Phyllotis Darwini Research Articles

THE QUANTITATIVE GENETICS OF SUSTAINED ENERGY BUDGET IN A WILD MOUSE

We explored how morphological and physiological traits associated with energy expenditure over long periods of cold exposure would be integrated in a potential response to natural selection in a wild mammal, Phyllotis danwini. In particular, we studied sustained energy expenditure (SusMR), the rate of expenditure fueled by concurrent energy intake, basal metabolic rate (BMR), and sustained metabolic scope (SusMS = SusMR/BMR), a measure of the reserve for sustained work. We included the masses of different central processing organs as an underlying factor that could have a mechanistic link with whole animal traits. Only the liver had heritability statistically different from zero (0.73). Physiological and morphological traits had high levels of specific environmental variance (average 70%) and postnatal common environmental variance (average 30%) which could explain the low heritabilities estimates. Our results, (1) are in accordance with previous studies in mammals that report low heritabilities for metabolic traits (SusMR, BMR, SusMS), (2) but not completely with previous ones that report high heritabilities for morphological traits (masses of central organs), and (3) provide important evidence of the relevance of postnatal common environmental variance to sustained energy expenditure.

Body size as a latent variable in a structural equation model: thermal acclimation and energetics of the leaf-eared mouse.

Body size is one of the most important determinants of energy metabolism in mammals. However, the usual physiological variables measured to characterize energy metabolism and heat dissipation in endotherms are strongly affected by thermal acclimation, and are also correlated among themselves. In addition to choosing the appropriate measurement of body size, these problems create additional complications when analyzing the relationships among physiological variables such as basal metabolism, non-shivering thermogenesis, thermoregulatory maximum metabolic rate and minimum thermal conductance, body size dependence, and the effect of thermal acclimation on them. We measured these variables in Phyllotis darwini, a murid rodent from central Chile, under conditions of warm and cold acclimation. In addition to standard statistical analyses to determine the effect of thermal acclimation on each variable and the body-mass-controlled correlation among them, we performed a Structural Equation Modeling analysis to evaluate the effects of three different measurements of body size (body mass, m(b); body length, L(b) and foot length, L(f)) on energy metabolism and thermal conductance. We found that thermal acclimation changed the correlation among physiological variables. Only cold-acclimated animals supported our a priori path models, and m(b) appeared to be the best descriptor of body size (compared with L(b) and L(f)) when dealing with energy metabolism and thermal conductance. However, while m(b) appeared to be the strongest determinant of energy metabolism, there was an important and significant contribution of L(b) (but not L(f)) to thermal conductance. This study demonstrates how additional information can be drawn from physiological ecology and general organismal studies by applying Structural Equation Modeling when multiple variables are measured in the same individuals.

HERITABILITY OF ENERGETICS IN A WILD MAMMAL, THE LEAF-EARED MOUSE (PHYLLOTIS DARWINI)

As a first examination of the additive genetic variance of thermoregulatory traits in a natural population of endotherms, we studied the quantitative genetics of key physiological ecology traits in the leaf-eared mouse, Phyllotis darwini. We measured basal metabolic rate (BMR), nonshivering thermogenesis (NST), maximum metabolic rate for thermoregulation (MMR), thermal conductance (CT), body temperature (Tb), and factorial aerobic scope (FAS) in individuals acclimated to cold and warm conditions. For comparability with previous studies, we included the following morphological traits: foot length (FL), total length (TL), body mass (mb, at birth, sexual maturity, 6 months, and 8 months). Variance components were obtained from two different procedures: the expected variance component in an ANOVA Type III sum of squares and an animal model approach using restricted maximum likelihood. Results suggest the presence of additive genetic variance in FL (h2 = 0.47, P = 0.045), CT of cold-acclimated animals (h2 = 0.66, P = 0.041), and night body temperature, measured in cold-acclimated animals (h2 = 0.68, P = 0.080). Heritabilities of mb were near zero at all ages, but maternal effects and common environment effects were high and significant. We found no evidence of additive genetic variance in BMR, NST, MMR, or FAS (i.e., estimates were not significantly different from zero for all tests). Our results are in general agreement with previous studies of mammals that reported low heritability for: (1) BMR and MMR; (2) daytime body temperature; and (3) body mass for wild, but not laboratory or domestic, populations.

