Hostname: page-component-78c5997874-4rdpn Total loading time: 0 Render date: 2024-11-19T17:46:20.581Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparison of three shredders response to acute stress induced by eucalyptus leaf leachates and copper: single and combined exposure at two distinct temperatures

Published online by Cambridge University Press:  20 March 2014

M. Gama ,
L. Guilhermino  and
C. Canhoto
M. Gama*
Affiliation:
IMAR & Department of Life Sciences, University of Coimbra, 3004-517 Coimbra, Portugal CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, Laboratory of Ecotoxicology and Ecology, University of Porto, Rua dos Bragas, 289, 4050-123 Porto, Portugal
L. Guilhermino
Affiliation:
CIIMAR – Interdisciplinary Centre of Marine and Environmental Research, Laboratory of Ecotoxicology and Ecology, University of Porto, Rua dos Bragas, 289, 4050-123 Porto, Portugal ICBAS – Institute of Biomedical Sciences of Abel Salazar, Department of Populations Studies, Laboratory of Ecotoxicology, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050-313 Porto, Portugal
C. Canhoto
Affiliation:
IMAR & Department of Life Sciences, University of Coimbra, 3004-517 Coimbra, Portugal
*
*Corresponding author: [email protected]
Get access

Abstract

The objectives of this study were to compare the sensitivity of three freshwater macroinvertebrate shredder species (Atyaephyra desmarestii, Echinogammarus meridionalis and Schizopelex festiva) to acute stress induced by eucalyptus leaf extracts and copper, independently and in mixtures, and the ability of temperature to influence the chemicals’ toxicity. Laboratory bioassays based on mortality with single substances and mixtures were carried out with the three species at 10 and 20°C. After 96 h of exposure, S. festiva, A. desmarestii and E. meridionalis were found to have differences of sensitivity to copper, eucalyptus leaf extracts and their mixtures, with S. festiva being the least sensitive species at both 10 and 20°C. The relative sensitivity of A. desmarestii and E. meridionalis to chemical exposure seems to be chemical and temperature dependent. Overall, these findings suggest that chemical stress may modulate the biodiversity of stream shredders communities due to differential sensitivity of individual species to environmental contaminants, and that temperature may influence the process. Thus, more knowledge on the combined effects of multi-stressors is needed, particularly on temperature and chemicals’ interactions and on the molecular mechanisms underlying the responses observed at individual level.

Keywords

Chemical acute toxicitycombined effects of stressorsAtyaephyra desmarestiiEchinogammarus meridionalisSchizopelex festiva
Type
Research Article
Information
Annales de Limnologie - International Journal of Limnology , Volume 50 , Issue 2 , 2014 , pp. 97 - 107
Copyright
© EDP Sciences, 2014

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abele, D., Burlando, B., Viarengo, A. and Pfrtner, H.O., 1998. Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. Comp. Biochem. Physiol. B, 120, 425–435.CrossRefGoogle Scholar
Abele, D., Heise, K., Pfrtner, H.O. and Puntarulo, S., 2002. Temperature dependence of mitochondrial function and production of reactive oxygen species in the intertidal mud clam Mya arenaria. J. Exp. Biol., 205, 1831–1841.Google ScholarPubMed
Allan, J.D. and Castillo, M.M., 2007. Stream Ecology (2nd edn,), Springer, Dordrecht, The Netherlands, 436 p.CrossRefGoogle Scholar
ASTM – American Society for Testing and Materials., 1980. Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E – 790-80. American Society for Testing and Materials, Philadelphia.
