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Advances in the aquatic sciences
RESEARCH ARTICLE

Phenological and life-history responses of a tropical cladoceran Moina micrura to multiple environmental drivers

Muhammad Raznisyafiq Razak A , Ahmad Zaharin Aris https://orcid.org/0000-0002-4827-0750 A B * , Muhammad Rozaimi Mohd Zaki A , Fatimah Md Yusoff B C and Zetty Norhana Balia Yusof D E
+ Author Affiliations
- Author Affiliations

A Department of Environment, Faculty of Forestry and Environment, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia.

B International Institute of Aquaculture and Aquatic Sciences, Universiti Putra Malaysia, Port Dickson, Negeri Sembilan 71050, Malaysia.

C Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia.

D Department of Biochemistry, Faculty of Biotechnology and Biomolecular Science, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia.

E Institute of Bioscience, Universiti Putra Malaysia, Serdang, Selangor 43400, Malaysia.

* Correspondence to: zaharin@upm.edu.my

Handling Editor: Richard Marchant

Marine and Freshwater Research 75, MF23173 https://doi.org/10.1071/MF23173
Submitted: 11 September 2023  Accepted: 27 February 2024  Published: 11 April 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Climate change and global warming has led to changes in water-quality parameters, which in turn have negative consequences for zooplankton.

Aims

To investigate the effects of various environmental stressors (pH, temperature, photoperiod, and food concentration) on the tropical freshwater microcrustacean Moina micrura.

Methods

The study examined the effects of these stressors on survival (lifespan), reproduction (days to first brood, number of broods, and total offspring), growth (individual size and total moulting), physiology (heart rate), and sex-switching effects (total male offspring).

Key results

Significant (P < 0.05) reductions in the total offspring, individual size, and heart rate of M. micrura were observed when exposed to acidic (pH 5) and alkaline (pH 9) conditions. Conversely, higher water temperatures (31°C) and longer light exposure (20 h) were found to increase total offspring and heart rate in M. micrura. Furthermore, male offspring were produced only under conditions of food scarcity (no food supply and 1 × 102 cells mL−1).

Conclusions

Climate change has a significant effect on the life-history traits of M. micrura, a tropical cladoceran species.

Implications

Vital insights that can guide policymakers and practitioners in developing more effective strategies to safeguard and preserve tropical freshwater aquatic habitats, especially those of zooplankton species.

Keywords: climate change, environmental stressors, life-history traits, Moina micrura, phenological responses, sex switching, tropical freshwater, zooplankton.

Reference

Arafat MY, Bakhtiyar Y, Mir ZA, Tak HI (2021) Paradigm of climate change and its influence on zooplankton. Biosciences Biotechnology Research Asia 18, 423-438.
| Crossref | Google Scholar |

Azuraidi OM, Yusoff FM, Shamsudin MN, Raha RA, Alekseev VR, Matias-Peralta HM (2013) Effect of food density on male appearance and ephippia production in a tropical cladoceran, Moina micrura Kurz, 1874. Aquaculture 412–413, 131-135.
| Crossref | Google Scholar |

Balseiro E, Laspoumaderes C, Smufer F, Wolinski L, Modenutti B (2021) Short term fluctuating temperature alleviates Daphnia stoichiometric constraints. Scientific Reports 11, 12383.
| Crossref | Google Scholar | PubMed |

Blewett TA, Delompré PLM, He Y, Folkerts EJ, Flynn SL, Alessi DS, Goss GG (2017) Sublethal and reproductive effects of acute and chronic exposure to flowback and produced water from hydraulic fracturing on the water flea Daphnia magna. Environmental Science & Technology 51, 3032-3039.
| Crossref | Google Scholar | PubMed |

Bonatesta F, Emadi C, Price ER, Wang Y, Greer JB, Xu EG, Schlenk D, Grosell M, Mager EM (2022) The developing zebrafish kidney is impaired by Deepwater Horizon crude oil early-life stage exposure: a molecular to whole-organism perspective. Science of The Total Environment 808, 151988.
| Crossref | Google Scholar | PubMed |

