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Article

Substrate Preference and Seasonal Distribution of Bdelloid Rotifers in Mosses in a Primary Forest in Thailand

by
Poomipat Pokpongmongkol
1,
Rapeepan Jaturapruek
1,
Phannee Sa-ardrit
2 and
Supiyanit Maiphae
1,3,*
1
Animal Systematics and Ecology Research Unit, Department of Zoology, Faculty of Science, Kasetsart University, Bangkok 10900, Thailand
2
The Princess Maha Chakri Sirindhorn Natural History Museum and RSPG Southern Region Network Coordinating Center, Prince of Songkla University, Songkhla 90110, Thailand
3
Biodiversity Center Kasetsart University (BDCKU), Bangkok 10900, Thailand
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(3), 171; https://doi.org/10.3390/d17030171
Submission received: 11 February 2025 / Revised: 25 February 2025 / Accepted: 26 February 2025 / Published: 27 February 2025
(This article belongs to the Section Biodiversity Conservation)
Browse Figures
Versions Notes

Abstract

:
Previous studies have shown that the bdelloid rotifer diversity and composition vary across substrates, yet microscale investigations remain unexplored. To address this gap in knowledge, we examined the diversity, density, and composition of bdelloid rotifers across moss substrates and seasons. They were analyzed from 491 moss samples collected monthly from seven substrate types in a primary forest in Thailand between September 2021 and December 2022. Our study reveals high bdelloid rotifer diversity. The morphological and molecular analyses identified 17 species, including 4 new records for Thailand, increasing the total to 34. In addition, while moss on tree trunks and the wet season showed a high species richness and total density, the results revealed no significant variation across the substrates or seasons. However, the similarity of the species composition varied significantly between the substrates (<25%) and between seasons (36.99%). Moreover, rainfall and humidity appear to be key factors shaping the bdelloid rotifer community in this limnoterrestrial habitat.

1. Introduction

Substrates play a crucial role in shaping the richness, abundance, and ecological dynamics of invertebrate communities in aquatic environments [1,2,3] because they provide essential habitats and resources for a diverse array of invertebrates [4]. In addition, the complexity of substrates is likely to increase the heterogeneity of the invertebrate community [2,5], even in artificial substrates [6]. The texture and composition of substrates can influence the types of microhabitats available, such as crevices for shelter or surfaces for feeding, which directly impact species diversity and population densities [7]. For instance, in areas with varied and complex substrates, there tends to be a higher invertebrate richness due to the availability of multiple niches and the provision of different resources [8]. Additionally, substrates affect ecological processes by influencing nutrient cycling, sedimentation rates, and interactions between species [9]. Hard substrates, like stones and logs, often support diverse communities of algae and microorganisms, which in turn provide food for larger invertebrates, while softer substrates like silt and mud can support different assemblages adapted to these environments [10,11]. Overall, the characters of substrates are integral to the functioning of aquatic ecosystems, driving patterns of invertebrate distribution and their roles in ecological processes [12].
Besides the substrates being fundamental in shaping the diversity, abundance, and ecological roles of aquatic invertebrates, the terrestrial one is also affected as they provide essential resources and habitats for these organisms. The variety of substrates found in terrestrial environments, such as soil, leaf litter, decaying wood and rocky surfaces, creates a mosaic of microhabitats that support different invertebrate communities [13,14]. For example, leaf litter and decomposing wood offer critical resources for detritivores, which play a key role in nutrient cycling and soil formation [15]. The physical characteristics of substrates, including their moisture content, texture, and organic matter content, influence the distribution and activity of invertebrates such as beetles, ants, and spiders, by affecting their foraging efficiency, reproduction, and shelter availability [16]. Additionally, substrates can impact ecological processes by influencing the decomposition rates of organic matter and the dynamics of soil nutrients, which in turn affect plant communities and overall ecosystem functioning [17]. Thus, the composition and quality of substrates are integral to maintaining the structure and function of terrestrial ecosystems by supporting diverse invertebrate populations and their ecological roles.
Bdelloid rotifers are small invertebrates that are widespread and often abundant in freshwater and limnoterrestrial habitats. Most species can resist desiccation by entering a dormant state at any stage of their lifespan, producing resistant propagules that facilitate long-distance dispersal. Consequently, they exhibit remarkable adaptability and tolerance to harsh environmental conditions, including extreme temperatures [18], drought [19,20], and ionizing radiation [21]. However, the level of tolerance varies among species, as evidenced by differences in species composition across habitats. For instance, each species demonstrates distinct tolerance levels, allowing them to occupy habitats with varying humidity [5,22].
Previous studies have shown that some bdelloid species are more frequent on saprobic substrates, others are found in soft-bottom sediments, and some prefer diverse bog habitats. Only a few species exhibit exceptionally broad ecological ranges [23]. Furthermore, differences in species composition have been reported across habitats such as soil, tree roots, tree bark, plants, lichens, and moss [5,24].
An intriguing aspect of bdelloid biology is their substrate preference, which provides insights into their ecological roles and interactions within various habitats. This study aims to examine the species diversity of bdelloid rotifers within moss substrates and determine whether they exhibit specific preferences for different substrate types. By analyzing the species composition and relative abundance across various moss substrates, we also aim to test whether the substrate type influences the seasonal richness and composition of bdelloids in moss within a primary forest. Understanding these interactions can enhance our knowledge of their ecological niches and the factors driving their habitat selection.

