Abstract
Various types of pollutants derived from rapid industrialization and urbanization have largely threaten biodiversity and functioning of freshwater ecosystems globally. Morphological plasticity, especially body size–associated traits, is considered a functional response to water pollution in species, as such changes are often directly related to functioning of freshwater ecosystems through dynamics of food webs. However, detailed dynamics of pollution impacts on morphological plasticity remain largely unknown, particularly in the wild. Here, we used the model planktonic rotifer Brachionus calyciflorus to assess morphological response to chemical pollution in a river reach disturbed by sewage discharges. Multiple analyses showed dynamic morphological response to water pollution in wild B. calyciflorus populations. The distance between anterior lateral spines, lorica length, and egg short diameter were the most sensitive morphological indicators to water pollution, while spine length was stable in varied pollution conditions. Interestingly, body size and egg size were increased with accentuated water pollution, suggesting that wild populations maintain fitness by increasing feeding efficiency and reducing vulnerability to predation and ensure survival by producing large newborns in polluted environments. Total ammonia nitrogen was the leading nitrogen pollutant affecting body size, while total phosphorus and elements of Mn and As were the key factors relating to egg size. The results obtained here provide new sights into biological consequences of environmental pollution in the wild, thus advancing our understanding of pollution impacts on structure and functioning of freshwater ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
All data generated or analyzed during this study are included in this published article and its supplementary information file.
References
Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36(2):216–236. https://doi.org/10.1093/icb/36.2.216
Bogdan KG, Gilbert JJ (1984) Body size and food size in freshwater zooplankton. Proc Natl Acad Sci 81(20):6427–6431. https://doi.org/10.1073/pnas.81.20.6427
Bolnick DI, Amarasekare P, Araújo MS et al (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26(4):183–192. https://doi.org/10.1016/j.tree.2011.01.009
Boukal DS (2014) Trait- and size-based descriptions of trophic links in freshwater food webs: current status and perspectives. J Limnol 73(S1):171–185. https://doi.org/10.4081/jlimnol.2014.826
Brooks JL, Dodson SI (1965) Predation, body size, and composition of plankton. Science 150(3692):28–35. https://doi.org/10.1126/science.150.3692.28
Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85(7):1771–1789. https://doi.org/10.1890/03-9000
Calow P (1991) Physiological costs of combating chemical toxicants: ecological implications. Comp Biochem Physiol C Comp Pharmacol Toxicol 100(1-2):3–6. https://doi.org/10.1016/0742-8413(91)90110-F
Ciros-Pérez J, Gomez A, Serra M (2001) On the taxonomy of three sympatric sibling species of the Brachionus plicatilis (rotifera) complex from Spain with the description of B. ibericus n. sp. J Plankton Res 23:1311–1328. https://doi.org/10.1093/plankt/23.12.1311
Conde-Porcuna JM, Morales-Baquero R, Cruz-Pizarro L (1993) Effectiveness of the caudal spine as a defense mechanism in Keratella cochlearis. Hydrobiologia 255-256(1):283–287. https://doi.org/10.1007/BF00025850
Dalu T, Cuthbert RN, Taylor JC, Magoro ML, Weyl OLF, Froneman PW, Wasserman RJ (2020) Benthic diatom-based indices and isotopic biomonitoring of nitrogen pollution in a warm temperate Austral river system. Sci Total Environ 748:142452. https://doi.org/10.1016/j.scitotenv.2020.142452
Declerck SA, Papakostas S (2017) Monogonont rotifers as model systems for the study of micro-evolutionary adaptation and its eco-evolutionary implications. Hydrobiologia 796(1):131–144. https://doi.org/10.1007/s10750-016-2782-y
