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Integrating vital rates explains optimal worker size for resource return by bumble bee workers
Abstract
Size‐number trade‐offs in reproduction are commonly observed in nature. Bumblebee ( Bombus spp.) colonies produce workers that vary considerably in size. This variation suggests that colonies face potential size‐number trade‐offs when producing workers.
Here, we estimated size‐based vital rates of Bombus vosnesenskii workers using colonies reared from wild‐caught queens. We conducted a mark–recapture study to estimate worker survival as a function of body size. We also collected data on pollen and nectar loads as well as foraging trips using a radiofrequency identification system to estimate daily resource return as a function of body size. We integrated survival and daily resource return to estimate lifetime resource collection and offset these estimates by the size‐based worker production costs.
We found size‐based trade‐offs among workers of different sizes. Smaller workers had higher survival, but larger workers returned with more resources per day. The largest workers made slightly fewer foraging trips per day.
Overall, larger workers made the greatest lifetime contribution to both nectar and pollen collection. However, once the benefits of larger workers are offset by their higher production costs, intermediate‐sized workers were the optimal for net resource contribution according to our models. Many previous studies have found that larger workers outperformed smaller workers with foraging and in‐nest tasks, yet these studies have not integrated multiple fitness components or worker production costs to quantify net resource contribution towards colony growth.
Accounting for trade‐offs between costs and performance changed our conclusions about optimal body size from being large to being near the observed average. Similar approaches of integrating multiple vital rates may resolve apparently suboptimal life histories in other taxa.
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... In addition, larger bumble bees tend to have higher foraging rates (Spaethe and Weidenmüller 2002, Ings 2005, Peat et al. 2005a). Thus, larger workers generally return relatively larger pollen and nectar loads to the colony (Free 1955b, Kerr et al. 2019, and this may in part account for their greater metabolic needs (Plowright et al. 1993), which may increase the overall caloric needs of the colony (Cueva del Castillo et al. 2015, Hendriksma et al. 2019, Balfour et al. 2021. ...
... The relative benefits of large workers to the colony are likely dependent on the type of floral resources available in a local ecosystem, and these benefits may change across the growing season as the number and variety of available floral species changes (e.g., Simanonok andBurkle 2014, CaraDonna andWaser 2020). Larger workers may offset their high rearing cost through greater resource return (Goulson et al. 2002), but once production costs are accounted for, smaller workers may provide equivalent or greater resource contributions (but see Kerr et al. 2019). The optimal range of forager sizes may then vary by local floral resource conditions, at different times of the year, and the density of competitors for resources (Goulson 2003). ...
... If larger workers tend to have lower survival rates (Kelemen et al. 2019, Kerr et al. 2019) and tend to be less hardy against starvation (Couvillon and Dornhaus 2010), then a greater proportion of large workers may be less desirable when floral resources are lower in quality or quantity (but see Kelemen et al. 2020). High worker mortality is also associated with smaller new queens (Muller and Schmid-Hempel 1992). ...
Body size is arguably one of the most important traits influencing the physiology and ecology of animals. Shifts in animal body size have been observed in response to climate change, including in bumble bees (Bombus spp. [Hymenoptera: Apidae]). Bumble bee size shifts have occurred concurrently with the precipitous population declines of several species, which appear to be related, in part, to their size. Body size variation is central to the ecology of bumble bees, from their social organization to the pollination services they provide to plants. If bumble bee size is shifted or constrained, there may be consequences for the pollination services they provide and for our ability to predict their responses to global change. Yet, there are still many aspects of the breadth and role of bumble bee body size variation that require more study. To this end, we review the current evidence of the ecological drivers of size variation in bumble bees and the consequences of that variation on bumble bee fitness, foraging, and species interactions. In total we review: (1) the proximate determinants and physiological consequences of size variation in bumble bees; (2) the environmental drivers and ecological consequences of size variation; and (3) synthesize our understanding of size variation in predicting how bumble bees will respond to future changes in climate and land use. As global change intensifies, a better understanding of the factors influencing the size distributions of bumble bees, and the consequences of those distributions, will allow us to better predict future responses of these pollinators.
