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Article

Ecological Niche Modeling of Invasive Macrophyte (Urochloa subquadripara) and Co-Occurrence with South American Natives

by
Tayna Sousa Duque
1,*,
Iasmim Marcella Souza
1,
Débora Sampaio Mendes
1,
Ricardo Siqueira da Silva
1,
Danielle Piuzana Mucida
2,
Francisca Daniele da Silva
3,
Daniel Valadão Silva
3 and
José Barbosa dos Santos
1
1
Department of Agronomy, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina 39100-000, Minas Gerais, Brazil
2
Department of Geography, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina 39100-000, Minas Gerais, Brazil
3
Department of Water and Soil Management, Universidade Federal Rural do Semi-Árido, Mossoró 59625-900, Rio Grande do Norte, Brazil
*
Author to whom correspondence should be addressed.
Sustainability 2023, 15(17), 12722; https://doi.org/10.3390/su151712722
Submission received: 18 July 2023 / Revised: 10 August 2023 / Accepted: 14 August 2023 / Published: 22 August 2023
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Abstract

:
Invasive macrophytes are considered problematic in natural environments and hydroelectric reservoirs. Climate changes, the occurrences of watercourses, and biotic interactions influence biological invasions of macrophytes. The abundance of native species can be positively or negatively correlated with the occurrences of invasives. Urochloa subquadripara is an invasive in natural or disturbed habitats co-occurring with the natives Eichhornia crassipes and Salvinia minima in South America. Aquatic plant communities can be altered by climate change, so species distribution models (SDMs) are important tools for predicting invaded areas. This study aimed to apply an SDM to study correlations of U. subquadripara with the potential distributions of native species E. crassipes and S. minima. Occurrence data for U. subquadripara, E. crassipes, and S. minima were collected from databases and in consultation with the published literature. Parameters encompassing biological information of the species were entered into the CLIMEX software and used to generate the Ecoclimatic Index (EI). The species co-occurrence was performed based on multicriteria decision-making (MCDM), and weights were assigned using the analytical hierarchy process (AHP). It was observed that U. subquadripara, E. crassipes, and S. minima had a higher occurrence in tropical and subtropical regions. However, it is predicted that these species may move to high latitudes from climatic changes. Considering climate changes, such as the increase in temperature and CO2, the risk of invasion by U. subquadripara in the northern hemisphere is mainly in lakes, whereas the areas conducive to invasions are rivers and reservoirs in the southern hemisphere. In general, emerging and floating macrophyte species such as U. subquadripara, E. crassipes, and S. minima will be favored, causing suppression of submerged species. Therefore, identifying the potential distribution of these species allows the creation of pre-invasion intervention strategies.

1. Introduction

Macrophytes serve as the primary producers in freshwater ecosystems and play a crucial role in various biotic interactions [1]. While these ecosystems host endemic species that traverse watercourses, they are also susceptible to invasions due to substantial pressure of propagules [2]. Invasive exotic species can cause changes in the native community, such as the extinction of macrophytes, amphibians, and fish [1,3]; it is estimated that global expenditures on combating biological invasions have reached approximately USD 1.3 trillion since 1970 [4].
Urochloa subquadripara (Trin) R.D. Webster, “tenner-grass” (synonymous with Brachiaria subquadripara, Brachiaria arrecta, and Urochloa arrecta) [5,6,7], is an emergent macrophyte, rooted near the margins, which has long, floating branches, forming mats on the surface of the water [8,9]. It is a Poaceae native to Africa and is invasive in tropical and subtropical regions [10].
Due to the easy propagation by stolons, rhizomes, or fragments that can be transported in water, the invasion of U. subquadripara raises concerns about water use and the suppression of biodiversity [9,11]. Furthermore, the species can grow as an epiphytic life form, rooted on the banks but extending on the surface of the water using floating macrophytes such as Pistia stratiotes and Eichhornia crassipes as support [12].
Urochloa subquadripara is known to colonize both natural and artificial water bodies [13], occurring in Brazil in areas such as the Pantanal [14], Cerrado, and Atlantic Forest [15]. In addition, it is problematic in hydroelectric reservoirs such as Barra Bonita (SP) [16], Funil (MG) [17], and Santana (RJ) [18]. The invasive potential of U. subquadripara varies according to biotic and abiotic factors [19].
The invasion of U. subquadripara correlates with the composition of the native community, exhibiting variations across various spatial scales [7]. At smaller scales, the similarity between native and invasive species can result in competition; however, at larger spatial scales, the probability of occurrence increases with the richness of native macrophytes [20,21,22]. The co-occurrence between native and invasive species is explained by the “Theory of biotic acceptance”, which posits that the presence of native species correlates positively with the occurrence of invasive species [23,24].
The occurrence of U. subquadripara is associated, on a large scale, with emerging and floating native macrophytes, of which the genera Eichhornia and Salvinia stand out [8,20]. Eichhornia crassipes is a Pontederiaceae native to the Amazon basin in Brazil and Ecuador. It is considered an invader of water bodies and reservoirs worldwide [25]. Salvinia minima is a macrophyte native to Mexico and Central and South America [26]. Due to its rapid growth, it has earned a reputation as a troublesome weed [27].
The distribution of macrophytes is largely influenced by climatic regions and is constrained by increasing latitude and altitude [28,29]. Climate changes, particularly temperature and precipitation shifts, will influence the regimes of water masses, which may reduce volume and increase the water temperatures of lakes and reservoirs [29,30,31]. Consequently, climate changes interfere with the habitat of macrophytes, altering growth, reproduction, development [32], phenology, distribution, and species migration [33]. Emerging and floating macrophytes such as U. subquadripara, E. crassipes, and S. minima are more susceptible to temperature-related impacts due to their higher exposure to submerged macrophytes [34].
Some approaches, such as species distribution models (SDMs), can be adopted for ecological niche projection considering the climate [35,36]. SDMs allow for predicting the potential distribution of a species using occurrence and climate data [37], being an important tool in preventing the invasion of exotic species in new environments. The CLIMEX software generates SDMs from the Ecoclimatic Index (EI) based on the growth and stress parameters of the species under study [38]. This methodology has been widely used for modeling the ecological niche of invasive species and weeds [39,40,41,42,43].
Consequently, determining the potential distribution of an invasive species can be determined by paying attention only to the climate. Still, the integrated understanding of the factor that influences the invasive potential, such as the co-occurrence of species, allows the filtering of suitable places [37]. Multicriteria decision-making (MCDM) is an alternative tool combining several criteria in a single index [44]. Among MCDM techniques, the analytical hierarchy process (AHP) is extensively employed. It involves comparing criteria, thereby enhancing assigned weights [45].
Therefore, due to the invasive capacity of U. subquadripara, the risk to ecosystems and natural communities, and disturbances in reservoirs, it is necessary to study the potential distribution of the species to develop control strategies to minimize possible impacts. This study aimed to develop a potential distribution model for U. subquadripara using the CLIMEX software version 4. Furthermore, this study aimed to determine the potential distribution of E. crassipes and S. minima and, based on multicriteria decision-making, correlate the climatically suitable areas for native species with areas suitable for the occurrence of the invasive species.