SMALL-MAMMAL FORAGING BEHAVIOR: MECHANISMS FOR COEXISTENCE AND IMPLICATION FOR POPULATION DYNAMICS

We investigated predation risk and competition as they affected small-mammal foraging behavior in semiarid north-central Chile. Giving-up densities (GUD) of seeds were used to measure the foraging activity of the three most common small mammals at the site: degu (Octodon degus), Darwin's leaf-eared mouse (Phyllotis darwini), and the olivaceous field mouse (Akodon olivaceus), under shrubs (cover) and in the open on predator-excluded and competitor-excluded (Octodon) plots. Experiments were conducted during both new and full moons. Monthly small-mammal censuses using standard mark–recapture techniques provided data on movement, reproduction, and long-term fluctuations in density between 1989 and 1994. Diurnal Octodon foraged more (had lower GUD) in the absence of predators (although this was confounded by a numerical increase resulting from predator exclusion), and foraged more under shrubs than in the open. However, the lack of a significant cover × predator exclusion interaction and thermoregulation studies suggest that physiological constraints play a greater role than predation risk in determining microhabitat selection by Octodon. Predation risk, as influenced by lunar light levels and predator exclusion, had only weak effects on microhabitat selection by Phyllotis. The strong tendency of Octodon to forage under cover could depress food availability, forcing Phyllotis to feed more in the open. Concomitantly, Phyllotis exhibits several morphological characters that would favor detection and avoidance of predators. There is extensive evidence that interspecific competition is the primary constraint on Akodon foraging; predation risk appears to be relatively unimportant. Akodon is also a less efficient forager than the two other species, having significantly higher GUD, on average. This is partially offset by differences in reproductive biology; Akodon exhibits extremely rapid demographic responses to favorable changes in the environment. A fourth species, Abrothrix longipilis, may coexist in the system because of its opportunistic nature, but no data are available on its foraging efficiency. These behavioral and biotic interactions occur within a background of periodic El Niño–Southern Oscillations (ENSO), which may ultimately contribute to species coexistence.

The influence of heat increment of feeding on basal metabolic rate in Phyllotis darwini (Muridae)

One of the most important prerequisites for obtaining a reliable measure of basal metabolic rate (BMR) in endotherms is that the animal must be in a post-absorptive condition. However, because of the diversity of nutrition and digestion modes in vertebrates, it is not simple to generalize a standard procedure for BMR measurement. Thus, information in this regard must be experimentally obtained by measuring the heat increment of feeding (HIF). We used a repeated-measures design to test for the effects of HIF on BMR in Phyllotis darwini, a granivorous rodent. Our results suggest that, in this species, feeding induces an elevation in O 2 consumption that can persist up to 4 h after the last meal. In addition, and irrespective of the fasting period, measures made with less than 2 h of fasting yield BMR values that are significantly higher than measurements after longer fasting periods (i.e. 3 and 4 h).

Dynamic thermal balance in the leaf-eared mouse: the interplay among ambient temperature, body size, and behavior.

Endotherms maintain constant body temperature through physiological and behavioral adjustments. Behavioral thermoregulation is an important factor influencing energy balance. We exposed the leaf-eared mouse, Phyllotis darwini, to temperatures corresponding to its natural thermal range and studied two forms of behavioral thermoregulation: diminishing surface to volume ratio by huddling and heat dissipation by increasing physical contact with the substrate (flattening). We predicted that at low ambient temperatures (T(a)) huddling would be used as a heat conservation mechanism and at high T(a) flattening would be used for heat loss. We simultaneously measured oxygen consumption (VO2) and flattening, in response to three independent factors: huddling, T(a), and body mass. Each experiment was a 6-h VO2 trial where five virgin females were measured at constant T(a). We performed this protocol for two body mass groups, small (ca. 40 g) and large (ca. 70 g), in a metabolic chamber. Treatments were groups with and without the ability to huddle at five different T(a), ranging from 5 degrees to 35 degrees C. A significant interaction between all three factors was found. Huddling and flattening were used as strategies for conserving or dissipating heat, respectively, and the shift between both strategies occurred at the lower limit of thermoneutrality. At T(a) below thermoneutrality, huddling was a more effective way of reducing metabolic requirements and was more efficient (H(E)) in small individuals than large individuals. So, by huddling, small individuals save more energy. At high T(a), flattening appeared to be an equally useful mechanism for heat loss, for both large and small animals.

