Cities as hot stepping stones for tree migration

Cities around the world are promoting tree-planting initiatives to mitigate climate change. The potential of such efforts to assist tree migration has often been overlooked. Due to the urban heat island effect, cities could provide suitable climates for the establishment of outlier populations, serving as propagule sources for poleward tree migration.


INTRODUCTION
Cities around the world are increasingly encouraging and promoting tree-planting initiatives to sequester carbon and mitigate climate change. Picking the right tree in the right place is essential for maintaining the sustainability of urban landscapes 1,2 . As a response to recent climate warming, cities such as Philadelphia, Chicago, and London (Ontario, Canada) have already begun planting more southerly tree species on urban parks, streets, as well as other municipal lands. However, the potential of urban tree planting to assist species migration in a wider landscape has often been overlooked 3 . Due to the urban heat island effect, cities are experiencing a preview of future climates for nearby rural areas, potentially offering a climatic condition suitable for the persistence of outlier populations at higher latitudes than their native ranges. The outlier populations in cities could serve as propagule sources for species' poleward migration under climate change. Moreover, since trees can cool their environment, planting trees in cities can slow the rate of warming, which in turn allows them to grow for decades to reach reproductive maturity for further expansion. Here, we discuss the potential of urban tree plantings to assist the poleward migration of forest trees in temperate and boreal regions. Emphasis is placed on the unique climatic condition that cities could provide for the establishment, growth, and expansion of outlier populations.

THE NEED TO ASSIST TREE MIGRATION
Climate change is expected to shift the geographical distribution of tree species worldwide [4][5][6][7][8] . Increasing evidence has emerged showing that temperate and boreal forest trees are already moving toward higher latitudes to track suitable climatic conditions, with most of the evidence focusing on Europe and North America 9-12 . However, such movement cannot guarantee their survival, especially if the accessibility of suitable climates is highly constrained by species dispersal capabilities and humancreated barriers 13 . A study of recent climate mechanisms in the 1975-3013 period showed that rates of climate warming were fast across mid-and high-latitude forest biomes, particularly in boreal forests (1.70 km per year) and temperate broadleaf and mixed forests (1.07 km per year) 14 . These estimates were about 10 times faster than the rate of tree migration by long-distance dispersal (~100-200 m per year) 15 . It is projected that due to dispersal limitation, most of the wind-and animal-dispersed plant species in Europe will not be able to catch up with future climate change 16 .
In western North America, trees have already lagged behind their optimal climatic niches by~130 km in latitude or 60 m in elevation on average 17 . The stress induced by rapid climate warming will be exacerbated by the negative effect of extreme weather events (e.g., heat waves, drought, floods, and storms), which constrain the establishment and spread of tree species. The consequent decoupling between climate shifts and species migrations may result in species extinction 18 , as happened to a species of spruce, Picea critchfieldii, in eastern North America after the Last Glacial Maximum 19 .
Despite the pessimistic predictions, empirical studies of postglacial recolonization indicate that trees in boreal and temperate regions may not necessarily lag behind climate change, as species migration can be facilitated by the persistence of outlier populations in advance of their main ranges 20 . Rapid range shifts of boreal and temperate trees occurred following the retreat of ice sheets after the last glacial period 21 . Molecular evidence suggests that such range shifts were achieved by local dispersal from small, isolated populations occupying high-latitude microrefugia, where climates were favourable for their persistence outside of main ranges during the glacial period 22 . A well-documented example is ice-free refugia in northern Scandinavia, which supported the survival and expansion of conifer trees after the Last Glacial Maximum 23 . Recent models have also highlighted the favourable effects of outlier populations on poleward range shifts 24 . The role of outlier populations in the past may have an analogy under future climate change, as outlier populations not only can occur naturally as relicts of past climates but also could result from anthropogenic planting. Even a small number of trees planted far beyond their native range limit can be sufficient to establish naturalized populations 25 .