2. Materials and Methods

2.1. Study Area and Sample Collection

A total of 491 moss samples were collected monthly between September 2021 and December 2022 from a primary forest in Ban Rom Klao Phitsanulok Botanical Garden by Royal Initiative, Phitsanulok Province, Thailand (17.6109184506, 100.9049361433) (Figure 1A). Sampling months were categorized into two seasons based on rainfall: wet period: September–October 2021 and May–October 2022 (rainfall 79.2–385.9 mm, mean 231.04 mm); and dry period: November 2021–April 2022 and December 2022 (rainfall 0.3–114.6 mm, mean 43.88 mm) (http://www.cmmet.tmd.go.th/station/phit/index1.php, accessed on 20 January 2024).
Moss samples were collected from seven substrate types found in the sampling area, including the following: moss on tree trunks (vertical surfaces of living trees), moss on soil (ground-level moss), moss on roots (growing around exposed tree roots), moss on rotting logs (small, decaying pieces of dead trees on the ground), moss on rocks (covering the surfaces of stones and boulders), moss on logs (growing on fallen or partially decomposed tree trunks), and moss on leaves (growing on the surfaces of living or dead leaves on the ground) (Figure 1B–H). The collected moss samples were stored in zip-lock plastic bags and later examined in the laboratory. These samplings were conducted in compliance with ethical standards and approved by the Institutional Animal Care and Use Committee, Kasetsart University (approval no. ACKU65-SCI-025).

2.2. Sample Preparation and Species Identification and Count

Each moss sample was trimmed into 3 × 3 cm pieces and soaked in distilled water for 24 h to facilitate the recovery of bdelloid rotifers. After soaking, the water was separated from the moss, fresh water was added, and the sample was shaken thoroughly. The water from the second rinse was combined with the initial water sample.
Bdelloid rotifers from each water sample were sorted using a stereomicroscope (Olympus SZ51). Individual specimens were examined for morphological characteristics under a light microscope (Olympus CH2) while still alive. Taxonomic features were photographed and recorded on video for detailed analysis. The identification of bdelloid rotifers was based on morphological characteristics and followed the identification keys and descriptions from the up-to-date references [25,26,27,28].
In addition to morphological identification, molecular analysis was conducted to confirm species identity. Each specimen was soaked and preserved in 95% ethanol, then transferred to a 0.2 mL PCR tube and dried. DNA was extracted from the whole body of a single specimen using a modified HotSHOT protocol, following the method of Garcia-Morales and Elias-Gutierrez [29]. The target DNA fragment, mitochondrial cytochrome c oxidase subunit I (COI), was amplified via polymerase chain reaction (PCR) using universal primers LCO1490 (5′-GGTCAACAAATCATAAAGATATTGG-3′) and HCO2198 (5′-TAAACTTCAGGGTGACCAAAAAATCA-3′) [30]. PCR amplification was performed in a 25 µL reaction volume under the following conditions: initial denaturation at 94 °C for 5 min, followed by 35 cycles of a second denaturation at 94 °C for 1 min, annealing at 48 °C for 1 min, extension at 72 °C for 50 s, followed by a final extension at 72 °C for 7 min, which is then dropped to 4 °C. Post-PCR, 4 µL of each product was subjected to electrophoresis on a 1.2% agarose gel stained with SYBR Safe DNA Gel Stain at 100 V for 25 min. The results were visualized under a UV transilluminator. Samples with clearly visible expected bands were purified using the FavorPrep™ Gel/PCR Purification Kit (Favorgen, Ping Tung, Taiwan). The purified products were subsequently sequenced by Macrogen Inc. (Seoul, Republic of Korea).

2.3. Data Analysis

2.3.1. Species Richness and Diversity

Species richness was determined by counting the number of bdelloid species across different moss substrates. Bdelloid diversity was assessed using the Shannon–Wiener diversity index. Both species richness and the Shannon diversity index were employed to compare bdelloid rotifer diversity across various moss substrates and between wet and dry periods. All analyses were conducted in Microsoft Excel (Microsoft 365).
The Shapiro–Wilk test was performed using R Statistical Software (v4.1.2) [31] to assess data normality. Normality was confirmed for species richness (p = 0.069) but not for density (p = 0.003). Therefore, density was log-transformed to meet normality assumptions before performing the t-test. An independent sample t-test was then conducted in Microsoft Excel to compare mean species richness and density between seasons.

2.3.2. Species Composition

Differences in species composition were assessed using the Bray–Curtis index of community dissimilarity [32]. Principal Coordinates Analysis (PCoA) was performed to visualize variations in bdelloid community between samples based on dissimilarity distances. The analysis was conducted using the PC-ORD software, version 7.11 [33]. Prior to analysis, species abundance data were log-transformed to normalize the dataset. A Euclidean distance measure was used for the analysis. Convex hull polygons were applied to delineate groups of variables, including substrates and seasons.

2.3.3. Species–Environment Relationship

Species distributions in relation to environmental variables were assessed using Canonical Correspondence Analysis (CCA) [34] with the PC-ORD software, version 7.11 [32]. The significance of the environmental variables was tested using the Monte Carlo test with 1000 random permutations.

