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Article

Turnover, Uniqueness, and Environmental Filtering Shape Helminth Parasite Metacommunities in Freshwater Fish Pseudoxiphophorus bimaculatus (Cyprinodontiformes: Poeciliidae)

by
Ivonne López-del-Monte
1,2,*,
Oscar Rico-Chávez
3,
Juan Manuel Caspeta-Mandujano
4,
Edgar Fernando Mendoza-Franco
5,
Norman Mercado-Silva
6,
Jesús Montoya-Mendoza
7,
Miguel Rubio-Godoy
8,
Ismael Guzmán-Valdivieso
8,
Benjamín Quiroz-Martínez
9 and
Guillermo Salgado-Maldonado
2
1
Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Coyoacán C.P. 04510, Ciudad de México, Mexico
2
Laboratorio de Helmintología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Coyoacán C.P. 04510, Ciudad de México, Mexico
3
Departamento de Etología, Fauna Silvestre y Animales de Laboratorio, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad Universitaria, Coyoacán C.P. 04510, Ciudad de México, Mexico
4
Laboratorio de Parasitología de Animales Silvestres, Facultad de Ciencias Biológicas y Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Morelos, Colonia Chamilpa, Cuernavaca C.P. 62209, Morelos, Mexico
5
Instituto de Ecología, Pesquerías y Oceanografía del Golfo de México (EPOMEX), Universidad Autónoma de Campeche, San Francisco de Campeche C.P. 24029, Campeche, Mexico
6
Centro de Investigación en Biodiversidad y Conservación, Universidad Autónoma del Estado de Morelos, Colonia Chamilpa, Cuernavaca C.P. 62209, Morelos, Mexico
7
Laboratorio de Ecología y Helmintología, Tecnológico Nacional de México, Instituto Tecnológico de Boca del Río, Boca del Río C.P. 94290, Veracruz, Mexico
8
Red de Biología Evolutiva, Instituto de Ecología, A.C., Xalapa C.P. 91073, Veracruz, Mexico
9
Laboratorio de Ecología Numérica y Análisis de Datos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Ciudad Universitaria, Coyoacán C.P. 04510, Ciudad de México, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(12), 864; https://doi.org/10.3390/d17120864
Submission received: 31 October 2025 / Revised: 3 December 2025 / Accepted: 5 December 2025 / Published: 17 December 2025
(This article belongs to the Section Freshwater Biodiversity)
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Abstract

Understanding the processes that shape parasite community structure across spatial scales is essential for linking ecological theory with host–parasite dynamics. Using a metacommunity framework, we examined the metacommunity of helminth parasites infecting the freshwater fish Pseudoxiphophorus bimaculatus across 11 sites along the La Antigua River basin (Veracruz, Mexico). We combined β-diversity partitioning, local and species contributions to diversity, elements of metacommunity structure (EMS), and variance partitioning to identify the mechanisms underlying spatial variation in parasite composition. Helminth metacommunity was dominated by a few widespread taxa, with balanced variation in species abundances—indicative of turnover—emerging as the main driver of β-diversity at both host and site levels. Both rare and common species contributed disproportionately to regional diversity. EMS analyses revealed coherent, non-random community structures that varied from nested to quasi-Gleasonian and quasi-Clementsian types among sites and guilds, suggesting that species respond individually to shared environmental gradients. Variance partitioning indicated that environmental filtering, particularly through habitat structure, explained most of the variation in community composition, exceeding the effects of water quality and host size. Overall, our results demonstrate that turnover, species uniqueness, and environmental filtering interact to shape helminth parasite metacommunities in tropical freshwater systems, highlighting the integrative role of environmental heterogeneity and dispersal limitation in parasite community assembly.

1. Introduction

Understanding processes that structure biological communities remain a central theme in ecology [1,2]. Parasites represent a significant component of biodiversity and play a pivotal role in the functioning of ecosystems [3,4,5,6]. However, there is a paucity of knowledge regarding the processes that determine variations in their distribution at different spatial and temporal scales, and even less so regarding the characteristics (biotic or abiotic) that give rise to these distribution patterns [1,7]. In the field of parasite ecology, fish have been identified as optimal hosts for research on parasite communities, as these hosts offer a replicated, hierarchically structured environment that mirrors the fragmentation of their own habitat [8].
The metacommunity framework offers a powerful approach to evaluating distributional patterns at local and regional scales. A metacommunity is defined as a set of local communities that exist within patches linked by dispersal [9], enabling the study of both host–parasite transmission dynamics and broader ecological assembly processes [10,11,12,13,14]. Within this framework, the concept of β-diversity—the variation in community composition across sites [15]—and β-diversity partitioning is a useful tool to assess the processes underlying community structure, providing a key indicator of species turnover, nestedness, and abundance gradients [16,17], likewise a measure to assess the contribution of species and sites to the dissimilarity [18]. Complementary tools such as the elements of metacommunity structure (EMS) framework, variance partitioning, and linear models allow further exploration of the relative contributions of environmental filters and dispersal to community organization [19,20,21,22].
Despite the increasing use of beta diversity analyses and EMS in various systems (e.g., [23,24]), relatively few studies have applied these approaches to helminth parasites of neotropical freshwater fish (e.g., [25,26,27]). This contrasts with their increased use in terrestrial parasite-host systems (e.g., [28,29]), even though aquatic parasites provide suitable models for testing ecological hypotheses related to co-occurrence, dispersal, and environmental filtering [13].
To address this gap, we analyzed the metacommunity of helminth parasites in neotropical fish twospot livebearer (Pseudoxiphophorus bimaculatus (Heckel)) across the La Antigua River basin in Veracruz, México. Previous work on this model system documented that intraspecific aggregation decreases interspecific competition and promotes coexistence [30], but the spatial distribution patterns of helminths and the relative influence of abiotic and biotic factors remain unclear. In this study, we aimed to determine how helminth communities vary between locations, whether balanced variation in abundances (analogous to replacement) or abundance gradients (analogous to nestedness) are the dominant process driving community structuring, and if mid-basin sites and species with higher dispersal capacity play an important role in shaping regional diversity. We also evaluated whether helminth species are distributed individually along the environmental gradient and whether physicochemical variables exert a stronger influence than host traits in structuring the metacommunity structure.

