Collective control of nest climate parameters in bumblebee colonies

We examined two aspects of the social control of nest climate in bumblebee colonies: which parameters of nest climate bumblebees actively down-regulate by fanning and the dynamics of the colony response as colony size increased. Colonies of Bombus terrestris were exposed to an increase in carbon dioxide, temperature or relative humidity. We performed 70 temperature trials (six colonies), 58 CO₂ trials (four colonies) and four humidity trials (two colonies). An increase in CO₂ concentration and temperature elicited a fanning response whereas an increase in relative humidity did not. This is the first report of fanning in bumblebee colonies to control respiratory gases. The number of fanning bees increased with stimulus intensity. The colony response to a CO₂ concentration of 3.2% was comparable to the colony response to a temperature of 30°C. A marked fanning response occurred at 1.6% CO₂, a concentration never exceeded in a large field nest during a pilot measurement of 10 days. We investigated the colony response over a wide range of colony sizes (between 10 and 119 workers). The proportion of the total workforce invested by colonies in nest ventilation did not change significantly; thus, the number of fanning workers increased with colony size. Furthermore, as colony size increased, the dynamics of the colony response changed: colonies responded faster to perturbations of their environment when they were large (60 or more individuals) than when they were small. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The role of genetic diversity in nest cooling in a wild honey bee, Apis florea

Simulation studies of the task threshold model for task allocation in social insect colonies suggest that nest temperature homeostasis is enhanced if workers have slightly different thresholds for engaging in tasks related to nest thermoregulation. Genetic variance in task thresholds is one way a distribution of task thresholds can be generated. Apis mellifera colonies with large genetic diversity are able to maintain more stable brood nest temperatures than colonies that are genetically uniform. If this phenomenon is generalizable to other species, we would predict that patrilines should vary in the threshold in which they engage in thermoregulatory tasks. We exposed A. florea colonies to different temperatures experimentally, and retrieved fanning workers at these different temperatures. In many cases we found statistically significant differences in the proportion of fanning workers of different patrilines at different experimental temperatures. This suggests that genetically different workers have different thresholds for performing the thermoregulatory task of fanning. We suggest, therefore, that genetically based variance in task threshold is a widespread phenomenon in the genus Apis.     

Thresholds of Response in Nest Thermoregulation by Worker Bumble Bees, Bombus bifarius nearcticus (Hymenoptera: Apidae)

Regulation of nest temperature is important to the fitness of eusocial insect colonies. To maintain appropriate conditions for the developing brood, workers must exhibit thermoregulatory responses to ambient temperature. Because nest-mate workers differ in task performance, thermoregulatory behavior provides an opportunity to test threshold of response models for the regulation of division of labor. We found that worker bumble bees ( Bombus bifarius nearcticus ) responded to changes in ambient temperature by altering their rates of performing two tasks – wing fanning and brood cell incubation. At the colony level, the rate of incubating decreased, and the rate of fanning increased, with increasing temperature. Changes in the number of workers performing these tasks were more important to the colony response than changes in workers' task performance rates. At the individual level, workers' lifetime rates of incubation and fanning were positively correlated, and most individuals did not specialize exclusively on either of these temperature-sensitive tasks. However, workers differed in the maximum temperature at which they incubated and in the minimum temperature at which they fanned. More individuals fanned at high and incubated at low temperatures. Most of the workers that began incubating at higher temperatures continued performing this task at lower temperatures, when additional nest-mates became active. The converse was true for fanning behavior. These data are consistent with a threshold of response model for thermoregulatory behavior of B. bifarius workers.     

Ventilation response thresholds do not change with age or self-reinforcement in workers of the bumble bee Bombus impatiens

The response threshold model is a potential mechanism for task allocation in social insects, and it assumes that workers vary in the levels of task stimuli to which they respond. Furthermore, response thresholds of individual workers may change over time through self-reinforcement (experience), such that workers become more sensitive to task stimuli. However, in addition to self-reinforcement, aging is another process that occurs through time. Distinguishing whether response thresholds change within workers due to self-reinforcement or aging may give insight into the flexibility of this task allocation mechanism. Using a ventilation paradigm, we manipulated workers of Bombus impatiens to have either repeated or lack of exposures to increases in nest air temperature, thereby allowing us to manipulate experience and thus self-reinforcement. Nest air temperature was the task stimulus, and ventilation (fanning) was the behavioral response. We found that ventilation response thresholds do not decrease either with age or experience in workers of B. impatiens, contrary to what has been reported for B. terrestris workers (Weidenmüller, 2004). Instead, we found high levels of intra-individual variation in response thresholds. Our results also show that workers with lower average response thresholds respond to heating events with higher probability than those with higher ventilation thresholds. These results provide insight into the role of the response threshold framework for task allocation; we also discuss how response probabilities may play a role in task allocation among workers.     