Population-Level Consequences of Antipredator Behavior: A Metaphysiological Model Based on the Functional Ecology of the Leaf-Eared Mouse

We present a predator–prey metaphysiological model, based on the available behavioral and physiological information of the sigmodontine rodent Phyllotis darwini. The model is focused on the population-level consequences of the antipredator behavior, performed by the rodent population, which is assumed to be an inducible response of predation avoidance. The decrease in vulnerability is explicitly considered to have two associated costs: a decreasing foraging success and an increasing metabolic loss. The model analysis was carried out on a reduced form of the system by means of numerical and analytical tools. We evaluated the stability properties of equilibrium points in the phase plane, and carried out bifurcation analyses of rodent equilibrium density under varying conditions of three relevant parameters. The bifurcation parameters chosen represent predator avoidance effectiveness (A), foraging cost of antipredator behavior (C1′), and activity-metabolism cost (C4′). Our analysis suggests that the trade-offs involved in antipredator behavior plays a fundamental role in the stability properties of the system. Under conditions of high foraging cost, stability decreases as antipredator effectiveness increases. Under the complementary scenario (not considering the highest foraging costs), the equilibria are either stable when both costs are low, or unstable when both costs are higher, independent of antipredator effectiveness. No evidence of stabilizing effects of antipredator behavior was found.

Food web structure and climate effects on the dynamics of small mammals and owls in semi‐arid Chile

Population dynamics of small mammals and predators in semi‐arid Chile is positively correlated with rainfall associated with incursions of El Niño (El Niño Southern Oscillation: ENSO). However, the causal relationships between small mammal fluctuations, predator oscillations, and climatic disturbances are poorly understood. Here, we report time series models for three species of small mammal prey and two species of owl predators. The large differences in population fluctuations between the three small mammal species are related to differences in their respective feedback structures. The analyses reveal that per capita growth rate of the leaf‐eared mouse is a decreasing function of log density and of log barn owl abundance together with a positive rainfall effect. In turn, per capita population growth rate (R‐function) of the barn owl is a negative function of log barn owl abundance and a positive function of leaf‐eared mouse abundance, suggesting a predator–prey interaction. The dramatic population fluctuations exhibited by leaf‐eared mouse (Phyllotis darwini) are caused by climate effects coupled with a complex food web architecture.

Demographic dynamics of a neotropical small rodent (Phyllotis darwini): feedback structure, predation and climatic factors

Summary The leaf‐eared mouse (Phyllotis darwini) exhibits large numerical fluctuations associated with high‐ and low‐rainfall years in semi‐arid Chile. Using capture–mark–recapture (CMR) statistical modelling, we provide a detailed description of the demographic variation in this species. We studied between‐year and seasonal variation of demography, and tested for the relative importance of endogenous and exogenous factors as covariates of survival, recruitment, maturation and reproduction over a 12‐year period. The demographic variables studied show larger between‐year than within‐year (seasonal) variation, emphasizing the importance of this source of external variability. We found that both feedback structure and exogenous factors operate together on different demographic processes of this species. We found positive direct feedback effects on survival rate and negative feedback on recruitment, fraction of reproductive individuals and female maturation rates. The ratio between barn and magellanic horned owls showed an important effect on most of the demographic variables of leaf‐eared mice, in particular by influencing negatively survival rates and the fraction of reproductive individuals, thus suggesting the importance of non‐lethal predation. Hence, feedback intrinsic mechanisms (density‐dependence), owls and climate (rainfall and Southern Oscillation Index (SOI)) operate simultaneously in determining the demography of leaf‐eared mice. We hypothesize that trophic interactions with owls (and perhaps other predators) may cause second‐order feedback responses in demography and population dynamics of this small rodent species.