... Many studies have measured the importance of body size in determining how well workers perform various tasks, ranging from foraging and flight dynamics to thermoregulating and undertaking. Most of these have found that larger workers are better at multiple tasks, such as foraging and nursing (Cnaani & Hefetz, 1994;Goulson et al., 2002;Ings, 2007;Kerr et al., 2019;Spaethe et al., 2007;Spaethe & Weidenmüller, 2002), with a few studies concluding either that intermediate size is better (Jandt & Dornhaus, 2014), or that there is no size-based difference in performance (Jandt & Dornhaus, 2014). Although these studies demonstrate that body size affects worker performance at certain tasks, they do not demonstrate how their size-based performance at tasks may, in turn, affect colony growth and development. ...
... Therefore, their value may become more apparent when food resources are limiting. In addition, smaller workers have lower production costs, so they may be more cost-effective (Kerr et al., 2019). Here, we used FLMs to evaluate the contribution of workers of different sizes to worker production in bumblebee colonies under three different environments: a low-resource environment; an environment with an early season pulse followed by low resources ("high-low"); and a high-resource environment. ...
... We hand reared Bombus vosnesenskii colonies from wild-caught queens collected at the University of California McLaughlin Reserve (N38 52 25.74,W122 25 56.25) in early spring 2015 and 2016 while they searched for nest sites. These colonies were the basis for two separate studies, both of which are previously published (Kerr et al., 2019;Malfi et al., 2019). Here, we use previously unpublished data (Brood mapping, below) from these studies to investigate effects of worker size on colony growth, so we briefly describe the rearing process. ...
• Behavior and organization of social groups is thought to be vital to the functioning of societies, yet the contributions of various roles within social groups toward population growth and dynamics have been difficult to quantify. A common approach to quantifying these role‐based contributions is evaluating the number of individuals conducting certain roles, which ignores how behavior might scale up to effects at the population‐level. Manipulative experiments are another common approach to determine population‐level effects, but they often ignore potential feedbacks associated with these various roles.
• Here, we evaluate the effects of worker size distribution in bumblebee colonies on worker production in 24 observational colonies across three environments, using functional linear models. Functional linear models are an underused correlative technique that has been used to assess lag effects of environmental drivers on plant performance. We demonstrate potential applications of this technique for exploring high‐dimensional ecological systems, such as the contributions of individuals with different traits to colony dynamics.
• We found that more larger workers had mostly positive effects and more smaller workers had negative effects on worker production. Most of these effects were only detected under low or fluctuating resource environments suggesting that the advantage of colonies with larger‐bodied workers becomes more apparent under stressful conditions.
• We also demonstrate the wider ecological application of functional linear models. We highlight the advantages and limitations when considering these models, and how they are a valuable complement to many of these performance‐based and manipulative experiments.
... 4) weeks of access to supplemental forage owing to plant senescence within the cages. Bumble bee workers take about 3 weeks to develop into adults (Cnaani et al. 2002;Kerr et al. 2019); we supplemented colonies for up to 4 weeks to ensure that added forage would have the potential to fully and directly influence the development of at least one generation of workers. Supplemented colonies were constrained to forage in the cage for a full week to train them to use this space; after which they were permitted to forage either in the cage or in the natural environment through use of a bifurcated entrance tube (Fig. S1). ...
... Although floral resources naturally increased in the wider environment as the season progressed (Fig. S3), this forage did not allow unsupplemented colonies to catch-up. Previous work on select bumble bee species, including B. vosnesenskii, indicates that worker body size is an important aspect of individual-level quality: larger bodied workers tend to be more efficient foragers (Goulson et al. 2002;Spaethe and Weidenmüller 2002;Kerr et al. 2019). This individual effect can translate to overall colony performance. ...