Batista, D., Pascoal, C. and Cássio, F., 2012. Impacts of warming on aquatic decomposers along a gradient of cadmium stress. Environ. Pollut., 169, 35–41.CrossRefGoogle ScholarPubMed
Boeckman, C.J. and Bidwell, J.R., 2006. The effects of temperature, suspended solids, and organic carbon on copper toxicity to two aquatic invertebrates. Water Air Soil Pollut., 171, 185–202.CrossRefGoogle Scholar
Bouskill, N.J., Handy, R.D., Ford, T.E. and Galloway, T.S., 2006. Differentiating copper and arsenic toxicity using biochemical biomarkers in Asellus aquaticus and Dreissena polymorpha. Ecotox. Environ. Safe., 65, 342–349.CrossRefGoogle ScholarPubMed
Boveris, A., Musacco-Sebio, R., Ferrarotti, N., Saporito-Magriñá, C., Torti, H., Massot, F. and Repetto, M.G., 2012. The acute toxicity of iron and copper: biomolecule oxidation and oxidative damage in rat liver. J. Inorg. Biochem., 116, 63–69.CrossRefGoogle ScholarPubMed
Brix, K.V., DeForest, D.K. and Adams, W.J., 2011. The sensitivity of aquatic insects to divalent metals: a comparative analysis of laboratory and field data. Sci. Total Environ., 409, 4187–4197.CrossRefGoogle ScholarPubMed
Cain, D.J. and Luoma, S.N., 1998. Metal exposures to native populations of caddisfly Hydropsyche (Trichoptera: Hydropsychedae) determined from cytosolic and whole body metal concentrations. Hydrobiologia, 386, 103–117.CrossRefGoogle Scholar
Canhoto, C. and Graça, M.A.S., 1999. Leaf barriers to fungal colonization and shredders (Tipula lateralis) consumption of decomposing Eucalyptus globulus. Microb. Ecol., 37, 163–172.CrossRefGoogle ScholarPubMed
Canhoto, C. and Laranjeira, C., 2007. Leachates of Eucalyptus globulus in intermittent streams affect water parameters and invertebrates. Int. Rev. Hydrobiol., 92(2), 173–182.CrossRefGoogle Scholar
Canhoto, C., Calapez, R., Gonçalves, A.L. and Moreira-Santos, M., 2013. Effects of Eucalyptus leachates and oxygen on leaf-litter processing by fungi and stream invertebrates. Freshwat. Sci., 32(2), 411–424.CrossRefGoogle Scholar
Chatzinikolaou, Y., Dakos, V. and Lazaridou, M., 2006. Longitudinal impacts of anthropogenic pressures on benthic macroinvertebrate assemblages in a large transboundary Mediterranean river during the low flow period. Acta Hydrochim. Hydrobiol., 34, 453–463.CrossRefGoogle Scholar
Cummins, K.W., 1973. Trophic relations of aquatic insects. Annu. Rev. Entomol., 18, 183–206.CrossRefGoogle Scholar
Darlington, S.T. and Gower, A.M., 1990. Location of copper in larvae of Plectrocnemia conspersa (Curtis) (Trichoptera) exposed to elevated metal concentrations in a mine drainage stream. Hydrobiologia, 196, 91–100.CrossRefGoogle Scholar
Dédourge-Geffard, O., Palais, F., Biagianti-Risbourg, S., Geffard, O. and Geffard, A., 2009. Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere, 77, 1569–1576.CrossRefGoogle ScholarPubMed
De Schamphelaere, K.A.C. and Janssen, C.R., 2004. Development and field validation of a biotic ligand model predicting chronic copper toxicity to Daphnia magna. Environ. Toxicol. Chem., 23, 1365–1375.CrossRefGoogle ScholarPubMed
Dudgeon, D., Arthington, A.H., Gessner, M.O., Kawabata, Z., Knowler, D.J., Lévêque, C., Naiman, R.J., Prieur-Richard, A., Soto, D., Stiassny, M.L.J. and Sullivan, C.A., 2006. Freshwater biodiversity: importance, threats, status and conservation challenges. Biol. Ver., 81, 163–182.Google ScholarPubMed
