Insights into the molecular basis of social behaviour from studies on the honeybee, <Emphasis Type="Italic">Apis mellifera</Emphasis>

The honeybee, Apis mellifera, has been the most important insect species for the study of social behaviour. With the recent release of its genome sequence, the honeybee has emerged as an excellent model for molecular studies of social behaviour. A key feature of eusocial species is a complex division of labour. Adult honeybees perform a series of tasks in the hive when they are young and then shift to foraging for nectar or pollen outside the hive when they are 2–3 weeks of age. This transition from working in the hive to foraging involves changes in the expression of thousands of genes. In this review, we focus first on recent advances in understanding of the widespread changes in gene activity that accompany the transition to foraging. Thereafter, we examine three genes in particular, foraging, malvolio and vitellogenin, all implicated in this striking behavioural change in the life of the honeybee.     

Use of Social and Ecological Information in Tamarin Foraging Decisions

A major consequence of group living is that foragers may rely on social information in addition to ecological information to locate feeding sites. Although conspecifics can provide cues as to the spatial location of food patches, individual foraging decisions also must include some assessment of the likelihood of obtaining access to a resource other group members seek. This likelihood differs in the 2 models generally proposed to explain intragroup social foraging: the information-sharing model and the producer-scrounger model. We conducted an experimental field study on wild groups of emperor (Saguinus imperator) and saddleback (S. fuscicollis) tamarins to determine the foraging strategies adopted by individual group members and their relationship to social rank, food intake, and the ability to use ecological and social information in making intra-patch foraging decisions. Individual tamarins applied different behavioral strategies compatible with a finder-joiner paradigm to solve foraging problems. About half of the individuals in each study group initiated 74%–90% of all food searches and acted as finders. Most alpha individuals adopted a joiner strategy by monitoring the activities of others' to obtain a reward. The individual arriving first at a reward platform enjoyed a finder's advantage. Despite differences in search effort, both finders and joiners presented similar abilities in learning to associate ecological cues with the presence of food rewards at our experimental feeding stations. We conclude that within a group foraging context, tamarins integrate social and ecological information in decision-making.     

Social implications of gummivory in marmosets

Gummivory or exudate feeding is a major dietary specialization which has received relatively little attention in the literature. While plant exudates contribute to the diet of many primate species, we suggest that the callitrichid species Cebuella pygmaea and Callithrix jacchus are obligate exudate feeders under free-ranging conditions. Callithrix jacchus provides an excellent model for examining the effects of exudate feeding and foraging upon social behavior, since other callitrichid species of similar body size do not share this dietary specialization. We review the effects of exudate foraging on specific social behaviors observed both in field and laboratory populations of C. jacchus. By comparing this species to closely related species, exudate foraging is seen to (1) be retained under laboratory conditions, (2) increase the frequency of territorial marking behavior while decreasing the frequency of overt aggression in males, (3) decrease the duration of infant care, and (4) increase the number of nonadults in social groups but not affect group size. The evidence presented supports the hypothesis that the consequences of exudate foraging in C. jacchus are fundamental and socially complex. © 1994 Wiley-Liss, Inc.     

Molecular and spatial analyses reveal links between colony‐specific foraging distance and landscape‐level resource availability in two bumblebee species

Foraging distance is a key determinant of colony survival and pollination potential in bumblebees Bombus spp. However this aspect of bumblebee ecology is poorly understood because of the difficulty in locating colonies of these central place foragers. Here, we used a combination of molecular microsatellite analyses, remote sensing and spatial analyses using kernel density estimates to estimate nest location and foraging distances for a large number of wild colonies of two species, and related these to the distribution of foraging habitats across an experimentally manipulated landscape. Mean foraging distances were 755 m for Bombus lapidarius and 775 m for B. pascuorum (using our most conservative estimation method). Colony‐specific foraging distances of both species varied with landscape structure, decreasing as the proportion of foraging habitats increased. This is the first time that foraging distance in wild bumblebees has been shown to vary with resource availability. Our method offers a means of estimating foraging distances in social insects, and informs the scale of management required to conserve bumblebee populations and enhance their pollination services across different landscapes.     

