Resilient trees for urban environments: The importance of intraspecific variation

, outbreaks of pests and pathogens and an urban development with increasingly dense cities and a high proportion of impermeable surface materials. The importance of intraspecific variation needs to be better acknowledged in this context, since poor matching of trees and the local climate and growing conditions can lead to extensive loss of valuable trees. By using the right genetic plant material for the challenging urban environments, a more resilient tree population with a greater diversity and higher capacity for delivering ecosystem services can be gained. Here, we wish to discuss the need to consider intraspecific variation when planning resilient tree populations for urban environments and how seed banks and botanical garden play important roles in efforts to improve the matching of genetic plant material for future environmental challenges. Strategies to enrich urban tree diversity and increase resilience are outlined.


| INTRODUCTION
About 30% of the over 70,000 known tree species worldwide are likely under threat of extinction (Cazzolla Gatti et al., 2022).The main threats to tree diversity are forest clearance due to agriculture and urbanisation, direct exploitation for timber and other products, and pressures arising from climate change and biosecurity risk (Newton, 2021).Over the past 300 years, global forest area has decreased by about 40% and 29 countries have lost more than 90% of their forest cover (FAO and UNEP, 2020).From 2000 to 2020, the world experienced a net loss of over 100 million hectares (c.2.4%) in tree cover (FAO and UNEP, 2020).Trees are of immense ecological importance as they define and form the major structural components of forest ecosystems, which cover approximately 31% of the world's land surface.Forests play a major role in the Earth's biogeochemical processes, influencing soil production, hydrological, nutrient and carbon cycles, and the global climate.They contain about 50% of the world's terrestrial carbon stocks, while over 75% of the world's accessible freshwater is obtained from forested catchments (Newton, 2021).Forests provide habitat for a wide range of other species apart from trees, supporting at least half of the Earth's known terrestrial plant and animal species (Rivers et al., 2022).Conversely, trees are not only found in forests, but also occur on savannahs, shrubland and grasslands, in deserts, wetlands, coastal and rocky ecosystems, and urban environments.In cities, towns and villages, trees are vitally important to meet on-going and future social, economic and environmental challenges.Today, 55% of the world's population (4.2 billion people) lives in urban areas, a figure which is set to rise to 70% by 2050 (Callaghan et al., 2021).Urban trees are therefore essential to the lives of most of the human population.

| Urban environments and trees
Trees in urban environments offer multiple contributions to people including regulating, cultural, provisioning and supporting services, all of which are critical for sustainable urban development and human well-being (Cimburova & Pont, 2021) (Figure 1).Many of these benefits are strongly connected to tree size and vitality, with larger, healthier trees providing ecosystem services more effectively (Gomez-Muñoz et al., 2010;Hand et al., 2019).
Increasingly dense cities with a large proportion of paved and impermeable surfaces create challenging conditions for urban trees to develop successfully (Table 1).With climate change, multiple stressors such as heat waves, drought and temporary flooding will increasingly limit tree growth in urban environments and lead to higher tree mortality, and the potential loss of crucial ecosystem services.In a global study, Esperon-Rodriguez et al. (2022) found that the capacity to tolerate the projected conditions in urban environments has already been exceeded for 56-65% of the trees in 164 cities across 75 countries.It has been recommended that for long-term stability of urban forests, trees resilient to climate change must be chosen, so that they can survive and thrive (McPherson et al., 2018).Moreover, global movement of goods and people has enhanced the spread of invasive pests and pathogens worldwide (Aide & Grau, 2004;Crowl et al., 2008).Critically, climate change is allowing plant pests and pathogens to establish themselves in regions that previously had an unsuitable climate, increasing the mortality of common urban tree species.The combination of shifting climate compatibility interacting with novel biotic threats will limit the range of tree species that can deliver crucial ongoing resilience to the ecosystem services provided by the urban forest.
F I G U R E 1 Ecosystem services provided by trees in urban environments divided in four classes of services: provisioning, regulating, supporting, and cultural.
To create resilience to present and future challenges, where the exact consequences of future scenarios cannot be predicted in advance, a commonly proposed solution is to cultivate a large diversity of trees, that is, increase tree diversity at many taxonomic levels, including infraspecific variation.However, this will require substantial changes in national, regional and local policy as urban tree inventories often comprise of few species that dominates in many urban tree populations, many of which in Europe and North America are at risk from outbreaks of serious pests and diseases such as the Asian longhorned beetle Anoplophora glabripennis, the emerald ash borer Agrilus planipennis, Ramorum disease Phytophthora ramorum, and the ash dieback fungus Hymenoscyphus fraxineus (e.g., Cowett & Bassuk, 2020;Sjöman & Östberg, 2019;Tubby & Webber, 2010;Yan & Yang, 2017).
A clear example of a very limited diversity of urban trees is Helsinki, Finland, where almost 44% of all trees in public spaces are represented by Tilia spp. with a significant threat if these trees should be attacked by a serious pest or pathogen outbreak (Sjöman & Östberg, 2019).
Achieving an increased diversity of urban trees to improve the resilience of urban forests to future conditions is likely to involve greater use of non-traditional tree species, particularly in regions with relatively few native species, such as western and northern Europe.
Current literature guiding urban planners, landscape architects and garden designers about tree selection (e.g., Tabassum et al., 2023) relates to individual species.Such guidance does not adequately acknowledge the adaptive variation that results from the processes of natural selection found in more challenging climate conditions and stressful growing environments (Sjöman & Nielsen, 2010).Intraspecific variation, consisting of genetic and phenotypic diversity within and between populations of wild and domestic organisms, plays a critical role in regulating ecological processes in the face of adverse and often unpredictable stressors.

