Citizen Science to Investigate the Ecophysiological Responses of Mediterranean Shrubland Vegetation in an Urban Open-Air Laboratory


1. Introduction

Plant diversity plays a significant role in Mediterranean urban and suburban landscapes. Nowadays, it is well established that plant communities provide a multitude of ecosystem services that contribute to the overall liveability of urban environments [1,2]. In this context, it has been shown that the more biodiverse these communities are, the greater their contribution to ecosystem services [3,4]. Among these services, woody species can mitigate the urban heat island effect during the summer, improve air quality by removing particulate matter and gaseous pollutants, and enhance the aesthetic value of urban areas, as well as the restorative potential of green spaces [5,6]. Furthermore, many urban areas, including those recently developed, lack green spaces, resulting in environments that are unsuitable for wild flora and fauna, which contributes to an unhealthy environment for humans [7]. In this regard, urban parks, due to their proximity to city centres and ease of access, can be viewed as Open-Air Laboratories (OALs) where biodiversity and plant ecophysiology can be studied, with the assistance of visitors participating in citizen science activities [8,9]. Urban green spaces that maintain natural or semi-natural surfaces are particularly ideal for conducting such studies [10,11]. These areas are also referred to as “informal green spaces” and are recognised as providers of numerous ecosystem services, including the facilitation of educational activities [12].
Raising public awareness of environmental issues and the importance of biodiversity conservation among citizens is crucial, especially for children, who are tomorrow’s adults. Some authors have emphasised the significance of concepts such as the “extinction of experience” and the excess of virtual experiences that focus primarily on exotic species [13,14]. Engaging individuals, particularly schoolchildren, in hands-on, environment-related scientific research can be essential for making these topics more accessible and fostering a desire to learn more [15]. From this perspective, involving them in activities in OALs is an effective way to enhance their learning experience [16,17]. Citizen science is regarded as a powerful means of implementing initiatives aimed at biodiversity conservation [18] and has the potential to contribute to the United Nations’ Sustainable Development Goals [19], as well as to help reduce inequality [20]. Furthermore, identifying locations that are both easily accessible and sufficiently safe for schoolchildren, along with providing plant species suitable for an OAL, is a significant milestone in enhancing the general public’s environmental awareness and knowledge. Cities, particularly urban natural and semi-natural areas, can serve as laboratories for studying and evaluating the effectiveness of Nature-based Solutions (NbS), which seek to utilise native wild plant species for urban green infrastructures [21].
The Mediterranean urban environment is of particular interest for several reasons. Plant species that grow at low altitudes, especially during the dry season, must be able to tolerate severely stressful conditions, such as high temperatures and water scarcity [22]. The adaptation of the photosynthetic apparatus to Mediterranean environmental conditions results in these ecosystems exhibiting some of the highest net primary productivities worldwide [23]. Consequently, Mediterranean species are particularly intriguing due to their photosynthetic strategies before, during, and after the most stressful periods. Their ability to cope with such stresses makes them a viable choice for cultivation in urban green areas [24]. Thanks to their greater plasticity and variability in functional traits, they can survive in extreme environmental conditions, thereby enhancing overall ecosystem resilience and providing maximum ecosystem services [25]. The primary school curriculum in Italy encompasses the study of living organisms, including their structures, functions, and interactions with the environment. While photosynthesis is typically addressed in lower secondary school, previous research indicates that primary students can grasp this process to a certain extent [26]. Furthermore, the direct involvement of schoolchildren in studying seasonal changes in plants is particularly beneficial, especially when scientific instruments are utilised [27]. However, it is important to note the lack of projects that engage citizens in studying ecosystem functions [28], particularly those that provide young students with direct involvement in measuring photosynthesis.

To enhance public awareness of issues related to urban plant biodiversity and its interaction with the environment, an OAL has been established in the urban park of Villa Corridi, located in the Mediterranean coastal city of Livorno, Tuscany, Italy. This initiative leverages the presence of primary and secondary schools within the park, as well as the naturally occurring Mediterranean maquis vegetation. The OAL serves as a living laboratory for schoolchildren, aiming to (i) introduce them to the scientific study of plant biodiversity in Mediterranean thermophile woodlands; and (ii) encourage students to explore these environments and measure ecophysiological leaf traits using scientific instruments and methods employed by researchers to generate replicable and reliable scientific data.

