Abstract
The provision of ecosystem services in agriculture depends on the use of conservation practices and the biodiversity of each agroecosystem. In Brazil, however, knowledge and tools for evaluating the impact of different cultivation systems on the provision of ecosystem services remain deficient in several agroecosystems. We assessed whether the availability of support and regulation services provided by aquatic insects differs between rice fields irrigated under conventional and organic systems. A framework was implemented based on functional traits and the ecological functions performed by each taxon. Insect traits related to pollination capacity, soil fertilization and pest control were selected for analysis. Greater availability of soil fertilization services in conventional rice fields and pest control services in organic rice fields was detected. This study demonstrates the efficiency of the framework based on functional traits for the integrated assessment of ecosystem services in rice fields, being useful to support sustainable strategies in agriculture.
Keywords:
Agriculture; agroecology; aquatic entomofauna; associated biodiversity; sustainability
Resumo
A oferta de serviços ecossistêmicos na agricultura depende do uso de práticas conservacionistas e da biodiversidade de cada agroecossistema. No Brasil, porém, o conhecimento e ferramentas para a avaliação do impacto de diferentes sistemas de cultivo sobre a oferta de serviços ecossistêmicos seguem deficientes em vários tipos de agroecossistemas. Avaliou-se se a disponibilidade de serviços de suporte e regulação fornecidos por insetos aquáticos difere entre arrozais irrigados em sistemas convencional e orgânico. Implementou-se um framework baseado em atributos funcionais e nas funções ecológicas desempenhadas por cada táxon. Selecionou-se para análise atributos de insetos relacionados à capacidade de polinização, fertilização do solo e controle de pragas. Detectou-se maior disponibilidade de serviços de fertilização do solo em arrozais convencionais, e de controle de pragas em arrozais orgânicos. Este estudo demonstra a abrangência do framework baseado em atributos funcionais para avaliação integrada de serviços ecossistêmicos em arrozais, sendo útil para subsidiar estratégias sustentáveis na agricultura.
Palavras-chave:
Agricultura; agroecologia; biodiversidade associada; entomofauna aquática; sustentabilidade
Resumen
La provisión de servicios ecosistémicos en la agricultura depende del uso de prácticas de conservación y de la biodiversidad de cada agroecosistema. Sin embargo, en Brasil, los conocimientos y las herramientas para evaluar el impacto de diferentes sistemas de cultivo en la prestación de servicios ecosistémicos siguen siendo deficientes en los agroecosistemas. Evaluamos si la disponibilidad de servicios de apoyo y regulación proporcionados por los insectos acuáticos difiere entre los campos de arroz regados en sistemas convencionales y orgánicos. Se implementó un marco basado en los atributos funcionales y las funciones ecológicas realizadas por cada taxón. Se seleccionaron para el análisis los atributos de los insectos relacionados con la capacidad de polinización, la fertilización del suelo y el control de plagas. Se detectó una mayor disponibilidad de servicios de fertilización de suelos en arrozales convencionales y de servicios de control de plagas en arrozales orgánicos. Este estudio demuestra el alcance del marco basado en atributos funcionales para la evaluación integrada de servicios ecosistémicos en campos de arroz, siendo útil para apoyar estrategias sostenibles en agricultura.
Palabras-clave:
Agricultura; agroecología; biodiversidad asociada; entomofauna acuática; sostenibilidad
Introduction
One of the goals of the 2030 Agenda for Sustainable Development covers the stimulus to sustainable food production systems and resilient agricultural practices (FAO, 2018). Such systems are important for the 2030 Agenda because of their role in food security insofar as they provide a broad spectrum of ecosystem services (MEA, 2005). Swinton et al. (2007) detail how proper management of agricultural systems can provide a wide range of ecosystem services that benefit not only agriculture but also water resource regulation, carbon sequestering, erosion contention, agritourism, etc. In turn, Power (2010) underscores the relationship between proper and improper management of agricultural systems and the respective flows of ecosystem services and ‘disservices’ stemming from them (e.g. deforestation, pesticide pollution, loss of biodiversity, etc.).
