Effects of fish predators and litter pack size on leaf breakdown in a subtropical stream

  • Chih-Wei Tsai
  • Sen-Her Shieh
  • Ya-Hui Huang
  • Mei-Yin Lai
Primary Research Paper

Abstract

Many studies have examined trophic cascades in allochthonous lotic systems of temperate streams, but few have examined those in subtropical and tropical streams. Many subtropical and tropical streams are characterised as detritivore-poor stream systems, which might result in a fundamental difference in the trophic cascades of brown food webs. We performed an in situ experiment to test the effects of the presence or absence of a small-bodied endemic benthic fish and of the mass of litter packs (five levels), arranged in a full factorial design (10 treatments), on macroinvertebrate detritivore assemblages and invertebrate-mediated breakdown rates and to identify possible trophic cascades. Fish slightly reduced the invertebrate-mediated breakdown rates by depressing detritivore abundance. Effects of fish predators and litter pack size on detritivore abundance were species dependent. Nemouridae (Plecoptera), a non-camouflage detritivore (without a casing), was highly sensitive to the presence of fish predators. By contrast, camouflaged detritivores, such as Stenochironomus spp. (Diptera), which mine decayed leaves, and Anisocentropus sp. (Trichoptera), a case-building caddisfly, were able to avoid being preyed upon and thereby buffered the effect of predation on litter processing. These results suggest that ecosystem functioning of detritus-based stream systems could be regulated by the traits of dominant detritivores.

Keywords

Density-mediated Detritivores Macroinvertebrates Trait-mediated Trophic cascade 

Notes

Acknowledgements

We thank many volunteers who participated in the field work, in particular Jin-An Yu and two anonymous referees for helpful suggestions on various drafts of the manuscript. Thanks to the Ministry of Science and Technology, Taiwan for the support of this work through a funding (MOST 103-2313-B-126-001).

