Abstract
The grazing effects of zooplankton communities are predicted to be strongest in mesotrophic lakes relative to eutrophic and oligotrophic lakes, an idea known as the Mesotrophic Maximum Hypothesis. We tested if the predictions of this hypothesis depend on the community of zooplankton present by evaluating whether the community of zooplankton, in addition to lake trophic state, interact to determine the magnitude of grazing effects. We conducted mesocosm experiments to evaluate the effects of Daphnia spp., Epischura nevadensis, and juvenile and adult Mysis diluviana on ecosystem function in oligotrophic Lake Tahoe and its more productive embayment, Emerald Bay. In the Lake Tahoe experiment, the Daphnia and the Adult Mysid treatments produced lower dissolved organic carbon concentrations, and the Epischura treatment yielded lower soluble reactive phosphorus concentrations compared to a Control treatment that lacked macrozooplankton. In the Emerald Bay experiment, the Daphnia treatment lowered chlorophyll a concentrations, the Daphnia and Juvenile Mysid treatments reduced small particle (diameter 0.5 – < 5 µm) concentrations, and each of the species treatments produced higher ammonium concentrations and DIN/SRP ratios compared to the Control. Analyses of similarities (ANOSIM) indicated that these taxa differed from one another in their overall effects on Emerald Bay water, but not on Lake Tahoe water. This finding supports the Mesotrophic Maximum Hypothesis, but also shows that grazing effects are dependent on the taxonomic makeup of the zooplankton community in addition to lake trophic state. As ongoing cultural eutrophication continues to elevate Lake Tahoe's productivity, the roles and importance of the lake’s zooplankton taxa may diverge.
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The codes written for analyzing data in this study were created using R Studio version 3.6.3 and are available from the corresponding author on request.
References
Adrian R, Schneider-Olt B (1999) Top-down effects of crustacean zooplankton on pelagic microorganisms in a mesotrophic lake. J Plankton Res 21:2175–2190. https://doi.org/10.1093/plankt/21.11.2175
Andersen T, Hessen DO (1991) Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol Oceanogr 36:807–814. https://doi.org/10.4319/lo.1991.36.4.0807
Andri Signorell et al. (2019). DescTools: Tools for descriptive statistics. R package version 0.99.31.
Arar EJ, GB Collins (1997) Method 445.0 In Vitro Determination of Chlorophyll a and Pheophytin and Marine and Freshwater Algae by Fluorescence. U.S. Environmental Protection Agency, Washington, DC.
Beeton AM (1960) The vertical migration of Mysis relicta in Lakes Huron and Michigan. Can J Fish Aquat 17:517–539. https://doi.org/10.1139/f60-037
Benndorf J, Boing W, Koop J, Neubauer I (2002) Top-down control of phytoplankton: the role of time scale, lake depth and trophic state. Freshw Biol 47:2282–2295. https://doi.org/10.1046/j.1365-2427.2002.00989.x
Bigelow LK, Lasenby DC (1991) Particle size selection in cadmium uptake by the opossum shrimp, Mysis relicta. Bull Environ Contam Toxicol 47:790–796. https://doi.org/10.1007/BF01701151
Brett MT, Wiackowski K, Lubnow FS, Mueller-Solger A, Elser JJ, Goldman CR (1994) Species-dependent effects of zooplanktonic ecosystem processes in Castle Lake, California. Ecology 75:2243–2254. https://doi.org/10.2307/1940880
Burns C (1968) The relationship between body size of filter-feeding cladocera and the maximum size of particle ingested. Limnol Oceanogr 13:675–678. https://doi.org/10.4319/lo.1968.13.4.0675
Burns C, Schallenberg M (2001) Calanoid copepods versus cladocerans: consumer effects on protozoa in lakes of different trophic status. Limnol Oceanogr 46:1558–1565. https://doi.org/10.4319/lo.2001.46.6.1558
Byron E, Sawyer P, Goldman CR (1986) The recurrence of Daphnia rosea in Lake Tahoe: analysis of a population pulse. J Plankton Res 8:771–783. https://doi.org/10.1093/plankt/8.4.771
Carpenter SR, Bergquist AM (1984) Experimental tests of grazing indicators based on chlorophyll-a degradation products. Ach Hydrobiol 2:1–15
Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Coats R, Perez-Losada J, Schladow G, Richards R, Goldman C (2006) The warming of Lake Tahoe. Clim Change 76:121–148. https://doi.org/10.1007/s10584-005-9006-1
Cooper S, Goldman CR (1980) Opossum shrimp (Mysis relicta) predation on zooplankton. Can J Fish Aquat Sci 37:909–919. https://doi.org/10.1139/f80-120
Shimadzu Corporation. 2003. TOC-VCPH/CPN & TOC-Control V Software: User Manual. Retrieved from http://www.ecs.umass.edu/eve/facilities/equipment/TOC/TOCV/TOC-V_CP_Users_Manual_E.pdf.
