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Understanding the ecological consequences of supplemental feeding to both hummingbirds and the plants they pollinate is complicated by logistical challenges associated with assessing relative dietary resource use with commonly applied observational methods. Here, we describe the results of research conducted to assess the relative use of feeder and flower nectar by Broad-tailed (Selasphorus platycercus) and Rufous hummingbirds (Selasphorus rufus) using two distinct methodological variations to measure the δ13C values of exhaled CO2. Because of the relatively quick time in which both species switch from exogenous to endogenous resources to fuel metabolism, our experiment allowed us to assess resource use at two timescales. Our results suggest variability in the relative contributions of the two dietary sources within and among species and timescales, with most birds employing a mixture of feeder and flower sugars as fuel sources. This diversity in relative resource use may mitigate potential negative effects of supplemental feeding on hummingbirds and their plant symbionts.
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AbstractTrehalose is a nonreducing disaccharide that is a primary storage and energy source in prokaryotes, yeasts, fungi, and invertebrates. Vertebrates digest trehalose with the intestinal brush border membrane (BBM) enzyme trehalase. Intestinal trehalase activity is reported to be either very low or absent in several bird species. We assayed trehalase activity in 19 avian species, used proteomic analysis to quantify its abundance in the intestinal BBM, and used analyses of available genomes to detect the presence of the gene that codes for trehalase (Treh). We found no intestinal trehalase activity in birds, trehalase was absent from the proteome of their intestinal BBM, and the gene coding for trehalase was absent in their genomes. Surveys of available transcriptomes support the hypothesis that Treh is absent in birds. The trehalase gene was found in the same conserved syntenic block within the genome of all vertebrates surveyed except birds. Our analysis suggests that Treh was lost in an inversion followed by a reinsertion of a large gene block. This event appears to have taken place after the split between crocodiles and birds and dinosaurs. Birds are unable to digest a common dietary sugar like trehalose because their ancestor lost the trehalase gene. The loss of this gene seems to represent an ecological cost, as insectivorous birds seem to be unable to digest a carbohydrate present in their prey. We also speculate that the paucity of mycophagy in birds is due to the presence of large amounts of this sugar in fungal tissues.
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Trehalasa , Trehalosa , Animales , Aves , Digestión , Proteómica , Trehalasa/genética , VertebradosRESUMEN
The major lineages of nectar-feeding birds (hummingbirds, sunbirds, honeyeaters, flowerpiercers, and lorikeets) are considered examples of convergent evolution. We compared sucrose digestion capacity and sucrase enzymatic activity per unit intestinal surface area among 50 avian species from the New World, Africa, and Australia, including 20 nectarivores. With some exceptions, nectarivores had smaller intestinal surfaces, higher sucrose hydrolysis capacity, and greater sucrase activity per unit intestinal area. Convergence analysis showed high values for sucrose hydrolysis and sucrase activity per unit intestinal surface area in specialist nectarivores, matching the high proportion of sucrose in the nectar of the plants they pollinate. Plants pollinated by generalist nectar-feeding birds in the Old and New Worlds secrete nectar in which glucose and fructose are the dominant sugars. Matching intestinal enzyme activity in birds and nectar composition in flowers appears to be an example of convergent coevolution between plants and pollinators on an intercontinental scale.
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Relative to other vertebrates, birds have unusually high blood glucose levels. In humans, the hyperglycemia observed in birds would be associated with diabetes mellitus and the non-enzymatic glycation of proteins, which leads to the accumulation of advanced glycation products and to a plethora of microvascular pathologies. How do birds avoid the negative effects of hyperglycemia? Anthony-Regnitz et al. (J Mol Evol 88: 653-661, 2020) discovered that birds might have evolved glycation-resistant proteins. Serum albumin is an important multifunctional protein susceptible to glycation. Anthony-Regnitz et al. (J Mol Evol 88: 653-661, 2020) found that chicken albumin is resistant to glycation relative to bovine serum albumin. Protein glycation takes place primarily in lysine residues, which are less abundant in chicken than in bovine serum albumin. A multispecies comparison of serum albumin sequences revealed lower numbers of lysine residues in birds than in mammals. Benign hyperglycemia is a shared derived trait of birds and glycation resistance mechanisms appear to have accompanied its evolution. The evolution of benign hyperglycemia in birds coincided with a genomic upheaval that included the loss of important genes, including the one that codes for GLUT4, the transporter responsible for insulin-dependent glucose transport in other vertebrates' insulin-sensitive cells. This loss seems to have resulted in the remodeling of the insulin-signaling pathway in bird tissues. Avian hyperglycemia has been considered a mystery for a long time. Although we remain ignorant of its origins and its repercussions for the physiology of birds, the discovery of resistance to glycation in bird serum albumin offers a path forward to solve this mystery.
