Abstract
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.
Highlights
The metabolic theory of ecology (MTE) and biological stoichiometry (BS) have greatly advanced our understanding of the factors that control ecological processes [1,2]
Mesozooplankton was dominant in most lakes and mainly comprised copepods in the lakes of Sierra Nevada, Mixodiaptomus laciniatus, and cladocerans in the lakes of the Pyrenees (Fig. S1B)
Our results for 22 high mountain lakes support the role of phylogeny, life history strategies, and environmental constraints on the nucleic acid (NA) content of zooplankton, illustrating how the integration of MTE and BS principles can successfully explain fundamental processes at the organism level
Summary
The metabolic theory of ecology (MTE) and biological stoichiometry (BS) have greatly advanced our understanding of the factors that control ecological processes [1,2]. While the MTE focuses on energy as the primary currency of metabolism [3,4], BS studies the balance of energy and multiple chemical elements in living systems [1,5] Both theories place special emphasis on unraveling the mechanistic basis of individual metabolism and growth as it affects the energy flux, and the storage and turnover rates of elements in ecosystems [1,2]. The growth rate hypothesis (GRH), a central concept of BS, proposes that organisms lacking major phosphorus (P) storage capacity have elevated demands for increased P allocation to P-rich ribosomal RNA under rapid growth This drives variation in the P content (and C:P and N:P ratios) in these organisms and establishes the close connection among individual growth, ribosomal metabolism, and elemental composition [5]. It provides the rationale for the use of RNA-based biomarkers, e.g., RNA content (as % of dry weight [%RNA]) or RNA:DNA ratio, as proxies for GR in various species, including zooplankton (e.g. [8,9])
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