... In this post hoc analysis, only average body size was associated with male reproductive success across all treatments (Fig. S5), echoing the overall importance of body size for bumble bee colony success (cf. Herrmann et al. 2018;Kerr et al. 2019). ...
The temporal distribution of resources is an important aspect of habitat quality that can substantially impact population success. Although it is widely accepted that floral resources directly influence wild bee population sizes, we lack experimental data evaluating how resource availability affects colony growth via demographic mechanisms. To achieve this, we tracked marked individuals in bumble bee (Bombus vosnesenskii) colonies to evaluate whether worker survival and reproduction responded to experimentally elevated forage early in colony development. Specifically, we assessed the effect of early resource environment on worker and sexual offspring production, and the survival and body size of individual workers. We also assessed whether responses of colonies differed when exposed to higher or lower resource environments at a relatively smaller (~ 10 workers) or larger (~ 20 workers) size. Resource supplementation always resulted in greater total offspring and male production; however, the influence of supplementation on worker production and quality depended on colony size at the start of supplementation. Among colonies that were initially smaller, colonies that were supplemented produced fewer but larger bodied and longer lived workers compared to control counterparts. Among colonies that were initially larger, colonies that were supplemented produced more workers than corresponding controls, but without changes to worker quality. Collectively, these results provide clear experimental evidence that greater resource availability early in colony development increases overall productivity, and indicate that colonies may pursue different allocation strategies in response to the resource environment, investing in more or better workers.
... Larger brains allow, for instance, a better visual resolution (Spaethe and Chittka 2003) and faster learning (Worden et al. 2005). On the other hand, the colony costs of production of larger workers are relatively high, moreover, they have lower survivorship than medium and smaller ones (Kerr et al. 2019). In our experiment we found that bumblebee individuals of medium size were dominant visitors of flowers of I. glandulifera, while the numbers of large and small bumblebees were threefold lower. ...
... In our experiment we found that bumblebee individuals of medium size were dominant visitors of flowers of I. glandulifera, while the numbers of large and small bumblebees were threefold lower. A similar trend was noted in the study on B. vosnesenskii (Kerr et al. 2019), where such intermediate-sized workers were assessed as the most beneficial for the colony. We also found that the number of the recorded bumblebees increased with air temperature and decreased with sun radiation and wind speed. ...
Flower infestation by pathogens may influence pollination effectiveness. At the same time, by sharing infested flowers, pollinators increase transmission of pathogens. In the presented study we identified fungi that colonised flowers of the invasive alien Himalayan balsam Impatiens glandulifera , one of the most nectar rewarding plants in Europe, as well as its pollinators. We determined factors (e.g., plant size, length of flower lower sepal and the width of its entry, air temperature and sun illuminance) that affect pathogen species presence and pollinators numbers. The study was conducted in three regions in Poland differing in time from the I. glandulifera invasion onset. It allowed embedding our results in the context of the evolution of increased competitive ability (EICA) hypothesis. With reference to this hypothesis we tested whether I. glandulifera from the two younger populations are more frequently pollinated than individuals from the old one, which may be a result of the higher infection prevalence in the flowers of individuals from the latter population. Harmful primary pathogens of I. glandulifera (e.g., Botrytis cinerea and Fusarium graminearum ) were identified from its flowers. Although the knowledge of the impact of the recorded pathogen species on the pollinators that transmit them is still limited, these pathogens are known to cause devastating diseases of native plant species and to incur significant economic losses in crops. Therefore, the facilitation of their transmission by I. glandulifera in the invaded communities may pose a serious threat both to native biodiversity and nearby crop production. We did not find support for the EICA hypothesis that flower release from pathogens may increase the pollinator’s activity. Bombus hortorum was the most frequent visitor in the youngest surveyed population, while B. pascuorum was most frequent in the two others. So far the dominance of B. hortorum as a pollinator of I. glandulifera has not been recorded. A possible explanation is that flowers in the youngest population, with significantly wider entries than in the two older ones, were more accessible for this large bumblebee. We suggest that the shifts in flower dimensions may result from the evolutionary processes and/or phenotypic plasticity; however, this suggestion needs to be confirmed in further studies. At the same time, it can be expected that exceptionally frequent visits of B. hortorum in flowers of I. glandulifera in the youngest population may contribute to increasing transmission rate of pathogen species to the new native host plants that are particularly associated with this pollinator.