2. Materials and Methods

In June 2016, we collected 220 individuals of P. bimaculatus from 11 localities along the La Antigua River basin, Veracruz, Mexico (Supplementary Material Table S1). The sampling sites encompass a wide range of elevations and hydrological conditions, providing a natural gradient for examining parasite community dynamics. Detailed procedures for collection methods and parasitological examination are available in [30,31]. The complete dataset had been published [32] and was reanalyzed here to assess our hypothesis.

2.1. Community Structure

To evaluate the structure of helminth communities Whittaker rank-abundance curves were plotted, to allow visualization of abundance patterns among parasite species. We used the “rankabundance” function from the “BiodiversityR” package [33]. To assess spatial variation in parasite communities, we used nonparametric multidimensional scaling (NMDS) analysis based on Bray–Curtis dissimilarities and tested for significant differences among sites using analysis of one-way similarity (ANOSIM). We used the “metaMDS” and “anosim” functions from the “vegan” package [34].

2.2. Partitioning of β-Diversity

To evaluate the processes underlying variation in community composition we calculated the abundance-based multiple-site dissimilarity Bray–Curtis index (dBC) and partitioned beta diversity into balanced variation in abundance (dBC.BAL), whereby the individuals of some species in one site are substituted by the same number of individuals of different species in another site, i. e. analogous to species replacement; and abundance gradients (dBC.GRA) where some individuals are lost form one site to the other, i. e. analogous to nestedness [17,35]. This approach allows to distinguish whether dissimilarities among sites are driven primarily by species substitution or by differences in richness. For this analysis, we used the “beta.multi.abund” function from the “betapart” package [17,36].

2.3. Local and Species Contribution to β-Diversity

To evaluate each site’s contribution to parasite communities and the influence of helminth species to community turnover we calculated the local contribution to beta diversity (LCBD) and the species contribution to beta diversity (SCBD) based on abundance data (using the Hellinger transformation) [18,22]. These calculations were performed for all species combined and separately for each helminth guild (ectoparasites, adult endohelminths, and endohelminth larvae). Analyses were performed with the “adespatial” package [18].
Subsequently, we used second-degree terms from linear models to model the relationship between the number of sites where each helminth taxon was recorded and its contribution to beta diversity (SCBD values). We also modeled the relationship between LCBD values and helminth species richness. In addition, we used the beta regression model between environmental variables and LCBD values [22,37]. Finally, we performed a linear regression between helminth species abundance and environmental variables.

2.4. Elements Metacommunity Structure Framework

To characterize metacommunity structure, we applied the EMS framework [10,11,38], which evaluates coherence, species turnover, and boundary clustering. These metrics reveal whether communities exhibit patterns consistent with Gleasonian, Clementsian, nested or random structures. We performed this analysis using the “metacom” package [39]. Analyses were performed at two spatial scales: regional and local. The regional scale was evaluated at the component community level, encompassing all helminth species recovered from all P. bimaculatus individuals examined within each locality. The local scale was evaluated at the infracommunity level, representing the community of helminth species found within individual hosts [12,21].

2.5. Variance Models to Evaluate Environmental Factors and Host Size

We used variance partitioning to estimate the relative influence of environmental variables and host related factors on parasite community composition [20]. Prior to analysis, all variables except pH and connectivity were log transformed. Strong correlations (r > 0.70) among predictors were identified using Pearson correlation, and redundant variables were excluded. Variable selection was conducted with the “forward.sel” function of the “adespatial” package [12,21] to identify the most relevant predictors for helminth abundance.
We then performed a partial canonical redundancy analysis (pRDA) to quantify the variance explained by each set of predictors [19], using the “rda” function from the “vegan” package [34]. Variance partitioning was subsequently applied with analysis with three explanatory matrices: (1) physicochemical variables (practical salinity units, percentage of dissolved oxygen), (2) habitat structure variables (altitude, distance from the nearest population, land use, habitat diversity, water velocity, host density), and (3) a host-specific variable (host size). The helminth abundance matrix served as the response variable. Analysis was carried out using the “varpart” function in “vegan” package [34]. All analyses were performed using the statistical software RStudio version 4.4.1.

3. Results

3.1. Community Structure

A total of 18 helminth species were identified from 220 individuals of P. bimaculatus collected across 11 sites. These species were grouped into three guilds: four monogenean ectoparasites, four intestinal adults, and ten larval helminths (Supplementary Material Table S2).
Community composition varied markedly among sites and was strongly dominated by a few abundant species, particularly the trematode Centrocestus formosanus (Nishigori, 1924) and the monogenean Urocleidoides vaginoclaustroides Mendoza-Franco, Caspeta-Mandujano, Salgado-Maldonado and Matamoros, 2015, with the remaining species occurring at lower and more variable abundances (Figure 1). Species abundances differed widely across sites.
Spatial structuring of helminth communities was evident along the river gradient. NMDS ordination revealed moderate but significant differentiation between mid- and lower-basin sites (stress = 0.12; ANOSIM: R = 0.36, p = 0.02) (Figure 2).

