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Article

Differences in Tolerance of Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ to Environmental Stress in the First Year After Planting in Urban Conditions

by
Marek Kościesza
,
Mateusz Korbik
,
Agata Jędrzejuk
,
Tatiana Swoczyna
* and
Piotr Latocha
Department of Environmental Protection and Dendrology, Institute of Horticultural Sciences, Warsaw University of Life Sciences—SGGW, Nowoursynowska 159, 02-776 Warszawa, Poland
*
Author to whom correspondence should be addressed.
Forests 2025, 16(2), 277; https://doi.org/10.3390/f16020277
Submission received: 21 December 2024 / Revised: 23 January 2025 / Accepted: 1 February 2025 / Published: 6 February 2025
(This article belongs to the Section Urban Forestry)
Browse Figures
Versions Notes

Abstract

:
The success of establishing new trees in cities and their subsequent growth depend, among others, on the proper selection of tree species which can easily tolerate the post-planting stress. In the spring of 2023, young Italian alder (Alnus cordata (Loisel.) Duby) and common lime (Tilia × europaea L. ‘Pallida’) trees were planted in a street of heavy traffic in Warsaw. In the summer of 2023, leaf samples were collected during the growing season for chlorophyll a fluorescence measurements and chemical analyses. Additionally, the autumn phenological phases were monitored. Chlorophyll a fluorescence measurements revealed higher values of Fv/Fm, density of reaction centers per cross-section, and electron transport chain efficiency between photosystems II and I, as well as lower energy dissipation rate per active reaction center of photosystem II in A. cordata. Moreover, A. cordata revealed higher chlorophyll a, chlorophyll b, and carotenoid content. The flavonoid and proline content in both species was the highest by the end of July and then decreased. In T. × europea ‘Pallida’, the contents of these stress biomarkers increased in the late growing season. Our results showed that T. × europaea ‘Pallida’ is less resistant to post-planting stress in urban conditions, while A. cordata showed higher resistance to variable weather conditions, high photosynthetic efficiency, and long foliage lifespan.

