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    Rescuing Botany: using citizen-science and mobile apps in the classroom and beyond

    Global biodiversity has been dramatically declining over the last decades1,2,3,4. The current biodiversity crisis is primarily driven by human-induced factors, the most serious of which are land-use change, habitat fragmentation, and climate change5. While global public awareness of climate change matters is high6,7, public recognition of biodiversity loss has, historically, been low8. The understanding of biodiversity concepts highly varies among countries and social groups9,10,11: in Nigeria, the biodiversity concept was known of 20.5% of non-professional Nigerians (with basic education or no formal training) while among 88.8% of professionals with tertiary education, it reached 88.8%; 60% of participants in a study in Switzerland had never heard the term biodiversity and Chinese farmers in another pilot study have never heard about biodiversity. In the European Union, the global leader of the environmental movement on both the political and discursive levels12,13, in 2018, 71% of EU citizens had heard of biodiversity, but only around 41% of these knew what biodiversity meant14. This illiteracy is a significant constraint for conservation strategies because the development and success of actions to halt and reverse biodiversity loss strongly rely on public support15.If general awareness of biodiversity loss is low, knowledge about plant diversity is even lower16. Plants have traditionally been overlooked, and expressions such as “plant blindness”, defined as a human tendency to ignore plant species17, perfectly illustrate the situation in terms of plant conservation. And yet, current estimates suggest that two out of five plant species are threatened with extinction18. Moreover, plants play a crucial role in the world ecosystems by providing habitat, shelter, oxygen, and food, including for humans19. Local community support boosts the effectiveness of biodiversity conservation actions20,21,22. However, how biodiversity is perceived and the benefits it provides to local populations have a significant influence on this support23. Therefore, stopping the loss of plant biodiversity and the impact it has on ecosystem health and human well-being must also strive to raise public awareness on the importance of plant conservation24.A big challenge, however, is to engage people with conservation. Nowadays, in a world where a large part of the human population lives in urban areas, the contact of people with nature is declining. This is a trend that will be even more accentuated in the future25. Perhaps society’s interest in plants is decreasing because of limited exposure to plants in daily lives, schools, and work. However, by critically examining our roles as plant scientists and educators, we realize that there are probably things we could, and should, do differently. New strategies to connect people to nature are required to spark people’s interest in and knowledge of plants. Citizen science programs and mobile applications (apps) are noteworthy initiatives that are helping to achieve this goal.Citizen science is defined as the general public involvement in scientific research activities and currently is a mainstream approach to collect information and data on a wide range of scientific subjects26,27. The development of mobile technologies and the widespread use of smartphones have boosted citizen science and enabled the development of mobile apps, which are digital tools that integrate, in real-time, data from multiple sources28.The goal of this article is to show how citizen science and mobile apps can be used as educational tools to raise awareness about plant biodiversity and conservation among the general public. We focused on formal education activities, at the Bachelor of Science (BSc) level, that were designed to collect data on various aspects of plant community and functional ecology. We also present the outcomes of two informal education initiatives that used citizen science to gather data on the distribution of plant diversity. We discuss these activities and results in light of their potential to engage the public into biodiversity conservation, and as educational and outreach tools.Formal education: UniversityDuring the COVID-19 pandemic (2021), Ecology practical classes of the Bologna Bachelor Degree in Biology (Faculty of Sciences of the University of Lisbon) had to be adapted to remote learning. Fortunately, during the States of Emergency imposed by the Portuguese Government, citizens were allowed to take brief walks. Taking advantage of citizen’s ability to briefly travel outdoors, we created three activities for students, as alternatives to those typically carried out in the classroom/campus, which we describe below.Activity 1—Analysis of the impact of disturbance on plant diversity in grasslandsThe objective of this activity was for students to explore the impact of disturbance and site attributes (such as soil type) on the diversity of the herbaceous plant community and its associated pollinators. This was undertaken in grasslands located near their homes, within walking distance (due to COVID lockdown movement restrictions). To achieve this goal, we developed a comprehensive sampling protocol