Culturally determined interspecies communication between humans and honeyguides.

Species interactions that vary across environments can create geographical mosaics of genetic coevolution. However, traits mediating species interactions are sometimes culturally inherited. Here we show that traditions of interspecies communication between people and wild birds vary in a culturally determined geographical mosaic. Honey hunters in different parts of Africa use different calls to communicate with greater honeyguides (Indicator indicator) that lead them to bees' nests. We show experimentally that honeyguides in Tanzania and Mozambique discriminate among honey hunters' calls, responding more readily to local than to foreign calls. This was not explained by variation in sound transmission and instead suggests that honeyguides learn local human signals. We discuss the forces stabilizing and diversifying interspecies communication traditions, and the potential for cultural coevolution between species.

Demographic and hormonal evidence for menopause in wild chimpanzees.

Among mammals, post-reproductive life spans are currently documented only in humans and a few species of toothed whales. Here we show that a post-reproductive life span exists among wild chimpanzees in the Ngogo community of Kibale National Park, Uganda. Post-reproductive representation was 0.195, indicating that a female who reached adulthood could expect to live about one-fifth of her adult life in a post-reproductive state, around half as long as human hunter-gatherers. Post-reproductive females exhibited hormonal signatures of menopause, including sharply increasing gonadotropins after age 50. We discuss whether post-reproductive life spans in wild chimpanzees occur only rarely, as a short-term response to favorable ecological conditions, or instead are an evolved species-typical trait as well as the implications of these alternatives for our understanding of the evolution of post-reproductive life spans.

Lifestyle and patterns of physical activity in Hadza foragers.

OBJECTIVES: Physically active lifestyles are associated with several health benefits. Physical activity (PA) levels are low in post-industrial populations, but generally high throughout life in subsistence populations. The Hadza are a subsistence-oriented foraging population in Tanzania known for being physically active, but it is unknown how recent increases in market integration may have altered their PA patterns. In this study, we examine PA patterns for Hadza women and men who engage in different amounts of traditional foraging. MATERIALS AND METHODS: One hundred and seventy seven Hadza participants (51% female, 19-87 years) wore an Axivity accelerometer (dominant wrist) for ~6 days during dry season months. We evaluated the effects of age, sex, and lifestyle measures on four PA measures that capture different aspects of the PA profile. RESULTS: Participants engaged in high levels of both moderate-intensity PA and inactivity. Although PA levels were negatively associated with age, older participants were still highly active. We found no differences in PA between participants living in more traditional "bush" camps and those living in more settled "village" camps. Mobility was positively associated with step counts for female participants, and schooling was positively associated with inactive time for male participants. CONCLUSIONS: The similarity in PA patterns between Hadza participants in different camp types suggests that high PA levels characterize subsistence lifestyles generally. The sex-based difference in the effects of mobility and schooling on PA could be a reflection of the Hadza's gender-based division of labor, or indicate that changes to subsistence-oriented lifestyles impact women and men in different ways.

Safeguarding human-wildlife cooperation.

Human-wildlife cooperation occurs when humans and free-living wild animals actively coordinate their behavior to achieve a mutually beneficial outcome. These interactions provide important benefits to both the human and wildlife communities involved, have wider impacts on the local ecosystem, and represent a unique intersection of human and animal cultures. The remaining active forms are human-honeyguide and human-dolphin cooperation, but these are at risk of joining several inactive forms (including human-wolf and human-orca cooperation). Human-wildlife cooperation faces a unique set of conservation challenges, as it requires multiple components-a motivated human and wildlife partner, a suitable environment, and compatible interspecies knowledge-which face threats from ecological and cultural changes. To safeguard human-wildlife cooperation, we recommend: (i) establishing ethically sound conservation strategies together with the participating human communities; (ii) conserving opportunities for human and wildlife participation; (iii) protecting suitable environments; (iv) facilitating cultural transmission of traditional knowledge; (v) accessibly archiving Indigenous and scientific knowledge; and (vi) conducting long-term empirical studies to better understand these interactions and identify threats. Tailored safeguarding plans are therefore necessary to protect these diverse and irreplaceable interactions. Broadly, our review highlights that efforts to conserve biological and cultural diversity should carefully consider interactions between human and animal cultures. Please see AfricanHoneyguides.com/abstract-translations for Kiswahili and Portuguese translations of the abstract.

