While theoretical food web studies highlight the importance of alternative energy pathways in shaping community response to bottom-up and top-down forcing, empirical insight on the relevance of the predicted patterns is largely lacking. In marine plankton food webs differences in food size spectra between ciliates and copepods lead to alternative energy pathways, one expanding from small phytoplankton over ciliates to copepods, the other from large edible phytoplankton directly to copepods. Correspondingly, predation pressure by copepods leads to an increase of small phytoplankton through top-down control of copepods on ciliates, but to a decrease of large phytoplankton through direct predation by copepods. Hence, food web theory predicts a shift from the dominance of large to small algae along an enrichment gradient. This prediction clearly deviates from the general assumption of a shift from small fast growing to larger slow-growing phytoplankton taxa with increasing nutrient availability. However, if copepods themselves are under top-down control by strong predation through planktivores such as fish or jellyfish, dominance of large algae is expected throughout the enrichment gradient. We tested these predictions by analyzing the phytoplankton composition from numerous marine lakes and lagoon sites located on the archipelago of Palau covering a wide range of nutrient levels, comparing sites lacking large numbers of higher trophic levels with sites harboring high densities of jellyfish. The observed patterns strongly support that higher trophic levels influence the phytoplankton size distribution along a nutrient enrichment gradient, highlighting the importance of alternate energy pathways in food webs for community responses.
This is a preview of subscription content,to check access.
Access this article
Similar content being viewed by others
The datasets analysed during the current study are available from the corresponding author on reasonable request.
Arin L, Morán XAG, Estrada M (2002) Phytoplankton size distribution and growth rates in the Alboran Sea (SW Mediterranean): short term variability related to mesoscale hydrodynamics. J Plankton Res 24:1019–1033
Armstrong RA (1994) Grazing limitation and nutrient limitation in marine ecosystems: steady state solutions of an ecosystem model with multiple food chains. Limnol Oceanogr 39:597–608
Bezio N, Costello JH, Perry E, Colin SP (2018) Effects of capture surface morphology on feeding success of scyphomedusae: a comparative study. Mar Ecol Prog Ser 596:83–93
Carpenter SR, Kitchell JF, Hodgson JR (1985) Cascading trophic interactions and lake productivity. Bioscience 35:634–639
Casini M, Lövgren J, Hjelm J, Cardinale M, Molinero J, Kornilovs G (2008) Multi-level trophic cascades in a heavily exploited open marine ecosystem. Proc R Soc B 275:1793–1801
Chisholm SW (1992) Phytoplankton size. In: Falkowski PG, Woodhead AD (eds) Primary productivity and biogeochemical cycles in the sea. Plenum Press, New York, pp 213–237
Colin PL (2009) Marine environments of Palau. Indo-Pacific Press, Taiwan
Daskalov GM, Grishi AN, Rodionov S, Mihneva V (2007) Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc Natl Acad Sci USA 104:10518–10523
Dawson MN (2005) Morphological variation and systematics in the Scyphozoa: mastigias (Rhizostomeae, Mastigiidae) a golden unstandard? Hydrobiologia 537:185–206
Dawson MN, Hamner WM (2003) Geographic variation and behavioral evolution in marine plankton: the case of Mastigias (Scyphozoa, Rhizostomeae). Mar Biol 143:1161–1174
Dawson MN, Hamner WM (2005) Rapid evolutionary radiation of marine zooplankton in peripheral environments. Proc Natl Acad Sci USA 102:9235–9240
Fretwell SD (1985) Food chain dynamics: the central theory of ecology? Oikos 50:291–301
Fulton RS (1984) Effects of chaetognath predation and nutrient enrichment on enclosed estuarine copepod communities. Oecologia 62:97–101
Garmendia M, Borja À, Franco J, Revilla M (2013) Phytoplankton composition indicators for the assessment of eutrophication in marine waters: present state and challenges within the European directives. Mar Pollut Bull 66:7–16
Graham WM, Kroutil RM (2001) Size-based prey selectivity and dietary shifts in the jellyfish, Aurelia aurita. J Plankton Res 23:67–74
Graham WM, Pagès F, Hamner W (2001) A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451:199–212
Hairston NG, Smith FE, Slobodkin LB (1960) Community structure, population control, and competition. Am Nat 94:421–425
Hamner WM, Hamner PP (1998) Stratified marine lakes of Palau (Western Caroline Islands). Phys Geogr 19:175–220
