Abstract
Rivers and their riparian zones are linked by reciprocal subsidies such as leaf fall or the emergence of biphasic aquatic organisms. Transfers of subsidies from freshwater to terrestrial ecosystems have been broadly studied, yet few studies have explored the transfer of aquatic organic matter (AOM) to surrounding terrestrial ecosystems as a response of hydrological variability. When rivers dry or flood, AOM can be transferred to terrestrial ecosystems and decomposed by terrestrial organisms; however, this process remains poorly investigated. In this study, we monitored the decomposition rate of several types of AOM (algae, macroinvertebrate and fish) exposed to different drying intensity, on the gravel bars and in the riparian zone of an intermittent headwater stream. The contribution of different terrestrial organisms to this decomposition rate was also explored. We showed that decomposition rates did not differ between the gravel bars and riparian zone although the invertebrate assemblages, which colonized the AOM, did. The decomposition rates depended mainly on the type of organic matter, with AOM of animal origin being decomposed more rapidly than that of vegetal origin. Microorganisms and vertebrates contributed most to the decomposition. Our results suggest that stranded AOM is consumed by terrestrial organisms; however, environmental conditions such as temperature and humidity can affect its decomposition. As extreme hydrological events are becoming more frequent, we need further research to explore how stranded AOM decomposition changes across seasons, river types and climates to improve our understanding of this process and its importance for terrestrial food webs.
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Data availability
The dataset analyzed in this study are available at Figshare via the following links: 110.6084/m9.figshare.17049821 and 110.6084/m9.figshare.17049824
References
Anderson PK (1986) Foraging range in mice and voles: the role of risk. Can J Zool 64:2645–2653. https://doi.org/10.1139/z86-384
Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). Wiley StatsRef: statistics reference online. Wiley, pp 1–15. https://doi.org/10.1002/9781118445112.stat07841
Barton K, Barton MK (2015) Package ‘mumin.’ Version 1(18):439
Bastow JL, Sabo JL, Finlay JC, Power ME (2002) A basal aquatic–terrestrial trophic link in rivers: algal subsidies via shore-dwelling grasshoppers. Oecologia 131:261–268. https://doi.org/10.1007/s00442-002-0879-7
Bates AJ, Sadler JP, Perry JN, Fowles AP (2007a) The microspatial distribution of beetles (Coleoptera) on exposed riverine sediments (ERS). Eur J Entomol. 104:479–487. https://doi.org/10.14411/eje.2007.068
Bates D, Sarkar D, Bates MD, Matrix L (2007b) The lme4 package. R Package Vers 2(1):74
Baxter CV, Fausch KD, Saunders WC (2005) Tangled webs: reciprocal flows of invertebrate prey link streams and riparian zones. Freshw Biol 50:201–220. https://doi.org/10.1111/j.1365-2427.2004.01328.x
Ben-David M, Flynn RW, Schell DM (1997) Annual and seasonal changes in diets of martens: evidence from stable isotope analysis. Oecologia 111:280–291. https://doi.org/10.1007/s004420050236
Ben-David M, Hanley TA, Schell DM (1998) Fertilization of terrestrial vegetation by spawning pacific salmon: the role of flooding and predator activity. Oikos 83:47–55. https://doi.org/10.2307/3546545
Boulton AJ (2003) Parallels and contrasts in the effects of drought on stream macroinvertebrate assemblages. Freshw Biol 48:1173–1185. https://doi.org/10.1046/j.1365-2427.2003.01084.x
Bruder A, Chauvet E, Gessner MO (2011) Litter diversity, fungal decomposers and litter decomposition under simulated stream intermittency. Funct Ecol 25:1269–1277. https://doi.org/10.1111/j.1365-2435.2011.01903.x
Bunn SE, Balcombe SR, Davies PM, Fellows CS, McKenzie-Smith FJ (2006) Aquatic productivity and food webs of desert river ecosystems. In: Kingsford R (ed) Ecology of desert rivers. Cambridge University Press, pp 76–99