Farag, A.M., Woodward, D.F., Goldstein, J.N., Brumbaugh, W. and Meyer, J.S., 1998. Concentrations of metals associated with mining waste in sediments, biofilm, benthic macroinvertebrates, and fish from the Coeur d'Alene river basin, Idaho. Arch. Environ. Contam. Toxicol., 34, 119–127.CrossRefGoogle Scholar
Faria, M.S., Lopes, R.J., Nogueira, A.J.A. and Soares, A.M.V.M., 2007. In situ and laboratory bioassays with Chironomus riparius larvae to assess toxicity of metal contamination in rivers: the relative toxic effect of sediment versus water contamination. Environ. Toxicol. Chem., 26, 1968–1977.CrossRefGoogle ScholarPubMed
Faria, M.S., Lopes, R.J., Malcato, J., Nogueira, A.J.A. and Soares, A.M.V.M., 2008. In situ bioassays with Chironomus riparius larvae to biomonitor metal pollution in rivers and to evaluate the efficiency of restoration measures in mine areas. Environ. Pollut., 151, 213–221.CrossRefGoogle ScholarPubMed
Felten, V. and Guérold, F., 2006. Short-term physiological responses to a severe acid stress in three macroinvertebrate species: a comparative study. Chemosphere, 63, 1427–1435.CrossRefGoogle ScholarPubMed
Felten, V., Baudoin, J.M. and Guérold, F., 2006. Physiological recovery from episodic acid stress does not mean population recovery of Gammarus fossarum. Chemosphere, 65, 988–998.CrossRefGoogle Scholar
Felten, V., Charmantier, G., Charmantier-Daures, M., Aujoulat, F., Garric, J. and Geffard, O., 2008. Physiological and behavioural responses of Gammarus pulex exposed to acid stress. Comp. Biochem. Physiol C, 147, 189–197.Google ScholarPubMed
Ferreira, V., Gonçalves, A.L., Godbold, D.W. and Canhoto, C., 2010. Effect of increased atmospheric CO2 on the performance of an aquatic detritivore through changes in water temperature and litter quality. Glob. Change Biol., 16, 3284–3296.CrossRefGoogle Scholar
Forrow, D.M. and 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(8), 2100–2106.CrossRefGoogle Scholar
Gerhardt, A., Janssens de Bisthoven, L. and Soares, A.M.V.M., 2004. Macroinvertebrate response to acid mine drainage: community metrics and on-line behavioural toxicity bioassay. Environ. Pollut., 130, 263–274.CrossRefGoogle ScholarPubMed
Gessner, M.O., Swan, C.M., Dang, C.K., McKie, B.G., Bardgett, R.D., Wall, D.H. and Hättenschwiler, S., 2010. Diversity meets decomposition. Trends Ecol. Evol., 25, 372–380.CrossRefGoogle ScholarPubMed
Gomes, S.I.L., Novais, S.C., Gravato, C., Guilhermino, L., Scott-Fordsmand, J.J., Soares, A.M.V.M. and Amorim, M.J.B., 2012. Effect of Cu-nanoparticles versus one Cu-salt: analysis of stress biomarkers response in Enchytraeus albidus (Oligochaeta). Nanotoxicology, 6(2), 134–143.CrossRefGoogle Scholar
Graça, M.A.S., Pozo, J., Canhoto, C. and Elosegi, A., 2002. Effects of Eucalyptus plantations on detritus, decomposers, and detritivores in streams. Sci. World, 2, 1173–1185.CrossRefGoogle ScholarPubMed
Graça, M.A.S., Bärlocher, S.F. and Gessner, M.O., 2005. Methods to Study Litter Decomposition: A Practical Guide, Springer, The Netherlands, 329 p.CrossRefGoogle Scholar
Grosell, M., Nielsen, C. and Bianchini, A., 2002. Sodium turnover rate determines sensitivity to acute copper and silver exposure in freshwater animals. Comp. Biochem. Physiol. C, 133, 287–303.Google ScholarPubMed
Heise, K., Puntarulo, S., Pfrtner, H.O. and Abele, D., 2003. Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress. Comp. Biochem. Physiol. C, 134, 79–90.Google ScholarPubMed
Hogsden, K.L. and Harding, J.S., 2012. Consequences of acid mine drainage for the structure and function of benthic stream communities: a review. Freshwat. Sci., 31, 108–120.CrossRefGoogle Scholar
