Differential Stomatal Responses to Surface Permeability by Sympatric Urban Tree Species Advance Novel Mitigation Strategy for Urban Heat Islands

Abstract

As urbanization draws more people to metropolitan areas, a steadfast increase in impervious surfaces ultimately contributes to a pronounced urban heat island effect. While city greening strategies to mitigate urban thermal effects often tout street-tree cover expansion, many plant species are susceptible to heat stress, limiting survivorship, primary productivity, and ecosystem services. Our research objective was to characterize how urban imperviousness impacted the photosynthetic traits of four sympatric tree species in Old Town La Verne, California. We found that while Camphor trees (Camphora officinarum) and Carrotwood trees (Cupaniopsis anacardioides) did not differ significantly in photosynthetic traits at sites with impervious and pervious surfaces, both Coast Live Oak trees (Quercus agrifolia) and Olive trees (Olea europaea) showed significant differences in leaf stomatal length and density. Our findings suggest that the photosynthetic traits of some exotic tree species may be less susceptible to surface permeability than either native or floristically indigenous tree species. We propose that urban greening initiatives adopt a temporal strategy for mitigating urban heat island effects, starting with an urban canopy composed of exotic trees more resilient to impervious surfaces and later transitioning to a recombinant canopy ecology of floristically relevant tree species suited for the soil permeability native to southern California.

1. Introduction

As urbanization continues to draw more people to metropolitan areas [1], building resilience and adapting urban environments to anthropogenic climate change is an increasingly important challenge for cities [2,3]. Global warming, one of the most widely studied effects human activity is having on climate [4,5,6,7], results primarily from the emission of greenhouse gases into the atmosphere from the combustion of fossil fuels as well as land-use practices that compound deforestation [8]. Carbon dioxide, one of the most widely anthropogenically produced greenhouse gases [4,5,9,10], absorbs infrared radiation, correlates with increases in average temperature, and contributes to extreme weather phenomena that negatively impact communities and ecosystems [8,11].

The relationship between increasing urban population density and decreasing natural areas ultimately serves to strengthen urban heat island effects [12,13]. The limited green areas and the high density of infrastructure (e.g., roads, buildings, etc.) in urban landscapes absorb and re-emit solar radiation more intensely than natural landscapes (e.g., forests, water bodies, etc.), resulting in spatiotemporal islands of higher temperature relative to surrounding natural areas [12,14,15]. As such, the strength of urban heat islands can be influenced by factors such as weather, geography, heat generated from human activities, infrastructure geometry and material properties, as well as reduced natural landscapes [1,16]. Urban heat island effects are prominent in large cities and can manifest at temporal scales like year, season, and time of day [14,17,18] as well as spatial scales like greenspace density and surface permeability [19]. In urban landscapes, for example, diurnal temperatures can be 0.5–3 °C higher and nocturnal temperatures 1–3 °C higher than temperatures in adjacent natural areas [1,12,14].

Urban heat islands have diverse effects on city inhabitants by altering energy resource consumption, human health, and air quality [14]. Alternatively, the prevalence and persistence of urban heat islands can be effectively limited via infrastructure design, specifically by the density and diversity of vegetation, a type of materials used on exterior surfaces of buildings and roadways, as well as land and waterway conversion induced by urbanization [20]. As such, cities have adopted broad strategies to mitigate urban heat island effects by both reducing heat gains (e.g., vegetation cover and density of impervious surfaces) as well as promoting heat losses (e.g., evapotranspiration and evaporation) via the influence and design of green and blue spaces [20,21]. These mitigation strategies, however, often overlook functional ecology in advance of the incidence and cover of green spaces [22,23,24,25]. The result is a recombinant ecology of species interactions that share neither an evolutionary history [16] nor a natural history [1].

Ecosystem services are ecosystem processes that serve to advance human health benefits, such as the relationship between urban tree richness and the reduction in asthma incidence via improved air quality [26]. Environmental management strategies that integrate knowledge of the functional ecology of urban greening initiatives further cultivate diverse ecosystem services [22,27,28]. This approach requires both an exploration [28] and characterization [27] of the recombinant ecology of urban species [1,22]. For example, despite the ecological, physiological, and adaptive susceptibility of plant species to heat stress in urban environments [16,29], city greening strategies to mitigate urban heat island effects often tout the expansion of street trees [30].

