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Article

Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant

by
Yu Jin
1,2,†,
Jin-Song Chen
2,†,
Fang-Li Luo
3,
Lin Huang
1,*,
Ning-Fei Lei
4 and
Fei-Hai Yu
1,*
1
Institute of Wetland Ecology & Clone Ecology/Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou 318000, China
2
College of Life Science, Sichuan Normal University, Chengdu 610101, China
3
School of Ecology and Conservation, Beijing Forestry University, Beijing 318000, China
4
College of Ecology and Environment, Chengdu University of Technology, Chengdu 610059, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Diversity 2022, 14(8), 616; https://doi.org/10.3390/d14080616
Submission received: 19 June 2022 / Revised: 27 July 2022 / Accepted: 28 July 2022 / Published: 30 July 2022
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Abstract

:
Phenotypic variation of individuals within populations can be influenced by not only genetic diversity and environmental variation experienced by these individuals but also environmental variation experienced by their parents. Although many studies have tested impacts of phenotypic diversity caused by genotypic or species diversity on productivity, no study has assessed the effects of phenotypic diversity induced by parental environmental variation on productivity. To address this novel question, we conducted two experiments with the widespread, fast-growing, clonal, floating plant Spirodela polyrhiza. We first grew mother (ancestor) ramets of S. polyrhiza under different environmental conditions to obtain descendent ramets with different phenotypes. Then, these ramets were used to construct descendent populations with different levels of phenotypic diversity caused by ancestor environmental variation and examined the effect of phenotypic diversity on population productivity. Environmental variation (changes in nutrient availability, plant density and light intensity) had significant effects on descendent populations of S. polyrhiza. However, descendent phenotypic diversity induced by ancestor environmental variation had no significant effect on total biomass or number of ramets of the descendent populations and such an effect did not depend on the nutrient availability that the descendent populations experienced. Although our results failed to support the idea that phenotypic diversity induced by ancestor environment variation can influence descendent population productivity, we propose that this novel idea should be tested with more species in different ecosystems.

1. Introduction

Biodiversity plays an important role in maintaining ecosystem functions, such as productivity of plant communities or populations [1,2,3,4,5,6,7,8]. Previous studies have frequently shown that communities with higher species diversity or populations with higher genotypic diversity can result in higher productivity [8,9]. This is because species-richer communities or genotype-richer populations can make better use of available resources due to complementarity among species or genotypes or have a higher chance to possess competitively superior species or genotypes [8,9,10].
One potential mechanism underlying such a complementarity or sampling effect of biodiversity is that different species or genotypes possess phenotypes with different functional traits that have a close link with complementary resource use, niche differentiation or competitive dominance [11,12,13,14]. In other words, the effects of species diversity or genotypic diversity on productivity are indirectly mediated through the effects of phenotypic diversity caused by species or genotypic diversity [15,16,17]. In the past, the effects of phenotypic diversity mediated by species diversity and genotypic diversity on productivity has been extensively documented. However, to our knowledge, very few studies have tested the effects of phenotypic diversity mediated by environmental variation on productivity.
Similar to the effects of species diversity or genotypic diversity, we hypothesize that, if environmental variation can result in different phenotypes with different resource use strategies, niche occupation or competitive dominance, then phenotypic diversity of individuals within a population may influence its productivity via the complementarity effect of these phenotypes or the sampling effect of some competitively superior phenotypes. However, if the phenotypic differences caused by environmental variation are not large enough, then phenotypic diversity mediated by environmental variation may not influence population productivity.
Increasing studies have proven that not only are the current environmental conditions experienced by an individual but also the environmental conditions, experienced by its parent(s), can influence the phenotype of the individual [18,19,20,21,22,23,24,25,26,27]. Therefore, parental (environmental) effects may affect phenotypic diversity of plant populations and further influence their structure, dynamics and evolutionary direction [18,28,29,30,31]. Although a large number of studies have examined parental effects on plant performance [23,32,33,34,35,36,37], very few studies have addressed whether phenotypic diversity mediated by parental environmental variation influences ecosystem function, such as population productivity.
In this study, mother (ancestor) ramets of a clonal plant Spirodela polyrhiza were grown under different environmental conditions to obtain descendent ramets with different phenotypes. Then, the descendent ramets with different levels of phenotypic variation, mediated by ancestor environmental variation, were used to construct plant populations with different phenotypic diversity and the effects of phenotypic diversity on population productivity were examined. Specifically, we explored (1) whether nutrient availability, light availability and population density affect the performance (i.e., total biomass, number of ramets and mass per ramet) of S. polyrhiza, and (2) whether phenotypic diversity mediated by ancestor environmental variation affects its descendent population productivity.

