Claudio Veloso

Dietary and Digestive Constraints on Basal Energy Metabolism in a Small Herbivorous Rodent

McNab (1986, 1988) has hypothesized that mammals using food with low energy content should exhibit basal metabolic rates (BMR) lower than those expected on the basis of their body mass (mb). That is, those species that exploit food with low energy content and/or high cost of digestion tend to have low, mass-independent metabolic rates. To date there is not an experimental test of this pattern. The aim of this work was to examine experimentally the effect of diet quality on BMR, digestive efficiency, and the relationship between digestion and energy expenditure in a small herbivorous mammal. We used as a model the herbivorous caviomorph burrowing rodent Octodon degus (mb nearly 200 g), an inhabitant of semi-arid and mediterranean communities of northern and central Chile. Individuals maintained during 27 wk with a diet high in dietary fiber showed significantly lower BMRs (28%) than those feeding on low fiber. Daily food intake and ingestion rates (energy and dry matter) of individuals under a high-fiber diet were significantly higher than animals maintained with a low-fiber diet. The same pattern was obtained for total feces production and rate of feces production. The total intake and rate of ingestion of proteins were not significantly different between treatments. However, a significantly higher amount of protein was excreted by the individuals exposed to a high-fiber diet. Apparent digestibility of dry matter, energy, and protein were consistently lower in individuals maintained with high fiber. However, nonsignificant differences were observed between gut contents in the two treatments (P > .58), but a significantly higher digesta turnover rate was observed in animals exposed to a high-fiber diet (P < .05). A significant correlation was found between digestibility and the basal metabolic rate of individuals (r, = 0.781, P < .01), suggesting that elevated digestibilities on high-quality diets allow increased basal rates of metabolism. We suggest that, although small mammals like degus may select sparsely distributed plants of high quality in their habitat, their capability to drop their metabolic demands may help them meet their nutritional and energy requirements when nutritional conditions in the environment deteriorate.

Seasonal Changes in Energy Expenditure and Digestive Tract of Abrothrix andinus (Cricetidae) in the Andes Range

The South American field mouse Abrothrix andinus (Rodentia: Cricetidae) is a small mammal active throughout the year in the Andes, despite substantial seasonal environmental changes. Body mass exhibited a significant decrease during winter, and maximum metabolic rate for thermoregulation increased by 36.6%. In absolute terms, the maximum thermal differential between body and environmental temperatures increased 44° C during winter. On the other hand, body temperature and thermal conductance did not show significant changes through the year; however, mass-independent conductance decreased in winter. Parallel to these changes, the length and dry mass of the total digestive tract changed significantly with wintertime; at the same time the length and mass of the small intestine and the length of the large intestine also showed significance. Significant differences in gastrointestinal morphology between males andfemales were found only during the reproductive season (summer).

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.

Temporal dynamics of milk composition of the precocial caviomorph Octodon degus (Rodentia: Octodontidae)

During lactation, both the nutritional and energetic requirements of suckling change gradually. These changes normally are accompanied by modifications in chemical composition of the milk. We investigated the temporal course of milk composition during lactation in a precocial caviomorph rodent, the “degu” (Octodon degus) under laboratory condition. Female degus were kept in laboratory during gestation and lactation and fed with commercial food pellets. Milk was collected at three stages of lactation: early (days 5-8, n = 12), middle (days 15-21, n = 7) and late (days 26-40, n = 6), and analyzed for protein, carbohydrates, lipids, ash, total solids and energy. On average, carbohydrates decreased from 3.1 ± 0.3 % (early) to 1.1 ± 0.3 % (late) during lactation; lipids, protein, ash, total solids and energy remained about the same. Lipids, the main component of the milk, were 17.3 % and protein remained near 4.4 %. Over lactation, total energy concentration of milk remained near 4.0 kJ mL -1 . The maintenance of milk composition during lactation may be related to the initially high energetic and nutritional requirements associated with a precocial reproductive mode.

Respiratory Refinements In The Mygalomorph Spider Grammostola rosea Walckenaer 1837 (Araneae, Theraphosidae)

Abstract In this study we hypothesized that Grammostola rosea Walckenaer 1837, an active predator of large size that depends on its two paired book lungs for respiration, would have a refined low energy strategy based on its thin air-hemolymph barrier. The morphology of book lungs and the oxygen consumption at 20° and 30° C under normal and starvation conditions were studied. The oxygen consumption was low compared to that expected for spiders from the allometric relationship, 0.027 ± 0.01 ml O2 g−1 h−1 (average ± standard deviation), and it was depressed at 30° C under starvation. The harmonic mean thickness of the air-hemolymph barrier was 0.14 ± 0.03 µm, the respiratory surface density was 122.99 ± 35.84 mm−1, and the book lung volume ranged from 12.2 to 37.5 mm3. With these parameters a high oxygen diffusion capacity was estimated. The combination of low resting oxygen consumption and high pulmonary oxygen conductance results in very low gradients of partial oxygen pressures across the air-hemolymph barrier (0.12–0.16 kPa) required to satisfy the resting oxygen demands.