... Foragers tend to be larger in size compared to their nest mates that tend to the colony, a size-dependent form of behavioral specialization termed alloethism (Goulson et al., 2002;Jandt & Dornhaus, 2014;Yerushalmi et al., 2006). Larger bumblebee workers are more costly to rear (Kerr et al., 2019), but they outperform smaller-sized workers in a number of behaviors, such as increased nectar foraging rates Spaethe & Weidenmüller, 2002), faster flight speed inside flower patches (Pyke, 1978), faster thermoregulation , and faster ingestion of nectar (Harder, 1983). They also invest more in learning about flowers (Frasnelli et al., 2021). ...
... Another consideration is that the rearing of large-sized workers is costly for the colony (Kerr et al., 2019), even though they contribute considerably to its maintenance. Larger bumblebees can carry heavier loads of nectar and pollen (Goulson et al., 2002;Spaethe & Weidenmüller, 2002). ...
Foraging on flowers in low light at dusk and dawn comes at an additional cost for insect pollinators with diurnal vision. Nevertheless, some species are known to be frequently active at these times. To explore how early and under which light levels colonies of bumblebees, Bombus terrestris, initiate their foraging activity, we tracked foragers of different body sizes using RFID over 5 consecutive days during warm periods of the flowering season. Bees that left the colony at lower light levels and earlier in the day were larger in size. This result extends the evidence for alloethism in bumblebees and shows that foragers differ in their task specialization depending on body size. By leaving the colony earlier to find and exploit flowers in low light, larger-sized foragers are aided by their more sensitive eyes and can effectively increase their contributions to the colony's food influx. The decision to leave the colony early seems to be further facilitated by knowledge about profitable food resources in specific locations. We observed that experience accrued over many foraging flights determined whether a bee started foraging under lower light levels and earlier in the morning. Larger-sized bees were not more experienced than smaller-sized bees, confirming earlier observations of wide size ranges among active foragers. Overall, we found that most foragers left at higher light levels when they could see well and fly faster. Nevertheless, a small proportion of foragers left the colony shortly after the onset of dawn when light levels were below 10 lux. Our observations suggest that bumblebee colonies have the potential to balance the benefits of deploying large-sized or experienced foragers during dawn against the risks and costs of foraging under low light by regulating the onset of their activity at different stages of the colony's life cycle and in changing environmental conditions. © 2021 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
... The effects of resource availability may be expressed physiologically as well, with positive effects for both crop pollination and colony health because larger Bombus workers can be better foragers (Goulson et al. 2002, Kerr et al. 2019. In bees and other Hymenoptera individual size is the product of maternal investment (Bosch 2008), Honey bee abundance (no. ...
... Although our worker collections occurred two months following blueberry bloom, Malfi et al. (2019) found that access to early season resources increased worker body size during the early bloom period and that this positive effect persisted into the season. Detecting a physiological response to large scale environmental conditions is a challenge because bumble bees are known to have large intraspecific size variation (Goulson et al. 2002, Couvillon et al. 2010, possibly due to size-number tradeoffs (Kerr et al. 2019). ...
Spatial aspects of connectivity have received considerable attention from ecologists and conservationists, yet temporal connectivity – the periodic linking of habitats – plays an equally important, but largely overlooked role. Different biological and biophysical attributes of ecosystems underpin temporal connectivity, but here we focus on resource continuity, the uninterrupted availability of foraging sites. We test the response of pollinators to resource continuity at community, population and individual levels using a novel natural experiment consisting of farms with either single or sequential cropping systems. We found significant effects at the population level; colony density of an important crop pollinator (Bombus impatiens L.) was greater when crop floral resources were continuously available. However, we did not find significant effects at the community or individual level; wild bee abundance, diversity and body size did not respond to resource continuity. Raspberry farms with greater early season resources provided by blueberry had greater bumble bee populations, suggesting beneficial effects on resource availability due to crop diversity. Better understanding the impact of resource continuity via crop diversity on broader patterns of biodiversity is essential for the co‐management of biodiversity and ecosystem services.
