Trade-Offs between female food acquisition and child care among hiwi and ache foragers

Even though female food acquisition is an area of considerable interest in hunter-gatherer research, the ecological determinants of women’s economic decisions in these populations are still poorly understood. The literature on female foraging behavior indicates that there is considerable variation within and across foraging societies in the amount of time that women spend foraging and in the amount and types of food that they acquire. It is possible that this heterogeneity reflects variation in the trade-offs between time spent in food acquisition and child care activities that women face in different groups of hunter-gatherers. In this paper we discuss the fitness trade-offs between food acquisition and child care that Hiwi and Ache women foragers might face. Multiple regression analyses show that in both populations the daily food acquisition of a woman’s spouse is negatively related to female foraging effort. In addition, nursing mothers spend less time foraging and acquire less food than do nonnursing women. As the number of dependents that a woman has increases, however, women also increase foraging time and the amount of food they acquire. Some interesting exceptions to these general trends are as follows: (a) differences in foraging effort between nursing and nonnursing women are less pronounced when fruits and roots are in season than in other seasons of the year; (b) foraging return rates decrease for Ache women as their numbers of dependents increase; and (c) among Ache women, the positive effect of number of dependents on foraging behavior is less pronounced when fruits are in season than at other times of the year. Lastly, in the Hiwi sample we found that postreproductive women work considerably harder than women of reproductive age in the root season but not in other seasons of the year. We discuss how ecological variation in constraints, the number of health insults to children that Hiwi and Ache mothers can avoid, and the fitness benefits they can gain from spending time in food acquisition and child care might account for differences and similarities in the foraging behaviors of subgroups of Hiwi and Ache mothers across different seasons of the year. Valid tests of the explanations we propose will require considerable effort to measure the relationship between maternal food acquisition, child care, and adverse health outcomes in offspring. This paper is dedicated to Nutsiya, the hardest-working grandmother we ever observed Kristen Hawkes contributed useful information on female foraging among the Hadza. The research was funded by the National Science Foundation (BNS-8613215, BNS-538228, BNS-8309834, BNS-8121209) and the L. S. B. Leakey Foundation. The senior author was supported by fellowships from the Fundacion Gran Mariscal de Ayacucho of Venezuela and the National Institute of Health (Grant No. 1 RO1 HD16221-01A2). A. Magdalena Hurtado, Kim Hill, and Hillard Kaplan collaborate in research on the evolutionary ecology of the division of labor by sex. Ines Hurtado is Senior Research Scientist at the Instituto Venezolano de Investigaciones Científicas, Venezuela. She studies the immunology of parasite load and atopic illness in Hiwi foragers.     

Friendship, cliquishness, and the emergence of cooperation

The evolution of cooperation is a central problem in biology and the social sciences. While theoretical work using the iterated prisoner's dilemma (IPD) has shown that cooperation among non-kin can be sustained among reciprocal strategies (i.e. tit-for-tat), these results are sensitive to errors in strategy execution, cyclical invasions by free riders, and the specific ecology of strategies. Moreover, the IPD assumes that a strategy's probability of playing the PD game with other individuals is independent of the decisions made by others. Here, we remove the assumption of independent pairing by studying a more plausible cooperative dilemma in which players can preferentially interact with a limited set of known partners and also deploy longer-term accounting strategies that can counteract the effects of random errors. We show that cooperative strategies readily emerge and persist in a range of noisy environments, with successful cooperative strategies (henceforth, cliquers) maintaining medium-term memories for partners and low thresholds for acceptable cooperation (i.e. forgiveness). The success of these strategies relies on their cliquishness-a propensity to defect with strangers if they already have an adequate number of partners. Notably, this combination of medium-term accounting, forgiveness, and cliquishness fits with empirical studies of friendship and other long-term relationships among humans.     

