Stress‐induced peak (but not resting) metabolism correlates with mating display intensity in male guppies

Recent empirical and conceptual papers have highlighted the potential for metabolism to act as a proximate mechanism for behavior that could explain animal personality (consistency over time). Under this hypothesis, individuals with consistently high levels of behavioral activity should also have high resting metabolic rate (RMR) as it can reflect capacity to process food and generate energy. We tested for the predicted positive covariance between RMR and three behaviors that differ in energy demands in 30 male guppies, using multivariate mixed models; we repeatedly measured their activity (10 times each), courtship displays (nine times), voracity (10 times), and metabolism (four‐times). Resting metabolic rate (measured overnight in respirometry trials) did not consistently differ among males, whereas initial peak metabolism measured during those same trials (R = 0.42), and all behaviors were repeatable (R = 0.33–0.51). RMR declined over time suggesting habituation to the protocol, whereas peak metabolism did not. Initial peak metabolism was negatively correlated with courtship display intensity, and voracity was positively correlated with activity, but all other among‐individual correlations were not significant. We conclude that RMR does not provide a proximate explanation for consistent individual differences in behavior in male guppies, and therefore the potential for independent evolution of these physiological and behavioral traits seems possible. Finally, we identify peak metabolism as a potential measure of the stress response to confinement, which highlights the value of considering various aspects of metabolic rates recording during respirometry trials.     

Limited mass‐independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis)

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass‐independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long‐term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni‐ and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass‐dependent and mass‐independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co‐varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass‐independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass‐dependent and mass‐independent physiological variation.     

Individual variation in metabolism and thermal tolerance in juvenile qingbo (Spinibarbus sinensis)

Studies of individual variation in the physiological performance of animals and their relationship with metabolism may provide insight into how selection influences diversity in phenotypic traits. Thus, the aims of the present study were to investigate variation in thermal tolerance and its relationship with individual metabolism in juvenile qingbo (Spinibarbus sinensis). To fulfill our goal, we first measured the resting metabolic rate (RMR), maximum metabolic rate (MMR), metabolic scope (MS, MMR–RMR) and excess post-exercise oxygen consumption (EPOC) of 40 fish at 25 °C. We then measured the critical thermal minimum (CT_min), lethal thermal minimum (LT_min), critical thermal maximum (CT_max), and lethal thermal maximum (LT_max) of 20 fish. Both MMR and MS were positively correlated with the metabolic recovery rate (MRR) (p = 0.001), indicating that high aerobic metabolic performance individuals possessed an advantage for the recovery of anaerobic metabolism. However, the negative correlation between EPOC and MRR (p = 0.017) indicated a slow recovery of the metabolism of high anaerobic metabolic capacity individuals. The RMR was positively correlated with CT_min and LT_min, whereas all of the metabolic rate parameters (RMR, MMR, and MS) were negatively correlated with CT_max and LT_max (p < 0.05), indicating that high aerobic metabolic performance individuals have a weakened thermal tolerance. These results suggested that there is a trade-off between aerobic metabolic performance and thermal tolerance.     

Environmental and genetic influences on body mass and resting metabolic rates (RMR) in a natural population of weasel Mustela nivalis

Body mass (BM) and resting metabolic rates (RMR) are two inexorably linked traits strongly related to mammalian life histories. Yet, there have been no studies attempting to estimate heritable variation and covariation of BM and RMR in natural populations. We used a marker‐based approach to construct a pedigree and then the ‘animal model’ to estimate narrow sense heritability (h²) of these traits in a free‐living population of weasels Mustela nivalis—a small carnivore characterised by a wide range of BM and extremely high RMR. The most important factors affecting BM of weasels were sex and habitat type, whereas RMR was significantly affected only by seasonal variation of this trait. All environmental factors had only small effect on estimates of additive genetic variance of both BM and RMR. The amount of additive genetic variance associated with BM and estimates of heritability were high and significant in males (h² = 0.61), but low and not significant in females (h² = 0.32), probably due to small sample size for the latter sex. The results from the two‐trait model revealed significant phenotypic (r_P = 0.62) and genetic correlation (r_A = 0.89) between BM and whole body RMR. The estimate of heritability of whole body RMR (0.54) and BM corrected RMR (0.45) were lower than estimates of heritability for BM. Both phenotypic and genetic correlations between BM corrected RMR and BM had negative signals (r_P = ?0.42 and r_A = ?0.58). Our results indicate that total energy expenditures of individuals can quickly evolve through concerted changes in BM and RMR.     