2. Materials and Methods

2.1. Study Species and Material Preparation

Spirodela polyrhiza (L.) Schleiden (Lemnaceae) typically inhabits slow-moving streams, shallow pools and ditches [38,39,40,41] and can regenerate quickly by clonal growth, and number of vegetative individuals (ramets) can be doubled within only a few days (e.g., 1–2 days) [42,43,44,45]. Each ramet often consists of one or two leaves (commonly called “fronds”) and some roots. Offspring ramets are connected to their parent ramets by a stipe at the early stage of development and become independent after the breakage of the stipe due to aging or disturbance [46].
Ramets of S. polyrhiza were collected from a slow-moving stream in Taizhou (28°3′ N, 121°21′ E), Zhejiang Province, China. The plants were brought to a greenhouse at Taizhou University and rinsed with 0.01 M NaClO for 30 s after being cleaned with the distilled water [45,47]. Then, they were propagated vegetatively in 10% Hoagland solution in the greenhouse [48]. After five days of cultivation, we transferred a newly produced ramet into a different container, and offspring ramets vegetatively propagated from this mother ramet were used for the two experiments described below.

2.2. Experimental Design

Experiment 1: In the first phase, mother (ancestor) ramets of S. polyrhiza, each with two leaves and some roots, were randomly subjected to four levels of nutrient availability, i.e., 1/32, 1/2, 1 and 2 times of the concentration of the standard Hoagland solution (Figure S1). The nutrient levels were set according to our previous findings which showed significant phenotypic variation of descendent ramets of S. polyrhiza in response to these nutrient levels [49]. We grew eight ancestor ramets in each pot (17.5 cm in diameter and 10.5 cm in height) containing 1.2 L nutrient solution. Each treatment had 12 replicates (pots), and there were 48 pots in total. All pots were randomly placed on a bench in the greenhouse.
The treatments lasted for 15 days from 26 May to 10 June 2020. The nutrient solution in each pot was replaced at the middle of the experiment. During this period, the mean air temperature and mean relative humidity were 28.2 °C and 82.8%, respectively (iButton DS1923; Maxim Integrated Products, Sunnyvale, CA, USA). At harvest, the ramets in the two high nutrient levels (i.e., 1 and 2 times of Hoagland solution) had fully covered the water surface. The descendent ramets from the four nutrient treatments, i.e., with four different phenotypes, were used for the second phase of the experiment.
In the second phase, the descendent ramets of S. polyrhiza originated from ancestor ramets of the first phase were used to construct populations with four levels of phenotypic diversity (mediated by ancestor environmental variation), i.e., consisting of descendent ramets of one, two, three and four phenotypes (Figure S1). For the monoculture treatment, each population originally consisted of 12 descendent ramets of the same phenotype (ancestor ramets subjected to the same nutrient treatment, as shown in Figure 1. The monocultures of each of the four phenotypes were constructed with eight replicates, resulting in 32 pots. For the population consisting of descendent ramets of two phenotypes (2-phenotype mixtures), there were six phenotype combinations and each combination was replicated four times. Thus, there were 24 pots for the 2-phenotype mixtures and each pot contained six descendent ramets of each of the two phenotypes (12 descendent ramets per pot). For the population consisting of descendent ramets of three offspring phenotypes (3-phenotype mixtures), there were only four phenotype combinations and each combination was replicated four times. Thus, there were 16 pots for the 3-phenotype mixtures, and each pot contained four descendent ramets of each of the three phenotypes (12 descendent ramets per pot). For the population consisted of descendent ramets of four phenotypes (4-phenotype mixtures), there was only one phenotype combination and the combination was replicated 12 times. Thus, there were 24 pots for the 4-phenotype mixtures and each pot contained three descendent ramets of each of the four phenotypes (12 descendent ramets per pot).