Observations on the activity patterns and social interactions of a captive group of blackcapped or brown capuchin monkeys (Cebus apella)

Studies were conducted on a captive group of 16 blackcapped capuchin monkeys (Cebus apella), with observations being carried out for a total of 75 hr over a 6 month period. Records were kept of their activities and spatial distribution according to weather type and time of day. Evidence of a social hierarchy was sought and was characterized primarily by the stability of the environment in which the animals live, dominance playing little part. The behaviour of the blackcapped capuchin has been studied previously in captivity (Dobruruka, 1972;Weigel, 1979); this study is, however, unique in that the troop under observation enjoys more freedom. Weather had no effect on the rank order of behavioural activities but did affect both activity levels and distribution of individuals. TheCebus apella troop spent around 50% of its active time foraging and eating, 7–10% of this time walking and around 30% of the time inactive. These values lie between those reported for caged and wild animals. Social interactions contributed more than 10% of the time budget, which is greater than wild populations. The study here thus provides an interesting link between information collected from wildCebus apella populations and that from rather more restricted troops.     

Behavioral suites mediate group-level foraging dynamics in communities of tropical stingless bees

Competition for floral resources is a key force shaping pollinator communities, particularly among social bees. The ability of social bees to recruit nestmates for group foraging is hypothesized to be a major factor in their ability to dominate rich resources such as mass-flowering trees. We tested the role of group foraging in attaining dominance by stingless bees, eusocial tropical pollinators that exhibit high diversity in foraging strategies. We provide the first experimental evidence that meliponine group foraging strategies, large colony sizes and aggressive behavior form a suite of traits that enable colonies to improve dominance of rich resources. Using a diverse assemblage of Brazilian stingless bee species and an array of artificial “flowers” that provided a sucrose reward, we compared species’ dominance and visitation under unrestricted foraging conditions and with experimental removal of group-foraging species. Dominance does not vary with individual body size, but rather with foraging group size. Species that recruit larger numbers of nestmates (Scaptotrigona aff. depilis, Trigona hyalinata, Trigona spinipes) dominated both numerically (high local abundance) and behaviorally (controlling feeders). Removal of group-foraging species increased feeding opportunities for solitary foragers (Frieseomelitta varia, Melipona quadrifasciata and Nannotrigona testaceicornis). Trigona hyalinata always dominated under unrestricted conditions. When this species was removed, T. spinipes or S. aff. depilis controlled feeders and limited visitation by solitary-foraging species. Because bee foraging patterns determine plant pollination success, understanding the forces that shape these patterns is crucial to ensuring pollination of both crops and natural areas in the face of current pollinator declines.     

Ecological Differences in Social Learning between Adjacent,Mixing, Populations of Zenaida Doves

In Zenaida doves, Zenaida aurita, of Barbados, previous work has shown that social learning is associated with foraging ecology in the field: in captive experiments, group-foraging birds learn more readily from a conspecific tutor, while territorial birds learn from the heterospecific they most often feed with in mixed-species aggregations, the Carib grackle, Quiscalus lugubris. This study examines foraging ecology and social learning in a dove population that experiences both territorial defence and occasional group feeding, Brandon's Beach. In part I, we document the dual foraging pattern seen in this population, which lives only a few hundred metres from the group-foraging harbour population studied in previous work. In part II, we show that doves from Brandon's Beach, consistent with their dual foraging experience, learn as readily from a conspecific as they do from a heterospecific tutor; control doves from the adjacent harbour site learn primarily from a conspecific tutor. Field sightings of banded individuals caught at the harbour and Brandon's show strong site fidelity, but sufficient movement between areas (4%) to make reproductive divergence between the two neighbouring populations highly unlikely, suggesting that social learning differences between them are non-genetic.     

Advantages of social foraging in crab spiders: Groups capture more and larger prey despite the absence of a web

Among group‐living spiders, subsocial representatives in the family of crab spiders (Thomisidae) are a special case, as they build protective communal leaf nests instead of extensive communal capture webs. It could thus be inferred that antipredator benefits (e.g., enhanced protection in larger nests) rather than foraging‐related advantages (e.g., capture of more and larger prey) promote sociality in this family. Nonetheless, subsocial crab spiders do share prey, and if this behaviour does not reflect mere food scramble but has a cooperative character, crab spiders may offer insights into the evolution of social foraging applicable to many other cooperative predators that hunt without traps. Here, we performed a comparative laboratory feeding experiment on three of the four subsocial crab spider species—Australomisidia ergandros, Australomisidia socialis and Xysticus bimaculatus—to determine if crab spiders derive advantages from foraging in groups. In particular, we tested artificially composed groups of five sibling spiderlings vs. single siblings in terms of prey capture success and prey size preference. Across species, groups had higher prey capture success (measured in terms of capture rates and capture latency) and were more likely to attack large, sharable prey—dynamics leading to reduced food competition among group members in favour of living and foraging in groups. Within groups, we further compared prey extraction efficiency among the three applied social foraging tactics: producing, scrounging and feeding alone. In A. ergandros, individuals were exceptionally efficient when using the non‐cooperative scrounger tactic, which entails feeding on the prey provided by others. Thus, our multispecies comparison confirms foraging advantages in maintaining a cooperative lifestyle for crab spiders, but also demonstrates the relevance of research into exploitation of cooperative foraging in this family.     

