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Article

Impact of Biodiversity Loss on Pollen Allergies: A Bibliometric Analysis

by
Karoline Braun
and
Daniela Haluza
*
Department of Environmental Health, Center for Public Health, Medical University of Vienna, Kinderspitalgasse 15, 1090 Vienna, Austria
*
Author to whom correspondence should be addressed.
Sustainability 2024, 16(21), 9285; https://doi.org/10.3390/su16219285
Submission received: 4 September 2024 / Revised: 21 October 2024 / Accepted: 25 October 2024 / Published: 25 October 2024
(This article belongs to the Special Issue Challenges and Prospects of Sustainability in the Context of Global Health: 2nd Edition)
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Abstract

:
The incidence of allergic respiratory diseases has increased in recent decades, with declining biodiversity identified as a potential contributing factor. While directly linking this increase to biodiversity loss is challenging, the research on pollen offers crucial insights into how environmental changes impact patients with pollen allergies. This paper explores the complex relationship between declining biodiversity and type 1 pollen allergies from 1998 to 2022 by synthesizing the scientific insights using the mapping software VOSviewer version 1.6.19. The graphical representation provides a visual overview of the evolution of the research on pollen and biodiversity aspects combined, showing a shift from localized studies to global, interdisciplinary approaches. The research in this field has expanded significantly, particularly since 2010, with European countries leading the scholarly contributions. Pollen allergy has become a key intersection of public health and environmental science. This bibliometric review underscores the critical need for enhanced interdisciplinary research and international collaboration to address these interconnected challenges, promoting sustainable solutions in a rapidly advancing field.

1. Introduction

Nowadays, it is commonly accepted that climate change and outdoor air pollution affect vegetation all over the world, and consequently also in Central Europe [1,2]. Changing environmental conditions have a significant impact on the altered biodiversity and consistency of ecosystems. Affected by these changes are all conceivable types of plants, from small shrubs to large trees, including their pollen grains [1]. Almost in parallel with the global changes due to biodiversity loss, another trend of public health relevance has emerged over the last few decades: an increase in the prevalence of respiratory allergies and other chronic inflammatory respiratory diseases [3,4]. Whether and how exactly these two trends are related is still largely unexplained. Although there are already a variety of possible explanations, which also complement and influence each other, there is still much to be understood in the field of research [1].
Yet, the public health benefits of conserving and promoting biodiversity have been recognized by the Convention on Biological Diversity and the World Health Organization [5]. However, for the specific planning and consequent successful implementation of coordinated biodiversity and health goals, more concrete scientific knowledge on the causal mechanisms for these linkages is needed. Proximity to nature in the form of green spaces, such as parks or forests, has a significant positive impact on health and wellbeing [6]. This effect has been demonstrated in numerous studies and is well documented in a wide range of general literature, including prose [7,8].
Inflammation is a major factor in allergies and asthma [9,10,11]. While exposure to natural environments has demonstrated anti-inflammatory effects, the ongoing decline in biodiversity could contribute to an increase in chronic inflammatory diseases. This may occur due to the reduction in plant diversity, which affects microbiota composition and, in turn, disrupts immune system regulation, potentially impairing allergen tolerance [11]. The pathways of the development of allergic respiratory diseases are not yet fully understood. However, it is assumed that the amount of contact to greenspaces with high biodiversity might play a crucial role in the pathogenesis of allergies [12]. The biodiversity hypothesis provides a possible explanation regarding how biological diversity has a beneficial effect on human health and thus on allergies, more specifically pollen allergies [13]. This theory thus extends the hygiene hypothesis [9], which states that early childhood contact with microorganisms has a preventive effect against allergic disease [11]. According to the extended biodiversity hypothesis, rich biodiversity of the natural green environment now affects the microbiota found in all ecosystems, including the human body, and consequently the development and maintenance of a well-functioning immune system in humans [3,10,13].
Reduced biodiversity within the flora of natural habitats impacts the interactions between humans and microorganisms [9]. In this context, the microbiota act as a connecting bridge between the yet-distant components of plant biodiversity and the severity of pollen allergy. The degree of biodiversity at the level of the plant macrobiota is positively correlated with the biodiversity of the level of the environmental microbiota within its ecosystem, and a loss of biodiversity at one level results in the same at the other level [10]. The microbes then reach atopic patients either directly through the ambient air or sitting on the surface of pollen grains and can interact with their commensal microbiota [3]. Through their ability to interact with specific immune cell receptors, microbes play a significant role in the healthy development and proper functioning of epithelial cell integrity and the immunological tolerance mechanisms [10,14]. The consequent assumption that an environment with high microbial diversity and density is protective against allergies and allergic asthma has already been supported by studies [9,15].
Unlike many plant species, the population of microorganisms is not threatened or characterized by significant losses, but a decline in their diversity and abundance is already detectable in urban areas [16]. As an example, Hanski et al. investigated the biodiversity hypothesis by examining the impact of plant biodiversity on atopy in adolescents [3]. The authors found that adolescents with higher species richness regarding the native flowering plants in their gardens and more forested areas within three kilometers had significantly fewer allergies. Specifically, the gardens of allergy-free adolescents had 25% more native flowering plant species than those of atopic adolescents. Additionally, atopic adolescents had lower genetic diversity of Gram-negative gammaproteobacteria on their skin, including anti-inflammatory microbes like Acinetobacter. These findings suggest that environmental biodiversity may help to protect against allergies by promoting beneficial microbial diversity and anti-inflammatory responses.
To keep the risk of pollen allergy and the severity of symptoms as low as possible, it is essential to create and maintain the richest possible biodiversity already during the planning of recreational green spaces with regard to the selection and composition of plants [17,18]. A high level of biodiversity can also prevent a few allergenic species, and thus their pollen, from becoming over-present [17]. Although removing highly allergenic plants such as birch, alder, or hazel from green spaces might seem like a straightforward preventive measure, this approach oversimplifies the issue. Although it may reduce the risk of allergies to these specific pollens, it could increase the risk of allergies to other species. This is further exacerbated by environmental factors like air pollution and climate change, which influence allergenicity. Therefore, a well-considered selection of diverse tree and plant species in green spaces is essential to promote biodiversity and reduce the overall allergy risks [18].
This study examined the current status, the evolution towards it, and possible gaps in the research on the interacting and interrelated factors of biodiversity loss on various aspects of pollen and their impact on human health in relation to type 1 pollen allergy. For this purpose, the existing research situation was examined, in particular the period from 1998 to 2022, with a focus on European countries by conducting a bibliometric analysis of the research status on this topic. This bibliometric analysis aimed at exploring how the research on the effects of biodiversity loss on pollen allergies has evolved over the past decades (temporal dimension). Specifically, we examined the changes in the volume, focus, and direction of the research. Additionally, we sought to determine whether European countries have contributed more to this field compared to other geographical regions (spatial dimension) given Europe’s diverse ecosystems and the increasing focus on environmental health in public policies.