1. Introduction

Urban trees provide a wide range of ecosystem services for city dwellers, including aesthetic and cultural value, recreational and social benefits, microclimatic influence on city environment, and air pollution reduction [1]. Particularly, urban trees play a key role in the mitigation of climate change consequences in highly urbanized areas by providing protection from droughts and heat waves, as well as cooling and humidifying the air [2,3]. The recent COVID-19 pandemic experience additionally underlined the value of urban trees and forests [4]. In line with the EU Biodiversity Strategy for 2030 [5], planting trees in cities is one of the priority activities in the nearest future. In Poland and other European countries, tree planting is included in cities’ strategies for adaptation to climate change [6,7].
On the other hand, urban trees are often forced to grow in harsh habitat conditions. Except for parks and natural areas included within city areas, urban sites are mainly characterized by soil compaction and pollution, unbalanced nutrient supply, and restricted soil volume, which hampers proper water accumulation. Moreover, increased vapor pressure deficits in urban atmospheres and high wind speed along building facades and streets lead to higher water demand for normal water balance in trees [8,9]. Air and soil pollution are additional factors that affect trees’ physiology [10,11]. In consequence, tree lifespans in cities are shorter than in natural landscapes. The mortality of trees is the highest in the first years after planting [12,13]. According to Roman et al. [14], tree mortality in the first season after planting may reach 25%. The annual mortality of newly planted urban trees, in some cases, can reach up to 70% [15]. The increasing awareness of the importance of urban greenery and social pressure mobilize city authorities to increase expenditure for tree planting, although public funds must be spent in a way that determines success. Thus, along with improved conditions for planting and further maintenance, the proper selection of tree species is expected to ensure the long-term survival of the planted trees [16,17].
Planted tree species differ in mortality rates [18,19]. According to [14], climate-appropriate species selection influenced urban tree survival during the establishment phase in Sacramento. Wattenhofer and Johnson [13] found that taxa “whose (adjusted) average mortality remained under 10%” were mostly tolerant to “a wide range of soil moisture types”. However, “they prefer moist, well-drained soils, they are also tolerant of both drier soils as well as occasionally flooded soils”. On the other hand, Stratópoulos et al. [20] proved that species originating from drier habitats are able to maintain fully functional (green) foliage under lower volumetric soil water content. Species that cope better with drought stress may experience less disruption of critical physiological processes such as growth, photosynthesis, and transpiration [21,22,23]. Species resistance to drought and heat stress makes it possible to maintain good health conditions during heat waves in city centers, which are known as urban heat islands [24]. Drought stress in the city is associated with frequent drought in the soil and drought in the air (high vapor pressure deficit, VPD) [3,19,25]. One of the basic challenges for young trees is the ability to survive physiological drought in the first years after planting, which is related to the restoration of the root system and its proper development after planting [26]. Trees obtained from nurseries often have reduced root system, particularly when delivered B&B (field-grown root-ball excavated and burlap-wrapped) [27]. Such damage has significant impacts on physiological conditions and the growth of trees [28,29,30,31]. Stress experienced in this initial period may shorten the vegetation period, which leads the weakening of the conditions, excessive depletion of reserves, and unctioning of the trees in the following years. As Else et al. [30] found, the degree of regeneration of the root system translates into the overall condition of newly planted trees, which may be reflected in the condition of the photosynthetic apparatus.
Photosynthesis is a process that is sensitive to environmental stress [32,33] on the structural, functional, and gene-expressing level. Thus, tracking the phenomena and biochemistry related to photosynthesis makes it possible to find out whether plants are experiencing stress in the conditions in which they grow [19,34]. Numerous papers show the depletion of CO2 assimilation in the face of stress related to impaired root function, i.e., the uptake of water, soil salinity and nutrients, i.e., drought stress and nutrient deficiency [35,36,37,38]. Likewise, the photosynthetic efficiency of photosystems in chloroplasts estimated using the chlorophyll a fluorescence technique is affected by environmental stress [39,40,41]. The technique of prompt chlorophyll a fluorescence allows for rapid and non-invasive measurements of the signal from photosynthesizing samples, which describe energy fluxes occurring inside and around the reaction centers (RCs) of photosystem II units localized in chloroplasts [42]. Portable fluorimeters of high-time resolution measurements (with intervals of 10 μs) provide a dataset for plotting a fluorescence transient which, when shown on a logarithmic time scale, is called a fast (or prompt) fluorescence curve [43]. This curve with visible points marked as O, (K), J, I, and P makes it possible to calculate numerous parameters reflecting particular phenomena of light absorption and their conversion to biochemical energy [44,45].
Drought stress and root system dysfunctions can also affect photosynthetic pigment content [46,47]. Thus, chlorophyll (a and b) and carotenoid contents are used for stress detection in drought-treated trees [48,49]. Although chlorophyll content is usually associated with nitrogen nutrition [50], leaf senescence also leads to chlorophyll degradation [51]. The fate of carotenoids is different both in stressed and senescing leaves, and their content may slightly increase or stay at the same level; in case of stress, they play a key role in protection against reactive oxygen species formation [52]. Likewise, flavonoids play a protective role in plant tissues [53]; in case of drought, UV-B radiation, or cold or salinity stress, increased flavonoid content, e.g., rutin, makes it possible to scavenge ROS, and it serves as a UV screen and controller of cellular ionic homeostasis [54,55,56,57]. There are numerous other compounds that allow plants to maintain chemical homeostasis and water balance in the face of stress. Proline is an amino acid and highly soluble organic compound of low molecular weight, providing protection to plants from stress by contributing to cellular osmotic adjustment. Additionally, proline supports the protection of membrane integrity, ROS detoxification, and enzyme/protein stabilization [58]. Its concentration increases in the case of drought stress [59]. Recently, proline content has also been used for stress detection in urban trees [60]. Increased ammonium concentration under drought stress was also observed [61]. Ammonium is a basic inorganic nitrogen-bearing compound necessary for metabolic processes, but at high concentrations, it induces toxic effects. Recent papers show that ammonium also serves as a signaling molecule [62].
Finally, the disturbed duration of the vegetation period reflects the health condition of trees growing in situ [63]. Early senescence of leaves is a common response to drought stress [64]. For numerous species, premature leaf senescence triggered by drought makes it possible to avoid excess transpiration and to maintain favorable water balance in the whole plant [20,64]. Moreover, in species that adopt such a strategy, controlled leaf senescence enables the remobilization of nutrients. However, in the face of severe stress, premature leaf dropping can contribute to diminish the resources necessary for recovery and may lead to further tree dieback [65].
Taking into account species selection for urban planting, in the past, decisions were made about the species and cultivars used traditionally [66]. One of them is Tilia × europaea L. ‘Pallida’, which is a classic tree taxon for streets, boulevards, and other representative public spaces. Tilia × europaea, known also as Tilia × vulgaris Hayne, is a hybrid of T. platyphyllos Scop. and T. cordata Mill. It occurs naturally in scattered localities in Europe [67]. The most popular clone ‘Pallida’ (called also ‘Koningslinde’ or ‘Kaiserlinde’) has been widely used in Europe since the seventeen century because of its regular shape and the ease of production [67,68]. Recently, the awareness of difficult urban conditions for tree growth and climate change force researchers and decision makers to search for species that can cope with new challenges. One of the promising species for Central Europe cities is Alnus cordata (Loisel.) Duby, which is a species originating from Italy and Corsica [69]. It is less dependent on riparian habitats than other alders and is considered to be more tolerant to drought stress [70]. Tognetti and Borghetti [71] found that A. cordata shows low level of xylem embolism throughout the summer. As a native European species, it does not raise any controversy regarding invasiveness, contrary to species originating from North America or the Far East.
To our knowledge, although there are numerous papers discussing the possible physiological causes of dieback of newly planted trees, there is still a gap in the research on the physiological and biochemical reactions of such trees during the initial post-planting period. The aim of our study was to assess the early response of two taxa recommended for urban plantings to transplanting stress in urban environment. We compared Alnus cordata and Tilia × europaea ‘Pallida’, which is a commonly planted cultivar of Tilia in European cities. The first species was planted in Poland for only a few years. We analyzed the timing of leaf senescence, photosynthetic efficiency, and contents of photosynthetic pigments, which represent the crucial traits for the sugar production necessary for growth and regeneration in newly planted trees. We also used biochemical markers like ammonium concentration in leaf tissues and the contents of protective compounds that reduce oxidative stress (flavonoids) and water stress at the cell level (proline).