Given the adaptive capacity of plant photosynthetic traits to changes in the environment [31], our research objective was to characterize how impervious surfaces impacted leaf stomatal dynamics in four sympatric tree species commonly growing along the streets of Old Town La Verne, California (Figure 1): Coast Live Oak trees (Quercus agrifolia Née) are native to the California Floristic Province [32], Camphor trees (Camphora officinarum Nees) are native to south China [33], Olive trees (Olea europaea L.) are native to the Mediterranean region [34], and Carrotwood trees (Cupaniopsis anacardioides [A.Rich.] Radlk.) are native to northeast Australia [35]. Stomatal dynamics, involving the opening and closing of stomata on plant leaves, play a critical role in regulating the exchange of water vapor and carbon dioxide between plants and the atmosphere [36]. Quantifying stomatal dynamics offers valuable insights into evaluating microclimates by understanding the physiological responses of plants to environmental conditions, including transpiration, temperature regulation, CO₂ exchange, and air quality [37]. As such, we hypothesized that leaf stomatal length, density, dispersion pattern, and diversity of size classes on said urban tree species would change relative to the perviousness of the ground surface.

2. Materials and Methods

We used Google Map satellite imagery to characterize the proportional abundance of both pervious and impervious surfaces at two locations sympatric to Old Town La Verne, CA: Moon Valley Nurseries (3000 B Street, Figure 1a) and University of La Verne (1950 Third Street, Figure 1b). The ground cover at Moon Valley Nurseries primarily comprises decomposed granite, a highly pervious substrate, and is accompanied by a single one-story building. In contrast, the University of La Verne campus features a diverse ground cover consisting of gardens intermingled with various impervious surfaces such as asphalt roads, cement sidewalks, and multiple multi-story buildings.

In order to mitigate the impact of spatiotemporal variations of CO₂ in different urban landscapes [38], we carefully chose our sampling locations within a distance of less than 800 m from each other. The deliberate selection of sympatric locations allowed us to achieve a higher degree of homogeneity in terms of factors that may contribute to differential CO₂ levels in the built environment, such as vehicle emissions, industrial activities, power generation from fossil fuels, residential and commercial energy consumption, as well as low species richness of urban vegetation and the overall form of the urban landscape [38,39]. Additionally, all of our sampling locations, as reported by CityOfLaVerne.org (accessed 11 July 2023), are designated as residential zones and exhibit similar urban environmental characteristics.

Our field sampling took place during the first week of March 2023, characterized by predominantly clear cloud cover (58%) and an average temperature of 20.6 °C, ranging from a minimum of 9.4 °C to a maximum of 19.4 °C. Throughout this period, temperatures remained within the range of 5 °C to 26.7 °C, as reported by weather.com (accessed 11 July 2023). During this period, the air quality index (AQI), which characterizes ozone, PM2.5, and PM10 levels, was reported as 42 and 41, respectively, for Glendora-Laurel (Site ID: 060370016) located 8.5 km NW of our study location, and Pomona (Site ID: 060371701) situated 4.3 km SSE of our study location, as reported by AirNow.gov (accessed 11 July 2023).

We selected four sympatric tree species that are common throughout the streets of Old Town La Verne, CA (2232 D Street, Figure 2): Coast Live Oak trees (Q. agrifolia), Camphor trees (C. officinarum), Olive trees (O. europaea), and Carrotwood trees (C. anacardioides). Approximately 2–3 leaves were collected from 5–7 trees of each of the 4 street tree species at each of the two study locations, using the following criteria: 20–30 cm diameter at 1.3 m height (DBH), presence of a sprinkler system, presence of seasonal soil fertilizing and branch pruning. A total of 14–15 leaves per species per location were harvested using shears, using the following criteria: proximal to terminal bud, sun-exposed, average size (leaflet), and at a height of 2–3 m above ground level.

A single-leaf epidermal peel of the abaxial surface was conducted for each leaf using clear nail polish and clear packaging tape. These peels were then mounted on glass slides and evaluated for stomata impressions at 400× magnification using an MT-40 compound microscope (Meiji Techno, Saitama, Japan), following the methodology described by [40]. The length of a single stomata (guard cell length) on each leaf was measured using an ocular micrometer, which was calibrated using a 0.01 mm ruled stage micrometer (Ward’s Science, Rochester, New York, NY, USA). The diameter of the field of view (FOV_diameter) was measured using the stage micrometer, enabling the calculation of stomatal density (ρ) on a given sample slide by counting the total number of stomata observed within said FOV (No. Stomata) by means of Equation (1):

$$\rho =\frac{No. Stomata}{\pi {\left(\frac{{FOV}_{diameter}}{2}\right)}^2}$$

(1)

A digital image of the field of view was obtained using a microscope adapter for a smartphone camera. The dispersion pattern of leaf stomata was then assessed from the captured digital image using a grid-overlay technique, following the established guidelines described in reference [41]. The diversity of stomata size classes was calculated using the Shannon Diversity Index (H) by means of Equation (2):

$$H=-\sum _{i=1}^s{p}_i·\ln \left(p_i\right)$$

(2)

where p_i is the proportional abundance of the ith stomata size class relative to the total number of stomata observed across all size classes (s).

