Marcela Franco

Whole-animal metabolic rate is a repeatable trait: a meta-analysis

SUMMARY Repeatability studies are gaining considerable interest among physiological ecologists, particularly in traits affected by high environmental/residual variance, such as whole-animal metabolic rate (MR). The original definition of repeatability, known as the intraclass correlation coefficient, is computed from the components of variance obtained in a one-way ANOVA on several individuals from which two or more measurements are performed. An alternative estimation of repeatability, popular among physiological ecologists, is the Pearson product–moment correlation between two consecutive measurements. However, despite the more than 30 studies reporting repeatability of MR, so far there is not a definite synthesis indicating: (1) whether repeatability changes in different types of animals; (2) whether some kinds of metabolism are more repeatable than others; and most important, (3) whether metabolic rate is significantly repeatable. We performed a meta-analysis to address these questions, as well as to explore the historical trend in repeatability studies. Our results show that metabolic rate is significantly repeatable and its effect size is not statistically affected by any of the mentioned factors (i.e. repeatability of MR does not change in different species, type of metabolism, time between measurements, and number of individuals). The cumulative meta-analysis revealed that repeatability studies in MR have already reached an asymptotical effect size with no further change either in its magnitude and/or variance (i.e. additional studies will not contribute significantly to the estimator). There was no evidence of strong publication bias.

Communal nesting, activity patterns, and population characteristics in the near-threatened monito del monte, Dromiciops gliroides

Abstract The “living fossil,” Dromiciops gliroides (monito del monte), is an endemic marsupial inhabiting the temperate rain forests of South America. It is cavity-dependent and faces high energetic costs associated with thermoregulation during the austral winter. Although D. gliroides is well known for seed dispersal in temperate rain forests, its ecology, behavior, and long-term population dynamics have received little attention. We monitored a population of D. gliroides and studied variation in abundance and density and seasonal changes in body mass and body condition index (BCI). In addition, we monitored activity and communal nesting with camera traps and nest boxes, respectively. Over 4 years we documented a mean population density of 26 (95% confidence interval  =  19–32) individuals/ha. We found significantly greater body mass and BCI for females than for males, suggesting different energetic strategies during the prehibernation period. Animals were nocturnal and active until dawn. Communal nesting occurred during summer and early fall, but torpor by single individuals and small groups was increasingly frequent during winter. Communal nesting could be a key behavioral strategy affecting survival. However, given the greater frequency in warm seasons and groups composed of postreproductive females and juveniles, communal nesting might be more related to parental care associated with kin selection than to thermoregulation.

Profound changes in blood parameters during torpor in a South American marsupial

Seasonal torpor or hibernation is a phenomenon characterized by a physiological transition to dormancy (torpor) during challenging periods in terms of energy availability or metabolic load. Extensive physiological reprogramming and changes in gene-expression, immune function, oxygen transport and intermediate metabolism, occur during eutherian hibernation. Here we studied the seasonality of blood parameters, and during daily torpor, in a South American marsupial (Dromiciops gliroides). Seasonal trends in blood parameters showed an increase in hematological parameters during winter, and increases in total proteins, albumin and globulin during autumn. In contrast, torpor induced a drastic drop during most blood parameters. PCV dropped significantly 60%, as well as RBC (58%), hemoglobin concentration (58%), WBC (79%), including neutrophils (51%), eosinophils (84%) and lymphocytes (82%). Biochemical parameters also showed reductions: triglycerides (81%), proteins (32%), albumin (24%), globulins (38%), albumin (24%), creatinine (48%) and glucose (42%). Our results confirm some patterns observed in hibernating eutherians, such as leukopenia, probably caused by sequestration of white blood cells in organs. However, red blood cells and hemoglobin concentration also were reduced, which is to the best of our knowledge has not been reported for marsupials. The observed reduction in biochemical parameters suggests that marsupials, as in eutherians, change from carbohydrate-based to lipid-based metabolism during hibernation. However, the absence of increases in beta-hydroxybutyrate is puzzling. Finally, we found an increase (although non-significant after statistical correction for multiple comparisons) of creatine kinase which together with an increase in neutrophil/lymphocyte ratio could be indicative of muscle lysis and inflammation. These results indicate profound changes in standard physiological processes during torpor.

Bioenergetics and intestinal phenotypic flexibility in the microbiotherid marsupial (Dromiciops gliroides) from the temperate forest in South America.

