Does wetland watershed land use influence amphibian larval development? A relevant effect of agriculture on biota
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摘要
Agriculture practices have been widely proposed as the major cause of amphibian population decline. However, the majority of these results have been based on laboratory experiments. The present study was conducted to test the repercussion of wetland sediment provenance on amphibian larval development.Bufo bufo larvae were used in two dif ferent treatments in an outdoor experiment, the ?rst one using sediment from one wetland surrounded by intensive agricultural practices, and the second using sediment with no record of agrochemical uses. A negative ef fect was observed in the agricultural treatment, from subcellular to individual level. The results showed that the sediment from agricultural practices watershed generates a reduction in survival. Furthermore, individuals that developed under this treatment showed a lower total length and a delay in the time necessary to complete metamorphosis; these features are connected with recruitment success. In the same way, biochemical analysis showed high values of lipid peroxidation in metamorphs developing in sediments from an agricultural area. Finally, the results obtained highlight the importance of considering the sediments, not only the water, as origin treatment, allowing us to understand the consequences on amphibian populations that inhabit areas af fected by intensive agriculture.
Agriculture practices have been widely proposed as the major cause of amphibian population decline. However, the majority of these results have been based on laboratory experiments. The present study was conducted to test the repercussion of wetland sediment provenance on amphibian larval development.Bufo bufo larvae were used in two dif ferent treatments in an outdoor experiment, the ?rst one using sediment from one wetland surrounded by intensive agricultural practices, and the second using sediment with no record of agrochemical uses. A negative ef fect was observed in the agricultural treatment, from subcellular to individual level. The results showed that the sediment from agricultural practices watershed generates a reduction in survival. Furthermore, individuals that developed under this treatment showed a lower total length and a delay in the time necessary to complete metamorphosis; these features are connected with recruitment success. In the same way, biochemical analysis showed high values of lipid peroxidation in metamorphs developing in sediments from an agricultural area. Finally, the results obtained highlight the importance of considering the sediments, not only the water, as origin treatment, allowing us to understand the consequences on amphibian populations that inhabit areas af fected by intensive agriculture.
Agriculture practices have been widely proposed as the major cause of amphibian population decline. However, the majority of these results have been based on laboratory experiments. The present study was conducted to test the repercussion of wetland sediment provenance on amphibian larval development.Bufo bufo larvae were used in two dif ferent treatments in an outdoor experiment, the ?rst one using sediment from one wetland surrounded by intensive agricultural practices, and the second using sediment with no record of agrochemical uses. A negative ef fect was observed in the agricultural treatment, from subcellular to individual level. The results showed that the sediment from agricultural practices watershed generates a reduction in survival. Furthermore, individuals that developed under this treatment showed a lower total length and a delay in the time necessary to complete metamorphosis; these features are connected with recruitment success. In the same way, biochemical analysis showed high values of lipid peroxidation in metamorphs developing in sediments from an agricultural area. Finally, the results obtained highlight the importance of considering the sediments, not only the water, as origin treatment, allowing us to understand the consequences on amphibian populations that inhabit areas af fected by intensive agriculture.
引文
Altwegg R,Reyer H U.2003.Patterns of natural selection on size at metamorphosis in water frogs.Evolution,57(4):872-882.
American Public Health Association.1995.Standard methods for the examination of water and wastewater.American Public Health Association,Washington,DC.874p.
Andreu V,PicóY.2004.Determination of pesticides and their degradation products in soils:current status,gaps and the future.Journal of Limnology,64:13-29.
Araújo C V M,Tornero V,Lubián L M,Blasco J,van Bergeijk S A,Ca?avate P,Cidá,Franco D,Prado R,Bartual A,López M G,Ribeiro R,Moreira-Santos M,Torreblanca A,Jurado B,Moreno-Garrido I.2010.Ring test for wholesediment toxicity assay with-a-benthic marine diatom.Science of the Total Environment,408(4):822-828.
Baier F,Jedinger M,Gruber E,Zaller J G.2016.Temperaturedependence of glyphosate-based herbicide’s ef fects on egg and tadpole growth of common toads.Frontiers in Environmental Science,4:51.