Results of a food addition experiment in a north‐central Chile small mammal assemblage: evidence for the role of “bottom‐up” factors

Since 1989, effects of biotic interactions including predation and herbivory have been examined in a replicated experimental study in a north‐central Chilean semiarid thorn scrub community. Strong responses of small mammals and plants to El Niño Southern Oscillations (ENSO) have also been documented suggesting that “bottom‐up” factors related to high rainfall are important. To simulate increased primary productivity effects on small mammals, ad lib rabbit pellet additions were initiated in mid‐1997 on unfenced grids near the experimental complex. Following the 1997 El Niño event with three times normal precipitation, numbers of small mammals during pre‐addition months and the first treatment year were similar on control and food addition grids. During the second year (1998–1999), a period of severe drought, food additions had significant positive effects on numbers of two predominantly herbivorous “core” (resident) species, Octodon degus and Phyllotis darwini, and an omnivorous “quasi‐core” (resident but highly fluctuating) species, Akodon olivaceus; however, all three species declined towards the end of the second treatment year. Two “opportunistic” (temporarily resident) species, Abrothrix longipilis (an insectivore) and Oligoryzomys longicaudatus (a granivore), showed no responses to food additions. An insectivorous marsupial, Thylamys elegans (also a “core species”), had significantly lower numbers on food addition grids. Changes in body weight distributions and proportions of reproductive individuals particularly in O. degus indicate in situ responses. Whereas no differences in residency, numbers of stations visited, and trappability were observed, energy compensation ratios greater than one suggest significant immigration in the second year. Thus, food additions elicited strong responses by herbivorous/omnivorous “core” and “quasi‐core species” whereas they had no effects on “opportunistic species”. These results reinforce the view that “bottom‐up” factors influencing food availability exert prevailing control on numerically important small mammal species by temporarily increasing carrying capacity, and that “top‐down” factors (i.e., biotic interactions) become important when small mammal numbers are at or near their carrying capacity. Spatial dynamics may be important in explaining declines of species populations exhibiting initially positive responses to food additions.

Patterns of daily activity in the leaf-eared mouse (Phyllotis darwini): effects of food availability

The daily locomotor activity pattern of the nocturnal sigmodontine rodent Phyllotis darwini was analysed when faced with a differential offer of food. Animals with restricted food supply were less active during the day compared to animals who had access to food ad libitum, but no differences in activity were observed during the night. Minimization of energy expenditure may account for this behavioural plasticity, and such flexibility is extremely important in the unpredictable and low productive environments inhabited by P. darwini.

Digestive plasticity and the cost of acclimation to dietary chemistry in the omnivorous leaf-eared mouse Phyllotis darwini

We examined the costs associated with acclimation in an omnivorous mouse (Phyllotis darwini) fed two contrasting diets (carbohydrate-rich and protein-rich). We studied the response of gut morphology and digestive performance in animals shifted to a novel diet at different developmental stages. When acclimated adult animals were shifted to the alternative diet, energy digestibility decreased. We also found long-term consequences to diet acclimation. Animals reacclimated for 15 days to an alternative diet did not increase digestive performance. Although no effects of diet on gut morphology were noted, a significant positive correlation between energy digestibility and small intestinal length was found, explaining most of the variability observed in energy digestibility. These results suggest that caution should be used when defining adaptive changes if the possible cost of acclimation is neglected.

The Interplay of Biotic and Abiotic Factors in a Semiarid Chilean Mammal Assemblage: Results of a Long-Term Experiment

Since early 1989, we have conducted a large-scale ecological manipulation in a semiarid thorn scrub community in north-central Chile. We have excluded vertebrate predators (raptors and mammalian carnivores), and larger small mammal herbivores/ competitors (i.e., degus, Octodon degus) from replicated 0.56-ha plots, and monitored small mammal population and plant responses over more than ten years. Repeated tneasures ANOVAs on minimum number known alive (MNKA) estimates of small mammals for a six-year period (1990-1996) spanning an El Nino event in 1991-1992 showed strong responses of some species to predator exclusions (e.g., O. degus; Darwin's leaf-eared mouse, Phyllotis darwini; the chinchilla-rat, Abrocoma bennetti). However, responses varied in time with significant effects during pre-El Nino (1990-1992) and El Nino (1992-1994) periods (i.e., O. degus), or pre-El Nino and post-El Nino (1994-1996) periods (P. darwini, A. bennetti). Other species showed no responses to predator exclusions (e.g., olivaceous field mouse, Akodon olivaceus; long-haired field mouse, Abrothrix longipilis; long-tailed rice rat. Oligoryzomys longi-caudatus). Some effects of competitor (degu) exclusions were detected (e.g., A. bennetti during the El Nino and post-El Nino periods; O. longicaudatus during the El Nino). Top-down' factors (i.e., biotic interactions) appear to have greater effects on core species (i.e., P. darwini, O. degus) which persist in the thorn scrub. Other species (e.g., A. longipilis, O. longicaudatus) are transitory residents or opportunistic with lesser effects of biotic interactions, and their populations may be controlled by source-sink dynamics. All species had strong responses to the 1991-1992 El Nino indicating primary control by bottom-up factors.