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Aves , Hiperglucemia , Albúminas , Animales , Hiperglucemia/veterinaria , Insulina , Transducción de SeñalRESUMEN
BACKGROUND: The New World leaf-nosed bats (Phyllostomids) exhibit a diverse spectrum of feeding habits and innovations in their nutrient acquisition and foraging mechanisms. However, the genomic signatures associated with their distinct diets are unknown. RESULTS: We conducted a genomic comparative analysis to study the evolutionary dynamics related to dietary diversification and specialization. We sequenced, assembled, and annotated the genomes of five Phyllostomid species: one insect feeder (Macrotus waterhousii), one fruit feeder (Artibeus jamaicensis), and three nectar feeders from the Glossophaginae subfamily (Leptonycteris yerbabuenae, Leptonycteris nivalis, and Musonycteris harrisoni), also including the previously sequenced vampire Desmodus rotundus. Our phylogenomic analysis based on 22,388 gene families displayed differences in expansion and contraction events across the Phyllostomid lineages. Independently of diet, genes relevant for feeding strategies and food intake experienced multiple expansions and signatures of positive selection. We also found adaptation signatures associated with specialized diets: the vampire exhibited traits associated with a blood diet (i.e., coagulation mechanisms), whereas the nectarivore clade shares a group of positively selected genes involved in sugar, lipid, and iron metabolism. Interestingly, in fruit-nectar-feeding Phyllostomid and Pteropodids bats, we detected positive selection in two genes: AACS and ALKBH7, which are crucial in sugar and fat metabolism. Moreover, in these two proteins we found parallel amino acid substitutions in conserved positions exclusive to the tribe Glossophagini and to Pteropodids. CONCLUSIONS: Our findings illuminate the genomic and molecular shifts associated with the evolution of nectarivory and shed light on how nectar-feeding bats can avoid the adverse effects of diets with high glucose content.
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Evolución Biológica , Quirópteros/genética , Conducta Alimentaria , Genómica , Adaptación Fisiológica , Alimentación Animal , Animales , Evolución Molecular , Genoma , Genómica/métodos , Masculino , Familia de Multigenes , Filogenia , Selección Genética , Relación Estructura-ActividadRESUMEN
A simple method for the identification of brush-border membrane α-glucosidases is described. The proteins were first solubilized and separated in a gel under native, non-denaturing, conditions. The gel was then incubated in substrate solutions (maltose or sucrose), and the product (glucose) exposed in situ by the oxidation of o-dianisidine, which yields a brown-orange color. Nano-liquid chromatography coupled to mass spectrometry analyses of proteins (nano LC-MS/MS) present in the colored bands excised from the gels, was used to confirm the presence of the enzymes. The stain is inexpensive and the procedure permits testing several substrates in the same gel. Once enzymes are identified, their abundance, relative to that of other proteins in the brush border, can be semi-quantified using nano LC-MS/MS.
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Vertebrate diets and digestive physiologies vary tremendously. Although the contribution of ecological and behavioral features to such diversity is well documented, the roles and identities of individual intestinal enzymes shaping digestive traits remain largely unexplored. Here, we show that the sucrase-isomaltase (SI)/maltase-glucoamylase (MGAM) dual enzyme system long assumed to be the conserved disaccharide and starch digestion framework in all vertebrates is absent in many lineages. Our analyses indicate that independent duplications of an ancestral SI gave rise to the mammalian-specific MGAM, as well as to other duplicates in fish and birds. Strikingly, the duplicated avian enzyme exhibits similar activities to MGAM, revealing an unexpected case of functional convergence. Our results highlight digestive enzyme variation as a key uncharacterized component of dietary diversity in vertebrates.
