Skip to main content

The Influence of Leaf Type on Carbon and Nitrogen Assimilation by Aquatic Invertebrate Communities: A New Perspective on Trophic Efficiency

Ecosystems volume 24, pages 788–805 (2021)Cite this article

Abstract

Despite abounding evidence that leaf litter traits can predict decomposition rate, the way these traits influence trophic efficiency and element transfer to higher trophic levels is not resolved. Here, we used litter labeled with 13C and 15N stable isotopes to trace fluxes of litter C and N from four leaf types to freshwater invertebrate communities. We measured absolute (mg C or N) and relative assimilation (percentage of litter C or N incorporated into invertebrate biomass relative to C and N lost during decomposition). Four patterns emerged: (1) Invertebrate communities assimilated more C and N from slowly decomposing litter than communities feeding on rapidly decomposing litter; (2) absolute assimilation of both C and N in leaf packs was positively correlated with the relative biomass of invertebrate taxa in leaf packs; (3) Chironomidae larvae, which colonize packs in the early decomposition stages, assimilated the most C and N by the end of the 35-day experiment; and (4) most taxa, spanning five functional feeding groups (collector–gatherers, shredders, collector–filterers, scrapers, and predators), showed similar patterns in both absolute and relative assimilation across leaf types. These results challenge traditional views of litter quality by demonstrating that trophic efficiency is negatively associated with decomposition rate across these four leaf types.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

References

  • Alonso A, González-Muñoz N, Castro-Díez P. 2010. Comparison of leaf decomposition and macroinvertebrate colonization between exotic and native trees in a freshwater ecosystem. Ecol Res 25:647–53.

    Google Scholar 

  • Anderson NH, Lehmkuhl DM. 1968. Catastrophic drift of insects in a woodland stream. Ecology 49:198–206.

    Google Scholar 

  • Barlöcher F. 1980. Leaf-eating invertebrates as competitors of aquatic hyphomycetes. Oecologia 47:303–6.

    PubMed  Google Scholar 

  • Benke AC. 1998. Production dynamics of riverine chironomids: extremely high biomass turnover rates of primary consumers. Ecology 79:899–910.

    Google Scholar 

  • Benke AC, Huryn AD, Smock LA, Wallace JB. 1999. Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States. J N Am Benthol Soc 18:308–43.

    Google Scholar 

  • Brittain JE, Eikeland TJ. 1988. Invertebrate drift—a review. Hydrobiologia 166:77–93.

    Google Scholar 

  • Canhoto C, Graça MAS. 1995. Food value of introduced eucalypt leaves for a Mediterranean stream detritivore: Tipula lateralis. Freshw Biol 34:209–14.

    Google Scholar 

  • Cheever BM, Webster JR, Bilger EE, Thomas SA. 2013. The relative importance of exogenous and substrate-derived nitrogen for microbial growth during leaf decomposition. Ecology 94:1614–25.

    CAS  PubMed  Google Scholar 

  • Chung N, Suberkropp K. 2009. Contribution of fungal biomass to the growth of the shredder, Pycnopsyche gentilis (Trichoptera: Limnephilidae). Freshw Biol 54:2212–24.

    CAS  Google Scholar 

  • Compson ZG, Adams KJ, Edwards JA, Maestas JM, Whitham TG, Marks JC. 2013. Leaf litter quality affects aquatic insect emergence: contrasting patterns from two foundation trees. Oecologia 173:507–19.

    PubMed  Google Scholar 

  • Compson ZG, Hungate BA, Koch GW, Hart SC, Maestas JM, Adams KJ, Whitham TG, Marks JC. 2015. Closely related tree species differentially influence the transfer of carbon and nitrogen from leaf litter up the aquatic food web. Ecosystems 18:186–201.

    CAS  Google Scholar 

  • Compson ZG, Hungate BA, Whitham TG, Meneses N, Busby PE, Wojtowicz T, Ford AC, Adams KJ, Marks JC. 2016. Plant genotype influences aquatic-terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7:e01331. https://doi.org/10.1002/ecs2.1331.