Survival, Recruitment and Immigration Processes in Four Subpopulations of the Leaf-Eared Mouse in Semiarid Chile

The leaf-eared mouse (Phyllotis darwini) undergoes periodical population irruptions in semiarid Chile associated with unusual rainfall driven by ENSO (El Nino/Southern Oscillation) disturbances. In this study, we estimated survival, immigration, and recruitment between contiguous subpopulations in opposite-facing slopes of two creeks by means of probabilistic models. Population trajectories were similar in all four subpopulations. However, xeric-habitat subpopulations were larger than mesic-habitat subpopulations in the two creeks studied. On the other hand, survival showed strong temporal effects, but no habitat-type or life-stage effects. The most parsimonious models were those that included seasonal effects on survival rate. Numbers of births and immigrants were correlated with total population changes in both subpopulations of El Cobre creek, but the two subpopulations at El Grillo creek showed juvenile and adult mortality plus emigration as the most important processes contributing to population change. Our study demonstrates spatiotemporal variability in population processes (survival, birth, immigration, and recruitment) between neighboring subpopulations.

Test of the adaptive modulation hypothesis in rodents: dietary flexibility and enzyme plasticity

The phenotypic response of digestive enzymes was assessed in two species of rodents with different foods habits. Species were Phyllotis darwini (omnivorous) and Octodon degus (herbivorous). The activity of sucrase, maltase and aminopeptidase-N were determined in vitro in animals feeding two contrasting diets. No effect of dietary chemistry on sucrase and maltase activities was observed. Nevertheless, aminopeptidase-N showed a reversible response to diet in P. darwini but not in O. degus. Through Principal Component Analysis we separated the specific and non-specific modulation of the enzymes. The analysis showed that aminopeptidase-N activity is up-regulated by dietary protein in P. darwini. Differences in the phenotypic response of this species apparently reflect the historic levels of specific substrates of the natural diets for this enzyme, linking dietary flexibility and digestive plasticity in an evolutionary context.

El Niño-Southern Oscillation-Driven Rainfall Variability and Delayed Density Dependence Cause Rodent Outbreaks in Western South America: Linking Demography and Population Dynamics.

It is well known that some rodent populations display dramatic density fluctuations in semiarid regions of western South America after the unusual rainfall levels associated with El Niño-southern oscillation (ENSO) disturbances. These correlated phenomena have led some ecologists to believe that rodent outbreaks are determined solely by density-independent factors (e.g., rainfall regime). However, demographic studies have detected strong delayed density-dependent effects in one of the most irruptive rodent species, the leaf-eared mouse Phyllotis darwini. We tested the effects of rainfall and delayed density-dependent factors by constructing a structured model based on demographic data estimated from a capture-mark-recapture study of this species in Chile. A model including both rainfall and delayed density-dependent effects predicts the observed population dynamics rather accurately over a 10-yr period. Interestingly, small changes in model parameters result in large changes in model dynamics, which strongly suggests that local variations in demographic features are important in explaining the asynchronous pattern in outbreak occurrences. These findings suggest that inextricably intertwined endogenous and exogenous forces cause rodent outbreaks in western South America. The former are characterized by delayed nonlinear feedbacks, whereas the latter are characterized by the positive effects of the El Niño phases and the negative effects of the La Niña phases of the ENSO disturbance.