Hessen DO, Kaartvedt S (2014) Top-down cascades in lakes and oceans: different perspectives but same story? J Plankton Res 36:914–924
Holt RD, Grover J, Tilman D (1994) Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144:741–771
Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732
Irwin AJ, Finkel ZV, Schofield OME, Falkowski PG (2006) Scaling-up from nutrient physiology to the size-structure of phytoplankton communities. J Plankton Res 28:459–471
Kiørboe T (1993) Turbulence, phytoplankton cell size, and the structure of pelagic food webs. Adv Mar Biol 29:1–72
Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. Am Nat 147:784–812
McCloskey LR, Muscatine L, Wilkerson FP (1994) Daily photosynthesis, respiration, and carbon budgets in a tropical marine jellyfish (Mastigias sp.). Mar Biol 119:13–22
Myers RA, Baum JK, Shepherd TD, Powers SP, Peterson CH (2007) Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315:1846–1850
Oksanen L, Fretwell SD, Arruda J, Niemela P (1981) Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–261
Øresland V (1987) Feeding of the chaetognaths Sagitta elegans and S. setosa at different seasons in Gullmarsfjorden, Sweden. Mar Ecol Prog Ser 39:69–79
Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F Jr (1998) Fishing down marine food webs. Science 279:860–863
Rabalais NN, Turner RE, Díaz RJ, Justić D (2009) Global change and eutrophication of coastal waters. ICES J Mar Sci 66:1528–1537
Raimbault P, Pouvesle W, Diaz F, Garcia N, Sempéré R (1999) Wet-oxidation and automated colorimetry for simultaneous determination of organic carbon, nitrogen and phosphorus dissolved in seawater. Mar Chem 66:161–169
Shin Y-J, Travers M, Maury O (2010) Coupling low and high trophic levels models: towards a pathways-orientated approach for end-to-end models. Prog Oceanogr 84:105–112
Shurin JB, Borer ET, Seabloom EW, Anderson K, Blanchette CA, Broitman B, Cooper SD, Halpern BS (2002) A cross-ecosystem comparison of the strength of trophic cascades. Ecol Lett 5:785–791
Sommer U, Sommer F (2006) Cladocerans versus copepods: the cause of contrasting top–down controls on freshwater and marine phytoplankton. Oecologia 147:183–194
Stibor H, Vadstein O, Diehl S et al (2004) Copepods act as a switch between alternative trophic cascades in marine pelagic food webs. Ecol Lett 7:321–328
R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Thingstad TF (1998) A theoretical approach to structuring mechanisms in the pelagic food web. Hydrobiologia 363:59–72
Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitteilung Inernationale Vereinigung fuer Theoretische und Angewandte Limnologie 9:1–38
West EJ, Pitt KA, Welsh DT, Koop K, Rissik D (2009) Top-down and bottom-up influences of jellyfish on primary productivity and planktonic assemblages. Limnol Oceanogr 54:2058–2071
Wollrab S, Diehl S (2015) Bottom-up responses of the lower oceanic food web are sensitive to copepod mortality and feeding behavior. Limnol Oceanogr 60:641–656
Wollrab S, Diehl S, De Roos AM (2012) Simple rules describe bottom-up and top-down control in food webs with alternative energy pathways. Ecol Lett 15:935–946
We thank P. Colin, L. Colin, S. Patris, G. Urcham, E. Basilis, M. Mesubed, M. Dawson, M. Le Goff, M. Stockenreiter for help in data collection, and S. Diehl, G. Singer, K. Pohlmann, U. Sommer and two anonymous reviewers for helpful comments on an earlier version of the manuscript. We also thank the Coral Reef Research Foundation (CRRF) for their help with the logistic, and the Palau National Bureau of Marine Resources and Koror State Government for permitting our research in Palau. The project was funded by the European Commission MC CIG MICRODIVE. P.P. acknowledges the support of the Labex Mer (ANR-10-LABX-19).
This study was partly funded by the European Commission FP7 MC CIG MICRODIVE (322133).
Conflict of interest
All authors declare that he/she has no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Experiments were approved by the Republic of Palau and the State of Koror, research permit holders were Herwig Stibor & Philippe Pondaven. Jellyfish were released into their natural habitat after the experiments.
Responsible Editor: N. Aberle-Malzahn.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Reviewed by Undisclosed experts.
About this article
Cite this article
Wollrab, S., Pondaven, P., Behl, S. et al. Differences in size distribution of marine phytoplankton in presence versus absence of jellyfish support theoretical predictions on top-down control patterns along alternative energy pathways. Mar Biol 167, 9 (2020). https://doi.org/10.1007/s00227-019-3621-2