Hunter-gatherer males are more risk-seeking than females,even in late childhood

Observed economic and labor disparities between the sexes may, in part, result from evolved sex differences in risk preferences. Using incentivized economic games, we report on sex differences in risk preferences in the Hadza, a population of hunter-gatherers. One game played in 2010 (n = 233) found that more Hadza males than females prefer to gamble for a chance to earn more maize rather than settle for a sure, but smaller, amount. Similarly, a second game played in 2013 (n = 102) found that male Hadza gamble a greater proportion of honey for a chance to earn more compared to female Hadza. Effect sizes are small to medium. We find weak evidence that risk-taking increases in men as their mating opportunities increase. In both games, the sex difference widens throughout childhood and is greatest among adolescents; though note that child samples are small. We explore developmental trends further using observational data on food returns in children (n = 357). Our data suggest that while the mean number of calories boys bring to camp remains stable with age, the variance in their caloric returns increases. Among girls, the variance remains stable with increased age. Both the economic games and food return data are consistent with the sexual division of labor wherein boys, beginning in late childhood, begin to target riskier foods. To the extent that the Hadza allow us to make inferences about long-standing patterns of human behavior, we suggest that sex differences in risk preferences may have been present long before agriculture and the modern work environment.     

Male and female contributions to provisioning rates of thin-billed prions, Pachyptila belcheri , in the South Atlantic

We recorded individual provisioning patterns of male and female thin-billed prions in the largest known colony on New Island (Falkland Islands, South Atlantic Ocean), to determine male and female contributions to provisioning rates and to compare them with data from their other main breeding site, on Kerguelen, in the Southern Indian Ocean. Both male and female birds from New Island undertook trips of 1–8 days’ duration (median 3 days), similar to those on Kerguelen, although we did not observe a clear distinction between long and short trips. Meal sizes increased with longer trips but did not differ between male birds and female birds. Thus, as on Kerguelen, male and female thin-billed prions on New Island contributed equally to chick provisioning. The proportion of short trips was comparable to those observed in a more favourable year, and was higher than those in a poor year, on Kerguelen. In order to avoid potential disturbance to the birds in the colony by frequent capture and handling, we used miniature radio-tags to record the presence of individuals in the colony and to evaluate the influence of transmitter load on the birds. Despite generally deteriorating conditions towards the end of the breeding season, chicks of tagged adults were fed normally, indicating that the method is adequate.     

Age- and task-dependent foraging gene expression in the bumblebee Bombus terrestris

In eusocial insects, the division of labor within a colony, based on either age or size, is correlated with a differential foraging (for) gene expression and PKG activity. This article presents in the first part a study on the for gene, encoding a cGMP-dependent protein kinase (PKG) in the bumblebee Bombus terrestris. Cloning of the open reading frame allowed phylogenetic tracing, which showed conservation of PKGs among social insects. Our results confirm the proposed role for PKGs in division of labor. Btfor gene expression is significantly higher in the larger foragers compared with the smaller sized nurses. More importantly, we discovered an age-related decrease in Btfor expression in both nursing and foraging bumblebees. We therefore speculate that the presence of BtFOR is required for correct adaptation to new external stimuli and rapid learning for foraging. In a second series of experiments, worker bumblebees of B. terrestris were treated with two insecticides imidacloprid and kinoprene, which have shown to cause impaired foraging behavior. Compared with controls, only the latter treatment resulted in a decreased Btfor expression, which concurs with a stimulation of ovarian growth and a shift in labor toward nest-related tasks. The data are discussed in relation to Btfor expression in the complex physiological event of foraging and side-effects by pesticides.     

Plastin and spectrin cooperate to stabilize the actomyosin cortex during cytokinesis

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An agent-based model to investigate the roles of attractive and repellent pheromones in ant decision making during foraging

Pharaoh's ants organise their foraging system using three types of trail pheromone. All previous foraging models based on specific ant foraging systems have assumed that only a single attractive pheromone is used. Here we present an agent-based model based on trail choice at a trail bifurcation within the foraging trail network of a Pharaoh's ant colony which includes both attractive (positive) and repellent (negative) trail pheromones. Experiments have previously shown that Pharaoh's ants use both types of pheromone. We investigate how the repellent pheromone affects trail choice and foraging success in our simulated foraging system. We find that both the repellent and attractive pheromones have a role in trail choice, and that the repellent pheromone prevents random fluctuations which could otherwise lead to a positive feedback loop causing the colony to concentrate its foraging on the unrewarding trail. An emergent feature of the model is a high level of variability in the level of repellent pheromone on the unrewarding branch. This is caused by the repellent pheromone exerting negative feedback on its own deposition. We also investigate the dynamic situation where the location of the food is changed after foraging trails are established. We find that the repellent pheromone has a key role in enabling the colony to refocus the foraging effort to the new location. Our results show that having a repellent pheromone is adaptive, as it increases the robustness and flexibility of the colony's overall foraging response.     