Human total, basal and activity energy expenditures are independent of ambient environmental temperature.

Lower ambient temperature (Ta) requires greater energy expenditure to sustain body temperature. However, effects of Ta on human energetics may be buffered by environmental modification and behavioral compensation. We used the IAEA DLW database for adults in the USA (n = 3213) to determine the effect of Ta (-10 to +30°C) on TEE, basal (BEE) and activity energy expenditure (AEE) and physical activity level (PAL). There were no significant relationships (p > 0.05) between maximum, minimum and average Ta and TEE, BEE, AEE and PAL. After adjustment for fat-free mass, fat mass and age, statistically significant (p < 0.01) relationships between TEE, BEE and Ta emerged in females but the effect sizes were not biologically meaningful. Temperatures inside buildings are regulated at 18-25°C independent of latitude. Hence, adults in the US modify their environments to keep TEE constant across a wide range of external ambient temperatures.

Acoustic regularities in infant-directed speech and song across cultures.

When interacting with infants, humans often alter their speech and song in ways thought to support communication. Theories of human child-rearing, informed by data on vocal signalling across species, predict that such alterations should appear globally. Here, we show acoustic differences between infant-directed and adult-directed vocalizations across cultures. We collected 1,615 recordings of infant- and adult-directed speech and song produced by 410 people in 21 urban, rural and small-scale societies. Infant-directedness was reliably classified from acoustic features only, with acoustic profiles of infant-directedness differing across language and music but in consistent fashions. We then studied listener sensitivity to these acoustic features. We played the recordings to 51,065 people from 187 countries, recruited via an English-language website, who guessed whether each vocalization was infant-directed. Their intuitions were more accurate than chance, predictable in part by common sets of acoustic features and robust to the effects of linguistic relatedness between vocalizer and listener. These findings inform hypotheses of the psychological functions and evolution of human communication.

Effects of Evolution, Ecology, and Economy on Human Diet: Insights from Hunter-Gatherers and Other Small-Scale Societies.

We review the evolutionary origins of the human diet and the effects of ecology economy on the dietary proportion of plants and animals. Humans eat more meat than other apes, a consequence of hunting and gathering, which arose ∼2.5 Mya with the genus Homo. Paleolithic diets likely included a balance of plant and animal foods and would have been remarkably variable across time and space. A plant/animal food balance of 50/50% prevails among contemporary warm-climate hunter-gatherers, but these proportions vary widely. Societies in cold climates, and those that depend more on fishing or pastoralism, tend to eat more meat. Warm-climate foragers, and groups that engage in some farming, tend to eat more plants. We present a case study of the wild food diet of the Hadza, a community of hunter-gatherers in northern Tanzania, whose diet is high in fiber, adequate in protein, and remarkably variable over monthly timescales.

Hunter-Gatherers in context: Mammal community composition in a northern Tanzania landscape used by Hadza foragers and Datoga pastoralists.

In many regions of sub Saharan Africa large mammals occur in human-dominated areas, yet their community composition and abundance have rarely been described in areas occupied by traditional hunter-gatherers and pastoralists. Surveys of mammal populations in such areas provide important measures of biodiversity and provide ecological context for understanding hunting practices. Using a sampling grid centered on a Hadza hunter-gatherer camp and covering 36 km2 of semi-arid savannah in northern Tanzania, we assessed mammals using camera traps (n = 19 stations) for c. 5 months (2,182 trap nights). In the study area (Tli'ika in the Hadza language), we recorded 36 wild mammal species. Rarefaction curves suggest that sampling effort was sufficient to capture mammal species richness, yet some species known to occur at low densities in the wider area (e.g. African lions, wildebeest) were not detected. Relative abundance indices of wildlife species varied by c. three orders of magnitude, from a mean of 0.04 (African wild dog) to 20.34 capture events per 100 trap-nights (Kirk's dik dik). To contextualize the relative abundance of wildlife in the study area, we compared our study's data to comparable camera trap data collected in a fully protected area of northern Tanzania with similar rainfall (Lake Manyara National Park). Raw data and negative binomial regression analyses show that wild herbivores and wild carnivores were generally detected in the national park at higher rates than in the Hadza-occupied region. Livestock were notably absent from the national park, but were detected at high levels in Tli'ika, and cattle was the second most frequently detected species in the Hadza-used area. We discuss how these data inform current conservation efforts, studies of Hadza hunting, and models of hunter-gatherer foraging ecology and diet.