Cottingham KL, Knight SE, Carpenter SR, Cole JJ, Pace ML, Wagner AE (1997) Response of phytoplankton and bacteria to nutrients and zooplankton: a mesocosm experiment. J Plankton Res 19:995–1010. https://doi.org/10.1093/plankt/19.8.995
Cyr H (1998) Cladoceran- and copepod-dominated zooplankton communities graze at similar rates in low-productivity lakes. Can J Fish Aquat Sci 55:414–422. https://doi.org/10.1139/f97-217
Cyr H, Curtis JM (1999) Zooplankton community size structure and taxonomic composition affects size-selective grazing in natural communities. Oecologia 118:306–315. https://doi.org/10.1007/s004420050731
Daley RJ (1973) Experimental characterization of lacustrine chlorophyll diagenesis. II. Bacterial, viral and herbivore grazing effects. Arch Hydrobiol 72:409–439
Daley RJ, Brown SR (1973) Experimental characterization of lacustrine chlorophyll diagenesis. I. Physiological and environmental effects. Arch Hydrobiol 72:277–304
DeMott WR (1982) Feeding selectivities and relative ingestion rates of Daphnia and Bosmina. Limnol Oceanogr 27:518–527. https://doi.org/10.4319/lo.1982.27.3.0518
DeMott WR, Kerfoot WC (1982) Competition among cladocerans: nature of the interaction between Bosmina and Daphnia. Ecology 63:1949–1966. https://doi.org/10.2307/1940132
Dunnett CW (1955) A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc 272:1096–1121. https://doi.org/10.1080/01621459.1955.10501294
Ekvall MK, Urrutia-Cordero P, Hansson L (2014) Linking cascading effects of fish predation and zooplankton grazing to reduced cyanobacterial biomass and toxin levels following biomanipulation. PLoS ONE 9:1–10. https://doi.org/10.1371/journal.pone.0112956
Elser JJ, Goldman CR (1991) Zooplankton effects on phytoplankton in lakes of contrasting trophic status. Limnol Oceanogr 36:64–90. https://doi.org/10.4319/lo.1991.36.1.0064
Elser JJ, Elser MM, MacKay NA, Carpenter SR (1988) Zooplankton-mediated transitions between N- and P-limited algal growth. Limnol Oceanogr 33:1–14. https://doi.org/10.4319/lo.1988.33.1.0001
Elser JJ, Carney HJ, Goldman CR (1990) The zooplankton-phytoplankton interface in lakes of contrasting trophic status: an experimental comparison. Hydrobiologia 200(201):69–82. https://doi.org/10.1007/BF02530330
Evans MS, Eadie BJ, Glover GM (1998) Sediment trap studies in southeastern Lake Michigan: fecal pellet express or the more traveled route? J Great Lake Res 24:555–568. https://doi.org/10.1016/S0380-1330(98)70844-5
Goldman CR (1960) Primary productivity and limiting factors in the three lakes of the Alaskan Peninsula. Ecol Monogr 30:207–230. https://doi.org/10.2307/1948552
Goldman CR (1988) Primary productivity, nutrients, and transparency during the early onset of eutrophication in ultra-oligotrophic Lake Tahoe, California-Nevada. Limnol Oceanogr 33:1321–1333. https://doi.org/10.4319/lo.1988.33.6.1321
Goldman CR (2000) Four decades of change in two subalpine lakes. Verh Internat Verein Limnol 27:7–26. https://doi.org/10.1080/03680770.1998.11901200
Goldman CR, Morgan MD, Threlkeld ST, Angeli N (1979) A population dynamics analysis of the cladoceran disappearance from Lake Tahoe, California-Nevada. Limnol Oceanogr 24:289–297. https://doi.org/10.4319/lo.1979.24.2.0289
Goldman CR, Jassby AD, Hackley SH (1993) Decadal, interannual, and seasonal variability in enrichment bioassays at Lake Tahoe, California-Nevada, USA. Can J Fish Aquat Sci 50:1489–1496. https://doi.org/10.1139/f93-170
Grossnickle NE (1982) Feeding habits of Mysis relicta—an overview. Hydrobiologia 93:101–107. https://doi.org/10.1007/BF00008103
Heyvaert AC, Nover DM, Caldwell TG, Trowbridge WB, Schladow SG, Reuter JE (2011) Assessment of particle size analysis in the Lake Tahoe Basin. Prepared by Desert Research Institute, Division of Hydrologic Sciences and University of California, Davis, Tahoe Environmental Research Center. Submitted to the USDA Forest Service Pacific Southwest Research Station. 165 pp.
