Seasonal variation of temporal niche in wild owl monkeys (Aotus azarai azarai) of the Argentinean Chaco: a matter of masking?

Among the more than 40 genera of anthropoid primates (monkeys, apes, and humans), only the South American owl monkeys, genus Aotus, are nocturnal. However, the southernmostly distributed species, Aotus azarai azarai, of the Gran Chaco may show considerable amounts of its 24-h activity during bright daylight. Due to seasonal changes in the duration of photophase and climatic parameters in their subtropical habitat, the timing and pattern of their daily activity are expected to show significant seasonal variation. By quantitative long-term activity recordings with Actiwatch AW4 accelerometer data logger devices of 10 wild owl monkeys inhabiting a gallery forest in Formosa, Argentina, the authors analyzed the seasonal variation in the temporal niche and activity pattern resulting from entrainment and masking of the circadian activity rhythm by seasonally and diurnally varying environmental factors. The owl monkeys always displayed a distinct bimodal activity pattern, with prominent activity bouts and peaks during dusk and dawn. Their activity rhythm showed distinct lunar and seasonal variations in the timing and daily pattern. During the summer, the monkeys showed predominantly crepuscular/nocturnal behavior, and a crepuscular/cathemeral activity pattern with similar diurnal and nocturnal activity levels during the cold winter months. The peak times of the evening and morning activity bouts were more closely related to the times of sunset and sunrise, respectively, than activity-onset and -offset. Obviously, they were better circadian markers for the phase position of the entrained activity rhythm than activity-onset and -offset, which were subject to more masking effects of environmental and/or internal factors. Total daily activity was lowest during the two coldest lunar months, and almost twice as high during the warmest months. Nighttime (21:00-06:00 h) and daytime (09:00-18:00 h) activity varied significantly across the year, but in an opposite manner. Highest nighttime activity occurred in summer and maximal daytime activity during the cold winter months. Dusk and dawn activity, which together accounted for 43% of the total daily activity, barely changed. The monkeys tended to terminate their nightly activity period earlier on warm and rainy days, whereas the daily amount of activity showed no significant correlation either with temperature or precipitation. These data are consistent with the dual-oscillator hypothesis of circadian regulation. They suggest the seasonal variations of the timing and pattern of daily activity in wild owl monkeys of the Argentinean Chaco result from a specific interplay of light entrainment of circadian rhythmicity and strong masking effects of various endogenous and environmental factors. Since the phase position of the monkeys' evening and morning activity peaks did not vary considerably over the year, the seasonal change from a crepuscular/nocturnal activity pattern in summer to a more crepuscular/cathemeral one in winter does not depend on a corresponding phase shift of the entrained circadian rhythm, but mainly on masking effects. Thermoregulatory and energetic demands and constraints seem to play a crucial role.     

Do Forest Composition and Fruit Availability Predict Demographic Differences Among Groups of Territorial Owl Monkeys (Aotus azarai)?

Small-scale ecological variables, such as forest structure and resource availability, may affect primate groups at the scale of group home ranges, thereby influencing group demography and life-history traits. We evaluated the complete territories of 4 groups of owl monkeys (Aotus azarai), measuring and identifying all trees and lianas with a diameter at breast height ≥10 cm (n = 7485). We aimed to determine all food sources available to each of those groups and to relate food availability to group demographics. For analyses, we considered the core areas of the home range separately from the 80% home range. Our results showed that groups occupy territories that differ in size, species evenness, stem density, and food species’ stem abundances. The territories differed in the availability of fruits, flowers, and leaves, and most fruit sources were unevenly distributed in space. Differences among territories were more pronounced for the whole range than they were for the core areas. Despite marked differences among territories in structure and food availability, the number of births and age at natal dispersal were quite similar, but 1 group had a consistently lower group size. Our results suggest that owl monkey groups occupy territories of different structure and composition and food availability, yet ones that contain similar quantities of, mostly, dry season fruit sources. We propose that groups inhabit these territories to overcome food shortages safely during limiting periods, specifically the dry season, in this markedly seasonal forest. The occupancy and defense of territories with strict boundaries may therefore be associated with food resources available during limiting seasons that may be the ones influencing life history patterns and demographics.     

