Ecotoxicology

, Volume 23, Issue 5, pp 830–839 | Cite as

Effects of cadmium and resource quality on freshwater detritus processing chains: a microcosm approach with two insect species

  • Diana Campos
  • Artur Alves
  • Marco F. L. Lemos
  • António Correia
  • Amadeu M. V. M. Soares
  • João L. T. Pestana
Article

Abstract

Detritus processing is vital for freshwater ecosystems that depend on the leaf litter from riparian vegetation and is mediated by microorganisms and aquatic invertebrates. Shredder invertebrates transform coarse particulate organic matter into fine particulate organic matter used as food by collector species. Direct and indirect effects of contaminants can impair detritus processing and thus affect the functioning of these ecosystems. Here, we assessed the combined effects of a toxic metal (cadmium) and resource quality (leaf species) on detritus processing and shredder-collector interactions. We considered two types of leaves, alder and eucalyptus that were microbially conditioned under different Cd concentrations in the laboratory. The microbial communities present on leaves were analyzed by Denaturing Gradient Gel Electrophoresis (DGGE), and we also measured microbial respiration rates. Sericostoma vittatum (a caddisfly shredder) and Chironomus riparius (a midge collector) were also exposed to Cd and allowed to consume the corresponding alder or eucalyptus leaves. We evaluated C. riparius growth and leaf mass loss in multispecies microcosms. Cadmium exposure affected leaf conditioning and fungal diversity on both leaf species, as assessed by DGGE. Cadmium exposure also affected the mass loss of alder leaves by reductions in detritivore feeding, and impaired C. riparius growth. Chironomus riparius consumed alder leaf discs in the absence of shredders, but S. vittatum appear to promote C. riparius growth in treatments containing eucalyptus. These results show that indirect effects of contaminants along detritus-processing chains can occur through effects on shredder-collector interactions such as facilitation but they also depend on the nutritional quality of detritus and on sensitivity and feeding plasticity of detritivore species.

Keywords

Shredder-collector interactions Facilitation Indirect effects Leaf decomposition Chironomus 

Notes

Acknowledgments

We are grateful to two anonymous reviewers for their comments and suggestions that greatly improved this manuscript. Financial support for this work was provided by the projects “MIDGE - MIcroevolutionary Dynamics and Genetic Erosion in pollution-affected Chironomus populations” ref: FCOMP-01-0124-FEDER-008954 (Ref. FCT PTDC/BIA-BEC/104125/2008) and project “IDEAL—Insecticides, DEtritivores and ALiens: Combined effects of invasive species and insecticides along detritus based stream food webs”, ref: FCOMP-01-0124-FEDER-019380 (Ref. FCT: PTDC/AAC-AMB/119433/2010) both supported by the COMPETE program (Programa Operacional Fatores de Competitividade,) (FEDER component) and by the Fundação para a Ciência e Tecnologia (FCT). FCT also financed a post-doctoral research grant to JLT Pestana (SFRH/BPD/45342/2008). AMVM Soares is “Bolsista CAPES/BRASIL”, Project NºA058/2013. This work was supported by European Funds through COMPETE and by National Funds through the Portuguese Science Foundation (FCT) within project PEst-C/MAR/LA0017/2013.