Ho JC, Michalak AM, Pahlevan N (2019) Widespread global increase in intense lake phytoplankton blooms since the 1980s. Nature 574:667–670. https://doi.org/10.1038/s41586-019-1648-7
Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2006) A Lego system for conditional inference. Am Stat 60(3):257–263. https://doi.org/10.1198/000313006X118430
Jari Oksanen F, Guillaume B, Michael F, Roeland K, Pierre L, Dan McGlinn PRM, O'Hara RB, Simpson GL, Peter S, Henry M, Stevens H, Eduard S, Helene W (2019) Vegan: community ecology package. R package version 2.5–6. https://CRAN.R-project.org/package=vegan
Jeppesen E, Jensen J, Jensen C, Faafeng B, Hessen DO, Sondergaard M, Lauridsen T, Brettum P, Christofferson K (2003) The impact of nutrient state and lake depth on top-down control in the Pelagic Zone of Lakes: a study of 466 Lakes from the temperate zone to the arctic. Ecosystems 6:313–325. https://doi.org/10.1007/PL00021503
Johannsson OE, Leggett MF, Rudstam LG, Servos MR, Mohammadian MA, Gal G, Dermott RM, Hesslein RH (2001) Diet of Mysis relicta in Lake Ontario as revealed by stable isotope and gut content analysis. Can J Fish Aquat Sci 58:1975–1986. https://doi.org/10.1139/cjfas-58-10-1975
Kagami M, Yoshida T, Gurung TB, Urabe J (2002) Direct and indirect effects of zooplankton on algal composition in in situ grazing experiments. Oecologia 133:356–363
Kirk KL (1991) Suspended clay reduces Daphnia feeding rate. Freshw Biol 25:357–365. https://doi.org/10.1111/j.1365-2427.1991.tb00498.x
Lampert W (1978) Release of dissolved organic carbon by grazing zooplankton. Limnol Oceanogr 23:831–834. https://doi.org/10.4319/lo.1978.23.4.0831
Lampert W (1987) Feeding and nutrition in Daphnia. In: Peters RH, De Bernardi R (eds) Daphnia. Mem Istit ital Idrobiol 45:143–192
Lampert W, Fleckner W, Rai H, Taylor BE (1986) Phytoplankton control by grazing zooplankton: a study on the spring clear-water phase. Limnol Oceanogr 31:478–490. https://doi.org/10.4319/lo.1986.31.3.0478
Lamphake LJ, Hannah SA, Cohen JM (1967) Automated analysis for nitrate by hydrazine reduction. Water Res 1:205–216. https://doi.org/10.1016/0043-1354(67)90011-5
Lasenby DC, Langford RR (1973) Feeding and assimilation of Mysis relicta. Limnol Oceanogr 18:280–285. https://doi.org/10.4319/lo.1973.18.2.0280
Lesutiene J, Gorokhova E, Gasiunate ZR, Razinkovas A (2007) Isotopic evidence for zooplankton as an important food source for the mysid Paramysis lacustris in the Curonian Lagoon, the South-Eastern Baltic Sea. Estuar Coast Shelf Sci 73:73–80. https://doi.org/10.1016/j.ecss.2006.12.010
Linden E, Kuosa H (2004) Effects of grazing and excretion by pelagic mysids (Mysis spp.) on the size structure and biomass on the phytoplankton community. Hydrobiologia 514:73–78. https://doi.org/10.1023/B:hydr.0000018207.42449.fb
Madeira PT, Brooks AS, Seale DB (1982) Excretion of total phosphorus, dissolved reactive phosphorus, ammonia, and urea by Lake Michigan Mysis relicta. Hydrobiologia 93:145–154. https://doi.org/10.1007/BF00008107
Mauchline J (1998) The biology of calanoid copepods. Adv Mar Biol 33:1–701
McCarthy V, Donohue I, Irvine K (2006) Field evidence for stoichiometric relationships between zooplankton and N and P availability in a shallow calcareous lake. Freshw Biol 51:1589–1604. https://doi.org/10.1111/j.1365.2427.2006.01599.x
McCoy A (2015) An assessment of the impact of non-native lake trout Salvelinus namaycush and Mysis diluviana on the growth and survival of Pelagic Planktivores in Lake Tahoe. Thesis, University of Washington.