2. Methods

Bibliometric analysis is a valuable method for identifying patterns and trends in scientific research by analyzing the volume, focus, and impact of publications. To investigate how research on the effects of biodiversity loss on pollen allergies changed in recent decades (1998–2022), we performed a bibliometric analysis using the mapping software VOSviewer version 1.6.19 [19]. This application offered the possibility to create maps of relevant terms and datasets from bibliometric networks. For this purpose, we examined the databases PubMed (for the keyword search) and Scopus (for the country-specific search). This enabled illustrating the co-occurrence of terms or institutions. Only objects of interest, so-called items, from one group could be displayed per map, such as exclusively keywords or exclusively publication countries [20]. These items were represented as circles whose size depended on their weighting. In addition, the items were grouped into color-coded clusters. Between the different items, independent of the clusters, connections and relationships were drawn in the form of lines, referred to as links [21]. The strength of the respective links was represented by a positive numerical value, referred to as link strength. This value corresponded, for example, to the number of papers in which the two linked items appear together. The number of all links of a single item determined the weighting of the item, referred to as total link strength.
In this study, the aim was to investigate the relationship between pollen allergies and biodiversity. To achieve this, the search query “pollen AND plant AND biodiversity” was constructed to retrieve relevant research articles from the databases, and this combination of terms was selected for specific reasons. The term “pollen” was included as it directly related to the primary focus of the study. Given that our analysis examined the intersection of plant biodiversity and allergic reactions, it was crucial to capture studies focusing specifically on pollen as a key factor influencing allergy prevalence [1,22,23]. The term “plant” was added to narrow the scope of the search as “biodiversity” is an expansive term, covering a vast array of ecosystems, species, and genetic diversity [9,24]. Without the inclusion of “plant”, the search results would have included a wide array of studies unrelated to the study’s focus, such as those on the diversity of gut microbiomes or animal species. The inclusion of “plant” ensures that the results were filtered to focus specifically on plant biodiversity, which is directly related to the pollen production and consequently the prevalence of allergies.
By combining these terms, the search query effectively balanced specificity with comprehensiveness, ensuring that relevant studies on the intersection of plant biodiversity and pollen-related allergies were retrieved while avoiding less relevant research on other forms of biodiversity. The resulting datasets were then used to create visualization maps, which graphically represent the research landscape, including the temporal and spatial trends in studies on pollen allergies and biodiversity. Two types of maps were used in this bibliometric analysis. The first was the network visualization map, where the color of circles and connecting lines represents cluster membership. This map provided an overview of the entire dataset of keywords and illustrated the interconnectedness of research between countries. The second type was the overlay visualization map, in which colors are based on specific scores, such as the year of publication. This map was used to identify the most prominent keywords during different time periods. These maps visually represent the temporal and spatial developments in research on pollen allergies in relation to biodiversity loss, revealing key trends in the field [19].

3. Results

3.1. Keywords—Network Visualization Map of Complete Dataset (1998–2022)

To illustrate the most relevant research contributions, track the evolution of the key concepts over time, and map out the collaborative networks within the specific area of studies on biodiversity and pollen allergies, the search query “pollen AND plant AND biodiversity” on PubMed was used to create the maps in Figure 1, Figure 2 and Figure 3. The described search query returned a total of 839 results from 1998 to 2022 in PubMed. A total of 3198 keywords could be filtered from the 839 papers. For a better overview, only those 60 keywords were integrated into the map that occurred at least 20 times. These keywords could be assigned to four clusters and were connected via 1288 links and a total link strength of 10,195. The Cluster Pollen Ecology, shown in Figure 1 with red circles and lines, describes the relationship between environmental impacts and biodiversity. The Cluster Genetics category, in green, summarizes the keywords on genetic diversity and evolutionary concepts. The Cluster Pollination category, with the blue circles and lines, describes the concepts related to plant reproduction, whereas the Cluster Pollinators and Microbiota category, in yellow, describes the impact by animals and microbiota like bacteria.
Table 1 shows a list of the 15 most important keywords per cluster, ranked according to their total link strength (right column) and the number of documents in which the term occurs (left column).