2. Materials and Methods

2.1. Site Location and Climatic Conditions

The experiment was carried out in the southern district of Warsaw, Poland, (52°10′32.56″ N, 21°02′39.50″ E, 98 m asl) along an arterial road of heavy traffic (Al. Gen. W. Sikorskiego) (Figure 1). Examined trees were planted in four rows on the interlane lawn strip.
Meteorological data, i.e., mean daily temperature and daily precipitation, were obtained from the Department of Hydrology, Meteorology, and Water Management, Warsaw University of Life Science—SGGW (WULS). Due to technical failure, the dataset from June was not available. Thus, mean daily temperatures and precipitation were obtained from Meteo Station of the Warsaw University of Life Sciences (SGGW), Energy Management Department (Source: SGGW Warszawa, sggw.meteo.waw.pl, 52°09′37″ N, 21°03′11″ E, 100 m asl) and Meteo Station Warsaw (Source: meteo.waw.pl, 52°10′53″ N, 20°52′13″ E, 110 m asl)), respectively. WULS sources were located ca. 2000 m away from experimental site (Figure 1).

2.2. Plant Material

B&B trees of trunk circumference 16–18 cm at 100 cm, obtained from commercial nurseries, were planted on 24–26 April 2023 (T. × europaea ‘Pallida’) and 5–6 April 2023 (A. cordata). A total of 48 specimens of each taxon were planted randomly in a spacing of 3.0 × 3.5 m. Tree pits were filled with standard soil mixture due to the standard planting procedures used by the Warsaw Municipal Greenspace Authority. After planting, each tree was stabilized using three wooden stakes. The trunks were whitewashed, mulching was applied, and each tree was watered with a minimum of 60 L of water. During drought periods, all the trees were watered twice a week with an amount of 50 L per tree.

2.3. Chlorophyll a Fluorescence

Fluorescence measurements were done on 24 trees of each species. Leaf samples (1 fully expanded leaf per tree) were collected in the morning before 10:00 a.m. five times during the summer of 2023: on 15 June, 4 and 22 July, 19 August, and 8 September (on the 166, 185, 203, 231, and 251 day of the year—DOY—respectively), as the weather was stable following at least 2 days without raining (except 19 August). Leaves were collected from the shaded part of a crown (if possible) and transported to the laboratory in paper bags placed in a plastic bag in order to avoid both photoinhibition and severe dehydration. Measurements of chlorophyll a fluorescence were performed within 2 h using HandyPEA fluorimeter (Hansatech Instruments Ltd., King’s Lynn, Norfolk, UK). Leaves were dark-adapted using light-excluding clips for 30 min. Then, dark-adapted leaf samples of 4 mm diameter (cross-section area) within each clip were illuminated with 660 nm light of 3444 μmol (photon) m–2 s−1. The following chlorophyll a fluorescence parameters were analyzed: maximum quantum efficiency of photosystem II (Fv/Fm), probability that a trapped exciton moves an electron into the electron transport chain beyond the primary acceptor QA (ψEo), the concentration of active reaction centers in the tested cross-section (RC/CS0), energy dissipation expressed per active reaction center (DI0/RC), the ratio of variable fluorescence at 300 μs to variable fluorescence at 2 ms showing limitations in the donor side (at oxygen-evolving complex) of photosystem II (VK/VJ), and an integrative parameter Performance Index on absorption basis (PIABS) [42,43]. A graphical description of the analyzed parameters is shown in Figure 2.

