 75 m wide, which may affect their capacity to provide particular ES, and resulting management approaches and priorities. Maps and data were produced by drawing polygons around road verges using satellite imagery from Google Earth and verifying using Google Street View (Google, 2019), then importing to ArcMap 10.5.1 (ESRI, 2017). Road verge widths were calculated by creating centrelines for each road verge, converting them to points at 5 m intervals, measuring the distance from each point to the nearest road verge edge, then multiplying by 2 average value for grasslands (0.054 kg C m −2 year −1 ; reviewed in Conant, Paustian, & Elliott, 2001), which is probably a conservative estimate (Bouchard et al., 2013;Vasenev & Kuzyakov, 2018), then they may sequester 0.015 Gt C/year globally-nearly 1% of the annual carbon sink provided by the world's 4 million km 2 of forests (Pan et al., 2011).  Kämpf, Hölzel, Störrle, Broll, & Kiehl, 2016) and the establishment of vegetated strips around agricultural fields benefits biodiversity, reduces nutrient, soil and water loss (reviewed in Haddaway et al., 2018), though obviously reduces crop provisioning. However, the ES from road verges will very rarely outweigh the negative environmental impacts of roads, so road construction should principally aim to minimize environmental impacts (Laurance et al., 2014) and only consider road verges as a tool for partially mitigating and offsetting them.

| DEMAND FOR E S ALONG ROADS AND IN ADJACENT L ANDSC APE S
The landscapes in which roads occur can broadly be classified as urban or rural. In Britain, 38% of roads occur in urban areas and 62% in rural areas (Department for Transport, 2018a), while in the United States just 21% of roads occur in urban areas and 79% in rural areas (Forman et al., 2003). These two land-use types give rise to demand for different suites of ES (Figure 2). Urban areas are defined by high densities of people and currently hold 55% of the global population, though numbers are as high as 82% in North America and 74% in Europe (United Nations, 2018). ES required in urban areas include those that improve human health and well-being, reduce pollution (e.g. through air filtration and noise reduction) and regulate environmental conditions (e.g. local temperature; Gómez-Baggethun & Barton, 2013; Figure 2).
Rural areas are often dominated by agriculture, which gives rise to demands for ES that improve agricultural production (e.g. maintaining soil health and providing crop pollination) and sustainability (e.g. reducing soil erosion and flooding), or otherwise by natural and semi-natural habitats, which give rise to demands for ES that mitigate environmental pollution (Figure 2). In both urban and agricultural landscapes, there are often few other highquality habitats, so measures to increase both biodiversity and ES are especially important, and in all cases there will be demand for ES that minimize negative impacts of roads.
The extent of demand for ES that mitigate pollution and benefit road users will be affected by the traffic density of a particular road and the proximity and density of people, dwellings and natural resources. In Britain, major roads constitute just 13% (50,500 km) of roads but carry 66% of road traffic (Department for Transport, 2018a). In the United States, the interstate highway network comprises just 1.2% of roads, but carries 22.8% of traffic (Forman et al., 2003). The majority of the demand for pollution-mitigating ES is therefore associated with these heavily used roads, which are also likely to have the widest road verges (Figure 3). Proximity to the pollution source is one of the most important factors determining the effectiveness of pollution-mitigation measures (e.g. Janhäll, 2015), so road verges are well positioned for this purpose.
Given that a minority of roads support a majority of traffic, focusing efforts on improving road verges next to heavily used roads (e.g. through strategic habitat creation, tree planting or improved mowing regimes) will provide disproportionate improvements in ES provision.