Huang, F., Rabson, D. and Chen, W., 2009. Distribution of the Na/K Pumps’ turnover rates as a function of membrane potential, temperature, and ion concentration gradients and effect of fluctuations. J. Phys. Chem. B., 113, 8096–8102.CrossRefGoogle Scholar
IPCC, 2007. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. In: Pachauri, R.K. and Reisinger, A. (eds.), Core Writing Team, IPCC, Geneva, Switzerland, 104 p.Google Scholar
Janssens de Bisthoven, L., Gerhardt, A., Guhr, K. and Soares, A.M.V.M., 2006. Behavioral changes and acute toxiciy to the freshwater shrimp Atyaephyra desmarestii Millet (Decapoda: Natantia) from exposure to acid mine drainage. Ecotoxicology, 15, 215–227.CrossRefGoogle Scholar
Kominoski, J.S., Follstad Shah, J.J., Canhoto, C., Fischer, D.G., Giling, D.P., González, E., Griffiths, N.A., Larrañaga, A., LeRoy, C.J., Mineau, M.M., McElarney, Y.R., Shirley, S.M., Swan, C.M., and Tiegs, S.D., 2013. Forecasting functional implications of global changes in riparian plant communities. Front. Ecol. Environ., 11, 423–432.CrossRefGoogle Scholar
Lapointe, D., Pierron, F. and Couture, P., 2011. Individual and combined effects of heat stress and aqueous or dietary copper exposure in fathead minnows (Pimephales promelas). Aquat. Toxicol., 104, 80–85.CrossRefGoogle Scholar
Larrañaga, A., Basarugen, A. and Pozo, J., 2009. Impacts of Eucalyptus globulus plantations on physiology and population densities of invertebrates inhabiting Iberian Atlantic streams. Int. Rev. Hydrobiol., 94(4), 497–511.CrossRefGoogle Scholar
Lecerf, A. and Richardson, J.S., 2010. Litter decomposition can detect effects of high and moderate levels of forest disturbance on stream condition. Forest Ecol. Manage., 259, 2433–2443.CrossRefGoogle Scholar
Leslie, H.A., Pavluk, T.I., Bij de Vaate, A. and Kraak, M.H.S., 1999. Triad assessment of the impact of chromium contamination on benthic macroinvertebrates in the Chusovaya River (Urals, Russia). Arch. Environ. Contam. Toxicol., 37, 182–189.CrossRefGoogle Scholar
Liess, M. and Beketov, M., 2011. Traits and stress: keys to identify community effects of low levels of toxicants in test systems. Ecotoxicology, 20, 1328–1340.CrossRefGoogle ScholarPubMed
Liess, M. and Schulz, R., 1999. Linking insecticide contamination and population response in an agricultural stream. Environ. Toxicol. Chem., 18(9), 1948–1955.CrossRefGoogle Scholar
Macedo-Sousa, J.A., Pestana, J.L.T., Gerhardt, A., Nogueira, A.J.A. and Soares, A.M.V.M., 2007. Behavioural and feeding responses of Echinogammarus meridionalis (Crustacea, Amphipoda) to acid mine drainage. Chemosphere, 67, 1663–1670.CrossRefGoogle ScholarPubMed
Macedo-Sousa, J. A., Gerhardt, A., Brett, C.M.A., Nogueira, A.J.A. and Soares, A.M.V.M., 2008. Behavioural responses of indigenous benthic invertebrates (Echinogammarus meridionalis, Hydropsyche pellucidula and Choroterpes picteti) to a pulse of Acid Mine Drainage: a laboratorial study. Environ. Pollut., 156, 966–973.CrossRefGoogle ScholarPubMed
Malmqvist, B. and Rundle, S., 2002. Threats to the running water ecosystems of the world. Environ. Conserv., 29, 134–153.CrossRefGoogle Scholar
Maltby, L. and Hills, L., 2008. Spray drift of pesticides and stream macroinvertebrates: experimental evidence of impacts and effectiveness of mitigation measures. Environ. Pollut., 156, 1112–1120.CrossRefGoogle ScholarPubMed