Dias JD, Bonecker CC, Miracle MR (2014) The rotifer community and its functional role in lakes of a neotropical floodplain. Int Rev Hydrobiol 99(1-2):72–83. https://doi.org/10.1002/iroh.201301706
Díaz S, Settele J, Brondízio ES, Ngo HT, Agard J, Arneth A, Balvanera P, Brauman KA, Butchart SHM, Chan KMA, Garibaldi LA, Ichii K, Liu J, Subramanian SM, Midgley GF, Miloslavich P, Molnár Z, Obura D, Pfaff A et al (2019) Pervasive human-driven decline of life on Earth points to the need for transformative change. Science 366(6471):eaax3100
Duncan A (1983) The composition, density and distribution of the zooplankton in Parakrama Samudra. Limnology of Parakrama Samudra-Sri Lanka. Springer, Netherlands. https://doi.org/10.1007/978-94-009-7281-0_7
Dusabe MC, Wronski T, Gomes-Sliva G et al (2019) Biological water quality assessment in the degraded Mutara rangelands, northeastern Rwanda. Environ Monit Assess 191:139. https://doi.org/10.1007/s10661-019-7226-5
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome coxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299. https://doi.org/10.4028/www.scientific.net/DDF.7.460
Gama-Flores JL, Castellanos-Paez ME, Sarma SSS, Nandini S (2007) Effect of pulsed exposure to heavy metals (copper and cadmium) on some population variables of Brachionus calyciflorus Pallas (Rotifera: Brachionidae: Monogononta). Hydrobiologia 593(1):201–208. https://doi.org/10.1007/s10750-007-9042-0
Garza-Mouriño G, Silva-Briano M, Nandini S, Sarma SSS, Castellanos-Paez ME (2005) Morphological and morphometrical variations of selected rotifer species in response to predation: a seasonal study of selected brachionid species from Lake Xochimilco (Mexico). Hydrobiologia 546(1):169–179. https://doi.org/10.1007/1-4020-4408-9_16
Gerbersdorf SU, Hollert H, Brinkmann M, Wieprecht S, Schüttrumpf H, Manz W (2011) Anthropogenic pollutants affect ecosystem services of freshwater sediments: the need for a “triad plus x” approach. J Soils Sediments 11(6):1099–1114. https://doi.org/10.1007/s11368-011-0373-0
Gianuca AT, Pantel JH, De Meester L (2016) Disentangling the effect of body size and phylogenetic distances on zooplankton top-down control of algae. Proc R Soc B Biol Sci 283(1828):20160487. https://doi.org/10.1098/rspb.2016.0487
Gilbert JJ (2013) The cost of predator-induced morphological defense in rotifers: experimental studies and synthesis. J Plankton Res 3:461–472. https://doi.org/10.1093/plankt/fbt01
Gilbert JJ (2018) Morphological variation and its significance in a polymorphic rotifer: environmental, endogenous, and genetic controls. BioScience 68(3):169–181. https://doi.org/10.1093/biosci/bix162
Glazier DS (1998) Does body storage act as a food-availability cue for adaptive adjustment of egg size and number in Daphnia magna? Freshw Biol 40(1):87–92. https://doi.org/10.1046/j.1365-2427.1998.00333.x
Green J, Lan OB (2010) Asplanchna and the spines of Brachionus calydflorus in two Javanese sewage ponds. Freshw Biol 4:223–226. https://doi.org/10.1111/j.1365-2427.1974.tb00092.x
Griffiths JI, Petchey OL, Pennekamp F, Childs DZ (2018) Linking intraspecific trait variation to community abundance dynamics improves ecological predictability by revealing a growth-defence trade-off. Funct Ecol 32:496–508. https://doi.org/10.1111/1365-2435.12997
Gunn IDM, O’Hare MT, Maitland PS, May L (2011) Long-term trends in Loch Leven invertebrate communities. In Loch Leven: 40 years of scientific research. Springer, Dordrecht, pp. 59-72 https://doi.org/10.1007/978-94-007-4333-5_7
Hanazato T (2001) Pesticide effects on freshwater zooplankton: an ecological perspective. Environ Pollut 112(1):1–10. https://doi.org/10.1016/S0269-7491(00)00110-X
