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Joint effects of temperature and litter quality on detritivore-mediated breakdown in streams

Abstract

Global warming causes concomitant changes in several environmental factors that often have synergistic effects on populations and ecosystem processes. We examined how increased water temperature and reduced litter quality affected a leaf-shredding detritivore’s performance and its effect on litter breakdown. Detritivores were exposed in microcosms at two temperatures (10 and 15 °C) and four categories of litter quality (based on nitrogen and condensed tannin concentrations). We hypothesized that (1) high-quality litter mixtures would breakdown faster, improving detritivore performance; (2) differences would occur regardless of which plant species in the mixture were preferentially consumed; and (3) litter quality effects on detritivore-mediated breakdown and performance would be intensified at higher temperatures. Unexpectedly, we found faster breakdown at intermediate litter quality and lower temperature. Additionally, we found cases of detritivore selection and rejection of different resources driven by litter traits other than nitrogen and tannin concentrations. Detritivore performance increased with temperature, regardless of litter quality. Our results support non-additive and unpredictable joint effects of temperature and litter quality, suggesting that these concomitant changes may affect stream functioning.

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References

  1. Aerts R (2006) The freezer defrosting: global warming and litter decomposition rates in cold biomes. J Ecol 94(4):713–724. https://doi.org/10.1111/j.1365-2745.2006.01142.x

    Article  Google Scholar 

  2. Atkinson D, Sibly RM (1997) Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends Ecol Evol 12(6):235–239. https://doi.org/10.1016/S0169-5347(97)01058-6

    CAS  Article  PubMed  Google Scholar 

  3. Balibrea A, Ferreira V, Gonçalves V, Raposeiro PM (2017) Consumption, growth and survival of the endemic stream shredder Limnephilus atlanticus (Trichoptera, Limnephilidae) fed with distinct leaf species. Limnologica 64:31–37. https://doi.org/10.1016/j.limno.2017.04.002

    Article  Google Scholar 

  4. Balseiro E, Albariño RJ (2006) C–N mismatch in the leaf litter–shredder relationship of an Andean Patagonian stream detritivore. J N Am Benthol Soc 25(3):607–615. https://doi.org/10.1899/0887-3593(2006)25%5B607:CMITLL%5D2.0.CO;2

    Article  Google Scholar 

  5. Bärlocher F (2005) Leaf mass loss estimated by litter bag technique. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition. Springer, Dordrescht, pp 37–42

    Chapter  Google Scholar 

  6. Battle M, Bender ML, Tans PP, White JWC, Ellis JT, Conway T, Francey RJ (2000) Global carbon sinks and their variability inferred from atmospheric O2 and δ13C. Science 287(5462):2467–2470. https://doi.org/10.1126/science.287.5462.2467

    CAS  Article  PubMed  Google Scholar 

  7. Boyero L, Pearson RG (2017) Global-scale coordinated networks as a tool for exploring the functioning of stream ecosystems. Limnetica 36:557–565

    Google Scholar 

  8. Boyero L, Pearson RG, Dudgeon D, Graça MAS, Gessner MO, Albariño RJ, Ferreira V, Yule CM, Boulton AJ, Arunachalam M, Callisto M, Chauvet E, Ramírez A, Chará J, Moretti MS, Gonçalves JF Jr, Helson JE, Chará-Serna AM, Encalada AC, Davies JN, Lamothe S, Cornejo A, Li AOY, Buria LM, Villanueva VD, Zúñiga MC, Pringle CM (2011) Global distribution of a key trophic guild contrasts with common latitudinal diversity patterns. Ecology 92(9):1839–1848. https://doi.org/10.1890/10-2244.1

    Article  PubMed  Google Scholar 

  9. Boyero L, Pearson RG, Dudgeon D, Ferreira V, Graça MAS, Gessner MO, Boulton AJ, Chauvet E, Yule CM, Albariño RJ, Ramírez A, Helson JE, Callisto M, Arunachalam M, Chará J, Figueroa R, Mathooko JM, Gonçalves JF Jr, Moretti M, Chará AM, Davie JN, Encalada AC, Lamothe S, Buria LM, Castela J, Cornejo A, Li AOY, M’erimba C, Villanueva VD, Zúñiga MC, Swan C, Barmuta LA (2012) Global patterns of stream detritivore distribution: implications for biodiversity loss in changing climates. Glob Ecol Biogeogr 21:134–141. https://doi.org/10.1111/j.1466-8238.2011.00673.x