The allometry of echolocation call frequencies of insectivorous bats: why do some species deviate from the pattern?

The peak echolocation frequency of insectivorous bats generally declines as body size increases. However, there are notable exceptions to this rule, with some species, such as Rhinolophus clivosus, having a higher than expected peak frequency for their body size. Such deviations from allometry may be associated with partitioning of foraging habitat (the foraging habitat hypothesis) or insect prey (the prey detection hypothesis). Alternatively, the deviations may be associated with the partitioning of sonar frequency bands to allow effective communication in a social context (the acoustic communication hypothesis). We tested the predictions of these hypotheses through comparisons at the family, clade and species level, using species of rhinolophids in general and R. clivosus, a species with a wide distribution, as a specific test case. We compared the wing parameters, echolocation frequency and ecology of R. clivosus to those of the sympatric R. capensis. Rhinolophus clivosus has a much higher echolocation frequency than predicted from its wing loading or body mass. Furthermore, contrary to the predictions of the foraging habitat hypothesis, we found no difference in foraging habitat between R. clivosus and R. capensis. The size range of insect prey taken by the two species also overlapped almost completely, contrary to the prey detection hypothesis. On the other hand, the variation of echolocation frequencies around the allometric relationship for rhinolophids was smaller than that for Myotis spp., supporting the prediction of the acoustic communication hypothesis. We thus propose that the relatively high peak frequency of R. clivosus is the result of partitioning of sonar frequency bands to minimize the ambiguity of echolocation calls during social interactions.     

Comparative proteomics reveal characteristics of life-history transitions in a social insect

Background  

Honey bee (Apis mellifera) workers are characterized by complex social behavior. Their life-history is dominated by a period of within-nest activity followed by a phase of long-distance flights and foraging. General insights into insect metabolism imply that foraging onset is associated with fundamental metabolic changes, and theory on social evolution suggests metabolic adaptations that are advantageous for the colony as a whole.     

Individual foraging in the antPachycondyla apicalis

Summary A model of individual foraging in social insects as presented that formalises the dynamics of foraging and concentrates on the collective rather than the individual benefit, quantifying the relationships between a colony's foraging area, number of foragers and foraging energy budget and the food sources' rate of arrival, disappearance and capture. A series of experiments, in which a number of prey were offered to colonies of the individually foraging antPachycondyla (ex-Neoponera) apicalis confirm the hypotheses implicit in the model and measured the rates of capture and competition. 60 days observation of 3P. apicalis colonies' foraging activity are summarised and used in conjunction with the model to obtain estimations of the density and rate of arrival of available prey in the foraging area. We examine how a colony's foraging benefit may be influenced by its foraging area, the number of foragers, and the forager/non-forager ratio and show that a colony's jocial structure strongly limits its potential foraging benefit. Within these limits,P. apicalis does not appear to be an optimal forager.     

Social and foraging components of the home range in Antechinus stuartii (Dasyuridae: Marsupialia)

The home range of Antechinus stuartii has two components. A small area (0.94 ha for males, 0.38 ha for females) is used for foraging, while a much greater social range (mean for males in a given year may exeed 5 ha; the mean for females never exceeded 3 ha) encompasses communal nests, which are used by both males and females. The foraging range of females is stable throughout the year. The foraging range may not coincide at all, or only partially coincide with her social range. By contrast, male foraging ranges drift through the year, and generally lie within their social range. Intersexual differences reflect the different selection pressures on the sexes. Females require access to resources to sustain a costly lactation, while males require a knowledge of many possible sites for mating and early resolution of agonistic interactions with other males with which they cohabit during mating.     

Intragroup competition predicts individual foraging specialisation in a group‐living mammal

Individual foraging specialisation has important ecological implications, but its causes in group‐living species are unclear. One of the major consequences of group living is increased intragroup competition for resources. Foraging theory predicts that with increased competition, individuals should add new prey items to their diet, widening their foraging niche (‘optimal foraging hypothesis’). However, classic competition theory suggests the opposite: that increased competition leads to niche partitioning and greater individual foraging specialisation (‘niche partitioning hypothesis’). We tested these opposing predictions in wild, group‐living banded mongooses (Mungos mungo), using stable isotope analysis of banded mongoose whiskers to quantify individual and group foraging niche. Individual foraging niche size declined with increasing group size, despite all groups having a similar overall niche size. Our findings support the prediction that competition promotes niche partitioning within social groups and suggest that individual foraging specialisation may play an important role in the formation of stable social groupings.     