References

  1. Bartlett, M. S., 1937. Properties of sufficiency and statistical tests. Proceedings of the Royal Society of London A 160: 268–282.CrossRefGoogle Scholar
  2. Bates, D., M. Maechler & B. Bolker, 2012. lme4: Linear mixed-effects models using S4 classes. In: http://cran.r-project.org/web/packages/lme4/index.html.
  3. Boyero, L., R. G. Pearson & R. Camacho, 2006. Leaf breakdown in tropical streams: the role of different species in ecosystem functioning. Archiv für Hydrobiologie 166: 453–466.CrossRefGoogle Scholar
  4. Bruder, A., M. H. Schindler, M. S. Moretti & M. O. Gessner, 2014. Litter decomposition in a temperate and a tropical stream: the effects of species mixing, litter quality and shredders. Freshwater Biology 59: 438–449.CrossRefGoogle Scholar
  5. Bruder, A., R. K. Salis, P. E. Jones & C. D. Matthaei, 2017. Biotic interactions modify multiple-stressor effects on juvenile brown trout in an experimental stream food web. Global Change Biology 23: 3882–3894.CrossRefPubMedGoogle Scholar
  6. Cebrian, J., 1999. Patterns in the fate of production in plant communities. The American Naturalist 154: 449–468.CrossRefPubMedGoogle Scholar
  7. Chen, J.-P., C. K.-C. Wen, P.-J. Meng, K. L. Cherh & K.-T. Shao, 2015. Ain’t no mountain high enough: the impact of severe typhoon on montane stream fishes. Environmental Biology of Fishes 98: 35–44.CrossRefGoogle Scholar
  8. Chen, L.-H., K. C.-M. Chu & Y.-W. Chiu, 2004. Impacts of natural disturbance on fish communities in the Tachia River, Taiwan. Hydrobiologia 522: 149–164.CrossRefGoogle Scholar
  9. Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.CrossRefGoogle Scholar
  10. Crawley, M. J., 2007. The R Book. John Wiley & Sons, England.CrossRefGoogle Scholar
  11. Dobson, M., A. Magana, J. M. Mathooko & F. K. Ndegwa, 2002. Detritivores in Kenyan highland streams: more evidence for the paucity of shredders in the tropics? Freshwater Biology 47: 909–919.CrossRefGoogle Scholar
  12. Dudgeon, D., 1999. Tropical Asian Stream: Zoobenthos, Ecology, and Conservation. Hong Kong University Press, Hong Kong.Google Scholar
  13. Eggert, S. L. & J. B. Wallace, 2003. Litter breakdown and invertebrate detritivores in a resource-depleted Appalachian stream. Archiv für Hydrobiologie 156: 315–338.CrossRefGoogle Scholar
  14. Gessner, M. O. & E. Chauvet, 1994. Importance of stream microfungi in controlling breakdown rates of leaf litter. Ecology 75: 1807–1817.CrossRefGoogle Scholar
  15. Gessner, M. O., C. M. Swan, C. K. Dang, B. G. McKie, R. D. Bardgett, D. H. Wall & S. Hättenschwiler, 2010. Diversity meets decomposition. Trends in Ecology & Evolution 25: 372–380.CrossRefGoogle Scholar
  16. González-Bergonzoni, I., P. B. Kristensen, A. Baattrup-Pedersen, E. A. Kristensen, A. B. Alnoee & T. Riis, 2018. Riparian forest modifies fuelling sources for stream food webs but not food-chain length in lowland streams of Denmark. Hydrobiologia 805: 291–310.CrossRefGoogle Scholar
  17. Greig, H. S. & A. R. McIntosh, 2006. Indirect effects of predatory trout on organic matter processing in detritus-based stream food webs. Oikos 112: 31–40.CrossRefGoogle Scholar
  18. Ho, B. S. K. & D. Dudgeon, 2016. Are high densities of fishes and shrimp associated with top-down control of tropical benthic communities? A test in three Hong Kong streams. Freshwater Biology 61: 57–68.CrossRefGoogle Scholar
  19. Horng, F.-W., H.-M. Yu & F.-C. Ma, 1995. Typhoons of 1994 doubled the annual litterfall of the Fu-Shan mixed hardwood forest ecosystem in Northeastern Taiwan. Bulletin of Taiwan Forestry Research Institute 10: 485–491.Google Scholar
  20. Hsia, Y.-J. & C.-L. Huang, 1999. Hydrological characteristics of Fushan Experimental Forest. Quarterly Journal of Chinese Forestry 32: 39–51.Google Scholar
  21. Hsia, Y.-J., L.-J. Wang, C.-L. Huang & H.-B. King, 1996. Pathways of hillslope runoff in the Fushan watershed. Quarterly Journal of Chinese Forestry 11: 481–486.Google Scholar
  22. Huang, I., Y. Lin, C. Chen & H. Hsieh, 2007. Food web structure of a subtropical headwater stream. Marine and Freshwater Research 58: 596–607.CrossRefGoogle Scholar
  23. Jabiol, J., B. G. McKie, A. Bruder, C. Bernadet, M. O. Gessner & E. Chauvet, 2013. Trophic complexity enhances ecosystem functioning in an aquatic detritus-based model system. Journal of Animal Ecology 82: 1042–1051.CrossRefPubMedGoogle Scholar
  24. Jabiol, J., J. Cornut, M. Danger, M. Jouffroy, A. Elger & E. Chauvet, 2014. Litter identity mediates predator impacts on the functioning of an aquatic detritus-based food web. Oecologia 176: 225–235.CrossRefPubMedGoogle Scholar
  25. Jarque, C. M. & A. K. Bera, 1987. A test for normality of observations and regression residuals. International Statistical Review/Revue Internationale de Statistique 55: 163–172.Google Scholar