Maria, V.L. and Bebianno, M.J., 2011. Antioxidant and lipid peroxidation responses in Mytilus galloprovincialis exposed to mixtures of benzo(a)pyrene and copper. Comp. Biochem. Physiol. C, 154, 56–63.Google Scholar
McFeeters, B.J. and Frost, P.C., 2011. Temperature and the effects of elemental food quality on Daphnia. Freshwat. Biol., 56, 1447–1455.CrossRefGoogle Scholar
McMahon, T.A., Halstead, N.T., Johnson, S., Raffel, T.R., Romansic, J.M., Crumrine, P.W. and Rohr, J.R., 2012. Fungicide-induced declines of freshwater biodiversity modify ecosystem functions and services. Ecol. Lett., 15, 714–722.CrossRefGoogle ScholarPubMed
Molinero, J. and Pozo, J., 2004. Impact of a eucalyptus (Eucalyptus globulus Labill.) plantation on the nutrient content and dynamics of coarse particulate organic matter (CPOM) in a small stream. Hydrobiologia, 528, 143–165.CrossRefGoogle Scholar
Morrill, J.C., Bales, R.C. and Conklin, M.H., 2005. Estimating stream temperature from air temperature: implications for future water quality. J. Environ. Eng., 131(1), 139–146.CrossRefGoogle Scholar
Olivari, F.A., Hernández, P.P. and Allende, M.L., 2008. Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res., 124, 1–12.CrossRefGoogle Scholar
Ormerod, S. J., Dobson, M., Hildrew, A.G. and Townsend, C.R., 2010. Multiple stressors in freshwater ecosystems. Freshwat. Bio., 55(1), 1–4.CrossRefGoogle Scholar
Pantani, C., Pannunzio, G., DeCristofaro, M., Novelli, A.A. and Salvatori, M., 1997. Comparative acute toxicity of some pesticides, metals, and surfactants to Gammarus italicus Goedm and Echinogammarus tibaldii Pink, and stock (Crustacea: Amphipoda). Bull. Environ. Contam. Toxicol., 59, 963–967.CrossRefGoogle Scholar
Paquin, P.R., Gorsuch, J.W., Apte, S., Batley, G.E., Bowles, K.C., Campbell, P.G.C., Delos, C.G., Di Toro, D.M., Dwyer, R.L., Galvez, F., Gensemer, R.W., Goss, G.G., Hogstrand, C., Janssen, C.R., McGreer, J.C., Naddy, R.B., Playle, R.C., Santore, R.C., Schneider, U., Stubblefield, W.A., Wood, C.M., Wu, K.B., 2002. The biotic ligand model: a historical overview. Comp. Biochem. Physiol. C, 133, 3–35.Google ScholarPubMed
Perkins, D.M., Reiss, J., Yvon-Durocher, G. and Woodward, G., 2010. Global change and food webs in running waters. Hydrobiologia, 657, 181–198.CrossRefGoogle Scholar
Pestana, J.L.T., Ré, A., Nogueira, A.J.A. and Soares, A.M.V.M., 2007. Effects of cadmium and zinc on the feeding behavior of two freshwater crustaceans: Atyaephyra desmarestii (Decapoda) and Echinogammarus meridionalis (Amphipoda). Chemosphere, 68, 1556–1562.CrossRefGoogle Scholar
Peters, A., Crane, P. and Adams, W.J., 2011. Effects of iron on Benthic Macroinvertebrate Communities in the field. Bull. Environ. Contam. Toxicol., 86, 591–595.CrossRefGoogle ScholarPubMed
Pradhan, A., Seena, S., Pascoal, C. and Cássio, F., 2012. Copper oxide nanoparticles can induce toxicity to the freshwater shredder Allogamus ligonifer. Chemosphere, 89, 1142–1150.CrossRefGoogle ScholarPubMed
Prato, E., Biandolino, F. and Scardicchio, C., 2009. Effects of temperature on the sensitivity of Gammarus aequicauda (Martynov, 1931) to cadmium. Bull. Environ. Contam. Toxicol., 83, 469–473.CrossRefGoogle ScholarPubMed
Rainbow, P.S., 2002. Trace metal concentrations in aquatic invertebrates: why and so what? Environ. Pollut., 120, 497–507.CrossRefGoogle Scholar
Rainbow, P.S., 2007. Trace metal bioaccumulation: models, metabolic availability and toxicity. Environ. Int., 33, 576–582.CrossRefGoogle ScholarPubMed