3. Results

An OAL has been established in the urban park of Villa Corridi, involving 19 schoolchildren aged 10 years and 22 schoolchildren aged 11–12 years, along with their teachers, in two separate events. A dedicated project on the iNaturalist website was created, featuring georeferenced photos of selected evergreen shrub and tree species taken by the teachers (https://www.inaturalist.org/projects/la-biodiversita-del-parco-villa-corridi, accessed on 18 October 2024; Figure S5). Additionally, an educational classroom herbarium has been developed and is now available for teaching activities (Figures S6 and S7). The meteorological data recorded by the schoolchildren and their teachers using the school’s meteorological station are presented in Figure 1b. These data reveal the typical trends of the Mediterranean climate, characterised by significant seasonal fluctuations in both temperature and precipitation. Average daily temperatures fell below 10 °C almost only during winter, while precipitation was mostly concentrated in autumn, with few occurrences in other seasons. The meteorological trends were used to assess the interaction between climate and ecophysiological leaf traits (i.e., chlorophyll fluorescence parameters and leaf pigment indices) of the studied species. Seasonal variations in light energy dissipation within the Mediterranean shrubland formation, through both photochemical and non-photochemical processes, are illustrated in Figure 2. The average values for the 11 plant species in this formation revealed a significant decrease in Y(II) during January and August, which was associated with an increase in Y(NO) and Y(NPQ), respectively. This seasonal change in light energy dissipation processes was reflected in the ETR values, which exhibited the lowest seasonal values in January and August, corresponding to the minimum and maximum seasonal daily air temperatures, respectively (Figure 1b). The reduced ETR in January was linked to the lowest seasonal values of both Fv/Fm and Rfd, while the pigment indices (i.e., Chl, Flv, and Anth) reached their maximum seasonal values (Table 3). In contrast, the decreased ETR values in August were associated with only a slight decline in Fv/Fm and a significant reduction in the Chl index (Table 3). Significant interspecific differences in energy dissipation processes (Figure 3a–c), Fv/Fm (Figure 4a), ETR (Figure 4b), and Chl index (Figure 4c) were observed among the 11 Mediterranean species. The significance levels (p-values) for the factors of time and species are reported in Tables S1 and S2. All the species tended to increase Y(NPQ) and Y(NO) in summer and winter, respectively (Figure 3b,c). The Fv/Fm values showed only a slight decrease in winter and summer for most species (Figure 4a). This was reflected in a transient decrease in Y(II) (Figure 3a) and ETR (Figure 4b) in all the species, except for Q. ilex and P. angustifolia in August, and of Q. ilex, P. angustifolia and C. creticus in January. A partial or total recovery of ETR after the summer inhibition was observed in September for all the species, except for L. lucidum (Figure 4b). The species that exhibited a reduced ETR in August also showed a decrease in the Chl index (Figure 4c). Consequently, a positive relationship between ETR and Chl index was observed in August (R = 0.83; p < 0.01), with Q. ilex, P. angustifolia, P. halepensis, and P. lentiscus displaying higher values of both ETR and Chl compared to the other species (Figure 5a). These sclerophyllous species were also characterised by higher LMA values, leading to a positive relationship between ETR and LMA (R = 0.89; p < 0.01) (Figure 5b). Conversely, in January, a positive relationship between ETR and Anth index was observed (R = 0.89; p < 0.05), with P. angustifolia, Q. ilex, P. halepensis, and C. creticus showing the highest Anth index values (Figure 5c).

Approximately 200 schoolchildren (ages 9 to 11 years) and 16 teachers participated in additional training sessions in the OAL, identifying and collecting samples of wild woody species, measuring their photosynthetic performance, and gathering meteorological data.