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Arsuffi TL, Suberkropp K (1989) Selective feeding by shredders on leaf-colonizing stream fungi: comparison of macroinvertebrate taxa. Oecologia 79:30–37CrossRefGoogle Scholar
  2. Bärlocher F, Graça MAS (2002) Exotic riparian vegetation lowers fungal diversity but not leaf decomposition in Portuguese streams. Freshwater Biol 47:1123–1135CrossRefGoogle Scholar
  3. Batish DR, Singh HP, Kohli RK, Kaur S (2008) Eucalyptus essential oil as a natural pesticide. Forest Ecol Manag 256:2166–2174Google Scholar
  4. Batista D, Pascoal C, Cássio F (2012) Impacts of warming on aquatic decomposers along a gradient of cadmium stress. Environ Pollut 169:35–41CrossRefGoogle Scholar
  5. Blockwell SJ, Taylor EJ, Jones I, Pascoe D (1998) The influence of fresh water pollutants and interaction with Asellus aquaticus (L.) on the feeding activity of Gammarus pulex (L.). Arch Environ Con Tox 34:41–47CrossRefGoogle Scholar
  6. Brix KV, DeForest DK, Adams WJ (2011) The sensitivity of aquatic insects to divalent metals: A comparative analysis of laboratory and field data. Sci Total Environ 409:4187–4197CrossRefGoogle Scholar
  7. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  8. Bundschuh M, Zubrod JP, Kosol S et al (2011) Fungal composition on leaves explains pollutant-mediated indirect effects on amphipod feeding. Aquat Toxicol 104:32–37CrossRefGoogle Scholar
  9. Callisto M, Goncalves JF, Graça MAS (2007) Leaf litter as a possible food source for chironomids (Diptera) in Brazilian and Portuguese headwater streams. Rev Bras Zool 24:442–448CrossRefGoogle Scholar
  10. Calow P (1991) Physiological costs of combating chemical toxicants: ecological implications. Comp Biochem Phys C 100:3–6CrossRefGoogle Scholar
  11. Campos J, Gonzalez JM (2009) Sericostoma vittatum (Trichoptera) Larvae are able to use pine litter as an energy source. Int Rev Hydrobiol 94:472–483CrossRefGoogle Scholar
  12. Canhoto C, Graça MAS (1996) Decomposition of Eucalyptus globulus leaves and three native leaf species (Alnus glutinosa, Castanea sativa and Quercus faginea) in a Portuguese low order stream. Hydrobiologia 333:79–85CrossRefGoogle Scholar
  13. Canhoto C, Graça M (1999) Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus. Microb Ecol 37:163–172CrossRefGoogle Scholar
  14. Canhoto C, Laranjeira C (2007) Leachates of eucalyptus globulus in intermittent streams affect water parameters and invertebrates. Internat Rev Hydrobiol 92:173–182Google Scholar
  15. Cardinale BJ, Palmer MA, Collins SL (2002) Species diversity enhances ecosystem functioning through interspecific facilitation. Nature 415:426–429CrossRefGoogle Scholar
  16. Costantini M, Rossi L (1998) Competition between two aquatic detritivorous isopods - a laboratory study. Hydrobiologia 368:17–27CrossRefGoogle Scholar
  17. Costantini ML, Rossi L (2010) Species diversity and decomposition in laboratory aquatic systems: the role of species interaction. Freshwater Biol 55:2281–2295Google Scholar
  18. Daugherty MP, Juliano SA (2002) Testing for context-dependence in a processing chain interaction among detritus-feeding aquatic insects. Ecol Entomol 27:541–553CrossRefGoogle Scholar
  19. De Coen WM, Janssen CR (2003) The missing biomarker link: relationships between effects on the cellular energy allocation biomarker of toxicant-stressed Daphnia magna and corresponding population characteristics. Environ Toxicol Chem 22:1632–1641CrossRefGoogle Scholar
  20. Diaz Villanueva V, Albarino R, Canhoto C (2011) Detritivores feeding on poor quality food are more sensitive to increased temperatures. Hydrobiologia 678:155–165CrossRefGoogle Scholar
  21. Dietrich M, Anderson NH, Anderson T (1997) Shredder-collector interactions in temporary streams of western Oregon. Freshwater Biol 38:387–393CrossRefGoogle Scholar
  22. Englert D, Bundschuh M, Schulz R (2012) Thiacloprid affects trophic interaction between gammarids and mayflies. Environ Pollut 167:41–46CrossRefGoogle Scholar
  23. Faria MS, Ré A, Malcato J et al (2006) Biological and functional responses of in situ bioassays with Chironomus riparius larvae to assess river water quality and contamination. Sci The Total Environ 371:125–137CrossRefGoogle Scholar
  24. Feio M, Graça M (2000) Food consumption by the larvae of Sericostoma vittatum (Trichoptera), an endemic species from the Iberian Peninsula. Hydrobiologia 439:7–11CrossRefGoogle Scholar
  25. Fernandes I, Pascoal C, Cássio F (2011) Intraspecific traits change biodiversity effects on ecosystem functioning under metal stress. Oecologia 166:1019–1028CrossRefGoogle Scholar
  26. Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317:207–233CrossRefGoogle Scholar