    Article  Google Scholar 

  10. Boyero L, Graça MAS, Perez J, Pearson RG, Swafford A, Ferreira V, Landeira-Dabarca A, Tonin LM, Alexandrou M, Albarino RJ, Barmuta LA, Callisto M, Chara J, Chauvet E, Colon-Gaud C, Dudgeon D, Encalada AC, Figueroa R, Flecker AS, Fleituch T, Gessner MO, Goncalves JF Jr, Helson JE, Iwata T, Mathooko J, McKie BG, Pringle CM, Ramirez A, Swan CM, Yule CM (2017) Riparian plant litter quality increases with latitude. Scient Rep 7:10562. https://doi.org/10.1038/s41598-017-10640-3

    CAS  Article  Google Scholar 

  11. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789. https://doi.org/10.1890/03-9000

    Article  Google Scholar 

  12. Carvalho EM, Graça MAS (2007) A laboratory study on feeding plasticity of the shredder Sericostoma vittatum Rambur (Sericostomatidae). Hydrobiol 575:353–359. https://doi.org/10.1007/s10750-006-0383-x

    Article  Google Scholar 

  13. Cebrián J, Duarte CM (1995) Growth-rate dependence of detrital carbon storage in ecosystems. Science 268:1606–1608. https://doi.org/10.1126/science.268.5217.1606

    Article  PubMed  Google Scholar 

  14. Cebrián J, Lartigue J (2004) Patterns of herbivory and decomposition in aquatic and terrestrial ecosystems. Ecol Monogr 74:237–259. https://doi.org/10.1890/03-4019

    Article  Google Scholar 

  15. Cherif M, Iwabuchi T, Katano I, Stegen JC, Striebel M (2010) Integrating elements and energy through the metabolic dependencies of gross growth efficiency and the threshold elemental ratio. Oikos 119:752–765. https://doi.org/10.1111/j.1600-0706.2009.18540.x

    CAS  Article  Google Scholar 

  16. Conant RT, Drijber RA, Haddix ML, Parton WJ, Paul EA, Plante AF, Six J, Steinweg JM (2008) Sensitivity of organic matter decomposition to warming varies with its quality. Glob Change Biol 14:868–877. https://doi.org/10.1111/j.1365-2486.2008.01541.x

    Article  Google Scholar 

  17. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Pérez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, Van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Díaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M (2008) Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11(10):1065–1071. https://doi.org/10.1111/j.1461-0248.2008.01219.x

    Article  PubMed  Google Scholar 

  18. Correa-Araneda F, Boyero L, Figueroa R, Sánchez C, Abdala R, Ruiz-García A, Graça MAS (2015) Joint effects of climate warming and exotic litter (Eucalyptus globulus Labill.) on stream detritivore fitness and litter breakdown. Aquat Sci 77:197–205. https://doi.org/10.1007/s00027-014-0379-y

    Article  Google Scholar 

  19. Cruz-Rivera E, Hay ME (2000) Can quantity replace quality? Food choice, compensatory feeding, and fitness of marine mesograzers. Ecology 81:201–219. https://doi.org/10.1890/0012-9658(2000)081%5B0201:CQRQFC%5D2.0.CO;2

    Article  Google Scholar 

  20. Danger M, Cornut J, Chauvet E, Chavez P, Elger A, Lecerf A (2013) Benthic algae stimulate leaf litter decomposition in detritus-based headwater streams: a case of aquatic priming effect? Ecology 94:1604–1613. https://doi.org/10.1890/12-0606.1

    Article  PubMed  Google Scholar 

  21. Davidson EA, Janssens IA (2006) Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440:165–173. https://doi.org/10.1038/nature04514

    CAS  Article  PubMed  Google Scholar 

  22. Díaz-Villanueva V, Albariño R, Canhoto C (2011) Detritivores feeding on poor quality food are more sensitive to increased temperatures. Hydrobiol 678:155–165. https://doi.org/10.1007/s10750-011-0837-7

    CAS  Article  Google Scholar 

  23. Donnelly P, Entry J, Crawford D, Cromack K (1990) Cellulose and lignin degradation in forest soils: response to moisture, temperature, and acidity. Microb Ecol 20:289–295

    CAS  Article  Google Scholar 

  24. 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. https://doi.org/10.3389/fmicb.2017.01184

    Article  PubMed  PubMed Central  Google Scholar 

  25. Fernandes I, Pascoal C, Guimarães H, Pinto R, Sousa I, Cássio F (2012) Higher temperature reduces the effects of litter quality on decomposition by aquatic fungi. Freshw Biol 57:2306–2317. https://doi.org/10.1111/fwb.12004