2. Materials and Methods

2.1. Global Distribution of Urochloa subquadripara, Eichhornia crassipes and Salvinia minima

The global distributions of U. subquadripara, E. crassipes, and S. minima were defined from occurrence points collected in the Global Biodiversity Information Facility [46,47,48] and Invasive Species Compendium [49,50] online databases. New occurrence points were searched in the Web of Science and Google Scholar databases and added to the global distribution of the species. Incomplete or duplicate information has been omitted.
The occurrence points of U. subquadripara encompassed searches with synonyms of the species, totaling 478 points after filtering 286. The global distribution of E. crassipes resulted in 8803 and, after data filtering, 2970 occurrence points. S. minima resulted in 1594 and, after data filtering, 534 occurrence points (Table S1).

2.2. CLIMEX

CLIMEX software is used for climate-based species ecological niche modeling [51]. From the known distribution and biological information of the species, it is possible to generate the potential climate distribution [51]. The CLIMEX software is based on Shelford’s Law of Tolerance, which determines that the growth of a species has an optimal value according to a given environmental resource, in addition to an upper and lower limit [52]. Climate suitability is defined according to the Ecoclimatic Index, which combines functions adjusted for growth and stress (Equation (1)) [40,41]. The Ecoclimatic Index ranges from 0 to 100. Areas with EI = 0 were considered unsuitable; 0 < EI < 30 with moderate adequacy; and EI ≥ 30 highly suitable [41].
E I = G I A × S I × S X
where EI: Ecoclimatic Index; GIA: annual growth index; SI: annual stress index; and SX: interaction between stress indices.

2.3. Parameter Adjustments and Model Validation in the CLIMEX Software

The ecological niche models for U. subquadripara, E. crassipes, and S. minima were generated considering biological information of the species and known distributions. In the CLIMEX software, the “Compare location” function was used, and the biological parameters searched were adjusted so that most of the species occurrence points were inserted in locations considered by the model as highly suitable (EI ≥ 30) [41].
Urochloa subquadripara had the African continent and South America as validation regions; e, E. crassipes, and S. minima had the United States of America, Mexico, and South America, considering native areas and in places invaded by the species.

2.3.1. Urochloa Subquadripara

Growth Indices

Edaphoclimatic characteristics that affect U. subquadripara seed germination have already been described [53]. The seed germination begins at 20–21 °C, with the optimum at 25 °C [53]. In addition, U. subquadripara has been reported to occur in places such as Paragominas (Brazil) [9] and Bantul Yogyakarta (Indonesia) [54], where the minimum and maximum average temperatures were 21 and 34 °C. Therefore, the parameters related to the ideal temperature for the growth of U. subquadripara (DV1 and DV2) were set at 22 and 35 °C. Research carried out with the species also adopted temperature values within the range established as optimal [55,56,57].
The lower and upper-temperature limits (DV0 and DV3) for the growth of U. subquadripara were established at 4 and 39 °C. The lower temperature was defined as reported for species of the same genus U. panicoides [39] and from the best fit to the global distribution of U. subquadripara. The upper temperature was set at 39 °C because the species had a priority distribution in tropical and subtropical regions, with occurrence reported in Autazes (Brazil) [58] and Córdoba (Colombia) [59], where the maximum temperatures reached 38 and 39 °C, respectively.
The lower limit, upper limit, and ideal soil moisture adopted in making the model were defined considering that the species grew in different soil moisture and according to the best fit in the global distribution: SM0, SM1, SM2, and SM3 being 0, 0.1, 8, and 10, respectively (Table 1).