| Future developments in ES demand from verges
ES provision by road verges will become more important as human populations increase, urbanization continues and surrounding habitats are further degraded. By 2050, the proportion of the global population living in urban areas is projected to increase from 55% to 68%-an estimated 2.5 billion additional urban residents (United Nations, 2018). This will dramatically increase pressures to use urban and peri-urban land to benefit the health and quality of life of urban residents, with road verges offering a major opportunity for doing so.
Although the total length of road is predicted to remain relatively stable in many regions with already well-developed networks (e.g. Europe and North America; International Energy Agency, 2013), traffic densities are still expected to increase. In Britain, the total distance driven on roads was 530 billion km in 2017-an increase of 8% over the previous 5 years-with similar increases across all road types (Department for Transport, 2018b). Rising traffic densities will increase the demand for pollution-mitigating ES along existing roads, though vehicle emissions will reduce in the long term. In Britain, CO 2 emissions from road transport decreased by 4% between 2000 and 2015, with similar decreases in NO x and particulate matter (despite a 9.3% increase in vehicle miles), largely due to improvements in fuel efficiency and the uptake of ultra-low emission vehicles (Department for Transport, 2018b). Reductions in road transport emissions will be further accelerated by the phasing out of diesel vehicles and uptake of electric vehicles, which suggests an overall reduction in demand for ES that mitigate road and traffic pollution in many European countries. However, road traffic and associated pollution will increase in countries such as India and China due to the expansion of road networks (International Energy Agency, 2013), growing populations and rising GDP.

| Future developments in connectivity provided by verges
Projected increases in the extent of the global road network will further fragment habitats and reduce connectivity in natural landscapes. However, road verges might increase connectivity in highly modified urban and agricultural landscapes if road verges of suitable size, habitat quality and continuity are created alongside roads, at least for species that are highly mobile or able to persist in narrow, linear habitats (e.g. Tremblay & St. Clair, 2009). Strategic design and management of road verges might improve the capacity of many species to use them for movement and dispersal, though limitations to verge size and shape will still make them unsuitable for many.
There are a number of national-and international-scale projects that aim to increase habitat connectivity.

The ES or ES bundle(s)
What is the context of the surrounding landscape and the people that live there? Which ES are needed by those people, and which can be provided by the road verge, given ecological, climatic and social constraints? Broadly, this will be dictated by the road type and surrounding land-use ( Figure 2), but local-or region-specific considerations or issues may justify prioritizing specific ES Surrounding land-use: prioritize ES related to human health and well-being in urban areas, agricultural production and sustainability in agricultural areas, and mitigation of pollution and other negative ecological impacts of roads in natural areas (Figure 2) Road type: prioritize ES related to pollution mitigation on heavily used roads Social considerations: identify social factors that might facilitate or limit peoples' use of ES from road verges, for example, socio-economic status and access to nature may affect health and recreational benefits from road verges Environmental issues: identify climatic issues (e.g. extreme temperatures or flooding) and other environmental issues (e.g. poor air or water quality, soil erosion) that might be addressed by road verges