Camp AA, Haeba MH, LeBlanc GA (2019) Complementary roles of photoperiod and temperature in environmental sex determination in Daphnia spp. Journal of Experimental Biology 222, jeb195289.
| Crossref | Google Scholar |

Chen L, Fu X, Zhang G, Zeng Y, Ren Z (2012) Influences of temperature, pH and turbidity on the behavioral responses of Daphnia magna and Japanese Medaka (Oryzias latipes) in the biomonitor. Procedia Environmental Sciences 13, 80-86.
| Crossref | Google Scholar |

Chen R, Xu N, Zhao F, Wu Y, Huang Y, Yang Z (2015) Temperature-dependent effect of food size on the reproductive performances of the small-sized cladoceran Moina micrura. Biochemical Systematics and Ecology 59, 297-301.
| Crossref | Google Scholar |

Chen H, Gu X, Zeng Q, Mao Z (2019) Acute and chronic toxicity of carbamazepine on the release of chitobiase, molting, and reproduction in Daphnia similis. International Journal of Environmental Research and Public Health 16, 209.
| Crossref | Google Scholar | PubMed |

Connelly SJ, Stoeckel JA, Gitzen RA, Williamson CE, González MJ (2016) Effect of clonal selection on Daphnia tolerance to dark experimental conditions. PLoS ONE 11, e0159628.
| Crossref | Google Scholar | PubMed |

Deng D, Xie P (2003) Effect of food and temperature on the growth and development of Moina irrasa (Cladocera: Moinidae). Journal of Freshwater Ecology 18, 503-513.
| Crossref | Google Scholar |

Elías-Gutiérrez M, Juračka PJ, Montoliu-Elena L, Miracle MR, Petrusek A, Kořínek V (2019) Who is Moina micrura? Redescription of one of the most confusing cladocerans from terra typica, based on integrative taxonomy. Limnetica 38, 227-252.
| Crossref | Google Scholar |

Engert A, Chakrabarti S, Saul N, Bittner M, Menzel R, Steinberg CEW (2013) Interaction of temperature and an environmental stressor: Moina macrocopa responds with increased body size, increased lifespan, and increased offspring numbers slightly above its temperature optimum. Chemosphere 90, 2136-2141.
| Crossref | Google Scholar | PubMed |

Gao X, Chen H, Govaert L, Wang W, Yang J (2019) Responses of zooplankton body size and community trophic structure to temperature change in a subtropical reservoir. Ecology and Evolution 9, 12544-12555.
| Crossref | Google Scholar | PubMed |

Ghazy MME-D, Habashy MM, Mohammady EY (2011) Effects of pH on survival, growth and reproduction rates of the crustacean, Daphnia Magna. Australian Journal of Basic and Applied Sciences 5, 1-10.
| Google Scholar |

Grilo TF, Rosa R (2017) Intersexuality in aquatic invertebrates: prevalence and causes. Science of The Total Environment 592, 714-728.
| Crossref | Google Scholar | PubMed |

Gökçe D, Özhan Turhan D (2014) Effects of salinity tolerances on survival and life history of 2 cladocerans. Turkish Journal of Zoology 38, 347-353.
| Crossref | Google Scholar |

Hamid A, Bhat SU, Jehangir A (2020) Local determinants influencing stream water quality. Applied Water Science 10, 24.
| Crossref | Google Scholar |

Hochmuth JD, De Schamphelaere KAC (2014) The effect of temperature on the sensitivity of Daphnia magna to cyanobacteria is genus dependent. Environmental Toxicology and Chemistry 33, 2333-2343.
| Crossref | Google Scholar | PubMed |

Hoffschröer N, Grassl N, Steinmetz A, Sziegoleit L, Koch M, Zeis B (2021) Microplastic burden in Daphnia is aggravated by elevated temperatures. Zoology 144, 125881.
| Crossref | Google Scholar |