2.4. Chemical Analyses

Chemical analyses were done on 48 trees of each species (1 fully expanded leaf per tree). Leaf samples were collected on the same days as for chlorophyll a fluorescence method (the leaves used for ChF were also included), except 15 June when the foliage in the tree crowns was too sparse. Flavonoid (Flv) content in the samples from 4 July was not determined due to technical reasons. The sampled material was divided into 12 replications performed for each species for each sampling date. The samples were frozen and kept below −18 °C and analyzed in the next months.
Chlorophyll (Chl) a, b, and carotenoid (Car) contents were quantified following the method of Lichtenthaler and Wellburn [72]. Samples of 0.5 g of leaves (frozen fresh material) were ground in 50 mL of 80% acetone for 40 s. The suspension was filtered, and the absorbance was determined at the wavelengths 470, 646, 652, and 663 nm.
Absorption coefficients of chlorophylls a (Ca) and b (Cb) were calculated as follows:
Ca = 12.21 × Abs663 − 2.81 × Abs646
Cb = 20.13 × Abs646 − 5.03 × Abs663
Chlorophyll pigments concentrations (mg g−1 FW) were calculated as follows:
Chlorophyll a = (12.21 × Abs663 − 2.81 × Abs646) × 50/1000 × 0.5
Chlorophyll b = (20.13 × Abs646 − 5.03 × Abs663) × 50/1000 × 0.5
The sum of carotenoid (xanthophylls + β-carotene; x + c) concentrations (μg g−1 FW) were calculated as follows:
Carotenoids = Carx+c × 50/1000 × 0.5, where
Carx+c = (1000 × Abs470 − 3.27 × Ca − 104 × Cb)/229
For Flv determination, the procedure by Eom et al. [73] was used. Frozen 0.5 g leaf samples were homogenized in 5 mL 80% methanol and filtered. An aliquot of 0.5 mL of sample was mixed with 0.1 mL of 10% aluminum chloride and 0.1 mL of potassium acetate (1 M). In this mixture, 4.3 mL of 80% methanol was added to make 5 mL volume. Finally, 2 mL of NaOH (1 mM mL−1) and distilled water were added to obtain a total volume of 10 mL. The absorbance was measured spectrophotometrically at 510 nm. The Flv content was determined based on a standard curve of rutin (mg(rutin) g−1 FW).
Flavonoid concentration (mg g−1 FW) was calculated as follows:
Flv = Abs510 × 0.256 × FW
where 0.256 is the proportion resulting from the standard curve for rutin.
Determination of proline (Pro) was performed according to Bates et al. [74]. An amount of 0.5 g of plant tissue was triturated in 10 mL sulfosalicylic acid 3%. After being filtered, 1 mL of the supernatant was added to 1 mL sulfosalicylic acid 3% and 1 mL of glacial acetic acid (AcAc). The resulting mixture was subjected to thermal treatment at 100 °C for 1 h. After the heat treatment, the solution was left to cool to room temperature, after which it was placed in an ice bath. Then, the mixture was added to 2 mL toluene, mixed, and afterward left to separate into two fractions. A toluene extract was used for the measurements of absorbance at 520 nm.
Proline content was calculated based on standard regression curve:
Pro = [(Abs520 × Ve/0.5)/Vp]/FW
where 0.5 is a value obtained from toluene standard regression curve, where we include the following values:
  • Ve—extract volume (10 mL);
  • Vp—sample volume used for spectrophotometric analysis.
Determination of ammonium was performed by the Berthelot reaction modified according to Weatherburn [75], as described by Lin and Kao [76]. Frozen 0.5 g leaf samples were homogenized in 3 mL 0.3 mM sulfuric acid (pH 3.5). The homogenate was filtered, and 200 μL of clear supernatant was diluted by 3.8 mL 0.3 mM sulfuric acid (to a final volume of 4 mL). Afterwards, 0.5 mL of solution A (25 mg nitroprusside and 5 g phenol dissolved in 100 mL water) and 0.5 mL of solution B (2.5 g NaOH and 40 mL 5% NaOCl were mixed, and then a final volume was made up to 100 mL using distilled water) were added. The mixture was incubated with gentle shaking in a water bath at 37 °C for 20 min. The absorbance was measured at 625 nm against the control without extract. Ammonium levels were calculated using an extinction coefficient of 3.9982 μmol– 1 cm– 1 and expressed as μmol g−1 fresh weight. For all the chemical analyses, the absorbance was determined using a spectrophotometer Aoelab UV-VIS UV1600 (AOE Instruments, Shanghai, China).

2.5. Phenological Observations

As the trees were planted in the spring, phenological phases of leaf development were not analyzed. Phenological observations were carried out on 24 trees of each species twice a week since 23 August (235 DOY) and continued until the first ground frost on 18 November (322 DOY). Observations were conducted visually. The BBCH (Biologische Bundesanstalt, Bundessortenamt and Chemical Industry) scale was adopted according to Bleiholder et al. [77] and modifications by Finn et al. [78] for woody plants. The following stages were compared:
  • BBCH 92—beginning of leaf discoloration (when 10% of leaves turned yellow);
  • BBCH 94—full leaf discoloration (50% of leaves turned yellow);
  • BBCH 93—beginning of leaf fall (10% of leaves had dropped);
  • BBCH 95—full leaf fall (50% of leaves had dropped);
  • BBCH 97—end of leaf fall (100% or nearly 100% of leaves had dropped).
The percentage of discolored/fallen leaves in each specimen was assessed individually. Thus, we obtained a set of data enabling statistical analysis. Based on the collected data, the lengths of autumn phases were determined.

2.6. Statistical Analysis

Since most variables were non-normally distributed, non-parametric tests were used for the assessment of significant differences between both species and measurement dates. Two species were compared using Mann–Whitney U test, Kruskal–Wallis test, and Dunn–Bonferroni post hoc test were performed for comparison between dates using STATISTICA version 13.0 software (TIBCO Software Inc., Santa Clara, CA, USA).

3. Results

3.1. Weather Conditions

The precipitation in June was exceptionally low, only 34.6 mm in total, while in May and July, 53.1 and 63.5 mm, respectively, were measured. Moreover, the rainfall was unevenly distributed, resulting in 19 days without precipitation prior to 13 June (personal information). All sampling dates followed sunny days except for 19 August (231 DOY) (Figure 3). The total monthly precipitation in August was 106.1 mm, while in September, it was only 18.7 mm, and the dry period lasted until the middle of October.