For each level of phenotypic diversity, half of the replicates were subjected to a low nutrient treatment (1/32 times of Hoagland solution) and the other half to a high nutrient treatment (1/2 times of Hoagland solution). Each population was grown under the same setting as described in the previous section. The treatments lasted for 12 days, from 10 June to 22 June 2020. At harvest, plants in all containers had fully covered the water surface. The nutrient solutions in all pots were replaced once at the middle of the treatments. All pots were randomly positioned on a bench in the greenhouse. During the treatments, the mean air temperature and mean relative humidity were 27.8 °C and 82.0%, respectively.
Experiment 2: In the first phase, ancestor ramets of S. polyrhiza, each with two leaves and some roots, were randomly subjected to two levels of initial density (low vs. high: 4 vs. 36 ramets per pot), four levels of nutrient availability (1/32, 1/2, 1 and 2 times of the standard Hoagland solution) and two levels of light intensity (low vs. high: 20% vs. 100% of light intensity in the greenhouse) in a factorial design, making a total of 16 treatments. Ramets were grown under the same setting as described above. Each high-density treatment was replicated 6 times and each low-density treatment 18 times. The low-density treatments had more replicates to ensure sufficient descendent ramets for the second phase of the experiment. High light intensity was the natural sunlight in the greenhouse and low light intensity was realized by covering the plants with a black shading net.
The pots were randomly placed on a bench in the greenhouse. The treatments lasted for 25 days, from 4 June to 29 June 2020. The nutrient solution in each pot was replaced every eight days. During the treatments, the mean air temperature and mean relative humidity were 27.9 °C and 82.1%, respectively. At harvest, descendent ramets in the high-density treatments and the high-light treatments had fully covered the water surface. The descendent ramets from the 16 treatments, i.e., with 16 different phenotypes, were used for the second phase of the experiment.
In the second phase, we constructed S. polyrhiza populations consisting of 1, 3, 6, 9 and 12 phenotypes that were originated from the ancestor ramets in the first phase. For the monoculture treatment, there were 3 replicates (pots) for each of the 16 phenotypes, resulting in 48 pots. For the 3-, 6-, 9- and 12-phenotype mixtures, 16 different combinations were randomly selected in the way that each phenotype had equal chance to be selected. Each population consisted of 36 offspring ramets and was kept in a pot (23.5 cm in diameter and 5.5 cm in height) containing 1.5 L of the standard Hoagland solution. All pots were under the nature sunlight of light intensity in the greenhouse. The treatments lasted for 14 days, from 29 June to 13 July 2020. At harvest, plants in all pots had fully covered the water surface. The nutrient solutions were replaced at the middle of the treatments. During the treatments, the mean air temperature and mean relative humidity were 28.4 °C and 83.2%, respectively. The pots were randomly arranged on a bench in the greenhouse.

2.3. Measurements

At harvest, we counted number of descendent ramets of S. polyrhiza in each pot. Then, descendent ramets from each pot were oven-dried at 70 °C for 48 h and weighed. Dry mass per ramet was calculated.

2.4. Data Analyses

For the first phase of Experiment 1, all data were transformed to logarithm before analyses. Then, one-way ANOVA was used to test the effects of nutrient availability on total mass, number of ramets and mass per ramet of the descendent ramets. For the second phase of Experiment 1, data on total mass and number of ramets were, respectively, transformed to square root and logarithm before analyses. A linear mixed model was used to investigate the effects of descendent phenotypic diversity and nutrient availability on total mass and number of ramets of S. polyrhiza. In this model, phenotypic composition was included as a random factor nested within phenotypic diversity.
For the first phase of Experiment 2, data on number of ramets and mass per ramet were log-transformed before analyses. Then, three-way ANOVA was used to test the effects of nutrient availability, population density and light intensity on total mass, number of ramets and mass per ramet of the descendent plants. For the second phase of Experiment 2, all data were log-transformed before analyses. A linear mixed model was used to investigate the effect of descendent phenotypic diversity on total mass and number of ramets of S. polyrhiza. Statistical analyses were carried out with SPSS 22.0 (IBM Corp., Armonk, NY, USA).