    Article  Google Scholar 

  26. Ferreira V, Canhoto C (2014) Effect of experimental and seasonal warming on litter decomposition in a temperate stream. Aquat Sci 76:155–163. https://doi.org/10.1007/s00027-013-0322-7

    CAS  Article  Google Scholar 

  27. Ferreira V, Chauvet E (2011) Synergistic effects of water temperature and dissolved nutrients on litter decomposition and associated fungi. Glob Change Biol 17:551–564. https://doi.org/10.1111/j.1365-2486.2010.02185.x

    Article  Google Scholar 

  28. Fierer N, Craine JM, Mclaughlan K, Schimel J (2005) Litter quality and the temperature sensitivity of decomposition. Ecology 86:320–326. https://doi.org/10.1890/04-1254

    Article  Google Scholar 

  29. Flindt M, Lillebø A (2005) Determination of total nitrogen and phosphorus in leaf litter. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition. Springer, Dordrescht, pp 53–59

    Chapter  Google Scholar 

  30. Flores L, Larrañaga A, Elosegi A (2014) Compensatory feeding of a stream detritivore alleviates the effects of poor food quality when enough food is supplied. Freshw Sci 33:134–141. https://doi.org/10.1086/674578

    Article  Google Scholar 

  31. Follstad Shah JJ, Kominoski JS, Ardón M, Dodds WK, Gessner MO, Griffiths NA, Hawkins CP, Johnson SL, Lecerf A, LeRoy CJ, Manning DWP, Rosemond AD, Sinsabaugh RL, Swan CM, Webster JR, Zeglin LH (2017) Global synthesis of the temperature sensitivity of leaf litter breakdown in streams and rivers. Glob Change Biol 23:3064–3075. https://doi.org/10.1111/gcb.13609

    Article  Google Scholar 

  32. Forster J, Hirst AG, Woodward G (2011) Growth and development rates have different thermal responses. Am Nat 178:668–678. https://doi.org/10.1086/662174

    Article  PubMed  Google Scholar 

  33. Frainer A, Jabiol J, Gessner MO, Bruder A, Chauvet E, McKie BG (2016) Stoichiometric imbalances between detritus and detritivores are related to shifts in ecosystem functioning. Oikos 125:861–871. https://doi.org/10.1111/oik.02687

    CAS  Article  Google Scholar 

  34. Frost PC, Evans-White MA, Finkel ZV, Jensen TC, Matzek V (2005) Are you what you eat? Physiological constraints on organismal stoichiometry in an elementally imbalanced world. Oikos 109:18–25. https://doi.org/10.1111/j.0030-1299.2005.14049.x

    Article  Google Scholar 

  35. Fuller RL, Mackay RJ (1981) Effects of food quality on the growth of three Hydropsyche species (Trichoptera: Hydropsychidae). Can J Zool 59(6):1133–1140

    Article  Google Scholar 

  36. Galic N, Forbes VE (2017) Effects of temperature on the performance of a freshwater amphipod. Hydrobiol 785:35–46. https://doi.org/10.1007/s10750-016-2901-9

    Article  Google Scholar 

  37. Gessner MO, Steiner D (2005) Acid butanol assay for proanthocyanidins (condensed tannins). In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition. Springer, Dordrescht, pp 107–114

    Chapter  Google Scholar 

  38. González JM, Graça MAS (2003) Conversion of leaf litter to secondary production by a shredding caddisfly. Freshw Biol 48:1578–1592. https://doi.org/10.1046/j.1365-2427.2003.01110.x

    Article  Google Scholar 

  39. González AL, Romero GQ, Srivastava DS (2014) Detrital nutrient content determines growth rate and elemental composition of bromeliad-dwelling insects. Freshw Biol 59:737–747. https://doi.org/10.1111/fwb.12300

    CAS  Article  Google Scholar 

  40. Graça MAS, Cressa C (2010) Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Int Rev Hydrobiol 95(1):27–41. https://doi.org/10.1002/iroh.200911173

    Article  Google Scholar 

  41. Graça MAS, Poquet JM (2014) Do climate and soil influence phenotypic variability in leaf litter, microbial decomposition and shredder consumption? Oecologia 174:1021–1032. https://doi.org/10.1007/s00442-013-2825-2

    Article  PubMed  Google Scholar 

  42. Graça M, Zimmer M (2005) Leaf toughness. In: Graça MAS, Bärlocher F, Gessner MO (eds) Methods to study litter decomposition. Springer, Dordrescht, pp 121–125

