Abstract
Terrestrially-derived carbon (C) and organic matter (OM)—often of significant age—dominate in many streams and rivers, yet little is known about their potential nutritional contributions to aquatic macroinvertebrate consumers. Impacts of watershed characteristics (e.g., land use and lithology) on the sources and ages of C and OM utilized by aquatic consumers are also poorly understood. To assess these factors, macroinvertebrates were collected from six headwater streams having different watershed lithologies and land uses in the Hudson-Mohawk River system (New York, USA) and analyzed for natural δ13C, δ15N, δ2H, and ∆14C. A Bayesian stable isotopic mixing model revealed that autochthonous primary production dominated (62–92%) the biomass of all functional feeding groups (FFGs) across all sites, with allochthonous sources being of secondary but still significant (21–31%) importance. Macroinvertebrates collected from streams in watersheds having low vs. high agricultural land use were estimated to assimilate 0–13 and 4–31% soil-derived C and OM, respectively. ∆14C values and apparent ages of macroinvertebrates from shale-rich and shale-poor sites were also significantly different (mean ∆14C = −75 and −34‰; equivalent 14C ages = 630 and 280 years B.P., respectively). Inclusion of ∆14C data in mixing models confirmed the importance of autochthonous primary production, and also demonstrated indirect lithological control of nutritional resource utilization by influencing stream substrate type and potential retention of allochthonous C and OM. Findings from this study further showed that the relative magnitudes of autochthonous vs. allochthonous contributions to macroinvertebrates were dependent on FFG, land use type, and lithology.
Similar content being viewed by others
References
Allan JD (2004) Landscapes and riverscapes: the influence of land use on stream ecosystems. Annu Rev Ecol Evol Syst 35:257–284
Arsuffi TL, Suberkropp K (1989) Selective feeding by shredders on leaf-colonizing stream fungi: comparison of macroinvertebrate taxa. Oecologia 79:30–37
Baxter CV, Fausch KD, Saunders CW (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220
Bellamy AR, Bauer JE (2017) Nutritional support of inland aquatic food webs by aged carbon and organic matter. Limnol Oceanogr Lett. doi:10.1002/lol2.10044
Berggren M, Laudon H, Jansson M (2009) Aging of allochthonous organic carbon regulates bacterial production in unproductive boreal lakes. Limnol Oceanogr 54:1,333–1,342
Boix-Fayos C, de Vente J, Albaladejo J, Martínez-Mena M (2009) Soil carbon erosion and stock as affected by land use changes at the catchment scale in Mediterranean ecosystems. Agric Ecosyst Environ 133:75–85
Brett MT, Bunn SE, Chandra S, others (2017) How important are terrestrial organic carbon inputs for secondary production in freshwater ecosystems? Freshw Biol 62:833–853
Broecker WS, Walton A (1959) The geochemistry of C-14 in fresh-water systems. Geochim Cosmochim Acta 16:15–38
Brooke LT, Ankley GT, Call DJ, Cook PM (1996) Gut content weight and clearance rate for three species of freshwater invertebrates. Environ Toxicol Chem 15:223–228
Bunn SE, Boon PI (1993) What sources of organic carbon drive food webs in billabongs? A study based on stable isotope analysis. Oecologia 96:85–94
Burdon FJ, McIntosh AR, Harding JS (2013) Habitat loss drives threshold response of benthic invertebrate communities to deposited sediment in agricultural streams. Ecol Appl 23:1,036–1,047
Butman D, Raymond PA (2011) Significant efflux of carbon dioxide from streams and rivers in the United States. Nat Geosci 4:839–842
Butman DE, Wilson HF, Barnes RT, Xenopoulos MA, Raymond PA (2015) Increased mobilization of aged carbon to rivers by human disturbance. Nat Geosci 8:112–116
Caraco N, Bauer JE, Cole JJ, Petsch S, Raymond P (2010) Millennial-aged organic carbon subsidies to a modern river food web. Ecology 91:2,385–2,393
Carlson PE, McKie BG, Sandin L, Johnson RK (2016) Strong land-use effects on the dispersal patterns of adult stream insects: implications for transfers of aquatic subsidies to terrestrial consumers. Freshw Biol 61:848–861
