Biodiversity Data Journal :
Research Article
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Corresponding author: Sujeephon Athibai (sujiat@kku.ac.th)
Academic editor: Spiros Papakostas
Received: 15 May 2023 | Accepted: 07 Aug 2023 | Published: 14 Aug 2023
© 2023 Nattaporn Plangklang, Sujeephon Athibai
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Plangklang N, Athibai S (2023) Viability of zooplankton resting eggs in rice field sediment after pesticide applications. Biodiversity Data Journal 11: e106418. https://doi.org/10.3897/BDJ.11.e106418
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Many herbicide products are commonly used in agricultural areas to prevent and eliminate weeds. Contamination from these toxicants in water might affect aquatic organisms not only in the active stage, but also in the diapause stage. To test the effect of herbicide on the resting eggs of zooplankton, we prepared two rice fields: one field without the application of pesticides (RF−NPA) and one with the application of pesticides (RF−PA) in a sampling year. We conducted a hatching experiment for 30 days. Twenty–four taxa of zooplankton were found. Sixteen species of these were rotifers, seven species were cladocerans and one taxon was an unidentified nauplius copepod. The species richness of zooplankton between RF–NPA (17 taxa) and RF–PA (16 taxa) was close, but species compositions between RF–NPA and RF–PA were different, indicated by the similarity index of 0.545. Lecanidae was the most diverse family of rotifers in both rice fields with nine species, while Chydoridae was the most diverse family of cladocerans (four species). The total abundance of zooplankton of RF−NPA was higher than RF−PA with 1,897 and 1,286 individuals, respectively. The Shannon–Wiener diversity index (H´) and Pielou’s evenness (J) in RF−NPA were higher than in RF−PA. The high species richness of zooplankton in both rice fields occurred on days 18 to 30. On the other hand, the highest abundance was recorded on day 18 for RF−NPA and on day 24 for RF−PA. The non-metric multidimensional scaling (NMDS) demonstrated significant differences in zooplankton community composition between RF–NPA and RF–PA (p < 0.05; ANOSIM test). According to the diversity indices, the RF–NPA has more diversity than the RF–PA, which might be a result of herbicide application in the sampling year. This study suggests that the toxicity of glyphosate should be a concern in terms of the biodiversity of rice field ecosystems.
biodiversity, resting egg, temporary habitat, glyphosate
In Southeast Asian countries such as Thailand, a large number of pesticides (over 198,000 tonnes) have been used in rice cultivation (
Zooplankton have the ability to form resting eggs so they can survive under poor environmental conditions (
The effects of pesticides on hatching resting eggs of zooplankton from sediment have been conducted by applying pesticides directly to sediment under laboratory conditions (
The data underpinning the analysis reported in this paper are deposited at GBIF, the Global Biodiversity Information Facility, https://doi.org/10.15468/w8h9tn.
Sediment samples were collected from two rice fields in Ban Non Lukki, Than Lalot Subdistrict, Phimai District, Nakhon Ratchasima Province, north-eastern Thailand (Fig.
Map of RF–NPA and RF–PA showing ten sampling stations in Than Lalot Subdistrict, Phimai District, Nakhon Ratchasima Province, Thailand. Location maps and sampling stations in satellite view (Google satellite, accessed 30.04.2023), generated from QGIS 3.28.3 (QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.osgeo.org).
In each of the ten sampling stations, approximately 1 kg of wet sediment was collected from each rice field during the reproductive stage of the rice growing season on 14 October 2018. Then sediment samples were kept in a non-transparent plastic bag at 4°C for one month (
All zooplankton samples were identified and counted under an Olympus CH30 compound light microscope. Identification to species level focused on rotifers and cladocerans following the identification keys of
The number of species and abundance of each station were normalised using the Shapiro–Wilk test. Owing to a non–normal distribution in the data (p < 0.05), the non–parametric statistics were required. The number of taxa and abundance of zooplankton between RF−NPA and RF−PA were compared using the Mann−Whitney U test (df = 9). Pearson’s correlation was used to explore the relationship between the distances amongst sampling points and the similarity of zooplankton species in the rice fields. These three statistics were conducted in IBM SPSS Statistics for Windows (version 28.0; IBM Corp., Armonk, NY, USA).
The Sørensen−Dice similarity index (Cs) (
The species accumulation curve (
A total of 24 taxa of zooplankton were found. Sixteen species of these corresponded to rotifers, seven species were cladocerans and one taxon was nauplius of copepods. The species list of zooplankton is shown in Table
Species list of zooplankton and their abundance in RF−NPA and RF−PA amongst five incubation times (−: absent).