3. Results

3.1. Growth Performance in Experiment 1

For the first phase, nutrient availability significantly affected total mass (p < 0.001) and number of ramets (p < 0.001) of the descendent populations of S. polyrhiza (Figure 1A,B). Total mass and number of ramets of S. polyrhiza increased with increasing nutrient level, reached the highest value at 1 × Hoagland solution, and then decreased at 2 × Hoagland solution (Figure 1A,B). Nutrient availability also significantly affected the size of the descendent ramet, indicated by mass per descendent ramet (p < 0.001, Figure 1C). Ramet size was the highest in 1/2 × Hoagland solution, became smaller in 1/32 and 1 × Hoagland solution, and was the lowest in 2 × Hoagland solution (Figure 1C).
For the second phase, nutrient availability had significant effects on total mass and number of ramets of S. polyrhiza (Table 1; Figure 2). Across the phenotypic diversity treatments, total mass and number of ramets of S. polyrhiza were higher under high nutrient availability than under low nutrient availability (Figure 2). Descendent phenotypic diversity or its interaction with nutrient availability had no significant effect on total mass and number of ramets (Table 1; Figure 2).

3.2. Growth Performance in Experiment 2

For the first phase, total mass, number of ramets and mass per ramet varied under different levels of nutrient availability, light intensity and population density, as indicated by the significant main/or effects and the two-way and the three-way interaction effects (Table 2; Figure 3). For the second phase, descendent phenotypic diversity mediated by parent environmental variation had no significant effects on total mass (p = 0.383) or number of ramets (p = 0.773) of the S. polyrhiza (Figure 4).