Patch choice from a distance and use of habitat information during foraging by the parasitoid Ibalia leucospoides

1. In environments in which resources are distributed heterogeneously, patch choice and the length of time spent on a patch by foragers are subject to strong selective pressures. This is particularly true for parasitoids because their host foraging success translates directly into individual fitness. 2. The aim of this study was to test whether: (i) females of the parasitoid Ibalia leucospoides (Hymenoptera: Ibaliidae) can discriminate among patches according to host numbers; (ii) the surrounding context affects the initial choice of patch, as well as time spent on patch; and (iii) the perceived quality of a given patch is affected by the quality of the surrounding patches. 3. Each female was randomly exposed to one of three different three‐patch environments which differed in host number per patch, mean environment host number and host distribution among patches. For each treatment level, the first patch chosen and the time allocated to each patch visited by the female were recorded. 4. Females of I. leucospoides were able to discriminate different levels of host numbers among patches from a distance. The patch bearing the highest number of hosts was, predominantly, the first choice. Patch host number in association with mean habitat profitability influenced the length of time spent on the first patch visited. By contrast, variance in habitat profitability did not influence time allocation decisions. Contrary to the study prediction, there were no significant habitat‐dependent time allocation differences among patches holding the same number of hosts. 5. The results indicate that, for I. leucospoides, patch exploitation decisions are partially influenced by information obtained from the habitat as a whole, a behaviour that may prove to indicate adaptive ability in highly patchy environments, as well as suggesting the presence of good cognitive abilities in this parasitoid species.     

Cutters,carriers and transport chains: Distance-dependent foraging strategies in the grass-cutting ant <Emphasis Type="Italic">Atta vollenweideri</Emphasis>

Summary Most studies on leaf-cutting ant foraging examined forest species that harvest dicot leaves. We investigated division of labor and task partitioning during foraging in the grass-cutting ant Atta vollenweideri. Workers of this species harvest grass fragments and transport them to the nest for distances up to 150 m along well-established trunk trails. We recorded the behavior of foraging ants while cutting and monitored the transport of individually-marked fragments from the cutting site until they reached the nest. A. vollenweideri foragers showed division of labor between cutting and carrying, with larger workers cutting the fragments, and smaller ones transporting them. This division was less marked when plants were located very close to the nest and no physical trail was present, i.e., the cutter often transported its own fragment back to the nest. On long foraging trails, the transport of fragments was a partitioned task, i.e., workers formed transport chains composed of 2 to 5 carriers. This sequential load transport occurred more often on long than on short trails. The first carriers in a transport chain covered only short distances before dropping their fragments, and they were observed to turn back and revisit the patch. The last carriers covered the longest distance. The probability of dropping the carried fragment on the trail was independent of both worker and fragment size, and there was no particular location on the trail for dropping, i.e., fragments were not cached. Transport time of fragments transported by a chain was longer than for those transported by single workers all the way to the nest, i.e., sequential transport did not save foraging time. Two hypotheses concerning the possible adaptive value of transport chains are discussed. The first one argues that sequential transport may lead to an increased material transport rate compared to individual transport. The second one considers sequential transport as a way to enhance the information flow among foragers, thus leading to a quicker build-up of workers at particular harvesting places. It is suggested that rather than increasing the gross transport rate of material, transport via chains may favor the transfer of information about the kind of resource being actually harvested.Received 19 December 2002; revised 14 March 2003; accepted 19 March 2003     

Cooperation during prey digestion between workers and larvae in the ant, Pheidole spadonia

