Flexible feeding patterns of copepod <i>Centropages tenuiremis</i> in fluctuating conditions: a possible survival strategy to cope with disturbance

Cuilian Xu; Simin Hu; Zhiling Guo; Tao Li; Hui Huang; Leo Lai Chan; Sheng Liu

doi:10.1007/s13131-020-1553-9

Volume 39 Issue 2

Turn off MathJax

Article Contents

Article Navigation > Acta Oceanologica Sinica > 2020 > 39(2): 59-68

Cuilian Xu, Simin Hu, Zhiling Guo, Tao Li, Hui Huang, Leo Lai Chan, Sheng Liu. Flexible feeding patterns of copepod Centropages tenuiremis in fluctuating conditions: a possible survival strategy to cope with disturbance[J]. Acta Oceanologica Sinica, 2020, 39(2): 59-68. doi: 10.1007/s13131-020-1553-9

Citation:

Cuilian Xu, Simin Hu, Zhiling Guo, Tao Li, Hui Huang, Leo Lai Chan, Sheng Liu. Flexible feeding patterns of copepod Centropages tenuiremis in fluctuating conditions: a possible survival strategy to cope with disturbance[J]. Acta Oceanologica Sinica, 2020, 39(2): 59-68. doi: 10.1007/s13131-020-1553-9

Citation:

PDF( 447 KB)

Flexible feeding patterns of copepod Centropages tenuiremis in fluctuating conditions: a possible survival strategy to cope with disturbance

doi: 10.1007/s13131-020-1553-9

Cuilian Xu^{1, 2},
Simin Hu¹,
Zhiling Guo^{1, 2, 3},
Tao Li^{1, 4},
Hui Huang^{1, 4},
Leo Lai Chan^{5, 6},
Sheng Liu^{1
,
,}

1.
Key Laboratory of Tropical Marine Bio-resources and Ecology/Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou 510301, China
2.
University of Chinese Academy of Sciences, Beijing 100049, China
3.
State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
4.
Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya 572000, China
5.
Shenzhen Key Laboratory for the Sustainable Use of Marine Biodiversity, Research Centre for the Oceans and Human Health, City University of Hong Kong Shenzhen Research Institute, Shenzhen 518057, China
6.
State Key Laboratory in Marine Pollution, City University of Hong Kong, Hong Kong 999077, China

Funds: The Strategic Priority Research Program of the Chinese Academy of Sciences under contract No. XDA13020100; the National Key Research and Development Project of China under contract No. 2016YFC0502800; the Science and Technology Planning Projects of Guangdong Province, China under contract Nos 2015A020216013 and 2017B030314052.

More Information

Corresponding author: E-mail: shliu@scsio.ac.cn
Received Date: 2018-08-23
Accepted Date: 2018-12-28

Available Online: 2020-04-21

Publish Date: 2020-02-25

Abstract

Abstract

Centropages tenuiremis is a species with a wide distribution range in disturbed coastal waters. However, due to a lack of dietary information, it remains unclear as to how they maintain such dominance in fluctuating conditions. In this study, C. tenuiremis was collected from the Daya Bay Nuclear Power Plant both in inlet and outfall regions at 06:00, 12:00 and 18:00 on April 27, 2011 and their in situ diet was analyzed using a PCR protocol targeting 18S ribosomal genes. Thirty-four species of prey organisms were identified totally, including Dinophyta, Baciliariophyta, Viridiplantae, Rhizaria, Apicomplexa, Chordata, Mollusca, Arthropoda and Fungi, indicating an obvious omnivorous feeding habit of C. tenuiremis. Centropages tenuiremis obviously exhibited spatial and temporal variations in diet composition. More plant prey (land plants and phytoplankton) were consumed in the morning (~50%), while more animal prey (metazoans and protozoans) were ingested at midday and night (60%–70%). Furthermore, a more diverse diet was detected in the outfall region (10–11 taxa), where the temperatures were relatively higher and more fluctuating, than in the control region (5–10 taxa). This finding indicated that C. tenuiremis could potentially expand its food spectrum under stressful condition. Specifically, C. tenuiremis exhibited phytoplankton preference (58.62%–67.64%) in the outfall region with a lower omnivory index (0.27–0.35) than in the control region (0.51–0.95). However, phytoplankton density was lower than that in the control region, suggesting a possible herbivorous tendency of C. tenuiremis under elevated temperatures to balance the energy acquirement and feeding effort. The flexible food choices of C. tenuiremis observed here could effectively buffer environmental fluctuations and might be an important survival strategy in coastal ecosystems.
- Centropages,
- feeding response,
- feeding strategy,
- coastal ecosystem,
- Daya Bay