Prolactin Receptor Gene Diversity in Azara’s Owl Monkeys (Aotus azarai) and Humans (Homo sapiens) Suggests a Non-Neutral Evolutionary History among Primates

Although paternal care is rare in mammals, males of several primate taxa exhibit high degrees of this behavior. Studies a number of vertebrate species found a positive correlation between prolactin (PRL) levels and paternal care. Studies of maternal care in knockout mice also indicate that the prolactin receptor (PRLR) plays a critical role in the neural regulation of parental care. To better understand the extent of PRLR genetic variation within primates, we characterized intraspecific coding variation in Azara’s owl monkeys (Aotus azarai) from northern Argentina, a species with intensive paternal care. We then examined PRLR variation in 1088 humans (Homo sapiens) from the 1000 Genomes Project. Lastly, we assessed interspecific variation in PRLR in 4 different Aotus spp. and 12 phylogenetically (and behaviorally) disparate primate taxa. Our analyses revealed that the coding region of PRLR exhibits significant variation in all species of primates, with nonsynonymous amino acid substitutions being enriched in the intracellular domain, a region responsible for activation of downstream targets in the PRL pathway. In addition, several species exhibit entire codon deletions in this region. These results suggest a non-neutral evolutionary history of the PRLR locus within different primate lineages, and further imply that the translated PRLR protein has undergone considerable change throughout primate evolution. Such changes may be driven by selection for different behaviors and physiologies resulting from modulations of the pleiotropic prolactin pathway. Yet, the genetic variants in PRLR among primate taxa do not discretely cluster with species-level differences in paternal care behaviors. These observations imply that other mechanisms must be involved in the regulation of paternal care in primates.     

Alien Invasive Slider Turtle in Unpredicted Habitat: A Matter of Niche Shift or of Predictors Studied?

Background

Species Distribution Models (SDMs) aim on the characterization of a species'' ecological niche and project it into geographic space. The result is a map of the species'' potential distribution, which is, for instance, helpful to predict the capability of alien invasive species. With regard to alien invasive species, recently several authors observed a mismatch between potential distributions of native and invasive ranges derived from SDMs and, as an explanation, ecological niche shift during biological invasion has been suggested. We studied the physiologically well known Slider turtle from North America which today is widely distributed over the globe and address the issue of ecological niche shift versus choice of ecological predictors used for model building, i.e., by deriving SDMs using multiple sets of climatic predictor.

Principal Findings

In one SDM, predictors were used aiming to mirror the physiological limits of the Slider turtle. It was compared to numerous other models based on various sets of ecological predictors or predictors aiming at comprehensiveness. The SDM focusing on the study species'' physiological limits depicts the target species'' worldwide potential distribution better than any of the other approaches.

Conclusion

These results suggest that a natural history-driven understanding is crucial in developing statistical models of ecological niches (as SDMs) while “comprehensive” or “standard” sets of ecological predictors may be of limited use.     

Does Temporal Variation in Predation Risk Influence the Intensity of Antipredator Responses? A Test of the Risk Allocation Hypothesis

Temporal variation in predation risk may fundamentally influence antipredator responses of prey animals. To maximize lifetime fitness, prey must be able to optimize energy gain and minimize predation risk, and responses to current levels of risk may be influenced by background levels of risk. A ‘risk allocation’ model has recently been proposed to predict the intensity of antipredator responses that should occur as predation risk varies over time. Prey animals from high‐risk environments should respond to predators with relatively low intensities of antipredator behaviour because long periods of antipredator behaviour may result in unacceptable decreases in levels of foraging activity. Moreover, animals that are under frequent risk should devote more energy to foraging during brief pulses of safety compared with animals under infrequent attack. In this study, we experimentally tested the risk allocation hypothesis. We exposed juvenile rainbow trout, Oncorhynchus mykiss, to three levels of risk (high, moderate and low) crossed with two levels of temporal variation (exposed to risk three times a day and once a day). In accordance with the model, we found that trout exposed to risky situations more frequently responded with significantly less intense antipredator behaviour than trout exposed to risk infrequently. The intensity of response of trout exposed to moderate risk three times a day decreased to levels similar to situations of no risk. However, in contrast to the second prediction of the model, animals under frequent risk were not more active during periods of safety compared with animals under infrequent risk. Although behaviour in the face of predation risk was dependent on the broader temporal context in which risk varied, the specific predictions of the risk allocation model were only partly supported.     

