Daniel E. Naya

Latitudinal trends in digestive flexibility: testing the climatic variability hypothesis with data on the intestinal length of rodents.

Flexibility of digestive features can be understood considering the benefits of digestion, which links animal foraging to metabolizable energy and nutrient gain, and its costs, which are partly indexed by digestive tract tissue mass, one of the most expensive to maintain in terms of energy and protein metabolism. In this article, we applied a meta‐analytical approach to current data on rodents’ small intestine length flexibility to evaluate the climatic variability hypothesis (CVH). This hypothesis states the following: (1) as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should be more flexible to persist at a site; (2) the greater phenotypic flexibility allows species to occupy more habitats and to become more widely distributed. We compiled data from 25 articles, which provided a total of 86 estimations of flexibility involving 20 rodent species. Consistent with CVH predictions, we found a positive correlation between small intestine length flexibility and latitude and between small intestine length flexibility and the number of habitats occupied by different species. When seen from the perspective of digestive physiology, our analysis is an important piece of evidence on the adaptive value of digestive flexibility in small mammals.

Diet of the South American frog Leptodactylus ocellatus (Anura, Leptodactylidae) in Uruguay

The diet of Leptodactylus ocellatus (L., 1758) was studied in specimens collected at Maldonado Department (Uruguay), where monthly surveys were made between August 1998 and March 2000. A total of 143 frogs were collected, measured, sexed, and dissected, to assess stomach contents. The anurans were grouped into three age classes and four categories (considering sex and capture date). The trophic amplitude for each age class and sex-season category was quantified using Shannon-Weaver Index, and the trophic niche overlap between ages and categories by using the Pianka Index. Comparisons among treatments were made by G-tests. The most important prey items were coleopterans (IRI = 2547), and significant correlations were found between predator and prey sizes. The major differences on diet composition were found between extreme age classes (froglets and adults). Significant differences were also detected between sexes in the cold season but not in the warm season. Any of these changes in diet may be related with the availability of prey.

Adjusting energy expenditures to energy supply: food availability regulates torpor use and organ size in the Chilean mouse-opossum Thylamys elegans

We studied how food abundance and consumption regulates torpor use and internal organ size in the Chilean mouse-opossum Thylamys elegans (Dielphidae), a small nocturnal marsupial, endemic in southern South America. We predicted that exposure to food rations at or above the minimum energy levels necessary for maintenance would not lead to any signs of torpor, while reducing food supply to energy levels below maintenance would lead to marked increases in frequency, duration and depth of torpor bouts. We also analyzed the relationship between food availability and internal organ mass. We predicted a positive relationship between food availability and internal organ size once the effect of body size is removed. Animals were randomly assigned to one of two groups and fed either 70, 100 or 130% of their daily energy requirement (DER). We found a positive and significant correlation between %DER and body temperature, and also between %DER and minimum body temperature. In contrast, for torpor frequency, duration and depth, we found a significant negative correlation with %DER. Finally, we found a significant positive correlation between the %DER and small intestine and ceacum dry mass. We demonstrate that when food availability is limited, T. elegans has the capacity to reduce their maintenance cost by two different mechanisms, that is, increasing the use of torpor and reducing organ mass.

Digestive and Metabolic Flexibility Allows Female Degus to Cope with Lactation Costs

Lactation is the most energetically demanding period in the life cycle of female mammals, and its effects on digestive flexibility and the size of internal organs have been extensively studied in laboratory mice and rats since the early 1900s. However, there have been only two studies on this topic for wild rodent species. Here, we analyzed digestive flexibility—that is, changes in gut content, activity of digestive enzymes, and gut morphology—during lactation in the caviomorph rodent Octodon degus. In addition, we evaluated changes in the size of other internal organs and analyzed their relationship with the resting metabolic rate. We found that gut content, the dry masses of digestive chambers, the dry mass of liver, and resting metabolic rate were greater in lactating than in nonbreeding control females. In contrast, fat stores were higher in control subjects. Maltase and aminopeptidase‐N specific activity did not change with lactation, and both enzymes had greater activity values in the middle portion of the small intestine. Thus, our data indicate that the previously reported increase in food assimilation that occurs during lactation in O. degus is related to a mass increase in several central organs, leading, in turn, to higher energetic costs. Fat stores may help to mitigate these costs, but, as expected for small animals, to a limited extent. Our study reveals a complex interplay among energy acquisition, storage, and expenditure processes that ultimately determine an organism’s fitness.