Colony size affects collective decision-making in the ant Temnothorax albipennis

Social insects are well-known for their ability to achieve robust collective behaviours even when individuals have limited information. It is often assumed that such behaviours rely on very large group sizes, but many insect colonies start out with only a few workers. Here we investigate the influence of colony size on collective decision-making in the house-hunting of the ant Temnothorax albipennis. In experiments where colony size was manipulated by splitting colonies, we show that worker number has an influence on the speed with which colonies discover new nest sites, but not on the time needed to make a decision (achieve a quorum threshold) or total emigration time. This occurred because split colonies adopted a lower quorum threshold, in fact they adopted the same threshold in proportion to their size as full-size colonies. This indicates that ants may be measuring relative quorum, i.e. population in the new nest relative to that of the old nest, rather than the absolute number. Experimentally reduced colonies also seemed to gain more from experience through repeated emigrations, as they could then reduce nest discovery times to those of larger colonies. In colonies of different sizes collected from the field, total emigration time was also not correlated with colony size. However, quorum threshold was not correlated with colony size, meaning that individuals in larger colonies adopted relatively lower quorum thresholds. Since this is a different result to that from size-manipulated colonies, it strongly suggests that the differences between natural small and large colonies were not caused by worker number alone. Individual ants may have adjusted their behaviour to their colony’s size, or other factors may correlate with colony size in the field. Our study thus shows the importance of experimentally manipulating colony size if the effect of worker number on the emergence of collective behaviour is to be studied. Received 13 December 2005; revised 9 May 2006; accepted 15 May 2006.     

Responses to CO2 Enrichment by Two Genotypes of Arabidopsis thaliana Differing in their Sensitivity to Nutrient Availability

The responses of two genotypes of Arabidopsis thaliana, whichdiffer in their sensitivities to nutrients to present and predictedfuture CO₂ concentration were determined under rich vs. poornutrient regimes on the basis of both single traits and thewhole plant. Based on individual traits, the two genotypes respondedsimilarly to CO₂ enrichment for all the traits measured exceptfor rate of increase in crown diameter, for which a decreasewas observed in the less nutrient-sensitive genotype grown atincreased CO₂. Based on the overall response of the whole plant,by analysing groups of plant traits using multivariate analysis,the two genotypes differed substantially from one another andboth responded more strongly to nutrient availability than toCO₂ concentration, especially for traits measured at harvestthat related to reproductive fitness. The less nutrient-sensitivegenotype also showed a weaker overall response to CO₂, and thepattern of the overall response was strikingly similar at differentnutrient supply. In contrast, the more nutrient-sensitive genotyperesponded more strongly to CO₂ than the less nutrient-sensitivegenotype, and responded differently to CO₂ at low vs. high nutrientavailability.Copyright 1995, 1999 Academic Press Plasticity, CO₂ enrichment, nutrient status, nutrient x CO₂ interaction, Arabidopsis thaliana, canonical analysis     

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens. Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.     

Genetic effects on task performance,but not on age polyethism,in a swarm-founding eusocial wasp

Division of labour among workers in insect societies often includes two major components: age-related changes in behaviour (age polyethism) and specialization in task performance. The aim of this study was to test whether similarity in inside-nest task performance and in rate of age polyethism correspond to genetic similarity among nestmates in the polygynous eusocial waspPolybia aequatorialis.Behavioural data were collected on marked, known-age workers from three source colonies introduced into two observation colonies in the field. Genetic similarity among workers was assessed by quantifying sharing of random amplified polymorphic DNA (RAPD) marker alleles. Workers were categorized by whether they engaged in nest cleaning as an indicator of individual differences in inside-nest task performance. Within source colonies, workers that performed nest-cleaning tasks were more genetically similar to each other than they were to workers not performing these tasks. Workers also differed in their rates of passage through the age-related task sequence, but no association was found between sharing of RAPD marker alleles and rate of age polyethism. These results accord with earlier studies demonstrating flexibility in age polyethism in swarm-founding wasps, and with findings that worker genotypic variability corresponds to specialization in task performance inP. aequatorialis. Polybiaspp. workers rarely switch among tasks, even in response to changes in colony conditions, and workers’ genotypes may constrain flexibility in task performance at the individual level. Conversely, colonies may accrue benefits from having genotypically diverse worker forces, which could favour the maintenance of polygyny in swarm-founding wasps.     