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Metabolismo de los Hidratos de Carbono/genética , Evolución Molecular , Duplicación de Gen , Vertebrados/genética , alfa-Glucosidasas/genética , Animales , Pollos , Ratones , Ratas , Pájaros Cantores , Vertebrados/metabolismo , alfa-Glucosidasas/metabolismoRESUMEN
Because a broad spectrum of resource use allows species to persist in a wide range of habitat types, and thus permits them to occupy large geographical areas, and because broadly distributed species have access to more diverse resource bases, the resource breadth hypothesis posits that the diversity of resources used by organisms should be positively related with the extent of their geographic ranges. We investigated isotopic niche width in a small radiation of South American birds in the genus Cinclodes. We analysed feathers of 12 species of Cinclodes to test the isotopic version of the resource breadth hypothesis and to examine the correlation between isotopic niche breadth and morphology. We found a positive correlation between the widths of hydrogen and oxygen isotopic niches (which estimate breadth of elevational range) and widths of the carbon and nitrogen isotopic niches (which estimates the diversity of resources consumed, and hence of habitats used). We also found a positive correlation between broad isotopic niches and wing morphology. Our study not only supports the resource breadth hypothesis but it also highlights the usefulness of stable isotope analyses as tools in the exploration of ecological niches. It is an example of a macroecological application of stable isotopes. It also illustrates the importance of scientific collections in ecological studies.
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Ecosistema , Passeriformes/anatomía & histología , Passeriformes/fisiología , Animales , Isótopos de Carbono/análisis , Deuterio/análisis , Plumas/química , América del SurAsunto(s)
Aves/metabolismo , Ácidos Docosahexaenoicos/administración & dosificación , Ácido Eicosapentaenoico/administración & dosificación , Insectos/metabolismo , Animales , Organismos Acuáticos/metabolismo , Dieta , Ácidos Docosahexaenoicos/metabolismo , Ecosistema , Ácido Eicosapentaenoico/metabolismo , Cadena Alimentaria , Insectos/químicaRESUMEN
Norway rats (Rattus norvegicus) were introduced to the Falkland Islands and are detrimental to native passerines. Rat eradication programmes are being used to help protect the avifauna. This study assesses the effectiveness of eradication programmes while using this conservation practice as a natural experiment to explore the ecological resistance, resilience and homeostasis of bird communities. We conducted bird surveys on 230 islands: 85 in the presence of rats, 108 that were historically free of rats and 37 from which rats had been eradicated. Bird detection data were used to build occupancy models for each species and estimate species-area relationships. Count data were used to estimate relative abundance and community structure. Islands with invasive rats had reduced species richness of passerines and a different community structure than islands on which rats were historically absent. Although the species richness of native passerines was remarkably similar on eradicated and historically rat-free islands, community structure on eradicated islands was more similar to that of rat-infested islands than to historically rat-free islands. The results suggest that in the Falkland Islands, species richness of passerines is not resistant to invasive rats, but seems to be resilient following their removal. In contrast, community structure seems to be neither resistant nor resilient. From a conservation perspective, rat eradication programmes in the Falkland Islands appear to be effective at restoring native species richness, but they are not necessarily beneficial for species of conservation concern. For species that do not recolonize, translocations following eradications may be necessary.
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Conservación de los Recursos Naturales/métodos , Especies Introducidas , Passeriformes/fisiología , Ratas , Animales , Biodiversidad , Islas Malvinas , Modelos Teóricos , Evaluación de Programas y Proyectos de SaludRESUMEN
The use of stable isotopes in ecological studies requires that we know the magnitude of discrimination factors between consumer and element sources. The causes of variation in discrimination factors for carbon and nitrogen have been relatively well studied. In contrast, the discrimination factors for hydrogen have rarely been measured. We grew cabbage looper caterpillars (Trichoplusia ni) on cabbage (Brassica oleracea) plants irrigated with four treatments of deuterium-enriched water (δDâ=â-131, -88, -48, and -2, respectively), allowing some of them to reach adulthood as moths. Tissue δD values of plants, caterpillars, and moths were linearly correlated with the isotopic composition of irrigation water. However, the slope of these relationships was less than 1, and hence, discrimination factors depended on the δD value of irrigation water. We hypothesize that this dependence is an artifact of growing plants in an environment with a common atmospheric δD value. Both caterpillars and moths were significantly enriched in deuterium relative to plants by â¼45 and 23 respectively, but the moths had lower tissue to plant discrimination factors than did the caterpillars. If the trophic enrichment documented here is universal, δD values must be accounted for in geographic assignment studies. The isotopic value of carbon was transferred more or less faithfully across trophic levels, but δ(15)N values increased from plants to insects and we observed significant non-trophic (15)N enrichment in the metamorphosis from larvae to adult.