  27. Forrow DM, Maltby L (2000) Toward a mechanistic understanding of contaminant-induced changes in detritus processing in streams: Direct and indirect effects on detritivore feeding. Environ Toxicol Chem 19:2100–2106CrossRefGoogle Scholar
  28. Fugère V, Andino P, Espinosa R et al (2012) Testing the stress-gradient hypothesis with aquatic detritivorous invertebrates: insights for biodiversity-ecosystem functioning research. J Anim Ecology 81:1259–1267CrossRefGoogle Scholar
  29. Gardes M, Bruns TT (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118Google Scholar
  30. Gessner M, Chauvet E (2002) A case for using litter breakdown to assess functional stream integrity. Ecol Appl 12:498–510CrossRefGoogle Scholar
  31. Gessner MO, Swan CM, Dang CK et al (2010) Diversity meets decomposition. Trends Ecol Evol 25:372–380CrossRefGoogle Scholar
  32. Golovanova IL (2008) Effects of heavy metals on the physiological and biochemical status of fishes and aquatic invertebrates. Inland Water Biol 1:93–101CrossRefGoogle Scholar
  33. Graça MAS, Canhoto C (2006) Leaf litter processing in low order streams. Limnetica 25:1–10Google Scholar
  34. Graça MAS, Cressa C (2010) Leaf quality of some tropical and temperate tree species as food resource for stream shredders. Internat Rev Hydrobiol 95:27–41CrossRefGoogle Scholar
  35. Graça M, Cressa C, Gessner M et al (2001) Food quality, feeding preferences, survival and growth of shredders from temperate and tropical streams. Freshwater Biol 46:947–957CrossRefGoogle Scholar
  36. Graça MAS, Pozo J, Canhoto C, Elosegi A (2002) Effects of eucalyptus plantations on detritus, decomposers, and detritivores in streams. Sci World J 2:1173–1185CrossRefGoogle Scholar
  37. Greig H, McIntosh A (2006) Indirect effects of predatory trout on organic matter processing in detritus-based stream food webs. Oikos 112:31–40CrossRefGoogle Scholar
  38. Heard SB (1994) Processing chain ecology: resource condition and interspecific interactions. J Anim Ecol 63:451–464Google Scholar
  39. Heard SB, Richardson JS (1995) Shredder-collector facilitation in stream detrital food webs - Is there enough evidence. Oikos 72:359–366CrossRefGoogle Scholar
  40. Hernandez AD, Sukhdeo MVK (2008) Parasite effects on isopod feeding rates can alter the host’s functional role in a natural stream ecosystem. Int J Parasitol 38:683–690CrossRefGoogle Scholar
  41. Hill WR, Ryon MG, Schilling EM (1995) Light limitation in a stream ecosystem: responses by primary producers and consumers. Ecology 76:1297–1309CrossRefGoogle Scholar
  42. Hullett CR, Levine TR (2003) The overestimation of effect Sizes from F values in meta-analysis: the cause and a solution. Commun Monogr 70:52–67CrossRefGoogle Scholar
  43. Iwai N, Pearson RG, Alford RA (2009) Shredder–tadpole facilitation of leaf litter decomposition in a tropical stream. Freshwater Biol 54:2573–2580CrossRefGoogle Scholar
  44. Jabiol J, McKie BG, Bruder A et al (2013) Trophic complexity enhances ecosystem functioning in an aquatic detritus-based model system. J Anim Ecology 82:1042–1051CrossRefGoogle Scholar
  45. Janssens L, Stoks R (2013) Exposure to a widespread non-pathogenic bacterium magnifies sublethal pesticide effects in the damselfly Enallagma cyathigerum: From the suborganismal level to fitness-related traits. Environ Pollut 177:143–149CrossRefGoogle Scholar
  46. Jonsson M, Malmqvist B (2003) Mechanisms behind positive diversity effects on ecosystem functioning: testing the facilitation and interference hypotheses. Oecologia 134:554–559Google Scholar
  47. Kawai T, Tokeshi M (2007) Testing the facilitation-competition paradigm under the stress-gradient hypothesis: decoupling multiple stress factors. Proc Biol Sci 274:2503–2508CrossRefGoogle Scholar
  48. Larrañaga A, Basaguren A, Elosegi A, Pozo J (2009) Impacts of Eucalyptus globulus plantations on Atlantic streams: changes in invertebrate density and shredder traits. Fund App Lim 175:151–160CrossRefGoogle Scholar
  49. Luís AT, Teixeira P, Almeida SFP et al (2011) Environmental impact of mining activities in the Lousal area (Portugal): Chemical and diatom characterization of metal-contaminated stream sediments and surface water of Corona stream. Sci Total Environ 409:4312–4325CrossRefGoogle Scholar
  50. McKie BG, Woodward G, Hladyz S et al (2008) Ecosystem functioning in stream assemblages from different regions: contrasting responses to variation in detritivore richness, evenness and density. J Anim Ecology 77:495–504CrossRefGoogle Scholar
  51. Moreirinha C, Duarte S, Pascoal C, Cássio F (2011) Effects of cadmium and phenanthrene mixtures on aquatic fungi and microbially mediated leaf litter decomposition. Arch Environ Contam Toxicol 61:211–219CrossRefGoogle Scholar
  52. Murrell EG, Juliano SA (2008) Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera: Culicidae). J Med Entomol 45:375–383CrossRefGoogle Scholar