Digestion and distribution of nutrients are central to the growth and reproduction of social insect colonies, just as they are to individual organisms. In the case of eusocial insect species, different components of food handling and processing can be distributed among castes. This paper reports on an ant species, Pheidole spadonia, in which the adult workers butcher prey and 4^th instar larvae dissolve prey for distribution among other colony members including workers, larvae and queens. To characterize the process, six groups, each composed of twenty-five workers and thirty larvae, were provisioned with a fruit fly carcass, and then video-taped continuously for 24 hours. On average, five adult workers and twenty-two 4^th instar larvae invested 12.8 labor hours into butchering and predigesting one fly carcass. Workers contributed a mean total of 3.3 labor hours to butcher the carcass into small fragments. Fourth instar larvae contributed a mean total of 9.5 labor hours to pre-orally dissolve the solid fragments. Surprisingly, larvae did not ingest during the dissolving process. Instead, workers ingested the dissolved prey tissue into their crops and then regurgitated it to colony members, larvae and workers, that solicited for feedings. The cooperative interactions reported here between workers and larvae extend the mechanistic and evolutionary explanations for eusociality. Received 13 January 2005; revised 22 April 2005; accepted 25 April 2005.     

Monogamy,strongly bonded groups,and the evolution of human social structure

Human social evolution has most often been treated in a piecemeal fashion, with studies focusing on the evolution of specific components of human society such as pair‐bonding, cooperative hunting, male provisioning, grandmothering, cooperative breeding, food sharing, male competition, male violence, sexual coercion, territoriality, and between‐group conflicts. Evolutionary models about any one of those components are usually concerned with two categories of questions, one relating to the origins of the component and the other to its impact on the evolution of human cognition and social life. Remarkably few studies have been concerned with the evolution of the entity that integrates all components, the human social system itself. That social system has as its core feature human social structure, which I define here as the common denominator of all human societies in terms of group composition, mating system, residence patterns, and kinship structures. The paucity of information on the evolution of human social structure poses substantial problems because that information is useful, if not essential, to assess both the origins and impact of any particular aspect of human society.     

Properties of food loads delivered to nestlings in the pied flycatcher: effects of clutch size manipulation, year, and sex

Experimental manipulation of the number of altricial offspring is supposed to modify parental expenditure in birds. In addition to the observed increase in parental feeding rate, it is also possible that the choice of prey or the size of load may change with the changing demand for food. Sexual differences in the provisioning response are also expected, on the basis of earlier studies. We examined the effect of brood size manipulation on choice of prey brought to nestlings and load size in the pied flycatcher. The composition and size of loads differed between years, possibly depending on varying availability of different prey types. Males responded to brood size enlargement by gathering heavier loads, whereas females showed no response. The alteration of load size in males was not explained by a larger number of prey items or mean prey size, but was a combination of these components. It is likely that males also increased their work rate in response to increased food demand at the nest. The absence of response in females might be because they are unable to increase work rate any further, or because food delivery rate in females can not be optimized by changing load properties. Received: 18 December 1997 / Accepted: 1 March 1998     

Worker Age, Ovary Development, and Temporal Polyethism in the Swarm-Founding Wasp Polybia occidentalis (Hymenoptera: Vespidae)

I measured oocyte sizes of Polybia occidentalis workers to assess whether ovary development corresponded with adult age or with individual variation in behavior. Workers exhibited temporal polyethism by first working inside the nest, then performing on-nest tasks, and later foraging and defending the nest. Individuals varied in their ages at first performance of each of these sets of behavioral acts. Ovary development corresponded strongly with adult age. Workers' ovaries declined quickly after an initial phase of partial development. The period of ovary decline overlapped with the age range at which most workers began performing tasks on the exterior nest surface. However, after accounting for age effects, individual behavioral differences (rate of temporal polyethism and performance of foraging and defense tasks) did not correspond with ovary development. These data suggest that ovary development had little or no effect on variation in task performance by P. occidentalis workers on the nest surface.     

Ovarian development and insulin-signaling pathways during reproductive differentiation in the queenless ponerine ant Diacamma sp.