3.2. Partitioning of β-Diversity

Helminth communities showed high abundance-based dissimilarity both regionally (among sites) and locally (among individual hosts). At the component community level, overall Bray–Curtis dissimilarity between sites was high (dBC = 0.92), largely driven by balanced variation in species abundances (dBC.BAL = 0.65), indicating species replacement as the dominant process. A smaller but significant portion was attributed to abundance gradients (dBC.GRA = 0.27) (Table 1).
At the infracommunity level, dissimilarity was even higher (dBC = 0.99), almost entirely due to species replacement (dBC.BAL >> dBC.GRA). Within sites, dissimilarity remained consistently high (dBC range: 0.85–0.98, mean = 0.89, SD = 0.04), again with balanced variation as the primary driver (range 0.60–0.88, mean dBC.BAL = 0.75, SD = 0.08).
Patterns varied by site. Three lower-basin sites (L7, L9, L10) exhibited particularly strong species replacement (dBC.BAL = 0.82–0.88), whereas one mid-basin site (M5) showed a relatively high nestedness component (dBC.GRA = 0.29), suggesting it hosts a depauperate subset of the regional fauna. Other mid-basin sites (M2, M3, M4, L11) also showed a modest but notable nestedness component, indicating that both species turnover and abundance gradients shape community differentiation in this region.
Guild-level analyses revealed strong spatial structuring across all groups (Table 1), with consistently high dissimilarity between sites (dBC > 0.82) and between hosts across sites (dBC > 0.65). In nearly all cases, balanced variation (dBC.BAL) exceeded abundance gradients (dBC.GRA), reinforcing species replacement as the primary mechanism driving community differentiation across spatial scales and guilds.

3.3. Local and Species Contributions to β-Diversity

Helminth richness and abundance varied along the elevational gradient in the La Antigua River (Figure 3). Local Contributions to Beta Diversity (LCBD) did not follow a linear trend with elevation; instead, high LCBD values occurred at both ends of the gradient—for example, M2 (upper basin) and M6 (mid-elevation) exhibited high compositional uniqueness.
Guild-specific patterns also emerged. Monogeneans were present at all sites, but the most abundant communities showed low LCBD values, indicating limited uniqueness. Adult intestinal helminths were absent in the lower basin but peaked in mid-elevation (M6, N = 188), with upper basin sites (M1–M3) hosting more unique communities. Larval helminths had low richness at higher elevations but also peaked at M6 (S = 6), while sites M3, M5, and L8 contributed disproportionately to regional β-diversity due to the presence of rare or localized larval taxa (Supplementary Material Figure S1).
Across all sites, LCBD exhibited a significant non-linear U-shaped relationship with species richness (DF = 8, F = 3.03, p = 0.10, adjusted R2 = 0.97; Figure 4A). Values were highest at low and high richness and lowest at intermediate richness (6–8 taxa). This curvilinear pattern was consistent across guilds but explained less variation (Figure 4B: DF = 8, F = 8.29, p = 0.01, adjusted R2 = 0.59; Figure 4C: DF = 4, F = 3.04, p = 0.15, adjusted R2 = 0.40; Figure 4D: DF = 5, F = 5.98, p = 0.05, adjusted R2 = 0.59). For monogeneans, however, an inverted U-shaped relationship indicated that intermediate richness (~2 species) contributed most to β-diversity.
Environmental models showed that LCBD was not strongly driven by simple abiotic gradients. Among tested predictors, land use (DF = 3, p = 0.03, adjusted R2 = 0.29) and host density (DF = 3, p = 0.16, adjusted R2 = 0.21) explained moderate amounts of LCBD variance across sites (Supplementary Material Figure S2).
Species Contribution to Beta Diversity (SCBD) identified eight species with above-average contributions (SCBD > 0.059): C. formosanus, Gyrodactylus sp. von Nordmann, 1832, U. vaginoclaustroides, Phyllodistomum inecoli Razo-Mendivil, Pérez-Ponce de León and Rubio-Godoy, 2013, Contracaecum sp. Rudolphi, 1809, Freitascapillaria moraveci Caspeta-Mandujano, Salgado-Maldonado and Vázquez, 2009, Gyrodactylus xalapensis Rubio-Godoy, Paladini, García-Vásquez and Shinn, 2010, and Gyrodactylus takoke García-Vásquez, Razo-Mendivil and Rubio-Godoy, 2015. Species abundance explained 70% (DF = 16, F = 49.48, p < 0.001, adjusted R2 = 0.70) of the variation in SCBD (Figure 5). A significant curvilinear relationship was found between site occupancy and SCBD (DF = 15, F = 9.32, p < 0.005, adjusted R2 = 0.49), with both rare and widespread species contributing disproportionately to β-diversity, while intermediate species contributed less (Figure 6).
When analyzed by guild, the top contributors included two monogeneans (U. vaginoclaustroides, Gyrodactylus sp.), three adult helminths (P. inecoli, Paracreptotrematoides heterandriae (Salgado-Maldonado, Caspeta-Mandujano and Vázquez, 2012), F. moraveci), and four larvae (C. formosanus, Uvulifer cf. ambloplitis (Hughes, 1927), Eustrongylides sp. Jägerskiöld, 1909, Contracaecum sp.). For adult helminths, a curvilinear model explained nearly all the variation in SCBD (DF = 1, F = 56.31, p =0.09, adjusted R2 = 0.97), suggesting that site occupancy is a strong predictor of contribution. Monogeneans and larval helminths showed weaker fits (R2 ≈ 0.40), suggesting other factors (e.g., host specificity, environmental variation) also influence SCBD (Supplementary Material Figure S3).

3.4. Metacommunity Structure (EMS Framework)

The EMS analysis revealed non-random species distributions with significant coherence (z = −5.62, p < 0.001). At the component community level, boundary clumping was also significant (Morisita index = 2.15, p < 0.003), but turnover did not deviate from null expectations (z = 2.03, p = 0.04), indicating limited species replacement, supporting a nested metacommunity structure, i.e., a pattern of clustered species loss (Table 2).
At the infracommunity level, most sites showed significant coherence, indicating species distributions were shaped by shared environmental gradients. However, EMS varied. For instance, M4 and L7 showed Clementsian structures (M4: z = −4.81, p < 0.001, L7: z = −4.45, p < 0.001; M4 Morisita index = 2.5, p = 0.03, L7 Morisita index = 1.75, p = 0.05), while M2, M5, and L9 exhibited quasi-Clementsian structures (M2: z = −2.98, p < 0.001, M5: z = −6.11, p < 0.001, L9: z = −3.61, p < 0.001; M2 Morisita index = 4.5, p = 0.05, M5 Morisita index = 2.07, p = 0.02, L9: Morisita index = 1.8, p = 0.04). In contrast, M6 showed a Gleasonian structure (z = −4.91, p = < 0.001; Morisita index ≈ 0.98, p = 0.53), and sites like M1, M3, L8, L10, and L11 displayed quasi-Gleasonian patterns, indicating more individualistic species responses (Table 2).
Guild-level EMS analyses revealed non-random assembly across all groups (Supplementary Material Table S3). Larval endohelminths showed a Gleasonian pattern, while monogeneans and adult endohelminths exhibited quasi-Gleasonian structures.