Stress Parameters

The temperature limit of cold stress (TTCS) was defined according to the DV0, 4 °C, limiting the potential distribution of U. subquadripara in temperate regions without reports of the species. Furthermore, U. subquadripara occurs in Naples (United States of America) [53] and Alto Paraná (Brazil) [60], regions with minimum temperatures of up to 7 °C. The cold stress accumulation rate (THCS), cold stress degrees threshold (DTCS), and the day cold stress degrees rate (DHCS) were defined at −0.001 week−1, 4 °C, and −0.01 week−1, respectively.
The temperature limit of heat stress (TTHS) was set at 40 °C because seed germination of U. subquadripara was reduced from that value on [53]. The threshold of degrees of heat stress (DTHS) was set at 39 °C according to the upper-temperature limit (DV3). The heat stress accumulation rate (THHS) and the degree of heat stress-day rate (DHHS) was set to 0.01 week−1.
Under drought conditions, seeds of U. subquadripara show dormancy, and germination occurs when soil moisture is restored [53]. In modeling the ecological niche, the drought stress threshold (SMDS) and the drought stress accumulation rate (HDS) were considered at 0.1 and 0.005 week−1.

2.3.2. Eichhornia crassipes

Growth Indices

Ecological niche modeling for E. crassipes was performed, but the authors considered only places where the species was considered naturalized [41]; in addition, new occurrences were reported [47]. Therefore, new modeling was generated with adjustments in the parameters of the old one to encompass most of the current distribution points. The modeling proposed by Kriticos and Brunel [41] and the current distribution of E. crassipes are presented in Figure S1.
The ideal lower (DV1) and higher (DV2) temperatures were maintained at 25 and 30 °C, as defined by [41]. The lower (DV0) and upper (DV3) temperature limits were changed. The DV0 was defined at 0.5 °C because the species is sensitive to frost [41], and damage to the leaf blades occurs from air temperatures close to 0.5 °C [61].
The DV3 was defined at 36 °C because research carried out in tanks suggests that the death of E. crassipes occurs in water temperatures above 34 °C [61]. However, other reports demonstrated that the species can withstand temperatures up to 43 °C [62,63]; therefore, an intermediate value was established.
In addition, to create the new model, humidity and degree days (PDD) parameters were inserted. The maximum leaf area of E. crassipes occurs between 1800 and 2000 °C days; therefore, the defined PDD value was 1916 °C days [64]. Eichhornia crassipes is a macrophyte; thus, the species is highly dependent on water in soil [41]. However, other factors such as water salinity [65,66] and pH [67] influence the occurrence. The lower limit, upper limit, and ideal soil moisture adopted in making the model were defined considering the suitability for high moisture values and according to the best fit in the global distribution, with SM0, SM1, SM2, and SM3 being 0, 0.1, 8, and 10, respectively (Table 1).

Stress Parameters

The temperature limits of cold stress (TTCS) and heat stress (TTHS) were maintained at 0.5 and 37 °C according to the methodology proposed by [41]. The accumulation rate of cold stress (THCS) and heat stress (THHS) were defined as −0.001 week −1 and 0.001 week −1, respectively.
The drought stress threshold (SMDS) (0.02) and the drought stress accumulation rate (HDS) (−0.005 week−1) were adopted in this model because there are reductions in the photosynthesis of E. crassipes under progressive drought. However, the defined values were low because the species tolerates conditions of up to 6% of the volumetric content of water in the soil [68] (Table 1).

2.3.3. Salvinia minima

Growth Indices

Research on the influence of climatic factors on the development of S. minima is scarce, so the minimum and maximum temperature values were based on studies carried out with Salvinia molesta. The species have a similar global distribution [48,69], so such a comparison is valid.
The development of S. minima is maximized at temperatures of 23 and 35 °C, and there is a decline in growth and chlorophyll production at 15 °C [70]. In addition, experiments with S. minima adopted the average temperature range of 20–25 °C [71,72]. Therefore, the temperature range established as ideal for the growth of S. minima (DV1 and DV2) was 23–30 °C.
The minimum temperature values for S. molesta vary between 5 and 10.7 °C [73,74] and those with maximum temperature between 39 and 43 °C [63,73,74,75]. The definition of the lower limit (DV0) and the upper-temperature limit (DV3) was carried out considering the best adjustment to the occurrence data of S. minima, being 0.5 and 39 °C, respectively.
The lower and upper limits and the ideal soil moisture adopted in the making of the model were defined considering the best fit in the global distribution, with SM0, SM1, SM2, and SM3 being 0.1, 0.2, 8, and 10, respectively (Table 1).