FullText(HTML)

References(52)

References

[1]	Barbier E B, Hacker S D, Kennedy C, et al. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs, 81(2): 169–193. doi: 10.1890/10-1510.1
[2]	Benedetti F, Gasparini S, Ayata S D. 2016. Identifying copepod functional groups from species functional traits. Journal of Plankton Research, 38(1): 159–166. doi: 10.1093/plankt/fbv096
[3]	Boersma M, Mathew K A, Niehoff B, et al. 2016. Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it's hot?. Ecology Letters, 19(1): 45–53. doi: 10.1111/ele.12541
[4]	Calbet A. 2001. Mesozooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnology and Oceanography, 46(7): 1824–1830. doi: 10.4319/lo.2001.46.7.1824
[5]	Calbet A, Carlotti F, Gaudy R. 2007. The feeding ecology of the copepod Centropages typicus (Kröyer). Progress in Oceanography, 72(2–3): 137–150. doi: 10.1016/j.pocean.2007.01.003
[6]	Carlotti F, Harris R. 2007. The biology and ecology of Centropages typicus: an introduction. Progress in Oceanography, 72(2–3): 117–120. doi: 10.1016/j.pocean.2007.01.012
[7]	Carstensen J, Klais R, Cloern J E. 2015. Phytoplankton blooms in estuarine and coastal waters: seasonal patterns and key species. Estuarine, Coastal and Shelf Science, 162: 98–109. doi: 10.1016/j.ecss.2015.05.005
[8]	Chao A. 1984. Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11(4): 265–270
[9]	Christensen V, Pauly D. 1992. ECOPATH II—a software for balancing steady-state ecosystem models and calculating network characteristics. Ecological Modelling, 61(3–4): 169–185. doi: 10.1016/0304-3800(92)90016-8
[10]	Daan R, Gonzalez S R, Klein Breteler W C M. 1988. Cannibalism in omnivorous calanoid copepods. Marine Ecology Progress Series, 47: 45–54. doi: 10.3354/meps047045
[11]	Dagg M. 1977. Some effects of patchy food environments on copepods. Limnology and Oceanography, 22(1): 99–107. doi: 10.4319/lo.1977.22.1.0099
[12]	Floeter S R, Behrens M D, Ferreira C E L, et al. 2005. Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology, 147(6): 1435–1447. doi: 10.1007/s00227-005-0027-0
[13]	Gao Yahui, Li Song. 1990. Observational experiments on feeding rates of Centropages tenuiremis. Tropic Oceanology (in Chinese), 9(3): 59–65
[14]	Garrido S, Cruz J, Santos A M P, et al. 2013. Effects of temperature, food type and food concentration on the grazing of the calanoid copepod Centropages chierchiae. Journal of Plankton Research, 35(4): 843–854. doi: 10.1093/plankt/fbt037
[15]	Gaudy R, Thibault-Botha D. 2007. Metabolism of Centropages species in the Mediterranean Sea and the North Atlantic Ocean. Progress in Oceanography, 72(2-3): 151–163. doi: 10.1016/j.pocean.2007.01.005
[16]	Guo Zhiling, Liu Sheng, Hu Simin, et al. 2012. Prevalent ciliate symbiosis on copepods: high genetic diversity and wide distribution detected using small subunit ribosomal RNA gene. PLoS One, 7(9): e44847. doi: 10.1371/journal.pone.0044847
[17]	Han Wuying, Ma Kemei. 1991. Study on the process of sea water exchang in Daya Bay. Marine Sciences, (2): 64–67
[18]	Hoppenrath M, Leander B S. 2006. Dinoflagellate, Euglenid, or Cercomonad? The ultrastructure and molecular phylogenetic position of Protaspis grandis n. sp. The Journal of Eukaryotic Microbiology, 53(5): 327–342. doi: 10.1111/j.1550-7408.2006.00110.x
[19]	Hu Simin, Guo Zhiling, Li Tao, et al. 2014. Detecting in situ copepod diet diversity using molecular technique: development of a copepod/symbiotic ciliate-excluding eukaryote-inclusive PCR protocol. PLoS One, 9(7): e103528. doi: 10.1371/journal.pone.0103528
