Aquatic Toxicology 144–145 (2013) 199–207
Contents lists available at ScienceDirect
Aquatic Toxicology journal homepage: www.elsevier.com/locate/aquatox
Phosphorus availability modulates the toxic effect of silver on aquatic fungi and leaf litter decomposition J. Arce Funck a , H. Clivot a,b , V. Felten a,b , P. Rousselle a,b , F. Guérold a,b , M. Danger a,b,∗ a b
Université de Lorraine, LIEC (Laboratoire Interdisciplinaire des Environnements Continentaux), UMR 7360, Rue C. Bernard, 57070 Metz, France CNRS, LIEC, UMR 7360, Rue C. Bernard, 57070 Metz, France
a r t i c l e
i n f o
Article history: Received 31 January 2013 Received in revised form 16 September 2013 Accepted 1 October 2013 Keywords: Aquatic hyphomycetes Gammarus fossarum Ionic silver Detritus stoichiometric quality Detritivore consumption rates Denaturing gradient gel electrophoresis
a b s t r a c t The functioning of forested headwater streams is intimately linked to the decomposition of leaf litter by decomposers, mainly aquatic hyphomycetes, which enables the transfer of allochthonous carbon to higher trophic levels. Evaluation of this process is being increasingly used as an indicator of ecosystem health and ecological integrity. Yet, even though the individual impacts of contaminants and nutrient availability on decomposition have been well studied, the understanding of their combined effects remains limited. In the current study, we investigated whether the toxic effects of a reemerging contaminant, silver (Ag), on leaf litter decomposition could be partly overcome in situations where microorganisms were benefitting from high phosphorus (P) availability, the latter being a key chemical element that often limits detritus decomposition. We also investigated whether these interactive effects were mediated by changes in the structure of the aquatic hyphomycete community. To verify these hypotheses, leaf litter decomposition by a consortium of ten aquatic hyphomycete species was followed in a microcosm experiment combining five Ag contamination levels and three P concentrations. Indirect effects of Ag and P on the consumption of leaf litter by the detritivorous crustacean, Gammarus fossarum, were also evaluated. Ag significantly reduced decomposition but only at the highest concentration tested, independently of P level. By contrast, P and Ag interactively affected fungal biomass. Both P level and Ag concentrations shaped microbial communities without significantly affecting the overall species richness. Finally, the levels of P and Ag interacted significantly on G. fossarum feeding rates, high [Ag] reducing litter consumption and low P availability tending to intensify the feeding rate. Given the high level of contaminant needed to impair the decomposition process, it is unlikely that a direct effect of Ag on leaf litter decomposition could be observed in situ. However, subtle Ag effects in relation to nutrient levels in ecosystems could be expected. In particular, owing to higher consumption of low P leaf litter, shredding invertebrates could increase the ingestion of contaminated resources, which could, in turn, represent an important threat to headwater stream ecosystems. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The functioning of forested headwater streams relies on the processing of allochthonous organic matter (mainly leaf litter and woody debris) by decomposers, particularly aquatic hyphomycetes (Fisher and Likens, 1973). The detritus conditioned by microorganisms can then be consumed by invertebrate detritivores and incorporated into the food web (Hieber and Gessner, 2002). These processes are considered to be vital for downstream ecosystems because headwater streams are important sources of water,
∗ Corresponding author at: Université de Lorraine, Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), CNRS UMR 7360, Campus Bridoux, Rue du Général Delestraint, 57070 Metz Borny, France. E-mail address: [email protected] (M. Danger). 0166-445X/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.aquatox.2013.10.001
nutrients and carbon for downstream reaches (Gomi et al., 2002). Yet, the structural and functional integrity of headwater streams is vulnerable. In addition to the current intensification of land use (Revenga et al., 2005) and atmospheric deposition of pollutants (Mannio, 2001), these ecosystems can receive effluents of wastewater treatment plants, which not only contribute to eutrophication, but also contain emerging xenobiotics, such as trace metals (Lanceleur et al., 2012; Vystavna et al., 2012) or organic chemicals (Dickenson et al., 2011). Although leaf litter decomposition and aquatic hyphomycete activity have long been studied in unpolluted streams, several studies have shown that this process can be strongly altered by pollutants. In particular, owing to the naturally ultra-oligo- to oligotrophic status of headwater streams [