2.3.4. Molecular Analysis

Chromatograms for all DNA sequences were reviewed and manually edited using Chromas software, version 2.6.6 [35]. COI sequences of related species from the genera Habrotrocha, Macrotrachela, Mniobia, and Rotaria were downloaded from GenBank and included in the analysis (Table 1). Sequences were aligned using the MAFFT web server (https://mafft.cbrc.jp/alignment/server/, accessed on 19 February 2024) with default settings [36]. The alignments were double-checked manually using Mesquite, version 3.70 [37]. To minimize redundant information, COI haplotypes were described using the Fabox web server (https://birc.au.dk/~palle/php/fabox/, accessed on 19 February 2024) [38].
Phylogenetic relationships were inferred using Bayesian Inference (BI) analysis on the CIPRES Science Gateway (https://www.phylo.org/, accessed on 19 February 2024) [39]. The BI analysis was performed using BEAST v.1.8.4 [40], with the input file created using BEAUti v.1.8.0 [41]. The General Time-Reversible model of evolution with a proportion of invariable sites and a discrete gamma-distributed rate among sites (GTR + I + G) was selected as the best-fitting model for the COI dataset. An uncorrelated lognormal relaxed clock was applied. Markov chain Monte Carlo (MCMC) analyses were conducted for 100 million generations, with sampling every 10,000 generations. Convergence of the MCMC runs was assessed based on effective sample size (ESS) values greater than 200, and the burn-in was determined using Tracer v.1.7.1 [42]. The consensus tree was constructed after discarding the first 10 million generations as burn-in using TreeAnnotator v.1.10.4 [40]. Lecane bulla was used as the outgroup for phylogenetic reconstruction.

2.3.5. Species Delimitation

Four independent methods were applied for species delimitation based on the COI dataset. The Automatic Barcode Gap Discovery (ABGD) method [43] was run through the online ABGD web server (https://bioinfo.mnhn.fr/abi/public/abgd/abgdweb.html, accessed on 19 February 2024) with the following settings: 1.0 × (relative gap width) and Jukes–Cantor (JC69) as the substitution model.
The Assemble Species by Automatic Partitioning (ASAP) method was implemented using the online ASAP web server (https://bioinfo.mnhn.fr/abi/public/asap/, accessed on 19 February 2024) with the simple distance setting. The Bayesian implementation of Poisson Tree Processes (bPTP) [44] was performed using the online PTP web server (https://species.h-its.org/, accessed on 19 February 2024). The General Mixed Yule Coalescent (GMYC) model [45] was analyzed using the GMYC web server (https://species.h-its.org/gmyc/, accessed on 19 February 2024). Genetic distances were calculated within and between species using the Kimura 2-parameter model with pairwise deletion and 1000 bootstrap replications in MEGA X [46].

3. Results

3.1. Molecular Taxonomy

A total of 32 bdelloid rotifer sequences from moss samples in Thailand, along with 39 sequences of related species downloaded from NCBI, were molecularly analyzed. The COI marker was successfully amplified in 32 individuals from four genera. However, some species, including Adineta bartosi Wulfert 1960; A. tuberculosa Janson, 1893; A. vaga (Davis, 1873); Adineta sp.; Habrotrocha sp.3; Habrotrocha sp.4; Habrotrocha sp.5; and Habrotrocha sp.6, were excluded from the analysis due to the failure of COI amplification.
The phylogenetic tree, based on the aligned 661 bp of the COI dataset, shows strong to moderate branch support. Sixty-eight haplotypes from all 71 sequences were used for DNA taxonomy approaches (Figure 2). A sequence of Lecane bulla (Gosse, 1851) from the NCBI was included in the phylogenetic reconstruction as an outgroup. For Mniobia russeola Zelinka 1891, the ABGD, ASAP, bPTP, and GMYC models produced the same results, identifying four distinct entities. One specimen from moss on roots (SP157_MRO) was separated from two specimens on tree trunks (SP158_MT and SP159_MT). For Rotaria sordida (Western, 1893), 13–17 entities were identified within a single morphospecies.
The Thai R. sordida populations revealed four major groups with strong branch support, which are primarily separated by the type of moss substrate. Group 1 consists of seven specimens (SP138, SP147, SP193, SP198, SP199, SP202, and SP207), mostly found on logs, with the exception of SP193, which was found on a tree trunk. Group 2 contains two specimens (SP190 and SP196), both from soil substrates. Group 3 includes three specimens (SP203, SP204, and SP206), all found on logs. Group 4 consists of two specimens: SP155 from a root and SP200 from a log (Figure 2). Habrotrocha spp. from Thailand are clearly separated into five groups, which correspond to their distinct morphological characteristics. However, Habrotrocha lata (Bryce, 1892) (SP130) was an exception, as it was divided from the other two sequences of the same species and clustered closely with the H. ligula sequence from GenBank. Additionally, SP123 and SP205 from Thailand clustered with Macrotrachela quadricornifera Milne, 1886 and M. multispinosa Thompson, 1892 from other countries, respectively, confirming their morphological identity.
The genetic distances between and within the 16 species are presented in Table 2. The genetic distance between species ranged from 0.11 to 0.29, while the genetic distance within species ranged from 0.00 (for Mniobia incrassata (Murray, 1905); Habrotrocha antarctica Iakovenko, Smykla, Convey, Kasparona, Kozeretska, Trokhymets, Dykyy, Plewka, Devetter & Janko, 2015; and Habrotrocha sp.1) to 0.15 (for M. russeola).