Barata C,Varo I,Navarro J C,Arun S,Porte C.2005.Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds.Comparative Biochemistry and Physiology Part C:Toxicology&Pharmacology,140(2):175-186.
Barnett M L,Mathisen A M.1997.Tyranny of the P-value:The con?ict between statistical signi?cance and common sense.Journal of Dental Research,76(1):534-536.
Beck C W,Congdon J D.2003.Energetics of metamorphic climax in the southern toad(Bufo terrestris).Oecologia,137(3):344-351.
Beja P,Alcazar R.2003.Conservation of Mediterranean temporary ponds under agricultural intensi?cation:an evaluation using amphibians.Biolog ical Conservation,114(3):317-326.
Bókony V,MikóZ,MóriczáM,Krüzselyi D,Hettyey A.2017.Chronic exposure to a glyphosate-based herbicide makes toad larvae more toxic.Proc eedings of the Royal Society B,284(1858):20170493.
Boone M D,James S M.2003.Interactions of an insecticide,herbicide,and natural stressors in amphibian community mesocosms.Ecological Applications,13(3):829-841.
Boone M D,Semlitsch R D.2002.Interactions of an insecticide with competition and pond drying in amphibian communities.Ecological Applications,12(1):307-316.
Bradford M M.1976.A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Analytical Biochemistry,72(1-2):248-254.
Breden F,Kelly C H.1982.The ef fect of conspeci?c interactions on metamorphosis in Bufo americanus.Ecology,63(6):1 682-1 689.
Brunelli E,BernabòI,Berg C,Lundstedt-Enkel K,Bonacci A,Tripepi S.2009.Environmentally relevant concentrations of endosulfan impair development,metamorphosis and behaviour in Bufo bufo tadpoles.Aquatic Toxicology,91(2):135-142.
Burton Jr G A.2013.Sediment ecotoxicity.In:Férard J F,Blaise C eds.Encyclopedia of Aquatic Ecotoxicology.Springer,Dordrecht.p.1 003-1 014.
Camargo J B D A,Cruz A C F,Campos B G,Araújo G S,Fonseca T G,Abessa D M S.2015.Use,development and improvements in the protocol of whole-sediment toxicity identi?cation evaluation using benthic copepods.Marine Pollution Bulletin,91(2):511-517.
Casado C,Montes C.1995.Guide of Spanish lakes and wetlands.In:Reyero J M ed.Madrid.293p.
Cavas L,Tarhan L.2003.Glutathione redox system,GSH-Px activity and lipid peroxidation(LPO)levels in tadpoles of R ridibunda and B.viridis.Cell Biochemistry and Function,21(1):75-79.
Congdon J D,Dunham A E,Hopkins W A,Rowe C L,Hinton T G.2001.Resource allocation-based life histories:a conceptual basis for studies of ecological toxicology.Environmental Toxicology and Chemistry,20(8):1 698-1 703.
Cooke A S.1973.The ef fects of DDT,when used as a mosquito larvicide,on tadpoles of the frog Rana temporaria.Environmental Pollution,5(4):259-273.
Courcelles D M M.2016.Inorganic?ne sediment deposition in rivers with run-of-river hydropower projects and Coastal Tailed Frog(Ascaphus truei)tadpoles in coastal British Columbia.University of British Columbia’s Information Repository.64p.
Day K E,Kirby R S,Reynoldson T B.1995.The ef fect of manipulations of freshwater sediments on responses of benthic invertebrates in whole‐sediment toxicity tests.Environmental Toxicology and Chemistry,14(8):1 333-1 343.
de Vicente I,Guerrero F,Cruz-Pizarro L.2010.Chemical composition of wetland sediments as an integrator of trophic state.Aquatic Ecosystem Health and Management,13(1):99-103.
Edwards T M,McCoy K A,Barbeau T,McCoy M W,Thro JM,Guillette Jr L J.2006.Environmental context determines nitrate toxicity in Southern toad(Bufo terrestris)tadpoles.Aquatic Toxicology,78(1):50-58.