Scientific Name |
RF−NPA |
RF−PA |
||||||||
Day 6 |
Day 12 |
Day 18 |
Day 24 |
Day 30 |
Day 6 |
Day 12 |
Day 18 |
Day 24 |
Day 30 |
|
Rotifers |
||||||||||
1. Cephalodella forficula (Ehrenberg, 1830) |
3 |
− |
1 |
− |
− |
− |
− |
− |
− |
− |
2. C. gibba (Ehrenberg, 1830) |
− |
− |
− |
2 |
1 |
− |
2 |
5 |
− |
− |
3. Colurella obtusa (Gosse, 1886) |
− |
1 |
3 |
11 |
1 |
− |
26 |
31 |
9 |
1 |
4. Euchlanis incisa Carlin, 1939 |
− |
− |
− |
− |
− |
− |
− |
1 |
15 |
4 |
5. Lecane arcula Harring, 1914 |
− |
2 |
3 |
1 |
− |
− |
− |
− |
− |
− |
6. L. bulla (Gosse, 1851) |
4 |
81 |
355 |
325 |
172 |
5 |
16 |
4 |
− |
1 |
7. L. closterocerca (Schmarda, 1859) |
3 |
− |
− |
72 |
10 |
− |
163 |
408 |
171 |
16 |
8. L. haliclysta Harring & Myers, 1926 |
− |
− |
− |
− |
− |
− |
− |
− |
2 |
2 |
9. L. hamata (Stokes, 1896) |
7 |
98 |
198 |
164 |
50 |
5 |
74 |
96 |
70 |
4 |
10. L. inopinata Harring & Myers, 1926 |
− |
− |
− |
− |
− |
2 |
− |
− |
− |
− |
11. L. signifera (Jennings, 1896) |
− |
− |
− |
− |
− |
1 |
− |
− |
− |
− |
12. L. tenuiseta Harring, 1914 |
− |
3 |
18 |
23 |
6 |
− |
20 |
38 |
46 |
9 |
13. L. undulata Hauer, 1938 |
− |
− |
− |
− |
− |
− |
− |
− |
3 |
1 |
14. Lepadella patella (Müller, 1773) |
− |
9 |
5 |
5 |
− |
1 |
− |
− |
− |
− |
15. Sinantherina spinosa (Thorpe, 1893) |
− |
− |
− |
1 |
1 |
− |
− |
3 |
− |
− |
16. Testudinella patina (Hermann, 1783) |
− |
− |
2 |
1 |
1 |
− |
− |
− |
− |
− |
Cladocerans |
||||||||||
17. Ephemeroporus barroisi (Richard, 1894) |
− |
− |
9 |
43 |
48 |
− |
− |
− |
− |
− |
18. Ilyocryptus spinifer Herrick, 1882 |
− |
− |
− |
− |
7 |
− |
− |
− |
− |
− |
19. Karualona karua (King, 1853) |
− |
− |
− |
− |
− |
− |
2 |
6 |
8 |
12 |
20. Leberis diaphanus (King, 1853) |
2 |
5 |
5 |
23 |
35 |
− |
− |
− |
1 |
1 |
21. Leydigia ciliata (Gauthier, 1939) |
− |
− |
1 |
1 |
− |
− |
− |
− |
− |
− |
22. Macrothrix triserialis Brady, 1886 |
2 |
5 |
17 |
39 |
11 |
− |
− |
− |
− |
− |
23. Moina micrura Kurz, 1874 |
− |
− |
− |
− |
− |
1 |
− |
− |
− |
− |
Copepods |
||||||||||
24. Nauplius larva |
1 |
− |
− |
− |
− |
− |
− |
− |
− |
− |
Total species richness |
7 |
8 |
12 |
14 |
12 |
6 |
7 |
9 |
9 |
10 |
Total abundance (individuals) |
22 |
204 |
617 |
711 |
343 |
15 |
303 |
592 |
325 |
51 |
Some rotifers (a–f) and cladocerans (g–h) a: Colurella obtusa (Gosse, 1886); b: Lecane bulla (Gosse, 1851); c: Lecane closterocerca (Schmarda, 1859); d: Lecane hamata (Stokes, 1896); e: Lecane signifera (Jennings, 1896); f: Testudinella patina (Hermann, 1783); g: Ephemeroporus barroisi (Richard, 1894) and h: Macrothrix triserialis Brady, 1886.