4. Discussion

Nutrient availability greatly affected the growth of the S. polyrhiza populations. Total mass and number of ramets of S. polyrhiza showed an initial increase, followed by a decrease over a nutrient concentration range, agreeing with the response of other aquatic plants [50,51]. Nutrient, as an essential resource for plant growth, is correlated with the biomass accumulation of plants [52,53,54]. Under the low nutrient level, plants grew slowly due to lack of nutrients, whereas under the extremely high nutrient level, the plant growth may be inhibited due to NH4+ toxicity or algal growth [51,55,56]. Therefore, the extreme high nutrient level may not be conducive to the growth of the floating plants.
Nutrient availability also influenced the size of the descendent ramets (Figure 1C), suggesting that nutrient availability can result in differences in the phenotypes of the descendent ramets. When the nutrient level was higher than 1/2 times of the standard Hoagland solution, mass per ramet declined with the increase in nutrient level, which is likely because of a trade-off between ramet mass and number, as commonly reported in clonal plants [57,58]. Rapid asexual propagation in a short time can be a competitive advantage of S. polyrhiza populations to adapt to the environment [59,60].
The effect of nutrient availability on total mass, number of ramets and mass per ramet of the S. polyrhiza populations varied with diffident levels of initial population density and light intensity. Under low density, total mass and number of ramets under low light intensity were rather low among all nutrient levels. Under high density, the nutrient saturation for the number of ramets happened earlier under low light intensity than high light intensity. The results suggest that light intensity played an important role in regulation of the responses of S. polyrhiza populations to nutrient utilization. Before nitrogen saturation, higher light intensity was beneficial to biomass accumulation of both individual ramets (i.e., mass per ramet) and populations. After nutrient saturation, higher light was beneficial to biomass accumulation and ramet production of populations. This finding is in agreement with the previous studies on other aquatic clonal plants [51]. For instance, under higher light intensity, the response of total mass and ramet number of Salvinia natans populations showed a unimodal pattern in response to increasing nutrient availability [51]. However, in our study, with higher nutrient levels, mass per ramet was greater under low than high light intensity. This is likely because the floating clonal plant S. polyrhiza can accumulate more starch grains to survive in unfavorable environmental conditions [38,41,61]. Changes in mass per ramet in response to nutrient availability, population density and light intensity also indicate the occurrence of environment-induced phenotypic variation of the descendent ramets.
It is well known that environmental conditions experienced by parent plants can influence the phenotype and performance of their offspring [29,62,63,64]. For instance, offspring of Plantago lanceolata had higher biomass production and root carbohydrate storage when parental and offspring plants were grown under the same nutrient conditions than when they were grown under different nutrient conditions [33]. When parental plants of Polygonum persicaria were grown under high light conditions, their offspring plants had larger total leaf area than those whose when parents grown under low light conditions [65]. When both grandparental and parental generations were grown under low plant density, the offspring population of S. polyrhiza had higher biomass accumulation, compared with that when only the parental generation was grown under low plant density. Thus, within-species phenotypic variation induced by environmental variation experienced by parental plants can potentially influence productivity of offspring populations.
Unfortunately, however, we found that descendent phenotypic diversity mediated by ancestor environmental variation had a significant effect on neither biomass nor the number of ramets of the S. polyrhiza populations. This phenomenon was also independent of the nutrient conditions of the environments that offspring were experienced. No impact of phenotypic diversity mediated by parental/ancestor environmental variation on population productivity could be due to two potential reasons. One likely reason is that in the present study phenotypic variation of the descendent ramets of S. polyrhiza is not sufficiently large to result in a significant effect of phenotypic diversity on productivity. We did observe significant changes in phenotypic traits of the descendent ramets in response to nutrient availability, population density and light intensity (Figure 1C and Figure 3C). However, these phenotypic changes may be much smaller compared to those mediated by genetic or species variation and thus insufficient to result in significant differences in resource use strategies, niche differentiations or competitive dominances among the descendent ramets. Consequently, descendent phenotypic diversity of S. polyrhiza induced by ancestor environmental variation could not result in a significant complementarity or sampling effect, which could increase its population productivity.
Another likely reason could be due to the homogenized conditions of aquatic environments. Our experiments used nutrient solution as the growth media and the tiny floating species as the model plant. Compared with diverse terrestrial environments that are diverse and frequently allow a large number of plant species and genotypes to coexist, aquatic environments are much more similar and are commonly monopolized by only a few plant species [41,42]. Thus, unlike terrestrial environments that can provide more niches for plants to coexist, the aquatic environment (nutrient solution) in our study may not provide enough niches to allow complementarity among different phenotypes of S. polyrhiza. As a result, the descendent phenotypic diversity of S. polyrhiza induced by ancestor environmental variation could not increase its population productivity.
In summary, we tested, with a single clone of a duckweed, the novel hypothesis that offspring phenotypic diversity mediated by environmental variation of parent plants can increase population productivity. However, our findings failed to support this hypothesis likely due to the insufficient environment-mediated phenotypic variation and the simple aquatic environments. We propose that future studies could be conducted in terrestrial environments with land plants to facilitate a potential positive effect of environment-mediated phenotypic diversity on population productivity. Moreover, relative long-term experiments should be considered since some epigenetic changes might take generations to occur or stabilize [24].

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d14080616/s1, Figure S1: The schematic representation of the design of Experiment 1. In the first phase, ancestor ramets of Spirodela polyrhiza produced the descendent ramets under four levels of nutrient availability. In the second phase, the descendent ramets were used to construct populations with four levels of phenotypic diversity and were grown under either low or high nutrient availability.

Author Contributions

Conceptualization, Y.J., J.-S.C. and F.-H.Y.; data curation, Y.J. and N.-F.L.; formal analysis, Y.J. and L.H.; writing—original draft preparation, Y.J.; writing—review and editing, F.-L.L., L.H. and F.-H.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by NSFC, grant number 32071527 and 32071525.

Institutional Review Board Statement

No applicable.

Data Availability Statement

Data are available on request.

Conflicts of Interest

The authors declare no conflict of interest.