Interpretation of the Results: Keywords 1998–2022

The network visualization map of the PubMed search dataset (1998–2022) provides key insights into the evolution of the research connecting biodiversity-, pollen-, and allergy-related studies. A total of 839 papers were analyzed, from which 3198 keywords were extracted. The visualization offers an overview of how these keywords cluster into four main thematic areas, illustrating the interdisciplinary nature of the research on biodiversity and its links to allergic reactions, pollen ecology, genetics, and pollination dynamics. The Cluster Pollen Ecology (red) captures the relationship between environmental changes and biodiversity. The research in this area highlights how ecological shifts, such as climate change, habitat loss, and urbanization, might alter plant biodiversity and pollen production, leading to increased allergic sensitization in humans. This cluster aligns with studies like Hanski et al., which connects changes in biodiversity to airborne allergens [3]. The environmental shifts driving alterations in pollen loads and allergen exposure are increasingly recognized as significant contributors to public health challenges [25].
The Genetics cluster (green) groups the keywords related to genetic diversity and evolutionary biology. This cluster reflects how genetic variations among plant species, as well as among human populations, influence susceptibility to pollen allergies [1,18,26]. The research in this field, such as the findings by Ortiz and Barnes, emphasizes the genetic predispositions to allergic diseases [27]. These studies underscore the complex interplay between genetic factors and environmental triggers, which are crucial for understanding the spread of allergic diseases [28].
The Cluster Pollination (blue) category refers to plant reproduction and its relevance to both pollen production and allergy incidence. The increased pollen production during the peak pollination seasons is a major factor in the rising allergic reactions [29,30]. This body of research is crucial in contexts where shifts in pollination dynamics are influenced by climate or land use changes, thus linking changes in pollen seasons to allergic disease trends [31].
Finally, the Cluster Pollinators and Microbiota (yellow) category describes the role of animals (pollinators) and microbial communities in shaping plant biodiversity and allergy-related outcomes. Pollinators like bees and other insects affect plant reproduction and pollen distribution while foraging, indirectly impacting allergy prevalence [32]. The microbial biodiversity hypothesis posits that the reduced microbial diversity in modern environments contributes to the rise of allergic diseases [9,33].

3.2. Keywords Before the Year 2000

The research on the interplay between biodiversity, pollen, and allergic reactions is relatively recent. Prior to the 21st century, the field was still emerging. The first paper relevant to this topic appeared in 1998. Thus, the creation of a meaningful map over this data was not possible. The limited research during this period indicates that the connection between biodiversity loss and pollen allergies was not yet a focus of scholarly research, perhaps due to a lack of third-party funding and public awareness.

3.3. Keywords 2001–2011

Beginning in 2001, the number of published papers on PubMed saw a steady annual increase. By 2011, 140 papers had been published, from which 391 keywords were identified. Of these, 61 keywords appeared at least five times and were integrated in the map shown in Figure 2. These keywords are connected by 939 links, with a total link strength of 3041.
The most important keywords from the first papers in 2001 to 2006, in purple to dark blue, were trees (TLS 190), geography (TLS 120), plant physiological phenomena (TLS 112), environment (TLS 85), geological sediment (TLS 59), crops, agricultural (TLS 59), time (TLS 50), hybridization, genetic (TLS 38), and symbiosis (TLS 33).
Around 2007, in light blue to turquoise, the most frequent keywords were pollen (TLS 553), biodiversity (TLS 399), animals (TLS 361), ecosystem (TLS 305), plants (TLS 175), reproduction (TLS 170), bees (TLS 154), population dynamics (TLS 138), fossils (TLS 135), insecta (TLS 118), conservation of natural resources (TLS 101), climate (TLS 99), and biological evolution (TLS 62). Further, 2008 was the average publication year for the expressions flowers (TLS 218), seeds (TLS 143), phylogeny (TLS 136), agriculture (TLS 83), ecology (TLS 80), fruit (TLS 66), plants, genetically modified (TLS 61), models, genetic (TLS 53), Diptera (TLS 43), feeding behavior (TLS 43), human (TLS 42), temperature (TLS 40), DNA, chloroplast (TLS 36), and altitude (TLS 35), shown in green.
The yellow circles represent the terms that occurred most frequently from 2009 to 2011. These included pollination (TLS 148), time factors (TLS 98), gene flow (TLS 94), genetic variation (TLS 77), evolution, molecular (TLS 63), microsatellite repeats (TLS 51), introduced species (TLS 48), climate change (TLS 42), sequence analysis, and DNA (TLS 42).
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Figure 2. Keywords 2001 to 2011—color-coded to publication year on PubMed (created using VOSviewer).
Figure 2. Keywords 2001 to 2011—color-coded to publication year on PubMed (created using VOSviewer).
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Interpretation of the Results: Keywords 2001–2011