In many social hymenopteran species, workers possess functional ovaries that are physiologically inactive in the presence of queens. We investigated the ovarian regulatory mechanism of workers and reproductives in a queenless ponerine ant, Diacamma sp., using histological and molecular techniques. In this ant, clear reproductive differentiation occurs via a highly sophisticated dominance behavioral interaction called “gemmae mutilation”. This clear and rapid bifurcation of reproductive physiology allows us to elucidate the detailed ovarian differentiation process. Histological characteristics of functional ovaries (fusomes and ring canals) were found in both workers and reproductives, suggesting that early oogenesis is not blocked in workers. Since insulin/insulin-like growth factor signaling (IIS) is known to control insect reproduction, orthologs of 2 positive IIS regulators, insulin receptor and serine-threonine kinase Akt (protein kinase B), were cloned in Diacamma (DiaInR, DiaAkt); their expression patterns during reproductive differentiation were examined by real-time quantitative polymerase chain reaction; DiaInR and DiaAkt were strongly expressed in the gasters of reproductives. Whole-mount in situ hybridization of ovaries indicated that DiaInR and DiaAkt were expressed in nurse cells, oocytes, and upper germarial regions of reproductives but not of workers. Our data suggest that the IIS pathway accounts for reproductive differentiation in late oogenesis.     

Age and ovarian development are related to worker personality and task allocation in the ant Leptothorax acervorum

In social insects, workers of different morphological castes and age are known to act differently. Yet, it is unclear how body size and ovarian development influence worker personalities （i.e. consistent behavioral variation） and task allocation in similar aged ant workers of monomorphic species. Behavioral variation is thought to be a key element of division of labor, but few studies have linked worker personality to task allocation. We investigated individual behavior in Leptothorax acervorum ant workers at two time points during the first three months of their life and in two different settings. We observed worker behavior in the nest （i.e. task allocation） and in standardized aggression, exploration and brood care experiments （i.e. personality） and found behavioral repeatability in foraging and exploration. Further, workers acted consistently across settings： workers with a more ag gressive and exploratory personality type were more active in the nest. Moreover, ovarian development was associated with worker personality and task allocation： older workers with welldeveloped ovaries foraged less, but were more aggressive and exploratory. In accordance with the typical agepolyethism of social insects, workers became more active and foraged more as they grew older. Consequently, our study suggests that task allocation in Leptothorax acervorum is not only influenced by ovari an development and age, but moreover by the personalities of its workers .     

Seasonality, division of labor, and dynamics of colony-level nutrient storage in the ant Pheidole morrisi

Nutritional provisioning is a critical component of life history strategies, and of particular interest in social insect colonies because of the role that division of labor plays in resource allocation. To explore the mechanisms that underlie colony nutritional strategies, I examined three populations of the ant Pheidole morrisi across a gradient of overwinter food scarcity over two seasons. P. morrisi colonies were found to employ amixed strategy of fat storage with regard to a longer overwinter period: members of both worker castes increase their percent-fat in a graded manner, while the proportion of a specialized subcaste of majors known as “repletes”, also increased within the colony. Geographic variation in other colony traits such as mean colony size, mean worker size, and minor/major caste ratio were also found, although not always in a manner clearly relating to fat storage. These results indicate that colony demography responds to seasonal fluctuations in food availability through behavioral alterations (increased fat stores and recruitment of replete workers) rather than physical alterations (changes in lean body sizes or caste ratio). The findings illustrate the dynamic role division of labor plays in the success of insect colonies confronting environmental variability. Received 9 May 2006; revised 19 July 2006; accepted 24 July 2006.     