The Convention on Biological Diversity (2008) states that the maintenance of biodiversity and the ecosystem services are crucial to agriculture and should be incorporated into public policies. In that context, there is increasing emphasis on the role of non-agricultural living organisms found in agroecosystems, that is, agrobiodiversity, in regulating ecosystem services in agricultural systems (Altieri, 1999). Many biodiversity components associated with agricultural systems do effectively offer or contribute to various ecosystem services (FAO, 2019).
Recently, governments and international development agencies have been adopting programs to stimulate agricultural practices that protect biodiversity and ecosystem services in agricultural systems (FAO, 2019; Convention on Biological Diversity, 2020). In Brazil, Federal Government policies to support sustainable agricultural practices are relatively recent (Parron; Garcia 2015). Initiatives like the National Agroecology and Organic Production Plan (Plano Nacional de Agroecologia e Produção Orgânica) seek to foster the sustainable use of agrobiodiversity (FAO, 2019) in alignment with the National Payment for Ecological Services policy instituted by Federal Act nº 14.119/2021 (Brasil, 2021).
Despite the inclusion of the themes of biodiversity and ecosystem services in food security and sustainability policies, there are still many technical gaps to fill. As an example, the functions of many agrobiodiversity components are still poorly understood (FAO, 2019). Wood et al. (2015) state that an understanding of biodiversity’s role in the ecosystem services of agriculture is restricted to just a few processes and types of service. Furthermore, according to the FAO (2019) the lack of data on the relation of ecosystem services in agricultural systems to the respective biodiversity has the effect of hampering the planning and prioritizing of measures to foster the implementation of sustainable practices in agriculture. Furthermore, the FAO (2023) considers that the assessment and valorization of ecosystem services are the first important steps towards acknowledging the degree to which they contribute to agriculture.
In regard to the aspect of sustainability in agriculture, the investigation of ecosystem services provided by the associated biodiversity is normally related to the need for integrated studies that identify conflicting demands between the ecosystem services and disservices of agricultural activities (Power, 2010; Wood et al., 2015; Saunders et al., 2016). In that context, Wood et al. (2015) propose that a functional traits approach could make a strong contribution towards predicting how ecosystem services vary according to agricultural practices. The idea that species can provide information on ecosystem services is linked to the ecological knowledge of the role each species plays in the natural environment (Cadotte et al., 2011; Carlucci et al., 2020).
Invertebrates make up the greater part of the biodiversity associated with agroecosystems (Saunders et al., 2016) and the entomofauna is the animal group with the greatest number of known species (Rafael et al., 2012). Especially in the field of agriculture, research has identified a series of benefits that aquatic insects provide to agriculture among which are support services like soil fertilization and pollination, and regulatory services like pest control (Raitif et al., 2019). Prather et al. (2013) have described the biological control that generalist predators like insects of the Odonata order perform. However, Macadam and Stockan (2015) point out that many of such services actually depend on the characteristics of each taxon. The rate of organic matter decomposition, for example, is strongly dependent on shredding insects such as Diptera of the Chironomidae family (Raitif et al., 2019). Benthonic larvae of the Odonata and Ephemeroptera orders and Trichoptera larvae with their burrowing habit, stir up sediments, contributing towards bioturbation and bio-irrigation (Macadam; Stockan, 2015).
Brazil is the greatest rice producer in the Americas and the State of Rio Grande do Sul is responsible for 70% of its national production (IRGA, 2022). In irrigated rice fields, insects make up most of the invertebrate biomass (Bambaradeniya; Amarasinghe, 2003). In conventional rice fields, herbicides and pesticides are used to control weeds and insects and that tends to diminish the diversity of aquatic insects (Stenert et al., 2018). Furthermore, prior to irrigation and after the rice has sprouted, that cultivation system involves the application of nitrogen, potassium, and phosphorus-based fertilizers to the crop. Linke et al. (2014) report that in organic systems water levels are carefully managed prior to, and during the crop-growing period. Prior inundation of the field stimulates plant germination and their organic material is incorporated to the soil during the process of preparing the land for crop cultivation. The same strategy could be employed to combat both weeds and undesirable insects during the crop growing period (Linke et al., 2014). Other authors relate the application of pesticides to differences between the taxonomic and functional compositions of aquatic insects in organic rice fields and those in conventional ones (Dalzochio et al., 2016).