    Article  Google Scholar 

  • Compson ZG, Hungate BA, Whitham TG, Koch GW, Dijkstra P, Siders AC, Wojtowicz T, Jacobs R, Rakestraw DN, Allred KE, Sayer CK. 2018. Linking tree genetics and stream consumers: isotopic tracers elucidate controls on carbon and nitrogen assimilation. Ecology 99:1759–70.

    PubMed  Google Scholar 

  • Cornwell WK, Cornelissen JH, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM. 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–71.

    PubMed  Google Scholar 

  • Cross WF, Johnson BR, Wallace JB, Rosemond AD. 2005. Ecological stoichiometry in freshwater benthic systems: recent progress and perspectives. Limnol Oceanogr 50:1730–9.

    CAS  Google Scholar 

  • Cross WF, Wallace JB, Rosemond AD, Eggert SL. 2006. Whole-system nutrient enrichment increases secondary production in a detritus-based ecosystem. Ecology 87:1556–65.

    CAS  PubMed  Google Scholar 

  • Demi LM, Benstead JP, Rosemond AD, Maerz JC. 2018. Litter P content drives consumer production in detritus-based streams spanning an experimental N: P gradient. Ecology 99:347–59.

    PubMed  Google Scholar 

  • Dickman EM, Newell JM, González MJ, Vanni MJ. 2008. Light, nutrients, and food-chain length constrain planktonic energy transfer efficiency across multiple trophic levels. Proc Natl Acad Sci 105:18408–12.

    CAS  PubMed  Google Scholar 

  • Driebe EM, Whitham TG. 2000. Cottonwood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123:99–107.

    CAS  PubMed  Google Scholar 

  • Evans-White MA, Halvorson HM. 2017. Comparing the ecological stoichiometry in green and brown food webs—a review and meta-analysis of freshwater food webs. Front Microbiol 8:1184.

    PubMed  PubMed Central  Google Scholar 

  • Fioretto A, Di Nardo C, Papa S, Fuggi A. 2005. Lignin and cellulose degradation and nitrogen dynamics during decomposition of three leaf litter species in a Mediterranean ecosystem. Soil Biol Biochem 37:1083–91.

    CAS  Google Scholar 

  • Fogelman KJ, Bilger MD, Holt JR, Matlaga DP. 2018. Decomposition and benthic macroinvertebrate communities of exotic Japanese knotweed (Fallopia japonica) and American sycamore (Platanus occidentalus) detritus within the Susquehanna River. J Freshw Ecol 33:299–310.

    CAS  Google Scholar 

  • Fugère V, Andino P, Espinosa R, Anthelme F, Jacobsen D, Dangles O. 2012. Testing the stress-gradient hypothesis with aquatic detritivorous invertebrates: insights for biodiversity-ecosystem functioning research. J Anim Ecol 81:1259–67.

    PubMed  Google Scholar 

  • Fuller CL, Evans-White MA, Entrekin SA. 2015. Growth and stoichiometry of a common aquatic detritivore respond to changes in resource stoichiometry. Oecologia 117:837–48.

    Google Scholar 

  • Gessner MO, Chauvet E. 1994. Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75:1807–17.

    Google Scholar 

  • Golladay S, Webster J, Benfield EF. 1983. Factors affecting food utilization by a leaf shredding aquatic insect: leaf species and conditioning time. Ecography 6:157–62.

    Google Scholar 

  • Gonçalves JF, Graça MAS, Callisto M. 2006. Leaf-litter breakdown in 3 streams in temperate, Mediterranean, and tropical Cerrado climates. J N Am Benthol Soc 25:344–55.

    Google Scholar 

  • Graça MAS. 2001. The role of invertebrates on leaf litter decomposition in streams—a review. Int Rev Hydrobiol 86:383–93.

    Google Scholar 

  • Graça MAS, Cressa C, Gessner MO, Feio MJ, Callies KA, Barrios C. 2001. Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshw Biol 46:947–57.

    Google Scholar 

  • Grubbs SA, Cummins KW. 1994. Processing and macroinvertebrate colonization of black cherry (Prunus serotina) leaves in two streams differing in summer biota, thermal regime and riparian vegetation. Am Midl Nat 132:284–93.