3.2. Species Diversity

Out of 491 moss samples examined, 40 were found to contain living bdelloid rotifers, accounting for 8.15% of the total samples. Based on the examination of the morphological characteristics and molecular data, a total of 5 genera and 17 species were identified. Four species—A. bartosi, A. tuberculosa, H. lata, and M. russeola—were new records for Thailand (Table 3, Figure 3). The highest species richness was found in the mosses on tree trunks (14 species), followed by mosses on soil (7 species), mosses on logs (5 species), mosses on rotting logs (3 species), and mosses on roots (3 species), which corresponds with the Shannon diversity index (Table 4). Additionally, the wet period exhibited a higher species richness and a higher Shannon diversity index compared to the dry period (Table 4). The results also showed that the most diverse genera tended to be the most abundant, with the exception of Rotaria. Among them, Habrotrocha was the most speciose (nine species) and the dominant genus (40.67% of the total individuals found across all substrates), followed by Adineta (four species, 9.33%), Rotaria (one species, 13.33%), Macrotrachela (two species, 4.67%), and Mniobia (one species, 2%) (Figure 4). When examining the distribution of bdelloid rotifers across the different moss substrates, it was found that two substrates—moss on rocks and moss on leaves—did not contain any bdelloid rotifers. Additionally, all genera were observed in the moss on tree trunks, with most genera predominantly distributed in this substrate (57.38–100%), except for Macrotrachela and Rotaria, which were primarily found in the moss on logs (42.86% and 65%, respectively) (Figure 5).

3.3. Bdelloid Rotifer Community in Substrate Type of Mosses

The PCoA results indicate a low similarity in the bdelloid species across each variable (Figure 6A,B). The first two PCoA axes for the moss substrate and season accounted for a substantial proportion of the total variance (50.17%), with 29.78% explained by the first axis and 20.39% by the second axis. These findings align with the Bray–Curtis index, which shows only a 36.99% similarity between seasons (Table S1). Among the substrates, the bdelloid species composition is generally dissimilar, with the moss on tree trunks showing the greatest difference from the others (5.66–21.14% similarity). Although most of the species were widely distributed, all of the Adineta species were exclusively found in the moss on tree trunks and during the wet season. In contrast, R. sordida was present in the moss from all substrates, while the member of genus Habrotrocha was found in the moss from all substrates except for the moss on tree roots (Figure 6A,B).

3.4. Distribution of Bdelloid Rotifers in Each Period

The species richness and total density of bdelloid rotifers fluctuated across the months. The number of species peaked at 9 in November 2021, while it was low in December 2021 and April 2022, with only 0–1 species observed (Figure 7A). The bdelloid density also fluctuated throughout the study, decreasing during low rainfall periods, gradually rising until the dry period, and then declining again (Figure 7B,D). The density peaked in September 2021 during the wet period and reached its lowest in December 2021, February, and April 2022 during the dry period. Although the total density was higher in the wet period than in the dry period, the difference was not statistically significant (p = 0.38). Similarly, the species richness was higher in the wet season, but monthly comparisons between the two seasons showed no significant difference (p = 0.84) (Figure 7C).

3.5. Influences of Environmental Variables on Bdelloid Rotifer

The Canonical Correspondence Analysis (CCA) revealed a significant correlation between the bdelloid community and environmental variables (Monte Carlo test, p = 0.01) (Figure 8). The eigenvalues for Axis 1 and Axis 2 were 0.644 and 0.147, respectively. Among the environmental variables, relative humidity (Axis 1 r = 0.836, Axis 2 r = 0.122) and rainfall (Axis 1 r = 0.619, Axis 2 r = 0.364) showed the strongest correlations with the bdelloid communities. A strong positive correlation was observed between these factors and all of the Adineta species, including A. vaga, A. bartosi, A. tuberculosa, Adineta sp., and M. russeola, as well as Habrotrocha sp. 4. These species were predominantly found during the wet season, when the humidity levels ranged from 83% to 85%, and the rainfall varied between 312.1 mm and 378.7 mm.

4. Discussion

4.1. Species Diversity

The results of this study reveal a high diversity of bdelloid rotifers in limnoterrestrial habitats. Seventeen taxa were identified, representing approximately 3% of the known global bdelloid species diversity [27,47]. Additionally, four new records have increased the number of bdelloid rotifer species reported in Thailand from 30 to 34 [28,48,49,50]. The first records of A. bartosi, A. tuberculosa, H. lata, and M. russeola in the country have expanded their geographical range. The first two species have been reported from limited geographical regions [27], suggesting a broader distribution than previously documented. Additionally, the first records of H. lata and M. russeola in Thailand, despite their widespread distribution [27], highlight the importance of studying bdelloid diversity across various microhabitats to accurately assess the actual species richness of the country. Notably, the discovery of M. russeola in this study suggests that its distribution is widespread across all geographic regions, except for the Palaearctic [27]. Among the species found in the moss on soil, H. lata was the only species recorded for the first time in this substrate [25,51]. However, it was found that this primary forest has a lower bdelloid species richness compared to that in beach forests, despite year-round monthly sampling [52]. This difference may be attributed to the wider range of environmental variables in beach forests, which provide a variety of ecological niches that support a greater diversity of species. In contrast, the more stable environmental conditions in primary forests may limit the diversity of bdelloid species. Additionally, the species composition between these two forest types is notably distinct, with an 89% dissimilarity [52].
In terms of the density and distribution, Habrotrocha, Adineta, and Rotaria are the three genera with the highest density found in mosses in this area. These genera are present year-round, in both the wet and dry periods, indicating their ability to thrive under varying environmental conditions [25,53]. Notably, R. sordida, which was found in mosses from all substrates, is recognized as a successful anhydrobiotic species [54], suggesting that it is an effective disperser. Furthermore, the high density of Adineta found in this study is consistent with previous research [24], which identified Adineta as a dominant genus in terrestrial habitats such as moss, soil, and especially bark. Among the various substrates, the mosses growing on trees exhibited the highest species richness, accounting for approximately 82% of all the recorded species. This is likely due to the superior moisture retention capacity of moss on tree trunks compared to other substrates. The ability of tree moss to retain moisture likely contributes to the greater richness and abundance of bdelloid individuals observed [55]. This substrate appears to maintain a stable microenvironment, even during dry periods, which supports the cryptobiotic survival strategies of bdelloids. The constant moisture helps sustain their metabolic activity more continuously than in less stable habitats [56,57]. Consequently, moss on tree trunks provides a suitable habitat, fostering the high diversity of bdelloid rotifers. However, the moisture content was not measured in this study, highlighting the need for further research to assess its role in the bdelloid distribution and diversity.