[20]	Hu Simin, Guo Zhiling, Li Tao, et al. 2015. Molecular analysis of in situ diets of coral reef copepods: evidence of terrestrial plant detritus as a food source in Sanya Bay, China. Journal of Plankton Research, 37(2): 363–371. doi: 10.1093/plankt/fbv014
[21]	Huang Jiaqi, Zheng Zhong. 1986. The effects of temperature and salinity on the survival of some copepods from Xiamen Harbour. Oceanologia et Limnologia Sinica (in Chinese), 17(2): 161–167
[22]	Jagadeesan L, Jyothibabu R, Arunpandi N, et al. 2017. Feeding preference and daily ration of 12 dominant copepods on mono and mixed diets of phytoplankton, rotifers, and detritus in a tropical coastal water. Environmental Monitoring and Assessment, 189(10): 503. doi: 10.1007/s10661-017-6215-9
[23]	Kiørboe T. 2011. How zooplankton feed: mechanisms, traits and trade-offs. Biological Reviews, 86(2): 311–339. doi: 10.1111/j.1469-185X.2010.00148.x
[24]	Kiørboe T, Saiz E, Tiselius P, et al. 2018. Adaptive feeding behavior and functional responses in zooplankton. Limnology and Oceanography, 63(1): 308–321. doi: 10.1002/lno.10632
[25]	Kondoh M. 2003. Foraging adaptation and the relationship between food-web complexity and stability. Science, 299(5611): 1388–1391. doi: 10.1126/science.1079154
[26]	Larsen P S, Madsen C V, Riisgård H U. 2008. Effect of temperature and viscosity on swimming velocity of the copepod Acartia tonsa, brine shrimp Artemia salina and rotifer Brachionus plicatilis. Aquatic Biology, 4(1): 47–54
[27]	Lee Shaoching. 1964. Preliminary studies on the food and feeding habits of some marine planktonic copepods in Amoy waters. Journal of Xiamen University (Natural Science) (in Chinese), 11(3): 93–109
[28]	Li Wei, Gao Kunshan. 2012. A marine secondary producer respires and feeds more in a high CO₂ ocean. Marine Pollution Bulletin, 64(4): 699–703. doi: 10.1016/j.marpolbul.2012.01.033
[29]	Li Tao, Liu Sheng, Huang Liangmin, et al. 2011. Diatom to dinoflagellate shift in the summer phytoplankton community in a bay impacted by nuclear power plant thermal effluent. Marine Ecology Progress Series, 424: 75–85. doi: 10.3354/meps08974
[30]	Li Kaizhi, Yin Jianqiang, Tan Yehui, et al. 2014. Short-term variation in zooplankton community from Daya Bay with outbreaks of Penilia avirostris. Oceanologia, 56(3): 583–602
[31]	Lin Hui. 2016. Composition and size distribution of colloidal organic matter in the Chukchi Sea and Daya Bay: application of asymmetric flow field-flow fractionation (in Chinese) [dissertation]. Xiamen: Xiamen University
[32]	Lin Xianzhi, Hu Simin, Liu Sheng, et al. 2018. Unexpected prey of juvenile spotted scat (Scatophagus argus) near a wharf: the prevalence of fouling organisms in stomach contents. Ecology and Evolution, 8(16): 8547–8554. doi: 10.1002/ece3.4380
[33]	Liu Guangxing, Li Song. 1998. Seasonal variations in body length and weight and ingestion rate of Centropages tenuiremis thompson and scott. Haiyang Xuebao (in Chinese), 20(3): 104–109
[34]	Liu Huaxue, Li Kaizhi, Huang Honghui, et al. 2013. Seasonal community structure of mesozooplankton in the Daya Bay, South China Sea. Journal of Ocean University of China, 12(3): 452–458. doi: 10.1007/s11802-013-1991-5
[35]	Ma Aijun, Wang Xin’an, Zhuang Zhimeng, et al. 2007. Structure of retina and visual characteristics of the half-smooth tongue-sole Cynoglossus semilaevis Günter. Acta Zoologica Sinica (in Chinese), 53(2): 354–363