Clarke KR, Gorley RN (2006) User manual/tutorial. Primer-E Ltd, Plymouth, p 93
Collins SM, Kohler TJ, Thomas SA, Fetzer WW, Flecker AS (2015) The importance of terrestrial subsidies in stream food webs varies along a stream size gradient. Oikos 125:674–685
Cummins KW (2016) Combining taxonomy and function in the study of stream macroinvertebrates. J Limnol 75:235–241
Cummins KW, Klug MJ (1979) Feeding ecology of stream invertebrates. Annu Rev Ecol Syst 10:147–172
de Castro, D.M.P., de Carvalho DR, dos Santos Pompeu P, Moreira MZ, Nardoto GB, Callisto M (2016) Land use influences niche size and the assimilation of resources by benthic macroinvertebrates in tropical headwater dtreams. PloS One 11:e0150527
Docile T, Rosa DC, Figueiró R, Nessimian J (2016) Urbanisation alters the flow of energy through stream food webs. Insect Conserv Divers 9:416–426
Doi H, Takemon Y, Ohta T, Ishida Y, Kikuchi E (2007) Effects of reach-scale canopy cover on trophic pathways of caddisfly larvae in a Japanese mountain stream. Mar Freshw Res 58:811–817
Doucett RR, Marks JC, Blinn DW, Caron M, Hungate BA (2007) Measuring terrestrial subsidies to aquatic food webs using stable isotopes of hydrogen. Ecology 88:1,587–1,592
Durand B (1980) Sedimentary organic matter and kerogen. Definition and quantitative importance of kerogen. In: Durand B (ed) Kerogen: insoluble organic matter from sedimentary rocks. Editions Technip, Paris, pp 13–34
England LE, Rosemond AD (2004) Small reductions in forest cover weaken terrestrial-aquatic linkages in headwater streams. Freshw Biol 49:721–734
Finlay JC, Kendall C (2007) Stable isotope tracing of temporal and spatial variability in organic matter sources to freshwater ecosystems. Stable Isot Ecol Environ Sci 2:283–333
Finlay JC, Khandwala S, Power ME (2002) Spatial scales of carbon flow in a river food web. Ecology 83:1,845–1,859
Finlay JC, Doucett RR, McNeely C (2010) Tracing energy flow in stream food webs using stable isotopes of hydrogen. Freshw Biol 55:941–951
Goedkoop W, Demandt M, Ahlgren G (2007) Interactions between food quantity and quality (long-chain polyunsaturated fatty acid concentrations) effects on growth and development of Chironomus riparius. Can J Fish Aquat Sci 64:425–436
Goñi MA, Hatten JA, Wheatcroft RA, Borgeld JC (2013) Particulate organic matter export by two contrasting small mountainous rivers from the Pacific Northwest, USA. J Geophys Res Biogeosci 118:112–134
Graz Y, Di-Giovanni C, Copard Y, Mathys N, Cras A, Marc V (2012) Annual fossil organic carbon delivery due to mechanical and chemical weathering of marly badlands areas. Earth Surf Process Landf 37:1,263–1,271
Guillemette F, Bianchi TS, Spencer RG (2017) Old before your time: Ancient carbon incorporation in contemporary aquatic foodwebs. Limnol Oceanogr. doi:10.1002/lno.10525
Guo F, Kainz MJ, Sheldon F, Bunn SE (2016) The importance of high-quality algal food sources in stream food webs–current status and future perspectives. Freshw Biol 61:815–831
Hall RO, Meyer JL (1998) The trophic significance of bacteria in a detritus-based stream food web. Ecology 79:1,995–2,012
Hall RO, Yackulic CB, Kennedy TA, Yard MD, Rosi-Marshall EJ, Voichick N, Behn KE (2015) Turbidity, light, temperature, and hydropeaking control primary productivity in the Colorado River, Grand Canyon. Limnol Oceanogr 60:512–526
Hamilton H, Clifford F (1983) The seasonal food habits of mayfly (Ephemeroptera) nymphs from three Alberta, Canada, streams, with special reference to absolute volume and size of particles ingested. Arch Hydrobiol Suppl 65:197–234
Hayden B, McWilliam-Hughes SM, Cunjak RA (2016) Evidence for limited trophic transfer of allochthonous energy in temperate river food webs. Freshw Sci 35:544–558
Hedges JI (1992) Global biogeochemical cycles: progress and problems. Mar Chem 39:67–93
Henley WF, Patterson MA, Neves RJ, Lemly AD (2000) Effects of sedimentation and turbidity on lotic food webs: a concise review for natural resource managers. Rev Fish Sci 8:125–139
Hilton RG, Galy A, Hovius N, Horng M-J, Chen H (2011) Efficient transport of fossil organic carbon to the ocean by steep mountain rivers: an orogenic carbon sequestration mechanism. Geology 39:71–74