  26. Jones, D. L., 2015. Fathom Toolbox for Matlab: software for multivariate ecological and oceanographic data analysis. In: College of Marine Science, University of South Florida. http://www.marine.usf.edu/user/djones/.
  27. Kath, J., E. Harrison, B. J. Kefford, L. Moore, P. J. Wood, R. B. Schäfer & F. Dyer, 2016. Looking beneath the surface: using hydrogeology and traits to explain flow variability effects on stream macroinvertebrates. Ecohydrology 9: 1480–1495.CrossRefGoogle Scholar
  28. Kato, M., 2015. Intense inhabitation and relaxed host-leaf preference of aquatic chironomid leaf-miners in headwater streams in Asian lucidophyllous forests. Journal of Natural History 49: 1891–1903.CrossRefGoogle Scholar
  29. Kawai, T. & K. Tanida, 2005. Aquatic Insects of Japan: Manual with Keys and Illustrastions. Tokai University Press, Kanagawa.Google Scholar
  30. Klemmer, A. J. & J. S. Richardson, 2013. Quantitative gradient of subsidies reveals a threshold in community-level trophic cascades. Ecology 94: 1920–1926.CrossRefPubMedGoogle Scholar
  31. Kobayashi, S. & T. Kagaya, 2008. Differences in patches of retention among leaves, woods and small litter particles in a headwater stream: the importance of particle morphology. Limnology 9: 47–55.CrossRefGoogle Scholar
  32. Kochi, K., T. Asaeda, T. Chibana & T. Fujino, 2009. Physical factors affecting the distribution of leaf litter patches in streams: comparison of green and senescent leaves in a step-pool streambed. Hydrobiologia 628: 191–201.CrossRefGoogle Scholar
  33. Kochi, K. & T. Kagaya, 2005. Green leaves enhance the growth and development of a stream macroinvertebrate shredder when senescent leaves are available. Freshwater Biology 50: 656–667.CrossRefGoogle Scholar
  34. Koljonen, S., P. Louhi, A. Mäki-Petäys, A. Huusko & T. Muotka, 2012. Quantifying the effects of in-stream habitat structure and discharge on leaf retention: implications for stream restoration. Freshwater Science 31: 1121–1130.CrossRefGoogle Scholar
  35. Konishi, M., S. Nakano & T. Iwata, 2001. Trophic cascading effects of predatory fish on leaf litter processing in a Japanese stream. Ecological Research 16: 415–422.CrossRefGoogle Scholar
  36. Kuznetsova, A., P. B. Brockhoff & R. H. B. Christensen, 2013. lmerTest: tests for random and fixed effects for linear mixed effect models (lmer objects of lme4 package). In: https://cran.r-project.org/web/packages/lmerTest/index.html.
  37. Lecerf, A. & J. S. Richardson, 2011. Assessing the functional importance of large-bodied invertebrates in experimental headwater streams. Oikos 120: 950–960.CrossRefGoogle Scholar
  38. Leroux, S. J. & M. Loreau, 2008. Subsidy hypothesis and strength of trophic cascades across ecosystems. Ecology Letters 11: 1147–1156.CrossRefPubMedGoogle Scholar
  39. Li, A. O. Y. & D. Dudgeon, 2009. Shredders: species richness, abundance, and role in litter breakdown in tropical Hong Kong streams. Journal of the North American Benthological Society 28: 167–180.CrossRefGoogle Scholar
  40. Lin, T.-C., S. P. Hamburg, H.-B. King & Y.-J. Hsia, 2000. Throughfall patterns in a subtropical rain forest of northeastern Taiwan. Journal of Environmental Quality 29: 1186–1193.CrossRefGoogle Scholar
  41. Lin, T.-C., S. P. Hamburg, K.-C. Lin, L.-J. Wang, C.-T. Chang, Y.-J. Hsia, M. A. Vadeboncoeur, C. M. Mabry McMullen & C.-P. Liu, 2011. Typhoon disturbance and forest dynamics: lessons from a Northwest Pacific subtropical forest. Ecosystems 14: 127–143.CrossRefGoogle Scholar
  42. MATLAB, 2009. Version 7.8.0.347 R2009a. The MathWorks, Inc., Natick.Google Scholar
  43. Mazerolle, M., 2006. Improving data analysis in herpetology: using Akaike’s Information Criterion (AIC) to assess the strength of biological hypotheses. Amphibia-Reptilia 27: 169–180.CrossRefGoogle Scholar
  44. Melillo, J. M., J. D. Aber & J. F. Muratore, 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63: 621–626.CrossRefGoogle Scholar
  45. Merritt, R. W., K. W. Cummins & M. B. Berg, 2008. An Introduction to the Aquatic Insects of North America. Kendall/Hunt Publishing Company, Dubuque.Google Scholar
  46. Mfilinge, P. L., T. Meziane, Z. Bachok & M. Tsuchiya, 2005. Litter dynamics and particulate organic matter outwelling from a subtropical mangrove in Okinawa Island, South Japan. Estuarine, Coastal and Shelf Science 63: 301–313.CrossRefGoogle Scholar
  47. Naiman, R. J., J. M. Melillo, M. A. Lock, T. E. Ford & S. R. Reice, 1987. Longitudinal patterns of ecosystem processes and community structure in a subarctic river continuum. Ecology 68: 1139–1156.CrossRefGoogle Scholar
  48. Nakagawa, S. & H. Schielzeth, 2013. A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods in Ecology and Evolution 4: 133–142.CrossRefGoogle Scholar
  49. Nakano, S., H. Miyasaka & N. Kuhara, 1999. Terrestrial-aquatic linkages: riparian anthropod inputs alter trophic cascades in a stream food web. Ecology 80: 2435–2441.Google Scholar