URBAN HEAT ISLANDS AS STEPPING STONES
Cities are already ahead of their surroundings in terms of climate warming, therefore potentially offering suitable climate conditions for the establishment of outlier populations (Fig. 1). Urban areas tend to have higher temperatures than their surrounding rural areas as if a warmer city air lies in a "sea" of cooler rural air 26 . This phenomenon has been commonly observed and investigated around the world, known as the urban heat island effect 27 . Generally, the urban heat island effect is an "inadvertent" modification of local climates during urbanization, caused by anthropogenic modifications of the landscape, anthropogenic 1 heat emissions, and the physical properties of buildings and other urban structures 28 .
Although the urban heat island effect is a local phenomenon with negligible impact on global warming 29 , its intensity and effect may represent harbingers of future climates. Observation of 419 big cities around the world showed that the average annual surface temperature difference between urban and rural areas can be as much as 1.5 ± 1.2°C during the day and 1.1 ± 0.5°C at night 30 . In contrast, the observed global mean surface temperature has increased by~0.87°C above 1850-1900 levels 31 . Such warming is expected to reach 1.5°C between 2030 and 2052 if it continues to increase at the current rate of about 0.2°C per decade. In Baltimore, for example, urban-rural differences in air temperature are similar to projected climate changes over the next 50-100 years 32 . Higher temperatures in urban areas affect species' living by stimulating their photosynthetic activity and extending growing season length 33 . Indeed, urban trees have been observed to grow faster than their counterparts in rural surroundings [34][35][36] . Although tree growth is driven by a combination of multiple biotic and abiotic factors (e.g., local climate, CO 2 concentration, pollution, light regime, interspecific competition, soil condition, nutrient, and water availability), the higher growth rates of urban trees seem to be closely related to the urban heat island effect.
Planting outlier populations in urban heat islands is expected to provide a substantial head start on poleward range shifts. Taking temperate broadleaf forests as an example, if the current rate of global warming continues, forest trees would need to move at least 107 km poleward over the next 100 years 14 . Given their migration rates (<100 m per year) during the early Holocene 37 , trees are likely to lag behind climate change by at least 97 km in the coming century without considering habitat fragmentation. On the other hand, daytime surface temperatures in temperate cities are as much as 0.46-1.43°C higher than in their surrounding rural areas 38 , which means that outlier populations in the cities could be closer to their future ranges by about 59-182 km than their native ranges with analogous climates (taking into account a 0.87°C increase in urban-rural temperature differences as being equivalent to a 111 km poleward movement of species' optimal climatic conditions) 39 . It is, therefore, possible to shorten or even eliminate migration lags in tree species by planting outlier populations in cities.

OUTLIER POPULATIONS IN URBAN HEAT ISLANDS
Cities have a long history of establishing outlier populations, either intentionally or accidentally 40,41 . Urban green spaces such as forest remnants, public parks, and gardens have great potential to receive and accommodate translocated tree species. During the last 200 years, international exchanges of plant material among botanic gardens have played a considerable role in the development of the alien flora in Central Europe 42 . An investigation of 357 European plant species showed that 73% of them have been moved into nurseries and gardens hundreds or even thousands of kilometres north of their natural range limits 43 . In the eastern United States, southern species planted in northern urban areas as ornamental plants are expected to speed the process of tree migration to a rate of 1 km per year 11 .
Trees planted in urban heat islands can slow the rate of warming, leading to more stable microclimate conditions in urban areas relative to surrounding rural areas. Trees cool their environment through shading, evapotranspiration, and solar radiation reflection 44 . In the context of global warming, the cooling effect of trees could partially or fully offset increases in urban background climate. For example, in Greater Manchester, a 10% increase of tree cover in high-density residential areas or town centres can counterbalance projected increases in maximum surface temperature due to climate change in the 2050s relative to 1961-1990 45 . The combined effect of urban background climate and the tree cooling effect has been observed in urban parks, which experience growing seasons longer than rural areas but shorter than nearby urban areas 46 . The relatively stable microclimate conditions in cities could allow trees to grow for a few decades to reach reproductive maturity.
Reproductive populations could then serve as propagule sources, from which species spread into surrounding areas and subsequently develop naturalized populations as climatic conditions allowed 47 . The process of range expansion can be supported by urban green spaces, such as private gardens, agricultural islands, roadside hedges, and copses 48 . These man-made landscapes could work as a series of habitat islands that provide stopover points, food, and shelters for the movement of seed dispersal agents (such as crows, jays, and nutcrackers) from urban to rural areas.

