Michael Danger

Priming effect: bridging the gap between terrestrial and aquatic ecology

Understanding how ecosystems store or release carbon is one of ecologys greatest challenges in the 21st century. Organic matter covers a large range of chemical structures and qualities, and it is classically represented by pools of different recalcitrance to degradation. The interaction effects of these pools on carbon cycling are still poorly understood and are most often ignored in global-change models. Soil scientists have shown that inputs of labile organic matter frequently tend to increase, and often double, the mineralization of the more recalcitrant organic matter. The recent revival of interest for this phenomenon, named the priming effect, did not cross the frontiers of the disciplines. In particular, the priming effect phenomenon has been almost totally ignored by the scientific communities studying marine and continental aquatic ecosystems. Here we gather several arguments, experimental results, and field observations that strongly support the hypothesis that the priming effect is a general phenomenon that occurs in various terrestrial, freshwater, and marine ecosystems. For example, the increase in recalcitrant organic matter mineralization rate in the presence of labile organic matter ranged from 10% to 500% in six studies on organic matter degradation in aquatid ecosystems. Consequently, the recalcitrant organic matter mineralization rate may largely depend on labile organic matter availability, influencing the CO2 emissions of both aquatic and terrestrial ecosystems. We suggest that (1) recalcitrant organic matter may largely contribute to the CO2 emissions of aquatic ecosystems through the priming effect, and (2) priming effect intensity may be modified by global changes, interacting with eutrophication processes and atmospheric CO2 increases. Finally, we argue that the priming effect acts substantially in the carbon and nutrient cycles in all ecosystems. We outline exciting avenues for research, which could provide new insights on the responses of ecosystems to anthropogenic perturbations and their feedbacks to climatic changes.

Benthic algae stimulate leaf litter decomposition in detritus‐based headwater streams: a case of aquatic priming effect?

In detritus-based ecosystems, autochthonous primary production contributes very little to the detritus pool. Yet primary producers may still influence the functioning of these ecosystems through complex interactions with decomposers and detritivores. Recent studies have suggested that, in aquatic systems, small amounts of labile carbon (C) (e.g., producer exudates), could increase the mineralization of more recalcitrant organic-matter pools (e.g., leaf litter). This process, called priming effect, should be exacerbated under low-nutrient conditions and may alter the nature of interactions among microbial groups, from competition under low-nutrient conditions to indirect mutualism under high-nutrient conditions. Theoretical models further predict that primary producers may be competitively excluded when allochthonous C sources enter an ecosystem. In this study, the effects of a benthic diatom on aquatic hyphomycetes, bacteria, and leaf litter decomposition were investigated under two nutrient levels in a factorial microcosm experiment simulating detritus-based, headwater stream ecosystems. Contrary to theoretical expectations, diatoms and decomposers were able to coexist under both nutrient conditions. Under low-nutrient conditions, diatoms increased leaf litter decomposition rate by 20% compared to treatments where they were absent. No effect was observed under high-nutrient conditions. The increase in leaf litter mineralization rate induced a positive feedback on diatom densities. We attribute these results to the priming effect of labile C exudates from primary producers. The presence of diatoms in combination with fungal decomposers also promoted decomposer diversity and, under low-nutrient conditions, led to a significant decrease in leaf litter C:P ratio that could improve secondary production. Results from our microcosm experiment suggest new mechanisms by which primary producers may influence organic matter dynamics even in ecosystems where autochthonous primary production is low.

Impaired Leaf Litter Processing in Acidified Streams

Anthropogenic acidification in headwater streams is known to affect microbial assemblages involved in leaf litter breakdown. Far less is known about its potential effects on microbial enzyme activities. To assess the effects of acidification on microbial activities associated with decaying leaves, a 70-day litter bag experiment was conducted in headwater streams at six sites across an acidification gradient. The results revealed that microbial leaf decomposition was strongly and negatively correlated with total Al concentrations (r = −0.99, p < 0.001) and positively correlated with Ca2+ concentrations (r = 0.94, p = 0.005) and pH (r = 0.93, p = 0.008). Denaturing gradient gel electrophoresis analyses showed that microbial assemblages differed between non-impacted and impacted sites, whereas fungal biomass associated with decaying leaves was unaffected. The nutrient content of leaf detritus and ecoenzymatic activities of carbon (C), nitrogen (N) and phosphorus (P) acquisition revealed that N acquisition was unaltered, while P acquisition was significantly reduced across the acidification gradient. The P content of leaf litter was negatively correlated with total Al concentrations (r = −0.94, p < 0.01) and positively correlated with decomposition rates (r = 0.95, p < 0.01). This potential P limitation of microbial decomposers in impacted sites was confirmed by the particularly high turnover activity for phosphatase and imbalanced ratios between the ecoenzymatic activities of C and P acquisition. The toxic form of Al has well-known direct effects on aquatic biota under acidic conditions, but in this study, Al was found to also potentially affect microbially mediated leaf processing by interfering with the P cycle. These effects may in turn have repercussions on higher trophic levels and whole ecosystem functioning.