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Brassica/metabolismo , Cadena Alimentaria , Lepidópteros/crecimiento & desarrollo , Lepidópteros/metabolismo , Metamorfosis Biológica , Animales , Isótopos de Carbono/química , Óxido de Deuterio/química , Óxido de Deuterio/metabolismo , Larva/metabolismo , Isótopos de Nitrógeno/químicaRESUMEN
The morphological and functional design of gastrointestinal tracts of many vertebrates and invertebrates can be explained largely by the interaction between diet chemical constituents and principles of economic design, both of which are embodied in chemical reactor models of gut function. Natural selection seems to have led to the expression of digestive features that approximately match digestive capacities with dietary loads while exhibiting relatively modest excess. Mechanisms explaining differences in hydrolase activity between populations and species include gene copy number variations and single-nucleotide polymorphisms. In many animals, both transcriptional adjustment and posttranscriptional adjustment mediate phenotypic flexibility in the expression of intestinal hydrolases and transporters in response to dietary signals. Digestive performance of animals depends also on their gastrointestinal microbiome. The microbiome seems to be characterized by large beta diversity among hosts and by a common core metagenome and seems to differ flexibly among animals with different diets.
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Dieta , Fenómenos Fisiológicos del Sistema Digestivo , Sistema Digestivo/microbiología , Animales , Aves/genética , Aves/fisiología , Proteínas Portadoras/genética , Proteínas Portadoras/fisiología , Sistema Digestivo/metabolismo , Peces/genética , Peces/fisiología , Dosificación de Gen/fisiología , Humanos , Hidrolasas/genética , Hidrolasas/fisiología , Ratones , Polimorfismo de Nucleótido Simple , Primates/genética , Primates/microbiología , Primates/fisiología , Procesamiento Proteico-Postraduccional/fisiología , Ratas , Selección Genética/fisiología , Transcripción Genética/fisiologíaRESUMEN
Seed dispersal has a powerful influence on population dynamics, genetic structuring, evolutionary rates, and community ecology. Yet, patterns of seed dispersal are difficult to measure due to methodological shortcomings in tracking dispersed seeds from sources of interest. Here we introduce a new method to track seed dispersal: stable isotope enrichment. It consists of leaf-feeding plants with sprays of 15N-urea during the flowering stage such that seeds developed after applications are isotopically enriched. We conducted a greenhouse experiment with Solanum americanum and two field experiments with wild Capsicum annuum in southern Arizona, USA, to field-validate the method. First, we show that plants sprayed with 15N-urea reliably produce isotopically enriched progeny, and that delta 15N (i.e., the isotopic ratio) of seeds and seedlings is a linear function of the 15N-urea concentration sprayed on mothers. We demonstrate that three urea dosages can be used to distinctly enrich plants and unambiguously differentiate their offspring after seeds are dispersed by birds. We found that, with high urea dosages, the resulting delta 15N values in seedlings are 10(3) - 10(4) times higher than the delta 15N values of normal plants. This feature allows tracking not only where seeds arrive, but in locations where seeds germinate and recruit, because delta 15N enrichment is detectable in seedlings that have increased in mass by at least two orders of magnitude before fading to normal delta 15N values. Last, we tested a mixing model to analyze seed samples in bulk. We used the delta 15N values of batches (i.e., combined seedlings or seeds captured in seed traps) to estimate the number of enriched seeds coming from isotopically enriched plants in the field. We confirm that isotope enrichment, combined with batch-sampling, is a cheap, reliable, and user-friendly method for bulk-processing seeds and is thus excellent for the detection of rare dispersal events. This method could further the study of dispersal biology, including the elusive, but critically important, estimation of long-distance seed dispersal.