that included methods for (i) selecting and characterizing sampling sites based on the level of human perturbation, (ii) soil characterization, (iii) sampling, identifying, and registering plants using the iNaturalist/Biodiversity4All platform and Flora-on web (Box 1), and (iv) pollinator sampling (Supplementary Data 1). To ensure accurate plant and pollinators identification, all observations were verified by professors responsible for each topic.First, each student chose one sampling site and teachers, using photographs, classified all sites regarding their perturbation level (low, medium, and high). Then, using the sampling protocol, students were invited to study different aspects of their sampling site, in loco or at their homes. Soil samples were analysed using simple methods and available household instruments (such as plastic cups, kitchen scale, and oven). Students were introduced to soil biodiversity as well as soil parameters (humidity, texture, structure, infiltration and draining) during the remote classes. Plants were sampled using a home-made 1 m2 quadrat. All species within were counted and identified to the lowest taxonomic level possible, using the mentioned apps and website. Before plant sampling, students were also asked to count and identify pollinators within their quadrats (broad taxonomic groups, bees, butterflies, flies, beetles) for 5 min, again using the apps to aid identification.Following field sampling, students were asked to calculate two taxonomic indices of plant communities. These included species richness, which measures the number of different species that occur in a sample, and the Simpson Diversity Index, which evaluates the probability that two individuals randomly selected from a sample will belong to the same species. Students also calculated functional diversity indices such as Functional Richness and Functional Dissimilarity, since functional diversity explores functional differences between species and how these differences reflect and affect the interactions with the environment and with other species29. Then, students assessed the relation between these indices and perturbation level. They analysed several functional traits of plants that are likely to respond to local perturbation (e.g., height, leaf size). Finally, they attempted to relate plant indices with the occurrence of pollinators.Overall, students sampled 147 grasslands that were affected by low (n = 17); medium (n = 86) and high (n = 40) levels of perturbation, scattered across mainland Portugal (Fig. 1a). In total, 3015 observations corresponding to 543 species of plant and 88 of insects (Fig. 1b) were registered in the iNaturalist/Biodiversity4All project Ecologia2_FCUL, created specifically to record all of the diversity data associated with this activity. Other registered taxa included six species of molluscs and 13 of arachnids, and other occasional soil macrofauna.Fig. 1: Analysis of the impact of disturbance on plant diversity in grasslands.a Location of grasslands sampled; b Banner and overview of main results of the project created in the platform iNaturalist/Biodiversity4All to register the sampled species; c Boxplots include data of the taxonomic diversity indices (plant species richness and Simpson Diversity Index) of sampled grasslands at three different perturbation levels: low, medium and high. Central lines represent median values, box limits indicate the upper and lower quartiles, whiskers correspond to 1.5 × the interquartile range above and below the upper and lower quartiles and points are the outliers. Boxplots with different letters indicate statistically significant differences among perturbation levels based on multiple pairwise comparisons.Full size imageThe results showed that the number of species (richness) decreased consistently with the level of perturbation. Simpson Diversity Index values increased, indicating low diversity values in highly perturbed herbaceous plant communities (Fig. 1c). Results revealed a trend towards an increase in the proportion of species with lower stature as perturbation increased. However, with no clear relationship with either biodiversity or perturbation. Finally, results indicated no clear relation of pollinator abundance or richness with plant richness and diversity, although field records relate a lower number of pollinators as wind intensity increased. In fact, pollinator sampling is extremely weather sensitive, which may have contributed to the lack of consistent relationships between pollinator diversity and perturbation.Box 1 Citizen science platforms and apps used for formal and informal educational activitiesiNaturalist (https://www.inaturalist.org/home): is a social network of naturalists, citizen scientists, and biologists that is based on mapping and sharing biodiversity observations. They describe themselves as “an online social network of people sharing biodiversity information in order to help each other learn about nature”. iNaturalist may be accessed via website or mobile app. Records are validated by the iNaturalist community. Observations reached approximately 110 million as of July 2022. This app allows the development of both open-access and registration-restricted projects. BioDiversity4All (https://www.biodiversity4all.org/) is a Portuguese biodiversity citizen science