Abstract
Submerged macrophytes are regarded as being hardly assimilated by zooplankton for their lack of essential nutrients such as polyunsaturated fatty acids (PUFAs) thus serve as poor quality food, contrary to field stable isotopic investigations with observed macrophyte carbon contributions to zooplankton. However, periphyton growing on them produces the PUFAs and is thus a nutrient supplement. We hypothesize that with this supplement, zooplankton can be supported by macrophyte carbon. To test this hypothesis, we fed zooplankton with (1) 13C enriched Vallisneria natans detritus, (2) periphyton and (3) a mix of the two. We compared growth and reproduction of zooplankton under these three food treatments and calculated zooplankton assimilation of macrophyte carbon when fed a mixed diet, using a stable isotope-mixing model. The fatty acid profile of the two carbon resources was also analyzed. Our results demonstrate that Daphnia magna can grow and reproduce well, and use V. natans carbon when a supplement of periphyton is available.
Similar content being viewed by others
Data availability
The data that support this study are available from the corresponding author upon reasonable request.
References
Bakker ES, Wood KA, Pagès JF et al (2016) Herbivory on freshwater and marine macrophytes: a review and perspective. Aquat Bot 135:18–36. https://doi.org/10.1016/j.aquabot.2016.04.008
Batt RD, Carpenter SR, Cole JJ et al (2012) Resources supporting the food web of a naturally productive lake. Limnol Oceanogr 57:1443–1452. https://doi.org/10.4319/lo.2012.57.5.1443
Bearham D, Vanderklift MA, Downie RA, Thomson DP, Clementson LA (2020) Macrophyte-derived detritus in shallow coastal waters contributes to suspended particulate organic matter and increases growth rates of Mytilus edulis. Mar Ecol Prog Ser 644:91–103. https://doi.org/10.3354/meps13314
Becker C, Boersma M (2003) Resource quality effects on life histories of Daphnia. Limnol Oceanogr 48:700–706. https://doi.org/10.4319/lo.2003.48.2.0700
Becker C, Boersma M (2005) Differential effects of phosphorus and fatty acids on Daphnia magna growth and reproduction. Limnol Oceanogr 50:388–397. https://doi.org/10.4319/lo.2005.50.1.0388
Brett MT, Kainz MJ, Taipale SJ, Seshan H (2009) Phytoplankton, not allochthonous carbon, sustains herbivorous zooplankton production. Proc Natl Acad Sci 106:21197–21201. https://doi.org/10.1073/pnas.0904129106
Brothers SM, Hilt S, Meyer S, Köhler J (2013) Plant community structure determines primary productivity in shallow, eutrophic lakes. Freshw Biol 58:2264–2276. https://doi.org/10.1111/fwb.12207
Carpenter SR, Lodge DM (1986) Effects of submerged macrophytes on ecosystem processes. Aquat Bot 26:341–370. https://doi.org/10.1016/0304-3770(86)90031-8
Cattaneo A, Kalff J (1980) The relative contribution of aquatic macrophytes and their epiphytes to the production of macrophyte beds. Limnol Oceanogr 25:280–289. https://doi.org/10.4319/lo.1980.25.2.0280
Cazzanelli M, Forsström L, Rautio M, Minhelsen A, Christoffersen KS (2012) Benthic resources are the key to Daphnia middendorffiana survival in a high arctic pond. Freshw Biol 57:541–551. https://doi.org/10.1111/j.1365-2427.2011.02722.x
Cebrian J, Lartigue J (2004) Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecol Monogr 74:237–259. https://doi.org/10.1890/03-4019
Connolly RM, Hindell JS, Gorman D (2005) Seagrass and epiphytic algae support nutrition of a fisheries species, Sillago schomburgkii, in adjacent intertidal habitats. Mar Ecol Prog Ser 286:69–79. https://doi.org/10.3354/meps286069
Dalu T, Richoux NB, Froneman PW (2016) Nature and source of suspended particulate matter and detritus along an austral temperate river-estuary continuum, assessed using stable isotope analysis. Hydrobiologia 767:95–110. https://doi.org/10.1007/s10750-015-2480-1
De Kluijver A, Ning J, Liu Z, Jeppesen E, Gulati R, Middelburg J (2015) Macrophytes and periphyton carbon subsidies to bacterioplankton and zooplankton in a shallow eutrophic lake in tropical China. Limnol Oceanogr 60:375–385. https://doi.org/10.1002/lno.10040
Downing JA, Prairie YT, Cole JJ et al (2006) The global abundance and size distribution of lakes ponds, and impoundments. Limnol Oceanogr 51:2388–2397. https://doi.org/10.4319/lo.2006.51.5.2388