Horner RR, Welch EB, Seeley MR, Jacoby JM (1990) Responses of periphyton to changes in current velocity, suspended sediment and phosphorus concentration. Freshw Biol 24:215–232
Hossler K, Bauer JE (2012) Estimation of riverine carbon and organic matter source contributions using time-based isotope mixing models. J Geophys Res 117:G03035
Hossler K, Bauer JE (2013a) Amounts, isotopic character and ages of organic and inorganic carbon exported from rivers to ocean margins: 1. Estimates of terrestrial losses and inputs to the Middle Atlantic Bight. Glob Biogeochem Cycles 27:331–346
Hossler K, Bauer JE (2013b) Amounts, isotopic character, and ages of organic and inorganic carbon exported from rivers to ocean margins: 2. Assessment of natural and anthropogenic controls. Glob Biogeochem Cycles 27:347–362
Ishikawa NF, Hyodo F, Tayasu I (2013) Use of carbon-13 and carbon-14 natural abundances for stream food web studies. Ecol Res 28:759–769
Ishikawa NF, Uchida M, Shibata Y, Tayasu I (2014) Carbon storage reservoirs in watersheds support stream food webs via periphyton production. Ecology 95:1,264–1,271
Ishikawa NF, Yamane M, Suga H, Ogawa NO, Yokoyama Y, Ohkouchi N (2015) Chlorophyll a-specific ∆14C, δ13C and δ15N values in stream periphyton: implications for aquatic food web studies. Biogeosciences 12:6,781–6,789
Ishikawa NF, Togashi H, Kato Y, Yoshimura M, Kohmatsu Y, Yoshimizu C, Ogawa NO, Ohte N, Tokuchi N, Ohkouchi N, others (2016) Terrestrial–aquatic linkage in stream food webs along a forest chronosequence: multi-isotopic evidence. Ecology 97:1,146–141,158
Kautza A, Sullivan, S.M.P. (2016) The energetic contributions of aquatic primary producers to terrestrial food webs in a mid-size river system. Ecology 97:694–705
Keaveney EM, Reimer PJ (2012) Understanding the variability in freshwater radiocarbon reservoir offsets: a cautionary tale. J Archaeol Sci 39:1,306–1,316
Keaveney EM, Reimer PJ, Foy RH (2015) Young, old, and weathered carbon—part 2: using radiocarbon and stable isotopes to identify terrestrial carbon support of the food web in an alkaline, humic lake. Radiocarbon 57:425–438
Kleber M (2010) What is recalcitrant soil organic matter? Environ Chem 7:320–332
Kleber M, Johnson MG (2010) Advances in understanding the molecular structure of soil organic matter: implications for interactions in the environment. Adv Agron 106:77–142
Kruger BR, Werne JP, Branstrator DK, Hrabik TR, Chikaraishi Y, Ohkouchi N, Minor EC (2016) Organic matter transfer in Lake Superior’s food web: insights from bulk and molecular stable isotope and radiocarbon analyses. Limnol Oceanogr 61:149–164
Lal R (2003) Soil erosion and the global carbon budget. Environ Int 29:437–450
Lau DC, Sundh I, Vrede T, Pickova J, Goedkoop W (2014) Autochthonous resources are the main driver of consumer production in dystrophic boreal lakes. Ecology 95:1,506–1,519
Leberfinger K, Bohman I, Herrmann J (2011) The importance of terrestrial resource subsidies for shredders in open-canopy streams revealed by stable isotope analysis. Freshw Biol 56:470–480
Leithold EL, Blair NE (2001) Watershed control on the carbon loading of marine sedimentary particles. Geochim Cosmochim Acta 65:2,231–2,240
Leithold EL, Blair NE, Perkey DW (2006) Geomorphologic controls on the age of particulate organic carbon from small mountainous and upland rivers. Glob Biogeochem Cycles 20:GB3030
Leithold EL, Blair NE, Wegmann KW (2016) Source-to-sink sedimentary systems and global carbon burial: a river runs through it. Earth Sci Rev 153:30–42
Lenat DR (1984) Agriculture and stream water quality: a biological evaluation of erosion control practices. Environ Manag 8:333–343
Lenat DR, Crawford JK (1994) Effects of land use on water quality and aquatic biota of three North Carolina Piedmont streams. Hydrobiologia 294:185–199
Levin I, Kromer B, Hammer S (2013) Atmospheric ∆14CO2 trend in Western European background air from 2000 to 2012. Tellus B 65:20092
Longworth BE, Petsch ST, Raymond PA, Bauer JE (2007) Linking lithology and land use to sources of dissolved and particulate organic matter in headwaters of a temperate, passive-margin river system. Geochim Cosmochim Acta 71:4,233–4,250