USING CITIES AS STEPPING STONES
Establishing outlier populations in cities can be regarded as a form of assisted migration (also called managed relocation or assisted colonization), which refers to the intentional translocation of species and populations outside their historic ranges to facilitate their range shifts under climate change 49 . Here, cities are perceived as 'hot' stepping stones for poleward migration, whilst species' future distributions are viewed as moving targets, which can be achieved by successively establishing outlier populations in cities along latitudinal gradients (Fig. 2). The 'climate analogues' approach developed by CCAFS 50 can help identify cities that have similar climatic conditions with those of species' native ranges at lower latitudes. Besides, the outlier populations established in cities can provide additional nursery capacity for assisted migration in local and regional spheres. For example, public parks and botanic gardens could serve as nurseries to test and accommodate translocated seeds and seedlings, providing a future supply of trees for efforts of assisted migration in nearby rural areas. Such efforts also avoid some problems associated with planting species outside their native ranges: not only because cities could provide them with extensive horticultural expertise, regular care, and record-keeping, but also because cities could offer real-world laboratories for ecologists, foresters, and managers to monitor and minimize the invasiveness of translocated species in their new environments, as well as their potential for creating pest problems 51 , before the implementation of largescale tree plantings.
It should be noted urban tree plantings that aim to assist tree migration will be able to reduce losses of ecosystem services in urban environments due to climate change 52 . Trees are a vital part of urban ecosystems. Maintaining and enhancing the long-term health of trees is essential for urban forests so that they can continue to provide ecosystem services, such as climate regulation, air purification, and carbon sequestration. The rate of recent climate change has exceeded the capacity of some native trees in urban environments to adapt, leading to increased mortality and susceptibility to fungal disease, insects, and other pathogens. One example is the native trees in the city of Bellevue, Washington, including western red cedar, western hemlock, and Douglas fir, which are experiencing a higher mortality rate due to drought stress. Efforts of assisted migration in urban areas can help establish new and better-adapted urban forests that support the sustainability of urban ecosystems.
Nevertheless, the success of assisted migration in urban areas will depend on the close cooperation among urban foresters, biologists, urban designers, and landscape architects. Besides urban heat island effects, intensive human activities in cities often result in harsh growing conditions for trees, which include altered hydrology and soil, air quality, invasive species, and heavy anthropogenic disturbances 2 . These conditions might have Fig. 2 Illustration of using cities as stepping stones for poleward tree migration.
Step (1): Seeds and seedlings collected from their native ranges are used to establish outlier populations in a higher latitude city where the climate is suitable.
Step (2): Assuming the first step is successful, translocated species will grow and reach reproductive maturity, accompanied by their ability to cool the city.
Step (3): Seeds produced by the outlier populations in the city are then dispersed to surrounding rural areas to establish naturalized populations, or are collected and planted in a more poleward city if the climate warms faster than projected, repeating steps (1) and (2).
negative effects on the outcome of the practice and thus need to be considered in efforts to establish outlier populations. Another important consideration will be the selection of seed provenance. Urban forests often have high risks of inbred effects and genetic narrowing. To maintain the genetic diversity of outlier populations, translocated seeds and seedlings should be selected by collaborating with experts in provenance selection. Further research is also required to enhance landscape connectivity to facilitate seed dispersal and accelerate the speed of colonization in and around urban areas 53 . Good understandings of the topology of urban forests and seed dispersal networks are needed to identify 'hub' woodlands where seed dispersal events are concentrated and outlier populations should be initiated 54 . Finally, to better share urban spaces with outlier populations, the practice of assisted migration must be assimilated within urban planning and design projects, which treat urban landscaping as an experimental substrate to study the persistence and invasiveness of translocated species whilst maintaining and improving ecosystem services for human beings. Gardeners need to think beyond beauty when selecting species and more on the potential of horticulture to serve as a route of assisted migration.