Stress Parameters

The cold stress temperature threshold (TTCS) was set at 5 °C per the DV0, and the cold stress accumulation rate (THCS) was established at −0.0003 week−1.
The temperature limit of heat stress (TTHS) was 39 °C, according to the established DV3, and because the maximum temperature for the growth of S. molesta is 39.6 °C [74]. Values for heat stress accumulation rate (THHS), heat stress degree threshold (DTHS), and heat stress degree rate-day (DHHS) were defined as 0.1 week−1, 35 °C, and −0.1 week−1, considering the global distribution of S. minima. Salvinia minima, when exposed to periods of drought, manages to return to its primary state due to its morphology that forms a mat, protecting the apical meristem and allowing the re-establishment of the species when the humidity conditions are adequate [76,77]. This tolerance occurs because there is exposure to floods but also long periods of drought in the native area of the species [77]. Therefore, drought stress was not considered in modeling the ecological niche of S. minima (Table 1).

2.4. Climate Data, Models, and Scenarios

Modeling of U. subquadripara, E. crassipes, and S. minima were carried out using climatic data on a Climond 10’ grid. The files contained weather data on average minimum and maximum temperatures, precipitation, and monthly relative humidity. Data from 1961 to 1990, centered on 1975, represented the historical climate [78].

2.5. Multicriteria Decision-Making and Analytical Hierarchy Process

The use of multicriteria decision making (MCDM) based on GIS (Geographic Information Systems) has as basic units layers represented by polygons (vectors) or pixels (raster) (Figure 1); it allows the combination of weights of a large number of criteria [79] and obtaining results on spatial scales [44,80].
The criteria for making the multicriteria decision were based on the modeling results for the invasive species (U. subquadripara) and native species (E. crassipes and S. minima). Each criterion was divided into classes considering the Ecoclimatic Index; the values of the classes were normalized so that they were on a scale between 0 and 1 (Table 2).
The analytical hierarchy process (AHP) is widely used in MCDM to determine the weight of each criterion [80,81,82]. The AHP method uses a square preference matrix, in which all criteria are compared to each other based on the intensity of importance, where value 1 expresses “equal importance” and value 9 “extreme importance” over another factor (Table 3) [83,84].
Considering the theory of biotic acceptance, the foundation used to determine the importance of each criterion was the relevance in the potential distribution of U. subquadripara. For example, the ecological niche for U. subquadripara (criterion 1) was considered of substantial or of essential importance to the ecological niche for E. crassipes (criterion 2); therefore, the value 5 was assigned to the corresponding position in the matrix. The transposition position obtained the reciprocal value, in this case, was 1/5, equivalent to 0.20 (Table 3).
The criteria weights were obtained by calculating the eigenvectors of the paired comparison matrix [80]. Thus, each criterion assumed a weight based on its importance compared to the others [85] (Table 4).
The calculation of the consistency ratio (CR) was carried out to measure the consistency of the judgments and avoid inconsistencies in the definition of the values of the paired comparison matrix [80,83,85].
The consistency ratio is obtained as described in Equations (2) and (3) [84]. RC values < 0.1 indicate that the pairwise comparison was properly performed [83].
C I = ( λ m a x . − n ) ( n − 1 )
C R = C I × R I
where CI: Consistency index; λmax.: maximum eigenvalue of the paired comparison matrix; n: array order; CR: consistency ratio (default value); and RI: Resultant Average Consistency Index.
The consistency ratio calculated in this study was equal to 0; therefore, the judgments were considered consistent.
After the analytical hierarchy and consistency analysis process, the model maps of the species were classified (Table 2), multiplied with the established weighting (Table 4), and integrated into the raster calculator of ArcGIS® Software version 10.5.

2.6. Global Lakes and Wetlands Database (GLWD)

To compare regions considered highly suitable with the existence of bodies of water for the establishment of species, we present a map with the global database of lakes and wetlands (GLWD). Data used include level 1 (lakes with surface area ≥50 km2 and reservoirs with storage capacity ≥0.5 km3) and level 2 (lakes, reservoirs, and rivers with surface area ≥0.1 km2) [86].

3. Results

3.1. Invasive Exotic Species (Urochloa subquadripara)

The global distribution of U. subquadripara generated 276 points of occurrence in 30 countries, with Australia (48.20%), Brazil (14.35%), and Taiwan (11.53%) being the regions with the most reports (Figure 2a). Approximately 28.74% of the world area was considered very suitable for the occurrence of the species (EI ≥ 30); 5.28% moderately adequate (0 < EI < 30); and 65.98% inadequate (EI = 0). The model predicted high climate suitability in tropical regions and did not predict suitability in temperate regions such as European and American countries (Figure 2b).
The ecological niche model for U. subquadripara was validated using the native region (African continent) [8], considering that the species has high adaptation to the climatic conditions of that area. Additionally, South America was selected as a validation region. The choice stems from U. subquadripara’s presence as an invader of hydroelectric reservoirs across Brazil [8,13,87], its occurrence in natural environments in Argentina [88], and as pasture in Ecuador [89] and Venezuela [90,91]. In these validation regions, approximately 98.6% of the reported data points fell within areas deemed highly suitable, with the remaining 1.4% displaying moderate suitability; thus, there was a high correlation between the occurrence of the species and the generated model (Figure 3).