platform created by the Biodiversity for All Association. This platform was founded in 2010 and is currently linked to the “iNaturalist” network43. All the projects presented in this article were developed on the Biodiversity4All platform.Flora-on (https://flora-on.pt/): this portal contains occurrence data of vascular plants from the Portuguese flora collected by project collaborators (over 575,000 records as of July 2022). Flora-on was created by the Botanical Society of Portugal (SPBotânica), a Portuguese association devoted to the promotion and study of botany in Portugal. Botanists and naturalists provide most of the data, but occasional contributors are welcomed. Records are supervised by the portal editors, ensuring the dataset’s quality level. The portal includes stunning images of leaves, flowers, fruits, and other plant parts for 2299 of the 3300 taxa occurring in Portugal44. Additionally, the portal includes a powerful search engine that allows geographical, morphological, and taxonomical searches.LeafBite (https://zoegp.science/leafbyte): is a free, open-source iPhone app that measures total leaf area as well as consumed leaf area when herbivory is present45.Leaf-IT is a free and simple Android app created for scientific purposes. It was designed to measure leaf area under challenging field conditions. It has simple features for area calculation and data output, and can be used for ecological research and education46.Activity 2—Leaf trait assessment of shrub and tree speciesStudents were asked to assess three leaf traits Specific leaf area (SLA), Specific leaf mass (LMA), and Leaf Water Content (LWC) of two or three shrub or tree species. Each species should ideally fall into one of three functional groups known for their water adaptations, namely Hydrophytes, Mesophytes and Xerophytes. Students were challenged to choose charismatic Mediterranean species that grew nearby, such as Olea europaea, Nerium oleander or Phillyrea angustifolia. Alternatively, they could take the “Quercus challenge”, which involved ranking the Portuguese oak species based on their drought tolerance. A detailed protocol was developed to assist students for this purpose (Supplementary Data 2). In this protocol was demonstrated how to calculate the leaf area using the LeafBite and Leaf-IT apps (Box 1).The students calculated the SLA, LMA, and LWC of a total of 104 species (Supplementary Data 3) belonging to the main functional groups under study. Regarding the “Quercus challenge”, they were able to classify the six most representative oak species in Portugal and confirm the relationship among these indices and their tolerance to drought (Fig. 2).Fig. 2: Leaf trait assessment of shrub and tree species: Quercus challenge.Classification of Portuguese oak species regarding their drought tolerance (higher tolerance, left-up, lower tolerance right-down).Full size imageOne of the students, accomplished to present his own learning experience related to these activities at the XXIII Conference of the Environmental Research Network of Portuguese-speaking Nations – REALP, under the title “Plant Ecology during Confinement – A Digital Approach”.Activity 3—Evaluating the impact on the biodiversity of lawn management at the University of Lisbon campusAlthough, after the lockdown, practical classes returned to the laboratories and the field in 2021/22, we continued to use the iNaturalist/Biodiversity4All platform and the Flora-on website for biodiversity registering and identification, because of the success of the activities, as evidenced by the positive comments we received from students.The goal of this activity was to study the impact of lawn management on plant diversity and pollination on the University of Lisbon campus. To accomplish this, the students described the herbaceous communities and pollinators on four lawns (named C8, RL, RR, and TT) that had different management practices (mowing and irrigation). A comprehensive document with sampling guidelines was developed (Supplementary Data 4).The project Ecologia 2 Relvados 2022 registered 100 plant and 17 pollinator species (Fig. 3a). Given that the sampling took place during a cold and rainy week, which limited pollinator activity, the low number of pollinators registered was expectable (Lawson and Rands 2019). Following these analyses, the TT lawn (Fig. 3b), which had low levels of mowing and no watering, showed a significantly higher value of diversity, indicating it had the best management strategy for these systems (Fig. 3c), if the goal is to increase biodiversity.Fig. 3: Evaluating the impact on the biodiversity of lawn management at the University of Lisbon campus.a Banner and overview of main results of the project Ecologia 2 Relvados created in the platform iNaturalist/BioDiversity4All to register the sampled species; b Location of the lawns sampled in the Campus of the University of Lisbon; c Boxplots include data of the taxonomic diversity indices (plant species richness and Simpson Diversity Index) of sampled grasslands. Central lines represent median values, box limits indicate the upper and lower quartiles, whiskers correspond to 1.5 × the interquartile range above and below the upper and lower quartiles and points are the outliers. Boxplots with different letters indicate statistically significant differences among