The underlying distribution of dependent variables stomatal length, stomatal density, stomatal dispersion index, and stomatal diversity index of size classes were each evaluated using a Shapiro–Wilks test for normality in the software app Statistica version 13 [37]. Differences in mean stomatal length, stomatal density, stomatal dispersion index, and stomatal diversity index of size classes relative to surface perviousness (i.e., pervious or impervious surface) were each evaluated using a respective parametric (for normally distributed dependent variables) or non-parametric (for non-normally distributed dependent variables) t-test in the software app Statistica version 13 [42].

3. Results

The Google Maps satellite image analysis of Moon Valley Nurseries showed that its approximate 7.3 ha footprint comprised of 99.4% pervious surfaces (i.e., combined canopy and ground cover) and 0.6% impervious surfaces (i.e., building rooftops and parking lots) (Figure 1a). The Google Map satellite image analysis of the University of La Verne campus showed that its approximate 12.8 ha footprint comprised 54.9% pervious surfaces and 45.1% impervious surfaces (Figure 1b).

In Coast Live Oak trees, the leaf stomata length differed significantly with respect to surface perviousness, where longer stomata were detected on trees growing on impervious surfaces and shorter stomata on trees growing on pervious surfaces (

Table 1. Mean leaf stomatal size, density, dispersion pattern, and diversity of size classes in four tree species growing in pervious and impervious surface conditions.

Street Tree Species	Stomatal Responses
	Size (mm ± s)			Density (No./mm2 ± s)			Dispersion (Pattern)			Diversity of Class Sizes (H)
	Pervious	Impervious	p	Pervious	Impervious	p	Pervious	Impervious	p	Pervious	Impervious	p
Coast Live Oak (N = 30 leaves)	24.3 ± 2.5	27.7 ± 2.9	0.010	7.1 ± 0.7	2.4 ± 1.1	<0.001	clumped	clumped	>0.05	0.2	0.2	>0.05
Camphor Tree (N = 28 leaves)	16.0 ± 6.1	17.2 ± 3.4	>0.05	333.2 ± 157.4	281.7 ± 107.9	>0.05	clumped	clumped	>0.05	1.0	1.1	>0.05
Olive Tree (N = 28 leaves)	7.5 ± 3.0	9.6 ± 4.9	>0.05	1306.3 ± 662.8	191.6 ±1 87.9	<0.001	clumped	clumped	>0.05	1.3	1.1	>0.05
Carrotwood Tree (N = 30 leaves)	101.0 ± 19.3	85.7 ± 19.1	>0.05	118.4 ± 31.4	95.6 ± 27.8	>0.05	clumped	clumped	>0.05	1.2	1.2	>0.05

). The density of leaf stomata in Coast Live Oak trees also differed significantly with respect to surface perviousness, where stomatal density was greater on trees growing on pervious surfaces and smaller stomatal densities detected on trees growing on impervious surfaces (Table 1). However, both the leaf stomatal dispersion and the diversity of stomatal size classes in Coast Live Oak trees did not differ significantly with respect to surface perviousness (Table 1). Coast Live Oak trees growing on both pervious and impervious surfaces showed a clumped distribution pattern of leaf stomata (Table 1). In Camphor trees, leaf stomatal length, density, dispersion, and diversity of class sizes did not differ significantly with respect to surface perviousness (Table 1). Camphor trees growing on both pervious and impervious surfaces showed a clumped distribution pattern of leaf stomata (Table 1).

In Olive trees, leaf stomatal length, dispersion, and diversity of class sizes did not differ significantly with respect to surface perviousness (Table 1). However, the density of leaf stomata in Olive trees differed significantly with respect to surface perviousness, where stomatal density was greater on trees growing on pervious surfaces and smaller stomatal densities detected on trees growing on impervious surfaces (Table 1). Olive trees growing on both pervious and impervious surfaces showed a clumped distribution pattern of leaf stomata (Table 1). In Carrotwood trees, the leaf stomatal length, density, dispersion, and diversity of class sizes in Carrotwood trees did not differ significantly with respect to surface perviousness (Table 1). Carrotwood trees growing on both pervious and impervious surfaces showed a clumped distribution pattern of leaf stomata (Table 1).

4. Discussion

Camphor trees (C. officinarum) and Carrotwood trees (C. anacardioides) growing at sites with impervious and pervious surfaces did not show significant differences in terms of stomatal length, stomatal density, dispersion pattern of stomata, or diversity of stomatal sizes. However, both Coast Live Oak trees (Q. agrifolia) and Olive trees (O. europaea) growing at sites with impervious and pervious surfaces showed significant differences in leaf stomatal length as well as stomatal density (Table 1). Cost Live Oak trees growing on pervious surfaces had significantly shorter-length stomata at higher densities, while trees growing on impervious surfaces had significantly longer-length stomata at lower densities (Table 1). Olive trees growing on pervious surfaces had stomata at significantly higher densities relative to trees growing on impervious surfaces (Table 1).