The species richness of rotifers hatched from the RF−NPA sediment (11 species) was lower than the RF−PA (13 species). Lecanidae with nine species accounting for 56.25% of the total richness of rotifers, was the most diverse family in both rice fields, followed by Lepadellidae and Notommatidae, each with two species. The species richness of cladocerans in the RF−NPA was higher than the RF−PA with five and three species, respectively. The most diverse family was Chydoridae with four species (57.14% of total richness of cladocerans), followed by Ilyocryptidae, Macrothricidae and Moinidae (one species in each family) (Table
The species richness of zooplankton in both rice fields tended to increase over incubation periods (Table
The highest species richness of rotifers in RF−NPA was reported on day 24 with 10 species, whereas the maximum number of species for RF−PA was noted on days 18 and 30 (eight species, each one) (Table
The highest species richness of cladocerans for RF−NPA was recorded on days 18, 24 and 30, with four species each, while the greatest number of species for RF−PA was found on days 24 and 30, with two species each (Fig.
The total number of species per sampling station in RF–NPA ranged from 2–8 species. Eight species have been identified at stations 5 and 7, for the greatest species total (Fig.
The greatest Shannon–Wiener diversity index (H´ = 1.521) and Pielou’s evenness index (J = 0.536) were recorded in RF–NPA (Table
The Shannon–Wiener diversity index (H´) and Pielou's evenness index (J) of zooplankton community from RF–NPA and RF–PA sediments.
Diversity indices |
Rice field |
Incubation time |
Total data |
||||
Day6 |
Day12 |
Day18 |
Day24 |
Day30 |
|||
H´ |
RF–NPA |
1.831 |
1.172 |
1.116 |
1.632 |
1.566 |
1.521 |
RF–PA |
1.542 |
1.289 |
1.040 |
1.370 |
1.845 |
1.339 |
|
J |
RF–NPA |
0.941 |
0.563 |
0.449 |
0.618 |
0.630 |
0.536 |
RF–PA |
0.861 |
0.662 |
0.473 |
0.623 |
0.801 |
0.483 |
According to the species accumulation curves, both rice fields had a similar pattern with an increase in the number of species of hatched zooplankton. However, the steepness of the accumulation curve was initially greater in RF–NPA than in RF–PA, resulting in a higher number of species in RF–NPA (Fig.
The estimation of the number of zooplankton species in RF–NPA and RF–PA revealed that three estimators (Chao1, Jackknife1 and Jackknife2) extrapolated the number of zooplankton taxa in RF–PA greater than that in RF–NPA. On the other hand, bootstrap provided the estimated value for RF–NPA being higher than RF–PA. Jackknife2 revealed the lower estimated number of taxa for RF–NPA (14.24 species) compared to the number of observed taxa (17 species) (Table
Summary of estimates of total species richness (± SE) for RF–NPA and RF–PA.
RF |
Species observed |
Chao1 |
Jackknife1 |
Jackknife2 |
Bootstrap |
RF–NPA |
17 |
17.09 ± 0.38 |
17.98 ± 0.98 |
14.24 |
18.11 ± 0.95 |
RF–PA |
16 |
18.61 ± 3.48 |
19.92 ± 2.40 |
20.94 |
17.96 ± 1.34 |
The highest similarity index for RF–NPA was 0.800 which related to stations 7 and 9, but the lowest value was only 0.154 which corresponded with stations 3 and 5. In RF–PA, the maximum value of the similarity index (0.889) was recorded from stations 4 and 6, while the minimum value (0.182) was from stations 7 and 8 (Suppl. material
The total number of zooplankton in RF−NPA was higher than in RF−PA with 1,897 and 1,286 individuals, respectively. The total abundance of rotifers in RF–NPA was significantly greater than that in RF–PA (Z = –2.228, p = 0.026) only on day 30 with 34.57 ± 17.18 and 5.14 ± 2.81 individuals, respectively (Fig.
For cladocerans, the total number of individuals in RF−NPA on days 24 and 30, with 26.50 ± 12.23 and 25.25 ± 16.76 individuals, respectively, were significantly higher than RF−PA, which had 4.50 ± 4.94 and 6.50 ± 7.78 individuals, respectively (Z = –2.141, p = 0.032 for day 24; Z = –2.121, p = 0.034 for day 30) (Fig.
Zooplankton abundance in RF–NPA ranged between 1 and 209 individuals. Station 2 revealed the greatest abundance of zooplankton, with 209 individuals (Fig.
The NMDS analysis demonstrated distinct groupings and the dissimilarity between RF–NPA and RF–PA zooplankton communities, indicated by ANOSIM test results with the R statistic value and the corresponding significance level (p–value) (Fig.