3.5. Environmental Drivers of Community Composition

RDA indicated that environmental variables explained a large proportion of variation in helminth community composition (Figure 7). The first two axes accounted for 93.5% of constrained variance, clearly separating sites M5 and M6 along distinct environmental gradients.
Variance partitioning revealed that water physiochemistry, habitat structure, and host size jointly explained 86% of total variation (adjusted R2 = 0.86, p = 0.002). Habitat structure alone accounted for the largest unique fraction (69%, p = 0.05), while water quality (42%, p = 0.10) and host size (27%, p = 0.08) contributed moderately but were not statistically significant (Table 3). Only 14% of the variation remained unexplained, highlighting the role of environmental heterogeneity in shaping helminth community composition.
Guild-specific models revealed contrasting patterns. For monogeneans, the combined model explained 93% of the variance (adjusted R2 = 0.93, p = 0.05), with host size as the only significant individual predictor (R2 = 0.27, p = 0.02), suggesting larger hosts support distinct assemblages. In contrast, adult endohelminth distributions were poorly explained by measured variables (adjusted R2 = 0.39, NS), while larval helminths were significantly influenced by habitat structure (28%, p = 0.004), though large residual variance (61%) remained for both groups (Supplementary Material Table S4).
Regression analyses of the six most abundant species (Supplementary Material Table S5) revealed species-specific responses. Salinity negatively affected U. vaginoclaustroides and F. moraveci, while proximity to human settlements reduced occurrences of U. vaginoclaustroides and P. heterandriae. Conversely, altitude positively influenced U. vaginoclaustroides, P. heterandriae, P. inecoli, and F. moraveci. Gyrodactylus sp. abundance increased with host density. Other variables (e.g., habitat diversity, water velocity, dissolved oxygen, land use) showed weak or non-significant effects (all p > 0.1).