lawns based on multiple pairwise comparisons.Full size imageInformal education: BioBlitzesIntense biological surveys known as “BioBlitz” are carried out to record all organisms found in certain locations, such as cities, protected areas, or even entire countries. They are being used all over the world to collect and share georeferenced biodiversity data30. We developed two Plant Bioblitzes based on the BioDiversity4All/iNaturalist and Flora-on platforms. Social media, such as Facebook, Instagram, and Twitter, were used to promote these events and engage citizens (Fig. 4). The BioBlitzes were developed by SPBotânica in collaboration with BioDiversity4All.Fig. 4: Bioblitz I & II – Flora of Portugal.Posters created for the promotion of the two Flora of Portugal Bioblitzes.Full size imageBioblitz I & II – Flora of PortugalThe celebration of Fascination of Plants Day (18th of May) served as the backdrop for the organization of two-weekend Bioblitzes: Bioblitz Flora of Portugal I and Bioblitz Flora of Portugal II.In 2021, the Bioblitz was solely focused on project members, which meant that only those who had voluntarily joined the initiative could participate. In total, the 119 project members registered 4234 observations of 890 plant species. In contrast, the 2022 Bioblitz was an open project (no registration required). In total, the 323 observers made 6547 records of 1198 species. To evaluate the impact of the Bioblitz events, we compared the data registered in BioDiverstiy4All during the weekends of both events (2021 and 2022) with (i) the data registered in the platform during the equivalent weekends of 2019 and 2020 and (ii) also during the weekends before both Bioblitzes. The number of species, observations, and observers increased significantly from 2019 to 2020, 2021, and 2022, but, when comparing values from 2020 with 2021 and 2022, this rise was only verified during the Bioblitz weekends, proving the importance of Bioblitzes in this increase (Fig. 5).Fig. 5: Number of observations, species and observers registered on the BioDiversity4All/iNaturalist platform over equivalent weekends in 2019, 2020, 2021, and 2022.Numbers for 2021 and 2022 correspond to the weekends in which Bioblitzes I & II – Flora of Portugal were conducted, as well as previous ones.Full size image More

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    Alcobiosis, an algal-fungal association on the threshold of lichenisation

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    Astragalus-cultivated soil was a suitable bed soil for nurturing Angelica sinensis seedlings from the rhizosphere microbiome perspective

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    Shifts from cooperative to individual-based predation defense determine microbial predator-prey dynamics

    In co-culture with the bacterivorous flagellate Poteriospumella lacustris, the prey bacterium Pseudomonas putida exhibited a characteristic succession of predation defenses. The initial and the final defense differed substantially from one another with regard to their mechanism and their population-level benefits to the bacteria.Our results strongly indicate that the initial bacterial defense falls into the category of chemical defense, and is regulated by phenotypic plasticity. This would require P. putida to be able to sense predator density and to regulate the excretion of inhibitory substances accordingly. Because a considerable proportion of the P. putida genome is known to be involved in regulation and signal transduction allowing for very flexible responses to environmental triggers [41] both conditions are likely to be met. The filtrate exposure tests (Fig. 3) provide specific evidence for the ability of P. putida KT2440 to up- and downregulate the excretion of compounds inhibiting flagellate growth in response to grazing pressure. Previous research [25] corroborated the ability of P. putida to escape grazing from bacterivorous flagellates through induced responses like aggregation or biofilm formation.To provide a possible characterization for the apparent bacterial toxin, the whole-genome sequences of P. putida KT2440 obtained here were aligned against the antiSMASH [42] database. The output suggests the existence of non-ribosomal peptide synthetase clusters mediating the production of pyoverdines, a particular class of siderophores. The latter are molecules released by bacteria into the environment, which enhance the uptake of essential metals like, e.g., iron under deficient conditions. Specific pyoverdines associated with P. putida KT2440 have previously been identified [43]. Recent findings have shown that the benefits from siderophore production are not limited to competitive advantages gained from enhanced resource exploitation [44]. Pyoverdines were also demonstrated to determine the virulence of Pseudomonads via the damage of mitochondria in colonized hosts [45]. Moreover, pyoverdines were shown to be involved in the inducible defense of P. putida against predatory myxobacteria [46]. Such multiple functions have been reported for a number of bacterial metabolites, especially in Pseudomonads [47], and the particular combination of pyoverdin effects would explain the observed simultaneous flagellate inhibition and promoted bacterial growth.In contrast to the initial chemical defense