| Intraspecific variation and effects of its loss
There is growing evidence of large intraspecific variation within many tree species in response to different growing conditions, such as gradients in water availability.For example, drought-adaptation traits in tree species such as Acer grandidentatum, Acer rubrum, Acer saccharum, Betula pendula, Fraxinus Americana, Quercus ilex and Quercus rubra have been shown to differ across environmental gradients, relating to habitat type and precipitation (e.g., Alder et al., 1996;Bauerle et al., 2003;Hannus et al., 2021;Marchin et al., 2008;Schuldt et al., 2016;Sjöman et al., 2015).A robust body of biogeographical literature links some of this intraspecific variation to local adaptation (Temunovi c et al., 2012;Zohner et al., 2020).This is also apparent when comparing precipitation and temperature regimes throughout distribution ranges.
Intraspecific variation in traits is reported to be most common among species with a large natural distribution, as these species can occur in many different types of climates and growing environments (Royer et al., 2009).A species' capacity to tolerate an increasingly stressful situation may rely strongly on beneficial variants already present in the stressed population, rather than on new variants arising through genetic mutation (Orr & Unckless, 2008;Teotónio et al., 2009).Indeed, it has been suggested that an effective evolutionary response is positively related to the amount of standing genetic variation (Blows & Hoffmann, 2005;Lynch & Lande, 1993).Thus, the ability to cope with changing and stressful environmental conditions depends largely on how well individuals can adjust phenotypically to the altered conditions, and on the genetic variation present in the population upon which selection can act (Bijlsma & Loeschcke, 2012).
The genetic variation that can be lost in a single generation when converting forests to agriculture through clearcutting may take hundreds of generations to restore, which for long-lived organisms such as trees could mean thousands of years.In the face of rapid climate T A B L E 1 List of current and future challenges that can affect urban trees.

Climate change
Drought -many regions of the world will experience more frequent long periods of drought.
Heatmany regions of the world will experience more frequent heat waves.
Flooding -In connection with more frequent extreme weather, heavy and prolonged periods of rain will become a challenge for urban trees in specific regions with hypoxic conditions as a result.
Storms -Some regions of the world will experience more storms with intensively high winds Wildfires -Because of a warmer and drier climate intense wildfires will become more frequent and threaten urban settings

Pests & Pathogens
Pests and pathogens will affect many urban trees globally with extensive tree loss likely.These biotic threats will limit the number of species that can be introduced into urban environments.A changing climate will also aid the establishment of pests and pathogens in new regions.Such expansions of pest or pathogen distributional ranges, can lead to these threats becoming much more widely spread within both natural and urban tree environments.