Predation selects for low resting metabolic rate and consistent individual differences in anti-predator behavior in a beetle

Significant between-individual variation in resting metabolic rate (RMR) of animals is a widespread phenomenon that may have important implications for our understanding of variation in behavior and animal personality. By using wild caught mealworm beetles, Tenebrio molitor, we examined the relationships among survival rate under predator tests, individual response latency time to become immobile under the risk of predation, duration of immobility time, and RMR. Individuals with higher levels of RMR were bold, and bold individuals were found to be more exposed to the risk of bird predation. We found that RMR was positively correlated with the latency of immobility response and negatively correlated with the total duration of immobility. The correlation between behavioral responses suggests a behavioral syndrome in the anti-predator behavior of T. molitor. The results indicate that energy metabolism may be part of a syndrome that involves behavior and life history traits in animals.     

Testing the phenotype‐linked fertility hypothesis in the presence and absence of inbreeding

The phenotype‐linked fertility hypothesis suggests that females can judge male fertility by inspecting male phenotypic traits. This is because male sexually selected traits might correlate with sperm quality if both are sensitive to factors that influence male condition. A recent meta‐analysis found little support for this hypothesis, suggesting little or no shared condition dependence. However, we recently reported that in captive zebra finches (Taeniopygia guttata) inbreeding had detrimental effects both on phenotypic traits and on measures of sperm quality, implying that variation in inbreeding could induce positive covariance between indicator traits and sperm quality. Therefore, we here assess empirically the average strength of correlations between phenotypic traits (courtship rate, beak colour, tarsus length) and measures of sperm quality (proportion of functional sperm, sperm velocity, sperm length) in populations of only outbred individuals and in mixed populations consisting of inbreds (F = 0.25) and outbreds (F = 0). As expected, phenotype sperm‐trait correlations were stronger when the population contained a mix of inbred and outbred individuals. We also found unexpected heterogeneity between our two study populations, with correlations being considerably stronger in a domesticated population than in a recently wild‐derived population. Correlations ranged from essentially zero among outbred‐only wild‐derived birds (mean Fisher's Zr ± SE = 0.03 ± 0.10) to moderately strong among domesticated birds of mixed inbreeding status (Zr ± SE = 0.38 ± 0.08). Our results suggest that, under some conditions, the phenotype‐linked fertility hypothesis might apply.     

Predation promotes survival of beetles with lower resting metabolic rates

The energetic definition of fitness predicts that natural selection will maximize the residual energy available for growth and reproduction suggesting that energy metabolism might be a target of selection. In this experimental study, we investigated whether female and male yellow mealworm beetles, Tenebrio molitor L. (Coleoptera: Tenebrionidae), differ in their hiding behaviour, individual response latency time, and duration of immobility to treatments mimicking an approaching predation threat. We experimentally tested whether consistently repeatable anti‐predatory responses and resting metabolic rates (RMR) correlated with survival rates of individuals exposed to a nocturnal predator, the brown rat, Rattus norvegicus (Berkenhout) (Rodentia: Muridae). Resting metabolic rate was part of a syndrome involving anti‐predator behaviour. Individuals with lower RMR concealed themselves against predators in substrate more successfully than individuals with higher RMR, and hiding was associated with longer periods of immobility. Ultimately, mortality was higher in the high‐RMR beetles compared to the low‐RMR beetles. Our results provide direct evidence of natural selection against mobility, i.e., for reduced RMR in T. molitor beetles.     