[36]	Madden N, Lewis A, Davis M. 2013. Thermal effluent from the power sector: an analysis of once-through cooling system impacts on surface water temperature. Environmental Research Letters, 8(3): 035006. doi: 10.1088/1748-9326/8/3/035006
[37]	Masclaux H, Bec A, Kagami M, et al. 2011. Food quality of anemophilous plant pollen for zooplankton. Limnology and Oceanography, 56(3): 939–946. doi: 10.4319/lo.2011.56.3.0939
[38]	Masclaux H, Perga ME, Kagami M, et al. 2013. How pollen organic matter enters freshwater food webs. Limnology and Oceanography, 58(4): 1185–1195. doi: 10.4319/lo.2013.58.4.1185
[39]	Perez-Moreno J, Read D J. 2001. Exploitation of pollen by mycorrhizal mycelial systems with special reference to nutrient recycling in boreal forests. Proceedings of the Royal Society of London B: Biological Sciences, 268(1474): 1329–1335. doi: 10.1098/rspb.2001.1681
[40]	Quéméré E, Hibert F, Miquel C, et al. 2013. A DNA metabarcoding study of a primate dietary diversity and plasticity across its entire fragmented range. PLoS One, 8(3): e58971. doi: 10.1371/journal.pone.0058971
[41]	Richardson A J. 2008. In hot water: zooplankton and climate change. ICES Journal of Marine Science, 65(3): 279–295. doi: 10.1093/icesjms/fsn028
[42]	Saage A, Vadstein O, Sommer U. 2009. Feeding behaviour of adult Centropages hamatus (Copepoda, Calanoida): functional response and selective feeding experiments. Journal of Sea Research, 62(1): 16–21. doi: 10.1016/j.seares.2009.01.002
[43]	Saiz E, Calbet A. 2011. Copepod feeding in the ocean: scaling patterns, composition of their diet and the bias of estimates due to microzooplankton grazing during incubations. Hydrobiologia, 666(1): 181–196. doi: 10.1007/s10750-010-0421-6
[44]	Shannon C E, Weaver W. 1949. The Mathematical Theory of Communication. Urbana: University of Illinois Press, 6–28
[45]	Simpson E H. 1949. Measurement of diversity. Nature, 163(4148): 688. doi: 10.1038/163688a0
[46]	Taylor J D, Cottingham S D, Billinge J, et al. 2014. Seasonal microbial community dynamics correlate with phytoplankton-derived polysaccharides in surface coastal waters. The ISME Journal, 8(1): 245–248. doi: 10.1038/ismej.2013.178
[47]	Troedsson C, Grahl-Nielsen O, Thompson E M. 2005. Variable fatty acid composition of the pelagic appendicularian Oikopleura dioica in response to dietary quality and quantity. Marine Ecology Progress Series, 289: 165–176. doi: 10.3354/meps289165
[48]	Yabuki A, Ishida KI. 2011. Mataza hastifera n. g., n. sp.: a possible new lineage in the Thecofilosea (Cercozoa). The Journal of Eukaryotic Microbiology, 58(2): 94–102. doi: 10.1111/j.1550-7408.2010.00524.x
[49]	Yang Jiming. 2001. A study on food and trophic levels of Bohai Sea copepoda. Modern Fisheries Information (in Chinese), 16(6): 6–10
[50]	Yang Yufeng, Wang Zhaoding, Pan Mingxiang, et al. 2002. Zooplankton community structure of the sea surface microlayer near nuclear power plants and marine fish culture zones in Daya Bay. Chinese Journal of Oceanology and Limnology, 20(2): 129–134. doi: 10.1007/BF02849649
[51]	Yu Juan, Zhang Yu, Yang Guipeng, et al. 2012. Effects of diet, temperature and salinity on ingestion and egestion of two species of marine copepods. Periodical of Ocean University of China (in Chinese), 42(7–8): 45–52
[52]	Zhang Wenquan, Zhou Ruming. 2004. Thermal impact analysis of discharge of circulating cooling water at Daya Bay nuclear power station (GNPS) and Ling Ao nuclear power station (LNPS). Radialization Protection (in Chinese), 24(3–4): 257–263