... Empirical evidence suggests that colony performance also increases with worker body size [51] and that larger workers outperform smaller ones at various tasks, including foraging [52,53]. Thus, colonies comprising mainly large workers will presumably acquire more resources and produce more workers and gynes than colonies with smaller workers [33,47,[54][55][56]. Yet, larger workers are likely more costly to produce as their size seems to be directly linked to the quantity of food ingested during the larval stage [57,58]. ...
... In spite of this apparent advantage, producing larger workers is not without costs to a colony. For instance, although the largest B. terrestris workers are better at gathering resources, their life expectancy and rearing costs are such that the best trade-off for a colony lays with intermediate-size workers [56]. Similarly, intermediate-size Megachile rotundata females were found to carry the largest pollen loads [68]. ...
Bumble bee communities are strongly disrupted worldwide through the population decline of many species; a phenomenon that has been generally attributed to landscape modification, pesticide use, pathogens, and climate change. The mechanisms by which these causes act on bumble bee colonies are, however, likely to be complex and to involve many levels of organization spanning from the community down to the least understood individual level. Here, we assessed how the morphology, weight and foraging behavior of individual workers are affected by their surrounding landscape. We hypothesized that colonies established in landscapes showing high cover of intensive crops and low cover of flowering crops, as well as low amounts of local floral resources, would produce smaller workers, which would perform fewer foraging trips and collect pollen loads less constant in species composition. We tested these predictions with 80 colonies of commercially reared Bombus impatiens Cresson placed in 20 landscapes spanning a gradient of agricultural intensification in southern Québec, Canada. We estimated weekly rate at which workers entered and exited colonies and captured eight workers per colony over a period of 14 weeks during the spring and summer of 2016. Captured workers had their wing, thorax, head, tibia, and dry weight measured, as well as their pollen load extracted and identified to the lowest possible taxonomic level. We did not detect any effect of landscape habitat composition on worker morphology or body weight, but found that foraging activity decreased with intensive crops. Moreover, higher diversity of local floral resources led to lower pollen constancy in intensively cultivated landscapes. Finally, we found a negative correlation between the size of workers and the diversity of their pollen load. Our results provide additional evidence that conservation actions regarding pollinators in arable landscapes should be made at the landscape rather than at the farm level.
... Nevertheless, shifts in worker body size distribution due to heat exposure could have carryover effects on subsequent colony growth throughout a season. Larger workers have larger foraging ranges (Greenleaf et al., 2007;Kendall et al., 2022) and increased flight endurance (Kenna et al., 2021), both of which facilitate their ability to collect more resources (Kerr et al., 2019), thereby potentially contributing more to colony growth. Without compensation at the colony level, heat exposure could lead to smaller workers which gather fewer resources, limiting colony Frontiers in Physiology frontiersin.org ...
Global declines in abundance and diversity of insects are now well-documented and increasingly concerning given the critical and diverse roles insects play in all ecosystems. Habitat loss, invasive species, and anthropogenic chemicals are all clearly detrimental to insect populations, but mounting evidence implicates climate change as a key driver of insect declines globally. Warming temperatures combined with increased variability may expose organisms to extreme heat that exceeds tolerance, potentially driving local extirpations. In this context, heat tolerance limits (e.g., critical thermal maximum, CT max ) have been measured for many invertebrates and are often closely linked to climate regions where animals are found. However, temperatures well below CT max may also have pronounced effects on insects, but have been relatively less studied. Additionally, many insects with out-sized ecological and economic footprints are colonial (e.g., ants, social bees, termites) such that effects of heat on individuals may propagate through or be compensated by the colony. For colonial organisms, measuring direct effects on individuals may therefore reveal little about population-level impacts of changing climates. Here, we use bumble bees (genus Bombus ) as a case study to highlight how a limited understanding of heat effects below CT max and of colonial impacts and responses both likely hinder our ability to explain past and predict future climate change impacts. Insights from bumble bees suggest that, for diverse invertebrates, predicting climate change impacts will require a more nuanced understanding of the effects of heat exposure and additional studies of carry-over effects and compensatory responses by colonies.