Digestive Phenotypic Flexibility in Post-Metamorphic Amphibians: Studies on a Model Organism

Studies of phenotypic flexibility are central to the understanding of evolutionary and comparative physiology. Research conducted on many vertebrate species has shown that the digestive system is highly responsive and sensitive to environmental cues. However, amphibians, which are a standard and classic model organism for the study of many physiological processes, have been poorly considered in the study of ecological consequences on digestive flexibility. Here we review and analyze the current information on this topic for amphibians. We identify three major bodies of empirical evidence: a) seasonal changes in gut development, b) lack of dietary modulation of gut attributes in adult individuals, c) a relationship between feeding habits and the magnitude of digestive performance regulation. Once the natural history characteristics of the species under study are taken into account, all the evidence is in full agreement with the predictions of digestive theory. We propose that evolutionary and comparative physiology could benefit greatly from the study of phenotypic flexibility in amphibians.

The effect of short- and long-term fasting on digestive and metabolic flexibility in the Andean toad, Bufo spinulosus

SUMMARY Hibernation in ectothermic animals was historically considered as a simple cold-induced torpor state resulting from the inability to maintain a high body temperature at low ambient temperatures. During the last decades this vision changed and nowadays there is a myriad of studies showing that hibernation implies different adjustments at the genetic, molecular, biochemical and cellular levels. However, studies oriented to evaluate changes of whole organism structure and physiology still are scarce, which is particularly true for amphibians that hibernate on land. Accordingly, in the Andean toad (Bufo spinulosus), we investigated the effect of short-term fasting and hibernation on the hydrolytic activity of digestive enzymes, histology of the small intestine, gross morphology of digestive and other internal organs and standard metabolic rate. Based on the pattern of size variation, internal organs may be grouped into those that were affected by both season and feeding condition (small intestine, stomach and liver), those that were only affected by season (fat bodies), those that were only affected by feeding condition (kidneys) and, finally, those that did not change between the three groups (large intestine, heart and lungs). Hydrolytic activity of maltase, trehalase and aminopeptidase-N followed the same pattern of variation (feeding>fasting>hibernating toads), although the change for the latter enzyme was less noticeable than for the disaccharidases. Enzymatic adjustments were correlated with changes in small intestine histology: villus and enterocyte height increased from hibernating to fasting and more markedly from fasting to feeding toads. Metabolic rate decreased during hibernation to 7.8% (at 5°C) and 13.6% (at 15°C) of summer values, which is one of the highest metabolic depressions reported for any ectothermic vertebrate. Our results suggest that amphibian persistence in highly seasonal environments is related to a large capacity of phenotypic flexibility at different organisational levels; an ability that may be related to the extensive ranges of temporal existence and geographic distribution of these vertebrates.

Physiological flexibility in the Andean lizard Liolaemus bellii: seasonal changes in energy acquisition, storage and expenditure

According to the “barrel model”, an organism may be represented by a container, with input energy constraints (foraging, digestion, and absorption) symbolized by funnels connected in tandem, and energy outputs (maintenance, growth, and reproduction) symbolized by a series of spouts arranged in parallel. Animals can respond to changes in environmental conditions, through adjustments in the size of the funnels, the fluid stored inside the barrel, or the output flow through the spouts. In the present study, we investigate the interplay among these processes through the analysis of seasonal changes in organ size and metabolic rate in a lizard species (Liolaemus bellii) that inhabits extremely seasonal environments in the Andes range. We found that digestive organ size showed the greatest values during spring and summer, that is, during the foraging seasons. Energy reserves were larger during summer and autumn, and then decreased through winter and spring, which was correlated with overwintering maintenance and reproductive costs. Standard metabolic rate was greater during the high-activity seasons (spring and summer), but this increase was only noticeable at higher environmental temperatures. The ability of many lizard species to reduce their maintenance cost during the cold months of the year, beyond what is expected from temperature decrease, is probably related to their success in coping with highly fluctuating environments. Here, we demonstrate that this ability is correlated with high physiological flexibility, which allows animals to adjust energy acquisition, storing and expenditure processes according to current environmental conditions.

Latitudinal Patterns in Rodent Metabolic Flexibility

Macrophysiology is defined as the study of variation in physiological traits—including physiological trait flexibility—over large geographical and temporal scales, and the ecological implications of this variation. A classic example of a macrophysiological trend is the one emerging from the climatic variability hypothesis, which states that as the range of climatic fluctuation experienced by terrestrial animals increases with latitude, individuals at higher latitudes should be more plastic than individuals inhabiting lower latitudes. In this context, we evaluate the correlation between absolute metabolic scope during cold exposure (an instantaneous measure of metabolic flexibility) and different geographic and climatic variables for 48 rodent species. Conventional and phylogenetic informed analyses indicated a positive correlation between metabolic scope and geographic latitude. These findings, together with previous reports on latitudinal pattern in phenotypic flexibility, suggest that an increase in physiological flexibility with latitude may hold for many phenotypic traits.