Huang J, Kang S, Zhang Q, Guo J, Sillanpää M, Wang Y, Sun S, Sun X, Tripathee L (2015) Characterizations of wet mercury deposition on a remote high-elevation site in the southeastern Tibetan Plateau. Environmental Pollution 206, 518-526.
| Crossref | Google Scholar | PubMed |

International Organization for Standardization (2012) ISO 6341:2012. Water quality: determination of the inhibition of the mobility of Daphnia magna Straus (Cladocera, Crustacea): acute toxicity test. (ISO) Available at https://www.iso.org/standard/54614.html

Iwai CB, Somparn A, Noller B (2011) Using zooplankton, Moina micrura kurz to evaluate the ecotoxicology of pesticides used in paddy fields of Thailand. In ‘Pesticides in the modern world – risks and benefits’. (Ed. M. Stoytcheva) pp. 267–280. (INTECH Open Access Publisher)

Jia J, Liu X, Li L, Lei C, Dong Y, Wu G, Hu G (2018) Transcriptional and translational relationship in environmental stress: RNAseq and ITRAQ proteomic analysis between sexually reproducing and parthenogenetic females in Moina micrura. Frontiers in Physiology 9, 812.
| Crossref | Google Scholar | PubMed |

Jones NT, Gilbert B (2016) Changing climate cues differentially alter zooplankton dormancy dynamics across latitudes. Journal of Animal Ecology 85, 559-569.
| Crossref | Google Scholar |

Khudr MS, Purkiss SA, Hager R (2019) Combined salinity and acidity stressors alter Daphnia magna population growth and structure under prolonged absence of photoperiod. bioRxiv 2019.12.11.872630. [Preprint, posted 3 May 2020].
| Crossref | Google Scholar |

Kim HJ, Koedrith P, Seo YR (2015) Ecotoxicogenomic approaches for understanding molecular mechanisms of environmental chemical toxicity using aquatic invertebrate, Daphnia model organism. International Journal of Molecular Sciences 16, 12261-12287.
| Crossref | Google Scholar | PubMed |

Li Z, Song L-L, Ma J, Li Y (2017) The characteristics changes of pH and EC of atmospheric precipitation and analysis on the source of acid rain in the source area of the Yangtze River from 2010 to 2015. Atmospheric Environment 156, 61-69.
| Crossref | Google Scholar |

Liang R, He J, Shi Y, Li Z, Sarvajayakesavalu S, Baninla Y, Guo F, Chen J, Xu X, Lu Y (2017) Effects of perfluorooctane sulfonate on immobilization, heartbeat, reproductive and biochemical performance of Daphnia magna. Chemosphere 168, 1613-1618.
| Crossref | Google Scholar |

Magnuson JJ, Crowder LB, Medvick PA (1979) Temperature as an ecological resource. American Zoologist 19, 331-343.
| Crossref | Google Scholar |

Martinez MR, Chakroff RP, Pantastica JB (1975) Note on direct phytoplankton counting technique using the haemocytometer. Philippine Agricultural 59, 1-12.
| Google Scholar |

Miracle MR, Nandini S, Sarma SSS, Vicente E (2011) Endocrine disrupting effects, at different temperatures, on Moina micrura (Cladocera: Crustacea) induced by carbendazim, a fungicide. Hydrobiologia 668, 155-170.
| Crossref | Google Scholar |

Murphy GEP, Romanuk TN, Worm B (2020) Cascading effects of climate change on plankton community structure. Ecology and Evolution 10, 2170-2181.
| Crossref | Google Scholar |

Pham T-L, Bui HM (2018) Comparison of diazinon toxicity to temperate and tropical freshwater Daphnia species. Journal of Chemistry 2018, 1-5.
| Crossref | Google Scholar |

Razak MR, Aris AZ, Md Yusoff F, Yusof ZNB, Kim SD, Kim KW (2022a) Assessment of RNA extraction protocols from cladocerans. PLoS ONE 17, e0264989.
| Crossref | Google Scholar | PubMed |