Evolution of water conservation in humans.

To sustain life, humans and other terrestrial animals must maintain a tight balance of water gain and water loss each day.1-3 However, the evolution of human water balance physiology is poorly understood due to the absence of comparative measures from other hominoids. While humans drink daily to maintain water balance, rainforest-living great apes typically obtain adequate water from their food and can go days or weeks without drinking4-6. Here, we compare isotope-depletion measures of water turnover (L/d) in zoo- and rainforest-sanctuary-housed apes (chimpanzees, bonobos, gorillas, and orangutans) with 5 diverse human populations, including a hunter-gatherer community in a semi-arid savannah. Across the entire sample, water turnover was strongly related to total energy expenditure (TEE, kcal/d), physical activity, climate (ambient temperature and humidity), and fat free mass. In analyses controlling for those factors, water turnover was 30% to 50% lower in humans than in other apes despite humans' greater sweating capacity. Water turnover in zoo and sanctuary apes was similar to estimated turnover in wild populations, as was the ratio of water intake to dietary energy intake (∼2.8 mL/kcal). However, zoo and sanctuary apes ingested a greater ratio of water to dry matter of food, which might contribute to digestive problems in captivity. Compared to apes, humans appear to target a lower ratio of water/energy intake (∼1.5 mL/kcal). Water stress due to changes in climate, diet, and behavior apparently led to previously unknown water conservation adaptations in hominin physiology.

The role of causal knowledge in the evolution of traditional technology.

Humans occupy a wider range of environments, process more energy, and have greater biomass than any other species because we are able to culturally evolve complex, locally adaptive technologies.1 Competing models make different predictions about the role of causal knowledge in this process. Some argue that innovation and transmission cannot occur without causal understanding,2-5 while others posit that complex technologies can evolve without causal understanding.1,6-10 Prior research on this topic has been restricted to theoretical work and experimental studies with student participants.11-13 The Hadza are foragers who rely on bows for subsistence.14-16 We interviewed skilled Hadza bowyers (bow-makers) and compared their beliefs regarding the tradeoffs in bow construction to those revealed by experimental and engineering research. If bowyers understand the tradeoffs, it is plausible that cultural evolution is rooted in causal understanding, while if they do not, the cultural accumulation of knowledge is likely more important in the process. We show that Hadza bowyers understand some mechanical trade-offs but not others, and therefore the evolution of a complex, highly adaptive technology is possible with incomplete causal knowledge regarding key mechanical trade-offs. Instead, some important design choices made by subjects seem to reflect cultural norms. Although previously published reports have suggested that some individuals are recognized by the Hadza as being especially skilled or knowledgeable,14,17 our results do not indicate that some individuals are significantly more knowledgeable about bow-making than others, nor is there statistical evidence that causal knowledge increases with age.

Gendered movement ecology and landscape use in Hadza hunter-gatherers.

Understanding how gendered economic roles structure space use is critical to evolutionary models of foraging behaviour, social organization and cognition. Here, we examine hunter-gatherer spatial behaviour on a very large scale, using GPS devices worn by Hadza foragers to record 2,078 person-days of movement. Theory in movement ecology suggests that the density and mobility of targeted foods should predict spatial behaviour and that strong gender differences should arise in a hunter-gatherer context. As predicted, we find that men walked further per day, explored more land, followed more sinuous paths and were more likely to be alone. These data are consistent with the ecology of male- and female-targeted foods and suggest that male landscape use is more navigationally challenging in this hunter-gatherer context. Comparisons of Hadza space use with space use data available for non-human primates suggest that the sexual division of labour likely co-evolved with increased sex differences in spatial behaviour and landscape use.