3.2. Chlorophyll a Fluorescence

All ChF parameters were more favorable in A. cordata (Figure 4). This species showed higher values of RC/CS0, Fv/Fm, ψEo, and, consequently, PIABS. Lower rates of dissipation per active reaction center confirm the overall higher efficiency of PSII, and the lower values of VK/VJ indicate a high efficiency of electron donation from water splitting complex in A. cordata. In both species, the Fv/Fm values were lower in June, and in T. × europaea ‘Pallida’, this parameter also decreased in September. The similar trend in T. × europaea ‘Pallida’ was also found in the case of ψEo and PIABS, where unfavorable DI0/RC results (higher values) in June and September reflected this pattern. On the contrary, A. cordata, after initial weakening, showed more or less stable values of most of the parameters.

3.3. Chemical Analyses

A. cordata showed higher concentrations of photosynthetic pigments (chlorophyll a, b, and carotenoids) in leaves than T. × europaea ‘Pallida’ throughout the entire growing season (Figure 5A–C). The Chl a content in both species decreased toward the end of the growing season, while the Chl b content decreased only in T. × europaea ‘Pallida’. The Flv content increased in T. × europaea ‘Pallida’ in the second part of the growing season, and on the contrary, it decreased in A. cordata in that time (Figure 5D). Likewise, the Pro content decreased in A. cordata during the end of the second half of the growing season (Figure 5E). Both of these stress biomarkers showed visible shifts on 22 July (203 DOY) in T. × europaea ‘Pallida’ and A. cordata compared to the preceding and following sampling dates. The ammonium content was higher in T. × europaea ‘Pallida’ than in A. cordata in July, but it decreased on the last sampling day. In A. cordata, the ammonium content increased gradually toward the end of the growing season (Figure 5F).

3.4. Autumn Phenology

Autumn phenological phases in T. × europaea ‘Pallida’ occurred earlier than in A. cordata. The differences were significant for all phases (Figure 6). The first symptoms of leaf discoloration were found in T. × europaea ‘Pallida’ in August, but in September, this phase was observed in all trees. In October, 50% of the leaves turned yellow (BBCH 94 median = 283 DOY, 10 October). Complete leaf fall in T. × europaea ‘Pallida’ occurred on 28 October (BBCH 97 median = 301 DOY). The A. cordata samples kept most of their leaves green. Thus, full leaf discoloration (50% of leaves turned yellow) was not observed. The first ground frost occurred on 18 November (322 DOY), and following that date, the observations were not continued. The beginning of leaf fall in A. cordata occurred significantly later than in T. × europaea ‘Pallida’, with medians = 298 and 290, respectively. Full leaf fall (50% of leaves dropped, BBCH 95) was also later in A. cordata compared to T. × europaea ‘Pallida’, with medians = 310 and 297, respectively.