Family association between immune parameters and resistance to Aeromonas hydrophila infection in the Indian major carp, Labeo rohita

Seven innate immune parameters were investigated in 64 full-sib families (the offspring of 64 sires and 45 dams) from two year-classes of farmed rohu carp (Labeo rohita). Survival rates were also available from Aeromonas hydrophila infection (aeromoniasis) recorded in controlled challenge tests on a different sample of individuals from the same families. Due to strong confounding between the animal additive genetic effect and the family effects (common environmental + non-additive genetic), reliable additive (co)variance components and hence heritabilities and genetic correlations could not be obtained for the investigated parameters. Therefore, estimates of the association of challenge test survival with the studied immune parameters were obtained as product moment correlations between family least square means. These correlations revealed statistically significant (p < 0.05) negative correlations of survival with bacterial agglutination titre (−0.48), serum haemolysin titre (−0.29) and haemagglutination titre (−0.34); and significant positive correlation with ceruloplasmin level (0.51). The correlations of survival to aeromoniasis with myeloperoxidase activity, superoxide production and lysozyme activity were found to be not significantly different from zero (p > 0.05). Assuming that the negatively correlated candidate traits are not favourable as indirect selection criteria, the results suggest that ceruloplasmin level could potentially be a marker for resistance to aeromoniasis in rohu. The use of this immune parameter as an indirect selection criterion for increased resistance to aeromoniasis in rohu will, however, require that the parameter shows significant additive genetic variation and a significant genetic correlation with survival. Further studies are therefore needed to obtain a reliable heritability estimate for ceruloplasmin and its genetic correlation with survival from aeromoniasis.     

Heritability of individual fitness in female macaques

Heritability of fitness is an important parameter for evolutionary studies, but it is controversial and difficult to estimate this quantitative genetic statistic. I compare two single-generation proxies of individual fitness estimated from demographic information (lifetime reproductive success, LRS; and individual finite rate of increase, individual λ) and lifespan for the female members of a free-ranging population of rhesus macaques (Macaca mulatta). All three variables have moderate heritabilities (λ = 0.36, LRS = 0.38, lifespan = 0.43) that are consistently depressed when non-reproductive individuals are censored from the analysis. This reduction suggests a large portion of the genetic variation in the fitness proxies is due to survival to reproductive age and commencement of reproduction in this population. This may be related to relatively benign, homogeneous environmental conditions. Any time gaps in modeling an animal’s life cycle can introduce similar inaccuracies in heritability of fitness proxies, although the direction of error is likely to vary with environmental conditions. Genetic correlations between the three variables were all indistinguishable from +1 implying no independent genetic variation. The similarity of heritability estimates for λ and LRS and strong genetic correlations are attributed to the dominance of adult lifespan in determining fitness for female macaques which are slow-reproducing by mammalian standards. While the heritabilities of both proxies were similar in this study, they should both be estimated when possible because they may provide different information, particularly in taxa with larger broods.     

Temperature Mediates Shifts in Individual Aggressiveness,Activity Level,and Social Behavior in a Spider

Although in recent years behavioral syndromes have received a wealth of attention, how traits within syndromes respond to changing environments is not well resolved. Here, we test the effects of temperature on a suite of behavioral traits in the spider Anelosimus studiosus to determine (1) whether there are shifts in individuals’ social tendency, activity level, and foraging behavior in response to temperature, (2) if these traits shift are in the direction predicted by within‐population axes of trait covariance, and (3) whether the effects of temperature differ among individuals. In previous work, we documented a behavioral syndrome in A. studiosus where increased tolerance of conspecifics is correlated with decreased activity level and aggressiveness toward prey. Furthermore, there are distinct among‐population differences in behavior, where individuals from warm sites tend to be more aggressive and active than individuals from cold sites. Our data here reveal that at warmer temperatures A. studiosus exhibit diminished tolerance of conspecifics, increased activity levels, shorter latencies of attack, and increased tendencies to attack multiple prey items. Furthermore, we found that individual differences in behavior were consistent across temperature regimes for the majority of behavioral traits considered here: social tendency, activity level, and latency of attack. These findings are consistent with the hypothesis that these behaviors are linked together by shared genetic underpinnings (e.g., metabolic differences) and shift non‐independently in response to contemporary abiotic environment (i.e., temperature). Furthermore, our data suggest that temperature itself could be responsible for the among‐population variation in social structure in A. studiosus.     