Esterbauer H,Schaur R J,Zollner H.1991.Chemistry and biochemistry of 4-hydroxynonenal,malonaldehyde and related aldehydes.Free Radical Biology and Medicine,11(1):81-128.
Falfushinska H,Loumbourdis N,Romanchuk L,Stolyar O.2008.Validation of oxidative stress responses in two populations of frogs from Western Ukraine.Chemosphere,73(7):1 096-1 101.
García-Mu?oz E,Gilbert J D,Parra G,Guerrero F.2010b.Wetlands classi?cation for amphibian conservation in Mediterranean landscapes.Biodiversity and Conservation,19(3):901-911.
García-Mu?oz E,Guerrero F,Parra G.2009.Ef fects of copper sulfate on growth,development,and escape behavior in Epidalea calamita embryos and larvae.Archives of Environmental Contamination and Toxicology,56(3):557-565.
García-Mu?oz E,Guerrero F,Parra G.2010a.Intraspeci?c and interspeci?c tolerance to copper sulphate in?ve Iberian amphibian species at two developmental stages.Archives of Environmental Contamination and Toxicology,59(2):312-321.
García-Mu?oz E,Guerrero F,Parra G.2011a.Ef fects of previous sublethal pulse to ammonium nitrate on mortality and total length on Epidalea calamita larvae.Chemosphere,84(5):671-675.
García-Mu?oz E,Guerrero F,Parra G.2011b.Larval escape behavior in anuran amphibians as a wetland rapid pollution biomarker.Marine and Freshwater Behaviour and Phy siology,44(2):109-123.
Gerdron A.2013.Amphibian Ecotoxicology.In:Férard J F,Blaise C eds.Encyclopedia of Aquatic Ecotoxicology.Springer,Dordrecht.p.21-37.
Gilbert J D,Guerrero F,Jiménez-Melero R,de Vicente I.2015.Is the bioproduction number a good index of the trophic state in Mediterranean wetlands?Knowledge and Management of Aquatic Ecosystems,416:05.
Gosner K L.1960.A simpli?ed table for staging anuran embryos and larvae with notes on identi?cation.Herpetologica,16(3):183-190.
Gripp H S,Freitas J S,Almeida E A,Bisinoti M C,Moreira AB.2017.Biochemical ef fects of?pronil and its metabolites on lipid peroxidation and enzymatic antioxidant defense in tadpoles(Eupemphix nattereri:Leiuperidae).Ecotoxicology and Environmental Safety,136:173-179.
Guerrero F,Parra G,Jiménez-Gómez F,Salazar C,JiménezMelero R,Galotti A,García-Mu?oz E,Lendínez M L,Ortega F.2006.Ecological studies in Alto Guadalquivir wetlands:a?rst step towards the application of conservation plans.Limnetica,25:95-106.
Hagger J A,Jones M B,Leonard D P,Owen R,Galloway T S.2006.Biomarkers and integrated environmental risk assessment:are there more questions than answers?Integrated Environmental Assessment and Management,2(4):312-329.
Halliwell B,Gutteridge J M C.1989.Free radicals in biology and medicine.Oxford University Press,New York.543p.
Handy R D,Galloway T S,Depledge M H.2003.A proposal for the use of biomarkers for the assessment of chronic pollution and in regulatory toxicology.Ecotoxicology,12(1-4):331-343.
Hopkins W A,Rowe C L,Congdon J D.1999.Elevated trace element concentrations and standard metabolic rate in banded water snakes(Nerodia fasciata)exposed to coal combustion wastes.Environmental Toxicology and Chemistry,18(6):1 258-1 263.
Hua J,Relyea R.2014.Chemical cocktails in aquatic systems:pesticide ef fects on the response and recovery of>20animal taxa.Environ men tal Pollution,189:18-26.
Ingersoll C G.1995.Sediment test.In:Rand G M.ed.Fundamentals of Aquatic Toxicology:Ef fects,Environmental Fate,and Risk Assessment.CRC Press,Florida.p.231-256.
Junta de Andalucía.2008.Reglamento especí?co de producción integrada de olivar.BOJA 83:9-38.