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Aves/fisiología , Capsicum/química , Conducta Alimentaria/fisiología , Isótopos de Nitrógeno/análisis , Semillas/química , Solanum/química , Animales , Capsicum/fisiología , Ecosistema , Monitoreo del Ambiente/métodos , Marcaje Isotópico , Movimiento , Dinámica Poblacional , Semillas/crecimiento & desarrollo , Semillas/fisiología , Solanum/fisiologíaRESUMEN
To maintain water and electrolyte balance, nectar-feeding vertebrates oscillate between two extremes: avoiding overhydration when feeding and preventing dehydration during fasts. Several studies have examined how birds resolve this osmoregulatory dilemma, but no data are available for nectar-feeding mammals. In this article, we 1) estimated the ability of Pallas's long-tongued bats (Glossophaga soricina; Phyllostomidae) to dilute and concentrate urine and 2) examined how water intake affected the processes that these bats use to maintain water balance. Total urine osmolality in water- and salt-loaded bats ranged between 31 +/- 37 mosmol/kgH(2)O (n = 6) and 578 +/- 56 mosmol/kgH(2)O (n = 2), respectively. Fractional water absorption in the gastrointestinal tract was not affected by water intake rate. As a result, water flux, body water turnover, and renal water load all increased with increasing water intake. Despite these relationships, glomerular filtration rate (GFR) was not responsive to water loading. To eliminate excess water, Pallas's long-tongued bats increased water excretion rate by reducing fractional renal water reabsorption. We also found that rates of total evaporative water loss increased with increasing water intake. During their natural daytime fast, mean GFR in Pallas's long-tongued bats was 0.37 ml/h (n = 10). This is approximately 90% lower than the GFR we measured in fed bats. Our findings 1) suggest that Pallas's long-tongued bats do not have an exceptional urine-diluting or -concentrating ability and 2) demonstrate that the bats eliminate excess ingested water by reducing renal water reabsorption and limit urinary water loss during fasting periods by reducing GFR.
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Líquidos Corporales/fisiología , Quirópteros/fisiología , Riñón/fisiología , Equilibrio Hidroelectrolítico/fisiología , Alimentación Animal , Animales , Ingestión de Líquidos/fisiología , Femenino , Tránsito Gastrointestinal/fisiología , Masculino , Mamíferos , Agua/metabolismoRESUMEN
Ecologists conduct isotopic incorporation experiments to determine the residence time of various stable isotopes in animal tissues. These experiments permit determining the time window through which isotopic ecologists perceive the course of diet changes, and therefore the scale of the inferences that we can make from isotopic data. Until recently, the results of these experiments were analyzed using first-order, one-compartment models. Cerling et al. (Oecologia 151:175-189, 2007) proposed an approach they named the reaction progress variable to: (1) determine how many compartments are needed to describe a pattern of istopic incorporation, and (2) to estimate the size and rate constant of each pool. We elaborate on the approach described by Cerling et al. (Oecologia 151:175-189, 2007) by providing a way to estimate average retention times for an isotope in a tissue (and its associate error) for multi-compartment models. We also qualify the interpretation of the parameters in multi-compartment models by showing that many possible mechanisms yield models with the same functional form. Multi-compartment models are phenomenological, rather than mechanistic descriptions, of incorporation data. Finally, we propose the use of information theoretic criteria to assess the number of compartments that must be included in models of isotopic incorporation.
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Dieta , Isótopos/farmacocinética , Modelos Biológicos , Animales , Factores de TiempoRESUMEN
The metabolic theory of ecology (MTE) claims to derive ecological relationships from the structure of resource distribution networks, which is assumed to determine the scaling of metabolism with body mass, and from the effect of temperature on the rate of biological processes. MTE is controversial. I propose that some of the controversy stems from the implicit adoption of different views of science by the proponents and critics of MTE. The perspective of proponents is consistent with the theory-centric view of science called the received view, whereas many of the critics implicitly adopt an alternative view consistent with a model-centric view of science. I propose that adopting the model-centric view can help to settle some of the differences among proponents and critics of MTE.