Improved Equations for Estimating the Resting Metabolic Rate

New models were developed for predicting the resting metabolic rate (RMR) with sufficient accuracy for use in epidemiologic studies and for weight control of individuals. For this purpose, the RMR of 213 women and 76 men was measured, and physical measurements were taken. The RMR was regressed on correlates of RMR, avoiding harmful degrees of collinearity by rejecting interregressor correlations exceeding r=0.5. For women, the best model (R₂=0.71) included the regressors age, race, weight, pulse rate, smoking, and body temperature. The best model for males (R2 = 0.81) included age, race, weight, blood pressure, smoking, time (of day the RMR was measured), and whether subjects had a meal prior to calorimetry. The models were cross validated internally and also validated using an external database. In both cases, the mean estimated RMR did not differ significantly from the measured RMR. The accuracy of the models was compared with four models reported in the literature, three of which overestimated the RMR by up to 17%. In conclusion, improved RMR prediction models have been developed, more accurate than existing models, rendering them suitable for application to epidemiological databases and for individual weight control programs.     

Individual and Temporal Variation in Outcrossing Rates and Pollen Flow Patterns in Ceiba pentandra (Malvaceae: Bombacoidea)

Ceiba pentandra is a tropical tree with high rates of selfing in some populations. In mixed‐mating species, variation in selfing is due to changes in adult density or variability of incompatibility systems. The effect of spatial isolation and phenology on selfing rates and pollen flow distances was analyzed using microsatellites in a fragmented population of Ceiba pentandra, in southern Costa Rica. Adult trees within a heterogeneous landscape were classified as grouped or isolated. We compared selfing rates at the individual level, between isolation conditions and 2 yr (2007, 2009), which differed in the number of flowering individuals. Mixed mating was estimated in both years (t_m = 0.624–0.759). Trees mated predominantly by outcrossing, while only a few trees reproduced through selfing. Spatial isolation did not significantly affect outcrossing rates. The progeny of grouped trees was mostly sired by near‐neighbors (<1 km) and by long‐distance pollen flow events in isolated trees. A reduction in the number of flowering individuals in 2009 reduced near‐neighbor matings, increased selfing in grouped trees, and decreased the number of unsampled sires in the progeny. Comparing selfing rates on individuals that flowered in both reproductive periods suggests a flexible mating system. Variation in self‐fertilization rates in this population appears to depend on variation of individual traits, such as genetic variability in self‐incompatibility genes, but it is independent of landscape heterogeneity. In contrast, pollen flow distances depend on local tree density as bats concentrate their foraging between near individuals to maximize energy efficiency.     

Modeling nitrous oxide emission from rivers: a global assessment

Estimates of global riverine nitrous oxide (N₂O) emissions contain great uncertainty. We conducted a meta‐analysis incorporating 169 observations from published literature to estimate global riverine N₂O emission rates and emission factors. Riverine N₂O flux was significantly correlated with NH₄, NO₃ and DIN (NH₄ + NO₃) concentrations, loads and yields. The emission factors EF(a) (i.e., the ratio of N₂O emission rate and DIN load) and EF(b) (i.e., the ratio of N₂O and DIN concentrations) values were comparable and showed negative correlations with nitrogen concentration, load and yield and water discharge, but positive correlations with the dissolved organic carbon : DIN ratio. After individually evaluating 82 potential regression models based on EF(a) or EF(b) for global, temperate zone and subtropical zone datasets, a power function of DIN yield multiplied by watershed area was determined to provide the best fit between modeled and observed riverine N₂O emission rates (EF(a): R² = 0.92 for both global and climatic zone models, n = 70; EF(b): R² = 0.91 for global model and R² = 0.90 for climatic zone models, n = 70). Using recent estimates of DIN loads for 6400 rivers, models estimated global riverine N₂O emission rates of 29.6–35.3 (mean = 32.2) Gg N₂O–N yr⁻¹ and emission factors of 0.16–0.19% (mean = 0.17%). Global riverine N₂O emission rates are forecasted to increase by 35%, 25%, 18% and 3% in 2050 compared to the 2000s under the Millennium Ecosystem Assessment's Global Orchestration, Order from Strength, Technogarden, and Adapting Mosaic scenarios, respectively. Previous studies may overestimate global riverine N₂O emission rates (300–2100 Gg N₂O–N yr⁻¹) because they ignore declining emission factor values with increasing nitrogen levels and channel size, as well as neglect differences in emission factors corresponding to different nitrogen forms. Riverine N₂O emission estimates will be further enhanced through refining emission factor estimates, extending measurements longitudinally along entire river networks and improving estimates of global riverine nitrogen loads.     