The keywords from 2001 to 2006, such as trees, geography, plant physiological phenomena, and geological sediment, suggest that the early research was primarily concerned with foundational ecological processes and plant biology. This indicates that the initial studies were likely focused on understanding the basic interactions between trees, plants, and their environments, as well as the physical processes shaping ecosystems. The presence of keywords like hybridization and symbiosis points to an interest in genetic relationships and interactions between species during this period.
From 2007 onward, a shift towards more specialized topics like pollen, biodiversity, and ecosystem can be observed, reflecting an increasing awareness of biodiversity’s role in ecosystem functionality and health. Terms like bees, population dynamics, and conservation of natural resources suggest a growing interest in pollination biology, the impacts of environmental change, and species conservation. This marks a shift toward applied ecological research, likely encouraged by growing concerns about biodiversity loss and its effects on ecosystem services like pollination. The rise of pollen and biodiversity as key terms around 2007 aligns with growing concerns over the effects of biodiversity loss on pollinator populations and the subsequent impacts on agriculture and food security [34]. This period witnessed an increasing number of studies investigating pollinator decline and its implications for crop pollination and biodiversity [34].
By 2008, the inclusion of terms like climate, DNA, and temperature indicates that genetic and molecular tools were becoming more prominent in ecological studies, alongside a stronger focus on how global changes, particularly climate change, were influencing biodiversity and ecosystem functioning. This is further supported by the appearance of terms like plants and genetically modified, reflecting the rising debates around genetically modified organisms. The appearance of genetic and molecular terms in 2008 reflects the broader trend towards integrating molecular techniques into biodiversity research as genetic tools became essential for understanding the evolutionary processes and biodiversity patterns in the face of climate change [35].
From 2009 to 2011, terms such as pollination, genetic variation, climate change, and introduced species demonstrate a heightened interest in understanding how climate and genetic diversity influence ecosystems, particularly in the context of pollination [34]. The presence of introduced species signals an awareness of how species invasions, driven by human activities and climate change, impact biodiversity and ecosystem services. The focus on climate change and genetic variation in the 2009–2011 period is consistent with the increasing recognition of climate change as a major driver of biodiversity loss, affecting the distribution and reproductive patterns of species [10].
These trends can be linked to broader scientific discussions in the literature. We suggest that the shift from foundational ecological research (2001–2006) to more specialized studies on pollination, biodiversity, and climate change (2007–2011) mirrors the increased global attention on biodiversity conservation following the publication of key reports such as the Millennium Ecosystem Assessment in 2005, which highlighted biodiversity’s role in human well-being and ecosystem services [36].

3.4. Keywords 2012–2022

Between 2012 and 2022, the number of research papers on PubMed related to our topic increased significantly, culminating in 702 publications by 2022. From these papers, 4088 unique keywords were identified. To highlight the most impactful terms, we limited Figure 3 to the 50 most frequently occurring keywords, each appearing at least 20 times.
These selected keywords are interconnected through 914 links, with a cumulative link strength of 6973, indicating robust thematic connections and a well-developed research network. Up to and including 2016, the most frequent keywords, colored in purple to dark blue, were seeds (TLS 324), genetic variation (TLS 276), introduced species (TLS 254), microsatellite repeats (TLS 212), species specificity (TLS 203), endangered species (TLS 200), conservation of natural resources (TLS 198), dna plant (TLS 176), fossils (TLS 170), agriculture (TLS 124), climate (TLS 111), and germination (TLS 82).
In turquoise, the most significant terms from 2017 are shown. These include pollen (TLS 1429), pollination (TLS 1060), flowers (TLS 788), biodiversity (TLS 679), ecosystem (TLS 587), reproduction (TLS 352), insecta (TLS 285), climate change (TLS 248), phylogeny (TLS 241), trees (TLS 234), seasons (TLS 185), and birds (TLS 128).
In green, the keywords that occurred most frequently in 2018 are shown. These were animals (TLS 1205), bees (TLS 599), plants (TLS 462), ecology (TLS 158), dna barcoding, taxonomic (TLS 109), allergens (TLS 94), and environmental monitoring (TLS 80).
Finally, the period 2019 to 2022 is shown on the map in yellow. The most significant keywords of this period included humans (TLS 245), forests (TLS 166), plant nectar (TLS 145), microbiota (TLS 135), bacteria (TLS 89), and pollen limitation (TLS 88).
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Figure 3. Keywords 2012 to 2022—color-coded to publication year on PubMed (created using VOSviewer).
Figure 3. Keywords 2012 to 2022—color-coded to publication year on PubMed (created using VOSviewer).
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Interpretation of the Results: Keywords 2012–2022

Between 2012 and 2022, the scope and volume of research related to pollen allergies and biodiversity expanded significantly. A key observation from this period is the thematic shift reflected by the keywords and their associated link strengths. Up to 2016, keywords such as seeds, genetic variation, introduced species, and conservation of natural resources indicate that the research was focused on genetics, species conservation, and the broader impact of biodiversity loss on agriculture and natural ecosystems [3,25,26,37]. This potentially shows the foundational exploration of how biodiversity loss may influence plant systems, agriculture, and the related ecological dynamics.
The research from 2017 focused on ecological interactions, with significant keywords such as pollen, pollination, flowers, biodiversity, and ecosystem. This suggests that the focus was shifting toward understanding how changes in ecosystems and biodiversity directly affect pollination patterns, which are crucial for the spread of allergens [12]. The emergence of keywords like phylogeny and trees further emphasizes the growing interest in evolutionary biology and its links to allergies.
During the later years, 2019–2022, there was a noticeable shift toward human health impacts, with keywords such as humans, microbiota, bacteria, and pollen limitation reflecting an increased focus on the role of human microbiota, interactions with environmental biodiversity, and limitations in pollen distribution. These findings support a growing recognition of how human health, such as allergies and immune responses, is intricately linked with broader environmental changes, such as biodiversity loss and climate change. Several scholars support the interpretation that biodiversity loss can have significant health implications, particularly in relation to allergies [3,5,9,10,18,23,33,38,39]. This supports the relevance of keywords like climate change and pollen limitation in the analysis.