Lu YH, Canuel EA, Bauer JE, Chambers RM (2014) Effects of watershed land use on sources and nutritional value of particulate organic matter in temperate headwater streams. Aquat Sci 76:419–436
Madsen JD, Chambers PA, James WF, Koch EW, Westlake DF (2001) The interaction between water movement, sediment dynamics and submersed macrophytes. Hydrobiologia 444:71–84
Marín-Spiotta E, Gruley KE, Crawford J, Atkinson EE, Miesel JR, Greene S, Cardona-Correa C, Spencer, R.G.M. (2014) Paradigm shifts in soil organic matter research affect interpretations of aquatic carbon cycling: transcending disciplinary and ecosystem boundaries. Biogeochemistry 117:279–297
Marwick TR, Tamooh F, Teodoru CR, Borges AV, Darchambeau F, Bouillon S (2015) The age of river-transported carbon: a global perspective. Glob Biogeochem Cycles 29:122–137
Matthaei CD, Piggott JJ, Townsend CR (2010) Multiple stressors in agricultural streams: interactions among sediment addition, nutrient enrichment and water abstraction. J Appl Ecol 47:639–649
Mayorga E, Aufdenkampe AK, Masiello CA, Krusche AV, Hedges JL, Quay PD, Richey JE, Brown TA (2005) Young organic matter as a source of carbon dioxide outgassing from Amazonian rivers. Nature 436:538–541
McCallister SL, del Giorgio PA (2012) Evidence for the respiration of ancient terrestrial organic C in northern temperate lakes and streams. Proc Natl Acad Sci USA 109:16,963–16,968
McCutchan JH, Lewis WM (2002) Relative importance of carbon sources for Macroinvertebrates in a Rocky Mountain Stream. Limnol Oceanogr 47:742–752
Merritt RW, Cummins KW (2008) An introduction to the aquatic macroinvertebrates of North America, 4 edn. Kendall-Hunt, Dubuque, Berg, M.B
Middelburg JJ (2014) Stable isotopes dissect aquatic food webs from the top to the bottom. Biogeosciences 11:2,357–2,371
Moore JW, Semmens BX (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecol Lett 11:470–480
Müller-Navarra DC (2008) Food web paradigms: the biochemical view on trophic interactions. Int Rev Hydrobiol 93:489–505
Neres-Lima V, Brito EF, Krsulović FA, Detweiler AM, Hershey AE, Moulton TP (2016) High importance of autochthonous basal food source for the food web of a Brazilian tropical stream regardless of shading. Int Rev Hydrobiol 101:132–142
Petsch ST, Eglinton TI, Edwards KJ (2001) C-dead living biomass: evidence for microbial assimilation of ancient organic carbon during shale weathering. Science 292:1,127–1,131
Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food-web studies. Can J Zool 92:823–835
Piscart C, Genoel R, Doledec S, Chauvet E, Marmonier P (2009) Effects of intense agricultural practices on heterotrophic processes in streams. Environ Pollut 157:1,011–1,018
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718
Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Del Toro I, Ho C-K, Kominoski J, Newbold TA, others (2013) Invertebrates, ecosystem services and climate change. Biol Rev 88:327–348
Raymond PA, Bauer JE (2001) Riverine export of aged terrestrial organic matter to the North Atlantic Ocean. Nature 409:497–500
Reuss NS, Hamerlik L, Velle G, Michelsen A, Pedersen O, Brodersen KP (2013) Stable isotopes reveal that chironomids occupy several trophic levels within West Greenland lakes: implications for food web studies. Limnol Oceanogr 58:1,023–1,034
Roach KA (2013) Environmental factors affecting incorporation of terrestrial material into large river food webs. Freshw Sci 32:283–298
Rosi-Marshall EJ, Wallace JB (2002) Invertebrate food webs along a stream resource gradient. Freshw Biol 47:129–141
Rosi-Marshall EJ, Vallis KL, Baxter CV, Davis JM (2016) Retesting a prediction of the River Continuum concept: autochthonous versus allochthonous resources in the diets of invertebrates. Freshw Sci 35:534–543
Schell DM (1983) Carbon-13 and carbon-14 abundances in Alaskan aquatic organisms: delayed production from peat in arctic food webs. Science 219:1,068–1,071
Schillawski S, Petsch S (2008) Release of biodegradable dissolved organic matter from ancient sedimentary rocks. Glob Biogeochem Cycles 22:GB3002