Koprivnikar J,Riepe T B,Calhoun D M,Johnson P T J.2017.Whether larval amphibians school does not af fect the parasite aggregation rule:testing the ef fects of host spatial heterogeneity in?eld and experimental studies.Oikos,127(1):99-110.
Luoma S N,Carter J L.1993.Understanding the toxicity of contaminants in sediments:beyond the bioassay-based paradigm.Environmental Toxicology and Chemistry,12:793-796.
Mann R M,Hyne R V,Choung C B,Wilson S P.2009.Amphibians and agricultural chemicals:Review of the risks in a complex environment.Environmental Pollution,157(11):2 903-2 927.
Montes C,Sala O.2007.La evaluación de los ecosistemas del milenio.Las relaciones entre el funcionamiento de los ecosistemas y el bienestar humano.Ecosistemas,16(3):137-147.
Parra G,Jiménez-Melero R,Guerrero F.2005.Agricultural impacts on Mediterranean wetlands:the ef fect of pesticides on survival and hatching rates in copepods.International Journal of Limnology,41(3):161-167.
Peakall D.1992.The role of biomarkers in environmental assessment.In:Peakall D ed.Animal Biomarkers as Pollution Indicators.Springer,Dordrecht.p.201-206.
Radi A A R,Matkovics B.1988.Ef fects of metal ions on the antioxidant enzyme activities,protein contents and lipid peroxidation of carp tissues.Comparative Biochemistry and Physiology Part C:Comparative Pharmacology,90(1):69-72.
Relyea R A,Mills N.2001.Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles(Hyla versicolor).Proceedings of the National Academy of Sciences of the United States of America,98(5):2 491-2 496.
Relyea R A.2006.The ef fects of pesticides,pH,and predatory stress on amphibians under mesocosm conditions.Ecotoxicol og y,15(6):503-511.
Robles-Molina J,Gilbert-López B,García-Reyes J F,MolinaDíaz A.2014.Monitoring of selected priority and emerging contaminants in the Guadalquivir River and other related surface waters in the province of Jaén,South East Spain.Science of the Total Environment,479-480:247-257.
Rodier J.1989.Análisis de las aguas.Omega,Barcelona.1 059p.
Rowe C L,Kinney O M,Nagle R D,Congdon J D.1998.Elevated maintenance costs in an anuran(Rana catesbeiana)exposed to a mixture of trace elements during the embryonic and early larval periods.Physiological and Biochemical Zoology,71:27-35.
Salvador A,Garcia-Paris M.2001.An?bios espa?oles:identi?cación,historia natural y distribución.Esfagnos,Madrid.269p.
Semlitsch R D,Scott D E,Pechmann J H K.1988.Time and size at metamorphosis related to adult?tness in ambystoma talpoideum.Ecology,69(1):184-192.
Sinsch U.1998.Biologie und?kologie der kreuzkr?te.Laurenti Verlag,Bochum.222p.
Slater T F.1984a.Overview of methods used for detecting lipid peroxidation.Methods in Enzymology,105:283-293.
Slater T F.1984b.Free-radical mechanisms in tissue injury.Biochemical Journal,222(1):1-15.
Smith D C.1987.Adult recruitment in chorus frogs:ef fects of size and date at metamorphosis.Ecology,68(2):344-350.
Snodgrass J W,Casey R E,Joseph D,Simon J A.2008.Microcosm investigations of stormwater pond sediment toxicity to embryonic and larval amphibians:variation in sensitivity among species.Environmental Pollution,154(2):291-297.
Troncoso L,Galleguillos R,Larrain A.2000.Ef fects of copper on the?tness of the Chilean scallop Argopecten purpuratus(Mollusca:Bivalvia).Hydrobiologia,420(1):185-189.
Vanwalleghem T,Amate J I,de Molina M G,Fernández D S,Gómez J A.2011.Quantifying the ef fect of historical soil management on soil erosion rates in Mediterranean olive orchards.Agriculture,Ecosystem and Environment,142(3-4):341-351.
Wood S L R,Richardson J S.2009.Impact of sediment and nutrient inputs on growth and survival of tadpoles of the western toad.Freshwater Biology,54(5):1 120-1 134.
