Manuel Villar-Argaiz

LINKING LIFE HISTORY STRATEGIES AND ONTOGENY IN CRUSTACEAN ZOOPLANKTON: IMPLICATIONS FOR HOMEOSTASIS

Work to date has established that consumers are constrained in their chemical content variability. Such a constraint generates many different kinds of ecological relationships ranging from aspects of animal mineral nutrition to factors affecting consumer-driven nutrient recycling. Although previous studies have shown variation in zooplankton nutrient content within and between taxa, most stoichiometric studies assume that consumers are homeostatic in their elemental composition. In this paper, this assumption is reexamined as we describe the variability in the elemental content of the calanoid copepod Mixodiaptomus laciniatus Lilljeborg throughout its ontogeny (interstage variability) and for its specific developmental stages (intrastage variability). Mean copepod carbon content as dry mass increased significantly during ontogeny from 36.3% in nauplii to 51.5% in immature copepodites and 55.8% in adults. Mean phosphorus content decreased from 0.98% in nauplii to 0.87% in immature copepodites and 0.51% in ...

Shifts in food quality for herbivorous consumer growth: multiple golden means in the life history

Consumer growth can be affected by imbalances between the nutrient content of the consumer and its food resource. Although ontogenetic-driven changes in animal composition are well documented, their potential consequences for the organisms sensitivity to food quality constraints have remained elusive. Here we show that the potential growth response of the copepod Mixodiaptomus laciniatus (as %RNA and RNA:DNA ratio) to the natural gradient of seston carbon (C) : nutrient ratio is unimodal and stage specific. Solution of the equation given by the first derivative function provided the optimum C : nutrient ratio for maximum stage-specific growth, which increased during ontogeny. The peakedness of the function indicated that animal vulnerability to suboptimal food quality decreased as juveniles reached adulthood. Consistent with these results, a field experiment demonstrated that potential consumer growth responded to variations in seston C: phosphorus ratio, and that early life stages were particularly vulnerable to suboptimal food quality.

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∼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.

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.

Saharan dust inputs and high UVR levels jointly alter the metabolic balance of marine oligotrophic ecosystems

The metabolic balance of the most extensive bioma on the Earth is a controversial topic of the global-change research. High ultraviolet radiation (UVR) levels by the shoaling of upper mixed layers and increasing atmospheric dust deposition from arid regions may unpredictably alter the metabolic state of marine oligotrophic ecosystems. We performed an observational study across the south-western (SW) Mediterranean Sea to assess the planktonic metabolic balance and a microcosm experiment in two contrasting areas, heterotrophic nearshore and autotrophic open sea, to test whether a combined UVR × dust impact could alter their metabolic balance at mid-term scales. We show that the metabolic state of oligotrophic areas geographically varies and that the joint impact of UVR and dust inputs prompted a strong change towards autotrophic metabolism. We propose that this metabolic response could be accentuated with the global change as remote-sensing evidence shows increasing intensities, frequencies and number of dust events together with variations in the surface UVR fluxes on SW Mediterranean Sea. Overall, these findings suggest that the enhancement of the net carbon budget under a combined UVR and dust inputs impact could contribute to boost the biological pump, reinforcing the role of the oligotrophic marine ecosystems as CO2 sinks.

Rising nutrient-pulse frequency and high UVR strengthen microbial interactions

Solar radiation and nutrient pulses regulate the ecosystem’s functioning. However, little is known about how a greater frequency of pulsed nutrients under high ultraviolet radiation (UVR) levels, as expected in the near future, could alter the responses and interaction between primary producers and decomposers. In this report, we demonstrate through a mesocosm study in lake La Caldera (Spain) that a repeated (press) compared to a one-time (pulse) schedule under UVR prompted higher increases in primary (PP) than in bacterial production (BP) coupled with a replacement of photoautotrophs by mixotrophic nanoflagellates (MNFs). The mechanism underlying these amplified phytoplanktonic responses was a dual control by MNFs on bacteria through the excretion of organic carbon and an increased top-down control by bacterivory. We also show across a 6-year whole-lake study that the changes from photoautotrophs to MNFs were related mainly to the frequency of pulsed nutrients (e.g. desert dust inputs). Our results underscore how an improved understanding of the interaction between chronic and stochastic environmental factors is critical for predicting ongoing changes in ecosystem functioning and its responses to climatically driven changes.

INTERANNUAL CHANGES IN THE C:N:P RATIOS OF SESTON AND ZOOPLANKTON OF A HIGH MOUNTAIN LAKE IN SIERRA NEVADA, SPAIN

We investigated the carbon, nitrogen and phosphorus content inthe seston and the zooplankton of a high-mountain lake duringthree years of contrasting physical and chemical conditions.Carbon in seston was ten times higher in 1995 than in 1996 and1997. Phosphorus content in seston was variable for the studyperiod, increasing gradually towards late summer in 1995, butpeaking abruptly in 1996 and 1997, reflecting atmosphericdepositions. Seston C:P were high and did not fit any definitepattern in 1995, and were particularly low after the thaw, increasing towards mid-summer in 1996 and 1997. As the seasonprogressed, major decreases in these ratios occurred coincidingwith important atmospheric inputs in the lake area. ZooplanktonN:P and C:P were negatively associated to the appearance ofrotifers and copepod nauplii in 1995, but positively correlatedto the ontogenetic development of the most abundant species,Mixodiaptomus laciniatus, in 1996. Seasonal variations inzooplankton N:P and C:P ratios showed limited interannual, butlarge intraannual variability. The comparison between the bulkcarbon in seston and zooplankton demands for this elementindicated that zooplankton were above food-quantity thresholdsfor maximum growth in 1995, 1996 and mid-season of 1997,therefore suffering only from food-quantity constraints afterthe thaw (nauplii dominance) and towards late season (adultdominance) in the latter year. The high C:P ratios in sestonrelative to zooplankton in 1995 imply that the zooplankton mayhave faced severe food-quality constraints (in terms ofphosphorus) during this year. Differences between bulkzooplankton and seston elemental nutrients are also discussed inrelation to the competitive abilities of species, andparticularly of Daphnia.

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.

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.

Vulnerability of mixotrophic algae to nutrient pulses and UVR in an oligotrophic Southern and Northern Hemisphere lake

Nutrient inputs and ultraviolet radiation (UVR) are global factors affecting the structure and functioning of aquatic ecosystems, particularly clear-water ecosystems. We performed experiments in two model lakes highly exposed to UVR fluxes in order to test the effect that future increases in mineral nutrients transported by dust aerosol might exert on primary producers depending on the likelihood of atmospheric inputs. Lake La Caldera (Northern Hemisphere) has been receiving recurrent dust inputs from the Sahara Desert while lake Los Cántaros (Southern Hemisphere) has been less affected by dust aerosol. UVR × Nutrient synergistically stimulated primary production (PP), chlorophyll a (Chl a), with a smaller increase in phytoplanktonic biomass in La Caldera, but not in Los Cántaros, where nutrient addition unmasked the UVR inhibitory effect on phytoplankton. The proportional decrease of mixotrophic nanoflagellates (MNFs) after the nutrient pulse (in Los Cántaros) and the long-term decline of MNFs in La Caldera associated with the increase in aerosol-dust intrusions from the Sahara during the last 40 years suggest that a future scenario of intensified aerosol events from desert and desertified areas would not only reduce functional diversity with the decline of MNFs, but would ultimately alter the C flux towards the grazing chain in oligotrophic ecosystems.