4. Discussion

The first year of growth of newly planted trees is particularly difficult [79]. So-called transplant shock is evoked by changes in the root system structure disrupting the balance between above- and below-ground biomass [80]. The examined trees were delivered as B&B, so we expected that the root system might be reduced when excavated in a nursery [27]. The partial loss of fine roots restricts water and mineral nutrient absorption from the soil. The additional loss of coarse roots, which store carbohydrates and nutrients (e.g., nitrogen), limits these resources for the restoration of lost organs. Restricted growth and photosynthetic activity in newly planted trees are usually considered as consequences of difficulties in water uptake by the root system [26,81]. On the other hand, the photosynthetic activity of plants (trees) is a key process determining sugar production for regeneration. Photosynthesis is a process that is highly susceptible to environmental stress. It may be impeded not only by water deficit but also by thermal stress and excess or limited light.
The examined trees were planted on the interlane lawn strip between two road lanes with heavy traffic. They experienced full sun, high summer temperatures, and gusts of winds, which additionally increase transpiration [82] and the water demand of the trees. These habitat conditions are difficult for newly planted individuals. A loss of vitality or poor physiological performance in young trees after transplanting was noted in forest and urban trees [22,83]. In this context, the results obtained from the chlorophyll a fluorescence measurements in our research indicate satisfying results. The most commonly used parameter, i.e., Fv/Fm, showed values exceeding 0.83 for most sampling dates, which is usually considered to be optimum [84]. However, a marked decrease in the Fv/Fm value was found in June, which can be attributed to unfavorably dry weather conditions earlier that month. This drought stress was also reflected by the other parameters, ψEo—an indicator of electron transport efficiency between PSII and PSI—and PIABS. The decrease in ψEo and PIABS values occurs when trees are affected by drought and thermal stress [85,86]. Thus, they are good biomarkers of abiotic stress when any drought or high-temperature effects are expected. Nevertheless, in the A. cordata samples, all ChF parameters were more favorable, reflecting a higher photosynthetic efficiency of PSII in this species. Higher maximum quantum efficiency, ψEo, PIABS, and proportion of active reaction centers per cross-section measurements in A. cordata compared to T. × europaea ‘Pallida’ were noted throughout the entire growing season. Likewise, lower values of VK/VJ, indicating a more favorable performance of the oxygen-evolving complex and lower rates of DI0/RC, confirmed an overall higher potential of A. cordata for high photosynthetic activity. The dissipation per active reaction center is a sensitive indicator of drought stress, but the appearance of a K-band in the fluorescence transient, expressed numerically by the VK/VJ ratio, may also show constraints connected with drought stress [87]. In many papers, these parameters were useful for assessing the resistance of species or cultivars to water deficiency [39,88]. Significant differences between the examined species in terms of the proportion of active reaction centers per cross-section (RC/CS0) were confirmed by the results of the photosynthetic pigment analysis. The chlorophyll a, b, and carotenoid contents were significantly higher in A. cordata regardless of the sampling date. Such results suggest that A. cordata can better withstand urban conditions than T. × europaea ‘Pallida’ or better adapt to a new habitat after transplanting. However, the differences can also be bound to specific ecophysiological traits of examined species [89,90,91,92]. Giri et al. [90] found that the chlorophyll a content in four species varied in the range of 1.65–2.71 mg g−1 DW, while the carotenoid content varied in the range of 0.32–1.22 mg g−1. Taking into account that chlorophyll contents are closely bound to photosynthetic capacity in trees, A. cordata seems to have a better potential to provide regulating ecosystem services [92].
Deciduous trees experience changes in their photosynthetic pigment concentrations during the last phase of the growing season due to the degradation of chlorophyll and fluctuations in carotenoid amounts [93,94,95]. In the initial phase of senescing, carotenoids play an important role in photoprotection in the face of chlorophylls’ decomposition, and they remain decomposed for some time [93], but finally, their concentrations are also affected by senescing [96,97]. The photosynthetic pigments and physiological parameters in A. cordata were not affected by the late phase of the growing season. In fact, leaf discoloration and senescence were not observed in this species, which can be attributed to specific traits of A. cordata, i.e., the ability of its leaves to remain green after the first frosts of winter [69]. In T. × europaea ‘Pallida’, the contents of chlorophyll a and the carotenoids slightly but not significantly decreased in early September compared to the middle of August, and only the chlorophyll b content significantly decreased in the late growing season. Scattolin et al. [98] showed that chlorophyll degradation can be the first symptom of further typical tree decline symptoms: defoliation, discolored leaves, canopy transparency, the presence of epicormic twigs, and the presence of dead branches. In our study, the gradual decrease in chlorophylls in T. × europaea ‘Pallida’ during the growing season could have been evoked by difficulties connected with transplant shock [99]. Similarly, the photosynthetic efficiency (expressed in maximum quantum efficiency and dissipation rate per active reaction center of PSII) was markedly restricted on the last day of sampling. On the contrary, neither the VK/VJ nor RC/CS0 values were changed significantly on that day in the T. × europaea ‘Pallida’ samples. We must note that leaf samplings taken for ChF measurements and chemical analyses were still green and showed no visible damage, so our results reflect some particular changes in physiology and biochemistry before visible symptoms of yellowing.
Increased DI0/RC values in T. × europaea ‘Pallida’ in early September were reflected by shifted flavonoid contents. However, the increase in flavonoids in T. × europaea ‘Pallida’ had been occurring since the second half of July. On the contrary, in A. cordata, the flavonoid content decreased during August and September. As increased flavonoid production is typically connected with drought stress [56,100], our findings show that T. × europaea ‘Pallida’ was forced to cope with growth conditions not favorable for this species. Proline accumulation tended to be similar in both species throughout the growing season: a marked shift was visible on 22 July (203 DOY). However, some differences can be found on 4 July (185 DOY), when T. × europaea ‘Pallida’ samples revealed lower proline contents, and on 8 September (231 DOY), while its leaves had higher proline concentrations. This confirms that T. × europaea ‘Pallida’ activates various mechanisms to manage environmental stress. According to Czaja et al. [101], T. × europaea ‘Pallida’, compared to Tilia cordata Mill. and Tilia tomentosa Moench., is more susceptible to drought stress. In the face of stress caused by transplanting, in the leaf tissues of T. × europaea ‘Pallida’, there were activated processes that allowed the trees to avoid both oxidative and osmotic stress.
Ammonium serves as a compound necessary for metabolic processes, including amino acids formation, but it may also play a role as a signaling molecule [57]. Some papers indicate that higher NH3/NH4+ concentrations trigger higher proline accumulation so that proline formation may also facilitate utilizing excess ammonia molecules [102,103,104]. Increased ammonium concentration may occur under drought stress [61]. Thus, we have used this compound as an additional indicator of stress. Our results showed increased ammonium concentrations in T. × europaea ‘Pallida’ samples in July but decreased concentrations toward September. The opposite trend was observed in A. cordata, where the lowest values were found in early July, while the highest values were found in the late growing season. The differences may be caused by specific properties of the Alnus genus, including root-associated bacterial communities. We did not sample roots from the examined trees in order to detect any possible interaction between the trees and their biome. Still, there is widely known evidence of bacterial communities settled in Alnus tissues that facilitate nutrient supply. Recently, Aslani et al. [105] found 3694 so-called operational taxonomic units belonging to 36 bacterial phyla on the root tips of 19 Alnus species from all over the world. Thus, it is possible that young A. cordata trees might be supported by their microbiome and remain rich in N compounds until the end of the growing season.
The possible nitrogen supply provided by the microbiome could be responsible for the lack of autumn leaf discoloration and delayed defoliation of A. cordata in our experiment. The first ground frost occurred on 18 November (322 DOY), and until this date, most of the A. cordata leaves remained green. This means that species-specific traits combined with proper tree maintenance enabled the particularly high longevity of A. cordata foliage despite transplanting. The first symptoms of leaf discoloration in T. × europaea ‘Pallida’ were found in August, in September, and October where 50% discoloration was observed (median = 283, 10 October). Complete leaf fall occurred on 28 October (301 DOY), which is not typical, as in Poland, the leaf fall in most trees, including Tilia species, lasts until at least mid-November. The acceleration of autumn leaf senescence in urban environments can be attributed to limited water intake bound to higher VPD [20] or restricted water availability due to soil contamination with deicing salts [106]. Therefore, such behavior of young T. × europaea ‘Pallida’ trees suggests that their survival under unfavorable growing conditions is supported by premature leaf senescence [64].