Ageing and physical function in East African foragers and pastoralists.

Human lifespans are exceptionally long compared with those of other primates. A key element in exploring the evolution of human longevity is understanding how modern humans grow older. Our current understanding of common age-related changes in human health and function stems mostly from studies in industrialized societies, where older adulthood is often associated with an increased incidence of chronic diseases. However, individuals who engage in different lifestyles across industrialized and non-industrialized contexts may display variance in age-related changes in health and function. Here, we explore aspects of physical function in a non-industrialized context using three objective measures of physical function. We assessed physical activity levels, walking endurance and muscle strength in two East African populations: Hadza hunter-gatherers in Tanzania and Pokot pastoralists in Kenya. Both Hadza and Pokot participants displayed significant age-related differences in most, but not all, functional measures. Our results suggest that some age-related differences in physical function seen in industrialized contexts could be consistently experienced by most humans, while other age-related differences may vary across populations. Studies of ageing should expand to include a broad range of populations so we can create a more comprehensive understanding of how senescence varies across different lifestyle contexts. This article is part of the theme issue 'Evolution of the primate ageing process'.

Sitting, squatting, and the evolutionary biology of human inactivity.

Recent work suggests human physiology is not well adapted to prolonged periods of inactivity, with time spent sitting increasing cardiovascular disease and mortality risk. Health risks from sitting are generally linked with reduced levels of muscle contractions in chair-sitting postures and associated reductions in muscle metabolism. These inactivity-associated health risks are somewhat paradoxical, since evolutionary pressures tend to favor energy-minimizing strategies, including rest. Here, we examined inactivity in a hunter-gatherer population (the Hadza of Tanzania) to understand how sedentary behaviors occur in a nonindustrial economic context more typical of humans' evolutionary history. We tested the hypothesis that nonambulatory rest in hunter-gatherers involves increased muscle activity that is different from chair-sitting sedentary postures used in industrialized populations. Using a combination of objectively measured inactivity from thigh-worn accelerometers, observational data, and electromygraphic data, we show that hunter-gatherers have high levels of total nonambulatory time (mean ± SD = 9.90 ± 2.36 h/d), similar to those found in industrialized populations. However, nonambulatory time in Hadza adults often occurs in postures like squatting, and we show that these "active rest" postures require higher levels of lower limb muscle activity than chair sitting. Based on our results, we introduce the Inactivity Mismatch Hypothesis and propose that human physiology is likely adapted to more consistently active muscles derived from both physical activity and from nonambulatory postures with higher levels of muscle contraction. Interventions built on this model may help reduce the negative health impacts of inactivity in industrialized populations.

Age-related decline in urine concentration may not be universal: Comparative study from the U.S. and two small-scale societies.

OBJECTIVES: Evidence from industrialized populations suggests that urine concentrating ability declines with age. However, lifestyle factors including episodic protein intake and low hypertension may help explain differences between populations. Whether this age-related decline occurs among small-scale populations with active lifestyles and non-Western diets is unknown. We test the universality of age-related urine concentration decline. MATERIALS AND METHODS: We used urine specific gravity (Usg) and urine osmolality (Uosm) data from 15,055 U.S. nonpregnant adults without kidney failure aged 18-80 in 2007-2012 participating in the National Health and Nutrition Examination Survey (NHANES). We tested the relationship of age on urine concentration biomarkers with multiple linear regressions using survey commands. We compared results to longitudinal data on Usg from 116 Tsimane' forager-horticulturalists (266 observations) adults aged 18-83 in 2013-2014 from Lowland Bolivia, and to 38 Hadza hunter-gatherers (156 observations) aged 18-75 in 2010-2015 from Tanzania using random-effects panel linear regressions. RESULTS: Among U.S. adults, age was significantly negatively associated with Usg (Adjusted beta [B] = -0.0009 g/mL/10 years; SE = 0.0001; p < 0.001) and Uosm (B = -28.1 mOsm/kg/10 yr; SE = 2.4; p < 0.001). In contrast, among Tsimane' (B = 0.0003 g/mL/10 yr; SE = 0.0002; p = 0.16) and Hadza (B = -0.0004 g/mL/10 yr; SE = 0.0004; p = 0.29) age was not associated with Usg. Older Tsimane' and Hadza exhibited similar within-individual variability in Usg equivalent to younger adults. DISCUSSION: While U.S. adults exhibited age-related declines in urine concentration, Tsimane' and Hadza adults did not exhibit the same statistical decline in Usg. Mismatches between evolved physiology and modern environments in lifestyle may affect kidney physiology and disease risk.