School’s Out: Seasonal Variation in the Movement Patterns of School Children

School children are core groups in the transmission of many common infectious diseases, and are likely to play a key role in the spatial dispersal of disease across multiple scales. However, there is currently little detailed information about the spatial movements of this epidemiologically important age group. To address this knowledge gap, we collaborated with eight secondary schools to conduct a survey of movement patterns of school pupils in primary and secondary schools in the United Kingdom. We found evidence of a significant change in behaviour between term time and holidays, with term time weekdays characterised by predominately local movements, and holidays seeing much broader variation in travel patterns. Studies that use mathematical models to examine epidemic transmission and control often use adult commuting data as a proxy for population movements. We show that while these data share some features with the movement patterns reported by school children, there are some crucial differences between the movements of children and adult commuters during both term-time and holidays.     

Seasonal Variation in Occurrence of Pulmonary Embolism: Analysis of the Database of the Emilia‐Romagna Region,Italy

Seasonal variation in the occurrence of cardiovascular and cerebrovascular events, including pulmonary embolism (PE), has been reported; however, recent large‐scale, population‐based studies conducted in the United States did not confirm such seasonality. The aim of this large‐scale population study was to determine whether a temporal pattern in the occurrence of PE exists. The analysis considered all consecutive cases of PE in the database of all hospital admissions of the Emilia Romagna region in Italy at the Center for Health Statistics between January 1998 and December 2005. PE cases were first grouped according to season of occurrence, and the data were analyzed by the χ² test for goodness of fit. Then, inferential chronobiologic (cosinor and partial Fourier) analysis was applied to monthly data, and the best‐fitting curve for the annual variation was derived. The total sample consisted of 19,245 patients (8,143 male, mean age 71.6±14.1 yrs; 11,102 female, mean age 76.1±13.7 yrs). Of these, 2,484 were <65 yrs, 5,443 were between 65 and 74, and 11,318 were ≥75 yrs. There were 4,486 (23.3%) fatal‐case outcomes. PE occurred least frequently in spring (n=4,442 or 23.1%) and most frequent in winter (n=5,236 or 27.2%, goodness of fit χ²=75.75, p<0.001). Similar results were obtained for subgroups formed by gender, age, fatal/non‐fatal outcome, presence/absence of major underlying co‐morbid conditions, and specific risk factors. Inferential chronobiological analysis identified a significant annual pattern in PE, with the peak between November and December for the total sample of cases (p<0.001), males (p<0.001), females (p=0.002), fatal and non‐fatal cases (p<0.001 for both), and subgroups formed by age (<65 yrs, p=0.012; 65–74 yrs, p<0.001; ≥75 yrs, p=0.012). This pattern was independent of the presence/absence of hypertension (p=0.003 and p<0.001, respectively), pulmonary disease (p<0.001 and p<0.001, respectively), stroke (p<0.001 and p=0.004, respectively), neoplasms (p=0.005 and p=0.001, respectively), heart failure (p=0.022 and p<0.001, respectively), and deep vein thrombosis (p=0.002 and p<0.001, respectively). However, only a non‐statistically significant trend was found for subgroups formed by cases of diabetes mellitus, infections, renal failure, and trauma.     

Do Monkeys Avoid Areas of Home Range Overlap Because They Are Dangerous? A Test of the Risk Hypothesis in White-Faced Capuchin Monkeys (Cebus capucinus)

International Journal of Primatology - In social animals, areas where the home ranges of neighboring groups overlap are often underused. The Risk Hypothesis posits that the costs of intergroup...     

A Taxonomic Signature of Obesity in the Microbiome? Getting to the Guts of the Matter

Obesity is an important and intractable public health problem. In addition to the well-known risk factors of behavior, diet, and genetics, gut microbial communities were recently identified as another possible source of risk and a potential therapeutic target. However, human and animal-model studies have yielded conflicting results about the precise nature of associations between microbiome composition and obesity. In this paper, we use publicly available data from the Human Microbiome Project (HMP) and MetaHIT, both surveys of healthy adults that include obese individuals, plus two smaller studies that specifically examined lean versus obese adults. We find that inter-study variability in the taxonomic composition of stool microbiomes far exceeds differences between lean and obese individuals within studies. Our analyses further reveal a high degree of variability in stool microbiome composition and diversity across individuals. While we confirm the previously published small, but statistically significant, differences in phylum-level taxonomic composition between lean and obese individuals in several cohorts, we find no association between BMI and taxonomic composition of stool microbiomes in the larger HMP and MetaHIT datasets. We explore a range of different statistical techniques and show that this result is robust to the choice of methodology. Differences between studies are likely due to a combination of technical and clinical factors. We conclude that there is no simple taxonomic signature of obesity in the microbiota of the human gut.     

Seasonal changes in the physiology of male Virginia opossums (Didelphis virginiana): signs of the Dasyurid semelparity syndrome?