4. Discussion

Our analyses revealed pronounced spatial variation in the helminth metacommunity of P. bimaculatus across the La Antigua River basin. NMDS ordination and ANOSIM both indicated that river slope and longitudinal position significantly influenced helminth composition, with distinct differences between central and lower basin sites. Notably, medium-elevation localities—especially M6—emerged as potential diversity hotspots, likely due to moderately stable environmental conditions that favor species coexistence. In contrast, peripheral sites at higher or lower elevations may support more specialized or isolated assemblages [40].
These patterns suggest that parasite community composition is shaped by the combined influence of environmental filtering, spatial separation, and host–parasite co-distributions. Similar longitudinal gradients in parasite communities have been reported elsewhere, driven by water flow, habitat heterogeneity, and passive downstream dispersal of both free-living stages and infected hosts [41,42]. Thus, elevation alone does not determine helminth diversity; rather, it is the interaction between landscape features and ecological filters along the river network that structures parasite communities.
The helminth fauna of P. bimaculatus forms a regional metacommunity composed of a few widespread, high-transmission species and a larger set of rarer, spatially restricted taxa—consistent with patterns reported in other freshwater parasite systems [43]. At both the local (site) and individual host levels, infracommunities were highly heterogeneous, primarily driven by variation in the abundance of dominant species.
Partitioning of β-diversity revealed that balanced variation in species abundance was the predominant mechanism across spatial scales and parasite guilds. This pattern indicates that changes in community composition mostly reflect replacement in species abundances between sites, rather than nested subsets of richer communities. Balanced variation likely arises from habitat heterogeneity and environmental filtering (i.e., species sorting), consistent with the strong explanatory power of environmental variables in our models.
High host-level dissimilarity across all guilds points to strong individual variation in infection status, likely influenced by microhabitat conditions and host traits (though see [1]). Similar dominance of balanced variation has been observed in other metazoan parasite systems [2,44], particularly where environmental filters maintain distinct community structures [45]. Our results highlight that even within a single host species, parasite communities are shaped by large-scale ecological processes.
The strong unimodal relationship between species richness and local contributions to β-diversity (LCBD) suggests that richness is a key driver of site uniqueness, consistent with patterns observed in free-living communities [46]. The observed U-shaped curve indicates that sites with very low or very high richness contributed disproportionately to regional β-diversity, while intermediate-richness sites contributed less.
Species-poor sites may support specialist parasites adapted to unique environmental conditions or host traits, while species-rich sites likely contain mosaics of generalists and specialists, each adding unique compositional elements. As noted by [18,23,47,48,49,50,51] low-richness sites often contribute strongly to β-diversity due to their rare or specialized communities, whereas high-richness, high-LCBD sites sustain much of the regional species pool [52].
The curvilinear decrease in LCBD with increasing richness may reflect a saturation effect, where additional species add little uniqueness. However, previous findings of a linear relationship between infracommunity and component community richness suggest nonsaturation [30].
When analyzed by parasite guild, LCBD–richness relationships varied. For monogeneans, LCBD peaked at intermediate richness, possibly due to species interactions such as competition or niche specialization. Conversely, sites with high monogenean richness could be approaching saturation, where the species pool become more homogeneous. In contrast, adult helminths showed declining LCBD with increasing richness, suggesting that species-poor sites host more distinct communities, potentially due to specialized life cycles. Larval helminths contributed most strongly to β-diversity at mid-basin sites, likely reflecting favorable environmental conditions for rare or transient taxa.
These results underscore the value of partitioning communities by guild, as aggregate analyses may obscure the ecological mechanisms driving spatial uniqueness [2,22,53,54].
Species-level contributions (SCBD) revealed that both rare and widespread taxa played disproportionate roles in community turnover. Key contributors included C. formosanus, Gyrodactylus sp., U. vaginoclaustroides, P. inecoli, and Contracaecum sp. As in other parasite systems [49,55], SCBD tended to increase with species abundance, indicating that variability in the dominance of abundant taxa can generate significant compositional differences between sites.
Rare, spatially restricted species (e.g., C. formosanus) likely depend on specific environmental conditions or host associations, resulting in limited dispersal but high local distinctness. In this system, C. formosanus may be a poor disperser, confined to few suitable habitats. Conversely, widespread species such as U. vaginoclaustroides and Gyrodactylus sp. occur across diverse habitats, indicating high ecological tolerance and dispersal capacity. Despite their broad occurrence, variation in local abundance still contributes to community turnover.
This dual role of dominant and rare species in structuring β-diversity reflects patterns seen in both parasitic and free-living communities [46,47,56], highlighting the complex interplay of abundance, rarity, and spatial distribution in a metacommunity.
The EMS analysis revealed that helminth communities were non-randomly structured and exhibited significant coherence with environmental gradients. This supports the hypothesis that both abiotic and host-related factors shape parasite distributions, as observed in other freshwater parasite communities [25,57,58].
At the regional scale, communities displayed nested structures with boundary clumping, suggesting non-random species loss along environmental gradients, species-poor communities being subsets of richer ones. This pattern is indicative of environmental filtering favoring generalist or tolerant species. At the infracommunity level, most sites also showed significant coherence, although the metacommunity structures varied: some exhibited Clementsian or quasi-Clementsian organization (cohesive species clusters), while others followed Gleasonian or quasi-Gleasonian patterns (individualistic responses).
The coexistence of multiple metacommunity types suggests that local factors—including water quality, habitat complexity, and host density—interact with regional dispersal processes to shape community structure.
Guild-level analyses further revealed that all parasite groups responded non-randomly to spatial and environmental gradients, but the nature and strength of these responses varied. Larval helminths exhibited Gleasonian structure with boundary clumping, suggesting more spatially and environmentally structured communities influenced by shared hosts and synchronized life cycles (e.g., bird-mediated transmission). Monogeneans showed a quasi-Gleasonian structure, likely reflecting their strong host affinity and the potential for passive spread in connected aquatic habitats, as monogeneans may disperse more freely across hosts in a connected aquatic environment [59,60]. Their individualistic responses are consistent with environmental filtering as site specificity on gills or fins [61,62,63]. Adult helminths exhibited similar quasi-Gleasonian patterns, likely shaped by food web interactions and habitat requirements of intermediate hosts. Such individualistic responses are typical of tropical freshwater systems [14], where helminth communities vary markedly even within a single host species.
Overall, the gradient from quasi-Gleasonian to Gleasonian structures across guilds reflects increasing influence of dispersal limitation and life-cycle complexity. Our findings support the view that helminth metacommunities are structured by the interplay of environmental filtering, dispersal constraints, and host–parasite interactions [11,50,64].
Variance partitioning analyses revealed that habitat structure accounted for the largest proportion of variation in helminth community composition, whereas water quality and host size contributed moderately but not significantly. This pattern highlights the dominant role of environmental filtering over host-specific traits in determining helminth metacommunity structure (see also [25,26,57,58]).
Complementary regression analyses indicate species-specific responses to environmental variables such as salinity, altitude, and host density. Among parasite groups, monogeneans exhibited strong spatial structuring, suggesting that dispersal limitation and local environmental conditions are key determinants of their distribution—consistent with their direct life cycles and high host specificity [60]. In contrast, larval helminths were more strongly influenced by host ecological traits, reflecting the importance of trophic interactions in their transmission pathways [65]. The lack of consistent predictors for adult helminths may arise from the complexity of their multi-host life cycles, host immunity, phylogenetic constraints, coevolutionary history, or stochastic processes that obscure deterministic patterns.
Previous research similarly indicates that local environmental variables often outweigh spatial factors in shaping species community composition within aquatic ecosystems [57,58,66,67].
Overall, these findings suggest that although environmental factors predominate at the community level, species-level responses vary according to differences in life-history strategies, ecological tolerances, and transmission modes [21,27,43,60].

5. Conclusions

Helminth metacommunities in P. bimaculatus are strongly structured along the environmental gradient of La Antigua River. This system represents a regional metacommunity composed of a core group of widespread helminth species characterized by high ecological tolerance, broad dispersal and transmission capacities, and occurrence across multiple hosts and sites. These common species exhibit considerable variability in abundance, captured consistently across analytical approaches. In contrast, a subset of rare species displays restricted distributions, limited dispersal potential, and narrower ecological tolerance. Balanced variation in species abundance emerges as the primary mechanism driving β-diversity, with both widespread and rare taxa contributing substantially to turnover. The observed patterns indicate that helminth communities possess both local and regional structure, exhibit non-random composition, and respond predictably to shared environmental gradients. In some sites, parasite transmission is dominated by group-level processes, whereas in others it occurs more individually. Each taxon and parasite guild shows distinct, idiosyncratic responses to external drivers.
Overall, environmental gradients and anthropogenic pressures function as ecological filters that structure helminth communities. Among these factors, environmental filtering —particularly habitat structure—plays a stronger role than host-related traits in shaping community composition. Together, these findings underscore the value of parasites as model systems for testing ecological and metacommunity theory, and they highlight how dispersal processes and environmental heterogeneity interact to structure biodiversity in tropical freshwater ecosystems. By integrating β-diversity partitioning with metacommunity structure analysis, this study provides empirical evidence for the mechanisms governing spatial diversity patterns in parasite communities.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d17120864/s1, Table S1: Main characteristics of the localities in the La Antigua River basin, Veracruz, Mexico; Table S2: Helminths of Pseudoxiphophorus bimaculatus in 11 localities of the La Antigua River basin, Veracruz, Mexico. SCBD = Contribution of helminth taxa to β-diversity; Table S3: Elements of the structure of the metacommunity of parasitic helminths of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz; Table S4: Variance partition analysis showing the influence of the physicochemical variables of water (FQ), habitat structure (EH) and host size (LT) on the composition of the metacommunity of parasitic helminths guilds of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz; Table S5: Linear regression of the abundance of the most abundant helminths against eight abiotic variables; Figure S1: Geographic position of the 11 sites sampled in the La Antigua River, Veracruz, Mexico; Figure S2: Beta regression models assessing the relationship between site contributions to beta diversity (LCBD) and eight environmental variables; Figure S3: Relationship between species contribution to β-diversity (SCBD) and number of sites occupied by each species.

