Mauricio Soto-Gamboa

Toward an integrative understanding of social behavior: New models and new opportunities

Social interactions among conspecifics are a fundamental and adaptively significant component of the biology of numerous species. Such interactions give rise to group living as well as many of the complex forms of cooperation and conflict that occur within animal groups. Although previous conceptual models have focused on the ecological causes and fitness consequences of variation in social interactions, recent developments in endocrinology, neuroscience, and molecular genetics offer exciting opportunities to develop more integrated research programs that will facilitate new insights into the physiological causes and consequences of social variation. Here, we propose an integrative framework of social behavior that emphasizes relationships between ultimate-level function and proximate-level mechanism, thereby providing a foundation for exploring the full diversity of factors that underlie variation in social interactions, and ultimately sociality. In addition to identifying new model systems for the study of human psychopathologies, this framework provides a mechanistic basis for predicting how social behavior will change in response to environmental variation. We argue that the study of non-model organisms is essential for implementing this integrative model of social behavior because such species can be studied simultaneously in the lab and field, thereby allowing integration of rigorously controlled experimental manipulations with detailed observations of the ecological contexts in which interactions among conspecifics occur.

Social cues and hormone levels in male Octodon degus (Rodentia): a field test of the Challenge Hypothesis.

Social interactions are important factors determining and regulating individual behaviors. Testosterone has been related to agonistic interactions, while glucocorticoids have been related to social stress, especially during interactions of dominance. We compared testosterone and cortisol concentrations in male degus (Octodon degus, Rodentia) under laboratory conditions without male social interactions, with data from wild males in nature. Under natural conditions, males should present higher levels of testosterone during the breeding season due to social interactions (Challenge Hypothesis). Alternatively, intense social instability could act as a stressing environment, raising glucocorticoids, which inhibit testosterone concentrations. Our results show a significant increase in agonistic interactions between males during the breeding season, and disappearance of non-agonistic male interactions during this period. Hormone levels in breeding season show nonsignificant differences between laboratory groups, but testosterone concentrations in field males were significantly higher than in laboratory males. Testosterone levels were similar among pre-breeding and breeding periods, but in field animals the concentration was approximately 30% higher than in laboratory degus. In field animals, we found two different mating strategies: resident males, with territorial behavior, and transient males, displayed an opportunistic approach to females. Finally, cortisol presents a similar pattern in both laboratory and field animals; pre-breeding values of cortisol are higher than during the breeding season. This suggests that social interactions in O. degus activate a rise in testosterone, supporting the Challenge Hypothesis, and could be considered as partial support of the Social Stress Hypothesis.

Sociality, glucocorticoids and direct fitness in the communally rearing rodent, Octodon degus

While ecological causes of sociality (or group living) have been identified, proximate mechanisms remain less clear. Recently, close connections between sociality, glucocorticoid hormones (cort) and fitness have been hypothesized. In particular, cort levels would reflect a balance between fitness benefits and costs of group living, and therefore baseline cort levels would vary with sociality in a way opposite to the covariation between sociality and fitness. However, since reproductive effort may become a major determinant of stress responses (i.e., the cort-adaptation hypothesis), cort levels might also be expected to vary with sociality in a way similar to the covariation between sociality and fitness. We tested these expectations during three years in a natural population of the communally rearing degu, Octodon degus. During each year we quantified group membership, measured fecal cortisol metabolites (a proxy of baseline cort levels under natural conditions), and estimated direct fitness. We recorded that direct fitness decreases with group size in these animals. Secondly, neither group size nor the number of females (two proxies of sociality) influenced mean (or coefficient of variation, CV) baseline cortisol levels of adult females. In contrast, cortisol increased with per capita number of offspring produced and offspring surviving to breeding age during two out of three years examined. Together, our results imply that variation in glucocorticoid hormones is more linked to reproductive challenge than to the costs of group living. Most generally, our study provided independent support to the cort-adaptation hypothesis, according to which reproductive effort is a major determinant, yet temporally variable, influence on cort-fitness covariation.

Fecal cortisol levels predict breeding but not survival of females in the short-lived rodent, Octodon degus

The cort-adaptation hypothesis indicates that an association between glucocorticoid (cort) levels and fitness may vary with the extent to which reproduction or breeding effort is a major determinant of cort levels. Support for a context dependent association between cort and fitness comes mostly from relatively long-lived, bird species. We tested the hypothesis that there are gender and context (life-history) specific cort-fitness relationships in degus, a short-lived and generally semelparous social rodent. In particular, we used demographical records on a natural population to estimate adult survival through seasons and years and linked that to records of baseline cort (based on fecal cortisol metabolites). We found no evidence for a direct relationship between baseline cort and adult survival across seasons, and this lack of association was recorded irrespective of sex and life history stage. Yet, cort levels during early lactation predicted the probability that females produce a second litter during the same breeding season, supporting a connection between baseline cort levels and breeding effort. Overall, the differential effects of cort on survival and breeding supported that the extent of cort-fitness relationships depends on the fitness component examined.