Semelparity, which is multiplying once in a lifetime, is a rare reproductive strategy among mammals. Several species of the marsupial family Dasyuridae experience 100% male mortality following an intense mating period. We investigated seasonal physiological changes that may be associated with early mortality in the male Virginia opossum (Didelphis virginiana; Didelphidae) and compared these changes with those of semelparous, male dasyurids. Free-ranging male Virginia opossums (n=36) were collected during 2001 at the Oklahoma State University Cross Timbers Experimental Range. Seasonal data were collected on hematological, morphological, and helminth parameters of these individuals. We used one-way ANOVA to determine whether there were seasonal differences among means for each parameter. It appeared that male Virginia opossums experienced some physiological changes similar to those of male dasyurids exhibiting semelparity. All males collected in summer (August) were juveniles of the year. Lack of adult males in August suggests high mortality of this cohort during the breeding season. Opossum characteristics exhibiting the dasyurid semelparity syndrome included packed cell volume, adrenal mass, and helminth numbers. Minor lymphocytopenia, neutrophilia, and testosterone concentrations also were similar to semelparous dasyurids. However, a lack of change in serum cortisol concentration and body mass and dynamics in immunoglobulin protein, serum protein, and testes mass were not consistent with previous reports of semelparous dasyurid physiology. Evolutionary divergence and differences in breeding behavior between dasyurids and didelphids may be responsible for the lack of consistency between the taxa.     

Spatial–Temporal Variation in Orchid Bee Communities (Hymenoptera: Apidae) in Remnants of Arboreal Caatinga in the Chapada Diamantina Region, State of Bahia, Brazil

The spatial and temporal distribution of organisms is a fundamental aspect of biological communities. The present study focused on three remnants of arboreal Caatinga in northeastern Brazil between May, 2009 and April, 2010. A total of 627 euglossine males were captured in traps baited with artificial aromatic compounds. The specimens belonged to 14 species and four genera: Euglossa Latreille, Eulaema Lepeletier, Eufriesea Cockerell, and Exaerete Hoffmannsegg. Eulaema nigrita Lepeletier (41.6), Euglossa carolina Nemésio (15.3%), Eulaema marcii Nemésio (13.6%), and Euglossa melanotricha Moure (12.8%) were the most common species sampled. The distribution of collected specimens per fragment was as follows: Braúna (280?ha)??259 individuals belonging to 14 species; Cambuí (179?ha)??161 individuals from eight species; and Pindoba (100?ha)??207 individuals represented by seven species. Braúna had the highest diversity (H???=?1.91) and estimated species richness. The largest fragment was the main source of the observed variation in species richness and abundance, indicating a non-random pattern of spatial distribution. The analysis of environmental factors indicated that seasonal variation in these factors was the principal determinant of species occurrence and abundance.     

Treefall Gaps and Regeneration Composition in the Laurel Forest of Anaga (Tenerife): a Matter of Size?

The size of treefall gaps is an important determinant of regeneration composition in tropical and temperate forests. Preliminary studies in the laurel forest of Tenerife have shown that small gaps (<100 m²) were the most numerous. However, due to this small size, no significant differences were found between regeneration in gaps and regeneration below the canopy. Because infrequent large gaps (>100 m²) are present in the laurel forest, we analyzed the regeneration in these large uncommon gaps, considering their potentially important role in the dynamics of the system. Our main hypothesis is that large gaps are important disturbance to ensure the regeneration and stablishment of shade intolerant species. Only five gaps larger than 100 m² (ranging from 125–268 m²) were found in the study area. Data from a further 20 small gaps (<100 m²), analysed in a previous study, was also included. Control plots were examined close to the gaps in order to determine regeneration below the closed canopy. We did not find a significant difference between regeneration density in the gaps (<100 m²) and regeneration below the canopy in the control plots. Contrary to our expectations, regeneration was lower in the large gaps than under the canopy. The open canopy in the large gaps increases light intensity, and has a negative effect on the germination and growth of shade-tolerant tree species like Viburnum tinus (although non-statistically significant); however, the increase in light intensity is not sufficient to stimulate the germination of shade-intolerant tree species. The effects of treefall gaps in the dynamics of the laurel forest of Anaga should be not considered as significant in comparison to other factors such as human disturbances or infrequent disturbances (land slides or hurricanes).     