Atmospheric carbon dioxide regulation in honey-bee (Apis mellifera) colonies

Carbon dioxide releases fanning behaviour in the honey-bee. The response is proportional to the atmospheric CO₂ level within the nest and regulates the atmospheric CO₂ concentration between 0·10 and 4·25 per cent in small colonies. Large colonies control atmospheric CO₂ more precisely than small colonies.     

Modelling the role of intracolonial genetic diversity on regulation of brood temperature in honey bee (Apis mellifera L.) colonies

In polyandrous social insects such as honey bees, a worker’s affinity for a particular task may be genetically infl uenced and so some patrilines may have lower stimulus thresholds for commencing a task than others. We used simulation models to investigate the effects of intracolonial diversity in the task thresholds that stimulate workers to engage in heating and cooling during nest thermoregulation. First, we simulated colonies comprised of one or 15 patrilines that were engaged in heating the brood nest, and observed that single patriline colonies maintained, on average, less stable brood nest temperatures than multiple patriline colonies. Second we simulated colonies with five patrilines that were engaged in cooling their nest, recording the proportions of bees of different patrilines that engaged in nest cooling in response to changing temperatures. Both of our simulations show remarkably similar qualitative patterns to those that we have previously observed empirically. This provides further support for the hypothesis that geneticallybased variability in task thresholds among patrilines within honey bee colonies is an important contributor to the ability of colonies to precisely thermoregulate their nests, and we suggest that diversity is important for optimal expression of a range of other colony-level phenotypes. Received 17 June 2005; revised 27 October 2005; accepted 23 December 2005.     

Foraging decisions of individual workers vary with colony size in the greenhead ant Rhytidoponera metallica (Formicidae, Ectatomminae)

Summary. The ability of worker ants to adapt their behaviour depending on the social environment of the colony is imperative for colony growth and survival. In this study we use the greenhead ant Rhytidoponera metallica to test for a relationship between colony size and foraging behaviour. We controlled for possible confounding ontogenetic and age effects by splitting large colonies into small and large colony fragments. Large and small colonies differed in worker number but not worker relatedness or worker/brood ratios. Differences in foraging activity were tested in the context of single foraging cycles with and without the opportunity to retrieve food. We found that workers from large colonies foraged for longer distances and spent more time outside the nest than foragers from small colonies. However, foragers from large and small colonies retrieved the first prey item they contacted, irrespective of prey size. Our results show that in R. metallica, foraging decisions made outside the nest by individual workers are related to the size of their colony.Received 23 March 2004; revised 3 June 2004; accepted 4 June 2004.     

Hissing in bumblebees: an interspecific defence signal

Summary: Bumblebees (Bombus terrestris) react to disturbances within the nest by a conspicuous hissing sound. The sound is characterised by a high intensity in the ultrasonic frequency range. It is elicited by vibrations of the nest and by mammalian breath and artificial air currents containing CO₂. Domestic mice entering a bumblebee nest elicit these sounds and retreat immediately in response to the bumblebees' signal. It is concluded that the hissing sounds serve as aposematic warning signals aimed at predators entering the nest.     

Movement of honey bee (Apis mellifera L.) queen mandibular gland pheromone in populous and unpopulous colonies

The mode of intranest transfer of the honey bee queen mandibular gland pheromone complex (QMP) was investigated in unpopulous and populous, slightly congested colonies, using synthetic QMP containing tritiated 9-keto-2(E)-decenoic acid, one of the QMP components. Radiolabel was rapidly transported from the center to the peripheral regions of the nest, and in a manner consistent with worker to worker transport. Population size and congestion had no effect on the relative rates of movement from the center to the periphery of the nest or on the mean amounts of radiolabel on individual bees. However, a significantly smaller proportion of the workers in the populous colonies received detectable amounts of radiolabel than in the uncongested colonies, and workers carrying especially large amounts of radiolabel were less numerous in the crowded colonies. It is suggested that, at the stage of colony development that the colonies were in, population size has more of an effect on intranest pheromone transmission than does crowding. Interference with pheromone transfer may occur only at higher levels of congestion than were created, and nearer to the reproductive phase of colony development. An alternative hypothesis is that colony crowding does not significantly affect QMP transport and that the onset of reproductive queen rearing may be associated more with changes in worker thresholds of response to QMP.     