Validation of a radioimmunoassay for measuring fecal cortisol metabolites in the hystricomorph rodent, Octodon degus.

Determination of fecal steroid metabolites is a noninvasive technique that characterizes the physiological state of organisms without the physiological and psychological stress of handling. Although this technique has many applications in the study of wildlife and/or captive animals without the necessity of capturing individuals, it requires a species-specific validation before use. A complete validation includes an analytical and a physiological one. In the latter changes in fecal hormone metabolites are induced by previous manipulations of the respective plasma hormones. Here we validated a method for measuring fecal cortisol metabolites (FCM) in the hystricomorph rodent Octodon degus. We extracted feces with 80% ethanol and quantified steroids using a commercial available cortisol radioimmunoassay. We first compared baseline levels of blood cortisol and FCM, and then performed a challenge test with adrenocorticotropic hormone (ACTH) to demonstrate that FCM accurately reflect adrenocortical activity. We found a significantly positive relationship between concentrations of blood cortisol and its fecal metabolites. During the ACTH challenge test, blood cortisol levels peaked 30 min after injection, and FCM mirrored this peak with a delay of about 6 hr. Our successfully validated noninvasive method provides new opportunities for studies assessing the influence of social and ecological factors on degus under natural conditions.

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.

Towards an integrative model of sociality in caviomorph rodents

Abstract In the late 1990s and early 2000s it was recognized that behavioral ecologists needed to study the sociality of caviomorph rodents (New World hystricognaths) before generalizations about rodent sociality could be made. Researchers identified specific problems facing individuals interested in caviomorph sociality, including a lack of information on the proximate mechanisms of sociality, role of social environment in development, and geographical or intraspecific variation in social systems. Since then researchers have described the social systems of many previously understudied species, including some with broad geographical ranges. Researchers have done a good job of determining the role of social environments in development and identifying the costs and benefits of social living. However, relatively little is known about the proximate mechanisms of social behavior and fitness consequences, limiting progress toward the development of integrative (evolutionary-mechanistic) models for sociality. To develop integrative models behavioral ecologists studying caviomorph rodents must generate information on the fitness consequences of different types of social organization, brain mechanisms, and endocrine substrates of sociality. We review our current understanding and future directions for research in these conceptual areas. A greater understanding of disease ecology, particularly in species carrying Old World parasites, is needed before we can identify potential links between social phenotypes, mechanism, and fitness.

Foxes, people and hens: Human dimensions of a conflict in a rural area of southern Chile

Los conflictos entre humanos y carnivoros han sido reconocidos como una de las mayores amenazas para la conservacion de carnivoros. Cuando existe ganado menor o aves domesticas disponibles, es esperable que pequenos carnivoros depreden sobre estas. Centinela -un area rural localizada en el sur de Chile y donde coexisten zorros chilla {Lycalopex griseus Gray) y pequenos agricultores- fue escogida como area de estudio. Para entender los posibles conflictos entre agricultores y zorros, evaluamos los conocimientos locales, experiencias, y actitudes hacia este zorro, asi como el manejo de los animales domesticos usando una encuesta. Casi un tercio de los encuestados reportaron la perdida de aves domesticas en el ultimo ano como consecuencia de la depredacion por parte de chillas. Estudios simultaneos de la dieta de chillas mostraron resultados coincidentes con esas denuncias. La mayoria de los participantes del estudio (67.4 %) manifesto actitudes negativas hacia la chilla. Las perdidas de aves parecieran estar relacionadas con su manejo, debido a que ningun agricultor reporto perdidas cuando las gallinas se encontraban encerradas en gallineros. Esto sugiere que el encierro permanente de las aves podria ser un metodo efectivo de prevencion de las perdidas. Las actitudes negativas se reflejaron tambien en el hecho de que la mayor parte de los encuestados reporto haber eliminado zorros chillas en al menos una ocasion.

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.

Cell size and basal metabolic rate in hummingbirds

La teoria nucleotipica sugiere que el tamano del genoma juega un rol indirecto en la adecuacion biologica, a traves de las variables con las que se relaciona. En endotermos esta teoria ha sido demostrada por la relacion inversa entre la tasa metabolica basal y el tamano del genoma. La acumulacion de variables, en grupos claves de endotermos, relacionadas con esta problematica (e.g., tamano celular) son ideales para poner a prueba esta teoria. En este sentido, los picaflores son de particular interes ya que son el extremo energetico dentro de los endotermos. Sabiendo que el tamano celular es proporcional al tamano del genoma, en este trabajo ponemos a prueba la relacion del volumen corpuscular medio y la tasa metabolica basal, e indirectamente el tamano del genoma, en cuatro especies de picaflores con masas corporales que van desde 4 a 20 g. Los datos de metabolismo mostraron estar dentro de los mayores descritos para aves, asimismo, los tamanos de los eritrocitos fueron los mas pequenos dentro de los valores reportados en la literatura, apoyando asi lo propuesto por la teoria nucleotipica