  53. Naylor C, Maltby L, Calow P (1989) Scope for growth in Gammarus-Pulex, a fresh-water benthic detritivore. Hydrobiologia 188/189:517–523Google Scholar
  54. Paradise CJ (2000) Effects of pH and Resources on a Processing Chain Interaction in Simulated Treeholes. J Anim Ecology 69:651–658CrossRefGoogle Scholar
  55. Paradise CJ, Dunson WA (1997) Insect species interactions and resource effects in treeholes: are helodid beetles bottom-up facilitators of midge populations? Oecologia 109:303–312CrossRefGoogle Scholar
  56. Pascoal C, Cássio F (2004) Contribution of fungi and bacteria to leaf litter decomposition in a polluted river. Appl Environ Microb 70:5266–5273CrossRefGoogle Scholar
  57. Pérez J, Descals E, Pozo J (2012) Aquatic Hyphomycete communities associated with decomposing alder leaf litter in reference headwater streams of the Basque Country (northern Spain). Microb Ecol 64:279–290CrossRefGoogle Scholar
  58. Pestana JLT, Ré A, Nogueira AJ, Soares AMVM (2007) Effects of Cadmium and Zinc on the feeding behaviour of two freshwater crustaceans: Atyaephyra desmarestii (Decapoda) and Echinogammarus meridionalis (Amphipoda). Chemosphere 68:1556–1562CrossRefGoogle Scholar
  59. Pestana JLT, Alexander AC, Culp JM et al (2009a) Structural and functional responses of benthic invertebrates to imidacloprid in outdoor stream mesocosms. Environ Pollut 157:2328–2334CrossRefGoogle Scholar
  60. Pestana JLT, Loureiro S, Baird DJ, Soares AMVM (2009b) Fear and loathing in the benthos: Responses of aquatic insect larvae to the pesticide imidacloprid in the presence of chemical signals of predation risk. Aquat Toxicol 93:138–149CrossRefGoogle Scholar
  61. Peters K, Bundschuh M, Schäfer RB (2013) Review on the effects of toxicants on freshwater ecosystem functions. Environ Pollut 180:324–329CrossRefGoogle Scholar
  62. Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171CrossRefGoogle Scholar
  63. Rohr JR, Kerby JL, Sih A (2006) Community ecology as a framework for predicting contaminant effects. Trends Ecol Evol 21:606–613CrossRefGoogle Scholar
  64. Roussel H, Chauvet E, Bonzom J-M (2008) Alteration of leaf decomposition in copper-contaminated freshwater mesocosms. Environ Toxicol Chem 27:637–644CrossRefGoogle Scholar
  65. Ruetz C, Newman R, Vondracek B (2002) Top-down control in a detritus-based food web: fish, shredders, and leaf breakdown. Oecologia 132:307–315CrossRefGoogle Scholar
  66. Soares HM, Boaventura RA, Machado AA, Esteves da Silva JC (1999) Sediments as monitors of heavy metal contamination in the Ave river basin (Portugal): multivariate analysis of data. Environ Pollut 105:311–323CrossRefGoogle Scholar
  67. Srivastava DS, Bell T (2009) Reducing horizontal and vertical diversity in a foodweb triggers extinctions and impacts functions. Ecol Lett 12:1016–1028CrossRefGoogle Scholar
  68. Starzomski BM, Suen D, Srivastava DS (2010) Predation and facilitation determine chironomid emergence in a bromeliad-insect food web. Ecol Entomol 35:53–60CrossRefGoogle Scholar
  69. Stief P, de Beer D (2002) Bioturbation effects of Chironomus riparius on the benthic N-cycle as measured using microsensors and microbiological assays. Aquat Microb Ecol 27:175–185CrossRefGoogle Scholar
  70. Stoler AB, Relyea RA (2013) Bottom-up meets top-down: leaf litter inputs influence predator-prey interactions in wetlands. Oecologia 173:249–257CrossRefGoogle Scholar
  71. Vannote RL, Minshall GW, Cummins KW, et al. (1980) The river continuum concept. Can J Fish Aquat Sci 37:130–137Google Scholar
  72. Wallace JB (1997) Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–104CrossRefGoogle Scholar
  73. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: A guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  74. Woodward G, Papantoniou G, Edwards F, Lauridsen RB (2008) Trophic trickles and cascades in a complex food web: impacts of a keystone predator on stream community structure and ecosystem processes. Oikos 117:683–692CrossRefGoogle Scholar
  75. Yee DA, Kaufman MG, Juliano SA (2007) The significance of ratios of detritus types and micro-organism productivity to competitive interactions between aquatic insect detritivores. J Anim Ecology 76:1105–1115CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Diana Campos
    • 1
  • Artur Alves
    • 1
  • Marco F. L. Lemos
    • 1
    • 2
  • António Correia
    • 1
  • Amadeu M. V. M. Soares
    • 1
    • 3
  • João L. T. Pestana
    • 1
  1. 1.Departamento de Biologia and CESAMUniversidade de AveiroAveiroPortugal
  2. 2.ESTM & GIRMInstituto Politécnico de LeiriaPenichePortugal
  3. 3.Programa de Pós-Graduação em Produção VegetalUniversidade Federal do TocantinsGurupiBrazil

Personalised recommendations