Even though Brazil is one of the world’s most important food producers, according to Brazil’s Environment Services in the Rural Landscape Network (Rede de Serviços Ambientais na Paisagem Rural Brasileira) (Prado et al., 2015), there is a lack of knowledge about environmental services in the rural sector. Most of the research on ecosystem services in agriculture focuses on agroforestry systems and tropical regions while works evaluating ecosystem services availability in Brazilian rice fields are nonexistent. Given that scenario, the present research has sought to test the hypothesis that, in the irrigated rice fields of southern Brazil, there are differences in the availability of ecosystem support and regulation services provided by aquatic insects between the conventional and the organic cultivation regimes. Considering that conventional systems tend to support a lesser diversity of aquatic insects than organic ones, we expect to find greater availability of ecosystem services in organic rice fields.
Material and methods
Study area
The studied rice fields are located in three municipalities of the State of Rio Grande do Sul. The regional climate is humid subtropical, with an annual average temperature of 17º C, and an average annual rainfall of 1,400 mm, without a marked dry season (Rio Grande do Sul, 2021). We sampled two conventionally-cultivated rice fields about 1 km apart in the municipality of Cachoeira do Sul (C1 and C2 in Figure 1), and two organic rice fields: one in the municipality of Sentinela do Sul (O1) and the other in the municipality of Santa Vitório do Palmar (O2) (Figure 1). Site selection met the following criteria: (i) irrigated cultivation; and (ii) pesticide use in the conventionally-cultivated rice fields and non-use of pesticides in the organic ones. Irrigation channel widths ranged from 1.5 to 2.5 m. The rice fields in Sentinela do Sul were irrigated from artificial reservoirs. The rice field in Santa Vitória do Palmar was irrigated from a natural lake.
Location of the studied rice fields. Abbreviations: (C): rice fields under conventional cultivation system; (O) rice fields under organic cultivation system.
Spatial autocorrelation analysis
The spatial independence of the biotic composition of the studied rice fields was tested using the Moran’s Eigenvector Maps method (Legendre; Legendre, 2012). As the test did not detect any significant spatial structure in the global variation of aquatic insect composition among the studied sites (P = 0.375), we did not include the geographical location of the rice fields in the subsequent analytical procedures.
Framework implementation
This exploratory study sets out to implement a framework proposed by Wood et al. (2015), which integrates species taxonomic and functional traits to evaluate availability of ecosystem services in agricultural systems. Researchers have increasingly recognized the use of the functional traits of species present in a biological community as an important environmental assessment tool in the context of ecosystem services (Cadotte et al., 2011). The framework proposed by Wood et al. (2015) covers six stages, briefly described below:
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Stage 1: Identify the agroecosystem components (e.g., crop species, cultivation system) and determine the sample units;
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Stage 2: For each component, determine the ecosystem service of interest and measure it in the sample units determined in Stage 1;
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Stages 3-4: For each component, identify the taxonomic biotic composition and determine the abundance of the taxa that are important for the ecosystem service of interest;
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Stage 5: Determine and measure the functional traits (e.g. morpho-physiological and behavioral characteristics) of the taxa deemed as important to the ecosystem service of interest;
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Stage 6: Compare the functional and biotic metrics (diversity indicator parameters, e.g. richness, composition, dominance, equitability, taxa, and trait variance) of the agroecosystem components under study to infer whether there are any variations in the ecosystem services offer.
Delimitation and selection of classes of service provided by aquatic insects
After Stage 1 (agroecosystem components definition: rice fields, organic and conventional cultivation systems) Stage 2 was initiated, that is, the delimitation of the classes of service that the aquatic insects provide directly to agriculture which Raitif et al. (2019 consider to be pollination, soil fertilization and pest control. Prather et al. (2013) reviewed the way in which invertebrates influence ecosystem services, classifying them according to the structure that the MEA (2005) recommends.