Castro CP, García MD, Martins-da-Silva P, Silva IF, Serrano A (2013) Coleoptera of forensic interest: a study of seasonal community composition and succession in Lisbon Portugal. Forensic Sci Int 232:73–83. https://doi.org/10.1016/j.forsciint.2013.06.014
Chapin FS, Matson PA, Mooney HA (2002) Terrestrial decomposition. Principles of terrestrial ecosystem ecology. Springer, New York, pp 151–175. https://doi.org/10.1007/0-387-21663-4_7
Collins SF, Baxter CV (2014) Heterogeneity of riparian habitats mediates responses of terrestrial arthropods to a subsidy of Pacific salmon carcasses. Ecosphere 5:art146. https://doi.org/10.1890/ES14-00030.1
Corti R, Datry T (2012) Invertebrates and sestonic matter in an advancing wetted front travelling down a dry river bed (Albarine, France). Freshw Sci 31:1187–1201. https://doi.org/10.1899/12-017.1
Corti R, Datry T (2016) Terrestrial and aquatic invertebrates in the riverbed of an intermittent river: parallels and contrasts in community organisation. Freshw Biol 61:1308–1320. https://doi.org/10.1111/fwb.12692
Corti R, Datry T, Drummond L, Larned ST (2011) Natural variation in immersion and emersion affects breakdown and invertebrate colonization of leaf litter in a temporary river. Aquat Sci 73:537. https://doi.org/10.1007/s00027-011-0216-5
Courtwright J, May CL (2013) Importance of terrestrial subsidies for native brook trout in Appalachian intermittent streams. Freshw Biol 58:2423–2438. https://doi.org/10.1111/fwb.12221
Dahm CN, Baker MA, Moore DI, Thibault JR (2003) Coupled biogeochemical and hydrological responses of streams and rivers to drought. Freshw Biol 48:1219–1231
Datry T, Corti R, Claret C, Philippe M (2011) Flow intermittence controls leaf litter breakdown in a French temporary alluvial river: the “drying memory.” Aquat Sci 73:471–483. https://doi.org/10.1007/s00027-011-0193-8
Datry T, Larned ST, Tockner K (2014) Intermittent rivers: a challenge for freshwater ecology. Bioscience 64:229–235. https://doi.org/10.1093/biosci/bit027
Den Ouden J, Jansen PA, Smit R (2005) Jays, mice and oaks: predation and dispersal of Quercus robur and Q. petraea in North-western Europe. In: Forget PM (ed) Seed fate: predation, dispersal, and seedling establishment. CABI, pp 223–241
Döll P, Schmied HM (2012) How is the impact of climate change on river flow regimes related to the impact on mean annual runoff? A global-scale analysis. Environ Res Lett 7:014037. https://doi.org/10.1088/1748-9326/7/1/014037
Driessen MM, Kirkpatrick JB, Mcquillan PB (2013) Shifts in composition of monthly invertebrate assemblages in moorland differed between lowland and montane locations but not fire-ages. Environ Entomol 42:58–73. https://doi.org/10.1603/EN12322
Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque C, Naiman RJ, Prieur-Richard A-H, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182. https://doi.org/10.1017/S1464793105006950
Dunkle MR, Lampman RT, Jackson AD, Caudill CC (2020) Factors affecting the fate of Pacific lamprey carcasses and resource transport to riparian and stream macrohabitats. Freshw Biol 65:1429–1439. https://doi.org/10.1111/fwb.13510
Foulquier A, Artigas J, Pesce S, Datry T (2015) Drying responses of microbial litter decomposition and associated fungal and bacterial communities are not affected by emersion frequency. Freshw Sci 34:1233–1244. https://doi.org/10.1086/682060
Henshall SE, Sadler JP, Hannah DM, Bates AJ (2011) The role of microhabitat and food availability in determining riparian invertebrate distributions on gravel bars: a habitat manipulation experiment. Ecohydrology 4:512–519. https://doi.org/10.1002/eco.188
Hering D (1998) Riparian Beetles (Coleoptera) along a small stream in the oregon coast range and their interactions with the aquatic environment. Coleopt Bull 52:161–170
Hering D, Plachter H (1997) Riparian ground beetles (Coeloptera, Carabidae) preying on aquatic invertebrates: a feeding strategy in alpine floodplains. Oecologia 111(2):261–270
Hilderbrand GV, Hanley TA, Robbins CT, Schwartz CC (1999) Role of brown bears (Ursus arctos) in the flow of marine nitrogen into a terrestrial ecosystem. Oecologia 121:546–550. https://doi.org/10.1007/s004420050961