Effect of salinity and body weight on ecophysiological performance of the Pacific white shrimp (Litopenaeus vannamei)

Ecophysiological responses of Litopenaeus vannamei were evaluated as functions of environmental salinity and animal size. Growth rate, routine metabolic rate, limiting oxygen concentration, and marginal metabolic scope were determined for L. vannamei acclimated to, and tested at, salinities of 2, 10, and 28 ppt, all at 28 °C. Routine metabolic rate (RMR), estimated as oxygen-consumption rate per unit body weight for fasted, routinely-active shrimp, was independent of salinity but decreased with increasing shrimp weight. Limiting oxygen concentration for routine metabolism (LOCr) decreased with increased shrimp weight for the 10 and 28 ppt treatments, but not for the 2 ppt treatment. Marginal metabolic scope (MMS = RMR/LOCr) also decreased with increasing shrimp weight and was independent of salinity. Growth rate was significantly less at 2 ppt than at either 10 or 28 ppt, which gave similar growth rates.     

Lower body mass and higher metabolic rate enhance winter survival in root voles,Microtus oeconomus

Although the biological significance of individual variation in physiological traits is widely recognized, studies of their association with fitness in wild populations are surprisingly scarce. We investigated the effect of individual phenotypic variation in body mass, resting (RMR) and peak metabolic rates (PMR) on mortality of the root vole Microtus oeconomus. Body mass and metabolic rates varied significantly among consecutive years and were also age dependent, as individuals born in late summer and autumn were characterized by significantly lower body mass and metabolic rates than animals born earlier. At the beginning of winter voles born in spring and early summer exhibited reduced body mass and metabolic rates, whereas animals born later maintained lower body mass and RMR, which may be interpreted as phenotypic plasticity enhancing the probability of survival. Body mass had no significant effect on vole survival during summer. In contrast, smaller individuals were characterized by lower mortality during early winter, whereas higher body mass was positively associated with survival later in the season. High body‐mass‐corrected RMR positively affected survival in both summer and winter. The effect of PMR was apparent only during winter, though its direction (and correlation with RMR) varied among years. Deep snow cover negatively affected the survival of voles in both early and late winter. Ambient temperature was positively associated with winter survival, except for late winter, when rising temperature caused flooding of vole habitat. We conclude that the lack of consistency in the directionality and strength of the effects of body mass and metabolic rates on winter survival does not undermine their importance, but rather demonstrates the ability of individuals to adjust metabolic rate to changing environmental conditions. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 297–309.     

What causes intraspecific variation in resting metabolic rate and what are its ecological consequences?

Individual differences in the energy cost of self-maintenance (resting metabolic rate, RMR) are substantial and the focus of an emerging research area. These differences may influence fitness because self-maintenance is considered as a life-history component along with growth and reproduction. In this review, we ask why do some individuals have two to three times the ‘maintenance costs’ of conspecifics, and what are the fitness consequences? Using evidence from a range of species, we demonstrate that diverse factors, such as genotypes, maternal effects, early developmental conditions and personality differences contribute to variation in individual RMR. We review evidence that RMR is linked with fitness, showing correlations with traits such as growth and survival. However, these relationships are modulated by environmental conditions (e.g. food supply), suggesting that the fitness consequences of a given RMR may be context-dependent. Then, using empirical examples, we discuss broad-scale reasons why variation in RMR might persist in natural populations, including the role of both spatial and temporal variation in selection pressures and trans-generational effects. To conclude, we discuss experimental approaches that will enable more rigorous examination of the causes and consequences of individual variation in this key physiological trait.     

Pace‐of‐life: Relationships among locomotor activity,life history,and circadian rhythm in the assassin bug,Amphibolus venator

The pace‐of‐life syndrome (POLS) hypothesis means that animal behavior is correlated with life history strategies. Studies have reported that the free‐running period of the circadian rhythm (length of the period) is correlated with life history strategies in some animals. Although the length of the circadian rhythm may be associated with the POLS hypothesis, few studies have investigated the relationships among animal behavior, life history traits, and circadian rhythm. We tested the POLS hypothesis in the assassin bug, Amphibolus venator, which shows individual variation in locomotor activity. We found higher repeatability of differences in locomotor activity between individuals. Moreover, we found a trade‐off between locomotor activity and developmental period such that active individuals developed faster. However, locomotor activity was not correlated with the length of the circadian rhythm in A. venator. Therefore, this study suggests that the length of the circadian rhythm in A. venator does not support the POLS hypothesis.     