Favorable ecological circumstances promote life expectancy in chimpanzees similar to that of human hunter-gatherers.

Demographic data on wild chimpanzees are crucial for understanding the evolution of chimpanzee and hominin life histories, but most data come from populations affected by disease outbreaks and anthropogenic disturbance. We present survivorship data from a relatively undisturbed and exceptionally large community of eastern chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. We monitored births, deaths, immigrations, and emigrations in the community between 1995 and 2016. Using known and estimated ages, we calculated survivorship curves for the whole community, for males and females separately, and for individuals ≤2 years old when identified. We used a novel method to address age estimation error by calculating stochastic survivorship curves. We compared Ngogo life expectancy, survivorship, and mortality rates to those from other chimpanzee communities and human hunter-gatherers. Life expectancy at birth for both sexes combined was 32.8 years, far exceeding estimates of chimpanzee life expectancy in other communities, and falling within the range of human hunter-gatherers (i.e., 27-37 years). Overall, the pattern of survivorship at Ngogo was more similar to that of human hunter-gatherers than to other chimpanzee communities. Maximum lifespan for the Ngogo chimpanzees, however, was similar to that reported at other chimpanzee research sites and was less than that of human-hunter gatherers. The absence of predation by large carnivores may contribute to some of the higher survivorship at Ngogo, but this cannot explain the much higher survivorship at Ngogo than at Kanyawara, another chimpanzee community in the same forest, which also lacks large carnivores. Higher survivorship at Ngogo appears to be an adaptive response to a food supply that is more abundant and varies less than that of Kanyawara. Future analyses of hominin life history evolution should take these results into account.

Physical activity patterns and biomarkers of cardiovascular disease risk in hunter-gatherers.

OBJECTIVES: Time spent in moderate-to-vigorous physical activity (MVPA) is a strong predictor of cardiovascular health, yet few humans living in industrialized societies meet current recommendations (150 min/week). Researchers have long suggested that human physiological requirements for aerobic exercise reflect an evolutionary shift to a hunting and gathering foraging strategy, and a recent transition to more sedentary lifestyles likely represents a mismatch with our past in terms of physical activity. The goal of this study is to explore this mismatch by characterizing MVPA and cardiovascular health in the Hadza, a modern hunting and gathering population living in Northern Tanzania. METHODS: We measured MVPA using continuous heart rate monitoring in 46 participants recruited from two Hadza camps. As part of a larger survey of health in the Hadza, we measured blood pressure (n = 198) and biomarkers of cardiovascular health (n = 23) including C-reactive protein, cholesterol (Total, HDL, and LDL), and triglycerides. RESULTS: We show that Hadza participants spend large amounts of time in MVPA (134.92 ± 8.6 min/day), and maintain these activity levels across the lifespan. In fact, the Hadza engage in over 14 times as much MVPA as subjects participating in large epidemiological studies in the United States. We found no evidence of risk factors for cardiovascular disease in this population (low prevalence of hypertension across the lifespan, optimal levels for biomarkers of cardiovascular health). CONCLUSIONS: Our results provide evidence that the hunting and gathering foraging strategy involves high levels of MVPA, supporting the evolutionary medicine model for the relationship between MVPA and cardiovascular health.

Energy expenditure and activity among Hadza hunter-gatherers.