Urban development
Through an increasing densification of urban environments, the space for trees above as well as below ground is limited.The dense settlement of cities results in an 'urban heat island' that will increase evapotranspiration, tree water use, and water stress.The paved inner-city environments of many cities combined with very efficient drainage make the growing conditions extremely challenging with dry and/or hypoxic conditions.
changewith marked changes documented at the scale of years or decadesthere is a twin need to both safeguard genetic variation to mitigate tree diversity loss and to retaining its potential for urban landscapes and horticulture (Leigh et al., 2019).
The list of tree species likely to show long-term resilience to serious pathogens and pests in urban environments in many parts of the world is very limited.It is, therefore, of great importance to find additional genetic material of these species with the capacity to cope with future climate conditions and resilience to known pests and pathogens.In the selection of future urban trees, good genetic matching for urban environments is essential in order to maximize the longevity and benefits of the trees (Figure 2).Today, urban tree nurseries, which supply most city trees worldwide, have very limited to non-existent awareness of intraspecific variation which may be a low interest priority for nurseries (Sjöman & Watkins, 2020).This indicates that the ornamental perspective has been prioritized in cultivar selection, at the expense of finding genetic material that has a higher tolerance for, e.g., drought.As a consequence, trees purchased for urban planting may not be genetically well suited to developing successfully in these challenging environments.There is thus a strong risk that many trees planted in towns and cities today will not develop into large, healthy trees with the capacity to deliver crucial ecosystem services.
Because of the current pace of habitat loss worldwide (in part due to urbanisation), there is a risk of losing valuable wild genotypes in many species of trees, compromising their ability to adjust to future challenges both in nature and when used in cities and horticulturally.
In addition, fragmentation of habitats leads to small, isolated populations that are subject to genetic erosion, as populations of normally outcrossing species come to show decreased levels of genetic variation and a decrease in fitness because of inbreeding depression (Nickolas et al., 2019).To make things worse, the magnitude of inbreeding depression generally increases considerably under stressful environmental conditions, such as extreme climatic events including heat waves and seasonal droughts (Armbruster & Reed, 2005).This makes inbred populations more vulnerable to environmental stressors.
For urban forests, genetic matching to future urban environments in a region is important to develop more resilient plant material (Sjöman et al., 2019).For instance, importing genotypes from warmer regions (e.g., lower latitudes) of a species distribution can improve the ability of the local population to cope with ongoing climate change by promoting genes of more distant and (slightly) different habitats within the species range (Leigh et al., 2019).