    Google Scholar 

  • Halvorson HM, Scott JT, Sanders AJ, Evans-White MA. 2015. A stream insect detritivore violates common assumptions of threshold elemental ratio bioenergetics models. Freshw Sci 34:508–18.

    Google Scholar 

  • Halvorson HM, Sperfeld E, Evans-White MA. 2017. Quantity and quality limit detritivore growth: mechanisms revealed by ecological stoichiometry and co-limitation theory. Ecology 93:2995–3002.

    Google Scholar 

  • Hladyz S, Gessner MO, Giller PS, Pozo J, Woodward G. 2009. Resource quality and stoichiometric constraints on stream ecosystem functioning. Freshw Biol 54:957–70.

    CAS  Google Scholar 

  • Hirabayashi K, Wotton RS. 1998. Organic matter processing by chironomid larvae (Diptera: Chironomidae). Hydrobiologia 382:151–9.

    Google Scholar 

  • Humphreys WF. 1979. Production and respiration in animal populations. J Anim Ecol 48:427–53.

    Google Scholar 

  • Hutchens JJ, Benfield EF, Webster JR. 1997. Diet and growth of a leaf-shredding caddisfly in southern Appalachian streams of contrasting disturbance history. Hydrobiologia 346:193–201.

    Google Scholar 

  • Kinzig AP, Harte J. 1998. Selection of micro-organisms in a spatially explicit environment and implications for plant access to nitrogen. J Ecol 86:841–53.

    Google Scholar 

  • Kohlmeier S, Smits TH, Ford RM, Keel C, Harms H, Wick LY. 2005. Taking the fungal highway: mobilization of pollutant-degrading bacteria by fungi. Environ Sci Technol 39:4640–6.

    CAS  PubMed  Google Scholar 

  • Kominoski JS, Larranaga S, Richardson JS. 2012. Invertebrate feeding and emergence timing vary among streams along a gradient of riparian forest composition. Freshw Biol 57:759–72.

    CAS  Google Scholar 

  • Lake PS, Doeg TJ. 1985. Macroinvertebrate colonization of stones in two upland southern Australian streams. Hydrobiologia 126:199–211.

    Google Scholar 

  • LeRoy CJ, Marks JC. 2006. Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshw Biol 51:605–17.

    Google Scholar 

  • LeRoy CJ, Whitham TG, Wooley SC, Marks JC. 2007. Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. J N Am Benthol Soc 26:426–38.

    Google Scholar 

  • Lindeman RL. 1942. The trophic-dynamic aspect of ecology. Ecology 23:399–417.

    Google Scholar 

  • Makkonen M, Berg MP, Handa IT, Hättenschwiler S, van Ruijven J, van Bodegom PM, Aerts R. 2012. Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15:1033–41.

    PubMed  Google Scholar 

  • Manning DWP, Rosemond AD, Gulis V, Benstead JP, Kominoski JS, Maerz JC. 2016. Convergence of detrital stoichiometry predicts thresholds of nutrient-stimulated breakdown in streams. Ecol Appl 26:1745–57.

    PubMed  Google Scholar 

  • Marcarelli AM, Baxter CV, Mineau MM, Hall RO. 2011. Quantity and quality: unifying food web and ecosystem perspectives on the role of resource subsidies in freshwaters. Ecology 92:1215–25.

    PubMed  Google Scholar 

  • Marks JC. 2019. Revisiting the fates of dead leaves that fall into streams. Annu Rev Ecol Evolut Syst 50:547–68.

    Google Scholar 

  • McCune B, Grace JB, Urban DL. 2002. Analysis of ecological communities. Gleneden Beach (OR): MjM Software Design.

    Google Scholar 

  • McCune B, Mefford MJ. 2011. PC-ORD. v. 6. Multivariate analysis of ecological data. Gleneden Beach (OR): MjM Software.

    Google Scholar 

  • McDowell WH, Fisher SG. 1976. Autumnal processing of dissolved organic matter in a small woodland stream ecosystem. Ecology 57:561–9.

    Google Scholar 

  • Melillo JM, Aber JD, Muratore JF. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–6.