OBJECTIVES: Studies of total energy expenditure, (TEE; kcal/day) among traditional populations have challenged current models relating habitual physical activity to daily energy requirements. Here, we examine the relationship between physical activity and TEE among traditional Hadza hunter-gatherers living in northern Tanzania. METHODS: Hadza adults were studied at two camps, with minimal intervention so as to monitor energy expenditure and activity during normal daily life. We measured daily walking distance and walking speed using wearable GPS units for 41 adults. For a subset of 30 adults, we measured TEE using doubly labeled water, three indices of work load (foraging return rate, maternal status, and number of dependent children), and urinary biomarkers of metabolic activity and stress (8-hydroxydeoxyguanosine, cortisol, and testosterone). RESULTS: Fat-free mass was the single strongest predictor of TEE among Hadza adults (r(2) = 0.66, P < 0.001). Hadza men used greater daily walking distances and faster walking speeds compared with that of Hadza women, but neither sex nor any measure of physical activity or work load were correlated with TEE in analyses controlling for fat-free mass. Compared with developed, industrial populations, Hadza adults had similar TEE but elevated levels of metabolic stress as measured by 8-hydroxydeoxyguanosine. CONCLUSION: Our results indicate that daily physical activity may not predict TEE within traditional hunter-gatherer populations like the Hadza. Instead, adults with high levels of habitual physical activity may adapt by reducing energy allocation to other physiological activity.

Pursuit : A Foraging Simulation Tool for Research and Teaching.

This article describes a software tool called "Pursuit" that is intended to be used for both research and teaching on the topic of optimal foraging theory. The tool provides a dynamic graphical and auditory interface in which users encounter different prey animals and then must decide whether to pursue or ignore the encountered prey. Based on the characteristics of the prey in the foraging environment and the decisions of the player, each user harvests a set of prey per round and achieves a corresponding foraging return rate. Administrators of Pursuit specify the environmental parameters that determine what prey users will encounter. All environmental parameters and user decisions are tracked and logged for analysis. We created this tool for laboratory experiments, but we believe Pursuit could also be an engaging and effective teaching tool, whereby students adopt the role of forager, and through such play, experience a simulated foraging context and learn about foraging theory. Pursuit is freely available and can run on any platform that supports Java, including Mac OS, Windows, and Linux.

Toward a reality-based understanding of Hadza men's work: a response to Hawkes et al. (2014).

Observations of Hadza men foraging out of camp and sharing food in camp show that men seeking to maximize the flow of calories to their families should pursue large game, and that hunting large game does not pose a collective action problem. These data also show that Hadza men frequently pursued honey, small game, and fruit, and that by doing so, provided a more regular flow of food to their households than would a putative big game specialist. These data support our earlier studies demonstrating that the goal of family provisioning is a robust predictor of Hadza men's behavior. As before, the show-off and costly signaling hypotheses advanced by Hawkes and colleagues fail as both descriptions of and explanations for Hadza men's work.

Hunter-gatherer inter-band interaction rates: implications for cumulative culture.

Our species exhibits spectacular success due to cumulative culture. While cognitive evolution of social learning mechanisms may be partially responsible for adaptive human culture, features of early human social structure may also play a role by increasing the number potential models from which to learn innovations. We present interview data on interactions between same-sex adult dyads of Ache and Hadza hunter-gatherers living in multiple distinct residential bands (20 Ache bands; 42 Hadza bands; 1201 dyads) throughout a tribal home range. Results show high probabilities (5%-29% per year) of cultural and cooperative interactions between randomly chosen adults. Multiple regression suggests that ritual relationships increase interaction rates more than kinship, and that affinal kin interact more often than dyads with no relationship. These may be important features of human sociality. Finally, yearly interaction rates along with survival data allow us to estimate expected lifetime partners for a variety of social activities, and compare those to chimpanzees. Hadza and Ache men are estimated to observe over 300 men making tools in a lifetime, whereas male chimpanzees interact with only about 20 other males in a lifetime. High intergroup interaction rates in ancestral humans may have promoted the evolution of cumulative culture.