American Public Health Association.1995.Standard methods for the examination of water and wastewater.American Public Health Association,Washington,DC.874p.
Andreu V,PicóY.2004.Determination of pesticides and their degradation products in soils:current status,gaps and the future.Journal of Limnology,64:13-29.
Araújo C V M,Tornero V,Lubián L M,Blasco J,van Bergeijk S A,Ca?avate P,Cidá,Franco D,Prado R,Bartual A,López M G,Ribeiro R,Moreira-Santos M,Torreblanca A,Jurado B,Moreno-Garrido I.2010.Ring test for wholesediment toxicity assay with-a-benthic marine diatom.Science of the Total Environment,408(4):822-828.
Baier F,Jedinger M,Gruber E,Zaller J G.2016.Temperaturedependence of glyphosate-based herbicide’s ef fects on egg and tadpole growth of common toads.Frontiers in Environmental Science,4:51.
Barata C,Varo I,Navarro J C,Arun S,Porte C.2005.Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran Daphnia magna exposed to redox cycling compounds.Comparative Biochemistry and Physiology Part C:Toxicology&Pharmacology,140(2):175-186.
Barnett M L,Mathisen A M.1997.Tyranny of the P-value:The con?ict between statistical signi?cance and common sense.Journal of Dental Research,76(1):534-536.
Beck C W,Congdon J D.2003.Energetics of metamorphic climax in the southern toad(Bufo terrestris).Oecologia,137(3):344-351.
Beja P,Alcazar R.2003.Conservation of Mediterranean temporary ponds under agricultural intensi?cation:an evaluation using amphibians.Biolog ical Conservation,114(3):317-326.
Bókony V,MikóZ,MóriczáM,Krüzselyi D,Hettyey A.2017.Chronic exposure to a glyphosate-based herbicide makes toad larvae more toxic.Proc eedings of the Royal Society B,284(1858):20170493.
Boone M D,James S M.2003.Interactions of an insecticide,herbicide,and natural stressors in amphibian community mesocosms.Ecological Applications,13(3):829-841.
Boone M D,Semlitsch R D.2002.Interactions of an insecticide with competition and pond drying in amphibian communities.Ecological Applications,12(1):307-316.
Bradford M M.1976.A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Analytical Biochemistry,72(1-2):248-254.
Breden F,Kelly C H.1982.The ef fect of conspeci?c interactions on metamorphosis in Bufo americanus.Ecology,63(6):1 682-1 689.
Brunelli E,BernabòI,Berg C,Lundstedt-Enkel K,Bonacci A,Tripepi S.2009.Environmentally relevant concentrations of endosulfan impair development,metamorphosis and behaviour in Bufo bufo tadpoles.Aquatic Toxicology,91(2):135-142.
Burton Jr G A.2013.Sediment ecotoxicity.In:Férard J F,Blaise C eds.Encyclopedia of Aquatic Ecotoxicology.Springer,Dordrecht.p.1 003-1 014.
Camargo J B D A,Cruz A C F,Campos B G,Araújo G S,Fonseca T G,Abessa D M S.2015.Use,development and improvements in the protocol of whole-sediment toxicity identi?cation evaluation using benthic copepods.Marine Pollution Bulletin,91(2):511-517.
Casado C,Montes C.1995.Guide of Spanish lakes and wetlands.In:Reyero J M ed.Madrid.293p.
Cavas L,Tarhan L.2003.Glutathione redox system,GSH-Px activity and lipid peroxidation(LPO)levels in tadpoles of R ridibunda and B.viridis.Cell Biochemistry and Function,21(1):75-79.
Congdon J D,Dunham A E,Hopkins W A,Rowe C L,Hinton T G.2001.Resource allocation-based life histories:a conceptual basis for studies of ecological toxicology.Environmental Toxicology and Chemistry,20(8):1 698-1 703.
Cooke A S.1973.The ef fects of DDT,when used as a mosquito larvicide,on tadpoles of the frog Rana temporaria.Environmental Pollution,5(4):259-273.