Metillo EB (1995) Comparative Feeding Behaviour and Morphology of Mysids (Crustacea: Mysidacea). Dissertation, University of Tasmania.
Morgan MD (1981) Abundance, life history, and growth of introduced populations of the opossum shrimp (Mysis relicta) in subalpine California lakes. Verh Internat Verein Limnol 21:339–345. https://doi.org/10.1139/f81-134
Morgan MD, Threlkeld ST (1982) Size-dependent horizontal migration of Mysis relicta. Hydrobiol 93:63–68
Morgan MD, Goldman CR, Richards RC (1981) Impact of introduced populations of Mysis relicta on zooplankton in oligotrophic subalpine lakes. Verh Internat Verein Limnol 21:339–345. https://doi.org/10.1080/03680770.1980.11897004
Murphy J, Riley JP (1962) A modified single-solution method for the determination of phosphate in natural waters. Analytica Chemica Acta 27:31–36. https://doi.org/10.1016/S0003-2670(00)88444-5
Ramcharan CW, Sprules WG, Nero RW (1985) Notes on the tactile feeding behaviour of Mysis relicta Loven (Malacostraca: Mysidacea). Verh Internat Verein Limnol 22:3215–3219. https://doi.org/10.1080/03680770.1983.11897862
Richards RC, Goldman CR, Frantz TC, Wickwire R (1975) Where have all the Daphnia gone? The decline of a major cladoceran in Lake Tahoe, California-Nevada. Verh Internat Verein Limnol 16:835–842. https://doi.org/10.1080/03680770.1974.11896129
Richards RC, Goldman CR, Byron E, Levitan C (1991) The Mysids and lake trout of Lake Tahoe: A 25-year history of changes in the fertility, Plankton, and fishery of an Alpine Lake. Am Fish Soc Symp 9:30–38
Richerson PJ (1969) Community Ecology of the Lake Tahoe Plankton. Dissertation, University of California, Davis.
Rigler FH (1971) Laboratory measurements of processes involved in secondary production: zooplankton. In: Edmondson WT, Winberg GG (eds) A manual on methods for the assessment of secondary productivity in fresh waters. Blackwell Scientific Publishers, Oxford, pp 228–250
Ross SM (2014) Introduction to probability and statistics for engineers and scientists, 5th edn. Elsevier, Amsterdam
Rudstam LG, Knudsen FR, Balk H, Gideon G, Boscarino BT, Axenrot T (2008) Acoustic characterization of Mysis relicta at multiple frequencies. Can J Fish Aquat Sci. 65:2769–2779. https://doi.org/10.1139/F08-179
Rybock JT (1978) Mysis relicta (Loven) in Lake Tahoe: vertical distribution and nocturnal predation. Dissertation, University of California—Davis
Sawyer P (1985) The predatory behavior and distribution of Mysis relicta in Lake Tahoe, California-Nevada. Thesis, University of California—Davis
Schindler DW (2012) The dilemma of controlling cultural eutrophication of lakes. Proc R Soc B 279:4322–4333. https://doi.org/10.1098/rspb.2012.1032
Schindler DW, Hecky RE, Findlay DL, Stainton MP, Parker BR, Paterson MJ, Beaty KG, Lyng M, Kasian SEM (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proc Natl Acad Sci 105:11254–11258. https://doi.org/10.1073/pnas.0805108105
Schladow, S. G. 2019. Tahoe: State of the Lake Report 2019. UC Davis Tahoe Environmental Research Center.