HOW DOES EVOLUTIONARY VARIATION IN BASAL METABOLIC RATES ARISE? A STATISTICAL ASSESSMENT AND A MECHANISTIC MODEL

Metabolic rates are related to the pace of life. Hence, research into their variability at global scales is of vital importance for several contemporary theories in physiology, ecology, and evolution. Here we evaluated the effect of latitude, climate, primary productivity, habitat aridity, and species trophic habits, on mass‐independent basal metabolic rates (BMRs) for 195 rodent species. The aims of this article were twofold. First, we evaluated the predictive power of different statistical models (via a model selection approach), using a dimensional reduction technique on the exogenous factor matrix to achieve a clear interpretation of the selected models. Second, we evaluated three specific predictions derived from a recently proposed hypothesis, herein called the “obligatory heat” model (OHM), for the evolution of BMR. Obtained results indicate that mean/minimum environmental temperature, rainfall/primary productivity and, finally, species trophic habits are, in this order, the major determinants of mass‐independent BMR. Concerning the mechanistic causes behind this variation, obtained data agree with the predictions of the OHM: (1) mean annual environmental temperature was the best single predictor of residual variation in BMR, (2) herbivorous species have greater mass‐independent metabolic rates, and tend to be present at high‐latitude cold environments, than species in other trophic categories.

Gut size flexibility in rodents: what we know, and don't know, after a century of research

La plasticidad fenotipica constituye un concepto medular en el entendimiento de como los organismos interactuan con su ambiente y, por tanto, un tema central en ecologia y evolucion. Un caso particular de la plasticidad fenotipica es la flexibilidad fenotipica, la cual refiere a los cambios reversibles en un organismo producto de cambios en las condiciones ambientales. La flexibilidad en los rasgos digestivos ha sido estudiada por mas de un siglo en diversas especies y contextos. Para el caso de los roedores, los estudios sobre la flexibilidad en el tamano del tracto digestivo han sido desarrollados principalmente desde dos areas de la biologia, la fisiologia y la ecologia. Sin embargo, como ha ocurrido con muchos topicos relacionados con la fisiologia ecologica, ambos tipos de estudios se desarrollaron por vias separadas. En este trabajo se intenta evaluar de forma conjunta la informacion proveniente de ambas areas. Las principales conclusiones alcanzadas son: (1) la flexibilidad en el tamano del tracto digestivo puede ser considerada un mecanismo fisiologico ampliamente distribuido, existiendo un clara congruencia entre los ajustes en la morfologia digestiva y los cambios en las condiciones ambientales. (2) Los factores experimentales mas investigados han sido la calidad de la dieta, el estatus reproductivo, la temperatura ambiental y el ayuno para las especies de laboratorio y la calidad de la dieta y la temperatura para las especies salvajes. (3) En especies salvajes no se han encontrado diferencias en la flexibilidad del largo intestinal entre estudios con distintas aproximaciones metodologicas ni entre especies con distintos habitos troficos. (4) Los cambios en la demanda energetica parecen ser principalmente afrontados mediante ajustes en el intestino delgado, mientras que los cambios en la cantidad de material indigestible en la dieta parecen ser principalmente afrontados mediante ajustes en el ciego e intestino grueso. (5) Los cambios en el largo del tracto digestivo parecen estar relacionados con la necesidad de ajustar el tiempo de retencion del alimento (e.g., durante la dilucion de la dieta), mientras que cambios en la masa del tracto parecen estar relacionados con la necesidad de modificar la tasa de absorcion especifica (e.g., durante un periodo de alta demanda energetica). (6) Las caracteristicas de una demanda energetica (e.g., su intensidad relativa), mas que su simple presencia o ausencia, pueden afectar la magnitud de los ajustes en las dimensiones del tracto digestivo. (7) A pesar de la gran cantidad de trabajos publicados, comparaciones cuantitativas de los datos existentes son dificiles de realizar, debido a factores tales como la disparidad en los tratamientos experimentales y en el tipo de informacion reportada. Para finalizar esta revision se presentan nuevas direcciones en cuanto al estudio de la flexibilidad digestiva en roedores.