Rainbow, P.S., Hildrew, A.G., Smith, B.D., Geatches, T. and Luoma, S. N., 2012. Caddisflies as biomonitors identifying thresholds of toxic metal bioavailability that affect the stream benthos. Environ. Pollut., 166, 196–207.CrossRefGoogle ScholarPubMed
Richardson, J.S. and Danehy, R.J., 2007. A synthesis of the ecology of headwater streams and their riparian zones in temperate forests. Forest Sci., 53, 131–147.Google Scholar
Roy, D.N., Mandal, S., Sen, G. and Biswas, T., 2009. Superoxide anion mediated mitochondrial dysfunction leads to hepatocyte apoptosis preferentially in the periportal region during copper toxicity in rats. Chem. Biol. Interact., 182, 136–147.CrossRefGoogle ScholarPubMed
Sacchetti, G., Maietti, S., Muzzoli, M., Scaglianti, M., Manfredini, S., Radice, M. and Bruni, R., 2005. Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chem., 91, 621–632.CrossRefGoogle Scholar
Sanpéra-Calbet, I., Lecerf, A. and Chauvet, E., 2009. Leaf diversity influences in-stream litter decomposition through effects on shredders. Freshwat. Bio., 54, 1671–1682.CrossRefGoogle Scholar
Santore, R.C., Di Toro, D.M., Paquin, P.R., Allen, H.E. and Meyer, J.S., 2001. Biotic ligand model of the acute toxicity of metals. 2. Application to acute copper toxicity in freshwater fish and daphnia. Environ. Toxicol. Chem., 20(10), 2397–2402.2.0.CO;2>CrossRefGoogle ScholarPubMed
Santos, R.L., 1997. The Eucalyptus of California: Seeds of Good or Seeds of Evil, Alley-Cass Publications, Denair, CA.Google Scholar
Singh, H.P., Kaur, S., Negi, K., Kumari, S., Saini, V., Batish, D.R. and Kohli, R.K., 2012. Assessment of in vitro antioxidant activity of essential oil of Eucalyptus citriodora (lemon-scented Eucalypt; Myrtaceae) and its major constituents. Food Sci. Technol., 48, 237–241.Google Scholar
Sroda, S. and Cossu-Leguille, C., 2011. Effects of sublethal copper exposure on two gammarid species: which is the best competitor? Ecotoxicology, 20, 264–273.CrossRefGoogle ScholarPubMed
Tattersall, G.J., Sinclair, B.J., Withers, P.C., Fields, P.A., Seebacher, F., Cooper, C.E. and Maloney, S. K., 2012. Coping with thermal challenges: physiological adaptations to environmental temperatures. Compr. Physiol., 2, 2151–2202.Google ScholarPubMed
Vannote, R.L., Minshall, G.W., Cummins, K.W., Sedell, J.R. and Cushing, C.E., 1980. The river continuum concept. Can. J. Fish. Aquat. Sci., 37, 130–137.CrossRefGoogle Scholar
Vieira, L.R. and Guilhermino, L., 2012. Multiple stress effects on marine planktonic organisms: influence of temperature on the toxicity of polycyclic aromatic hydrocarbons to Tetraselmis chuii. J. Sea Res., 72, 94–98.CrossRefGoogle Scholar
Vieira, L.R., Gravato, C., Soares, A.M.V.M., Morgado, F. and Guilhermino, L., 2009. Acute effects of copper and mercury on the estuarine fish Pomatoschistus microps: linking biomarkers to behavior. Chemosphere, 76, 1416–1427.CrossRefGoogle Scholar
Wojewodzic, M.W., Rachamim, T. and Hessen, D.O., 2011. Effect of temperature and dietary elemental composition on RNA/protein ratio in a rotifer. Funct. Ecol., 25, 1154–1160.CrossRefGoogle Scholar
Woodcock, T.S. and Huryn, A.D., 2005. Leaf litter processing and invertebrate assemblages along a pollution gradient in a Maine (USA) headwater stream. Environ. Pollut., 134, 363–375.CrossRefGoogle Scholar
Woodward, G., Perkins, D.M. and Brown, L.E., 2010. Climate change and freshwater ecosystems: impacts across multiple levels of organization. Phil. Trans. R. Soc. Lond. B Biol. Sci., 365, 2093–210.CrossRefGoogle ScholarPubMed

OLM_limn130038

Appendixes

Download OLM_limn130038(Audio)
Audio 41.8 KB