| The role of seed banks and botanical gardens in the face of environmental challenges
Evidence shows that we are facing a sixth mass extinction of species, if those species at risk today do in fact disappear (Barnosky et al., Filters that should be applied when selecting urban trees for a future climate.It is crucial to not only consider aspects such as resilience to pests and pathogens but also how the genetic material matches inner city environments in a future climate.The number of species that are not at risk of being affected by serious diseases and pathogens, and have the capacity to handle the local climate and tolerance for the growing conditions on site is usually very limited, especially in a more northern climate.This means that the few species that can handle the mentioned challenges should be of a genetic material that can also handle a future climate, which makes knowledge of the genetic variation within different tree species and its suitability for a future climate absolutely crucial. 2011; Brooks et al., 2019;Ceballos et al., 2017).In plants, two in five species are likely to be threatened (Antonelli et al., 2020;Nic Lughadha et al., 2020).This loss of diversity is unacceptable, especially since diversity is key for ecological resilience to future challenges.
Averting dramatic loss of diversity and associated loss of ecosystem services is still possible through intense conservation actions, but the window of opportunity is rapidly closing.Moreover, many existing conservation programmes are mainly directed towards preventing tree losses at the species level and seldom acknowledge loss of variation within species, despite the rate of loss of intraspecific variation being many times greater than the rate of species loss (Hughes et al., 1997;Leigh et al., 2019;Mimura et al., 2017).Indeed, diversity below the species level remains severely under-evaluated in global surveys (Laikre et al., 2020).
As political and social pressure to increase tree planting intensifies (Forest Commission, 2019), a golden rule for successful reforestation projects is to 'choose the right tree for the right place' (Di Sacco et al., 2021).Burley et al. (2019) identify two key components for the urban forestry sector in selection of trees for a future climate.
First, selection of species based on hierarchical filters using climate as the pivotal biophysical limiting factor would improve outcomes for cities.Second, species that may have been resilient in horticultural plantings under previous or current conditions may be unreliable in the future, while new opportunities will emerge as suitable climate space appears beyond the current range of species.However, even these identified factors reflect the pattern followed in the plant-guided literature, with the focus of attention firmly placed on speciesas if they were ecologically homogeneous unitsrather than genotypes which clearly shows a limited exchange of knowledge between science and practice.As global temperatures continue to rise in the 21st century and beyond, urban forestry and planning efforts should identify ecotypes and pools of genotypes within species that are most likely to thrive in future climates, in order to maximise planting success and provide a return on investment in the long term (Watkins et al., 2021).
Botanical gardens around the world have long worked on identification and conservation of biological diversity, but even in that context variation within species has been under-prioritised compared with variation between species.Many botanical gardens in the northern hemisphere have also attempted to identify trees that can grow in a more challenging cold climate by looking for cold-hardy plant genetic material growing at the northernmost limit of the species distribution.However, there have been very few recent botanical expeditions with the objective of finding genotypes of common species that are more exposed to heat and drought within their natural distribution, and thus possibly better adapted to a future with a warmer and periodically drier climate (Sjöman et al., 2019) et al., 2017).It has also become clear that conservation seed banks need to be complemented by seed banks focused on supplying seeds for habitat restoration, including tree planting initiatives (Breman et al., 2021;Goodale et al., 2023).
To explore these issues in practice, we considered four tree species with a very large natural distribution in the northern hemisphere, and with different rainfall and temperature regimes throughout their distribution: Acer platanoides, Acer rubrum, Betula pendula and Carpinus betulus.We then compared these with the provenances of the species found in the Millennium Seed Bank.This comparison shows that banked seeds have a very limited gene pool and lack provenances with natural growing conditions matching those found in urban environments in major European cities (Figure 3).
Apart from seed banks, living collections also preserve genetic material from extinction in the wild, with large botanical gardens and arboretums being critical organisations in this pursuit.However, recent research shows that most taxa within these collections are well below the genetic conservation targets, which means that existing collections of trees constitute a very small percentage of the available genetic variation (Hoban et al., 2020).One obvious reason for this is that many botanic gardens and arboretums lack the space to include large numbers of tree individuals with different genetic backgrounds in order to ensure that they have a broad representation of a particular species in their collection.Another reason is that, for economic, legal and logistic considerations, curators liberally share seeds and other propagating material between gardens, instead of making new acquisitions from wild populations, which means that many collections now have similar genetic material (Flower et al., 2018;Kashimshetty et al., 2017;Khoury et al., 2019).A telling example of this is Acer griseum from China, highly valued as an ornamental, for which all specimens in commercial cultivation and in botanical collections originate from Ernest H. Wilson's collection of the species in 1901, meaning that the species is represented by a very narrow genetic base (Aiello et al., 2020).In the wild this species occurs in many types of climates, although due to habitat loss, logging and wood harvesting it is formally classified in the IUCN Red List as Endangered, (Aiello et al., 2020).This distinction between the genetic base of plants in cultivation and those in the wild highlights the importance of in situ conservation of wild populations in protected areas and shows a need for propagation and ex situ preservation of trees in unprotected areas.