Variation in the Ichnofauna of the Collio Formation (Lower Permian) in the South-Alpine Region (Northern Italy)

In the Collio Formation (Lower Permian) of the South-Apine region (North Italy) paleobiodiversity consists of tetrapod footprints, invertebrate traces and rarer plants, and is characterized by an absolute poverty of taxa that becomes more acute from the lower to the upper part of the Collio Formation. Regionally, the drop in diversity can be explained by joint tectonic and climatic change; humid evergreen environments became mainly dry. Examination of ichnofossil distribution supports this hypothesis.     

Niche Expansion in Bacteria: Can Infectious Gene Exchange Affect the Rate of Evolution?

Recombination occurs by infectious gene transfer in bacteria, at rates much lower than recombination by sexual reproduction in other organisms. Thus, recombination may accelerate evolution in bacteria only under restricted conditions, such as occur when mutations at several loci are required for the evolution of an expanded ecological niche. Mathematical ("chemostat") models of several such cases--evolution of independence from three limiting essential or "interactive-essential" resources; evolution of the ability to use three new substitutable resources; and evolution of resistance to three growth inhibitors--were analyzed by computer simulation. All combinations of three mutation rates (U) and four values for the "infectious gene transfer rate parameter" (chi) were considered. Recombination accelerated evolution most when U was low and chi was high, but was unlikely to have large effects when chi was low enough to be realistic for natural populations of Escherichia coli. Recombination had the largest effects when resources were substitutable, and in that case could have substantially reduced the chance of random loss of the favored "triple mutant" while it was still rare. The simulations also revealed some interesting features of selection for an expanded niche. Evolution of independence from essential resources occurred more rapidly when the resources were weakly complementary than when they did not interact. Selection for the ability to use all substitutable resources was weak after all intermediate types that used only one or two of the resources had arisen.     

Differential Bird Predator Attack Rate on Seasonal Forms of the Map Butterfly (Araschnia levana L.): Does the Substrate Matter?

The European map butterfly (Araschnia levana L.) is a striking example of seasonal plasticity. Individuals of the spring generation are reddish with a fritillary‐like colour pattern, whereas the summer generation is black with a white dorsal stripe. Proximate factors explaining the development of the forms are well known, but ultimate explanations have not been tested experimentally yet. The reddish spring form is assumed to have a warning coloration, as found in other nymphalid butterflies that are unpalatable (Aglais urticae). We tested for differential predation by a visually hunting predator (Parus major) in a laboratory experiment using artificial butterflies designed to represent the spring and summer form. Birds were released individually in a flight cage where the alternative forms were presented. Summer forms were more frequently attacked than spring forms, which may point to some aversion against the reddish spring form. But there was also a strong effect of the interaction between seasonal form and type of substrate. Spring forms were much better protected from attacks on the brown substrate of dead leaves compared to the green substrate of nettle leaves. On the latter substrate, latency times before attacking spring forms were on average 2.5 times longer than for summer forms. Experiments with artificial butterflies simplify complex predator–prey interactions because they exclude potential taste or odour effects and they also exclude behavioural responses and interactions of the butterfly. However, our results based on static visual signals provide a promising first step to test the functional significance of this striking seasonal polyphenism.     

Recruitment Behavior During Foraging in the Neotropical Ant Gnamptogenys moelleri (Formicidae: Ponerinae): Does the Type of Food Matter?

Gnamptogenys moelleri nests in bromeliads and feeds on an array of food items, including dead and live animals, and nectar. Field data in Brazilian forests indicate that G. moelleri hunts solitarily, while retrieving is performed both by solitary workers for small items, or by a group of recruited workers for large items. This flexible foraging strategy was investigated in the laboratory through a series of experiments to assess the context in which recruitment is elicited. Three types of food were used: 50% honey solution, large insect prey, and cluster of small insects. For all food types the first encounter by a scout resulted in increased numbers of ants leaving the nest and finding the food in the arena. After finding liquid food or large prey, the forager returns to the nest and transmits information to nestmates about food location on the substrate. The successful scout repeatedly taps the sting on the ground, and recruited ants collectively retrieve the large insect to the nest. On the other hand, there is no transmission of information to nestmates about the location of small clumped prey, although the returning scout induces nestmates to leave the nest and hunt. Because foraging in G. moelleri is restricted mostly to the nest bromeliad, and small worker size (0.5 cm) precludes capturing large prey solitarily, recruitment behavior widens the spectrum of food items consumed by this ant species. Although recruitment behavior in ponerines has already been reported to vary with the type and size of a food source, this study also shows that the transmission of information about food location depends on the type of food found (large prey or liquid food versus cluster of small prey).