3.2. Native Species

3.2.1. Eichhornia crassipes

The distribution data for Eichhornia crassipes generated 2970 occurrence points, distributed in 110 countries. Notably, the United States of America accounted for the highest frequency of occurrences (35.6%), followed by Mexico (12.7%), Australia (5.8%), and India (4.1%) (Figure 4a).
The ecological niche modeling for E. crassipes aligned well with the species’ current distribution, with most of the points of occurrence inserted in moderately and very suitable places. In comparison to the model proposed by Kriticos and Brunel [41], the modeling covered occurrence points in European countries, the United States of America, and Japan. Moreover, the model helped delineate regions in Africa, where there was no occurrence of the species. About 45.72% of the world area was considered unsuitable (EI = 0) climatically for the occurrence of E. crassipes, 20.82% moderately adequate (0 < EI < 30), and 33.46% very adequate (EI ≥ 30) (Figure 4b).
South America is the region of origin of Eichhornia crassipes, so it was one of the areas chosen for validation, along with invaded areas (United States of America and Mexico). The invaded areas were defined due to the high occurrence of the species. Additionally, E. crassipes was problematic in at least thirteen states of the United States of America [92], being considered a critical invasive macrophyte in Florida [93]. About 94.8% of the occurrence points in the validation regions were found in very suitable areas, around 4.7% in regions with moderate adequacy, and 0.5% in inadequate regions, demonstrating high reliability in the final model (Figure 5).

3.2.2. Salvinia minima

The occurrence data of S. minima generated 534 points, distributed in African (0.56%), American (94.95%), Asian (2.62%), and European (1.87%) continents in 34 countries (Figure 6a).
Approximately 60.00, 14,19, and 25.81% of the world area were considered inadequate, moderately adequate, and very adequate for establishing S. minima, respectively (Figure 6b). Around 98.7% of the occurrence points of S. minima were in regions considered very suitable (EI ≥ 30) and 1.3% in moderately suitable places (0 < EI < 30). The occurrence of the species in inappropriate regions was not observed (EI = 0).
To validate the model, both South America and North American regions were delineated. About 79.5% of the occurrence points were located in the United States of America or Mexico; in addition, S. minima was present in fourteen states of the United States of America [94], colonizing natural habitats in Florida [95], Texas, and Louisiana [96], so this region was chosen for validation. Approximately 98.9% of the points in the areas were inserted in very suitable regions, and 1.1% had moderate climatic suitability (Figure 7).

3.3. Co-Occurrence of Urochloa subquadripara with Native Species

Combining the modeling of U. subquadripara, E. crassipes, and S. minima from the multicriteria decision-making generated a raster whose pixel values ranged from 0 to 1, where 0 were areas considered unsuitable for the occurrence of U. subquadripara and 1 very suitable areas (Figure 8a).
The suitability of U. subquadripara remained limited in northern temperate regions of the US, China, Canada, and Russia, but there was an increase in suitability compared to modeling alone (Figure 8a). The global database of lakes and wetlands showed a prevalence of lakes in the northern hemisphere; however, due to low temperatures, they were subject to freezing (Figure 8b).
Regions such as Brazil, the African continent, and Asia showed high suitability, and desert areas in Africa and Australia remained unsuitable for U. subquadripara (Figure 8a). In the southern hemisphere, the greatest risk of biological invasion by macrophytes was in reservoirs and large rivers (Figure 8b).

4. Discussion

4.1. Invasive Exotic Species (Urochloa subquadripara)

There are about 3457 macrophyte species in the world, and Brazil has the highest number [97]. The distribution of U. subquadripara follows the general pattern, with few occurrences in temperate climates. The species is found in 38.7% of the world’s area [97] and is restricted by cold, heat, and drought stress. Distribution limits are compatible with climatic regions, with restrictions observed in arid (BWh and BWk); Mediterranean and temperate (Cs and Cw); wet continental (D); and glacial (E) climates [98].
The presence of U. subquadripara is highly dependent on water availability and quality [99]. However, when compared to other macrophytes, such as Hymenachne pernambucensis, U. subquadripara is more resistant to periods of drought [100], which may be related to greater accumulation of biomass, efficiency in the use of N and P [101], and root and stem regrowth [11]. In addition, U. subquadripara is also terrestrial, being used as pasture [56]. Therefore, the species does not occur in arid climates but in semi-arid climate regions (BSh). In addition, species of the genus Urochloa have cold stress as the main distribution limiting factor [39].
The regions considered suitable in India and the African continent are classified as tropical savanna climate (Aw), monsoon climate (Am), and equatorial climate (Af), which are also predominant in Brazil. Likewise, areas in Argentina exhibiting high climatic suitability have humid subtropical climates (Cfa) and oceanic climates (Cfb) [98], similar to regions of Australia, the country with the highest number of occurrences. Sub-Saharan Africa concentrates the largest number of endemic macrophytes [29,97]; therefore, the dissemination of U. subquadripara, whose invasion success mechanism consists of a competition, mainly shading of submerged species [99], would pose a risk to these species.