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Ecología/tendencias , Metabolismo , Modelos BiológicosRESUMEN
The use of stable isotopes to investigate animal diets, habitat use, and trophic level requires understanding the rate at which animals incorporate the 13C and 15N from their diets and the factors that determine the magnitude of the difference in isotopic composition between the animal's diet and that of its tissues. We determined the contribution of growth and catabolic turnover to the rate of 13C and 15N incorporation into several tissues that can be sampled non-invasively (skin, scute, whole blood, red blood cells, and plasma solutes) in two age classes of a rapidly growing ectotherm (loggerhead turtles, Caretta caretta). We found significant differences in C and N incorporation rates and isotopic discrimination factors (Delta 13C = delta 13Ctissues - delta 13Cdiet and Delta 15N = delta 15Ntissues - delta 15Ndiet) among tissues and between age classes. Growth explained from 26 to 100% of the total rate of incorporation in hatchling turtles and from 15 to 52% of the total rate of incorporation in juvenile turtles. Because growth contributed significantly to the rate of isotopic incorporation, variation in rates among tissues was lower than reported in previous studies. The contribution of growth can homogenize the rate of isotopic incorporation and limit the application of stable isotopes to identify dietary changes at contrasting time scales and to determine the timing of diet shifts. The isotopic discrimination factor of nitrogen ranged from -0.64 to 1.77 per thousand in the turtles' tissues. These values are lower than the commonly assumed average 3.4 per thousand discrimination factors reported for whole body and muscle isotopic analyses. The increasing reliance on non-invasive and non-destructive sampling in animal isotopic ecology requires that we recognize and understand why different tissues differ in isotopic discrimination factors.
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Carbono/metabolismo , Nitrógeno/metabolismo , Tortugas/crecimiento & desarrollo , Tortugas/metabolismo , Factores de Edad , Animales , Isótopos de Carbono , Dieta , Modelos Biológicos , Isótopos de Nitrógeno , Factores de Tiempo , Distribución TisularRESUMEN
We sought to characterize the ability of hummingbirds to fuel their energetically expensive hovering flight using dietary sugar by a combination of respirometry and stable carbon isotope techniques. Broadtailed hummingbirds (Selasphorus platycercus) were maintained on a diet containing beet sugar with an isotopic composition characteristic of C3 plants. Hummingbirds were fasted and then offered a solution containing cane sugar with an isotopic composition characteristic of C4 plants. By monitoring the rates of CO2 production and O2 consumption, as well as the stable carbon isotope composition of expired CO2, we were able to estimate the relative contributions of carbohydrate and fat, as well as the absolute rate at which dietary sucrose was oxidized during hovering. The combination of respirometry and carbon isotope analysis revealed that hummingbirds initially oxidized endogenous fat following a fast and then progressively oxidized proportionately more carbohydrates. The contribution from dietary sources increased with each feeding bout, and by 20 min after the first meal, dietary sugar supported approximately 74% of hovering metabolism. The ability of hummingbirds to satisfy the energetic requirements of hovering flight mainly with recently ingested sugar is unique among vertebrates. Our finding provides an example of evolutionary convergence in physiological and biochemical traits among unrelated nectar-feeding animals.
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Aves/metabolismo , Metabolismo de los Hidratos de Carbono/fisiología , Metabolismo Energético/fisiología , Vuelo Animal/fisiología , Animales , Carbohidratos/química , Isótopos de Carbono , Carbohidratos de la Dieta , Conducta Alimentaria , Oxidación-ReducciónRESUMEN
Understanding the storage, flux, and turnover of nutrients in organisms is important for quantifying contributions of biota to biogeochemical cycles. Here we present a model that predicts the storage of phosphorus-rich RNA and whole-body phosphorus content in eukaryotes based on the mass- and temperature-dependence of ATP production in mitochondria. Data from a broad assortment of eukaryotes support the model's two main predictions. First, whole-body RNA concentration is proportional to mitochondrial density and consequently scales with body mass to the -1/4 power. Second, whole-body phosphorus content declines with increasing body mass in eukaryotic unicells but approaches a relatively constant value in large multicellular animals because the fraction of phosphorus in RNA decreases relative to the fraction in other pools. Extension of the model shows that differences in the flux of RNA-associated phosphorus are due to the size dependencies of metabolic rate and RNA concentration. Thus, the model explicitly links two biological currencies at the individual level: energy in the form of ATP and materials in the form of phosphorus, both of which are critical to the functioning of ecosystems. The model provides a framework for linking attributes of individuals to the storage and flux of phosphorus in ecosystems.