Sex ratio variation in the bumblebee Bombus terrestris

Patterns of sex allocation in bumblebees have been enigmaticand difficult to interpret in either a Fisherian context orin a kin-selection perspective. We gathered data on severalhundred laboratory-reared colonies of the bumblebee Bombus terrestrisand analyzed sex allocation as a function of diapause durationand a series of variables describing colony development. Ouranalyses addressed both sex allocation patterns across differentcohorts of laboratory colonies reared at different times andsex allocation patterns across individual colonies within thesecohorts. We used path analysis to test a hypothetical modellinking a sequence of colony-development variables to the crucialreproductive parameters at the end of the colony life cycle.We show that (1) population-wide patterns of sex allocationshow equal investment in the sexes and are thus consistent withqueen control, but not with worker control. (2) A significantpart of the colony-level and cohort-specific variation in sexallocation is related to the hibernation conditions of foundingqueens: Queens with longer than average winter diapause producelarger cohorts of first and second brood workers, switch tohaploid eggs early, and produce colonies that raise mostly malesand few new queens and vice versa. (3) Colony-level sex allocationis significantly related to the time span between the switchpoint (date of first haploid egg laid by the queen) and thecompetition point (date of first haploid egg laid by one ofthe workers): the longer this period, the more male biased thesex ratio. (4) The breeding constraints of an annual life cycle,the short reproductive season, and the presumably high premiumon early produced males imply that bumblebee workers have norealistic options to capitalize on their relatedness asymmetrytoward the different kinds of reproductive brood by biasingthe sex ratio.     

The role of competition in task switching during colony emigration in the ant Leptothorax albipennis

The decision-making process that determines when an animal should switch between tasks is a fundamental issue in the study of animal behaviour. We investigated, for the first time, such task switching in terms of the dynamics of worker populations in ant colonies. During colony emigration in the ant Leptothorax albipennis, the colony has to carry out the following three tasks: (1) transport of brood and nestmates to the new nest; (2) sorting of the brood into its characteristic pattern; and (3) building the nest wall. At the beginning of the emigration, the stimuli for all three tasks increase simultaneously but the tasks are performed sequentially by populations of workers in the colony. The issue here is how decision making at the colony level is based on the behaviour of individual workers. We used a mathematical model to explore the hypothesis that such colony level task switching is based on tasks competing for workers. The essential feature of this model is that the sequence of tasks performed by an individual worker need not match the sequence of tasks on which the colony concentrates. We base the parameterization of our model on our detailed experimental study of eight emigrations, one for each of eight L. albipennis colonies. We compared our results with earlier work that emphasizes the role of response thresholds in task-related decisions. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

The effects of colony characteristics on life span and foraging behavior of individual wasps (Polybia occidentalis,Hymenoptera: Vespidae)

Summary We studied the effects of intrinsic colony characteristics and an imposed contingency on the life span and behavior of foragers in the swarm-founding social waspPolybia occidentalis. Data were collected on marked, known-age workers introduced into four observation colonies.To test the hypothesis that colony demographic features affect worker life span, we examined the relationships of colony age and size with worker life span using survivorship analysis. Colony age and size had positive relationships with life span; marked workers from two larger, older colonies had longer life spans (¯X = 24.7 days) than those from two smaller, younger colonies (¯X = 20.1 days).We quantified the effects of experimentally imposed nest damage on forager behavior, to determine which of three predicted behavioral responses by foragers to this contingency (increased probability of foraging for building material, increased rate of foraging, or decrease in age of onset of foraging) would be employed. Increasing the colony level of need for materials used in nest construction (wood pulp and water) by damaging the nests of two colonies did not cause an increase in either the proportion of marked workers that gathered nest materials or in foraging rates of marked individuals, when compared with introduced workers in two simultaneously observed control colonies. Instead, nest damage caused a decrease in the age at which marked workers first foraged for pulp and water. The response to an increase in the need for building materials was an acceleration of behavioral development in some workers.     

Individual differences in sensitivity to bitter-tasting substances

Perception of several bitter-tasting compounds was tested in52 subjects. Stable individual differences in the perceivedintensity of the bitterness of suprathreshold concentrationsof quinine sulfate (QSO₄) and urea were found. Whereas 18 subjectsjudged selected concentrations of these compounds to be equallybitter, 17 found QSO₄ to be more bitter than urea, and 17 foundurea to be more bitter than QSO₄. These reliable individualdifferences were significantly related to threshold sensitivityto QSO₄; that is, individuals who perceived QSO₄ to be moreintense than urea at suprathreshold concentrations also hadlower QSO₄ thresholds than did those who perceived urea to bemore intense than QSO₄. There appeared to be no relationshipbetween the relative perceived intensities of these compoundsand rating of the bitterness of PROP (6-n-propylthiouracil).However, QSO₄-sensitive individuals tended to find the bitternessof suprathreshold caffeine and sucrose octaacetate to be greaterthan that of suprathreshold magnesium sulfate, whereas the reversewas true for urea-sensitive individuals. This pattern parallelsthe pattern of cross-adaptation among these compounds reportedby other investigators. These results are consistent with theexistence of multiple bitter transduction sequences and suggestthat individual differences in response to various bitter compoundsmay reflect differences in teh relative availability of specifictransduction sequences.     