4.2. Native Species

4.2.1. Eichhornia crassipes

The worldwide distribution of E. crassipes is the widest of the species studied, occurring in tropical and subtropical regions and extending into Mediterranean and temperate climates. Eichhornia crassipes are reported in 57.28% of the world, and only 1.2% of cataloged macrophytes have this vast distribution [97].
The occurrence of E. crassipes faces constraints posed by cold, heat [41], and drought. However, its distribution shifts to higher latitudes compared to U. subquadripara, colonizing regions with humid continental climate (Dfb and Dfa) [98]. The model proposed by Kriticos and Brunel [41] highlighted that the species may colonize higher latitudes due to reduced cold stress and be limited by increased heat stress in Africa, India, Brazil, and Australia with climate change [41]. This pattern is already evident in the current model, notably about the displacement to the north.
In the current model, occurrences of E. crassipes in temporary, permanent, or ephemeral water courses were considered [102]. However, the model by Kriticos and Brunel [41] did not include reports in ephemeral watercourses in the United States of America (Colorado, Connecticut, Illinois, Maryland, Seattle, and New England) and casual occurrences in European countries. While under periodic drought conditions, E. crassipes presents phenotypic plasticity [68]. Progressive drought can reduce the photosynthesis of the species; however, morphological adaptations are strategies of E. crassipes that survive both as an emergent macrophyte and as a terrestrial [68,103].
Control strategies after species establishment are difficult and costly. Biological, chemical, and mechanical control methods have been used to reduce the density of E. crassipes plants [104]; however, the main measure adopted is the prevention of dissemination, with the creation of laws that prevent the commercialization and distribution of the species [41,105].

4.2.2. Salvinia minima

S. minima exhibits the narrowest distribution among the studied species, occurring in 14.54% of the world area [97]. The species occurs in tropical (Af, Am, and Aw), humid subtropical (Cfa), and oceanic (Cfb) climatic regions [98]. The model generated concisely aligned with S. minima distribution data, with no occurrence points inserted in inappropriate regions.
Regions in Europe and China are considered suitable exhibit climatic attributes akin to those found in the United States of America and southern South America [98]. Meanwhile, regions of the African continent and Australia have similar climatic characteristics to Brazil and India [98]. Salvinia minima were first identified in South Africa in 2022 at the Hartbeespoort dam, where it already caused damage to recreational activities, fishing, and boat traffic [106]. The presence of the macrophyte is worrying because sub-Saharan Africa is suitable for the occurrence of S. minima, according to the model obtained; thus, laws that require its control have been applied [106].
In North America, Salvinia minima prevails extensively. The species was introduced to the United States through the aquarium trade [107], first identified in St. John’s in Florida in 1928 [108], and expanded in the country due to high propagation, with a leaf doubling time of 3.5 days [27]. It is widely found in the coastal region of the country and is problematic in the states of Florida and Louisiana, where biological control is carried out with Cyrtobagous salviniae Calder and Sands (Coleoptera: Curculionidae) [94,107].
In spite of the economic and ecological damage in inflicts, S. minima have a significant potential to be used in phytoremediation due to its rapid growth, adaptation to different climatic conditions, and tolerance to contaminants [70]. The species has already been identified as a phytoremediator of sewage treatment water, reducing the content of total suspended solids [109], heavy metals such as chromium [71,110], lead [111], cadmium, nickel, and zinc [112], and herbicides such as atrazine [113].

4.3. Co-Occurrence of Urochloa subquadripara with Native Species

Species distribution models generated by CLIMEX have limitations because they only consider climatic factors, not considering, for example, biotic interactions [114]. In addition to climate and the occurrence of watercourses, biological invasion by macrophytes depends on the composition of the community, the existence of natural enemies, and correlations with native species [24].
The invasion dynamics of U. subquadripara is positively correlated with the occurrence of E. crassipes and S. minima [8]. Furthermore, as it occurs in the epiphytic life form, the presence of native macrophytes such as E. crassipes increases the pressure of U. subquadripara propagules, favoring local colonization and the invasive expansion [12]. Therefore, considering the co-occurrence between species allows for identifying the potential distribution of the invader, minimizing model limitations.
The outcome of the co-occurrence of U. subquadripara with E. crassipes and S. minima has tropical and subtropical regions as very suitable areas. However, an elevation in moderately suitable regions with humid subtropical (Cfa) and oceanic (Cfb) climates in the United States of America, China, and European countries [98]. This occurs because the modeling of both native species identified these locations as climatically suitable and, therefore, likely for biological invasion by U. subquadripara.
These results align with climate forecasts, which estimate that northern latitudes will have higher warming rates than the rest of the world [115], which causes an increase in lake temperatures and a more extended melting period [116]. Furthermore, higher precipitation rates may occur [29], which, associated with surface runoff, transports more nutrients to the lakes, favoring the occurrences of emerging macrophytes [117]. Therefore, U. subquadripara can move to temperate climates [118].
The northern hemisphere host the majority of the world’s lakes [86] and the largest number of lakes larger than 10 ha [119]. Thus, the risk of invasion is aggravated because the surface area of the watercourse is positively correlated with the richness of macrophytes [28]. It is predicted that the number of invasive macrophytes in Europe and North America will increase with climate change [120], which would suppress native macrophytes, mainly underwater [29].
Brazil, the sub-Saharan Africa region, and the Asian continent were classified as very suitable. These locations are also subject to climate change; however, the impact on macrophytes’ occurrences depends on the lake’s depth [29]. Shallow lakes subject to warming [121] and decreases in precipitation [122] can reduce water volume and colonization by invasive macrophytes such as U. subquadripara. Nonetheless, in the southern hemisphere, the concern with the invasion of macrophytes is mainly in hydroelectric reservoirs and large watercourses.
Anthropogenic alterations, such as the creation of dams and hydroelectric plants, can interfere with natural geographic barriers and encourage the invasion of exotic species [11]. Notably, hydroelectric reservoirs are more invaded than natural lakes [123] due to the increase in nutrients in the water, sedimentation, and changes in biotic interactions [124,125]. Macrophytes obstruct the water intake in the reservoirs, reducing efficiency in energy generation and causing economic losses [126]. There are around 391 large hydroelectric plants in Brazil [127]; therefore, the modeling indicates a high risk of invasion since the country is climatically very suitable for U. subquadripara, E. crassipes, and S. minima.