4.2. Ecological and Temporal Distributions

Bdelloid rotifers exhibit a high degree of habitat specialization at the microscale, with limited overlap among communities across different substrate types, particularly in moss on tree trunks. This may be due to the unique characteristics of moss on tree trunks, especially its superior moisture retention compared to other substrates. These findings align with previous studies that have reported significant differences in bdelloid communities across various habitat types [5]. This is most likely due to the distinct characteristics of these habitats, particularly in terms of structural complexity, which has a strong influence on the occurrence of different bdelloid communities [58,59]. The observation of distinct species compositions among moss, lichen, soil, and bark habitats in Turkey highlighted habitat specialization among bdelloid rotifers [5]. However, only 15% of the bdelloid species overlapped across the different substrate types, whereas most of them were specific to certain types of substrates [60]. The habitat type influences bdelloid colonization, with small variations in factors such as moisture or humidity leading to significant differences in bdelloid communities [22,61]. Additionally, studies have shown that environmental parameters influencing the occurrence of bdelloid rotifers in temperate regions differ from those in tropical regions [49,62], as well as between freshwater ecosystems and limnoterrestrial habitats. In aquatic environments, the oxygen content plays a key role in bdelloid distribution [50], while in limnoterrestrial habitats, humidity and rainfall are more influential.
Habitats with limited environmental conditions often support low abundance, with only a few species being highly dominant [63]. In the present study, Adineta is a genus with a wide tolerance range [52,64,65,66], thriving under favorable conditions, such as high humidity, and possibly through competition. M. russeola was predominantly found during the wet season, when humidity levels were high. Both Adineta and Rotaria were found at high densities, but surprisingly, the two genera dominated different substrates. Adineta was more abundant on moss on tree trunks, while Rotaria was more abundant on moss on logs. However, it is premature to conclude that these two genera are competing and occupying separate niches. Further research is needed to confirm this observation.
Additionally, the species diversity and density were higher during the wet period compared to the dry period. The species composition between the two periods also showed significant differences. Only one species was found exclusively during the dry period, while others were found either in the wet period or in both periods. These findings suggest that seasonal trends play an important role in the dynamics and distribution of bdelloid rotifers, particularly in terms of abundance and diversity [50]. The higher moisture levels during the wet period likely contribute to these patterns, as previous studies have identified humidity as a key factor influencing bdelloid presence [55,56]. During wet periods, bdelloid populations tend to increase, likely due to the higher moisture availability, as well as increased food resources and optimal conditions for metabolism and reproduction.

5. Conclusions

In summary, our study revealed high bdelloid rotifer species diversity within this primary forest, with the greatest species richness found in moss on tree trunks, where the community structure differed from that of other substrates. Additionally, the species richness and total density of the bdelloid rotifers fluctuated over time, with peak diversity and density during the wet periods. In addition, rainfall and humidity were likely key factors influencing the populations of bdelloid rotifers in this limnoterrestrial habitat in the primary forest.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/d17030171/s1: Table S1: The Bray–Curtis dissimilarity between substrates and periods.

Author Contributions

Conceptualization, S.M. and P.P.; methodology, S.M. and P.P.; formal analysis, P.P., R.J., P.S. and S.M.; investigation, P.P., R.J., P.S. and S.M.; writing—original draft preparation, P.P., R.J., P.S. and S.M.; writing—review and editing, P.P., R.J., P.S. and S.M.; project administration, S.M.; funding acquisition, S.M. and P.P. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Graduate Program Scholarship from The Graduate School, Kasetsart University.

Institutional Review Board Statement

These samplings were conducted in compliance with ethical standards and approved by the Institutional Animal Care and Use Committee, Kasetsart University (approval no. ACKU65-SCI-025, approval date 22 July 2022).