Ontogenic development of intestinal disaccharidases in the precocial rodent Octodon degus (Octodontidae)

We studied the ontogeny of the intestinal brush border disaccharidases sucrase and lactase in the precocial rodent Octodon degus. Sucrase hydrolyze sugars from plants while lactase hydrolyzes sugars from milk. Enzyme expression varied inversely with dietary changes according to the developmental pattern. All new-born pups had high lactase and low sucrase activities. Also, a negative correlation between sucrase and lactase activity was found, supporting the economic design hypothesis for the intestinal tract. Profiles for development of sucrase expression exhibit some differences among precocial species, and in O. degus is correlated with the slower transition from milk to solid food consumption at weaning.

Participation of book lungs in evaporative water loss in Paraphysa parvula, a migalomorph spider from Chilean Andes

Small animals need efficient water conservation mechanisms for survival and reproduction, which is relevant for the spiders that have large book lungs with large respiratory surface. If lung evaporation is relevant to limit water loss, adjustments of the spiracle opening to metabolic demands should be expected. In this study, we measured the metabolic rate and total evaporative water loss mediated by the opening of the spiracles in the migalomorph spider Paraphysa parvula, a resident of fluctuating Mediterranean environments of the mountains of central Chile. We found that the metabolism of P. parvula was similar to other Theraphosidae and low compared to other arthropods. Carbon dioxide production and evaporative water loss increased with temperature, particularly at 40 degrees C. The total evaporative water loss at 40 degrees C increased dramatically to about 10 times that found with the lower temperatures. Thus, 40 degrees C will be the limit temperature for this species after which evaporative water loss starts to become damaging, so it has to avoid it. The exposition to hypercapnic environments had as a consequence an increase in evaporative water loss and the involvement of the book lungs in this loss was about 60%. The possibility of losing water could condition this species to seek temperate and oxygenated shelters under rocks.

Intraspecific basal metabolic rate varies with trophic level in rufous-collared sparrows.

One of the most controversial hypotheses that associate basal metabolic rate (BMR) with food habits and habitat productivity is the food habit hypothesis (FHH). Here we examined the relationship between BMR, diet, and climate among populations of the omnivorous passerine, Zonotrichia capensis (Emberizidae). We used nitrogen stable isotopes to estimate each individuals relative trophic level. To tease apart the effect of climatic variables and diet on BMR, we also used structural equation modeling. After the effect of body mass and climatic variables was taken into account, a significant effect of trophic level as estimated by delta(15)N on BMR was found. Our result seems to support the FHH at the intraspecific level, i.e., birds from the lower trophic levels - feeding on seeds and bud - had higher BMR than individuals from higher trophic levels.

Adaptation of the spiders to the environment: the case of some Chilean species.

Spiders are small arthropods that have colonized terrestrial environments. These impose three main problems: (i) terrestrial habitats have large fluctuations in temperature and humidity; (ii) the internal concentration of water is higher than the external environment in spiders, which exposes them continually to water loss; and (iii) their small body size determines a large surface/volume ratio, affecting energy exchange and influencing the life strategy. In this review we focus on body design, energetic, thermal selection, and water balance characteristics of some spider species present in Chile and correlate our results with ecological and behavioral information. Preferred temperatures and critical temperatures of Chilean spiders vary among species and individuals and may be adjusted by phenotypic plasticity. For example in the mygalomorph high-altitude spider Paraphysa parvula the preferred temperature is similar to that of the lowland spider Grammostola rosea; but while P. parvula shows phenotypic plasticity, G. rosea does not. The araneomorph spiders Loxosceles laeta and Scytodes globula have greater daily variations in preferred temperatures at twilight and during the night, which are set to the nocturnal activity rhythms of these species. They also present acclimation of the minimum critical temperatures. Dysdera crocata has a low preferred temperature adjusted to its favorite prey, the woodlouse. Spider metabolic rate is low compared to other arthropods, which may be associated with its sit and wait predatory strategy particularly in primitive hunter and weavers. In mygalomorph spiders the respiratory system is highly optimized with high oxygen conductance, for example G. rosea needs only a difference of 0.12–0.16 kPa in the oxygen partial pressure across the air-hemolymph barrier to satisfy its resting oxygen consumption demands. Water loss is a significant stress for spiders. Paraphysa parvula shows an evaporative water loss 10 times more than usual when the temperature approaches 40°C and the participation of book lungs in this loss is about 60%. This species and others show seasonal changes in water loss accounted for by changes in cuticle permeability. The case of Chilean spiders shows how the ecophysiology in spiders is associated to their design and body size and how is affected by fluctuating Mediterranean environments, suggesting that the adaptive process can be seen as a route of optimizing the use of energy to cope with environmental restrictions imposed by the interaction with the terrestrial environment and lifestyle.