5. Conclusions

The occurrences of U. subquadripara, E. crassipes, and S. minima are restricted by cold, heat, and drought, being found mostly in tropical regions. Climate changes, mainly in temperature and precipitation, can influence the occurrences of macrophytes, causing them to move to higher latitudes, increasing the risk of invasions in the northern hemisphere, which concentrates the largest number of lakes in the world.
Eichhornia crassipes and S. minima, although not considered exotic in Brazil, are highly aggressive invasive species that can colonize both natural and disturbed environments. Both species have climatic suitability in sub-Saharan Africa, the place with the highest number of endemic macrophytes in the world, so biological invasion would endanger native biodiversity.
Urochloa subquadripara, in addition to being highly competitive, presents phenotypic plasticity in relation to drought and high pressures of propagules. In Brazil, the dispersion of the species is worrying because it is a country with the greatest diversity of macrophytes in the world and the largest producer of hydroelectricity in Latin America.
Based on the predicted global distribution of the three species, it is possible to identify sites subject to invasion by adopting prevention policies. However, it is still necessary to develop control methods with low environmental impact and to invest in studies for the identification and early detection of macrophytes, minimizing expenses with control and damage containment.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/su151712722/s1, Table S1: Global distribution points of Urochloa subquadripara, Eichhornia crassipes and Salvinia minima; Figure S1: Current distribution of Eichhornia crassipes plants and Ecoclimatic Index (EI), modeled by Kriticos and Brunel, 2016 [41], using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light red (0 < EI < 30), and high suitable in red (EI ≥ 30). References [128,129,130,131,132,133,134,135,136,137,138,139,140,141,142,143,144,145,146,147,148,149,150,151,152,153,154,155,156,157,158,159,160,161,162,163,164,165,166,167,168,169,170,171,172,173,174,175,176,177,178,179,180,181,182,183,184,185,186,187,188,189,190] are cited in Supplementary Materials.

Author Contributions

T.S.D.: Conceptualization, Formal analysis, Investigation, Writing—Original Draft, and Writing—Review and Editing. I.M.S.: Formal analysis, Investigation, Writing—Original Draft, and Writing—Review and Editing. D.S.M.: Formal analysis, Investigation, and Writing—Original Draft. R.S.d.S.: Conceptualization, Methodology, Resources, and Writing—Review and Editing. D.P.M.: Resources, Writing—Original Draft, Writing—Review and Editing, and Supervision. F.D.d.S.: Writing—Review and Editing. D.V.S.: Writing—Review and Editing, Resources. J.B.d.S.: Conceptualization, Methodology, Resources, Writing—Original Draft, and Writing—Review and Editing. All authors have read and agreed to the published version of the manuscript.

Funding

“Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)—Código Financeiro 001” and “Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)”.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

To the “Syngenta Crop Protection”.