Razak MR, Aris AZ, Yusoff FM, Yusof ZNB, Abidin AAZ, Kim SD, Kim KW (2022b) Risk assessment of bisphenol analogues towards mortality, heart rate and stress-mediated gene expression in cladocerans Moina micrura. Environmental Geochemistry and Health 45, 3567-3583.
| Crossref | Google Scholar | PubMed |

Razak MR, Aris AZ, Yusoff FM, Yusof ZNB, Kim SD, Kim KW (2023) De novo transcriptomic and life-history responses of Moina Micrura under stress environment conditions. Marine Biotechnology 25, 473-487.
| Crossref | Google Scholar | PubMed |

Rodmongkoldee M, Taparhudee W (2020) Life table responses of Moina micrura fed with different food concentrations. Burapha Science Journal 25, 1136-1146 Available at http://science.buu.ac.th/ojs246/index.php/sci/article/view/3190.
| Google Scholar |

Rosli N, Gandaseca S, Gerusu GJ, Heng RKJ, Ahmed OH, Hanafi Idris MOHD, Pazi AMM (2020) Quality of tropical river water in different catchments of canopy cover. The Malaysian Forester 83, 128-148.
| Google Scholar |

Sarma SSS, Nandini S, Gulati RD (2005) Life history strategies of cladocerans: comparisons of tropical and temperate taxa. Hydrobiologia 542, 315-333.
| Crossref | Google Scholar |

Stenert C, Ehlert B, Ávila AC, Rocha Sousa FD, Esquinatti FM, Batzer DP, Maltchik L (2017) Dormant propagule banks of aquatic invertebrates in ponds invaded by exotic pine species in southern Brazil. Marine and Freshwater Research 68, 954-963.
| Crossref | Google Scholar |

Toyota K, Miyakawa H, Yamaguchi K, Shigenobu S, Ogino Y, Tatarazako N, Miyagawa S, Iguchi T (2015) NMDA receptor activation upstream of methyl farnesoate signaling for short day-induced male offspring production in the water flea, Daphnia pulex. BMC Genomics 16, 186.
| Crossref | Google Scholar |

Toyota K, Sato T, Tatarazako N, Iguchi T (2017) Photoperiodism of male offspring production in the water flea Daphnia pulex. Zoological Science 34, 312-317.
| Crossref | Google Scholar | PubMed |

Wang Y, He Z (2001) Effect of temperature and salinity on intrinsic increasing rate of Moina mongolica Daddy (Cladocera: Moinidae) population. Chinese Journal of Applied Ecology 12, 91-94.
| Google Scholar |

Wang L, Wang S, Zeng C, Wang Y, Zeng C (2021) Effects of food concentration and photoperiod on egg production, female life expectancy and population dynamics of the paracalanid copepod, Bestiolina amoyensis. Frontiers in Marine Science 8, 788744.
| Crossref | Google Scholar |

Weber AK, Pirow R (2009) Physiological responses of Daphnia pulex to acid stress. BMC Physiology 9, 9.
| Crossref | Google Scholar | PubMed |

Yuslan A, Najuwa S, Hagiwara A, Ghaffar MA, Suhaimi H, Rasdi NW (2021) Production performance of Moina macrocopa (Straus 1820) (Crustacea, cladocera) cultured in different salinities: the effect on growth, survival, reproduction, and fatty acid composition of the neonates. Diversity 13, 105.
| Crossref | Google Scholar |

Ślusarczyk M, Flis S (2019) Light quantity, not photoperiod terminates diapause in the crustacean Daphnia. Limnology and Oceanography 64, 124-130.
| Crossref | Google Scholar |

Šorf M, Davidson TA, Brucet S, Menezes RF, Søndergaard M, Lauridsen TL, Landkildehus F, Liboriussen L, Jeppesen E (2015) Zooplankton response to climate warming: a mesocosm experiment at contrasting temperatures and nutrient levels. Hydrobiologia 742, 185-203.
| Crossref | Google Scholar |