Gulati RD (1975) A study on the role of herbivorous zooplankton community as primary consumers of phytoplankton in Dutch lakes: With 2 figures and 3 tables in the text. Internationale Vereinigung für theoretische und angewandte Limnologie: Verhandlungen 19(2):1202–1210. https://doi.org/10.1046/j.1365-2427.1997.00275.x
Gulati RD, Demott WR (1997) The role of food quality for zooplankton: remarks on the state-of-the-art, perspectives and priorities. Freshw Biol 38:753–768. https://doi.org/10.1046/j.1365-2427.1997.00275.x
Harfmann J, Kurobe T, Bergamaschi B, Teh S, Hernes P (2019) Plant detritus is selectively consumed by estuarine copepods and can augment their survival. Sci Rep 9:9076. https://doi.org/10.1038/s41598-019-45503-6
Heckmann LH, Sibly RM, Timmermans MJTN, Callaghan A (2008) Outlining eicosanoid biosynthesis in the crustacean Daphnia. Front Zool 5:11. https://doi.org/10.1186/1742-9994-5-11
Hélène M, Alexandre B, Gilles B (2012) Trophic partitioning among three littoral microcrustaceans: relative importance of periphyton as food resource. Limnology 71:261–266. https://doi.org/10.4081/jlimnol.2012.e28
Hill WR, Rinchard J, Czesny S (2011) Light, nutrients and the fatty acid composition of stream periphyton. Freshw Biol 56:1825–1836. https://doi.org/10.1111/j.1365-2427.2011.02622.x
Jaschinski S, Brepohl DC, Sommer U (2008) Carbon sources and trophic structure in an eelgrass Zostera marina bed, based on stable isotope and fatty acid analyses. Mar Ecol Prog Ser 358:103–114. https://doi.org/10.3354/meps07327
Jeppesen E, Lauridsen TL, Kairesalo T, Perrow MR (1998) Impact of submerged macrophytes on fish-zooplankton interactions in lakes. In: Jeppesen E, Søndergaard M, Søndergaard M, Christoffersen K (eds) Ecological studies book series. Springer, New York, pp 91–114
Jeppesen E, Søndergaard M, Lauridsen TL et al (2012) Biomanipulation as a restoration tool to combat eutrophication: recent advances and future challenges. Adv Ecol Res 47:411–488. https://doi.org/10.1016/B978-0-12-398315-2.00006-5
Jones JI, Waldron S (2003) Combined stable isotope and gut contents analysis of food webs in plant-dominated, shallow lakes. Freshw Biol 48:1396–1407. https://doi.org/10.1046/j.1365-2427.2003.01095.x
Koussoroplis AM, Bec A, Perga ME, Koutrakis E, Bourdier G, Desvilettes C (2010) Fatty acid transfer in the food web of a coastal Mediterranean lagoon: evidence for high arachidonic acid retention in fish. Estuar Coast Shelf Sci 91:450–461. https://doi.org/10.1016/j.ecss.2010.11.010
Lampert W (1987) Feeding and nutrition in Daphnia. Mem Ist Ital Idrobiol 45:143–192
Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Bot 41:195–224. https://doi.org/10.1016/0304-3770(91)90044-6
Mahdy A, Scharfenberger U, Adrian R, Hilt S (2014) Experimental comparison of periphyton removal by chironomid larvae and Daphnia magna. Inland Waters 5:81–88. https://doi.org/10.5268/IW-5.1.755
Martin-Creuzburg D, Wacker A, Basena T (2010) Interactions between limiting nutrients: consequences for somatic and population growth of Daphnia magna. Limnol Oceanogr 55:2597–2607. https://doi.org/10.4319/lo.2010.55.6.2597
Miller RJ, Page HM (2012) Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence. Mar Biol 159:1391–1402. https://doi.org/10.1007/s00227-012-1929-2
Moss B (1990) Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. In: Martens K (ed) Developments in Hydrobiology. Springer, Berlin, pp 367–377
Müller-Navarra DC (1995) Biochemical versus mineral limitation in Daphnia. Limnol Oceanogr 40:1209–1214. https://doi.org/10.4319/lo.1995.40.7.1209
Nõges T, Luup H, Feldmann T (2010) Primary production of aquatic macrophytes and their epiphytes in two shallow lakes (Peipsi and Võrtsjärv) in Estonia. Aquat Ecol 44:83–92. https://doi.org/10.1007/s10452-009-9249-4
Paice RL, Chambers JM, Robson BJ (2017) Potential of submerged macrophytes to support food webs in lowland agricultural streams. Mar Freshw Res 68:549–562. https://doi.org/10.1071/MF15391
Palomar-Abesamis N, Juinio-Meñez MA, Slater MJ (2018) Macrophyte detritus as nursery diets for juvenile sea cucumber Stichopus cf. horrens. Aquac Res 49:3614–3623. https://doi.org/10.1111/are.13829
Parnell A, Inger R (2016) Package ‘simmr’. https://cran.rproject.org/web/packages/simmr/simmr.pdf
