Interactive effects of uvr and nutrients on the primary producer-consumer interactionan ecological-evolutionary perspective

Resumen

The major goal of this PhD Thesis Project was to investigate the interactive effects of ultraviolet radiation (UVR) and nutrients on the primary producer-consumer interaction. For this purpose, it was first evaluated how the combination of UVR and nutrients altered primary producers as food resource for herbivorous consumers using large field mesocosms in an oligotrophic high mountain lake (chapter II). Second, the nutritional suitability of the in situ raised food for consumers was assessed using a variety of experimental and observational approaches carried out at different spatial and temporal scales, from short-term bioassays to mid-term experiments and long-term field observations. From these heterogeneous studies, a single consistent picture of how the strength of the coupling might evolve in response to UVR and nutrient availability emerged (chapters III-VI). Our experimental results for the effects of UVR and phosphorus (P)- enrichment on the elemental and biochemical composition of seston showed that: (i) P-enrichment increased the content of total fatty acids (TFA), ¿3-polyunsaturated fatty acids (¿3-PUFA) [mainly 18:3n-3 (¿-linolenic acid)], chlorophyll a:carbon ratio (Chl a:C) and C:nitrogen (C:N) ratio, but lowered the content of highly unsaturated fatty acids (HUFA) [mainly 20:4n-6 (arachidonic acid, ARA)], the HUFA:PUFA ratio and, at high P loads, C:P ratio in seston; (ii) UVR increased TFA and ¿3-PUFA at control and highest P-enrichment, but decreased HUFA and C:P ratio of seston at all points of the trophic gradient. The interaction between UVR and P-enrichment was significant for seston HUFA and C:P ratio, indicating that the effect of UVR in reducing HUFA (decreased biochemical food quality) and C:P ratio (enhanced elemental food quality) was most pronounced at low nutrient concentrations, and vanished as P-enrichment increased. These results suggest that any potential future increase in UVR fluxes might affect more strongly the algal food quality inhabiting oligotrophic pristine waters, although these effects could be offset by P-inputs from atmospheric dust depositions. Food associated-effects of these factors on zooplankton growth were tested in coupled short-term laboratory experiments with the aim of separating food quantity from food quality effects at low food conditions, similar to those given in oligotrophic pristine waters (chapter III). This objective was carried out for three zooplankton species with contrasting life-history traits: The copepod Mixodiaptomus laciniatus, the cladoceran Daphnia pulicaria, and the rotifer Keratella cochlearis. Results showed that increased nutrient concentrations generated a large nutrient gradient that most affected zooplankton growth, with no significant role of UVR. The growth of each zooplankter adjusted well to a saturation curve that reached a plateau at increasing seston levels of ca. 250 for Keratella cochlearis, 500 for Mixodiaptomus laciniatus, and 1000 ¿g C L-1 for Daphnia pulicaria, and after which growth decreased for Mixodiaptomus laciniatus. By contrast, nutrients and also UVR affected food quality for zooplankton growth, although to a lesser extent compared to food quantity. The food quality parameter that best explained zooplankton growth was species-specific. Thus, in comparison with previous findings for single food quality predictors, we found that P-normalized ¿3-PUFA index (¿3-PUFA:P) of primary producers was the best predictor of the growth of Mixodiaptomus laciniatus and Daphnia pulicaria, two freshwater metazoans representing some of the major planktonic groups. A key to understand consumer growth appears to be offered by marrying hitherto opposed schools of thought in a joint consideration of essential fatty acids and mineral P, both indispensable for herbivorous consumers, and linked together in autotroph metabolism. Of all predictors, growth rate of the rotifer Keratella cochlearis was strongly related to the P-content of seston. Altogether, food quantity and quality bioassays suggest that seston increase associated with more intense and frequent atmospheric depositions could result in impaired growth for dominant copepods, but might favour C-limited cladocerans and P-limited rotifers in pristine ecosystems of the Mediterranean region. Because the above laboratory assays isolated the effects of food quantity and quality and excluded the impact of UVR, mid-term incubations (70 days) were carried out in situ to examine how the joint effects of UVR and nutrients might affect the strength of the phytoplankton-zooplankton coupling (PZC) in nature (chapter IV). Our experimental results on Mixodiaptomus laciniatus showed that zooplankton biomass unimodally responded to food quantity, challenging ¿the more is better (or at least never worse)¿ concept, since high levels of food resulted in weakened PZC. The effect of UVR on zooplankton