Shapiro S, Wilk MB (1965) An analysis of variance test for normality (complete samples). Biometrika 52:591–611. https://doi.org/10.1093/biomet/52.3-4.591
Shurin JB (2000) Dispersal limitation, invasion resistance, and the structure of pond zooplankton communities. Ecology 81:3074–3086. https://doi.org/10.1890/0012-9658(2000)081[3074:DLIRAT]2.0.CO;2
Sierszen ME, Brooks AS (1982) The release of dissolved organic carbon as a result of diatom fragmentation during feeding by Mysis relicta. Hydrobiologia 93:155–161. https://doi.org/10.1007/BF00008108
Smith VH (2003) Eutrophication of freshwater and coastal marine ecosystems a global problem. Environ Sci Pollut Res 10:126–139. https://doi.org/10.1065/esor2002.12.142
Snedecor GW, Cochran WG (1989) Statistical methods, 8th edn. Iowa State University Press, Ames
Steeman-Nielsen ES (1952) The use of radio-active carbon (C14) for measuring organic production in the sea. J Cons Int Expl Mer 18:117–140. https://doi.org/10.1093/icesjms/18.2.117
Swift TJ, Perez-Losada J, Schladow SG, Reuter JE, Jassby AD, Goldman CR (2006) Water clarity modeling in Lake Tahoe: linking suspended matter characteristics to Secchi depth. Aquat Sci 68:1–15. https://doi.org/10.1007/s00027-005-0798-x
Threlkeld ST, Rybock JT, Morgan MD, Folt CL, Goldman CR (1980) The effects of an introduced invertebrate predator and food resource variation on zooplankton dynamics in an ultraoligotrophic lake. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. University Press of New England, Oxford, pp 555–568
Turner JT, Ferrante JG (1979) Zooplankton fecal pellets in aquatic ecosystems. Bioscience 29:670–677. https://doi.org/10.2307/1307591
U.S. Environmental Protection Agency (1993) Method 350.1: determination of ammonia nitrogen by semi-automated colorimetry. Environmental Monitoring Systems Laboratory, Revision 2.0.
Vadeboncoeur Y, Jeppesen E, Vander Zanden MJ, Schierup H, Christoffersen K, Lodge DM (2003) From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnol Oceanogr 48:1408–1414. https://doi.org/10.4319/lo.2003.48.4.1408
Van Duyn-Henderson JA, Lasenby DC (1986) Zinc and cadmium transport by the vertically migrating opossum shrimp, Mysis relicta. Can J Fish Aquat Sci 43:1726–1732
VanLandingham SL (1987) Observations on the ecology and trophic status of Lake Tahoe (Nevada and California, USA) Based On The Algae From Three Independent Surveys (1965–1985). Great Basin Nat 47:562–582
Vrede K, Vrede T, Isaksson A, Karlsson A (1999) Effects of nutrients (phosphorus, nitrogen, and carbon) and zooplankton on bacterioplankton and phytoplankton—a seasonal study. Limnol Oceanogr 44:1616–1624
Walve J, Larsson U (1999) Carbon, nitrogen and phosphorus stoichiometry of crustacean zooplankton in the Baltic Sea: implications for nutrient recycling. J Plankton Res 21:2309–2321. https://doi.org/10.1093/plankt/21.12.2309
Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edn. Academic Press, San Diego
Zollner E, Santer B, Boersma M, Hoppe H, Jurgens K (2003) Cascading predation effects of Daphnia and copepods on microbial food web components. Freshw Biol 48:2174–2193. https://doi.org/10.1046/j.1365-2426.2003.01158.x
Acknowledgements
Drs. Steve Sadro (UC Davis) and Michael Brett (University of Washington) provided feedback in the design of the experiments. Dr. Kevin Shoemaker (University of Nevada, Reno) provided recommendations for the statistical analyses. Dan Shaw and Nita Suparek coordinated access and field collections from Emerald Bay. Cam McKay from the Glenbrook Water Facility assisted in water collections for the Lake Tahoe experiment. The following people assisted in the two semi-natural experiments: Dr. Tim Caldwell, Karly Feher, Emily Carlson, Dr. Emmanuele Ziaco, Elizabeth Everest, Dr. Facundo Scordo, Dr. Ed Krynak, James Simmons, Josh Culpepper, Loren Secor, Anna Cole, Shaye McMillen, and Logan Gregory. Aldo San Pedro assisted with software processing of the figures. Bonnie Teglas managed the funding for this project.
Funding
This work was funded by a grant from the California Tahoe Conservancy to G. Schladow (UC Davis Tahoe Environmental Research Center) and a subaward to S. Chandra. Additionally, Z. Bess received the Student Scholarship from the California Lake Management Society and the Paul A. Bosace Graduate Scholarship from the University of Nevada, Reno.
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ZB—designed experiment; conducted experiment; analyzed data; wrote manuscript. SC—assisted in experimental design; conducted experiment; edited manuscript and data analysis; secured funding for the project. ES—conducted experiment; edited manuscript. SK—conducted experiment; edited manuscript. AH—edited manuscript and assisted in data analysis.
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Bess, Z., Chandra, S., Suenaga, E. et al. Zooplankton influences on phytoplankton, water clarity, and nutrients in Lake Tahoe. Aquat Sci 83, 26 (2021). https://doi.org/10.1007/s00027-020-00772-6
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DOI: https://doi.org/10.1007/s00027-020-00772-6