The plant species and habitats
Which species or habitats can best provide the desired ES? Plant species can differ markedly in their capacity to provide ES, for example due to size, leaf surface characteristics, growth rates, and phenology. If the desired ES are delivered by animals, the aim should be to provide plant species or create habitats (through planting or management) that support populations of those animals (e.g. pollinators). Tools that are available to help with such decisions include i-  (Brown, Percivalle, Narkiewicz, & DeCuollo, 2010) Noise reduction: coniferous tree species are slightly better at reducing noise than broad-leaved tree species (Nasiri, Agricultural, & Reso, 2015) Pollinators: restored prairie road verge habitats support more pollinators than those dominated by non-native vegetation (Hopwood, 2008) Temperature regulation: tree species differ in their cooling ability (Stratópoulos, Duthweiler, Häberle, & Pauleit, 2018) Water filtration: infiltration system effectiveness is affected by the planted species (Leroy et al., 2017) 3. The spatial arrangement of plants and habitats The size and shape of a road verge will determine its capacity to provide ES, to support viable populations of species, and to act as a habitat corridor. This will be a major limitation for existing road verges, so future road construction should consider this from the outset, though must also account for the direct loss of habitats and ES due to road verge construction. Regardless of size, strategic spatial arrangement of plants and habitats can enhance road verge ES provision, and poor design may result in disservices. For ES-providing animals (e.g. pollinators and pest natural enemies), locating habitats along the exterior edges of road verges may reduce their exposure to traffic and facilitate their movement to ES beneficiaries in adjacent land (e.g. movement of pollinators to flowering crops). A mosaic approach, whereby different parts or sections of road verge are managed differently or at different times, may also provide multiple habitat requirements for ES-providing animal species or provide a greater range of ES Size: Increasing the width of farmland grass strips from 2 to 5 m increases their ability to intercept soil sediment from 55% to 84%, nitrogen from 29% to 58% and phosphorus from 23% to 48% (reviewed in Van Vooren et al., 2017). Spatial arrangement: Air filtration: affected by proximity of vegetation to the pollution source and other factors; poor design can reduce air quality, for example, trees in street canyons reduce air flow and concentrate pollutants (reviewed in Abhijith et al., 2017;Baldauf, 2017;Janhäll, 2015) Noise reduction: affected by tree density (Ow & Ghosh, 2017) Pollinators: benefit from mosaic management (e.g. Noordijk et al., 2009) and prioritizing habitats a few meters back from the road edge  Temperature regulation: affected by vegetation type and configuration (Sodoudi, Zhang, Chi, Müller, & Li, 2018) Water filtration: affected by swale design characteristics (Fardel et al., 2019) 4. Routine management Routine management of road verges (e.g. cutting regime) may affect ES provision. However, both the financial and environmental costs of management must be considered. For example, management frequency and the machinery required will affect the amount of noise pollution and fossil fuel emissions, and therefore the net benefits of the ES provided (Säumel et al., 2016), though also the demand for mitigating ES Mowing twice per year and removing hay is optimal for plant diversity (reviewed in Jakobsson et al., 2018) and insect pollinators (Noordijk et al., 2009) Leaving areas uncut reduces water flow and improves water filtration (Henderson et al., 2016) (Continues) species richness (reviewed in Jakobsson, Bernes, Bullock, Verheyen, & Lindborg, 2018), flower species richness, flower abundance and pollinator abundance (Noordijk, Delille, Schaffers, & Sýkora, 2009), which are likely to benefit pollination services and a range of other ES (Schwarz et al., 2017).
It has recently been suggested that road verges could be used for growing biofuel crops (Voinov, Arodudu, Van Duren, Morales, & Qin, 2015), which might provide a considerable provisioning ES (and free up other areas for nature conservation). But, replacing road verge vegetation with a monoculture crop is likely to be at the expense of most other ES. Other studies explore the use of grass cuttings for biogas production (e.g. Piepenschneider, Bühle, Hensgen, & Wachendorf, 2016; Appendix S1), which are often a by-product of routine road verge management. The diversity of plants and insects benefits from cuttings being removed from road verges, which reduces soil nutrients and provides gaps for seedlings (Jakobsson et al., 2018). Currently, cuttings are rarely removed due to the financial costs of collection and disposal but using cuttings for biogas might make their removal financially viable and even profitable. Furthermore, Piepenschneider et al. (2016) found that two cuts per year was optimal for maximizing biomass, which is also optimal for plant species richness (Jakobsson et al., 2018).
There are a growing number of 'green infrastructure' projects, which are pioneering the use of public infrastructure to deliver environmental benefits, including using road design and roadside vegetation to address problems of heat islands and water runoff, and produce better places for people to live (Black, Tara, & Pakzad, 2016

| CON CLUS IONS
The potential of road verges for nature conservation is a rapidly growing area of interest in science (e.g. Gardiner et al., 2018) and society (e.g. Plantlife, 2019). We argue that this should go one step further by considering other ES and environmental benefits. can be costly, and current management of road verges often aims to reduce costs while meeting safety guidelines. In some cases, management for ES may be cheaper and provide a win-win, but in most other cases it will provide long-term financial returns if environmental benefits are accounted for, and could be incentivized through payment for ES (Richards & Thompson, 2019). Capability project NEC06895. The manuscript was improved by comments from two anonymous reviewers.

AUTH O R S ' CO NTR I B UTI O N S
B.B.P. and K.J.G. conceived the ideas and led the writing of the manuscript. All authors contributed to the ideas, manuscript drafts and gave final approval for publication.