, Volume 178, Issue 3, pp 875–885 | Cite as

Autumn leaf subsidies influence spring dynamics of freshwater plankton communities

  • Samuel B. FeyEmail author
  • Andrew N. Mertens
  • Kathryn L. Cottingham
Community ecology - Original research


While ecologists primarily focus on the immediate impact of ecological subsidies, understanding the importance of ecological subsidies requires quantifying the long-term temporal dynamics of subsidies on recipient ecosystems. Deciduous leaf litter transferred from terrestrial to aquatic ecosystems exerts both immediate and lasting effects on stream food webs. Recently, deciduous leaf additions have also been shown to be important subsidies for planktonic food webs in ponds during autumn; however, the inter-seasonal effects of autumn leaf subsidies on planktonic food webs have not been studied. We hypothesized that autumn leaf drop will affect the spring dynamics of freshwater pond food webs by altering the availability of resources, water transparency, and the metabolic state of ponds. We created leaf-added and no-leaf-added field mesocosms in autumn 2012, allowed mesocosms to ice-over for the winter, and began sampling the physical, chemical, and biological properties of mesocosms immediately following ice-off in spring 2013. At ice-off, leaf additions reduced dissolved oxygen, elevated total phosphorus concentrations and dissolved materials, and did not alter temperature or total nitrogen. These initial abiotic effects contributed to higher bacterial densities and lower chlorophyll concentrations, but by the end of spring, the abiotic environment, chlorophyll and bacterial densities converged. By contrast, zooplankton densities diverged between treatments during the spring, with leaf additions stimulating copepods but inhibiting cladocerans. We hypothesized that these differences between zooplankton orders resulted from resource shifts following leaf additions. These results suggest that leaf subsidies can alter both the short- and long-term dynamics of planktonic food webs, and highlight the importance of fully understanding how ecological subsidies are integrated into recipient food webs.


Terrestrial-aquatic linkages Food webs Phenology Ponds Zooplankton 



We thank A. L. Ritger, J. V. Trout-Haney, and R. L. Wood for field and laboratory assistance and S. Stokoe for management of the Dartmouth Organic Farm. Comments from J. J. Gilbert, R. O. Hall, E. T. Irwin, and two anonymous reviewers greatly improved this manuscript. An Environmental Protection Agency STAR Fellowship and James S. McDonnell Complexity Postdoctoral Fellowship to S. B. F. and National Science Foundation grants DEB-1110369 to S. B. F. and K. L. C. and EF-0842267 to K. L. C., EF-0842112 to H. A. Ewing, and EF-0842125 to K. C. Weathers funded this research.