    CAS  Google Scholar 

  • Merritt RW, Cummins KW, Berg MB. 2008. An introduction to the aquatic insects of North America. Dubuque (IA): Kendall Hunt.

    Google Scholar 

  • Meyer JL. 1994. The microbial loop in flowing waters. Microb Ecol 28:195–9.

    CAS  PubMed  Google Scholar 

  • Minshall GW, Petersen RC, Nimz CF. 1985. Species richness in streams of different size from the same drainage basin. Am Nat 125:16–38.

    Google Scholar 

  • Motomori K, Mitsuhashi H, Nakano S. 2001. Influence of leaf litter quality on the colonization and consumption of stream invertebrate shredders. Ecol Res 16:173–82.

    Google Scholar 

  • Norman BC, Whiles MR, Collins SM, Flecker AS, Hamilton SK, Johnson SL, Rosi EJ, Ashkenas LR, Bowden WB, Crenshaw CL, Crowl T, Dodds WK, Hall RO, El-Sabaawi R, Griffiths NA, Marti E, McDowell WH, Peterson SD, Rantala HM, Riis T, Simon KS, Tank JL, Thomas SA, von Schiller D, Webster JR. 2017. Drivers of nitrogen transfer in stream food webs across continents. Ecology 98:3044–55.

    PubMed  Google Scholar 

  • Ostrofsky ML. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J N Am Benthol Soc 16:750–9.

    Google Scholar 

  • Pastor A, Compson ZG, Dijkstra P, Riera JL, Martí E, Sabater F, Hungate BA, Marks JC. 2014. Stream carbon and nitrogen supplements during leaf litter decomposition: contrasting patterns for two foundation species. Oecologia 176:1111–21.

    PubMed  Google Scholar 

  • Peckarsky BL. 1986. Colonization of natural substrates by stream benthos. Can J Fish Aquat Sci 43:700–9.

    Google Scholar 

  • Perry WB, Benfield EF, Perry SA, Webster JR. 1987. Energetics, growth, and production of a leaf-shredding stonefly in an Appalachian mountain stream. J N Am Benthol Soc 6:12–25.

    Google Scholar 

  • Petersen RC, Cummins KW. 1974. Leaf processing in a woodland stream. Freshw Biol 4:343–68.

    Google Scholar 

  • Rahman MM, Tsukamoto J, Rahman MM, Yoneyama A, Mostafa KM. 2013. Lignin and its effects on litter decomposition in forest ecosystems. Chem Ecol 29:540–53.

    CAS  Google Scholar 

  • Rosemond AD, Benstead JP, Bumpers PM, Gulis V, Kominoski JS, Manning DWP, Suberkropp K, Wallace JB. 2015. Experimental nutrient additions accelerate terrestrial carbon loss from stream ecosystems. Science 347:1142–5.

    CAS  PubMed  Google Scholar 

  • Romito AM, Eggert SL, Diez JM, Wallace JB. 2010. Effects of seasonality and resource limitation on organic matter turnover by Chironomidae (Diptera) in southern Appalachian headwater streams. Limnol Oceanogr 55:1083–92.

    CAS  Google Scholar 

  • Siders AC, Compson ZG, Hungate BA, Dijkstra P, Koch GW, Wymore AS, Grandy AS, Marks JC. 2018. Litter identity affects assimilation of carbon and nitrogen by a shredding caddisfly. Ecosphere 9:e02340. https://doi.org/10.1002/ecs2.2340.

    Article  Google Scholar 

  • Spain AV, Le Feuvre RP. 1987. Breakdown of four litters of contrasting quality in a tropical Australian rainforest. J Appl Ecol 24:279–88.

    Google Scholar 

  • Steffan SA, Chikaraishi Y, Currie CR, Horn H, Gaines-Day HR, Pauli JN, Zalapa JE, Ohkouchi N. 2015. Microbes are trophic analogs of animals. Proc Natl Acad Sci 112:15119–24.

    CAS  PubMed  Google Scholar 

  • Steffan SA, Chikaraishi Y, Dharampal PS, Pauli JN, Guédot C, Ohkouchi N. 2017. Unpacking brown food-webs: animal trophic identity reflects rampant microbivory. Ecol Evolut 7:3532–41.