  50. Peng, J.-H., 1999. Study on Coarse Particulate Organic Matter Budget in the Hapen Creek. National Taiwan University, Taipei.Google Scholar
  51. Peng, W.-H., 2013. The leaf litter composition and its use by macroinvetebrates at streams in Fushan area. Master Thesis, Providence University.Google Scholar
  52. Petersen, R. C. & K. W. Cummins, 1974. Leaf processing in a woodland stream. Freshwater Biology 4: 343–368.CrossRefGoogle Scholar
  53. Polis, G. A., W. B. Anderson & R. D. Holt, 1997. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28: 289–316.CrossRefGoogle Scholar
  54. R Core Team., 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.Google Scholar
  55. Rodríguez-Lozano, P., M. Rieradevall & N. Prat, 2016. Top predator absence enhances leaf breakdown in an intermittent stream. Science of The Total Environment 572: 1123–1131.CrossRefPubMedGoogle Scholar
  56. Rodríguez-Lozano, P., I. Verkaik, M. Rieradevall & N. Prat, 2015. Small but powerful: top predator local extinction affects ecosystem structure and function in an intermittent stream. PLoS ONE 10: e0117630.CrossRefPubMedPubMedCentralGoogle Scholar
  57. Rosa, B. F. J. V., V. C. Oliveira & R. G. Alves, 2011. Structure and spatial distribution of the Chironomidae community in mesohabitats in a first order stream at the Poço D’Anta Municipal Biological Reserve in Brazil. Journal of Insect Science 11: 36.PubMedGoogle Scholar
  58. Ruetz, C., R. Newman & B. Vondracek, 2002. Top-down control in a detritus-based food web: fish, shredders, and leaf breakdown. Oecologia 132: 307–315.CrossRefPubMedGoogle Scholar
  59. Satterthwaite, F. E., 1946. An approximate distribution of estimates of variance components. Biometrics Bulletin 2: 110–114.CrossRefPubMedGoogle Scholar
  60. Schmitz, O. J., P. A. Raymond, J. A. Estes, W. A. Kurz, G. W. Holtgrieve, M. E. Ritchie, D. E. Schindler, A. C. Spivak, R. W. Wilson, M. A. Bradford, V. Christensen, L. Deegan, V. Smetacek, M. J. Vanni & C. C. Wilmers, 2014. Animating the carbon cycle. Ecosystems 17: 344–359.CrossRefGoogle Scholar
  61. Shieh, S.-H., C.-B. Hsu, C.-P. Wang & P.-S. Yang, 2007. Leaf breakdown in a subtropical stream riffle and its association with macroinvertebrates. Zoological Studies 46: 609–621.Google Scholar
  62. Sitvarin, M. I., A. L. Rypstra & J. D. Harwood, 2016. Linking the green and brown worlds through nonconsumptive predator effects. Oikos 125(8): 1057–1068.CrossRefGoogle Scholar
  63. Taylor, B. R. & E. E. Chauvet, 2014. Relative influence of shredders and fungi on leaf litter decomposition along a river altitudinal gradient. Hydrobiologia 721: 239–250.CrossRefGoogle Scholar
  64. Terborgh, J. & J. A. Estes, 2010. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Island Press, Washington.Google Scholar
  65. Tiegs, S. D., F. D. Peter, C. T. Robinson, U. Uehlinger & M. O. Gessner, 2008. Leaf decomposition and invertebrate colonization responses to manipulated litter quantity in streams. Journal of the North American Benthological Society 27: 321–331.CrossRefGoogle Scholar
  66. Vanni, M. J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33: 341–370.CrossRefGoogle Scholar
  67. Wallace, J. B., S. L. Eggert, J. L. Meyer & J. R. Webster, 1999. Effects of resource limitation on a detrital-based ecosystem. Ecological Monographs 69: 409–442.CrossRefGoogle Scholar
  68. Wantzen, K. M. & R. Wagner, 2006. c. Journal of the North American Benthological Society 25: 216–232.CrossRefGoogle Scholar
  69. Werner, E. E. & S. D. Peacor, 2003. A review of trait-mediated indirect interactions in ecological communities. Ecology 84: 1083–1100.CrossRefGoogle Scholar
  70. Wiggins, G. B., 1996. Larvae of the North American Caddisfly genera (Trichoptera). University of Toronto Press, Toronto.Google Scholar
  71. Woodward, G., G. Papantoniou, F. Edwards & R. B. Lauridsen, 2008. Trophic trickles and cascades in a complex food web: impacts of a keystone predator on stream community structure and ecosystem processes. Oikos 117: 683–692.CrossRefGoogle Scholar
  72. Wu, C.-C., 1999. Suspended and dissolved phophorous concentration dynamics and output in the fushan forest stream. Master Thesis, National Taiwan University, Taipei.Google Scholar
  73. Wu, M.-Y., P.-Y. Hsu & S.-T. Chang, 2010. Feeding ecology of the endemic goby (Rhinogobius candidianus) in Chinshui Creek, Taiwan. Taiwan Journal of Biodiversity 12: 367–380.Google Scholar
  74. Wu, X., J. N. Griffin, X. Xi & S. Sun, 2015. The sign of cascading predator effects varies with prey traits in a detrital system. Journal of Animal Ecology 84: 1610–1617.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Ecological HumanitiesProvidence UniversityTaichungTaiwan
  2. 2.Shu Tang Information Technology (Shenzhen) Co., Ltd.ShenzhenChina
  3. 3.Add Care LtdKowloonHong Kong

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