Honeybee guards do not use food-derived odors to recognize non-nest mates: a test of the Odor Convergence hypothesis

Honeybee (Apis mellifera) colonies rob honey from each other during periods of nectar shortage. Persistent robbing can killweak colonies. Primarily responsible for preventing robbingare guard bees. Previous research has shown that the probabilityof both nest mate and non-nest mate workers being acceptedby guards at the nest entrance increases as nectar availability increases. The mechanism responsible for this change in guardacceptance can be explained by two competing hypotheses: OdorConvergence and Adaptive Threshold Shift. In this study wetested the Odor Convergence hypothesis. The acceptance by guardsat the nest entrance of workers transferred between four coloniesthat had been fed either odorless sucrose syrup (two colonies)or diluted heather honey (Calluna vulgaris) (two colonies)was measured for 3 days before feeding and during 2 weeks offeeding. Despite the large sample sizes, the probability ofguards accepting non-nest mates was not affected by the similaritiesor dissimilarities in food odor between guards' and non-nestmates' colonies. This finding contrasts with the accepted wisdom that food odors are important in nest mate recognition in honeybeesand the data, therefore, strongly reject the Odor Convergencehypothesis.     

A computational analysis of central CO2 chemosensitivity in Helix aspersa

We created a single-compartment computer model of a CO₂ chemosensory neuron using differential equations adapted from the Hodgkin-Huxley model and measurements of currents in CO₂ chemosensory neurons from Helix aspersa. We incorporated into the model two inward currents, a sodium current and a calcium current, three outward potassium currents, an A-type current (I_KA), a delayed rectifier current (I_KDR), a calcium-activated potassium current (I_KCa), and a proton conductance found in invertebrate cells. All of the potassium channels were inhibited by reduced pH. We also included the pH regulatory process to mimic the effect of the sodium-hydrogen exchanger (NHE) described in these cells during hypercapnic stimulation. The model displayed chemosensory behavior (increased spike frequency during acid stimulation), and all three potassium channels participated in the chemosensory response and shaped the temporal characteristics of the response to acid stimulation. pH-dependent inhibition of I_KA initiated the response to CO₂, but hypercapnic inhibition of I_KDR and I_KCa affected the duration of the excitatory response to hypercapnia. The presence or absence of NHE activity altered the chemosensory response over time and demonstrated the inadvisability of effective intracellular pH (pH_i) regulation in cells designed to act as chemostats for acid-base regulation. The results of the model indicate that multiple channels contribute to CO₂ chemosensitivity, but the primary sensor is probably I_KA. pH_i may be a sufficient chemosensory stimulus, but it may not be a necessary stimulus: either pH_i or extracellular pH can be an effective stimuli if chemosensory neurons express appropriate pH-sensitive channels. The lack of pH_i regulation is a key feature determining the neuronal activity of chemosensory cells over time, and the balanced lack of pH_i regulation during hypercapnia probably depends on intracellular activation of pH_i regulation but extracellular inhibition of pH_i regulation. These general principles are applicable to all CO₂ chemosensory cells in vertebrate and invertebrate neurons. hypercapnia; potassium channels; computer modeling; central chemoreceptors     

Delay in the Response of Stomata to Abscisic Acid in CO2-free Air

Abscisic acid (10^–5 M) was fed via their petioles to leavesdetached from well watered plants of Xanthium strumartum, whilethe intercellular spaces were flushed with air of known CO₂content. A closing response to ABA occurred in the presenceor absence of CO₂, and the stomata responded to CO₂ whetheror not ABA was supplied to the leaves. A factorial experimentrevealed no interaction between CO₂ and ABA, and suggested thattheir effect on the rate of closure was purely additive. Theonly evidence of interdependence between the two corn poundswas a delay in the response to ABA in C0 air, which was moremarked in a high light intensity. A hypothesis which is consistentwith the data is that ABA induces stomatal closure by interferingwith the energy supply required for the active transport processeson which guard cell turgor depends. The inhibitory action ofABA takes longer in CO₂-free air because, in the absence ofCO₂ fixation, energy is available from chioroplasts as wellas mitochondria.