3.5. Spatial Distribution—Network Visualization Map of Countries

We used the Scopus database to map the countries contributing to the research on the influence of biodiversity on pollen allergies given Scopus’ broader scope beyond medicine compared to PubMed. We conducted a document search using the terms “pollen AND allergy AND biodiversity AND plant”. When the term “plant” was included, the search yielded only 20 results. The subsequent search without this term then returned 61 results up to 2022, with the first paper published in 2002. Our analysis revealed that 47 countries were involved in the 61 publications identified. Figure 4 illustrates collaborative research efforts among these countries, indicated by color-coded clusters and the proximity of circles.
The red cluster in Figure 4 highlights the research connections among Bulgaria, Canada, Israel, Kuwait, New Zealand, Portugal, Saudi Arabia, the Republic of Korea, the United Arab Emirates, Zimbabwe, and Turkey. Countries like Finland, Spain, Venezuela, Brazil, Cuba, Colombia, Egypt, Singapore, Sweden, and Estonia form the green cluster. Germany, the United Kingdom, Switzerland, Greece, and Poland are grouped in the yellow cluster. The United States, France, The Netherlands, the Russian Federation, Serbia, Belgium, and Luxembourg are represented in dark blue. Italy, Costa Rica, and Mexico are clustered in light blue, while Australia, Pakistan, Argentina, and South Africa are shown in purple. Japan and Taiwan are linked in orange. Examples of collaborative research across clusters include Finland with Costa Rica, Italy with Turkey, and the UK with Germany and France. In addition to these 43 linked countries, China, Hong Kong, Croatia, and Iceland had only one document each and were not connected to any other countries on the map in Figure 4.
With twelve papers each, Spain (TLS 41) and the USA (TLS 36) were involved in the most research projects. They were followed by Germany (nine doc., 52 TLS), France (nine doc., 48 TLS), Italy (eight doc., 37 TLS), and Finland (seven doc., 42 TLS), which were involved in a smaller number of papers but were better linked, as can be seen from the total link strength. Also contributing to the research and well connected were Brazil (three doc., 38 TLS), the UK (five doc., 37 TLS), Argentina (three doc., 35 TLS), Japan (five doc., 33 TLS), and Mexico (four doc., 32 TLS). Again, the European countries were the most actively involved in the research once more, contributing to seventy-five documents on pollen allergy and biodiversity, followed by Asia with twenty-one, North and South America each with fifteen papers, Oceania with six, and Africa with four documents.
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Figure 4. Network visualization map, color-coded by country of publication, published on Scopus from 2002 to 2022 (created using VOSviewer).
Figure 4. Network visualization map, color-coded by country of publication, published on Scopus from 2002 to 2022 (created using VOSviewer).
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Interpretation of the Results on Spatial Distribution

Using the Scopus database to analyze the global research contributions to the study of biodiversity’s impact on pollen allergies has yielded valuable insights. The search query “pollen AND allergy AND biodiversity AND plant” produced 61 publications, and the first paper was published in 2002, underscoring the field’s growth. The inclusion of “plant” as a keyword restricted the results to just 20 publications, indicating that the broader context of biodiversity might be essential for understanding its effects on pollen allergies [9,13].
Our analysis highlighted the involvement of 47 countries in these publications. Notably, among the countries contributing most significantly to this research, Spain and the USA each published twelve papers. They were followed by Germany and France, with nine papers each, while Italy, Finland, and others showed strong linkages despite fewer publications. This finding reflects the collaborative nature of the research in this field, as exemplified by the connections between Finland and Costa Rica, Italy and Turkey, and the UK with Germany and France. Overall, the European countries led the research efforts with seventy-five documents, followed by Asia (twenty-one papers), North and South America (fifteen papers each), Oceania (six), and Africa (four). This distribution emphasizes the global interest in understanding the intricate relationships between biodiversity and pollen allergies, which can have profound implications for public health and environmental policy.
We suggest that the predominance of European countries in this research underscores a potential regional focus on biodiversity’s ecological impacts and the public health challenges associated with pollen allergies. The findings align with broader trends identified in the recent scholarly literature [40]. For instance, a study analyzing the airborne pollen trends across Europe highlights the significant role of climate change in altering pollen levels, which has direct implications for public health [25]. Specifically, increasing temperatures and CO2 levels have contributed to longer and more intense pollen seasons, exacerbating allergies like allergic rhinitis and asthma. These trends reflect the broader environmental and public health challenges faced by European populations.
Climate change and urbanization are linked to the rising incidence of pollen allergies [40]. Pollen grains are one of the main drivers behind allergic diseases in Europe, and the loss of biodiversity further complicates this by disrupting the ecological balances that control allergenic species. Together, these findings align with the scholarly literature that points to biodiversity loss and climate change as critical factors in the increasing prevalence of pollen-related allergic diseases in Europe [25].
As for further implications, the growing body of research on biodiversity and pollen allergies highlights the need for continued interdisciplinary collaboration and public health initiatives. Policymakers and researchers must work together to enhance awareness regarding the ecological factors influencing pollen allergies and to develop strategies that promote biodiversity conservation. The involvement of multiple countries in this research emphasizes the importance of a global perspective in addressing environmental and health challenges. The interconnectedness of research findings can lead to more effective allergen management strategies and contribute to better public health outcomes. In-depth investigation into the causal links between biodiversity and pollen allergies will be essential for informing future studies and health policies.