Parrish CC (2009) Essential fatty acids in aquatic food webs. In: Arts MT, Brett MT, Kainz MJ (eds) Lipids in aquatic ecosystems. Springer, New York, pp 309–326
Pettit NE, Warfe DM, Close PG et al (2017) Carbon sources for aquatic food webs of riverine and lacustrine tropical waterholes with variable groundwater influence. Mar Freshw Res 68:442–451. https://doi.org/10.1071/MF15365
Rautio M, Vincent WF (2006) Benthic and pelagic food resources for zooplankton in shallow high-latitude lakes and ponds. Freshw Biol 51:1038–1052. https://doi.org/10.1111/j.1365-2427.2006.01550.x
Ravet JL, Brett MT (2006) Phytoplankton essential fatty acid and phosphorus content constraints on Daphnia somatic growth and reproduction. Limnol Oceanogr 51:2438–2452. https://doi.org/10.4319/lo.2006.51.5.2438
Richoux NB, Bergamino L, Moyo S, Dalu T (2017) Spatial and temporal variability in the nutritional quality of basal resources along a temperate river/estuary continuum. Org Geochem 116:1–12. https://doi.org/10.1016/j.orggeochem.2017.11.009
Runge JA, Roff JC (2000) The measurement of growth and reproductive rates. ICES Zooplankton Methodol Manual. https://doi.org/10.1016/B978-012327645-2/50010-4
Sayanova OV, Napier JA (2004) Eicosapentaenoic acid: biosynthetic routes and the potential for synthesis in transgenic plants. Phytochemistry 65:147–158. https://doi.org/10.1016/j.phytochem.2003.10.017
Scheffer M, Jeppesen E (1998) Alternative stable states. In: Jeppesen E, Søndergaard M, Søndergaard M, Christoffersen K (eds) Ecological studies book series. Springer, New York, pp 397–406
Siehoff S, Hammers-Wirtz M, Strauss T, Ratte HT (2009) Periphyton as alternative food source for the filter-feeding cladoceran Daphnia magna. Freshw Biol 54:15–23. https://doi.org/10.1111/j.1365-2427.2008.02087.x
Søndergaard ML, Liboriussen R, Pedersen AR, Jeppesen E (2008) Lake restoration by fish removal: short- and long-term effects in 36 Danish lakes. Ecosystems 11:1291–1305. https://doi.org/10.1007/s10021-008-9193-5
Taipale SJ, Galloway AWE, Aalto SL, Kahilainen KK, Strandberg U, Kankaal P (2016) Terrestrial carbohydrates support freshwater zooplankton during phytoplankton deficiency. Sci Reprts 6:30897. https://doi.org/10.1038/srep30897
Tang Y, Yang X, Xu R, Zhang X, Liu Z, Zhang Y, Dumont HJ (2019) Heterotrophic microbes upgrade food value of a terrestrial carbon resource for Daphnia magna. Limnol Oceanogr 64:474–482. https://doi.org/10.1002/lno.11052
Verpoorter C, Kutser T, Seekell DA, Tranvik LJ (2014) A global inventory of lakes based on high-resolution satellite imagery. Geophys Res Lett 41:6396–6402. https://doi.org/10.1002/2014GL060641
Weers P, Siewertsen K, Gulati R (1997) Is the fatty acid composition of Daphnia Galeata determined by the fatty acid composition of the ingested diet? Freshw Biol 38(3):731–738. https://doi.org/10.1046/j.1365-2427.1997.00238.x
Wolters JW, Verdonschot RCM, Schoelynck J, Brion N, Verdonschot PFM, Meire P (2018) Stable isotope measurements confirm consumption of submerged macrophytes by macroinvertebrate and fish taxa. Aquat Ecol 52:269–280. https://doi.org/10.1007/s10452-018-9662-7
Zanden VMJ, Essington TE, Vadeboncoeur Y (2011) Is pelagic top-down control in lakes augmented by benthic energy pathways? Fish Aquat Sci 62:1422–1431. https://doi.org/10.1139/f05-042
Acknowledgements
National Natural Science Foundation of China (No. 32071566) supported this study financially. We are grateful for the work of numerous participants who collected and analyzed samples during the period of experiment.
Author information
Authors and Affiliations
Contributions
YT made substantial contributions to design, interpret the data and draft the manuscript; DZ contributed to design, acquire and analyze the data; LS contributed to conception. ZL, XZ and HJD revised the manuscript critically.
Corresponding author
Ethics declarations
Conflict of interest
We declared no conflicts of interest/competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Télesphore Sime-Ngando
Rights and permissions
About this article
Cite this article
Tang, Y., Zhou, D., Su, L. et al. Vallisneria natans detritus supports Daphnia magna somatic growth and reproduction under addition of periphyton. Aquat Ecol 55, 579–588 (2021). https://doi.org/10.1007/s10452-021-09846-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-021-09846-5