Contents lists available at ScienceDirect
Aquatic Toxicology journal homepage: www.elsevier.com/locate/aquatox
Phosphorus availability modulates the toxic effect of silver on aquatic fungi and leaf litter decomposition J. Arce Funck a , H. Clivot a,b , V. Felten a,b , P. Rousselle a,b , F. Guérold a,b , M. Danger a,b,∗ a b
Université de Lorraine, LIEC (Laboratoire Interdisciplinaire des Environnements Continentaux), UMR 7360, Rue C. Bernard, 57070 Metz, France CNRS, LIEC, UMR 7360, Rue C. Bernard, 57070 Metz, France
a r t i c l e
i n f o
Article history: Received 31 January 2013 Received in revised form 16 September 2013 Accepted 1 October 2013 Keywords: Aquatic hyphomycetes Gammarus fossarum Ionic silver Detritus stoichiometric quality Detritivore consumption rates Denaturing gradient gel electrophoresis
a b s t r a c t The functioning of forested headwater streams is intimately linked to the decomposition of leaf litter by decomposers, mainly aquatic hyphomycetes, which enables the transfer of allochthonous carbon to higher trophic levels. Evaluation of this process is being increasingly used as an indicator of ecosystem health and ecological integrity. Yet, even though the individual impacts of contaminants and nutrient availability on decomposition have been well studied, the understanding of their combined effects remains limited. In the current study, we investigated whether the toxic effects of a reemerging contaminant, silver (Ag), on leaf litter decomposition could be partly overcome in situations where microorganisms were benefitting from high phosphorus (P) availability, the latter being a key chemical element that often limits detritus decomposition. We also investigated whether these interactive effects were mediated by changes in the structure of the aquatic hyphomycete community. To verify these hypotheses, leaf litter decomposition by a consortium of ten aquatic hyphomycete species was followed in a microcosm experiment combining five Ag contamination levels and three P concentrations. Indirect effects of Ag and P on the consumption of leaf litter by the detritivorous crustacean, Gammarus fossarum, were also evaluated. Ag significantly reduced decomposition but only at the highest concentration tested, independently of P level. By contrast, P and Ag interactively affected fungal biomass. Both P level and Ag concentrations shaped microbial communities without significantly affecting the overall species richness. Finally, the levels of P and Ag interacted significantly on G. fossarum feeding rates, high [Ag] reducing litter consumption and low P availability tending to intensify the feeding rate. Given the high level of contaminant needed to impair the decomposition process, it is unlikely that a direct effect of Ag on leaf litter decomposition could be observed in situ. However, subtle Ag effects in relation to nutrient levels in ecosystems could be expected. In particular, owing to higher consumption of low P leaf litter, shredding invertebrates could increase the ingestion of contaminated resources, which could, in turn, represent an important threat to headwater stream ecosystems. © 2013 Elsevier B.V. All rights reserved.
1. Introduction The functioning of forested headwater streams relies on the processing of allochthonous organic matter (mainly leaf litter and woody debris) by decomposers, particularly aquatic hyphomycetes (Fisher and Likens, 1973). The detritus conditioned by microorganisms can then be consumed by invertebrate detritivores and incorporated into the food web (Hieber and Gessner, 2002). These processes are considered to be vital for downstream ecosystems because headwater streams are important sources of water,
∗ Corresponding author at: Université de Lorraine, Laboratoire Interdisciplinaire des Environnements Continentaux (LIEC), CNRS UMR 7360, Campus Bridoux, Rue du Général Delestraint, 57070 Metz Borny, France. E-mail address: [email protected] (M. Danger). 0166-445X/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.aquatox.2013.10.001
nutrients and carbon for downstream reaches (Gomi et al., 2002). Yet, the structural and functional integrity of headwater streams is vulnerable. In addition to the current intensification of land use (Revenga et al., 2005) and atmospheric deposition of pollutants (Mannio, 2001), these ecosystems can receive effluents of wastewater treatment plants, which not only contribute to eutrophication, but also contain emerging xenobiotics, such as trace metals (Lanceleur et al., 2012; Vystavna et al., 2012) or organic chemicals (Dickenson et al., 2011). Although leaf litter decomposition and aquatic hyphomycete activity have long been studied in unpolluted streams, several studies have shown that this process can be strongly altered by pollutants. In particular, owing to the naturally ultra-oligo- to oligotrophic status of headwater streams [