河南民权湿地公园青头潜鸭越冬行为模式及性别差异

为了更深入地了解青头潜鸭的越冬行为模式及性别差异,以期为后续青头潜鸭的保护管理提供科学的理论参考,2018年11-12月采用定点观察法、扫描取样法等方法,对河南民权国家湿地公园越冬期青头潜鸭的越冬行为模式及性别差异进行了观察分析。观察期间共记录到青头潜鸭158只,超过全球种群数量1000只的10%。分析结果表明：（1）民权湿地公园,青头潜鸭越冬期行为时间分配以静息、觅食和运动三类行为为主,其次是修整和飞行两类行为;运动行为与觅食、修整、社会等行为之间呈极显著正相关,修整行为与社会行为之间呈极显著正相关,静息行为与修整、运动、社会等行为之间呈极显著负相关,飞行行为与觅食、静息、修整等行为之间呈极显著负相关;（2）静息行为具有全时段高时间分配的特征,不存在峰期和谷期;觅食行为（峰期为10：30-11：30、13：30-14：30,谷期为11：30-12：30、14：30-15：30）和飞行行为（峰期为11：30-12：30、14：30-15：30,谷期为10：30-11：30、13：30-14：30、15：30-16：30）具有明显的错峰式节律;（3）不同性别青头潜鸭越冬行为时间分配存有差异,其中静息、觅食、运动是雄性青头潜鸭主要行为类别（超过70%）,雌性青头潜鸭的主要行为为运动、飞行、觅食（接近70%）;雌雄青头潜鸭在静息、修整、运动和飞行四类行为时间分配方面存在显著性差异,雄性的静息、修整行为的时间分配极显著高于雌性,而运动、飞行行为的时间分配极显著低于雌性;（4）不同性别青头潜鸭越冬行为活动节律方面,除飞行行为外,其余行为均在行为峰期与谷期节律方面存有差异。进一步分析表明：民权湿地公园青头潜鸭越冬行为模式符合行为投资与收益的能量学理论,越冬行为模式在行为时间分配和行为节律方面存在性别差异。     

Colony‐level behavioural variation correlates with differences in expression of the foraging gene in red imported fire ants

Among social insects, colony‐level variation is likely to be widespread and has significant ecological consequences. Very few studies, however, have documented how genetic factors relate to behaviour at the colony level. Differences in expression of the foraging gene have been associated with differences in foraging and activity of a wide variety of organisms. We quantified expression of the red imported fire ant foraging gene (sifor) in workers from 21 colonies collected across the natural range of Texas fire ant populations, but maintained under standardized, environmentally controlled conditions. Colonies varied significantly in their behaviour. The most active colonies had up to 10 times more active foragers than the least active colony and more than 16 times as many workers outside the nest. Expression differences among colonies correlated with this colony‐level behavioural variation. Colonies with higher sifor expression in foragers had, on average, significantly higher foraging activity, exploratory activity and recruitment to nectar than colonies with lower expression. Expression of sifor was also strongly correlated with worker task (foraging vs. working in the interior of the nest). These results provide insight into the genetic and physiological processes underlying collective differences in social behaviour. Quantifying variation in expression of the foraging gene may provide an important tool for understanding and predicting the ecological consequences of colony‐level behavioural variation.     

Temperature and the pollinating activity of social bees

Abstract.

• 1 Thermal constraints on flight acivity limit the pollinating effectiveness of bees. Each species of social bee has a microclimatic ‘window’ within which foraging flight can be sustained.
• 2 To predict whether a given species of social bee is worth testing as a pollinator in a given climate, it is useful to know at least the lower limits of that microclimatic ‘window’. We consider how information from a series of bee counts through a day can be used to characterize a bee species in terms of activity/microclimate relations as a basis for predicting the diel pattern of foraging activity of a bee introduced into a new climate as a pollinator.
• 3 We discuss the relative merits of bee counts at a foraging patch and counts based on hive traffic as indices of the proportion of bees active.
• 4 We suggest that the activity/microclimate relations of a species be expressed in terms of the lower threshold black globe temperature for flight activity. Black globe temperature, T_g, is easily measured with inexpensive equipment, and can substitute for measurements of ambient temperature and radiation as a predictor of diel patterns of bee activity.
• 5 We use examples of field data to explore the relationship between microclimate and activity for the honeybee Apis mellifera and several species of bumblebee, Bombus. Regression analysis is used to relate activity to T_g and to identify the lower temperature threshold for activity from field bee counts.
• 6 In field studies analysed here, the bumblebees Bombus terrestrisllucorum, B.pascuorum and B.hortorum began foraging at lower temperatures than honey-bees or B.lapidarius.