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Acknowledgments

We would like to thank the editor and reviewers for their time and effort in reviewing our manuscript. We sincerely appreciate the valuable comments and suggestions, which have greatly contributed to improving its quality. Charan Maknoi, Head of Ban Rom Klao Botanical Garden under the Royal Initiative, was grateful for providing all facilities for fieldwork. Rachaya Buathong and Natdanai Pan-in were thankful for field sampling assistance. We also acknowledge the facilities provided by Kasetsart University’s Faculty of Science and Department of Zoology.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Sampling site in Phitsanulok Province, Thailand. (A) Ban Rom Klao Phitsanulok Botanical Garden by Royal Initiative; (B–H) representatives of moss on substrates; (B) moss on tree; (C) moss on soil; (D) moss on root; (E) moss on rotting log; (F) moss on rock; (G) moss on log; (H) moss on leaf.
Figure 1. Sampling site in Phitsanulok Province, Thailand. (A) Ban Rom Klao Phitsanulok Botanical Garden by Royal Initiative; (B–H) representatives of moss on substrates; (B) moss on tree; (C) moss on soil; (D) moss on root; (E) moss on rotting log; (F) moss on rock; (G) moss on log; (H) moss on leaf.
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Figure 2. Bayesian phylogenetic tree of bdelloid rotifers in moss and other related species based on 661 bp of the COI dataset. Posterior probability values above 0.80 are presented at each branch. Rectangles on the right show the putative species detected by ABGD, ASAP, bPTP, and GMYC. Square brackets group the samples to refer to their morphological identification. Sequences from Thailand are marked in bold with their moss substrates (MS = soil; ML = log; MRO = root; MT = tree trunk). Sequences downloaded from NCBI are annotated with an accession number. Lecane bulla was used as an outgroup.
Figure 2. Bayesian phylogenetic tree of bdelloid rotifers in moss and other related species based on 661 bp of the COI dataset. Posterior probability values above 0.80 are presented at each branch. Rectangles on the right show the putative species detected by ABGD, ASAP, bPTP, and GMYC. Square brackets group the samples to refer to their morphological identification. Sequences from Thailand are marked in bold with their moss substrates (MS = soil; ML = log; MRO = root; MT = tree trunk). Sequences downloaded from NCBI are annotated with an accession number. Lecane bulla was used as an outgroup.
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Figure 3. New record of bdelloid rotifers in Thailand. Adineta bartosi: (A,B) creeping, lateral view. Adineta tuberculosa (C–E): (C) feeding, dorsal view; (D) creeping, lateral view; (E) head and rostrum. Habrotrocha lata (F–H): (F) creeping, dorsal view; (G) feeding head, dorsal view; (H) foot and spurs, ventral view. Macrotrachela russeola (I–K): (I) creeping, dorsal view; (J) foot and spurs, ventral view; (K) feeding, ventral view. Scale bars: (A–G,I,K) = 50 μm; (H,J) = 10 μm.
Figure 3. New record of bdelloid rotifers in Thailand. Adineta bartosi: (A,B) creeping, lateral view. Adineta tuberculosa (C–E): (C) feeding, dorsal view; (D) creeping, lateral view; (E) head and rostrum. Habrotrocha lata (F–H): (F) creeping, dorsal view; (G) feeding head, dorsal view; (H) foot and spurs, ventral view. Macrotrachela russeola (I–K): (I) creeping, dorsal view; (J) foot and spurs, ventral view; (K) feeding, ventral view. Scale bars: (A–G,I,K) = 50 μm; (H,J) = 10 μm.
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Figure 4. The proportion of each genus (% relative abundance) in all substrates.
Figure 4. The proportion of each genus (% relative abundance) in all substrates.
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Figure 5. Distribution of each genus in difference substrates.
Figure 5. Distribution of each genus in difference substrates.
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Figure 6. The Principal Coordinates Analysis plots show the variation in bdelloid species composition among substrates and seasonal preferences based on Euclidean distance. (A) Substrate preferences; (B) seasonal distribution of bdelloid rotifers. The axes PCoA1 and PCoA2 explain 29.78% and 20.39% of the total variation, respectively.
Figure 6. The Principal Coordinates Analysis plots show the variation in bdelloid species composition among substrates and seasonal preferences based on Euclidean distance. (A) Substrate preferences; (B) seasonal distribution of bdelloid rotifers. The axes PCoA1 and PCoA2 explain 29.78% and 20.39% of the total variation, respectively.
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Figure 7. (A) Species richness of bdelloid rotifer during the study period. (B) Total density of bdelloid rotifer from all substrates during the study period. (C) Species richness of bdelloid rotifer in wet and dry period. (D) Total density of bdelloid rotifer in wet and dry period.