  1. Anderson N, Sedell J (1979) Detritus processing by macroinvertebrates in stream ecosystems. Annu Rev Entomol 24:351–377. doi: 10.1146/annurev.en.24.010179.002031 CrossRefGoogle Scholar
  2. Batzer DP, Palik BJ (2007) Variable response by aquatic invertebrates to experimental manipulations of leaf litter input into seasonal woodland ponds. Fundam Appl Limnol 168:155–162. doi: 10.1127/1863-9135/2007/0168-0155 CrossRefGoogle Scholar
  3. Baxter CV, Fausch KD, Carl Saunders W (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshwater Biol 50:201–220. doi: 10.1111/j.1365-2427.2004.01328.x CrossRefGoogle Scholar
  4. Benfield EF, Webster JR, Tank JL, Hutchens JJ (2001) Long-term patterns in leaf breakdown in streams in response to watershed logging. Int Rev Hydrobiol 86:467–474. doi: 10.1002/1522-2632(200107)86:4/5<467:AID-IROH467>3.0.CO;2-1 CrossRefGoogle Scholar
  5. Berggren M, Ziegler SE, St-Gelais NF, Beisner BE, del Giorgio PA (2014) Contrasting patterns of allochthony among three major groups of crustacean zooplankton in boreal and temperate lakes. Ecology 95:1947–1959. doi: 10.1890/13-0615.1 PubMedCrossRefGoogle Scholar
  6. Bertilsson S, Burgin A, Carey CC, Fey SB, Grossart H, Grubisic LM, Jones ID, Kirillin G, Lennon JT, Shade A, Smyth RL (2013) The under-ice microbiome of seasonally frozen lakes. Limnol Oceanogr 58:1998–2012. doi: 10.4319/lo.2013.58.6.1998 CrossRefGoogle Scholar
  7. Bolsenga S, Vanderploeg H (1992) Estimating photosynthetically available radiation into open and ice-covered fresh-water lakes from surface characteristics—a high transmittance case study. Hydrobiologia 243:95–104. doi: 10.1007/BF00007024 CrossRefGoogle Scholar
  8. Brandstetter A, Sletten RS, Mentler A, Wenzel WW (1996) Estimating dissolved organic carbon in natural waters by UV absorbance (254 nm). Z Pflanzenernähr Bodenkd 159:605–607. doi: 10.1002/jpln.1996.3581590612 CrossRefGoogle Scholar
  9. Cederholm C, Kunze M, Murota T, Sibatani A (1999) Pacific salmon carcasses: essential contributions of nutrients and energy for aquatic and terrestrial ecosystems. Fisheries 24:6–15. doi: 10.1577/1548-8446(1999)024<0006:PSC>2.0.CO;2 CrossRefGoogle Scholar
  10. Cole J, Carpenter S, Pace M, Van de Bogert M, Kitchell J, Hodgson J (2006) Differential support of lake food webs by three types of terrestrial organic carbon. Ecol Lett 9:558–568. doi: 10.1111/j.1461-0248.2006.00898.x PubMedCrossRefGoogle Scholar
  11. Cotrufo M, Ineson P (1996) Elevated CO2 reduces field decomposition rates of Betula pendula (Roth) leaf litter. Oecologia 106:525–530. doi: 10.1007/BF00329711 CrossRefGoogle Scholar
  12. Cottingham KL, Narayan L (2013) Subsidy quantity and recipient community structure mediate plankton responses to autumn leaf drop. Ecosphere 4:7 art89CrossRefGoogle Scholar
  13. Crumpton WG, Isenhart TM, Mitchell PD (1992) Nitrate and organic N analyses with second-derivative spectroscopy. Limnol Oceanogr 37:907–913. doi: 10.4319/lo.1992.37.4.0907 CrossRefGoogle Scholar
  14. Dzialowski AR, Rzepecki M, Kostrzewska-Szlakowska I, Kalinowska K, Palash A, Lennon JT (2014). Are the abiotic and biotic characteristics of aquatic mesocosms representative of in situ conditions? J Limnol 73 doi: 10.4081/jlimnol.2014.721
  15. Earl JE, Castello PO, Cohagen KE, Semlitsch RD (2014) Effects of subsidy quality on reciprocal subsidies: how leaf litter species changes frog biomass export. Oecologia 175:209–218. doi: 10.1007/s00442-013-2870-x PubMedCrossRefGoogle Scholar
  16. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–1142. doi: 10.1111/j.1461-0248.2007.01113.x PubMedCrossRefGoogle Scholar
  17. Fey SB, Cottingham KL (2012) Thermal sensitivity predicts the establishment success of non-native species in a mesocosm warming experiment. Ecology 93:2313–2320. doi: 10.1890/12-0609.1 PubMedCrossRefGoogle Scholar
  18. Fey SB, Mertens AN, Beversdorf LJ, McMahon KD, Cottingham KL (2015). Recognizing cross-ecosystem responses to changing temperatures: soil warming impacts pelagic food webs. Oikos doi: 10.1111/oik.01939
  19. France R, Peters R (1995) Predictive model of the effects on lake metabolism of decreased airborne litterfall through riparian deforestation. Conserv Biol 9:1578–1586. doi: 10.1046/j.1523-1739.1995.09061578.x CrossRefGoogle Scholar
  20. Granéli W, Lindell M, De Faria BM, de Assis Esteves F (1998) Photoproduction of dissolved inorganic carbon in temperate and tropical lakes–dependence on wavelength band and dissolved organic carbon concentration. Biogeochemistry 43:175–195. doi: 10.1023/A:1006042629565 CrossRefGoogle Scholar