Behavioural and physiological responses of Gammarus fossarum (Crustacea Amphipoda) exposed to silver

The study aims at investigating the effects of silver (Ag), a re-emerging contaminant, on physiological and behavioural responses in Gammarus fossarum. In a first experiment, G. fossarum Ag LC50s were evaluated during 96 h under semi-static mode of exposure. Juveniles appeared to be more sensitive to Ag (LC5096h: 1.01 μg L(-1)) than ovigerous females (LC5096h: 1.9 μg L(-1)) and adult males (LC5096h: 2.2 μg L(-1)). In a second experiment, the physiological (osmo-/ionoregulation; antioxidant enzymes; lipid peroxidation (LPO)) and behavioural (locomotor activity and ventilation) responses of male G. fossarum exposed to Ag (0, 0.5, 1, 2, and 4 μg L(-1)) were investigated. The mortality and Ag bioconcentration of gammarids exposed to Ag were significantly higher than controls. Concerning physiological responses, a 48 h-exposure to Ag had no impact on catalase activity but led to a significant decrease of haemolymph osmolality and [Na(+)]. On the contrary, LPO, Se-GPx and Na(+)/K(+)-ATPase activity were significantly increased. Behavioural responses, such as locomotor and ventilatory activities, were also significantly reduced in Ag exposed gammarids. After 96 h-exposure, especially to 0.5 μg Ag L(-1), most responses (ventilation, locomotor activity, haemolymph osmolality and [Na(+)]) were even more pronounced and haemolymph [Cl(-)] was significantly decreased but, contrary to observations after 48 h-exposure, Na(+)/K(+)-ATPase activity was significantly reduced. Our results demonstrate the drastic effects of realistic [Ag] concentration (0.5 μg Ag L(-1)) on an ubiquitous and functionally important freshwater invertebrate (implied in detritus breakdown), but also strongly suggest an energetic reallocation to the detriment of locomotor activity and in favour of maintenance functions (i.e., osmoregulation and detoxification). These results highlight the risk represented by Ag and the need to perform integrated studies (at different scales, from individual to ecosystem).

Litter identity mediates predator impacts on the functioning of an aquatic detritus-based food web

During past decades, several mechanisms such as resource quality and habitat complexity have been proposed to explain variations in the strength of trophic cascades across ecosystems. In detritus-based headwater streams, litter accumulations constitute both a habitat and a resource for detritivorous macroinvertebrates. Because litter edibility (which promotes trophic cascades) is usually inversely correlated with its structural complexity (which weakens trophic cascades), there is a great scope for stronger trophic cascades in litter accumulations that are dominated by easily degradable litter species. However, it remains unclear how mixing contrasting litter species (conferring both habitat complexity and high quality resource) may influence top–down controls on communities and processes. In enclosures exposed in a second-order stream, we manipulated litter species composition by using two contrasting litter (alder and oak), and the presence–absence of a macroinvertebrate predator (Cordulegaster boltonii larvae), enabling it to effectively exert predation pressure, or not, on detritivores (consumptive versus non-consumptive predation effects). Leaf mass loss, detritivore biomass and community structure were mostly controlled independently by litter identity and mixing and by predator consumption. However, the strength of predator control was mediated by litter quality (stronger on alder), and to a lesser extent by litter mixing (weaker on mixed litter). Refractory litter such as oak leaves may contribute to the structural complexity of the habitat for stream macroinvertebrates, allowing the maintenance of detritivore communities even when strong predation pressure occurs. We suggest that considering the interaction between top–down and bottom–up factors is important when investigating their influence on natural communities and ecosystem processes in detritus-based ecosystems.

Can we use stable isotopes for ecotoxicological studies? Effect of DDT on isotopic fractionation in Perca fluviatilis

Nitrogen and carbon stable isotope analyses are frequently used to assess contaminant biomagnification in animals in the wild. Previous studies, mainly on plant but also on animal tissues, have shown that chemical stress can lead to shifts in delta(15)N. In order to assess if an exposure to DDT at realistic concentration disrupted stable isotope signature in animals, delta(15)N and delta(13)C were studied in several tissues (liver, muscle, gill) of Perca fluviatilis fed with the same commercial diet uncontaminated or contaminated with DDT. We observed no DDT effect on the delta(15)N and delta(13)C of fish tissues. Our results show that stable isotopes can remain useful for field ecotoxicological studies despite food-chain contamination. However, correlations between the delta(13)C or delta(15)N values measured in the different organs were only found in DDT treated fish, suggesting some disruption of major biochemical compound metabolism in tissues.