Hocking MD, Ring RA, Reimchen TE (2009) The ecology of terrestrial invertebrates on Pacific salmon carcasses. Ecol Res 24:1091–1100. https://doi.org/10.1007/s11284-009-0586-5
Kahlert M, Hasselrot AT, Hillebrand H, Pettersson K (2002) Spatial and temporal variation in the biomass and nutrient status of epilithic algae in Lake Erken Sweden. Freshw Biol 47:1191–1215. https://doi.org/10.1046/j.1365-2427.2002.00844.x
Lafage D, Bergman E, Eckstein RL, Österling EM, Sadler JP, Piccolo JJ (2019) Local and landscape drivers of aquatic-to-terrestrial subsidies in riparian ecosystems: a worldwide meta-analysis. Ecosphere 10:e02697. https://doi.org/10.1002/ecs2.2697
Lake PS (2003) Ecological effects of perturbation by drought in flowing water. Freshw Biol 48:1161–1172
Loreau M, Mouquet N, Holt RD (2003) Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecol Lett 6:673–679. https://doi.org/10.1046/j.1461-0248.2003.00483.x
Lövei GL, Sunderland KD (1996) Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu Rev Entomol 41(1):231–256. https://doi.org/10.1146/annurev.en.41.010196.001311
McCluney KE, Sabo JL (2009) Water availability directly determines per capita consumption at two trophic levels. Ecology 90:1463–1469. https://doi.org/10.1890/08-1626.1
Messager ML, Lehner B, Cockburn C, Lamouroux N, Pella H, Snelder T, Datry T (2021) Global prevalence of non-perennial rivers and streams. Nature 594(7863):391–397. https://doi.org/10.1038/s41586-021-03565-5
Milardi M, Käkelä R, Weckström J, Kahilainen KK (2016) Terrestrial prey fuels the fish population of a small, high-latitude lake. Aquat Sci 78(4):695–706. https://doi.org/10.1007/s00027-015-0460-1
Nakano S, Murakami M (2001) Reciprocal subsidies: dynamic interdependence between terrestrial and aquatic food webs. Proc Natl Acad Sci USA 98(1):166–170. https://doi.org/10.1073/pnas.98.1.166
Newton AF Jr, Thayer MK, Ashe JS, Chandler DS (2000) Staphylinidae Latreille 1802. In: Arnett RH Jr, Thomas MC (eds) American Beetles. Archostemata, Myxophaga, Adephaga, Polyphaga: Staphyliniformia, vol 1. CRC Press, Boca Raton, pp 272–418
Novais A, Souza AT, Ilarri M, Pascoal C, Sousa R (2015) From water to land: how an invasive clam may function as a resource pulse to terrestrial invertebrates. Sci Total Environ 538:664–671. https://doi.org/10.1016/j.scitotenv.2015.08.106
Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ, Suggests MASS (2007) The vegan package. Community Ecol Package 10(631–637):719
Paetzold A, Schubert C, Tockner K (2005) Aquatic terrestrial linkages along a braided-river: riparian arthropods feeding on aquatic insects. Ecosystems 8:748–759. https://doi.org/10.1007/s10021-005-0004-y
Paetzold A, Yoshimura C, Tockner K (2008) Riparian arthropod responses to flow regulation and river channelization. J Appl Ecol 45(3):894–903. https://doi.org/10.1111/j.1365-2664.2008.01463.x
Peterson CG, Vormittag KA, Valett HM (1998) Ingestion and digestion of epilithic algae by larval insects in a heavily grazed montane stream. Freshw Biol 40:607–623. https://doi.org/10.1046/j.1365-2427.1998.00358.x
Polis GA, Anderson WB, Holt RD (1997) Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst 28:289–316. https://doi.org/10.1146/annurev.ecolsys.28.1.289
Power ME, Dietrich WE (2002) Food webs in river networks. Ecol Res 17:451–471. https://doi.org/10.1046/j.1440-1703.2002.00503.x
Regester KJ, Lips KR, Whiles MR (2006) Energy flow and subsidies associated with the complex life cycle of ambystomatid salamanders in ponds and adjacent forest in southern Illinois. Oecologia 147:303–314. https://doi.org/10.1007/s00442-005-0266-2
Richardson JS, Zhang Y, Marczak LB (2010) Resource subsidies across the land–freshwater interface and responses in recipient communities. River Res Appl 26:55–66. https://doi.org/10.1002/rra.1283
Ripley B, Venables B, Bates DM, Hornik K, Gebhardt A, Firth D, Ripley MB (2013) Package ‘mass.’ Cran R 538:113–120
Sauquet E, Beaufort A, Sarremejane R, Thirel G (2021) Predicting flow intermittence in France under climate change. Hydrol Sci J 66:2046–2059. https://doi.org/10.1080/02626667.2021.1963444