  21. Gratton C, Donaldson J, Zanden MJV (2008) Ecosystem linkages between lakes and the surrounding terrestrial landscape in northeast Iceland. Ecosystems 11:764–774CrossRefGoogle Scholar
  22. Greig HS, Kratina P, Thompson PL, Palen WJ, Richardson JS, Shurin JB (2012) Warming, eutrophication, and predator loss amplify subsidies between aquatic and terrestrial ecosystems. Glob Change Biol 18:504–514. doi: 10.1111/j.1365-2486.2011.02540.x CrossRefGoogle Scholar
  23. Guyette RP, Cole WG (1999) Age characteristics of coarse woody debris (Pinus strobus) in a lake littoral zone. Can J Fish Aquat Sci 56:496–505CrossRefGoogle Scholar
  24. Hieber M, Gessner MO (2002) Contribution of stream detrivores, fungi, and bacteria to leaf breakdown based on biomass estimates. Ecology 83:1026–1038CrossRefGoogle Scholar
  25. Higgs ND, Gates AR, Jones DOB (2014) Fish food in the deep sea: revisiting the role of large food-falls. PLoS One 9:e96016. doi: 10.1371/journal.pone.0096016 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Hongve D (1999) Production of dissolved organic carbon in forested catchments. J Hydrol 224:91–99. doi: 10.1016/S0022-1694(99)00132-8 CrossRefGoogle Scholar
  27. Karlsson J, Bystrom P, Ask J, Ask P, Persson L, Jansson M (2009) Light limitation of nutrient-poor lake ecosystems. Nature 460:506–509. doi: 10.1038/nature08179 PubMedCrossRefGoogle Scholar
  28. Kelly PT, Solomon CT, Weidel BC, Jones SE (2014) Terrestrial carbon is a resource, but not a subsidy, for lake zooplankton. Ecology 95:1236–1242. doi: 10.1890/13-1586.1 PubMedCrossRefGoogle Scholar
  29. Kirillin G, Leppäranta M, Terzhevik A, Granin N, Bernhardt J, Engelhardt C, Efremova T, Golosov S, Palshin N, Sherstyankin P (2012) Physics of seasonally ice-covered lakes: a review. Aquat Sci 74:659–682CrossRefGoogle Scholar
  30. Larsson P, Wathne I (2006) Swim or rest during the winter—what is best for an alpine daphnid? Arch Hydrobiol 167:265–280. doi: 10.1127/0003-9136/2006/0167-0265 CrossRefGoogle Scholar
  31. Leech DM, Williamson CE (2000) Is tolerance to UV radiation in zooplankton related to body size, taxon, or lake transparency? Ecol Appl 10:1530–1540. doi: 10.1890/1051-0761(2000)010[1530:ITTURI]2.0.CO;2 CrossRefGoogle Scholar
  32. Lennon JT, Hamilton SK, Muscarella ME, Grandy AS, Wickings K, Jones SE (2013) A source of terrestrial organic carbon to investigate the browning of aquatic ecosystems. PLoS One 8:e75771PubMedCentralPubMedCrossRefGoogle Scholar
  33. Loiterton B, Sundbom M, Vrede T (2004) Separating physical and physiological effects of temperature on zooplankton feeding rate. Aquat Sci 66:123–129. doi: 10.1007/s00027-003-0668-3 CrossRefGoogle Scholar
  34. Marcarelli AM, Baxter CV, Mineau MM, Hall RO Jr (2011) Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–1225. doi: 10.1890/10-2240.1 PubMedCrossRefGoogle Scholar
  35. Marczak LB, Richardson JS (2008) Growth and development rates in a riparian spider are altered by asynchrony between the timing and amount of a resource subsidy. Oecologia 156:249–258PubMedCrossRefGoogle Scholar
  36. Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98:166–170. doi: 10.1073/pnas.98.1.166 PubMedCentralPubMedCrossRefGoogle Scholar
  37. Odum E, Finn J, Franz E (1979) Perturbation-theory and the subsidy-stress gradient. Bioscience 29:349–352. doi: 10.2307/1307690 CrossRefGoogle Scholar
  38. Oertli B (1993) Leaf-litter processing and energy-flow through macroinvertebrates in a woodland pond (Switzerland). Oecologia 96:466–477. doi: 10.1007/BF00320503 CrossRefGoogle Scholar
  39. Polis G, Anderson W, Holt R (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316. doi: 10.1146/annurev.ecolsys.28.1.289 CrossRefGoogle Scholar
  40. Pope R, Gordon A, Kaushik N (1999) Leaf litter colonization by invertebrates in the littoral zone of a small oligotrophic lake. Hydrobiologia 392:99–112. doi: 10.1023/A:1003537232319 CrossRefGoogle Scholar
  41. Porter K, Feig Y (1980) The use of DAPI for identifying and counting aquatic microflora. Limnol Oceanogr 25:943–948CrossRefGoogle Scholar
  42. Quinn G, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  43. Richardson J (1992) Food, microhabitat, or both? macroinvertebrate use of leaf accumulations in a montane stream. Freshwater Biol 27:169–176. doi: 10.1111/j.1365-2427.1992.tb00531.x CrossRefGoogle Scholar