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Provisioning services: provided by ecosystems and offered to society directly through consumption or trade, e.g. foods, fibers, wood etc.;
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Supporting services: provide the conditions needed to make other services available, e.g., nutrient cycling, decomposition, primary production, soil fertilization maintenance, pollination, seed dispersal;
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Regulation services: obtained through the maintenance of the stability of ecosystem processes, e.g. carbon sequestering, air and water purification, mitigation of extreme climate events, hydrological maintenance, pest control;
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Cultural services: recreational, educational, spiritual or aesthetic-landscape related benefits that contribute to social wellbeing, e.g., leisure, tourism, recreation, aesthetic and spiritual experiences, etc.;
The theoretical basis underlying the relationship between functional traits and the ecosystem services of interest is described below (Table 1).
Sampling and laboratory procedures
Stages 3 and 4 (determination of the composition and abundance of the taxon of interest) were conducted according to the following sampling and laboratory procedures: the sampling of insects took place during the 2021/2022 harvest period. Each rice field was sampled on four occasions (October, November and December 2021 and March 2022) thereby embracing the period of irrigation of the rice. No sampling was done in January or February due to the effects of the La Niña climate phenomenon. Collection was done in triplicate on each occasion in each rice field, adding up to 15 samples at the end of the sampling period. Collection involved making 1 meter sweeps of the sediment with an appropriate 0.2 mm mesh water net. The samples were fixed in 85% ethanol. In the laboratory the samples were washed in a 0.25 mm mesh sieve to remove detritus. The specimens were screened using a magnifying glass and identified on the basis of specialized bibliography (Merritt et al., 2008) and consultations with specialists. Samples were identified to the smallest possible taxonomic level and the insects were eventually deposited in the UNIVATES’ Natural Sciences Museum.
To estimate the ecosystem services available in the rice fields under study, the aquatic insects were grouped according to functional traits that could potentially be related to the ecosystem services of interest, based on the relevant literature (Dalzochio et al., 2016; Macadam; Stockan, 2015; Prather et al., 2013; Raitif et al., 2019; Suter; Cormier, 2014): habit, food chain trophic groups, and tolerance to pesticides. Table 2 below describes the categorization of each identified taxon and its potential effect on the offer of the ecosystem service of interest together with the theoretical foundations that relate its functional traits with the ecosystem service of interest.
Data analysis
To evaluate the differences in the taxonomic and functional composition of the aquatic entomofauna between the rice fields under different cultivation systems, a permutational variance analysis (PerMANOVA) was used with a significance level established as 5% (after 999 permutations). In this step, the assemblage taxonomic composition was weighted by the abundance of each taxon (log-transformed = logX+1), to reduce the influence of the abundant taxa in the analysis. The dissimilarity matrix of the composition was calculated based on the Bray-Curtis coefficient. To quantify the functional composition of the aquatic entomofauna of rice fields under different cultivation systems, the study used the community-weighted mean (CWM) which estimates the presence of an ecological role on the basis of the weighted abundance of the taxa in a given community that exhibits the trait under analysis (Laliberté et al., 2014). At that stage, given the binary nature of the traits, Gower’s coefficient was used to obtain the functional dissimilarity matrix of the species and the Bray-Curtis coefficient to obtain the functional dissimilarity of the communities.
To enable the graphic visualization of the differences in the total set of ecosystem services between the rice fields under different cultivation systems, a sorting diagram was generated based on a Principal Coordinates Analysis (PCoA) and taking into account the same dissimilarity matrix used for the PerMANOVA. Lastly, to evaluate whether there were any variations in the potential availability of ecosystem services between organic and conventional rice fields (based on the categorization of the service each taxon could potentially provide), a second functional matrix was generated, this time according to classes: fertilization, pollination, and pest control (Table 2).
Using the same procedure as that for the sorting graphs, from a second CWM matrix for services provided, mean values were adjusted for each ecosystem service to visualize any association between them and the respective type of environment. At every stage the potential effect of seasonal variation (collection event) was controlled for using the ‘condition’ function in the respective analysis routine. All the routines were elaborated in the R 4.03 statistical program. The services CWM matrix was calculated using the dbFD of the FD package (Laliberté et al., 2014). The PerMANOVA was conducted using the adonis function, the PCoA with the capscale function and the adjustment of the services scores to the PCoA with the envfit function using functions available in the vegan package (Oksanen et al., 2020).