Light exposure leads to reorganization of microglomeruli in the mushroom bodies and influences juvenile hormone levels in the honeybee

Honeybees show a remarkable behavioral plasticity at the transition from nursing inside the hive to foraging for nectar and/or pollen outside. This plasticity is important for age‐related division of labor in honeybee colonies. The behavioral transition is associated with significant volume and synaptic changes in the mushroom bodies (MBs), brain centers for sensory integration, learning, and memory. We tested whether precocious sensory exposure to light leads to changes in the density of synaptic complexes [microglomeruli (MG)] in the MBs. The results show that exposure to light pulses over 3 days induces a significant decrease in the MG density in visual subregions (collar) of the MB. Earlier studies had shown that foragers have increased levels of juvenile hormone (JH) co‐occurring with a decrease of vitellogenin (Vg). Previous work further established that RNAi‐mediated knockdown of vg and ultraspiracle (usp) induced an upregulation of JH levels, which can lead to precocious foraging. By disturbing both Vg and JH pathways using gene knockdown of vg and usp, we tested whether the changes in the hormonal system directly affect MG densities. Our study shows that MG numbers remained unchanged when Vg and JH pathways were perturbed, suggesting no direct hormonal influences on MG densities. However, mass spectrometry detection of JH revealed that precocious light exposure triggered an increase in JH levels in the hemolymph (HL) of young bees. This suggests a dual effect following light exposure via direct effects on MG reorganization in the MB calyx and a possible positive feedback on HL JH levels. © 2014 Wiley Periodicals, Inc. Develop Neurobiol 74: 1141–1153, 2014     

Task-Matching and Short-Term Size Shifts in Foragers of the Harvester Ant, Messor pergandei (Hymenoptera: Formicidae)

Some social insects produce workers of variable size and/or shape. One hypothesis to explain such variation is that it increases colony efficiency in performing diverse tasks, with greater efficiency leading to greater colony-level fitness. Using the granivorous ant Messor pergandei, which produces a unimodal distribution of worker sizes, I explored two corollaries of this ergonomic hypothesis: that there should be detectable task-matching and that the mean size should shift predictably with a change in task. In five experiments conducted in different years and sites in California deserts, colonies were baited with fragments of wheat or millet ground and sieved to different sizes. In six of eight colonies so baited the minimum linear dimension or mass of seeds carried by foragers was significantly related to forager size, with r² values ranging from 3 to 30%. In four of the five experiments, colonies were subsequently baited with either large seed fragments alone or small fragments alone. In three of these four experiments I detected a rapid response, over a few hours or days, in which foragers deployed by colonies shifted to larger or smaller mean size in directions predicted by size of the bait. These results suggest that an ergonomic function is one contributor to worker size polymorphism in M. pergandei. Although task-matching did not explain a substantial amount of the variance in forager size in all experiments, the rapid size shifts provide behavioral evidence that task-matching is important to colonies.     

Immunologic,genetic and social human risk factors associated to histoplasmosis: Studies in the State of Guerrero,Mexico

Immunologic and occupational aspects of the susceptible population exposed to Histoplasma capsulatum, the causative agent of histoplasmosis were analyzed in the Mexican State of Guerrero. Three areas were studied, Juxtlahuaca, Olinala, and Coyuca; in the first two, their populations refer contact with bat guano and/or avian excreta, which contain nutrients for fungal growth, while the Coyuca population referred no contact with the above mentioned excreta. Previous infection with H. capsulatum was determined by histoplasmin-skin test, and the response was higher in men than in women (93.87, 85.71, and 6.6% for men, and 78.94, 66.6, and 0% for women) in Juxtlahuaca, Olinala, and Coyuca, respectively. Labor activities related to a persistent contact with the fungus were considered as an occupational risk factor, histoplasmin-skin test reached 88.57 and 36.36% of positive response in individuals with high and low risk activities. A high percentage of histoplasmin responses was observed in subjects with constant contact with H. capsulatum, such as, cave-tourist guides, peasants, and game-cock handlers, and generally they developed the largest diameter of skin reactions. Genetic risk factor was determined by studying the gene frequency of the Major Histocompatibility Complex antigens in a sample of individuals and their first degree relatives in Juxtlahuaca, Olinala, and Coyuca. Significant differences were found for HLA-B22 and B17 antigens in Juxtlahuaca, and for HLA-B22 in Olinala, in comparison to the usual gene frequency observed in the normal Mexican population. HLA results were important, considering that HLA-B22 was previously found to be possibly related to pulmonary histoplasmosis in Guerrero. This revised version was published online in June 2006 with corrections to the Cover Date.