5. Conclusions

In order to achieve expected results in greening the cities, human efforts should be focused on proper tree maintenance, particularly young trees, and appropriate species selection. Our results showed that Alnus cordata is a valuable species for urban plantings due to its resistance to variable temperature and precipitation conditions, high photosynthetic efficiency, and long foliage lifespan. Compared to commonly planted Tilia × europaea ‘Pallida’, A. cordata seems to have a better potential to provide regulating ecosystem services. Nevertheless, T. × europaea ‘Pallida’, which is widely spread in European cities, may also be still appropriate due to its various physiological mechanisms, which help to withstand stressful periods. The chlorophyll a fluorescence method showed that when newly planted young trees are carefully cared for, this species is sufficiently resistant to prolonged photoinhibition and efficiently binds light energy for CO2 assimilation. Taking into account that tree species diversity supports total biodiversity in cities, it is worth using both species in urban plantings.

Author Contributions

Conceptualization, M.K. (Mateusz Korbik) and P.L.; methodology, A.J., T.S. and P.L.; software, M.K. (Marek Kościesza) and T.S.; validation, M.K. (Marek Kościesza), M.K. (Mateusz Korbik), A.J. and T.S.; formal analysis, M.K. (Mateusz Korbik) and M.K. (Marek Kościesza); investigation, M.K. (Mateusz Korbik) and M.K. (Marek Kościesza); resources, M.K. (Mateusz Korbik); data curation, M.K. (Mateusz Korbik) and M.K. (Marek Kościesza); writing—original draft preparation, M.K. (Marek Kościesza) and T.S.; writing—review and editing, T.S., M.K. (Mateusz Korbik), A.J. and P.L.; visualization, M.K. (Marek Kościesza) and T.S.; supervision, T.S. and P.L.; project administration, M.K. (Mateusz Korbik). All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author.

Acknowledgments

The examination site and plant material used for the experiment were supported by the Warsaw Municipal Greenspace Authority (Zarząd Zieleni M.St. Warszawy).