    Chapter  Google Scholar 

  43. Handa IT, Aerts R, Berendse F, Berg MP, Bruder A, Butenschoen O, Chauvet E, Gessner MO, Jabiol J, Makkonen M, McKie BG, Malmqvist B, Peeters ETHM, Scheu S, Schmid B, van Ruijven J, Vos VCA, Hättenschwiler S (2014) Consequences of biodiversity loss for litter decomposition across biomes. Nature 509:218–221. https://doi.org/10.1038/nature13247

    CAS  Article  PubMed  Google Scholar 

  44. Hutchens JJ, Benfield EF, Webster JR (1997) Diet and growth of a leaf-shredding caddisfly in southern Appalachian streams of contrasting disturbance history. Hydrobiol 346:193–201. https://doi.org/10.1023/A:1002930419317

    Article  Google Scholar 

  45. IPCC (2007) Climate Change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge

    Google Scholar 

  46. Kendrick MR, Benstead JP (2013) Temperature and nutrient availability interact to mediate growth and body stoichiometry in a detritivorous stream insect. Freshw Biol 58:1820–1830. https://doi.org/10.1111/fwb.12170

    CAS  Article  Google Scholar 

  47. Kraus TE, Dahlgren RA, Zasoski RJ (2003) Tannins in nutrient dynamics of forest ecosystems—a review. Plant Soil 256:41–66. https://doi.org/10.1023/A:1026206511084

    CAS  Article  Google Scholar 

  48. Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76. https://doi.org/10.1038/35083573

    CAS  Article  PubMed  Google Scholar 

  49. Makkonen M, Berg MP, Handa IT, Hättenschwiler S, Ruijven J, Bodegom PM, Aerts R (2012) Highly consistent effects of plant litter identity and functional traits on decomposition across a latitudinal gradient. Ecol Lett 15(9):1033–1041. https://doi.org/10.1111/j.1461-0248.2012.01826.x

    Article  PubMed  Google Scholar 

  50. Manning DW, Rosemond AD, Kominoski JS, Gulis V, Benstead JP, Maerz JC (2015) Detrital stoichiometry as a critical nexus for the effects of streamwater nutrients on leaf litter breakdown rates. Ecology 96:2214–2224. https://doi.org/10.1890/14-1582.1

    Article  PubMed  Google Scholar 

  51. Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106. https://doi.org/10.1890/09-0179.1

    Article  Google Scholar 

  52. Martínez A, Monroy S, Pérez J, Larrañaga A, Basaguren A, Molinero J, Pozo J (2016) In-stream litter decomposition along an altitudinal gradient: does substrate quality matter? Hydrobiology 766:17–28. https://doi.org/10.1007/s10750-015-2432-9

    Article  Google Scholar 

  53. Mas-Martí E, Muñoz I, Oliva F, Canhoto C (2014) Effects of increased water temperature on leaf litter quality and detritivore performance: a whole-reach manipulative experiment. Freshw Biol 60:184–197. https://doi.org/10.1111/fwb.12485

    Article  Google Scholar 

  54. Mas-Martí E, Romaní AM, Muñoz I (2015) Consequences of warming and resource quality on the stoichiometry and nutrient cycling of a stream shredder. PLoS One 10(3):e0118520. https://doi.org/10.1371/journal.pone.0118520

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  55. McKie BG, Cranston PS, Pearson RG (2004) Gondwanan mesotherms and cosmopolitan eurytherms: effects of temperature on the development and survival of Australian Chironomidae (Diptera) from tropical and temperate populations. Mar Freshw Res 55:759–768. https://doi.org/10.1071/MF04023

    Article  Google Scholar 

  56. McKie BG, Schindler M, Gessner MO, Malmqvist B (2009) Placing biodiversity and ecosystem functioning in context: environmental perturbations and the effects of species richness in a stream field experiment. Oecologia 160:757–770. https://doi.org/10.1007/s00442-009-1336-7

    Article  PubMed  Google Scholar 

  57. Melillo JM, Aber JD, Muratore JF (1982) Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–626

    CAS  Article  Google Scholar 

  58. Mulder C, Elser JJ (2009) Soil acidity, ecological stoichiometry and allometric scaling in grassland food webs. Glob Change Biol 15:2730–2738. https://doi.org/10.1111/j.1365-2486.2009.01899.x

    Article  Google Scholar 

  59. Ott D, Rall BC, Brose U (2012) Climate change effects on macrofaunal litter decomposition: the interplay of temperature, body masses and stoichiometry. Philos Trans R Soc Lond B Biol Sci 367:3025–3032. https://doi.org/10.1098/rstb.2012.0240