| The way forward in conserving genetic diversity for urban forests
A search for long-term sustainable plant material for local urban environments is needed to prevent loss of resilience of urban environments to future challenges and to maintain the supply of important ecosystem services.The outcome will be crucial for the growing human population living in urban environments worldwide.
In order for researchers, urban planners and other practitioners to identify these future trees, we need to immediately stop considering species as a uniform mass, without acknowledging the genetic variation they contain.We also need to collectively start applying concepts such as ecotypes or genetic origin (provenance), and focus on those that are adapted to the current and modelled future environmental conditions in the target location for their cultivation.
This means that extensive conservation efforts are required even for species that are not at risk of global extinction, but for which ecotypes with the greatest potential for urban environments are being lost regionally or locally.These rescue operations will require increasing both in situ and ex situ efforts.The in situ work will involve identifying areas where unique ecotypes of promising urban tree species have evolved to possess characteristics that make them valuable for urban environments in other regions.Actions in support of conservation of the genetic diversity within species need to be mandated through policies and legislation from local to international scales to reduce the risk of losing highly valuable ecotypes that could help urban environments to manage future challenges.In order to rescue valuable genotypes, ex situ activities are critical and should aim at collecting as much of the species geographic distribution as possible, in order to obtain a broad representation of the existing genetic material to be stored in seed banks or living plant collections such as botanical gardens.There is a particular challenge for ex situ collections of species that are very difficult to cultivate (Fant et al., 2016).While seed banks are an efficient genetic safeguard for many plant species, about 20% of plant species have recalcitrant seeds (those that cannot survive in standard seedbank conditions) or other sampling or storage challenges (Wyse et al., 2018).Although cryopreservation is often an option (although not always; see e.g., Wyse et al., 2018), it is very expensive, and consequently ex situ conservation efforts of species with recalcitrant seeds are usually limited to living plants in collections.
A key challenge for ex situ collections is capturing high genetic diversity in as few individuals as possible.A botanic garden might have resources to maintain a few to a few dozen (sometimes hundreds) of individuals of some priority species, but not the thousands that seed banks can or need to preserve (Hoban et al., 2020).Another limitation in ex situ collections is the increasing restrictions on material exchange imposed by global regulations on access, benefit sharing, and biosecurity.The purpose of these regulations is to protect the genetic material of one country from being exploited by other countries or organisations, but they have also made collection permits difficult to secure for conservation and especially for commercial horticultural use (Sirakaya, 2019).If the use of specific genetic material is restricted to non-commercial academic purposes, botanic gardens risk hosting potentially useful plant material that is unavailable for commercial cultivation and more widespread use in the urban landscape.
We suggest two strategies in order to enrich urban tree diversity and resilience: 1) widespread genetic screening of existing tree collections in botanical garden and arboretums, to assess the degree of intraspecific variation/number of distinct ecotypes captured within Moreover, for many countries with an exceptionally rich tree flora, it is possible to evaluate and use the native tree species to a much greater extent than today when many exotic species dominate urban plantations as seen in regions such as eastern Africa (Dharani, 2011).However, because of a very limited understanding of many native species capacity for urban horticulture, it is crucial to first thoroughly evaluate their usefulness and potential for substituting the dominating exotic species.For regions with a limited native tree flora, it is inevitable to use species from other parts of the world that can handle the city's challenging environments and deliver important ecosystem services while not becoming invasive threats (Sjöman et al., 2015).
. An example of recent conservation efforts with the aim of collecting and storing important genetic material is the joint work of the Millennium Seed Bank Partnership coordinated by the Royal Botanic Gardens, Kew.At the Millennium Seed Bank in West Sussex, England, over 2.4 billion seeds from more than 40,000 species collected all over the world are banked to conserve them for the future, with a focus on species that are economically important, threatened, or narrowly distributed.Important questions concerning this type of conservation effort are whether the seed material currently held in seed banks can already provide sufficient genetic material for a future climate, to what extent seeds from various ecotypes for different species are included, and how much of the whole distribution of each species is represented in the seed collection.These and related questions are now shaping agendas for seed banks and botanical gardens (Mounce

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I G U R E 3 Representation of provenances of four common tree species with a large natural distribution, including a large variation in climates, where genetic materials used in the study which are from the Millennium Seed Bank (MSB) are marked in orange, compared with their whole natural range (based on warmth index and annual precipitation) marked in blue.Figures modified fromSjöman and Watkins (2020) where distribution data is sourced from GBIF (Global Biodiversity Information Facility).collections for a given species.This will allow further evaluation and comparison of different genetic materials functional traits and their capacity for future climate scenarios in different plant collections (Hirons et al., 2021) (Figures4 and 2) identifying natural habitats with matching climate and growing conditions for those species within urban environments (nationally and internationally).This step will require climate modelling to identify specific regions and habitats that may include valuable genetic material with the capacity to tolerate challenging urban environments for the region.This latter direction can detect areas of a species distribution that are not existing in ex situ collection but have a good matching to urban environments in a future climate.

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I G U R E 4 Estimation of drought tolerance through evaluation of water potential at leaf turgor loss (TLP) of selected tree species taken from different botanical collections, including different genetic types within same species.An increased negative value in MPa indicates a higher level of drought tolerance.Where two gardens are compared, the significance level is indicated by *p < .05,**p < .01,and ***p < .001.Letters of heterogeneity indicate differences where three gardens are compared.nd = no significant difference.The error bars represents the standard error of collected TLP data (Hirons et al., 2021).
our best allies in the fight against climate change and biodiversity loss.Although we often think of them in forests, most of our interactions with trees take place in urban environments, where they provide us with shade, heat mitigation, flood abatement, noise and pollution reduction, pollination, beauty, and much more.However, to maintain and increase those manifold benefits we urgently need to rethink tree selection for urban environments, to include those species and provenances most suitable for the environmental conditions and stresses posed by a rapidly changing and unpredictable climate, spreading pests and emerging plant diseases.Major efforts now must take place to increase representation of future urban trees in living collections and seed banks, alongside genetic screening of potentially suitable genetic plant material for cultivation.With growing recognition of the current and future values of trees to our societies, we now have to realise these great opportunities.