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Diversity 14 00616 g001 550
Figure 1. Total mass (A) number of ramets (B) and mass per ramet (C) of Spirodela polyrhiza in response to different nutrient availability for the first phase of Experiment 1. The values are means and standard errors. Different letters indicate significant differences.
Figure 1. Total mass (A) number of ramets (B) and mass per ramet (C) of Spirodela polyrhiza in response to different nutrient availability for the first phase of Experiment 1. The values are means and standard errors. Different letters indicate significant differences.
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Diversity 14 00616 g002 550
Figure 2. Total mass (A) and number of ramets (B) of Spirodela polyrhiza in response to different descendent phenotypic diversity caused by ancestor environmental variation and nutrient availability for the second phase of Experiment 1. The values are means and standard errors. Different letters indicate significant differences among treatments. See Table 1 for ANOVA results.
Figure 2. Total mass (A) and number of ramets (B) of Spirodela polyrhiza in response to different descendent phenotypic diversity caused by ancestor environmental variation and nutrient availability for the second phase of Experiment 1. The values are means and standard errors. Different letters indicate significant differences among treatments. See Table 1 for ANOVA results.
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Diversity 14 00616 g003 550
Figure 3. Total mass (A), number of ramets (B) and mass per ramet (C) of Spirodela polyrhiza in response to nutrient availability, initial density and light intensity for the first phase of Experiment 2. The values are means and standard errors. Different letters indicate significant differences among treatments. See Table 2 for ANOVA results.
Figure 3. Total mass (A), number of ramets (B) and mass per ramet (C) of Spirodela polyrhiza in response to nutrient availability, initial density and light intensity for the first phase of Experiment 2. The values are means and standard errors. Different letters indicate significant differences among treatments. See Table 2 for ANOVA results.
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Diversity 14 00616 g004 550
Figure 4. Total mass (A) and number of ramets (B) of Spirodela polyrhiza in response to different descendent phenotypic diversity mediated by ancestor environmental variation for the second phase of Experiment 2. The values are means and standard errors.
Figure 4. Total mass (A) and number of ramets (B) of Spirodela polyrhiza in response to different descendent phenotypic diversity mediated by ancestor environmental variation for the second phase of Experiment 2. The values are means and standard errors.
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Table
Table 1. Effects of nutrient availability and phenotypic diversity on total mass and number of ramets of the populations of Spirodela polyrhiza for the second phase of Experiment 1.
Table 1. Effects of nutrient availability and phenotypic diversity on total mass and number of ramets of the populations of Spirodela polyrhiza for the second phase of Experiment 1.
EffectdfTotal MassNo. of Ramets
Nutrient availability (N)1, 77544.8 ***422.3 ***
Phenotypic diversity (D)3, 110.2 ns0.4 ns
N × D3, 770.5 ns1.0 ns
The given are F, degree of freedom (df) and significance levels: ns p > 0.05; *** p < 0.001.
Table
Table 2. Effects of nutrient availability, initial density and light intensity on total mass, number of ramets and mass per ramet of Spirodela polyrhiza for the first phase of Experiment 2.
Table 2. Effects of nutrient availability, initial density and light intensity on total mass, number of ramets and mass per ramet of Spirodela polyrhiza for the first phase of Experiment 2.
EffectdfTotal MassNo. of RametsMass per Ramet
Nutrient availability (N)3, 176394.5 ***94.1 ***108.8 ***
Initial density (D)1, 1761035.8 ***1670.1 ***8.9 **
Light intensity (L)1, 1763588.9 ***3300.8 ***1.5 ns
N × D3, 1769.5 ***5.3 **0.7 ns
N × L3, 176212.3 ***20.0 ***33.0 ***
D × L1, 17698.4 ***284.6 ***1.5 ns
N × D × L3, 1762.5 ns8.5 ***3.3 *
The given are F, degree of freedom (df) and significance levels: ns p > 0.05; * p = 0.01–0.05; ** p < 0.01; *** p < 0.001.
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Jin, Y.; Chen, J.-S.; Luo, F.-L.; Huang, L.; Lei, N.-F.; Yu, F.-H. Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant. Diversity 2022, 14, 616. https://doi.org/10.3390/d14080616

AMA Style

Jin Y, Chen J-S, Luo F-L, Huang L, Lei N-F, Yu F-H. Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant. Diversity. 2022; 14(8):616. https://doi.org/10.3390/d14080616

Chicago/Turabian Style

Jin, Yu, Jin-Song Chen, Fang-Li Luo, Lin Huang, Ning-Fei Lei, and Fei-Hai Yu. 2022. "Effects of Descendent Phenotypic Diversity Mediated by Ancestor Environmental Variation on Population Productivity of a Clonal Plant" Diversity 14, no. 8: 616. https://doi.org/10.3390/d14080616

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