Population rate of change in the leaf‐eared mouse: The role of density‐dependence, seasonality and rainfall

We analysed statistically the influence of density‐dependent regulation, seasonality and precipitation on the realized population rate of change of the Neotropical rodent Phyllotis darwini (Waterhouse 1837) at an intra‐annual time scale. We used four years of continuous live trapping at a semiarid locality of north central Chile. Results showed that density‐dependence, seasonal effects and precipitation were important factors influencing population growth rates in this species. An empirical population model including a sine function for seasonal effects, a linear form for density‐dependence, and precipitation was fitted to the full data set and to the data set with the first year removed (after an outbreak). The empirical model explained 33% and 48% of the variance in population growth. The natural rate of population increase, estimated from the empirical model, was rmax = 2.51 or 5.06 years−1. These estimates indicate a great potential for population increase and may explain the capability of this species to undergo large irruptions. We propose that merging empirical and theoretical modelling with field research is the most promising avenue to understand the outbreaks experienced by some rodent species in western South America.

Population dynamics of three Neotropical small mammals: Time series models and the role of delayed density‐dependence in population irruptions

It is widely believed that only precipitation levels (through increased primary production) determine irruptions of small mammals in semi‐arid areas of western South America. Nevertheless, density‐dependent factors may also drive population fluctuations. To test statistically these putative effects we analysed 11 years of population records on three sympatric species of small mammals at two different habitat types in north central Chile. We applied the classical diagnostic tools of time series analysis (the autocorrelation function: ACF) to the observed time series of three neotropical small mammals. We also used simple linear autoregressive time series models to reconstruct the endogenous dynamics of these populations. The analysis strongly suggests that population fluctuations of the three species have an important density‐dependent component, with the most irruptive species (Phyllotis darwini, Waterhouse 1837) displaying stronger second order population feedbacks than the other two (Akodon olivaceus, Waterhouse 1837 and Thylamys elegans, Waterhouse 1839). The latter two species showed direct density‐dependent feedbacks. We hypothesize that the frequent population outbreaks of P. darwini (and perhaps of other species) in semi‐arid regions of western South America, may be the result of population‐level (direct density‐ dependence) and community‐level processes (delayed density‐dependence), interacting with exogenous perturbations (rainfall and associated primary production).

Delayed density-dependent and rainfall effects on reproductive parameters of an irruptive rodent in semiarid Chile

We examined the influence of density-dependent and density-independent factors on reproductive processes of leaf-eared mouse Phyllotis darwini (Waterhouse, 1837) in a semiarid region of Chile subjected to El Nino-driven precipitation. This species undergoes periodic irruptions apparently triggered by unusually high precipitation. The effects of density and precipitation were analyzed statistically regarding the following reproductive parameters: fraction of reproductive females, reproductive number (juveniles + reproductive females), per capita reproductive rates, and reproduction index based on long-term data (10 years). The fraction of reproductive females was affected positively by precipitation during the preceding winter and negatively by population density one year before. The reproduction index and the reproductive rate was positively affected by population density the previous year. In addition, the reproductive number was positively correlated with precipitation levels. The P. darwini population studied was affected by delayed density-dependent and density-independent factors in reproductive parameters. We propose that both destabilizing effects on reproductive rates of P. darwini may be major factors underlying the frequent outbreaks of this mouse observed in semiarid regions of Chile.

Population extinction risks of three Neotropical small mammal species.

The population persistence and extinction probabilities of three small mammal species were analyzed by estimating growth and extinction properties obtained from 10 years of live-trapping data at two different habitat types in semiarid Chile. We used a stochastic formulation with an exponential growth model known as a Wiener-drift process, out of which growth and extinction quantities were estimated. The rodent Phyllotis darwini showed the lowest rates of growth, and the lowest infinitesimal variances, whereas the opposite trend was found for the rodent Akodonolivaceus. The marsupial Thylamys elegans showed intermediate values for growth rates and infinitesimal variances. The rodent P. darwini showed the lowest extinction risk in the study site. We also detected spatial differences between mesic and xeric habitats in the growth rates of P. darwini and T. elegans, and in the extinction risks of the three species studied. Although the population growth of these three species can be approximated by purely stochastic processes, the introduction of density dependence through autoregressive log-linear models reduced the extinction times of all species analyzed.