Evolutionary potential of thermal preference and heat tolerance in Drosophila subobscura

Evolutionary change of thermal traits (i.e., heat tolerance and behavioural thermoregulation) is one of the most important mechanisms exhibited by organisms to respond to global warming. However, the evolutionary potential of heat tolerance, estimated as narrow‐sense heritability, depends on the methodology employed. An alternative adaptive mechanism to buffer extreme temperatures is behavioural thermoregulation, although the association between heat tolerance and thermal preference is not clearly understood. We suspect that methodological effects associated with the duration of heat stress during thermal tolerance assays are responsible for missing this genetic association. To test this hypothesis, we estimated the heritabilities and genetic correlations for thermal traits in Drosophila subobscura, using high‐temperature static and slow ramping assays. We found that heritability for heat tolerance was higher in static assays (h² = 0.134) than in slow ramping assays (h² = 0.084), suggesting that fast assays may provide a more precise estimation of the genetic variation of heat tolerance. In addition, thermal preference exhibited a low heritability (h² = 0.066), suggesting a reduced evolutionary response for this trait. We also found that the different estimates of heat tolerance and thermal preference were not genetically correlated, regardless of how heat tolerance was estimated. In conclusion, our data suggest that these thermal traits can evolve independently in this species. In agreement with previous evidence, these results indicate that methodology may have an important impact on genetic estimates of heat tolerance and that fast assays are more likely to detect the genetic component of heat tolerance.     

Within‐Individual Correlations Reveal Link Between a Behavioral Syndrome,Condition, and Cortisol in Free‐Ranging Belding's Ground Squirrels

Animals often exhibit consistent individual differences in behavior (i.e., animal personality) and correlations between behaviors (i.e., behavioral syndromes), yet the causes of those patterns of behavioral variation remain insufficiently understood. Many authors hypothesize that state‐dependent behavior produces animal personality and behavioral syndromes. However, empirical studies assessing patterns of covariation among behavioral traits and state variables have produced mixed results. New statistical methods that partition correlations into between‐individual and residual within‐individual correlations offer an opportunity to more sufficiently quantify relationships among behaviors and state variables to assess hypotheses of animal personality and behavioral syndromes. In a population of wild Belding's ground squirrels (Urocitellus beldingi), we repeatedly measured activity, exploration, and response to restraint behaviors alongside glucocorticoids and nutritional condition. We used multivariate mixed models to determine whether between‐individual or within‐individual correlations drive phenotypic relationships among traits. Squirrels had consistent individual differences for all five traits. At the between‐individual level, activity and exploration were positively correlated whereas both traits negatively correlated with response to restraint, demonstrating a behavioral syndrome. At the within‐individual level, condition negatively correlated with cortisol, activity, and exploration. Importantly, this indicates that although behavior is state‐dependent, which may play a role in animal personality and behavioral syndromes, feedback mechanisms between condition and behavior appear not to produce consistent individual differences in behavior and correlations between them.     

Emergence,propagation or disappearance of novel behavioral patterns in the habituated chimpanzees of Mahale: a review

Each local population of chimpanzees shows cultural variation, but little is known about how behavioral variations first emerge, and how often variants spread to other individuals and then become fixed as a local culture in chimpanzee society. Although field studies of chimpanzees are still too short to answer these questions definitively, it may stimulate further study in various sites to summarize the developments observed over the past 40 years at Mahale, Tanzania. Innovative patterns were operationally defined as new behavioral patterns performed by M group chimpanzees from 1981 onwards. Innovations included patterns of feeding (n = 8), human-directed behavior (n = 3), hygiene behavior (n = 4), maternal carrying of infants (n = 2), courtship (n = 2), play (n = 6), intimidation displays (n = 3), and quasi-grooming (n = 4). Although most patterns were repeated later by other individuals, six patterns were never seen performed by another individual, and eight patterns were performed by one or a few individuals but social transmission was unlikely. Thus, innovation was not rare, but emergence of fashion or establishment of traditions seems to occur rarely in chimpanzee society.