  44. Rubbo M, Kiesecker J (2004) Leaf litter composition and community structure: translating regional species changes into local dynamics. Ecology 85:2519–2525. doi: 10.1890/03-0653 CrossRefGoogle Scholar
  45. Rubbo MJ, Cole JJ, Kiesecker JM (2006) Terrestrial subsidies of organic carbon support net ecosystem production in temporary forest ponds: evidence from an ecosystem experiment. Ecosystems 9:1170–1176. doi: 10.1007/s10021-005-0009-6 CrossRefGoogle Scholar
  46. Rubbo MJ, Belden LK, Kiesecker JM (2008) Differential responses of aquatic consumers to variations in leaf-litter inputs. Hydrobiologia 605:37–44. doi: 10.1007/s10750-008-9298-z CrossRefGoogle Scholar
  47. Sabo J, Power M (2002) Numerical response of lizards to aquatic insects and short-term consequences for terrestrial prey. Ecology 83:3023–3036. doi: 10.2307/3071839 CrossRefGoogle Scholar
  48. Schindler DE, Armstrong JB, Bentley KT, Jankowski K, Lisi PJ, Payne LX (2013) Riding the crimson tide: mobile terrestrial consumers track phenological variation in spawning of an anadromous fish. Biol Lett 9:20130048. doi: 10.1098/rsbl.2013.0048 PubMedCentralPubMedCrossRefGoogle Scholar
  49. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol Annu Rev 41:311–354Google Scholar
  50. Swan C, Palmer M (2004) Leaf diversity alters litter breakdown in a piedmont stream. J N Am Benthol Soc 23:15–28. doi: 10.1899/08873593(2004)023<0015:LDALBI>2.0.CO;2 CrossRefGoogle Scholar
  51. Swan C, Palmer M (2006) Composition of species leaf litter alters stream detritivore growth, feeding activity and leaf breakdown. Oecologia 147:469–478. doi: 10.1007/s00442-005-0297-8 PubMedCrossRefGoogle Scholar
  52. Takimoto G, Iwata T, Murakami M (2002) Seasonal subsidy stabilizes food web dynamics: balance in a heterogeneous landscape. Ecol Res 17:433–439. doi: 10.1046/j.1440-1703.2002.00502.x CrossRefGoogle Scholar
  53. Takimoto G, Iwata T, Murakami M (2009) Timescale hierarchy determines the indirect effects of fluctuating subsidy inputs on in situ resources. Am Nat 173:200–211. doi: 10.1086/595759 PubMedCrossRefGoogle Scholar
  54. Twiss MR, McKay RML, Bourbonniere RA, Bullerjahn GS, Carrick HJ, Smith REH, Winter JG, D’souza NA, Furey PC, Lashaway AR, Saxton MA, Wilhelm SW (2012) Diatoms abound in ice-covered Lake Erie: an investigation of offshore winter limnology in Lake Erie over the period 2007–2010. J Great Lakes Res 38:18–30. doi: 10.1016/j.jglr.2011.12.008 CrossRefGoogle Scholar
  55. Ueveges V, Tapolczai K, Krienitz L, Padisak J (2012) Photosynthetic characteristics and physiological plasticity of an Aphanizomenon flos-aquae (Cyanobacteria, Nostocaceae) winter bloom in a deep oligo-mesotrophic lake (Lake Stechlin, Germany). Hydrobiologia 698:263–272. doi: 10.1007/s10750-012-1103-3 CrossRefGoogle Scholar
  56. Vanderploeg HA, Ludsin SA, Cavaletto JF, Hoeoek TO, Pothoven SA, Brandt SB, Liebig JR, Lang GA (2009) Hypoxic zones as habitat for zooplankton in Lake Erie: refuges from predation or exclusion zones? J Exp Mar Biol Ecol 381:S108–S120. doi: 10.1016/j.jembe.2009.07.015 CrossRefGoogle Scholar
  57. Wallace J, Eggert S, Meyer J, Webster J (1999) Effects of resource limitation on a detrital-based ecosystem. Ecol Monogr 69:409–442. doi:10.1890/0012-9615(1999)069[0409:EORLOA]2.0.CO;2CrossRefGoogle Scholar
  58. Webster J, Meyer J (1997) Stream organic matter budgets. J N Am Benthol Soc 16:3–4. doi: 10.2307/1468223 CrossRefGoogle Scholar
  59. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll-a in the presence of chlorophyll-b and pheopigments. Limnol Oceanogr 39:1985–1992CrossRefGoogle Scholar
  60. Wilkinson GM, Carpenter SR, Cole JJ, Pace ML, Yang C (2013) Terrestrial support of pelagic consumers: patterns and variability revealed by a multilake study. Freshwat Biol 58:2037–2049. doi: 10.1111/fwb.12189 CrossRefGoogle Scholar
  61. Williamson CE, Reid JW (2009) Copepoda. In: Thorp JH, Covich AP (eds) Ecology and classification of North American freshwater invertebrates. Academic Press, San DiegoGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Samuel B. Fey
    • 1
    • 2
    Email author
  • Andrew N. Mertens
    • 1
  • Kathryn L. Cottingham
    • 1
  1. 1.Department of Biological SciencesDartmouth CollegeHanoverUSA
  2. 2.Department of Ecology and Evolutionary BiologyYale UniversityNew HavenUSA

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