The hatching of zooplankton resting eggs plays an important contribution to zooplankton diversity in rice fields. The existence of zooplankton communities not only comes from irrigation canals, but also from hatching of resting eggs remaining within rice fields (
The diversity and abundance of resting egg zooplankton collected from a rice field with pesticide application (RF–PA) in comparison to a non-treated pesticide rice field (RF–NPA) were conducted in the present study, based on incubation sediment for one month. The number of hatched zooplankton taxa in RF–NPA (17 taxa) and RF–PA (16 taxa) was close, whereas species composition between two water bodies is different (54.50% of the similarity). This was also supported by the NMDS ordinations, which revealed the significant differences in zooplankton composition between RF–NPA and RF–PA. The ordinations performed with a stress values range of 0.06 – 0.16, which were in the “good” to “usable picture” criteria range (
The zooplankton resting egg bank in RF–NPA and RF–PA demonstrates 25.80% and 25.50% similarity to active zooplankton in the water body itself which has been reported by
Chlorpyrifos and glyphosate have been used in both RF–NPA and RF–PA for at least ten years. The half-lives of chlorpyrifos and glyphosate in fields vary from a few days to several months, the mean half-lives of chlorpyrifos and glyphosate in sediment being 38 and 47 days, respectively (
Although there were no significant differences in numbers of taxa of hatched zooplankton between RF–NPA and RF–PA, differences in the species composition and abundance of hatched zooplankton between both rice fields were found.
The abundance of zooplankton between RF−NPA and RF−PA is different. Both rotifers and cladocerans in RF−NPA appeared higher in abundance in comparison to RF−PA, especially the number of individuals of cladocerans from the RF−PA sediment which showed less abundance throughout five incubation times. It seems likely that glyphosate applications might be a causative factor that disrupts resting egg production and the dormancy in resting eggs of some zooplankton in rice fields. This evidence is from the abundance of rotifers and cladocerans in RF–PA, with cladocerans having a lower number of individuals than rotifers. This result indicated that cladocerans were more sensitive to glyphosate than rotifers.
The number of individuals of L. bulla and L. hamata in RF−PA were low compared to RF–NPA. It seems that these two rotifers suffer from glyphosate application. Although there was no evidence on the sensitivity of L. bulla and L. hamata to glyphosate, L. bulla and L. hamata have been reported as the most sensitive to copper (Cu) and lead (Pb) (
Only one nauplius of copepod was found in RF−NPA sediment at the first incubation time (day 6), but it was not present in RF−PA. Although there is no evidence of resting egg production of eight diaptomids and three cyclopoid copepods which are recorded in the report of
Lecane was the most diverse genus of rotifers with nine species, accounting for 56.25% of the total richness of rotifers. The high diversity of Lecane confirms that all recorded lecanid species are widely distributed in the tropical region. L. bulla, L. closterocerca, L. hamata and L. tenuiseta are cosmopolitan, whereas L. arcula, L. haliclysta, L. inopinata, L. signifera and L. undulata exhibit as tropicopolitan species (
M. micrura was found only on day 6 of the RF−PA sediment. Our findings agree with the results of
Since zooplankton were sampled every six days, rotifers and cladocerans can reproduce during incubation. Therefore, the abundance was probably from both the egg bank and reproduction due to long sampling intervals over 3 days (
In our work, we have increased knowledge of the diversity of zooplankton hatching from different rice field sediments. We found that, although the number of taxa of zooplankton between RF−NPA and RF−PA was close, species compositions of zooplankton were different, indicated by the Sørensen–Dice index and NMDS result. RF–NPA also had a higher species diversity index and evenness index than RF–PA. In addition, the incubation time potentially influenced species richness and abundance of zooplankton. The highest species richness and abundance of zooplankton in RF–NPA occurred on day 24. However, some zooplankton species were found only on day 6, such as M. micrura for RF–PA and nauplius of copepods for RF–NPA. In RF−PA, L. bulla and L. hamata had a low number of individuals; moreover, Le. diaphanus appeared with delayed hatching. Our results indicate that RF−NPA has more diversity than the RF−PA, according to the diversity indices which might be the effect of herbicide application in the sampling year. We also suggest that the hatching of resting eggs is a potential method for the study of zooplankton diversity in temporary habitats.
This research was funded by Research and Graduate Studies Khon Kaen University and the Human Resource Development in Science Project (Science Achievement Scholarship of Thailand, SAST). Sincere thanks go to the referees for their insightful criticisms and suggestions. The authors thank Dr. Benjamart Suksai and Preeyanat Jantra for assistance in the field.
The study was reviewed and approved by the Institutional Animal Care and Use Committee of Khon Kaen University, Thailand (No. IACUC-KKU-42/61).
Diversity indices and species richness of zooplankton amongst ten sampling stations of RF–NPA and RF–PA.
Similarity index of zooplankton between sampling stations within rice fields.