Author Contributions

Idea/concept development, I.L.-d.-M. and G.S.-M.; study design, G.S.-M.; methodology, I.L.-d.-M. and G.S.-M.; data collection, G.S.-M., J.M.C.-M., E.F.M.-F., N.M.-S., M.R.-G., I.G.-V. and J.M.-M.; data curation, I.L.-d.-M., G.S.-M., J.M.C.-M., E.F.M.-F., N.M.-S., M.R.-G., I.G.-V. and J.M.-M.; formal analysis (Data analysis), I.L.-d.-M., G.S.-M., O.R.-C. and B.Q.-M.; writing—original draft preparation, I.L.-d.-M. and G.S.-M.; writing—review and editing, I.L.-d.-M., G.S.-M. and O.R.-C.; funding acquisition, G.S.-M.; software or coding, I.L.-d.-M.; visualization or figures, I.L.-d.-M., G.S.-M., O.R.-C. and B.Q.-M.; project administration, G.S.-M.; supervision, G.S.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the Universidad Nacional Autónoma de México, Dirección General de Asuntos del Personal Académico, PAPIIT grant IN217723 and IN205526 to Guillermo Salgado-Maldonado. And by the Secretaría de Ciencia, Humanidades, Tecnología e Innovación SECIHTI (formerly CONAHCYT), grant A1-S-19959 to Guillermo Salgado-Maldonado.

Data Availability Statement

The original contributions presented in the study are included in the article/Supplementary Material. The data used in this article have already been published by Salgado-Maldonado et al. [37].

Acknowledgments

The first author gratefully acknowledges the Posgrado en Ciencias del Mar y Limnología at Universidad Nacional Autónoma de México (UNAM) for guiding her PhD studies. Ivonne López-del-Monte has received a fellowship (No. 968174) from Secretaría de Ciencias, Humanidades, Tecnología e Innovación (SECIHTI, formerly CONAHCYT).

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

dBCAbundance-based multiple-site dissimilarity Bray–Curtis index
dBG.GRAPartitioned beta diversity into abundance gradients
dBC.BALPartitioned beta diversity into balanced variation in abundance
LCBDLocal contribution to beta diversity
SCBDSpecies contribution to beta diversity
EMSElements metacommunity structure