Figure 7. (A) Species richness of bdelloid rotifer during the study period. (B) Total density of bdelloid rotifer from all substrates during the study period. (C) Species richness of bdelloid rotifer in wet and dry period. (D) Total density of bdelloid rotifer in wet and dry period.
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Figure 8. The Canonical Correspondence Analysis shows the correlation between bdelloid rotifers and environmental variables (Monte Carlo test: p = 0.01; Pearson’s Correlation: Axis 1 = 0.86, Axis 2 = 0.53; eigenvalue Axis 1 = 0.644, eigenvalue Axis 2 = 0.147). The black circles represent bdelloid rotifer species and the arrows represent significant environmental variables. The colored squares represent the types of substrates. Species and lines in the same quadrant display a positive correlation, whereas those in the opposite quadrant display a negative correlation.
Figure 8. The Canonical Correspondence Analysis shows the correlation between bdelloid rotifers and environmental variables (Monte Carlo test: p = 0.01; Pearson’s Correlation: Axis 1 = 0.86, Axis 2 = 0.53; eigenvalue Axis 1 = 0.644, eigenvalue Axis 2 = 0.147). The black circles represent bdelloid rotifer species and the arrows represent significant environmental variables. The colored squares represent the types of substrates. Species and lines in the same quadrant display a positive correlation, whereas those in the opposite quadrant display a negative correlation.
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Table 1. List of the specimens from Thailand and other countries used in this study, including GenBank accession numbers and substrates of moss.
Table 1. List of the specimens from Thailand and other countries used in this study, including GenBank accession numbers and substrates of moss.
CodeGenBank Accession NumberSpeciesCountrySubstrates of Moss
SP120_MS Habrotrocha sp.8Thailandsoil
SP123_ML Macrotrachela quadricorniferaThailandlog
SP130_MT Habrotrocha lataThailandtree trunk
SP138_ML Rotaria sordidaThailandlog
SP147_ML Rotaria sordidaThailandlog
SP148_MT Habrotrocha sp.1Thailandtree trunk
SP149_MT Habrotrocha sp.2Thailandtree trunk
SP155_MRO Rotaria sordidaThailandroot
SP157_MRO Mniobia russeolaThailandroot
SP158_MT Mniobia russeolaThailandtree trunk
SP159_MT Mniobia russeolaThailandtree trunk
SP176_MRL Habrotrocha sp.7Thailandrotting log
SP180_MT Habrotrocha sp.1Thailandtree trunk
SP181_MT unidentified speciesThailandtree trunk
SP182_MT Habrotrocha sp.1Thailandtree trunk
SP190_MS Rotaria sordidaThailandsoil
SP191_MS Habrotrocha sp.2Thailandsoil
SP193_MT Rotaria sordidaThailandtree trunk
SP196_MS Rotaria sordidaThailandsoil
SP198_ML Rotaria sordidaThailandlog
SP199_ML Rotaria sordidaThailandlog
SP200_ML Rotaria sordidaThailandlog
SP201_ML Rotaria sordidaThailandlog
SP202_ML Rotaria sordidaThailandlog
SP203_ML Rotaria sordidaThailandlog
SP204_ML Rotaria sordidaThailandlog
SP205_ML Macrotrachela multispinosaThailandlog
SP206_ML Rotaria sordidaThailandlog
SP207_ML Rotaria sordidaThailandlog
SP209_MS Habrotrocha sp.8Thailandsoil
SP210_MS Habrotrocha sp.8Thailandsoil
SP211_MS Habrotrocha sp.8Thailandsoil
M. quadricornifera_EF650621_ITEF650621Macrotrachela quadricorniferaItaly
M. quadricornifera_EF650557_UKEF650557Macrotrachela quadricorniferaUK
M. quadricornifera_EU751278_UKEU751278Macrotrachela quadricorniferaUK
M. quadricornifera_FJ426419_FRFJ426419Macrotrachela quadricorniferaFrance
M. quadricornifera_MH251758MH251758Macrotrachela quadricorniferaSwitzerland
M. quadricornifera_FJ426414_TUFJ426414Macrotrachela quadricorniferaTurkey
M. multispinosa_EF650498_AUEF650498Macrotrachela multispinosaAustralia
M. multispinosa_EU751094_UKEU751094Macrotrachela multispinosaUK
M. multispinosa_EU751089_UKEU751089Macrotrachela multispinosaUK
M. multispinosa_EU751099_UKEU751099Macrotrachela multispinosaUK
M. multispinosa_EF650497_ITEF650497Macrotrachela multispinosaItaly
M. multispinosa_EU751100_UKEU751100Macrotrachela multispinosaUK
R. sordida_DQ656852_ITDQ656852Rotaria sordidaItaly
R. sordida_EF173268_ITEF173268Rotaria sordidaItaly
R. sordida_EF173269_ITEF173269Rotaria sordidaItaly
R. sordida_JQ309635_A783RS1JQ309635Rotaria sordidaUK
R. sordida_DQ656854_CHDQ656854Rotaria sordidaSwitzerland
R. sordida_EU751109_UKEU751109Rotaria sordidaUK
R. sordida_EU076899_TWEU076899Rotaria sordidaTaiwan
R. sordida_EU751110_UKEU751110Rotaria sordidaUK
R. sordida_DQ656855_FRDQ656855Rotaria sordidaFrance
R. sordida_EU751121_TUEU751121Rotaria sordidaTurkey
R. sordida_EU751162_TUEU751162Rotaria sordidaTurkey
Mni. russeola_KM043198_A953KM043198Mniobia russeola-
Mni. russeola_EF650513_ITEF650513Mniobia russeolaItaly
Mni. magna_KM043197_645aKM043197Mniobia magna-
Mni. incrassata_EF650571_ANEF650571Mniobia incrassataAntarctica
Mni. incrassata_EF650573_ANEF650573Mniobia incrassataAntarctica
Mni. incrassata_EF650576_ANEF650576Mniobia incrassataAntarctica