Phosphorus availability modulates the toxic effect of silver on aquatic fungi and leaf litter decomposition

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.

Litter chemistry prevails over litter consumers in mediating effects of past steel industry activities on leaf litter decomposition

Soil pollution has adverse effects on the performance and life history traits of microorganisms, plants, and animals, yet evidence indicates that even the most polluted sites can support structurally-complex and dynamic ecosystems. The present study aims at determining whether and how litter decomposition, one of the most important soil ecological processes leaf, is affected in a highly trace-metal polluted site. We postulated that past steel mill activities resulting in soil pollution and associated changes in soil characteristics would influence the rate of litter decomposition through two non-exclusive pathways: altered litter chemistry and responses of decomposers to lethal and sub-lethal toxic stress. We carried out a litter-bag experiment using Populus tremula L. leaf litter collected at, and allowed to decompose in, a trace metal polluted site and in three unpolluted sites used as controls. We designed a fully-factorial transplant experimental design to assess effects of litter origin and exposure site on the rate of litter decomposition. We further determined initial litter chemistry, fungal biomass, mesofauna abundance in litter bags, and the soil macrofauna community. Irrespective of the site of litter exposure, litter originating from the polluted site had a two-fold faster decomposition than litter from the unpolluted sites. Litter chemistry, notably the lignin content, seemed most important in explaining the degradation rate of the leaf litter. Abundance of meso and macro-detritivores was higher at the polluted site than at the unpolluted sites. However, litter decomposition proceeded at similar rates in polluted and unpolluted sites. Our results show that trace metal pollution and associated soil and litter changes do not necessarily weaken consumer control on litter decomposition through lethal and sub-lethal toxic stress.

Influence of food web structure on the biochemical composition of seston, zooplankton and recently deposited sediment in experimental freshwater mesocosms

The effects of food web structure on the quantity and biochemical composition of seston, zooplankton and recently deposited sediment in experimental freshwater mesocosms were examined. Food web structure was manipulated by addition of zooplanktivorous fish. Biochemical characterisations were carried out using lipid biomarkers (sterols, fatty acids, chlorophyll-derived compounds and long-chain alkanediols). Fish addition decreased zooplankton biomass and increased seston biomass and deposited sediment through a trophic cascade. Fish presence strongly influenced the biochemical characteristics of seston and sediment. In contrast, food web structure had a minor impact on the lipid biomarker composition of zooplankton. Although the relative abundance of sterols in the different compartments did not differ strongly between treatments, sterol profiles in seston and sediment depended on food web structure. The predominance of Δ7-sterols in seston and sediment in the fish treatment indicated a major contribution of Chlorophyceae. In contrast, the distribution of sterols in seston and sediment in the fishless treatment, dominated by cholesterol, indicated a major zooplanktonic input. The distribution of fatty acids and the relative abundance of chlorophyll-derived compounds and long-chain alkanediols agreed with the predominant contribution of phytoplankton or zooplankton to seston and sediment in the two treatments. The relative abundance of bacterial biomarkers suggested that the contribution of bacteria was rather low. The high relative abundance of polyunsaturated fatty acids (PUFAs) and the absence of stanols in sediments suggested low microbial reworking of organic matter in the recently accumulated sediments. The trophic cascade, generated by the addition of fish, increased the relative abundance of PUFAs in deposited organic matter, thus enhancing sediment quality and potential degradability.

Interactive effects of aluminium and phosphorus on microbial leaf litter processing in acidified streams: A microcosm approach

Decline in pH, elevated aluminium (Al) concentrations, and base cations depletion often covary in acidified headwater streams. These parameters are considered as the main factors reducing microbial activities involved in detritus processing, but their individual and interactive effects are still unclear. In addition to its direct toxicity, Al can also reduce the bioavailability of phosphorus (P) in ecosystems through the formation of stable chemical complexes. A three week microcosm experiment was carried out in acid conditions to assess the interactive effects of Al (three levels: 0, 200, and 1,000 μg L(-1)) and P (25, 100, and 1,000 μg L(-1)) on alder leaf litter processing by an aquatic hyphomycete consortium. Our results showed that Al alone reduced fungal growth and altered fungal decomposer activities. High P levels, probably through an alleviation of Al-induced P limitation and a reduction of Al toxic forms, suppressed the negative effects of Al on detritus decomposition.