Courcelles D M M.2016.Inorganic?ne sediment deposition in rivers with run-of-river hydropower projects and Coastal Tailed Frog(Ascaphus truei)tadpoles in coastal British Columbia.University of British Columbia’s Information Repository.64p.
Day K E,Kirby R S,Reynoldson T B.1995.The ef fect of manipulations of freshwater sediments on responses of benthic invertebrates in whole‐sediment toxicity tests.Environmental Toxicology and Chemistry,14(8):1 333-1 343.
de Vicente I,Guerrero F,Cruz-Pizarro L.2010.Chemical composition of wetland sediments as an integrator of trophic state.Aquatic Ecosystem Health and Management,13(1):99-103.
Edwards T M,McCoy K A,Barbeau T,McCoy M W,Thro JM,Guillette Jr L J.2006.Environmental context determines nitrate toxicity in Southern toad(Bufo terrestris)tadpoles.Aquatic Toxicology,78(1):50-58.
Esterbauer H,Schaur R J,Zollner H.1991.Chemistry and biochemistry of 4-hydroxynonenal,malonaldehyde and related aldehydes.Free Radical Biology and Medicine,11(1):81-128.
Falfushinska H,Loumbourdis N,Romanchuk L,Stolyar O.2008.Validation of oxidative stress responses in two populations of frogs from Western Ukraine.Chemosphere,73(7):1 096-1 101.
García-Mu?oz E,Gilbert J D,Parra G,Guerrero F.2010b.Wetlands classi?cation for amphibian conservation in Mediterranean landscapes.Biodiversity and Conservation,19(3):901-911.
García-Mu?oz E,Guerrero F,Parra G.2009.Ef fects of copper sulfate on growth,development,and escape behavior in Epidalea calamita embryos and larvae.Archives of Environmental Contamination and Toxicology,56(3):557-565.
García-Mu?oz E,Guerrero F,Parra G.2010a.Intraspeci?c and interspeci?c tolerance to copper sulphate in?ve Iberian amphibian species at two developmental stages.Archives of Environmental Contamination and Toxicology,59(2):312-321.
García-Mu?oz E,Guerrero F,Parra G.2011a.Ef fects of previous sublethal pulse to ammonium nitrate on mortality and total length on Epidalea calamita larvae.Chemosphere,84(5):671-675.
García-Mu?oz E,Guerrero F,Parra G.2011b.Larval escape behavior in anuran amphibians as a wetland rapid pollution biomarker.Marine and Freshwater Behaviour and Phy siology,44(2):109-123.
Gerdron A.2013.Amphibian Ecotoxicology.In:Férard J F,Blaise C eds.Encyclopedia of Aquatic Ecotoxicology.Springer,Dordrecht.p.21-37.
Gilbert J D,Guerrero F,Jiménez-Melero R,de Vicente I.2015.Is the bioproduction number a good index of the trophic state in Mediterranean wetlands?Knowledge and Management of Aquatic Ecosystems,416:05.
Gosner K L.1960.A simpli?ed table for staging anuran embryos and larvae with notes on identi?cation.Herpetologica,16(3):183-190.
Gripp H S,Freitas J S,Almeida E A,Bisinoti M C,Moreira AB.2017.Biochemical ef fects of?pronil and its metabolites on lipid peroxidation and enzymatic antioxidant defense in tadpoles(Eupemphix nattereri:Leiuperidae).Ecotoxicology and Environmental Safety,136:173-179.
Guerrero F,Parra G,Jiménez-Gómez F,Salazar C,JiménezMelero R,Galotti A,García-Mu?oz E,Lendínez M L,Ortega F.2006.Ecological studies in Alto Guadalquivir wetlands:a?rst step towards the application of conservation plans.Limnetica,25:95-106.
Hagger J A,Jones M B,Leonard D P,Owen R,Galloway T S.2006.Biomarkers and integrated environmental risk assessment:are there more questions than answers?Integrated Environmental Assessment and Management,2(4):312-329.
Halliwell B,Gutteridge J M C.1989.Free radicals in biology and medicine.Oxford University Press,New York.543p.