4. Discussion

In recent decades, the rise in allergic respiratory diseases has been linked to declining biodiversity, although directly establishing this link is challenging [31,40]. Studying pollen sheds light on this relationship, offering insights into the environmental impacts on pollen allergies [22,41]. Pollen allergy stands at the intersection of public health and environmental science as well as the related disciplines, emphasizing the need for interdisciplinary research and international collaboration to address these interconnected challenges in an evolving research landscape. In this paper, we aimed at contributing to the scientific knowledge by synthesizing the current research on the biodiversity decline and pollen allergies from 1998 to 2022 with the VOSviewer mapping software [19]. Notably, in bibliometric studies, the software choice presents both opportunities and challenges [42]. VOSviewer, a popular tool for mapping bibliometric networks, excels at visualizing co-authorship, co-citation, and keyword co-occurrence. However, its performance can be hindered by memory allocation issues when processing large datasets, leading to crashes or reduced efficiency. Additionally, its dependence on the Java Runtime Environment can cause visualization difficulties, particularly with complex networks. We mitigated these issues by optimizing the dataset and monitoring memory usage, ensuring effective use of VOSviewer to reveal the key research trends.
As for the research question on how the research on the effects of biodiversity loss on pollen allergies has changed in the last few decades, we found that, until the 21st century, only a handful of scientific papers existed on the relationship between biodiversity loss and pollen allergies. These early papers focused particularly on basic keywords such as ecosystem, reproduction, and seeds [43]. However, terms such as ethnoecology, fire ecology, and landscape ecology also shaped the first aspects of the research [44]. With the beginning of the current century, the research activity increased noticeably. During this period, keywords such as trees, flowers, crops, plant physiological phenomena, environment, and agriculture gained prominence in terms of research interest [30,45]. Notably, the understanding of the interactions between pollen, biodiversity, and the environment deepened. Starting from 2007, the research increasingly focused on specific areas, such as keywords related to reproduction, including pollination, animals, insects, and bees [26,29]. Also, such frequently used keywords as biological evolution, genetically modified plants, genetic models, and chloroplast DNA indicated increasing research interest in genetic factors [3,9,10], and keywords such as population dynamics, introduced species, and conservation of natural resources reflected the growing understanding of pollen allergy in the context of the changing environmental conditions [8].
Our bibliometric analysis highlights the rapid evolution of the research on the impact of biodiversity loss on pollen allergies, transforming this field from a niche topic into a critical intersection of public health and environmental science over the past two decades [10]. This shift reflects the growing awareness of the complex interactions between environmental changes and human health, driven by a broadening of the research topics from basic ecological studies to more comprehensive examinations of climate change, genetic factors, urbanization, and sustainability [39]. Over the past decade, the research landscape on pollen allergies and biodiversity has once again expanded considerably. Keywords such as genetic variation, introduced species, climate change, and conservation remained important and reflected the ongoing efforts to understand the genetic and ecological factors that influence pollen allergies [5,39,46]. The recent research has increasingly focused on topics such as forests, plant nectar, and pollen limitation [24]. Microbiota and bacteria have also become of great interest in research on biodiversity and pollen allergies [13,47].
The increasing focus on climate change in pollen allergy research is particularly noteworthy. Numerous studies have demonstrated that climate change is altering the distribution, abundance, and seasonality of allergenic pollen, exacerbating the health risks for allergic individuals [1,22,37,48]. One reason might be that rising temperatures and increased CO2 levels prolong pollen seasons and intensify pollen production, leading to higher exposure and greater sensitivity among susceptible populations. This underscores the need for further integrated studies that examine the combined effects of climate change and biodiversity loss on pollen allergies. Urbanization is another critical factor influencing the prevalence and severity of pollen allergies. Urban areas often experience higher concentrations of air pollutants, such as ozone and particulate matter, which can interact with pollen to increase its allergenic potential [41]. Studies suggest that urbanization, coupled with the “urban heat island” effect, can enhance pollen production and prolong pollen seasons, further intensifying the burden on allergy sufferers. Addressing the intersection of urbanization, air quality, and pollen exposure is crucial for developing comprehensive strategies to manage pollen allergies in rapidly growing urban environments.
The evolving research focus also suggests that future studies should prioritize areas that have received less attention, such as the impact of invasive species on pollen allergies. Invasive plant species can introduce new allergenic pollen into ecosystems, potentially increasing the prevalence and severity of allergies in the affected regions [21]. Understanding these dynamics is essential for accurate risk assessments and for developing targeted public health interventions. Another critical area for future research involves the genetic factors that influence individual susceptibility to pollen allergies. The advances in genomics and personalized medicine offer new opportunities to identify the genetic markers associated with allergic responses, enabling more precise risk assessments and tailored prevention strategies [9,38,47]. These developments could lead to improved management of pollen allergies, particularly in regions experiencing significant environmental changes due to climate change and biodiversity loss [31,39].
An additional research question to consider was whether European countries have made the most substantial research contributions regarding the relationship between biodiversity loss and pollen allergies [25]. Our analysis confirms that European countries have indeed been at the forefront of the research on biodiversity loss and its impact on pollen allergies. The bibliometric data show that a substantial proportion of the research output in this field originates from Europe, particularly from countries like Germany, Italy, and the United Kingdom [38]. This dominance can be potentially attributed to several factors, including Europe’s rich biodiversity, the high prevalence of allergic diseases in the region, and the continent’s strong emphasis on environmental and public health policies. Europe’s leadership in this research area is also reflected in the collaborative nature of the studies, with many research projects involving multiple institutions across different countries. For example, EU-funded programs have significantly contributed to understanding the links between environmental changes and health outcomes [9]. Furthermore, the European research often benefits from comprehensive environmental data collection systems and a strong tradition of epidemiological studies, which provide a robust foundation for investigating the public health implications of biodiversity loss [5,46].