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Location of the experimental site and Meteo Stations (Warsaw University of Life Sciences—SGGW) (A). Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ trees in the experimental site, photo by T.S. (B).
Figure 1. Location of the experimental site and Meteo Stations (Warsaw University of Life Sciences—SGGW) (A). Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ trees in the experimental site, photo by T.S. (B).
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Figure 2. A simplified scheme of chlorophyll a fluorescence parameters. QA, plastoquinone A, a primary electron acceptor at PSII reaction center; RC/CS0, concentration of active reaction centers in a tested cross-section; DI0/RC, energy dissipation expressed per active reaction center; TR0/ABS = Fv/Fm, maximum quantum efficiency of primary photochemistry; ET0/TR0 = ψEo, probability that a trapped exciton moves an electron into the electron transport chain beyond the primary acceptor QA; PIABS, Performance Index on absorption basis; VK/VJ, an indicator of limitations in the donor side (at oxygen-evolving complex) of photosystem II. For details, see Strasser et al. [42].
Figure 2. A simplified scheme of chlorophyll a fluorescence parameters. QA, plastoquinone A, a primary electron acceptor at PSII reaction center; RC/CS0, concentration of active reaction centers in a tested cross-section; DI0/RC, energy dissipation expressed per active reaction center; TR0/ABS = Fv/Fm, maximum quantum efficiency of primary photochemistry; ET0/TR0 = ψEo, probability that a trapped exciton moves an electron into the electron transport chain beyond the primary acceptor QA; PIABS, Performance Index on absorption basis; VK/VJ, an indicator of limitations in the donor side (at oxygen-evolving complex) of photosystem II. For details, see Strasser et al. [42].
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Figure 3. Daily mean temperatures and precipitation in June–November 2023. Data source: Department of Hydrology, Meteorology, and Water Management, Warsaw University of Life Science—SGGW; https://sggw.meteo.waw.pl/, https://www.meteo.waw.pl/ (accessed on 17 January 2025). Gray vertical lines indicate dates of sample collection; mean daily temperature and sum of daily precipitation are shown.
Figure 3. Daily mean temperatures and precipitation in June–November 2023. Data source: Department of Hydrology, Meteorology, and Water Management, Warsaw University of Life Science—SGGW; https://sggw.meteo.waw.pl/, https://www.meteo.waw.pl/ (accessed on 17 January 2025). Gray vertical lines indicate dates of sample collection; mean daily temperature and sum of daily precipitation are shown.
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Figure 4. Selected chlorophyll a fluorescence parameters. Maximum quantum efficiency, Fv/Fm, shown in (A). Efficiency of total electron transport beyond QA, ψEo, shown in (B). Energy dissipation expressed per active reaction center, DI0/RC, shown in (C). Concentration of active reaction centers in the tested cross-section, RC/CS0, shown in (D). The ratio of variable fluorescence at 300 μs and variable fluorescence at 2 ms showing limitations in the donor side (at oxygen-evolving complex) of photosystem II, VK/VJ, shown in (E). Performance Index on absorption basis, PIABS, shown in (F) for Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks; significant differences between sampling dates within each species are indicated by letters (at p ≤ 0.05).
Figure 4. Selected chlorophyll a fluorescence parameters. Maximum quantum efficiency, Fv/Fm, shown in (A). Efficiency of total electron transport beyond QA, ψEo, shown in (B). Energy dissipation expressed per active reaction center, DI0/RC, shown in (C). Concentration of active reaction centers in the tested cross-section, RC/CS0, shown in (D). The ratio of variable fluorescence at 300 μs and variable fluorescence at 2 ms showing limitations in the donor side (at oxygen-evolving complex) of photosystem II, VK/VJ, shown in (E). Performance Index on absorption basis, PIABS, shown in (F) for Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks; significant differences between sampling dates within each species are indicated by letters (at p ≤ 0.05).
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Figure 5. Results of chemical analysis of leaves. Chlorophyll a (A), chlorophyll b (B), carotenoids (C), flavanols (D), proline (E), and ammonium content (F) in leaves of Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks, and significant differences between sampling dates within each species are indicated by letters (at p ≤ 0.05).
Figure 5. Results of chemical analysis of leaves. Chlorophyll a (A), chlorophyll b (B), carotenoids (C), flavanols (D), proline (E), and ammonium content (F) in leaves of Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks, and significant differences between sampling dates within each species are indicated by letters (at p ≤ 0.05).
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Figure 6. Timing of autumn phenophases in Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season: beginning of leaf discoloration (when 10% of leaves turned yellow) BBCH 92, full leaf discoloration (50% of leaves turned yellow) BBCH 94, beginning of leaf fall (10% of leaves dropped) BBCH 93, full leaf fall (50% of leaves dropped) BBCH 95, end of leaf fall (100% or nearly 100% of leaves dropped) BBCH 97. Days of the year, DOY. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks (at p ≤ 0.05).
Figure 6. Timing of autumn phenophases in Alnus cordata and Tilia × europaea ‘Pallida’ newly planted trees during the first growing season: beginning of leaf discoloration (when 10% of leaves turned yellow) BBCH 92, full leaf discoloration (50% of leaves turned yellow) BBCH 94, beginning of leaf fall (10% of leaves dropped) BBCH 93, full leaf fall (50% of leaves dropped) BBCH 95, end of leaf fall (100% or nearly 100% of leaves dropped) BBCH 97. Days of the year, DOY. Box–whisker plots with median and 25 and 75 percentiles (boxes) and values extending to 1.5 times the interquartile range (whiskers) shown. Significant differences between species are indicated by asterisks (at p ≤ 0.05).
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MDPI and ACS Style

Kościesza, M.; Korbik, M.; Jędrzejuk, A.; Swoczyna, T.; Latocha, P. Differences in Tolerance of Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ to Environmental Stress in the First Year After Planting in Urban Conditions. Forests 2025, 16, 277. https://doi.org/10.3390/f16020277

AMA Style

Kościesza M, Korbik M, Jędrzejuk A, Swoczyna T, Latocha P. Differences in Tolerance of Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ to Environmental Stress in the First Year After Planting in Urban Conditions. Forests. 2025; 16(2):277. https://doi.org/10.3390/f16020277

Chicago/Turabian Style

Kościesza, Marek, Mateusz Korbik, Agata Jędrzejuk, Tatiana Swoczyna, and Piotr Latocha. 2025. "Differences in Tolerance of Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ to Environmental Stress in the First Year After Planting in Urban Conditions" Forests 16, no. 2: 277. https://doi.org/10.3390/f16020277

APA Style

Kościesza, M., Korbik, M., Jędrzejuk, A., Swoczyna, T., & Latocha, P. (2025). Differences in Tolerance of Alnus cordata (Loisel.) Duby and Tilia × europaea L. ‘Pallida’ to Environmental Stress in the First Year After Planting in Urban Conditions. Forests, 16(2), 277. https://doi.org/10.3390/f16020277

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