    Google Scholar 

  • Suberkropp K. 1992. Interactions with invertebrates. Barlöcher F, Ed. The ecology of aquatic hyphomycetes. Berlin: Springer. pp 118–31.

  • Triska FJ, Sedell JR. 1976. Decomposition of four species of leaf litter in response to nitrate manipulation. Ecology 57:783–92.

    CAS  Google Scholar 

  • Vadeboncoeur Y, Power ME. 2017. Attached algae: the cryptic base of inverted trophic pyramids in freshwaters. Annu Rev Ecol Evolut Syst 48:255–79.

    Google Scholar 

  • Webster JR, Waide JB. 1982. Effects of forest clearcutting on leaf breakdown in a southern Appalachian stream. Freshw Biol 12:331–44.

    Google Scholar 

  • Webster JR, Benfield EF. 1986. Vascular plant breakdown in freshwater ecosystems. Annu Rev Ecol Syst 17:567–94.

    Google Scholar 

  • Wise DH, Molles MC. 1979. Colonization of artificial substrates by stream insects: influence of substrate size and diversity. Hydrobiologia 65:69–74.

    Google Scholar 

  • Wymore AS, Compson ZG, McDowell WG, Potter JD, Hungate BA, Whitham TG, Marks JC. 2015. Leaf-litter leachate is distinct in optical properties and bioavailability to stream heterotrophs. Freshw Sci 34:857–66.

    Google Scholar 

Download references

Acknowledgements

We thank Phil Patterson from the NAU Research Greenhouse for assisting with growing and labeling plants. We thank Greg Florian for helping to build growth chambers. We are appreciative of Tom Kaminski, Jesse Maestas, David Green, Raemy Winton, David Rakestraw, Jordan Pletzer, Shannon Hagerty, Bri Finley, Janice Talley, Adriana Nimer, and Rosie Alling for help in the field and laboratory. We appreciate useful discussions with Mike Rotter, Sean Mahoney, and Danelle Larson. We thank members of the Center for Ecosystem Science and Society, at Northern Arizona University, for their valuable insights and feedback throughout the design of the field experiment and development of the manuscript. We appreciate the feedback from the editor and two anonymous reviewers, which substantially improved the manuscript. Funding was provided through NSF Grants DEB-1120343 and DEB-1655357.

Author information

Author notes

  1. Adam C. Siders

    Present address: Soil and Water Sciences Department, University of Florida, Gainesville, Florida, 32611, USA

Authors and Affiliations

  1. Center for Ecosystem Science and Society, Northern Arizona University, Flagstaff, Arizona, 86001, USA

    Adam C. Siders, Bruce A. Hungate, Paul Dijkstra, George W. Koch & Jane C. Marks

  2. Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona, 86011, USA

    Adam C. Siders, Bruce A. Hungate, Paul Dijkstra, George W. Koch & Jane C. Marks

  3. Centre for Environmental Genomics Applications (CEGA), 102-14 International Pl, St. John’s, Newfoundland and Labrador, A1A 5A1, Canada

    Zacchaeus G. Compson

Authors
  1. Adam C. Siders
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zacchaeus G. Compson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruce A. Hungate
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Paul Dijkstra
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. George W. Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jane C. Marks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adam C. Siders.

Additional information

Author Contributions

ACS, ZGC, BAH, PD, GWK, and JCM designed the study. ACS and ZGC grew and labeled the leaves and conducted the field experiment. ACS wrote the first draft of the manuscript and ZGC, BAH, GWK, and JCM made substantial contributions to revising the manuscript.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 31 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Siders, A.C., Compson, Z.G., Hungate, B.A. et al. The Influence of Leaf Type on Carbon and Nitrogen Assimilation by Aquatic Invertebrate Communities: A New Perspective on Trophic Efficiency. Ecosystems 24, 788–805 (2021). https://doi.org/10.1007/s10021-020-00550-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-020-00550-3

Keywords

  • Carbon
  • Nitrogen
  • Stable isotopes
  • Leaf litter
  • Decomposition
  • Invertebrates
  • Assimilation
  • Trophic efficiency