Anthropogenic characteristics, such as vehicle emissions, industrial activity, power generation facilities, residential and commercial energy consumption, soil degradation, plant community diversity, and the overall form of the urban landscape and urbanization stage of green spaces, can all contribute to the spatiotemporal variability of CO₂ levels in urban environments [38,39]. While increased CO₂ concentrations have the potential to enhance plant productivity in urban settings, it is important to note that the carbon fertilization effect is globally constrained by limitations in soil water availability and nutrient accessibility [43]. This suggests that the response of urban vegetation to differential CO₂ levels may vary depending on the local environmental conditions [44]. To minimize the impact of spatiotemporal variations of CO₂ across complex urban landscapes, we selected sympatric sampling locations within a distance of less than 800 m from each other, ensuring a higher degree of homogeneity in terms of urban environmental characteristics [45]. The consistency of air quality indices across the region encompassing our sampling locations, coupled with the same residential zone designation by the city of La Verne, further suggests that our sampling design minimized the potential impact of CO₂ variability, allowing for a preliminary investigation into the role of soil permeability on the stomatal dynamics of urban tree species.

Surface imperviousness interrupts water infiltration in soil, contributing directly to plant water stress [46], either by reducing water potential via dissolved contaminants [47] or limiting physiological processes key to plant water uptake [46], ultimately serving to limit plant productivity [48]. In natural landscapes, where soil permeability is geologically sustained, the productivity of exotic plant species is often outperformed by native plant species that are adapted to the conditions of indigenous soils [49]. However, our findings suggest that in the urban Chaparral landscapes of southern California, the photosynthetic traits of exotic tree species are less susceptible to surface permeability than are either native or floristically indigenous tree species. We propose a two-stage strategy in the mitigation of urban heat island effects by means of street trees: (1) when effects are pronounced, an early-to-intermediate mitigation strategy that relies on exotic tree species less susceptible to contemporary impervious surfaces, and (2) when effects become less pronounced, a late mitigation strategy that introduces native tree species that persist optimally in improved conditions of soil permeability.

For said two-stage strategy to work, it is imperative that urban development be informed by community improvement planning rooted in environmental principles, rather than the inverse [50,51]. Data-informed management strategies play a pivotal role in integrating biological principles into sustainable urban development practices [52,53]. By leveraging biological data and insights, urban planners and policymakers can adopt a data-driven approach that integrates system-level principles, such as habitat conservation, ecological connectivity, and sustainable resource management, into urban development practices [50,54]. By embracing sustainability initiatives as systems-level thinking (i.e., adopting a holistic perspective), decision-makers can identify synergies and trade-offs between different sustainability goals, striving for optimal solutions that simultaneously benefit multiple dimensions [52,54]. The ultimate goal of sustainability initiatives is to create cities that not only provide a high quality of life for residents but also contribute to the preservation and conservation of diverse ecosystem functions across landscape mosaics of biologically rich complexity [55].

There is support in the primary literature that ecosystem services in urban environments may be sustained by both exotic and native tree species, with perhaps the notable exception of cultural heritage services that are better documented for native tree species [56,57]. Furthermore, we propose that future studies evaluate the scale of how differential temperature measurements contribute to a given urban heat island effect, to better determine a timeline for transitioning from a street tree population composed of exotic tree species to one composed of more native species. For example, while there is evidence that small cities may be the most susceptible to urban heat island effects, the factors contributing to its intensity remain poorly understood [58,59]. While traditional explorations have championed canopy characteristics, such as leaf area index [58,60] and density [61], there is growing research on multi-species considerations of canopy identity [48] that better encourage recombinant ecologies [1] as an exciting new research direction for consideration in urban environments.

5. Conclusions

Camphor trees and Carrotwood trees exhibited no significant differences in stomatal characteristics between impervious and pervious surfaces. However, Coast Live Oak trees on pervious surfaces had shorter stomata at higher densities, while those on impervious surfaces had longer stomata at lower densities. Olive trees on pervious surfaces showed higher stomatal densities compared to those on impervious surfaces. Surface imperviousness has a direct impact on water infiltration, leading to increased plant water stress and reduced productivity, while also contributing to urban heat island effects. Our findings suggest that in urban Chaparral landscapes, exotic tree species appear less affected by surface permeability than native or floristically indigenous species. We propose a two-stage strategy for mitigating urban heat island effects using street trees, starting with less susceptible exotic species and transitioning to native species as impervious surfaces diminish across a given urban environment. Future research studies should further explore recombinant ecologies and communities as means to drive innovative sustainability solutions that integrate system-level approaches to effectively address environmental challenges in urban environments.