was nutrient dependent, significantly reducing zooplankton abundance at intermediate nutrient concentrations (20, 30 and 40 ¿g P L-1 treatments), but not at both extremes of the trophic gradient generated at control and 60 ¿g P L-1 treatments. These observed differences were not due to the role of UVR affecting food quantity or quality, suggesting direct deleterious effects of UVR on zooplankton at intermediate food ranges and, as a consequence, weakening PZC. These results contributed to explain the long-term decoupled dynamics of phyto- and zooplankton in Lake La Caldera as result of the increasing intensity and frequency of aerosol depositions over the past three decades (1973-2003) and the characteristic high UVR levels reaching high mountain lakes. Detrimental effects of UVR resulted in decreased zooplankton abundance but not in size, suggesting a direct lethal UVR effect. These detrimental effects of UVR were, however, not observed at both ends of the trophic gradient, where UVR exerted a more subtle effect by enhancing the somatic C content of zooplankton (increased body C:P ratio). Such an increase in C was interpreted as a protective mechanism against UVR stress. UVR-induced effects in zooplankton elemental composition contribute evidence on the non-strict homeostatic nature of herbivorous consumers. Interestingly, the opposed impact of UVR decreasing phytoplankton C:P ratios but increasing zooplankton C:P ratios would contribute to enhance the nutritional imbalance at the primary producer-consumer interface (chapter V). The use of nucleic acid indices (NAIs) (%RNA and RNA:DNA ratio) as proxies for growth during three years of intensive monitoring in Lake La Caldera allowed the examination of nutrient conditions that favoured maximal growth during the ontogenetic development of zooplankton (chapter VI). A most intriguing result was that zooplankton growth, primarily limited by food quantity in Lake La Caldera, was strongly affected by food quality as seston C:nutrient ratio (C:P and C:N ratios). Furthermore, the relationship between NAIs and seston C:nutrient ratio was unimodal and stage-specific. These results challenged ¿the more nutrient is better (or at least never worse)¿ concept for the consumer, and indicate that food quality effects not only occurred at extremely low food quantities, but also affected zooplankton growth in ways not described before. Thus, the performance at each consumer¿s developmental stage decreased towards both ends of a food quality gradient and was maximal at an optimal resource C:nutrient ratio. While several mechanisms might account for this phenomenon, the extended assumption that below a given threshold elemental ratio organism performance is not affected by the nutrient content of its food is challenged here. These results are consistent with the knife-edge hypothesis and has strong bearings on the nutritional imbalance at the primary producer-herbivorous consumer interface as it suggests that food C:nutrient ratio can impair consumer growth, whether that C:nutrient ratio is higher or lower than consumer¿s requirements. Likewise, the solution of the equations given by the first and second derivative of the stage-specific unimodal functions merited further attention. Thus, the solution of the equation given by the first derivate function provided the optimum C:nutrient ratio that increased ontogenetically, indicating decreased nutrient requirements across the development of the organism. The solution of the equation given by the second derivative function provided evidence that consumer¿s sensitivity to food quality decreased as nauplii grew and converted into juveniles and adults. Consistently with these results, a field-experiment, where manipulation of UVR and nutrients altered food quality, demonstrated that consumer growth responded to variations in seston C:P ratio and particularly for early life stages, more vulnerable to suboptimal food qualities compared to adults. Finally, to test the growth rate and P-allocation hypotheses (GRH, PAH) we measured the content of P and nucleic acids, and the RNA:DNA ratios in seven crustacean species of 22 high mountain lakes (Sierra Nevada and The Pyrenees) (chapter VII). The strong positive relationships among growth rate, P and RNA contents across and within crustacean species supported inter- and intraspecifically predictions of GRH, which proposes that elevated demands for increased P-allocation to ribosomal RNA under rapid organism growth drives variation in the P content (and thus C:P and N:P ratios) of many biota. RNA:DNA ratios were consistent with PAH that decreased genome size in cladocerans would be the consequence of the evolutionary pressure towards P-allocation from non-coding DNA to RNA to sustain rapid growth. However, our results also pointed out that, apart from phylogeny, ontogeny, life-history strategies and environmental pressures like nutritional constraints are determinant for P and nucleic acid contents in crustacean zooplankton.