These factors might have enabled European countries to make significant contributions to the global knowledge on how environmental factors, such as biodiversity loss, affect the incidence and severity of pollen allergies. However, we suggest that trends such as the increased personal mobility of researchers and international collaborations are blurring the distinction of the contributions being predominantly from a single continent.
Despite the numerous positive effects of green spaces on human health, plants are the source of allergenic pollen in the first place. So, the logical conclusion is that, the more allergenic plants there are near the living space, the higher the probability of contact with aeroallergens in the form of pollen [15]. The amount of specific allergenic pollen present in the breathing air and the duration of this exposure determine the intensity of the allergy symptoms in atopic patients [48]. The pollen supply relevant for allergy sufferers is significantly determined by the species diversity, i.e., by the amount, composition, and variety of the respective allergenic plants. The more plants of a specific allergenic species that are present in a defined green area, e.g., in the sense of a monoculture, the more pollen is present and the higher the respective allergy risk [17,22].
The plant biodiversity, and thus aeroallergen diversity, within green spaces is currently, and is expected to be in the future, undergoing significant changes [37]. This is due to numerous reasons, such as changes in land use for agriculture and living. On the one hand, there is the trend to cover more and more green areas with concrete, which results in the dwindling presence of grassland and arable land and thus less exposure to a variety of different grass pollens [49]. On the other hand, oil crops such as rapeseed are grown for agricultural use, and the changed supply regarding plant diversity could lead to exposure to other new types of allergenic pollen [22].
Travel and global trade, combined with climate change, are also changing the biodiversity compositions within green spaces. There is a carry-over of native plants, which can gain a foothold as neophytes in new areas and act there as new allergens [17,22], such as ragweed or pellitory now being found further north within Europe than they were originally. Due to the changing climatic conditions within Europe, many green plants are becoming native to new areas where the ideal temperatures for them prevail. An example of this is the allergenic birch, which requires a certain period of low temperatures to flower (the so-called chilling effect) and is forced by climate change to migrate to higher altitudes and latitudes. This pattern is also followed by numerous other alpine plant species, and there is a general upward migration of many tree taxa. This migration alters and threatens biodiversity both at higher elevations, where the existing species are displaced, and at lower elevations, where other species may suddenly become more prevalent [17].
In our study, we applied bibliometric analysis to assess the research output on the relationship between biodiversity loss and pollen allergies. Distinguishing our method from scientometric studies and literature reviews, bibliometric methods focus on quantifying the research output by analyzing the publication trends, citation counts, and keyword co-occurrences [42]. Using this approach, we explored the research contributions by tracking terms like “pollen”, “plant”, and “biodiversity” across scientific publications. This method enabled us to reveal the key trends and thematic clusters within the field, as well as the patterns of global collaboration. Bibliometric studies provide insights into the evolution of specific research topics [50]. For example, our analysis showed an increasing trend in research on pollen allergies in connection with environmental factors, reflecting the heightened public and scientific awareness of climate change and biodiversity loss and the impact on allergic diseases [5,10,39]. By mapping the collaborations between countries, we also identified the geographic distribution of the research contributions, showing that European countries were heavily involved in this area of study.
Compared to scientometric studies, which offer a more holistic view of the research ecosystems, taking into account aspects like research funding, institutional collaborations, and policy implications, our bibliometric analysis provides a targeted, empirical snapshot of the research output [21]. This complements the scientometric approaches by emphasizing the quantitative measurement of scientific progress. In contrast, comprehensive literature reviews synthesize the existing research to form a qualitative overview of a field, offering critical insights without extracting publication metrics [21]. While review articles are popular for interpreting research trends and identifying gaps in the available evidence, they do not aim at offering the same granular quantitative analysis as bibliometric approaches [41]. Taken together, we suggest that our bibliometric approach quantifies the research output and global collaboration patterns on biodiversity and pollen allergies, offering a clear empirical foundation. This approach complements the broader scope of scientometric studies and the qualitative depth of literature reviews, providing a well-rounded view of the research landscape.
This bibliometric analysis provides insights that can guide future research on the impact of biodiversity loss on pollen allergies. There is a pressing need for integrated studies that examine the interaction between biodiversity loss and allergenic pollen [10]. By approaching these factors in a holistic manner, researchers can gain a more comprehensive understanding of how environmental shifts reinforce or amplify allergic responses. Additionally, long-term studies are essential for mapping the evolving effects of biodiversity loss on pollen allergies, enabling more effective public health responses [13]. This includes investigating both the spread and intensity of allergenic pollen, as well as evaluating the preventive measures and emergency care protocols for allergy patients. Future studies should explore the impact of specific biodiversity losses across diverse geographic regions and ecosystems, employing long-term, data-driven methodologies [46]. This could lead to the development of predictive models that better anticipate pollen season shifts due to climate change. From a scholarly perspective, fostering interdisciplinary collaboration between medical experts and environmental scientists is crucial for unraveling the complex interactions between biodiversity loss and allergenic responses [5,38]. On a global scale, international collaboration could facilitate the exchange of knowledge, access to research resources, and development of common strategies that are adaptable to diverse geographic regions [5,39]. We suggest that such research might help to mitigate the risks posed by biodiversity loss on a global level, ensuring that the solutions are applicable across different ecological and social contexts.