Schlichting PE, Love CN, Webster SC, Beasley JC (2019) Efficiency and composition of vertebrate scavengers at the land-water interface in the Chernobyl Exclusion Zone. Food Webs 18:e00107. https://doi.org/10.1016/j.fooweb.2018.e00107
Schriever TA, Cadotte MW, Williams DD (2014) How hydroperiod and species richness affect the balance of resource flows across aquatic–terrestrial habitats. Aquat Sci 76:131–143. https://doi.org/10.1007/s00027-013-0320-9
Siebers AR, Paillex A, Robinson CT (2021) Riparian hunting spiders do not rely on aquatic subsidies from intermittent alpine streams. Aquat Sci 83:25. https://doi.org/10.1007/s00027-021-00779-7
Sousa R, Varandas S, Cortes R, Teixeira A, Lopes-Lima M, Machado J, Guilhermino L (2012) Massive die-offs of freshwater bivalves as resource pulses. Ann Limnol Int J Lim 48:105–112. https://doi.org/10.1051/limn/2012003
Stanley EH, Fisher SG, Grimm NB (1997) Ecosystem expansion and contraction in streams. Bioscience 47:427–435. https://doi.org/10.2307/1313058
Steward AL, Marshall JC, Sheldon F, Harch B, Choy S, Bunn SE, Tockner K (2011) Terrestrial invertebrates of dry river beds are not simply subsets of riparian assemblages. Aquat Sci 73:551. https://doi.org/10.1007/s00027-011-0217-4
Steward AL, von Schiller D, Tockner K, Marshall JC, Bunn SE (2012) When the river runs dry: human and ecological values of dry riverbeds. Front Ecol Environ 10:202–209. https://doi.org/10.1890/110136
Steward AL, Datry T, Langhans SD (2022) The terrestrial and semi-aquatic invertebrates of intermittent rivers and ephemeral streams. Biol Rev. https://doi.org/10.1111/brv.12848
Stott DE, Elliott LF, Papendick RI, Campbell GS (1986) Low temperature or low water potential effects on the microbial decomposition of wheat residue. Soil Biol Biochem 18:577–582. https://doi.org/10.1016/0038-0717(86)90078-7
Trenberth KE (2011) Changes in precipitation with climate change. Clim Res 47:123–138. https://doi.org/10.3354/cr00953
Twining CW, Brenna JT, Lawrence P, Winkler DW, Flecker AS, Hairston NG (2019) Aquatic and terrestrial resources are not nutritionally reciprocal for consumers. Funct Ecol 33:2042–2052. https://doi.org/10.1111/1365-2435.13401
Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE (1980) The river continuum concept. Can J Fish Aquat Sci 37(1):130–137. https://doi.org/10.1139/f80-017
Warburg MR (1987) Isopods and their terrestrial environment. Adv Ecol Res. Academic Press, pp 187–242. https://doi.org/10.1016/S0065-2504(08)60246-9
Weithmann S, von Hoermann C, Schmitt T, Steiger S, Ayasse M (2020) The attraction of the dung beetle Anoplotrupes stercorosus (Coleoptera: Geotrupidae) to volatiles from vertebrate cadavers. Insects 11:476. https://doi.org/10.3390/insects11080476
Wickham H (2011) ggplot2. Wiley Interdiscip Rev Comput Stat 3(2):180–185. https://doi.org/10.1002/wics.147
Acknowledgements
We thank two anonymous reviewers for their constructive comments on earlier drafts of the manuscript. We are grateful to Sara Puijalon for giving us access to the experimental platform “Les étangs, Université Lyon 1”. We thank Bernard Motte, Bertrand Launay, Julien Barnasson, Guillaume Le Goff, Teresa Silverthorn, Emmanuel Jaulin and Nils Dumarski for assistance in the preparation, field execution and lab processing of this experiment. We also thank Florian Lecorvaisier who provided valuable help with statistical analyses as well as Zoltán Csabai for providing data on the macroinvertebrate assemblages of the Buizin stream. This experiment was supported by the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie Grant agreement No. 891090 (MetaDryNet) and by the DRYvER project (http://www.dryver.eu/) under Grant agreement No. 869226.
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Barthélémy, N., Sarremejane, R. & Datry, T. Aquatic organic matter decomposition in the terrestrial environments of an intermittent headwater stream. Aquat Sci 84, 45 (2022). https://doi.org/10.1007/s00027-022-00878-z
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DOI: https://doi.org/10.1007/s00027-022-00878-z