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Figure 1. Weighted combination of criteria matrix datasets.
Figure 1. Weighted combination of criteria matrix datasets.
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Figure 2. (a) Known global distribution of Urochloa subquadripara plants and (b) Ecoclimatic Index (EI) for U. subquadripara, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 2. (a) Known global distribution of Urochloa subquadripara plants and (b) Ecoclimatic Index (EI) for U. subquadripara, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 3. Current distribution of Urochloa subquadripara in validation regions, native (African continent) and invaded areas (South America), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 3. Current distribution of Urochloa subquadripara in validation regions, native (African continent) and invaded areas (South America), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 4. (a) Known global distribution of Eichhornia crassipes plants and (b) Ecoclimatic Index (EI) for E. crassipes, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 4. (a) Known global distribution of Eichhornia crassipes plants and (b) Ecoclimatic Index (EI) for E. crassipes, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 5. Current distribution of Eichhornia crassipes in validation regions, native area (South America), and invaded area (United States of America and Mexico), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 5. Current distribution of Eichhornia crassipes in validation regions, native area (South America), and invaded area (United States of America and Mexico), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 6. (a) Known global distribution of Salvinia minima plants and (b) Ecoclimatic Index (EI) for S. minima, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 6. (a) Known global distribution of Salvinia minima plants and (b) Ecoclimatic Index (EI) for S. minima, modeled using CLIMEX. Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 7. Current distribution of Salvinia minima in validation regions, native area (South America), and invaded area (United States of America and Mexico), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
Figure 7. Current distribution of Salvinia minima in validation regions, native area (South America), and invaded area (United States of America and Mexico), based on the Ecoclimatic Index (EI). Unsuitable areas in white (EI = 0), low suitable in light orange (0 < EI < 30), and highly suitable in orange (EI ≥ 30).
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Figure 8. (a) Climate suitability for Urochloa subquadripara considering co-occurrence with native species (Eichhornia crassipes and Salvinia minima), considering Ecoclimatic Indices (EI) modeled using CLIMEX. Inappropriate areas in white (0) and very suitable areas in red (1); (b) global lakes and wetlands database (GLWD), including tier 1 (lakes with surface areas ≥50 km2 and reservoirs with storage capacity ≥0.5 km3) and tier 2 (lakes, reservoirs, and rivers with surface areas ≥0.1.
Figure 8. (a) Climate suitability for Urochloa subquadripara considering co-occurrence with native species (Eichhornia crassipes and Salvinia minima), considering Ecoclimatic Indices (EI) modeled using CLIMEX. Inappropriate areas in white (0) and very suitable areas in red (1); (b) global lakes and wetlands database (GLWD), including tier 1 (lakes with surface areas ≥50 km2 and reservoirs with storage capacity ≥0.5 km3) and tier 2 (lakes, reservoirs, and rivers with surface areas ≥0.1.
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Table 1. Adjusted parameter values for modeling the invasive species Urochloa subquadripara (US), native Eichhornia crassipes (EC), and Salvinia minima (SM) using CLIMEX.
Table 1. Adjusted parameter values for modeling the invasive species Urochloa subquadripara (US), native Eichhornia crassipes (EC), and Salvinia minima (SM) using CLIMEX.
ParametersIndexUnit.USECSM
Lower temperature thresholdDV0°C40.55
Lower optimum temperatureDV1°C222523
Upper optimum temperatureDV2°C353030
Upper optimum thresholdDV3°C393639
Lower soil moisture thresholdSM0--000.1
Lower optimum soil moistureSM1--0.10.10.2
Upper optimum soil moistureSM2--888
Upper soil moisture thresholdSM3--101010
Cold stress temperature thresholdTTCS°C40.55
Cold stress temperature rateTHCSWeek−1−0.001−0.0003−0.0003
Cold stress degree-day thresholdDTCS°C day4--------
Cold stress degree-day rateDHCSWeek−1−0.01--------
Heat stress temperature thresholdTTHS°C403739
Heat stress temperature rateTHHSweek−10.010.0010.1
Heat stress thresholdDTHS°C dia39----35
Heat stress degree-day rateDHHSweek−10.01----0.1
Dry stress thresholdSMDS--0.10.02----
Dry stress rateHDSweek−10.005−0.005
Degree days per generationPPD°C dia----1916----
Table 2. Criteria used in multicriteria decision-making, classes, and normalized values.
Table 2. Criteria used in multicriteria decision-making, classes, and normalized values.
Criteria
CriterionDescription
Criterion 1Ecological niche for U. subquadripara
Criterion 2Ecological niche for E. crassipes
Criterion 3Ecological niche for S. mínima
Criteria Classes
DescriptionClassNormalized value
EI = 000
0 < EI < 3010.5
EI ≥ 3021
Table 3. Paired comparison matrix describing preferences between the criteria identified in Table 2.
Table 3. Paired comparison matrix describing preferences between the criteria identified in Table 2.
Criterion 1Criterion 2Criterion 3
Criterion 1155
Criterion 20.211
Criterion 30.211
The intensity of importance: 1 (equal importance); 3 (moderate importance of one factor over the other); 5 (strong or essential importance); 7 (very strong importance); 9 (extreme importance); 2, 4, 6, and 8 (intermediate values); reciprocals (values for inverse comparison) (adapted from Saaty and Vargas [82]).
Table 4. Weights used in multicriteria decision making.
Table 4. Weights used in multicriteria decision making.
CriterionDescriptionWeight *
Criterion 1Ecological niche para U. subquadripara0.714
Criterion 2Ecological niche para E. crassipes0.143
Criterion 3Ecological niche para S. minima0.143
* Eigenvectors resulting from the paired comparison matrix.
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Duque, T.S.; Souza, I.M.; Mendes, D.S.; da Silva, R.S.; Mucida, D.P.; da Silva, F.D.; Silva, D.V.; dos Santos, J.B. Ecological Niche Modeling of Invasive Macrophyte (Urochloa subquadripara) and Co-Occurrence with South American Natives. Sustainability 2023, 15, 12722. https://doi.org/10.3390/su151712722

AMA Style

Duque TS, Souza IM, Mendes DS, da Silva RS, Mucida DP, da Silva FD, Silva DV, dos Santos JB. Ecological Niche Modeling of Invasive Macrophyte (Urochloa subquadripara) and Co-Occurrence with South American Natives. Sustainability. 2023; 15(17):12722. https://doi.org/10.3390/su151712722

Chicago/Turabian Style

Duque, Tayna Sousa, Iasmim Marcella Souza, Débora Sampaio Mendes, Ricardo Siqueira da Silva, Danielle Piuzana Mucida, Francisca Daniele da Silva, Daniel Valadão Silva, and José Barbosa dos Santos. 2023. "Ecological Niche Modeling of Invasive Macrophyte (Urochloa subquadripara) and Co-Occurrence with South American Natives" Sustainability 15, no. 17: 12722. https://doi.org/10.3390/su151712722

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