H. elusa_KM043193_HB001KM043193Habrotrocha elusa-
H. elusa_EF650487_UKEF650487Habrotrocha elusaUK
H. ligula_KM043194_HB003KM043194Habrotrocha ligula-
H. constricta_KM043192_HB005KM043192Habrotrocha constricta-
H. bidens_EF650488_UKEF650488Habrotrocha bidensUK
H. antarctica_MF503418_R6MF503418Habrotrocha antarcticaAntarctica
H. antarctica_MF503419_R7MF503419Habrotrocha antarcticaAntarctica
H. antarctica_MF503420_R8MF503420Habrotrocha antarcticaAntarctica
H. lata_MH251808_D05MH251808Habrotrocha lataSwitzerland
H. lata_MH251811_D06MH251811Habrotrocha lataSwitzerland
Lecane bulla_JX216667JX216667Lecane bullaMexico
Table 2. Intra- and interspecific genetic distances of bdelloid rotifers in moss, assessed by the Kimura 2-parameter based on COI dataset. Maximum and minimum values of genetic distance between species are reported in bold. The presence of n/c in the results signifies that the evolutionary distance for this taxa was not measured.
Table 2. Intra- and interspecific genetic distances of bdelloid rotifers in moss, assessed by the Kimura 2-parameter based on COI dataset. Maximum and minimum values of genetic distance between species are reported in bold. The presence of n/c in the results signifies that the evolutionary distance for this taxa was not measured.
TaxaHaplotype NumberWithin TaxaBetween Taxa
12345678910111213141516
1. Mniobia russeola50.15
2. Mniobia magna1n/c0.21
3. Mniobia incrassata20.000.230.24
4. Habrotrocha sp.140.000.230.250.15
5. Macrotrachela multispinosa70.120.250.270.190.15
6. Macrotrachela quadricornifera70.120.240.240.170.140.15
7. Habrotrocha antarctica30.000.230.250.180.160.160.15
8. Habrotrocha elusa20.130.220.260.170.150.160.150.11
9. Habrotrocha lata30.140.220.240.170.160.170.150.150.14
10. Habrotrocha ligula1n/c0.230.260.170.140.170.150.150.130.14
11. Habrotrocha sp.21n/c0.270.290.190.170.190.170.160.170.170.18
12. Habrotrocha sp.71n/c0.240.280.170.120.160.140.140.140.170.160.15
13. Habrotrocha constricta1n/c0.250.290.190.120.160.140.130.150.150.130.160.13
14. Habrotrocha sp.840.030.260.260.190.190.220.170.180.190.180.200.180.160.16
15. Habrotrocha bidens1n/c0.250.260.180.160.190.160.140.160.150.160.180.160.140.16
16. Rotaria sordida250.130.260.280.200.180.200.180.190.180.180.180.200.190.160.210.19
Table 3. Bdelloid species found in moss on each substrate and each period. TT = tree trunk; L = log; S = soil; R = root; RL = rotting log.
Table 3. Bdelloid species found in moss on each substrate and each period. TT = tree trunk; L = log; S = soil; R = root; RL = rotting log.
Bdelloid SpeciesSubstratesPeriods
Adineta bartosi Wulfert 1960 *TTwet
Adineta tuberculosa Janson, 1893 *TTwet, dry
Adineta vaga (Davis, 1873)TTwet, dry
Adineta sp.TTwet
Habrotrocha lata (Bryce, 1892) *TT, Swet, dry
Habrotrocha sp.1TT, L, Swet, dry
Habrotrocha sp.2TT, Swet
Habrotrocha sp.3TT, L, S, RLwet, dry
Habrotrocha sp.4TTwet
Habrotrocha sp.5TTwet, dry
Habrotrocha sp.6TTdry
Habrotrocha sp.7RLwet
Habrotrocha sp.8Swet, dry
Macrotrachela multispinosa Thompson, 1892TT, L, S, RLwet, dry
Macrotrachela quadricornifera Milne, 1886Lwet
Mniobia russeola (Zelinka, 1891) *TT, RLwet
Rotaria sordida (Western, 1893)TT, L, S, R, RLwet, dry
* = new records in Thailand.
Table 4. Species richness and Shannon diversity index of bdelloid species in each substrate and each season. Numbers in brackets represent the mean species richness ± standard deviation (SD).
Table 4. Species richness and Shannon diversity index of bdelloid species in each substrate and each season. Numbers in brackets represent the mean species richness ± standard deviation (SD).
Species RichnessShannon Diversity Index
Substrates
tree trunk14 (1.72 ± 0.83)2.15
log5 (1.43 ± 0.53)1.14
soil7 (1.18 ± 0.40)1.45
root3 (1.50 ± 0.71)1.04
rotting log3 (1.50 ± 0.71)0.99
Seasons
wet period16 (3.86 ± 4.14)2.29
dry period10 (3.50 ± 14.33)1.91
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Pokpongmongkol, P.; Jaturapruek, R.; Sa-ardrit, P.; Maiphae, S. Substrate Preference and Seasonal Distribution of Bdelloid Rotifers in Mosses in a Primary Forest in Thailand. Diversity 2025, 17, 171. https://doi.org/10.3390/d17030171

AMA Style

Pokpongmongkol P, Jaturapruek R, Sa-ardrit P, Maiphae S. Substrate Preference and Seasonal Distribution of Bdelloid Rotifers in Mosses in a Primary Forest in Thailand. Diversity. 2025; 17(3):171. https://doi.org/10.3390/d17030171

Chicago/Turabian Style

Pokpongmongkol, Poomipat, Rapeepan Jaturapruek, Phannee Sa-ardrit, and Supiyanit Maiphae. 2025. "Substrate Preference and Seasonal Distribution of Bdelloid Rotifers in Mosses in a Primary Forest in Thailand" Diversity 17, no. 3: 171. https://doi.org/10.3390/d17030171

APA Style

Pokpongmongkol, P., Jaturapruek, R., Sa-ardrit, P., & Maiphae, S. (2025). Substrate Preference and Seasonal Distribution of Bdelloid Rotifers in Mosses in a Primary Forest in Thailand. Diversity, 17(3), 171. https://doi.org/10.3390/d17030171

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