4. Discussion

The significance of involving children in citizen science activities related to the environment has been extensively discussed and promoted [17]. Active participation in ecological research is particularly valuable for enhancing children’s understanding of this scientific field [37]. These activities can also serve as a source of reliable data, provided that quality is ensured through meticulous verification [38,39]. Schoolchildren participating in the experimental campaigns in the park of Villa Corridi searched for selected species and recorded the morphophysiological leaf traits. This location has proven to be an effective living lab for studying wild plant biodiversity and its ecophysiological responses to seasonal environmental changes. This approach, combined with classroom lessons, enabled the participants to (1) enhance their understanding of their surrounding environment and foster a sense of belonging; (2) acquire foundational knowledge of botanical terminology used to identify eight common Mediterranean species and key ecological processes; (3) analyse the connections between biotic and abiotic components of the ecosystem; (4) improve skills such as communication, classification, measurement, inference, and prediction; (5) increase their awareness of the key role of urban green infrastructure, particularly Mediterranean evergreen species, in promoting human well-being and supporting ecosystems; and (6) practice group-collaboration while completing a task. The involvement of schoolchildren and their teachers in citizen science activities related to wild plant species and the environment is particularly significant. During the activities, the students demonstrated their ability to connect a picture and a simple list of diagnostic characters to a living plant. This can be viewed as a preliminary acquisition of basic plant identification knowledge, including habitus (tree vs. small or large shrub), phyllotaxy (opposite vs. alternate), leaf shape (simple vs. compound), leaf colour (concolorous vs. discolorous), leaf margins (entire vs. dentate), leaf scent (scented vs. grassy), and leaf indumentum (hairy vs. glabrous). Previous research has indicated that the general public may not fully understand what biodiversity is and how it relates to ecology [40]. Moreover, children may primarily be attracted to cultivated plants, while wild and less showy species may only capture the interest of researchers [41]. It appears that some children experience a form of “plant blindness” toward native species [14]. The fruitful engagement of children in these research activities through gamification and their direct involvement in specimen collection and analysis has demonstrated that this approach can effectively foster a connection between young students and science. The creation of a photographic atlas on the iNaturalist app, featuring georeferenced observations of the studied species, can also be useful for classroom activities [42]. Each project on iNaturalist includes a map displaying the georeferenced observations from the explored area, allowing for a review of observed biodiversity and familiarization with a technology that simplifies and makes the process of learning the names and identification of wild organisms enjoyable. Additionally, creating a classroom herbarium is an excellent method for teaching botany in schools [43]. Classroom discussions encouraged students to connect the observed plant species with recorded meteorological data and measurements related to plant ecophysiology obtained during activities in the park. This approach, which deviates from the typical classroom routine, exemplifies a multidisciplinary science teaching module [44]. Finally, it is important to emphasise that the informal green space within the park of Villa Corridi has facilitated the establishment of the OAL due to the abundant presence of native wild species. The significance of informal green spaces at the urban level, in terms of the ecosystem services they provide, has been extensively documented [12], particularly in comparison to formal green areas [45].
The direct engagement of schoolchildren with scientific instruments commonly used by researchers to measure photosynthesis and other leaf traits represents a novel approach to educational activities. Under expert supervision, they utilised the chlorophyll fluorescence technique as a powerful tool to assess the photosynthetic performance and health status of Mediterranean shrubland species [46]. This experience enabled the participants to (1) apply theoretical knowledge from school modules related to photosynthesis through hands-on field experience; (2) understand the instrumentation and techniques that scientists employ to generate replicable and reliable scientific data; and (3) evaluate how the photosynthetic performance of individual Mediterranean species is influenced by the environmental conditions in which they thrive (e.g., solar radiation, precipitation, air temperature, and relative humidity), as recorded by the school’s meteorological station. The results indicated a reduction in the PSII photochemical efficiency and electron transport rate of the Mediterranean shrub vegetation in both August and January. This finding highlights a diminished capacity to dissipate light energy through photochemistry during the hot, dry summer and the cold winter periods. In August, daily air temperatures reached their maximum seasonal values, coinciding with a lack of significant precipitation until the end of the month. Conversely, in January, minimum temperatures dropped to near 0 °C. The decreased Y(II) was linked to an increase in the quantum yield of light-dependent (August) and light-independent (January) non-photochemical fluorescence quenching. These processes represent the energy dissipated as heat through regulated and non-regulated energy dissipation pathways, respectively [47]. These results clearly indicate that the fate of absorbed radiation energy at the PSII level varies between winter and summer, alternating the direction of excessive absorbed energy between regulated and non-regulated energy dissipation pathways. Specifically, during