Interplay between resistance and resilience governs the stability of a freshwater microbial food web under multiple stressors.

Energy (photosynthetically active [PAR] and ultraviolet [UVR] radiation) and matter (organic and inorganic nutrients) fluxes regulate the ecosystem's stability. However, the mechanisms underpinning the potential interplay between resistance and resilience to shifts in nutrient inputs and UVR are poorly understood. To assess how the UVR × nutrients interaction alters ecosystem stability, we exposed in situ a microbial food web from an oligotrophic ecosystem to: (1) two light (UVR + PAR and PAR), and (2) four nutrient (ambient concentrations, phosphorus [P], carbon [C] and C × P addition) treatments for three weeks. During this period, we quantified the community composition and biomass, sestonic P and C:P ratio, primary [PP] and bacterial [BP] production, community [CR] and bacterial [BR] respiration, excreted organic carbon [EOC], as well as the commensalistic phytoplankton-bacteria interaction (i.e. bacterial carbon demand [BCD]:EOC ratio) and the metabolic balance of the ecosystem (i.e. [PP:R] ratio). The stability of all response variables under the four environmental scenarios tested (i.e. UVR, UVR × C, UVR × P, and UVR × C × P) was quantified by means of the resistance and resilience indexes. The microbial community was dominated by phototrophs during the experimental period regardless of the treatment considered. The most complex scenario, i.e. UVR × C × P, decreased the resistance for all variables, except for BR and the PP:R ratio. Despite that PP:R ratio showed the highest resistance under such scenario, it was >1 in all environmental scenarios (i.e. net autotrophic), except under the UVR × C interaction, where, concomitant with increased resilience, the balance shifted towards net heterotrophy (PP:R < 1). Under the UVR × C × P scenario, the metabolic balance of the ecosystem proved strongly resistant due mainly to high resistance of bacterial respiration and a firm stability of the commensalistic interaction. Our results evidence that the high resilience of phototrophs (favoring their predominance over mixo- and heterotrophs) may lead to the maintenance of the autotrophic nature and carbon (C) sink capacity of the ecosystem.

Climate-driven shifts in algal-bacterial interaction of high-mountain lakes in two years spanning a decade.

Algal-bacterial interactions include mutualism, commensalism, and predation. However, how multiple environmental conditions that regulate the strength and prevalence of a given interaction remains unclear. Here, we test the hypothesis that the prevailing algal-bacterial interaction shifted in two years (2005 versus 2015), due to increased temperature (T) and Saharan dust depositions in high-mountain lakes of Sierra Nevada (S Spain). Our results support the starting hypothesis that the nature of the prevailing algal-bacterial interaction shifted from a bacterivory control exerted by algae to commensalism, coinciding with a higher air and water T as well as the lower ratio sestonic nitrogen (N): phosphorous (P), related to greater aerosol inputs. Projected global change conditions in Mediterranean region could decline the functional diversity and alter the role of mixotrophy as a carbon (C) by-pass in the microbial food web, reducing the biomass-transfer efficiency up the web by increasing the number of trophic links.

Growth impacts of Saharan dust, mineral nutrients, and CO2 on a planktonic herbivore in southern Mediterranean lakes.

Rising levels of CO2 can boost plant biomass but reduce its quality as a food source for herbivores. However, significant uncertainties remain as to the degree to which the effect is modulated by other environmental factors and the underlying processes causing these responses in nature. To address these questions, we carried out CO2-manipulation experiments using natural seston from three lakes under nutrient-enriched conditions (mimicking eutrophication and atmospheric dust-input processes) as a food source for the planktonic Daphnia pulicaria. Contrary to expectations, there were no single effects of rising CO2 on herbivorous growth. Instead, synergistic CO2 × nutrient interactions indicated that CO2 did not support higher zooplankton growth rates unless supplemented with dust or inorganic nutrients (nitrogen, N; phosphorus, P) in two of three studied lakes. The overall positive correlation between zooplankton growth and seston carbon (C), but not seston C:P, suggested that this was a food quantity-mediated response. In addition, we found that this correlation improved when the data were grouped according to the nutrient treatments, and that the response was largest for dust. The synergistic CO2 × nutrient effects reported here imply that the effects of rising CO2 levels on herbivorous growth may be strongly influenced by eutrophication processes and the increase in dust deposition predicted for the Mediterranean region.

Nucleic acid content in crustacean zooplankton: bridging metabolic and stoichiometric predictions.