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Figure 1. Range-abundance curves of the 11 localities in the La Antigua River, Veracruz, Mexico. The numerically dominant taxa in each locality are indicated: Centrocestus formosanus (CEFO), Urocleidoides vaginoclaustrumoides (URVA), Gyrodactylus sp. (GYRO), Gyrodactylus takoke (GYTA), and Phyllodistomum inecoli (PHIN). Locations are ordered by their helminth richness. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11).
Figure 1. Range-abundance curves of the 11 localities in the La Antigua River, Veracruz, Mexico. The numerically dominant taxa in each locality are indicated: Centrocestus formosanus (CEFO), Urocleidoides vaginoclaustrumoides (URVA), Gyrodactylus sp. (GYRO), Gyrodactylus takoke (GYTA), and Phyllodistomum inecoli (PHIN). Locations are ordered by their helminth richness. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11).
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Figure 2. Non-metric Multidimensional Scaling (NMDS) analysis to visualize the relationships between component communities of helminth parasites of Pseudoxiphophorus bimaculatus examined from 11 localities along the La Antigua River. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11). Even though a certain tendency is observed, grouping the middle basin localities or the lower basin localities together as per their similarity, the overall clustering of the localities did not reveal any clear structure as per the altitudinal position along the river. The Analysis of Similarities (ANOSIM) indicate moderate and significant separation between groups (R = 0.36, p = 0.02).
Figure 2. Non-metric Multidimensional Scaling (NMDS) analysis to visualize the relationships between component communities of helminth parasites of Pseudoxiphophorus bimaculatus examined from 11 localities along the La Antigua River. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11). Even though a certain tendency is observed, grouping the middle basin localities or the lower basin localities together as per their similarity, the overall clustering of the localities did not reveal any clear structure as per the altitudinal position along the river. The Analysis of Similarities (ANOSIM) indicate moderate and significant separation between groups (R = 0.36, p = 0.02).
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Figure 3. Topographic profile of La Antigua River. (A) General map showing the position of La Antigua River basin in Veracruz state (shaded area) in the Gulf of Mexico. (B) General profile of the La Antigua River basin and geographic location of sampling sites. (C) Topographic profile of the La Antigua River basin showing elevation of the sampling sites. The y-axis represents elevation (meters above sea level) along the longitudinal river gradient; circles represent the 11 sampling sites, where circle size indicates species richness and color intensity represents the Local Contribution to β-diversity (LCBD) value; N is the total number of helminths recovered per locality. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11). Notably, mid-elevation sites such as Jalcomulco exhibited high richness and LCBD, while peripheral or extreme localities in highlands (e.g., Xico) and lowlands (e.g., Antigua Presa) showed lower richness but distinctive community composition, e.g., high LCBD values.
Figure 3. Topographic profile of La Antigua River. (A) General map showing the position of La Antigua River basin in Veracruz state (shaded area) in the Gulf of Mexico. (B) General profile of the La Antigua River basin and geographic location of sampling sites. (C) Topographic profile of the La Antigua River basin showing elevation of the sampling sites. The y-axis represents elevation (meters above sea level) along the longitudinal river gradient; circles represent the 11 sampling sites, where circle size indicates species richness and color intensity represents the Local Contribution to β-diversity (LCBD) value; N is the total number of helminths recovered per locality. Sites are Pixquiac (M1), Xico (M2), Agua Bendita (M3), Teocelo (M4), Baxtla (M5), Jalcomulco (M6), Apazapan (L7), Río Los Pescados (L8), El Carrizal (L9), Puente Nacional (L10), and Antigua Presa (L11). Notably, mid-elevation sites such as Jalcomulco exhibited high richness and LCBD, while peripheral or extreme localities in highlands (e.g., Xico) and lowlands (e.g., Antigua Presa) showed lower richness but distinctive community composition, e.g., high LCBD values.
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Figure 4. Relationship between the richness of helminth taxa and the Local Contribution to β-diversity (LCBD) across sampling sites. A non-linear (quadratic) regression model was fitted to the data (solid line); the shaded area represents the 95% confidence interval. Each circle represents a locality. (A) Overall (all together) helminths. (B) Monogeneans. (C) Adult helminths. (D) Larvae.
Figure 4. Relationship between the richness of helminth taxa and the Local Contribution to β-diversity (LCBD) across sampling sites. A non-linear (quadratic) regression model was fitted to the data (solid line); the shaded area represents the 95% confidence interval. Each circle represents a locality. (A) Overall (all together) helminths. (B) Monogeneans. (C) Adult helminths. (D) Larvae.
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Figure 5. Models evaluating the relationship between species contributions to beta diversity (SCBD) and the abundance of each helminth taxa (circles) the three most abundant of which are identified. CEFO, Centrocestus formosanus; GYRO, Gyrodactylus sp.; URVA, Urocleidoides vaginoclaustrumoides.
Figure 5. Models evaluating the relationship between species contributions to beta diversity (SCBD) and the abundance of each helminth taxa (circles) the three most abundant of which are identified. CEFO, Centrocestus formosanus; GYRO, Gyrodactylus sp.; URVA, Urocleidoides vaginoclaustrumoides.
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Figure 6. Models evaluating the relationship between species contributions to beta diversity (SCBD) and the number of sites occupied by each taxon. The species that contributed to the above-average β-diversity (SCBD > 0.06) are indicated: CEFO, Centrocestus formosanus; CONT, Contracaecum sp.; FRMO, Freitascapillaria moraveci; PHIN, Phyllodistomum inecoli; GYXA, Gyrodactylus xalapensis; GYRO, Gyrodactylus sp.; URVA, Urocleidoides vaginoclaustrumoides.
Figure 6. Models evaluating the relationship between species contributions to beta diversity (SCBD) and the number of sites occupied by each taxon. The species that contributed to the above-average β-diversity (SCBD > 0.06) are indicated: CEFO, Centrocestus formosanus; CONT, Contracaecum sp.; FRMO, Freitascapillaria moraveci; PHIN, Phyllodistomum inecoli; GYXA, Gyrodactylus xalapensis; GYRO, Gyrodactylus sp.; URVA, Urocleidoides vaginoclaustrumoides.
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Figure 7. Redundancy analysis (RDA) between multiple abiotic factors and the metacommunity of parasitic helminths of P. bimaculatus. PSU: Practical Salinity Units; LA_US: Land Use; PE_DO: Percentage of dissolved oxygen; ALTI: Altitude; HA_DI: Habitat diversity; HO_DE: Host density; WA_VE: Water velocity; DI_PO: Human distance population; BA_ER: Bank erosion.
Figure 7. Redundancy analysis (RDA) between multiple abiotic factors and the metacommunity of parasitic helminths of P. bimaculatus. PSU: Practical Salinity Units; LA_US: Land Use; PE_DO: Percentage of dissolved oxygen; ALTI: Altitude; HA_DI: Habitat diversity; HO_DE: Host density; WA_VE: Water velocity; DI_PO: Human distance population; BA_ER: Bank erosion.
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Table 1. Values of the Bray–Curtis multi-site dissimilarity index (dBC); and partition dBC.bal value of the component of balanced variation; dBC.gra value of the component of the abundance gradient. Values are the calculated values of Bray–Curtis and partitions obtained by comparing among the 11 localities (component community) and comparing the individual fish (infracommunities) examined from each locality. “Between localities” values were calculated by comparing the summed data of each fish examined from each of the 11 localities. “Between hosts” refers to values obtained by comparing across all infracommunities.
Table 1. Values of the Bray–Curtis multi-site dissimilarity index (dBC); and partition dBC.bal value of the component of balanced variation; dBC.gra value of the component of the abundance gradient. Values are the calculated values of Bray–Curtis and partitions obtained by comparing among the 11 localities (component community) and comparing the individual fish (infracommunities) examined from each locality. “Between localities” values were calculated by comparing the summed data of each fish examined from each of the 11 localities. “Between hosts” refers to values obtained by comparing across all infracommunities.
Overall Helminths
11 Localities, 220 Hosts		Monogeneans
11 Localities, 144 Hosts		Intestinal Adults
6 Localities; 75 Hosts		Larvae
6 Localities; 48 Hosts
LocalitiesdBC.baldBC.gradBCdBC.baldBC.gradBCdBC.baldBC.gradBCdBC.baldBC.gradBC
Between localities0.650.270.920.320.530.850.400.420.820.520.460.98
Between hosts0.960.030.990.910.070.980.920.050.970.760.210.97
M10.760.110.870.740.130.87
M20.690.180.870.290.390.680.090.590.68
M30.680.200.880.390.450.840.530.340.87
M40.720.160.880.560.300.860.690.130.82
M50.600.290.890.520.370.890.430.310.74101
M60.780.150.930.610.250.860.760.140.900.560.370.93
L70.820.080.9000.780.780.770.100.870.810.080.89
L80.780.070.850.750.090.84
L90.880.100.980.790.070.86 0.880.100.98
L100.840.050.890.820.050.87 101
L110.670.190.860.310.340.65 0.600.230.83
Table 2. Elements of the structure of the metacommunity of parasitic helminths of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz. * Significance p ≤ 0.05. Abs = number of absences embedded by the null model, Mean = mean value of null model simulations, Rep = number of replacements, M. I. = Morisita’s Index, V = variance.
Table 2. Elements of the structure of the metacommunity of parasitic helminths of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz. * Significance p ≤ 0.05. Abs = number of absences embedded by the null model, Mean = mean value of null model simulations, Rep = number of replacements, M. I. = Morisita’s Index, V = variance.
SiteScaleCoherenceTurnoverBoundary Clumping
AbsMeanVRepMeanVM. I.Structure
OverallComponent communities46 *87.588.15264270.1074.972.15 *Nestedness
(Clustered loss of species)
M1Infracommunities024.43 *5.80111.057.6629.440Quasi-Gleasonian
M2Infracommunities12.5813.0 *3.0447.026.1615.784.5 *Quasi-Clementsian
M3Infracommunities27.053.51 *8.20386.0229.9895.431.54Quasi-Gleasonian
M4Infracommunities28.059.48 *6.55287.0111.36 *69.182.5 *Clementsian
M5Infracommunities14.061.91 *7.87194170.4958.592.07 *Quasi-Clementsian
M6Infracommunities99.0147.791 *9.84817.0369.86 *149.400.98Gleasonian
L7Infracommunities24.074.12 *11.15258.0161.29 *45.721.75 *Clementsian
L8Infracommunities4.015.21 *3.7190.058.2027.121.79Quasi-Gleasonian
L9Infracommunities017.50 *4.6467.049.359.691.8 *Quasi-Clementsian
L10Infracommunities2.018.23 *4.3870.053.2414.741Quasi-Gleasonian
L11Infracommunities4.015.35 *3.0748.0339.9620.191.57Quasi-Gleasonian
Table 3. Variance partition analysis showing the influence of the physicochemical variables of water (FQ), habitat structure (EH) and host size (LT) on the composition of the metacommunity of parasitic helminths of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz. [FQ + EH + LT = Total variation explained]; [FQ|EH + LT = Variation explained only by the physicochemical variables]; [EH|FQ + LT = Variation explained only by the habitat structure variables]; [LT|FQ + EH = Variation explained only by host size]; Residual = residual variance; R2 = Adjusted coefficient of determination; * Significance = p < 0.05.
Table 3. Variance partition analysis showing the influence of the physicochemical variables of water (FQ), habitat structure (EH) and host size (LT) on the composition of the metacommunity of parasitic helminths of Pseudoxiphophorus bimaculatus in the La Antigua River, Veracruz. [FQ + EH + LT = Total variation explained]; [FQ|EH + LT = Variation explained only by the physicochemical variables]; [EH|FQ + LT = Variation explained only by the habitat structure variables]; [LT|FQ + EH = Variation explained only by host size]; Residual = residual variance; R2 = Adjusted coefficient of determination; * Significance = p < 0.05.
VariableR2p
FQ + EH + LT0.860.002 *
FQ|EH + LT0.420.10
EH|FQ + LT0.690.05 *
LT|FQ + EH0.270.08
Residual0.14
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López-del-Monte, I.; Rico-Chávez, O.; Caspeta-Mandujano, J.M.; Mendoza-Franco, E.F.; Mercado-Silva, N.; Montoya-Mendoza, J.; Rubio-Godoy, M.; Guzmán-Valdivieso, I.; Quiroz-Martínez, B.; Salgado-Maldonado, G. Turnover, Uniqueness, and Environmental Filtering Shape Helminth Parasite Metacommunities in Freshwater Fish Pseudoxiphophorus bimaculatus (Cyprinodontiformes: Poeciliidae). Diversity 2025, 17, 864. https://doi.org/10.3390/d17120864