Hartmann AC, Marhaver KL, Chamberland VF, Sandin SA, Vermeij MJ (2013) Large birth size does not reduce negative latent effects of harsh environments across life stages in two coral species. Ecology 94(9):1966–1976. https://doi.org/10.1890/13-0161.1
Jiang Y (2009) China’s water scarcity. J Environ Manag 90(11):3185–3196. https://doi.org/10.1016/j.jenvman.2009.04.016
Johnston TA, Leggett WC (2002) Maternal and environmental gradients in the egg size of an iteroparous fish. Ecology 83(7):1777–1791. https://doi.org/10.2307/3071764
Kang HM, Lee JS, Lee YH, Kim MS, Park HG, Jeong CB, Lee JS (2019) Body size-dependent interspecific tolerance to cadmium and their molecular responses in the marine rotifer Brachionus spp. Aquat Toxicol 206:195–202. https://doi.org/10.1016/j.aquatox.2018.10.020
Karlsson K, Winder M (2018) Ecosystem effects of morphological and life history traits in two divergent zooplankton populations. Front Mar Sci 5. https://doi.org/10.3389/fmars.2018.00408
Lass S, Spaak P (2003) Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491(1):221–239. https://doi.org/10.1023/A:1024487804497
Leppänen M (1995) The role of feeding behaviour in bioaccumulation of organic chemicals in benthic organisms. Ann Zool Fenn 32(3):247–255 Retrieved May 31, 2021, from http://www.jstor.org/stable/23735696
Malik DS, Sharma AK, Sharma AK, Thakur R, Sharma M (2020) A review on impact of water pollution on freshwater fish species and their aquatic environment. Adv Environ Pollut Manag: Wastewater Impacts Treatment Technol 1:10–28. https://doi.org/10.26832/aesa-2020-aepm-02
Michael ES, Stephen JL (1998) Zooplankton population and community responses to the pesticide azinphos-methyl in freshwater littoral enclosures. Environ Toxicol Chem 17(5):907–914. https://doi.org/10.1002/etc.5620170520
Montero-Pau J, Gómez A, Muñoz J (2008) Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnol Oceanogr Methods 6:218–222. https://doi.org/10.4319/lom.2008.6.218
Moore MV, Folt CL (1993) Zooplankton body size and community structure: effects of thermal and toxicant stress. Trends Ecol Evol 8(5):178–183. https://doi.org/10.1016/0169-5347(93)90144-E
Oksanen O, Blanchet FG, Kindt R et al (2016) Vegan: community ecology package. R Package Version 2:3–5 http://CRAN.R-project.org/package=vegan
Papakostas S, Michaloudi E, Proios K et al (2016) Integrative taxonomy recognizes evolutionary units despite widespread mitonuclear discordance: evidence from a rotifer cryptic species complex. Syst Biol 65(3):508–524. https://doi.org/10.1093/sysbio/syw016
R Core Team (2017) R: A language and environment for statistical computing, v. 3.3.3. R Foundation for Statistical Computing, Vienna
Santo N, Caprioli M, Orsenigo S, Ricci C (2001) Egg size and offspring fitness in a bdelloid rotifer. Hydrobiologia 446(1):71–74. https://doi.org/10.1023/A:1017525222744
Savage VM, Allen AP, Brown JH, Gillooly JF, West GB (2007) Scaling of number, size, and metabolic rate of cells with body size in mammals. Proc Natl Acad Sci 104(11):4718–4723. https://doi.org/10.1073/pnas.0611235104
Stemberger RS, Gilbert JJ (1985) Body size, food concentration, and population growth in planktonic rotifers. Ecology 66(4):1151–1159. https://doi.org/10.2307/1939167
Sun D, Niu C (2012) Adaptive significance of temperature-induced egg size plasticity in a planktonic rotifer, Brachionus calyciflorus. J Plankton Res 34(10):864–873. https://doi.org/10.1093/plankt/fbs050
Tessier AJ, Consolatti NL (1989) Variation in offspring size in Daphnia and consequences for individual fitness. Oikos 56:269–276. https://doi.org/10.2307/3565347
Uriarte I, Villate F (2004) Effects of pollution on zooplankton abundance and distribution in two estuaries of the Basque coast (Bay of Biscay). Mar Pollut Bull 49(3):220–228. https://doi.org/10.1016/j.marpolbul.2004.02.010
Vinebrooke RD, Cottingham KL, Norberg J et al (2004) Impacts of multiple stressors on biodiversity and ecosystem functioning: the role of species co-tolerance. Oikos 104(3):451–457. https://doi.org/10.1111/j.0030-1299.2004.13255.x