Metabolic and stoichiometric theories of ecology have provided broad complementary principles to understand ecosystem processes across different levels of biological organization. We tested several of their cornerstone hypotheses by measuring the nucleic acid (NA) and phosphorus (P) content of crustacean zooplankton species in 22 high mountain lakes (Sierra Nevada and the Pyrenees mountains, Spain). The P-allocation hypothesis (PAH) proposes that the genome size is smaller in cladocerans than in copepods as a result of selection for fast growth towards P-allocation from DNA to RNA under P limitation. Consistent with the PAH, the RNA:DNA ratio was >8-fold higher in cladocerans than in copepods, although 'fast-growth' cladocerans did not always exhibit higher RNA and lower DNA contents in comparison to 'slow-growth' copepods. We also showed strong associations among growth rate, RNA, and total P content supporting the growth rate hypothesis, which predicts that fast-growing organisms have high P content because of the preferential allocation to P-rich ribosomal RNA. In addition, we found that ontogenetic variability in NA content of the copepod Mixodiaptomus laciniatus (intra- and interstage variability) was comparable to the interspecific variability across other zooplankton species. Further, according to the metabolic theory of ecology, temperature should enhance growth rate and hence RNA demands. RNA content in zooplankton was correlated with temperature, but the relationships were nutrient-dependent, with a positive correlation in nutrient-rich ecosystems and a negative one in those with scarce nutrients. Overall our results illustrate the mechanistic connections among organismal NA content, growth rate, nutrients and temperature, contributing to the conceptual unification of metabolic and stoichiometric theories.

Maximum in the middle: nonlinear response of microbial plankton to ultraviolet radiation and phosphorus.

The responses of heterotrophic microbial food webs (HMFW) to the joint action of abiotic stressors related to global change have been studied in an oligotrophic high-mountain lake. A 2×5 factorial design field experiment performed with large mesocosms for >2 months was used to quantify the dynamics of the entire HMFW (bacteria, heterotrophic nanoflagellates, ciliates, and viruses) after an experimental P-enrichment gradient which approximated or surpassed current atmospheric P pulses in the presence vs. absence of ultraviolet radiation. HMFW underwent a mid-term (<20 days) acute development following a noticeable unimodal response to P enrichment, which peaked at intermediate P-enrichment levels and, unexpectedly, was more accentuated under ultraviolet radiation. However, after depletion of dissolved inorganic P, the HMFW collapsed and was outcompeted by a low-diversity autotrophic compartment, which constrained the development of HMFW and caused a significant loss of functional biodiversity. The dynamics and relationships among variables, and the response patterns found, suggest the importance of biotic interactions (predation/parasitism and competition) in restricting HMFW development, in contrast to the role of abiotic factors as main drivers of autotrophic compartment. The response of HMFW may contribute to ecosystem resilience by favoring the maintenance of the peculiar paths of energy and nutrient-mobilization in these pristine ecosystems, which are vulnerable to threats by the joint action of abiotic stressors related to global change.

Patterns of resource limitation of bacteria along a trophic gradient in Mediterranean inland waters.

The nature of the resource that limits heterotrophic bacteria, i.e. mineral nutrients or carbon (C), has consequences for biogeochemical cycles in aquatic ecosystems. Our aim was to identify the resource [C or phosphorus (P)] that mainly limits bacteria in a set of 31 Mediterranean inland water ecosystems spanning a wide trophic range. We followed an intersystem observational approach with three complementary perspectives, comparing the bacterial demand with the resource supply in terms of both the quantity (demand : supply ratio for C and P) and quality (C : P ratio of demand and supply), and assessing the relative strength of each resource in controlling bacterial production. The trophic gradient revealed a shift in the main limiting resource for bacteria, from C at the oligotrophic end (typically high-mountain, low-productivity lakes) to mainly P at the eutrophic end (typically nonmountain, high-productivity lakes). The patterns of resource limitation of bacteria found here may be related to the autotrophic nature of most of the studied ecosystems linked to a Mediterranean climate regime as representative of lakes with low inputs of allocthonous C. These patterns are consistent with the theoretical approaches and may potentially shape the contribution of this type of ecosystems to biogeochemical cycles.

Does microorganism stoichiometry predict microbial food web interactions after a phosphorus pulse?

Knowledge of variations in microbial food web interactions resulting from atmospheric nutrient loads is crucial to improve our understanding of aquatic food web structure in pristine ecosystems. Three experiments mimicking atmospheric inputs at different nitrogen/phosphorus (N/P) ratios were performed in situ covering the seasonal biological succession of the pelagic zone in a high-mountain Spanish lake. In all experiments, abundance, biomass, algal cell biovolume, P-incorporation rates, P-cell quota, and N/P ratio of algae strongly responded to P-enrichment, whereas heterotrophic bacteria remained relatively unchanged. Ciliates were severely restricted when a strong algal exploitation of the available P (bloom growth or storage strategies) led to transient (mid-ice-free experiment) or chronic (late ice-free experiment) P-deficiencies in bacteria. In contrast, maximum development of ciliates was reached when bacteria remained P-rich (N/P < 20) and algae approached Redfield proportions (N/P approximately 16). Evidence of a higher P-incorporation rate supports the proposition that algae and bacteria shifted from a mainly commensalistic-mutualistic to a competitive relationship for the available P when bacterial P-deficiency increased, as reflected by their unbalanced N/P ratio (N/P > 20-24). Hence, the bacterial N/P ratio proved be a key factor to understand the algae-bacteria relationship and microbial food web development. This study not only demonstrates the interdependence of life history strategies, stoichiometric nutrient content, and growth but also supports the use of bacterial N/P thresholds for diagnosing ciliate development, a little-studied aspect worthy of further attention.