of P. putida, the subsequent filamentation clearly provides an example of rapid evolution. Although the responsible mutation(s) could only be pinpointed in a few isolates so far (Table S1), there is no doubt about the genetic manifestation and heritability of the filamentous phenotype due to its demonstrated non-reversible nature.Only recently, similar observations were made by long-term co-cultivation of Pseudomonas fluorescence with the amoeboid predator Neaglena grubei [48]. In that system, protective adaptations like enhanced biofilm formation and altered motility were traced down to mutations in two particular genes (wspF, amrZ).From the perspective of the bacterial population, filamentation appears to be a much less efficient defense mechanism than toxin production. This is clearly reflected by the ratio of prey to predator biomass, which differed by two orders of magnitude between the initial and final defense (Table 6). It raises the question of why bacteria would abandon a highly effective form of defense in favor of a much less effective one. As demonstrated experimentally, adaptation of predators to the toxin can be excluded as a cause (Fig. 4). Moreover, it was not instantly evident how the small-sized flagellate was ultimately able to persist in large numbers given a very high proportion of completely inedible prey individuals (Fig. 1D and Fig. S2).Table 6 Average abundance of predator and prey during the temporary steady state following the initial bacterial defense (day 13–16) and during the final steady state (beyond day 30).Full size tableTo develop a comprehensive understanding of the system addressing the questions raised above, we set up a semi-continuous differential equation model to simulate the dynamics of predator and prey phenotypes. The model considers seven state variables (carbon, densities of four bacterial phenotypes, flagellate density, and toxin concentration) whose dynamics are controlled by nine processes (Table 3, Fig. 2). In addition to microbial growth and grazing, the model implements a phenotypically plastic predation defense (toxin production) as well as a genetic defense (filamentation) which arises via mutation. The particular assumptions implemented in the model are as follows:Dual effect of bacterial metabolitesIn line with the above discussion on siderophore-like compounds, secondary metabolites excreted by P. putida were assumed to exhibit a dual function, both inhibiting the growth of flagellates and allowing for a more efficient exploitation of the resources by bacteria. The inhibition of predators was demonstrated directly (Figs. 3 and 4) while enhanced resource exploitation was inferred from bacterial abundances in co-cultures exceeding the carrying capacity observed in predator-free controls (Fig. 1A, day 11–18).Metabolite production is costlyThe production of bacterial metabolites was assumed to be associated with a slight fitness cost [49] since resources are diverted from reproduction, thus resulting in a lowered growth rate of toxin-producing bacteria. The assumed fitness cost of 11% (parameter cBx in Table 5) allowed for the best agreement between simulated and observed data and is in agreement with data on the cost of pyoverdine production by P. aeruginosa [50]. The cost only manifests when toxin production is upregulated.Predator recognition and quorum sensing interactIn the model, the production of bacterial metabolites is upregulated when the two conditions of high flagellate abundance and high bacterial abundance coincide. That is, the expression of the toxin-based bacterial defense is assumed to be jointly controlled by predator recognition and quorum sensing (QS). Examples for such joint control of bacterial defenses have been reported previously [8, 26, 51]. The involvement of QS in chemical defense strategies is particularly likely as effective toxin concentrations can only be reached when producers are highly abundant. While multiple QS systems have been described for other Pseudomonads, only a single system has been identified in P. putida KT2440 so far [52, 53].Mutation rates are conditional on stressThe emergence of mutations resulting in the filamentation of P. putida was assumed to be conditional on a high ambient concentration of bacterial metabolites. The latter was considered as a proxy for bacterial stress which can affect mutagenesis either directly or indirectly by a variety of mechanisms [54,55,56]. Without this assumption, the almost synchronous appearance of filaments in all replicates at a late point in time would be very difficult to explain. Specifically, if mutation frequencies were high, filaments would become the predominant phenotype early (Fig. S3) which contradicts observations. On the other hand, if frequencies were low but unconditional, the timing of filament appearance should vary between replicates, which is in contrast to observations either (Fig. 1B).Filamentation is associated with a fitness costMeasurements of growth rate constants revealed a significant fitness disadvantage of filamentous isolates in comparison to single-celled, undefended isolates (p  More

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    Effect of different plant communities on NO2 in an urban road greenbelt in Nanjing, China

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