5. Limitations

While bibliometric analysis provides valuable insights into research trends and the evolution of scientific knowledge [20], several limitations should be acknowledged to contextualize the findings of this study. Firstly, the biases inherent in scientific literature can significantly influence the outcomes of bibliometric studies. Publication bias is a well-known issue where studies with statistically significant results are more likely to be published, potentially leading to an overrepresentation of certain findings in the literature [51]. Additionally, language bias is a concern as studies published in English are often more frequently cited, skewing the analysis towards English-language publications. This limitation is particularly relevant for our study as the VOSviewer software used for the analysis processes text files primarily in English, which may have excluded important contributions in other languages.
The selection of search terms and databases introduces another potential limitation. The choice in keywords and the formulation of search queries are critical factors that can impact the comprehensiveness and scope of the results. For instance, searching for “pollen AND biodiversity” yielded more results than the more specific query “pollen AND biodiversity AND plant”, demonstrating how the search term specificity can influence the outcomes [52]. Additionally, the use of synonyms and variations of key terms, such as “allergy”, might not have been fully captured, potentially leading to the omission of relevant studies. The misinterpretation of keywords due to the lack of context for individual words in a bibliometric analysis is another challenge as terms can have different meanings depending on the context in which they are used [53].
Database selection also plays a crucial role in bibliometric studies. Different databases, such as Scopus, Web of Science, and PubMed, vary in their coverage of journals and publications, which can lead to variations in data completeness and quality [54]. Furthermore, the quality, reliability, and currency of the data within these databases are critical factors that can affect the accuracy and relevance of the findings. Another significant limitation is the reliance on citation counts as a measure of the research impact. The citation counts may not always reflect the true influence or quality of a paper as highly cited papers might simply address popular topics rather than represent groundbreaking research. This limitation is particularly important when considering that some fields may have inherently higher citation rates than others, leading to potential misinterpretations of the data.
Lastly, the evolving nature of scientific language and terminology poses challenges for bibliometric analysis. As scientific language changes over time, the consistency and interpretation of keyword analyses can be affected, leading to potential inaccuracies in trend identification [20]. For example, the terms used to describe certain phenomena or concepts may evolve, and older studies may use different terminology than more recent research, complicating longitudinal analyses.

6. Conclusions

This bibliometric analysis highlights the growing scholarly interest in understanding how environmental factors such as biodiversity loss intertwine with the public health concerns on the example of pollen allergies. Our study reflects the existing research landscape, which shows a higher volume of research in this field in Europe compared to other regions. This trend highlights a potential research gap globally, and we suggest that future studies should explore this relationship in non-European contexts to provide a more comprehensive global understanding. Also, the speed at which changes in the climate and the environment occur underscores the importance of continuing interdisciplinary research and fostering international collaboration. To effectively tackle global challenges, it is crucial for environmental scientists, ecologists, and health professionals to work together and share their findings across borders. The ever-changing nature of this research field means that researchers and public health officials need to stay alert and adaptable. Policymakers should take into account the expanding research on how biodiversity loss affects pollen allergies when designing health policies. Additionally, clear communication strategies can help to address immediate health issues, but they also support the broader sustainability goals by integrating environmental and health perspectives into policy and practice.

Author Contributions

Conceptualization, D.H.; Data curation, K.B.; Formal analysis, K.B.; Investigation, K.B. and D.H.; Methodology, K.B. and D.H.; Project administration, D.H.; Resources, D.H.; Software, K.B.; Supervision, D.H.; Validation, K.B. and D.H.; Visualization, K.B.; Writing—original draft, K.B. and D.H.; Writing—review and editing, K.B. and D.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was financially supported by the Austrian Science Fund (FWF), Project Dr. FOREST, Grant number I 4411 (funding to Daniela Haluza).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

No new data were created. The paper is based on the diploma thesis “Impact of climate change, air pollution and dwindling plant biodiversity on Type 1 pollen—A bibliometric analysis” of 2023 by Karoline Braun, supervised by Daniela Haluza.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Keywords—network visualization map of complete dataset (1998–2022, created using VOSviewer).
Figure 1. Keywords—network visualization map of complete dataset (1998–2022, created using VOSviewer).
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Table 1. Important keywords on biodiversity per cluster, listed according to their occurrences (Occ.) and total link strength (TLS).
Table 1. Important keywords on biodiversity per cluster, listed according to their occurrences (Occ.) and total link strength (TLS).
Cluster Pollen EcologyCluster Genetics
Occ.TLS Occ.TLS
Pollen4201975seeds90473
Biodiversity2011063phylogeny85391
Ecosystem155898genetic variation65362
Plants119644gene flow61330
Trees71412microsatellite repeats45285
conservation of natural resources47306genetics, population42284
Fossils54290biological evolution48257
climate change58288dna, plant40250
Geography42282endangered species43239
Humans69277genotype22148
population dynamics43259sequence analysis, dna23141
Seasons41224models, genetic21139
Agriculture35203evolution, molecular22134
Climate33193phenotype25129
Forests30173hybridization, genetic29127
Cluster PollinationCluster Pollinators and Microbiota
Occ.TLS Occ.TLS
species specificity2441236animals2941565
Flowers1891014bees139745
Reproduction95538plant nectar31151
Insecta61413microbiota32136
species specificity53319feeding behavior20128
introduced species63306bacteria2289
Magnoliopsida49278
Ecology36240
models, biological31201
plant physiological phenomena26188
Fruit23151
Birds23150
pollen limitation2091
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Braun, K.; Haluza, D. Impact of Biodiversity Loss on Pollen Allergies: A Bibliometric Analysis. Sustainability 2024, 16, 9285. https://doi.org/10.3390/su16219285

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Braun K, Haluza D. Impact of Biodiversity Loss on Pollen Allergies: A Bibliometric Analysis. Sustainability. 2024; 16(21):9285. https://doi.org/10.3390/su16219285

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Braun, Karoline, and Daniela Haluza. 2024. "Impact of Biodiversity Loss on Pollen Allergies: A Bibliometric Analysis" Sustainability 16, no. 21: 9285. https://doi.org/10.3390/su16219285

APA Style

Braun, K., & Haluza, D. (2024). Impact of Biodiversity Loss on Pollen Allergies: A Bibliometric Analysis. Sustainability, 16(21), 9285. https://doi.org/10.3390/su16219285

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