Handy R D,Galloway T S,Depledge M H.2003.A proposal for the use of biomarkers for the assessment of chronic pollution and in regulatory toxicology.Ecotoxicology,12(1-4):331-343.
Hopkins W A,Rowe C L,Congdon J D.1999.Elevated trace element concentrations and standard metabolic rate in banded water snakes(Nerodia fasciata)exposed to coal combustion wastes.Environmental Toxicology and Chemistry,18(6):1 258-1 263.
Hua J,Relyea R.2014.Chemical cocktails in aquatic systems:pesticide ef fects on the response and recovery of>20animal taxa.Environ men tal Pollution,189:18-26.
Ingersoll C G.1995.Sediment test.In:Rand G M.ed.Fundamentals of Aquatic Toxicology:Ef fects,Environmental Fate,and Risk Assessment.CRC Press,Florida.p.231-256.
Junta de Andalucía.2008.Reglamento especí?co de producción integrada de olivar.BOJA 83:9-38.
Koprivnikar J,Riepe T B,Calhoun D M,Johnson P T J.2017.Whether larval amphibians school does not af fect the parasite aggregation rule:testing the ef fects of host spatial heterogeneity in?eld and experimental studies.Oikos,127(1):99-110.
Luoma S N,Carter J L.1993.Understanding the toxicity of contaminants in sediments:beyond the bioassay-based paradigm.Environmental Toxicology and Chemistry,12:793-796.
Mann R M,Hyne R V,Choung C B,Wilson S P.2009.Amphibians and agricultural chemicals:Review of the risks in a complex environment.Environmental Pollution,157(11):2 903-2 927.
Montes C,Sala O.2007.La evaluación de los ecosistemas del milenio.Las relaciones entre el funcionamiento de los ecosistemas y el bienestar humano.Ecosistemas,16(3):137-147.
Parra G,Jiménez-Melero R,Guerrero F.2005.Agricultural impacts on Mediterranean wetlands:the ef fect of pesticides on survival and hatching rates in copepods.International Journal of Limnology,41(3):161-167.
Peakall D.1992.The role of biomarkers in environmental assessment.In:Peakall D ed.Animal Biomarkers as Pollution Indicators.Springer,Dordrecht.p.201-206.
Radi A A R,Matkovics B.1988.Ef fects of metal ions on the antioxidant enzyme activities,protein contents and lipid peroxidation of carp tissues.Comparative Biochemistry and Physiology Part C:Comparative Pharmacology,90(1):69-72.
Relyea R A,Mills N.2001.Predator-induced stress makes the pesticide carbaryl more deadly to gray treefrog tadpoles(Hyla versicolor).Proceedings of the National Academy of Sciences of the United States of America,98(5):2 491-2 496.
Relyea R A.2006.The ef fects of pesticides,pH,and predatory stress on amphibians under mesocosm conditions.Ecotoxicol og y,15(6):503-511.
Robles-Molina J,Gilbert-López B,García-Reyes J F,MolinaDíaz A.2014.Monitoring of selected priority and emerging contaminants in the Guadalquivir River and other related surface waters in the province of Jaén,South East Spain.Science of the Total Environment,479-480:247-257.
Rodier J.1989.Análisis de las aguas.Omega,Barcelona.1 059p.
Rowe C L,Kinney O M,Nagle R D,Congdon J D.1998.Elevated maintenance costs in an anuran(Rana catesbeiana)exposed to a mixture of trace elements during the embryonic and early larval periods.Physiological and Biochemical Zoology,71:27-35.
Salvador A,Garcia-Paris M.2001.An?bios espa?oles:identi?cación,historia natural y distribución.Esfagnos,Madrid.269p.
Semlitsch R D,Scott D E,Pechmann J H K.1988.Time and size at metamorphosis related to adult?tness in ambystoma talpoideum.Ecology,69(1):184-192.
Sinsch U.1998.Biologie und?kologie der kreuzkr?te.Laurenti Verlag,Bochum.222p.
Slater T F.1984a.Overview of methods used for detecting lipid peroxidation.Methods in Enzymology,105:283-293.
Slater T F.1984b.Free-radical mechanisms in tissue injury.Biochemical Journal,222(1):1-15.
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