Schmidt MW, Torn MS, Abiven S, Dittmar T, Guggenberger G, Janssens IA, Kleber M, Kögel-Knabner I, Lehmann J, Manning DA, others (2011) Persistence of soil organic matter as an ecosystem property. Nature 478:49–56
Smits AP, Schindler DE, Brett MT (2015) Geomorphology controls the trophic base of stream food webs in a boreal watershed. Ecology 96:1,775–1,782
Sobczak WV, Cloern JE, Jassby AD, Cole BE, Schraga TS, Arnsberg A (2005) Detritus fuels ecosystem metabolism but not metazoan food webs in San Francisco estuary’s freshwater delta. Estuaries 28:124–137
Sullivan, S.M.P. (2013) Stream foodweb δ13C and geomorphology are tightly coupled in mountain drainages of northern Idaho. Freshw Sci:32:606–621
Tanentzap AJ, Kielstra BW, Wilkinson GM, others (2017) Terrestrial support of lake food webs: synthesis reveals controls over cross-ecosystem resource use. Sci Adv 3:e1601765
Torres-Ruiz M, Wehr JD, Perrone AA (2007) Trophic relations in a stream food web: importance of fatty acids for macroinvertebrate consumers. J Inf 26:509–522
Tourtelot HA (1979) Black shale—its deposition and diagenesis. Clays Clay Miner 27:313–321
Trumbore SE (1997) Potential responses of soil organic carbon to global environmental change. Proc Natl Acad Sci 94:8,284–8,291
Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137
Wallace JB, Eggert SL, Meyer JL, Webster JR (2015) Stream invertebrate productivity linked to forest subsidies: 37 stream-years of reference and experimental data. Ecology 96:1,213–1,228
Walters DM, Fritz KM, Phillips DL (2007) Reach-scale geomorphology affects organic matter and consumer δ13C in a forested Piedmont stream. Freshw Biol 52:1,105–1,119
Wang Y, Gu B, Lee M-K, Jiang S, Xu Y (2014) Isotopic evidence for anthropogenic impacts on aquatic food web dynamics and mercury cycling in a subtropical wetland ecosystem in the US. Sci Total Environ 487:557–564
Wassenaar LI, Hobson KA (2003) Comparative equilibration and online technique for determination of non-exchangeable hydrogen of keratins for use in animal migration studies. Isot Environ Health Stud 39:211–217
Weber AE, Bauer JE, Watters GT (2017) Assessment of nutritional subsidies to freshwater mussels using a multiple natural abundance isotope approach. Freshw Biol 62:615–629
Wilkinson GM, Cole JJ, Pace ML (2015) Deuterium as a food source tracer: sensitivity to environmental water, lipid content, and hydrogen exchange. Limnol Oceanogr Methods 13:213–223
Williams CJ, Yamashita Y, Wilson HF, Jaffé R, Xenopoulos MA, others (2010) Unraveling the role of land use and microbial activity in shaping dissolved organic matter characteristics in stream ecosystems. Limnol Oceanogr 55:1,159–1,171
Yule CM, Boyero L, Marchant R (2010) Effects of sediment pollution on food webs in a tropical river (Borneo, Indonesia). Mar Freshw Res 61:204–213
Zhu Y, Vieth-Hillebrand A, Wilke FD, Horsfield B (2015) Characterization of water-soluble organic compounds released from black shales and coals. Int J Coal Geol 150:265–275
Acknowledgements
We thank Brett Longworth for input during the development stage of this research and Amy Weber and Thomas Evans for help with field sampling. We are grateful to the University of California at Davis Stable Isotope Facility for δ13C and δ15N analyses, the Colorado Plateau Isotope Laboratory for δ2H analyses, and the National Ocean Sciences AMS Facility for Δ14C analyses. We also thank Jon Cole for his feedback on early drafts of the manuscript and two anonymous reviewers whose comments and suggestions helped to improve the final version of this manuscript. This work was supported by funding from the Hudson River Foundation to J.E.B. and A.R.B., National Science Foundation awards DEB-0234533, EAR-0403949 and OCE-0961860 to J.E.B., National Science Foundation awards OCE-1656292 and OCE-1514859 to A.G.G, and The Ohio State University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bellamy, A.R., Bauer, J.E. & Grottoli, A.G. Influence of land use and lithology on sources and ages of nutritional resources for stream macroinvertebrates: a multi-isotopic approach. Aquat Sci 79, 925–939 (2017). https://doi.org/10.1007/s00027-017-0542-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00027-017-0542-3