    Article  PubMed  PubMed Central  Google Scholar 

  60. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891. https://doi.org/10.1111/j.1600-0706.2009.17643.x

    Article  Google Scholar 

  61. Pérez-Casanova JC, Lall SP, Gamperl AK (2009) Effect of feed composition and temperature on food consumption, growth and gastric evacuation of juvenile Atlantic cod (Gadus morhua L.) and haddock (Melanogrammus aeglefinus L.). Aquaculture 294:228–235. https://doi.org/10.1016/j.aquaculture.2009.06.005

    CAS  Article  Google Scholar 

  62. Quinn JM, Burrell GP, Parkyn SMN (2000) Influences of leaf toughness and nitrogen content on in-stream processing and nutrient uptake by litter in a Waikato, New Zealand, pasture stream and streamside channels. N Z J Mar Freshw Res 34:253–271. https://doi.org/10.1080/00288330.2000.9516931

    Article  Google Scholar 

  63. Reich PB, Oleksyn J (2004) Global patterns of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006. https://doi.org/10.1073/pnas.0403588101

    CAS  Article  PubMed  Google Scholar 

  64. Sanpera-Calbet I, Lecerf A, Chauvet E (2009) Leaf diversity influences in-stream litter decomposition through effects on shredders. Freshw Biol 54(8):1671–1682. https://doi.org/10.1111/j.1365-2427.2009.02216.x

    Article  Google Scholar 

  65. Schofield JA, Hagerman AE, Harold A (1998) Loss of tannins and other phenolics from willow leaf litter. J Chem Ecol 24(8):1409–1421. https://doi.org/10.1023/A:1021287018787

    CAS  Article  Google Scholar 

  66. Shay PE, Constabel CP, Trofymow JA (2018) Evidence for the role and fate of water-insoluble condensed tannins in the short-term reduction of carbon loss during litter decay. Biogeochemistry 137(1–2):127–141. https://doi.org/10.1007/s10533-017-0406-x

    CAS  Article  Google Scholar 

  67. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  68. Sweeney BW, Vannote RL, Dodds PJ (1986) Effects of temperature and food quality on growth and development of a mayfly, Leptophlebia intermedia. Can J Fish Aquat Sci 43:12–18

    Article  Google Scholar 

  69. Tonin AM, Boyero L, Monroy S, Basaguren A, Pérez J, Pearson RG, Cardinale BJ, Gonçalves JF Jr, Pozo J (2017) Stream nitrogen concentration, but not plant N-fixing capacity, modulates litter diversity effects on decomposition. Funct Ecol 31(7):1471–1481. https://doi.org/10.1111/1365-2435.12837

    Article  Google Scholar 

  70. Tuchman NC, Wahtera KA, Wetzel RG, Russo NM, Kilbane GM, Sasso LM, Teeri JA (2003) Nutritional quality of leaf detritus altered by elevated atmospheric CO2: effects on development of mosquito larvae. Freshw Biol 48:1432–1439. https://doi.org/10.1046/j.1365-2427.2003.01102.x

    Article  Google Scholar 

  71. Woodward G, Perkins DM, Brown LE (2010) Climate change and freshwater ecosystems: impacts across multiple levels of organization. Philos Trans R Soc Lond B Biol Sci 365:2093–2106. https://doi.org/10.1098/rstb.2010.0055

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank the members of the Global Litter Breakdown Experiments (GLoBE) network who helped with leaf collection, Veronica Ferreira for field and laboratory work advice, Igor Morais and Joana Sotaia for the field survey, and Cristina Grela Docal for leaf chemical analyses. The study was funded by start-up funds from the Doñana Biological Station (EBD-CSIC) and Ikerbasque to LB, the Fundação para a Ciência e Tecnologia (FCT) strategic project ID/MAR/04292/2013 granted to MARE (Portugal), a research fellowship from Universidade de Vigo to ALD, and Basque Government funds (IT302-16) to Jesús Pozo.

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Correspondence to Andrea Landeira-Dabarca.

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Landeira-Dabarca, A., Pérez, J., Graça, M.A.S. et al. Joint effects of temperature and litter quality on detritivore-mediated breakdown in streams. Aquat Sci 81, 1 (2019). https://doi.org/10.1007/s00027-018-0598-8

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Keywords

  • Shredder
  • Consumption
  • Growth
  • Leaf traits
  • Warming