The microbiotherid marsupial Dromiciops gliroides inhabits the temperate forests of the Southern hemisphere, facing seasonal nutritional and energetic bottlenecks due to its apparently facultative insectivory/frugivory. In order to understand the physiological processes behind this ecological pattern, we studied the morpho-physiological changes that D. gliroides exhibits after dietary acclimation, in a sample of 21 wild-caught individuals fed over 1 month with ad libitum diet of: (1) fruit, (2) insects or (3) a mix of insects and fruit. In addition, we measured oxygen consumption (VO(2)) at resting conditions. We also performed enzyme assays (sucrase, maltase, trehalase and aminopeptidase N) and measurements of organ morphology. We found that D. gliroides cannot fulfil its nutrient requirements only from insects or fruit. It needs a mixed diet in order to maintain its body mass and energy balance. However, as a response of diet acclimation, individuals showed several-fold changes in the activities of aminopeptidase-N, maltase and sucrase (but not trehalase). This result, both the magnitude of change and the simultaneous effects on three enzymes suggests that D. gliroides could exhibit adaptive phenotypic plasticity in the activity of intestinal enzymes. This study suggests also that D. gliroides, the only living representative of the Microbiotheria order, exhibits physiological adaptations to a generalist diet.

Aerobic power, huddling and the efficiency of torpor in the South American marsupial, Dromiciops gliroides

Summary During periods of cold, small endotherms depend on a continuous supply of food and energy to maintain euthermic body temperature (Tb), which can be challenging if food is limited. In these conditions, energy-saving strategies are critical to reduce the energetic requirements for survival. Mammals from temperate regions show a wide arrange of such strategies, including torpor and huddling. Here we provide a quantitative description of thermoregulatory capacities and energy-saving strategies in Dromiciops gliroides, a Microbiotherid marsupial inhabiting temperate rain forests. Unlike many mammals from temperate regions, preliminary studies have suggested that this species has low capacity for control and regulation of body temperature, but there is still an incomplete picture of its bioenergetics. In order to more fully understand the physiological capacities of this “living fossil”, we measured its scope of aerobic power and the interaction between huddling and torpor. Specifically, we evaluated: (1) the relation between basal (BMR) and maximum metabolic rate (MMR), and (2) the role of huddling on the characteristics of torpor at different temperatures. We found that BMR and MMR were above the expected values for marsupials and the factorial aerobic scope (from CO2) was 6.0±0.45 (using CO2) and 6.2±0.23 (using O2), an unusually low value for mammals. Also, repeatability of physiological variables was non-significant, as in previous studies, suggesting poor time-consistency of energy metabolism. Comparisons of energy expenditure and body temperature (using attached data-loggers) between grouped and isolated individuals showed that at 20°C both average resting metabolic rate and body temperature were higher in groups, essentially because animals remained non-torpid. At 10°C, however, all individuals became torpid and no differences were observed between grouped and isolated individuals. In summary, our study suggests that the main response of Dromiciops gliroides to low ambient temperature is reduced body temperature and torpor, irrespective of huddling. Low aerobic power and low time-consistency of most thermoregulatory traits of Dromiciops gliroides support the idea of poor thermoregulatory abilities in this species.

Thermoregulatory capacities and torpor in the South American marsupial, Dromiciops gliroides

During periods of adverse conditions small endotherms depend on a continuous supply of food and energy to maintain body temperature. Thus, rapid and reversible phenotypic modifications at different organizational levels are key for an efficient use of resources and survival. In this study, we provide a quantitative description of thermoregulatory capacities and energy-saving strategies in the Chilean marsupial Dromiciops gliroides. In particular, we evaluated the effect of thermal acclimation on basal metabolic rate (BMR), thermal conductance (C) and torpor patterns, as well as the presence of non-shivering thermogenesis (NST) as a rewarming mechanism in this marsupial. Non-significant effects of thermal acclimation were observed in BMR, C and body mass, but cold-acclimated individuals exhibited significantly longer torpor bouts. Also, minimum body temperature during torpor, inter-bout body temperature and arousal rewarming rate were lower in cold-acclimated animals. Furthermore, we found that D. gliroides did not display NST in response to Norepinephrine. Hence, despite the high regulation of torpor of other species, D. gliroides shows low flexibility in the ability to adjust energy expenditure and insulation properties, and (as in other marsupials) NST do not seems to be important as thermoregulatory mechanism.