Results
We collected 680 specimens distributed among 16 genera from 13 families and six orders (Table 3). Seven genera were recorded in the conventionally-cultivated rice fields and 15 genera in the organic ones (Table 3). The taxonomic composition of the entomofauna significantly varied between cultivation systems (F1.14 = 2.46; R2adj = 0.15; P = 0.004). Sigara Fabricius, 1775 (Hemiptera, Corixidae) and Erythrodiplax Brauer, 1868 (Odonata, Libellulidae) were the most abundant genera in the organic rice fields, while Chironomus Meigen, 1803 (Diptera, Chironomidae) and Tropisternus Solier, 1934 (Coleoptera, Hydrophilidae; 6%) were the most abundant genera in the conventional rice fields (Table 3). The occurrence of taxa from the orders Odonata and Hemiptera was associated with the organic rice fields while of Diptera taxa, with conventional ones (Figure 2).
The functional composition of insects also significantly varied between organic and conventional rice fields (F1.10 = 6.87; R2adj = 0.31; P = 0.004). Insects with a high or medium level of tolerance to pesticides, collector trophic groups, and benthic habit (Chironomus, Tropisternus) were associated with conventional rice fields, whereas insects with predatory trophic groups and low pesticide tolerance (Odonata), were associated with organic rice fields (Figure 2b). Lastly, the potential composition of available ecosystem services also varied between cultivation systems (F2.15 = 2.9; P = 0.029). While the potential availability of soil fertilization (Chironomidae and Elmidae families) and pollination (Coleopters Order) services was more closely associated with conventional rice fields, the potential availability of pest control services (Odonata and Hemiptera orders) was more associated with organic rice fields (Figure 2c).
a) Association of taxa with cultivation systems; b) Functional diversity associated with cultivation systems; c) Association between potential availability of ecosystem services of interest and cultivation systems.
Discussion
The application of a framework based on the species’ functional traits demonstrated the outreach of that approach in assessing the availability of ecosystem services provided by the biodiversity associated with irrigated rice fields under different forms of cultivation in the south of Brazil. In addition to the usually employed occurrence of taxa in each location (Cadotte et al., 2011), this framework considers the ecological functions performed by each one of them (Wood et al., 2015), making it possible to estimate the ecological processes and, accordingly, the environmental services present in the environment in question.
The framework that Wood et al. (2015) proposed enables an understanding of how ecosystem services vary with different management practices in agricultural systems. The data stemming from the framework can be integrated with predictive approaches to generate specific objectives that maximize the offer of multiple ecosystem services (Wood et al., 2015). Thus the properties of that framework are in alignment with the FAO (2019) call for increased valorization, in agriculture, of associated biodiversity components in their aspect as ecosystem services providers.
In their work, Ferraz et al. (2019) state that researchers must be capable of assessing the impacts of anthropic actions on ecosystem services, and of proposing methods for their evaluation and valorization. In that light, the framework proved to be useful for evaluating the effect of different cultivation systems on the potential availability of ecosystem services that are provided by an important element of the biodiversity associated with irrigated rice systems (i.e. the aquatic entomofauna).
Regarding the relations between the cultivation systems and the ecosystem services offered, our results show that there was a variation in the potential availability of ecosystem services that aquatic insects provide between organic rice fields and conventionally cultivated ones. According to Maltby et al. (2017a: 2017b), differences between cultivation systems interfere with the ecosystem structure not only through their direct impacts on the species, but also insofar as they select species with different ecological functions. Those impacts directly affect the environment’s capacity to generate ecosystem services (Awuah et al., 2020; Liu et al., 2020). This result shows that it was possible to map the conflicting demands between costs and benefits of the interactions between the biodiversity and the associated agricultural systems under different forms of cultivation (Power, 2010; Wood et al., 2015) as recommended by authors who favor a mapping of the agricultural cycle with a much broader outreach (Saunders et al., 2016).