     

Influence of environmental and colony factors on the initial commodity choice of foragers of the stingless bee Plebeia tobagoensis (Hymenoptera, Meliponini)

Novice foragers of social bees have to decide what food commodity to collect when they start foraging for the first time. In this decision making process two types of factors are involved: internal factors (the response threshold) and external factors (environmental and colony conditions). In this study we will focus on the importance of two external factors, pollen storage level and information from experienced foragers about food availability in the field, on the initial commodity choice of foragers of the stingless bee species Plebeia tobagoensis. We also studied the effect of the initial choice of individuals on their subsequent foraging career. This study was performed in a closed greenhouse compartment, where food availability and colony condition could be controlled. Information on food availability in the field from experienced foragers and pollen storage level both greatly influenced the initial commodity choice of individuals, with more choices for the commodity communicated by experienced foragers or lacking in storage. The initial choice of foragers is of importance for their future foraging career, although a substantial proportion of foragers did switch between food commodities. Because of the ability of novice foragers to become flexibly distributed over foraging tasks, social bees are able to react to changes in their environment without directly having to decrease foraging effort devoted to other foraging tasks. This, in combination with individual flexibility during foraging careers makes it possible for colonies of P. tobagoensis to forage efficiently in an ever-changing environment. Received 7 November 2005; revised 12 January 2006; accepted 16 February 2006.     

Social facilitation does not reduce neophobia in Chestnut-sided Warblers (Parulinae:Dendroica pensylvanica)

Chestnut-sided Warblers (Dendroica pensylvanica) show aversion to feeding at a familiar food source if placed next to a novel object. I have suggested that neophobia is an adaptation of specialized animals to reduce wasteful exploration. In this experiment I tested whether social facilitation mitigates the fear and decreases the latency to forage at a novel foraging site. As far as I know, the effect of social factors on neophobia has not been previously investigated. Because Chestnut-sided Warblers are intraspecifically solitary during the non-breeding season, I examined their response to novel foraging sites in the presence of a Bay-breasted Warbler (D. castanea) “trainer”. Chestnut-sided Warblers commonly join flocks with this more generalized and less neophobic congener. Chestnut-sided Warblers showed no tendency to feed in the presence of a Bay-breasted Warbler that is freely feeding from the unfamiliar microhabitat. Specialized animals may be more resistant to social facilitation and observational learning than more generalized species.     

Individual forager profits in Apis mellifera unaffected by a range of colony Varroa destructor densities

The parasitic mite Varroa destructor Anderson and Trueman negatively affects honey bee health, flight activity, and foraging behavior, all of which can be expected to affect foraging energetics. We tested this hypothesis in a 3-year field study. In each year, four-frame nucleus colonies with varying loads of varroa were placed under cages with mature rabbiteye blueberry plants, Vaccinium ashei. Individual bee weights consistently decreased as colony varroa populations increased, affirming that the design produced a range of colony mite effects. However, average forager flower handling times and nectar ingestion rates were unaffected by changes in colony varroa levels. Moreover, there were no significant effects of colony varroa levels on individual net foraging energy gain determined per flower, per second handling time, or per second total foraging time. We conclude that individual forager profits in Apis mellifera are unaffected by the range of colony V. destructor densities used in this study. These results are relevant to the question of the extent to which foraging of individuals relates to colony state in social Hymenoptera.     

Location effects of social partner on experimental foraging in the squirrel monkey

The effect of social context on experimental foraging in squirrel monkeys (Saimiri sciureus) was investigated. The 12 subjects comprised six pairs in which strong social preference and attraction had been demonstrated during observations of a stable group. Individuals were first trained to discriminate spatially separated rich and poor foraging bins containing 75% and 25% of the food items, respectively, with their partners restrained equidistant from the two bins. The monkeys invested an average of 75.5% of their foraging time in the rich bin. Each individual was then tested with its partner restrained in different locations relative to the bins to determine the effect of partner proximity on foraging patterns. Foraging efficiency at the start of a session was enhanced when the partner was restrained adjacent to the rich bin compared to restraint away from this bin. Over an entire foraging session, however, all conditions providing partner accessibility were similar in yielding enhanced foraging efficiency compared to partner absence. Little time was spent in close physical proximity to the partner under any condition. It is suggested that accessibility of the social partner, rather than close physical proximity, has an important influence on the foraging squirrel monkey. © 1995 Wiley-Liss, Inc.