the hot and dry summer months, the Mediterranean maquis formation effectively protected PSII by dissipating excessive light energy through regulated non-photochemical processes. In contrast, during winter, the plants increased the proportion of energy lost through harmful non-regulated dissipative pathways [48]. It has been hypothesised that high Y(NO) values are associated with a longer lifetime of energy excitation, which can lead to the formation of reactive oxygen species [49]. This could lead to photoinhibition and photodamage, as indicated by the reduced Fv/Fm and vitality index observed in winter. Furthermore, the increase in the Flav and Anth indices in January suggests a crucial role for antioxidant defences in mitigating oxidative stress and reducing the risk of photoinhibition [50,51]. Conversely, during the hot and dry summer period, the reduction in photochemical efficiency was associated with an increase in Y(NPQ), highlighting the ability of Mediterranean shrub species to safely dissipate excessive absorbed energy as heat without exhibiting chronic photoinhibition signals. Nevertheless, the temporary decrease in Y(II) and ETR during summer confirms that high air temperatures and excessive solar radiation can lead to a reduction in photosynthetic capacity in Mediterranean vegetation [52,53]. Seasonal variations in photosynthetic performance and energy dissipation processes were examined in relation to changes in leaf pigment composition. The reduced ETR in August was linked to a decrease in the Chl index, indicating a rearrangement of the photosynthetic apparatus in response to multi-stress conditions typical of summer. Previous studies have shown that a reduction in chlorophyll content, which is associated with increased leaf reflectance, may help Mediterranean vegetation mitigate excessive light energy by reducing intercepted solar radiation [54,55]. These results highlight the capacity of evergreen Mediterranean maquis to safely dissipate excess energy as heat (i.e., thermal energy dissipation) during the hot and dry summer months. This mechanism helps prevent chronic photodamage to the photosynthetic apparatus, enabling the recovery of photosynthetic performance in September when environmental conditions become milder. Conversely, cold winter periods can negatively impact Mediterranean vegetation by inducing chronic photoinhibition processes and activating the antioxidant system, as indicated by the increase in the Anth index. Research has shown that Mediterranean species experience two main stress periods: winter and summer [56]. Low winter temperatures result in chronic photoinhibition, while the hot and dry summer months lead to dynamic photoinhibition and a reduction in pigment content. This suggests that summer photoprotection may arise from a combination of increased non-radiative energy dissipation, alternative electron sinks, and a higher carotenoid-to-chlorophyll ratio [56].
The other question addressed with the schoolchildren was whether there were interspecific differences in how plants respond to environmental changes. In fact, species-specific adaptive responses to seasonal environmental changes were observed among the studied Mediterranean species, depending on their peculiar morphophysiological characteristics. Specifically, sclerophyllous species exhibiting the highest LMA values, such as Q. ilex, P. angustifolia, P. lentiscus, and P. pinea, were able to maintain a higher ETR and Chl index during the summer compared to the other species investigated. This suggests a strong tolerance of their photosynthetic apparatus to photoinhibition under hot and dry environmental conditions [57,58,59]. Notably, the Mediterranean sclerophyllous species can achieve a high capacity for CO2 uptake despite their large LMA, resulting in high productivity [23]. Moreover, some of these species, such as P. angustifolia, are considered well suited for the multi-stress conditions typical of urban environments [60] and have been proposed as promising ornamental species for gardening and landscaping in Mediterranean areas [61]. An exception was represented by L. lucidum, which, despite exhibiting high LMA values, showed a limited ability to withstand summer stress conditions and did not recover its photochemical efficiency in September. This observation may be attributed to the optimal conditions for this species, which are found in the central and southern regions of China, where a humid subtropical climate prevails [62]. Quercus Ilex, P. angustifolia, and P. pinea maintained higher ETR values during the winter months compared to the other studied species, highlighting their capacity to mitigate cold stress. This ability is also associated with the synthesis of anthocyanins, which function as an antioxidant system to prevent chronic photoinhibition [50,51]. These findings confirm the significant growth plasticity and adaptability of these species to both summer drought and winter frost events in Mediterranean regions [63]. Conversely, the decline in ETR observed in P. lentiscus during the winter suggests a sensitivity of this species to cold stress [64]. A distinctive seasonal behaviour was observed in C. creticus, a semi-deciduous species of the Mediterranean maquis. Cistus species can shed a substantial portion of their leaves during the summer, showing a combination of drought-tolerance and drought-avoidance strategies [65]. According to our data, these species generally exhibited a downregulation of PSII associated with a reduction in leaf chlorophyll concentrations and a rearrangement in the structure of the light harvesting complex to minimise potential photoinhibition during the summer [66]. This was followed by a recovery of physiological performance during the autumn–winter period [67], thereby confirming the resilience of this semi-deciduous species to the Mediterranean climate [68].

Overall, these data support the plasticity and adaptability of shrubland species to both summer and winter stress periods, making them excellent candidates for NbS in urban areas located in coastal Mediterranean regions.



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Valerio Lazzeri www.mdpi.com