In regard to the association between the organic system and pest control services, this result involves establishing large taxa with predatory and generalist habits such as insects of the Odonata and Hemiptera orders. Dalzochio et al. (2016) found that organic crop management can favor the occurrence of Odonata. Prior to that, researchers (Landis et al., 2000; Yasumatsu et al., 1975) had verified the role of Odonata species as predators of potential rice field pests. Similarly, insects of the Hemiptera order (also highly abundant in organic rice fields) can be efficient controllers of disease vectors; experimental studies have demonstrated that Hemiptera of the Notonectidae family also have great potential for regulating populations of disease vectors such as mosquitos with aquatic larvae (Lacey; Orr, 1994; Prather et al., 2013). In that aspect, organic rice fields could act as potential reservoirs of regulation services
As for the greater association between the conventional cultivation system and the availability of pollination and soil fertilization services, this result reveals the dominance in them of generalist taxa typical of disturbed environments like Chironomidae, and of insects with benthonic and collector-gatherer habits like other Diptera species, or organic material shredders like Elmidae. Those taxa are capable of recycling organic material by means of various functions including bioturbation, bio-irrigation, and shredding (Macadam; Stockan, 2015). Another likely explanation is that association between conventional rice fields and the pollination offer is connected with the high frequency of occurrence of Coleoptera and Hemiptera in those agroecosystems, taxa capable of performing pollination in the adult stage of their cycles (Prather et al., 2013) and common in impacted rice fields (Dalzochio et al., 2016; Stenert et al., 2018).
Lastly, one of the probable sources of the variation between different cultivation systems in the potential offer of ecosystem services is related to the widespread use of pesticides in conventional rice fields. Rice fields under the continuous effect of pesticides present less abundance and richness of species in their waters during the period immediately after pesticide application (Stenert et al., 2018). In that sense, the impacts may have affected or damaged freshwater ecosystem functions due to the reduction of the performance and characteristics of the affected species (Oginah et al., 2023).
Final considerations
This article has underscored the potential of applying the framework that Wood et al. (2015) proposed to evaluate ecosystem services in agroecosystems. Integrating the species’ functional traits data with the biotic composition made it possible to estimate potential differences between different cultivation systems. That approach also enabled the estimation of variations in the support and regulation services that aquatic insects provide in irrigated rice fields under organic and conventional cultivation systems in the south of Brazil.
Framework implementation made it feasible to detect possible tradeoffs in the ecosystem services availability between the cultivation systems thereby demonstrating the method’s integrative capacity for monitoring the types and quality of ecosystem services that agroecosystems supply. Thus, the results show the potential of integrating taxonomic and functional data of agrobiodiversity as a tool to support strategies fostering sustainability in agriculture.
Even though this approach requires an additional step apart from the taxonomy, the use of this method corroborates the premise of Wood et al. (2015) in regard to suitability given its ability to extract more accurate information on the functioning of agroecosystems under different types of management.
That difference in the offer can easily be integrated to payment for environmental services policies. As an example, greater availability of regulation services in organic rice fields under organic cultivation can be incorporated to meso- or micro-regional public health strategies by providing incentives for landscape elements that assist in the maintenance of those species that control potential disease vectors.
Lastly, our results show that a greater ecosystem services offer in organic rice fields means fewer pests, less need for chemical control, and greater biodiversity, indicating an environment that is more balanced, healthier, and more complex in comparison with rice fields under conventional cultivation.
It is suggested that future research work could involve the replication of the tests for predators such as vertebrates that feed on insects to verify whether the detected differences in the services offer extends to other trophic levels. Another recommendation is that future studies involve more frequent sampling to see whether the presence of pesticides in conventional rice fields is unequivocally related to differences in ecosystem functions. Such studies could make it clear whether eventual differences in the effects offer are detectable in the observation of much broader spatial scales thereby enabling a more accurate assessment of the environmental costs and benefits of the different systems of rice crop management in Brazil.
Acknowledgments
We are grateful to the private landowners that granted us access to their properties to conduct the study. We also thank Carla Cenci Almeida and Cleber Sganzerla for help in fieldwork.
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Publication Dates
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Publication in this collection
16 May 2025 -
Date of issue
2025
History
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Received
18 Aug 2023 -
Accepted
16 Aug 2024



Font: Authors, 2025.
Font: Authors, 2025.