Wang Y, Niu J, Zhang L, Shi J (2014) Toxicity assessment of perfluorinated carboxylic acids (PFCAs) towards the rotifer Brachionus calyciflorus. Sci Total Environ 491:266–270. https://doi.org/10.1016/j.scitotenv.2014.02.028
Wilson DS (1975) The adequacy of body size as a niche difference. Am Nat 109(970):769–784. https://doi.org/10.1086/283042
Xiang XL, Chen YY, Han Y, Wang XL, Xi YL (2016) Comparative studies on the life history characteristics of two Brachionus calyciflorus strains belonging to the same cryptic species. Biochem Syst Ecol 69:138–144. https://doi.org/10.1016/j.bse.2016.09.003
Xiong W, Ni P, Chen Y, Gao Y, Shan B, Zhan A (2017) Zooplankton community structure along a pollution gradient at fine geographical scales in river ecosystems: the importance of species sorting over dispersal. Mol Ecol 26(16):4351–4360. https://doi.org/10.1111/mec.14199
Xiong W, Ni P, Chen Y, Gao Y, Li S, Zhan A (2019) Biological consequences of environmental pollution in running water ecosystems: a case study in zooplankton. Environ Pollut 252(part B):1483–1490. https://doi.org/10.1016/j.envpol.2019.06.055
Xue YH, Yang XX, Zhang G, Xi YL (2017) Morphological differentiation of Brachionus calyciflorus caused by predation and coal ash pollution. Sci Rep 7(1):15779. https://doi.org/10.1038/s41598-017-16192-w
Yan Z, Yang Q, Wang X, Torres OL, Tang S, Zhang S, Guo R, Chen J (2019) Correlation between antibiotic-induced feeding depression and body size reduction in zooplankton (rotifer, Brachionus calyciflorus): neural response and digestive enzyme inhibition. Chemosphere 218:376–383. https://doi.org/10.1016/j.chemosphere.2018.11.067
Yang J, Zhang X, Xie Y, Song C, Sun J, Zhang Y, Giesy JP, Yu H (2017) Ecogenomics of zooplankton community reveals ecological threshold of ammonia nitrogen. Environ Sci Technol 51(5):3057–3064. https://doi.org/10.1021/acs.est.6b05606
Yang Y, Gao Y, Huang X, Ni P, Wu Y, Deng Y, Zhan A (2019) Adaptive shifts of bacterioplankton communities in response to nitrogen enrichment in a highly polluted river. Environ Pollut 245:290–299. https://doi.org/10.1016/j.envpol.2018.11.002
Yuan LL, Pollard AI (2018) Changes in the relationship between zooplankton and phytoplankton biomasses across a eutrophication gradient. Limnol Oceanogr 63(6):2493–2507. https://doi.org/10.1002/lno.10955
Zhang L, Niu J, Li Y, Wang Y, Sun D (2013) Evaluating the sub-lethal toxicity of PFOS and PFOA using rotifer Brachionus calyciflorus. Environ Pollut 180:34–40. https://doi.org/10.1016/j.envpol.2013.04.031
Acknowledgements
The authors would like to thank members from Zhan Lab for their assistant during the field work.
Funding
This work was supported by the National Natural Science Foundation of China (grant numbers 31800307; 31572228).
Author information
Authors and Affiliations
Contributions
A. Z. and W. X. conceived the study. X. C. collected the samples and did the laboratory work. W. X. and X. C. analyzed the data. X. C., W. X., A. Z., and X. G. wrote the manuscript. All authors reviewed and commented on the early versions of this manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
This study collected rotifers from a river. Based on regulations in China, the collection and use of such a taxonomic group does not need any permit or ethics approval.
Consent for publication
Not applicable
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Xianliang Yi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(DOC 749 kb)
Rights and permissions
About this article
Cite this article
Chen, ., Guo, X., Xiong, W. et al. Pollution-driven morphological plasticity in a running water ecosystem. Environ Sci Pollut Res 29, 2783–2791 (2022). https://doi.org/10.1007/s11356-021-15802-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-15802-5