AMA Style

López-del-Monte I, Rico-Chávez O, Caspeta-Mandujano JM, Mendoza-Franco EF, Mercado-Silva N, Montoya-Mendoza J, Rubio-Godoy M, Guzmán-Valdivieso I, Quiroz-Martínez B, Salgado-Maldonado G. Turnover, Uniqueness, and Environmental Filtering Shape Helminth Parasite Metacommunities in Freshwater Fish Pseudoxiphophorus bimaculatus (Cyprinodontiformes: Poeciliidae). Diversity. 2025; 17(12):864. https://doi.org/10.3390/d17120864

Chicago/Turabian Style

López-del-Monte, Ivonne, Oscar Rico-Chávez, Juan Manuel Caspeta-Mandujano, Edgar Fernando Mendoza-Franco, Norman Mercado-Silva, Jesús Montoya-Mendoza, Miguel Rubio-Godoy, Ismael Guzmán-Valdivieso, Benjamín Quiroz-Martínez, and Guillermo Salgado-Maldonado. 2025. "Turnover, Uniqueness, and Environmental Filtering Shape Helminth Parasite Metacommunities in Freshwater Fish Pseudoxiphophorus bimaculatus (Cyprinodontiformes: Poeciliidae)" Diversity 17, no. 12: 864. https://doi.org/10.3390/d17120864

APA Style

López-del-Monte, I., Rico-Chávez, O., Caspeta-Mandujano, J. M., Mendoza-Franco, E. F., Mercado-Silva, N., Montoya-Mendoza, J., Rubio-Godoy, M., Guzmán-Valdivieso, I., Quiroz-Martínez, B., & Salgado-Maldonado, G. (2025). Turnover, Uniqueness, and Environmental Filtering Shape Helminth Parasite Metacommunities in Freshwater Fish Pseudoxiphophorus bimaculatus (Cyprinodontiformes: Poeciliidae). Diversity, 17(12), 864. https://doi.org/10.3390/d17120864

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