... By analyzing effects of stochastic environments on our predictions, future research could shed light on selection of different strategies to buffer environmental uncertainty, including more cautious egg-laying strategies than predicted here. Other interesting extensions include considering that smaller workers have longer life expectancies to offset lower foraging efficiency (Kerr et al. 2019) and/or that worker kin selective benefits influence laying rates or timing of the switch point (Avila et al. 2019) whether via direct fitness benefits through worker laid males or indirect fitness benefits through queen coercion (Gill and Hammond 2011). ...
Annual social insects are an integral functional group of organisms, particularly in temperate environments. An emblematic part of their annual cycle is the social phase, during which the colony-founding queen rears workers that later assist her in rearing sexual progeny (gynes and drones). In many annual social insects, such as species of bees, wasps, and other groups, developing larvae are provisioned gradually as they develop (progressive provisioning) leading to multiple larval generations being reared simultaneously. We present a model for how the queen in such cases should optimize her egg-laying rate throughout the social phase depending on number-size trade-offs, colony age-structure, and energy balance. Complementing previous theory on optimal allocation between workers vs. sexuals in annual social insects and on temporal egg-laying patterns in solitary insects, we elucidate how resource competition among overlapping larval generations can influence optimal egg-laying strategies. With model parameters informed by knowledge of a common bumblebee species, the optimal egg-laying schedule consists of two temporally separated early broods followed by a more continuous rearing phase, matching empirical observations. However, eggs should initially be laid continuously at a gradually increasing rate when resources are scarce or mortality risks high and in cases where larvae are fully supplied with resources at the egg-laying stage (mass-provisioning). These factors, alongside sexual:worker body size ratios, further determine the overall trend in egg-laying rates over the colony cycle. Our analysis provides an inroad to study and mechanistically understand variation in colony development strategies within and across species of annual social insects.
... All population parameters are considered constant during a major part of the season, except at the end, as the survival decreases and translate into increased mortality at the colony.Further model development, allowing for changes in survival along the season, could be useful to explore different scenarios of worker mortality during colony growth. This would for example allow exploring threats to workers during their active time, such as effects of pesticides(Gill et al., 2012), parasites, or predation, affecting their contribution to resource return to the colony and consequent development(Kerr et al., 2019). ...
Abstract The viability of wild bee populations and the pollination services that they provide are driven by the availability of food resources during their activity period and within the surroundings of their nesting sites. Changes in climate and land use influence the availability of these resources and are major threats to declining bee populations. Because wild bees may be vulnerable to interactions between these threats, spatially explicit models of population dynamics that capture how bee populations jointly respond to land use at a landscape scale and weather are needed. Here, we developed a spatially and temporally explicit theoretical model of wild bee populations aiming for a middle ground between the existing mapping of visitation rates using foraging equations and more refined agent‐based modeling. The model is developed for Bombus sp. and captures within‐season colony dynamics. The model describes mechanistically foraging at the colony level and temporal population dynamics for an average colony at the landscape level. Stages in population dynamics are temperature‐dependent triggered by a theoretical generalized seasonal progression, which can be informed by growing degree days. The purpose of the LandscapePhenoBee model is to evaluate the impact of system changes and within‐season variability in resources on bee population sizes and crop visitation rates. In a simulation study, we used the model to evaluate the impact of the shortage of food resources in the landscape arising from extreme drought events in different types of landscapes (ranging from different proportions of semi‐natural habitats and early and late flowering crops) on bumblebee populations.
... A direct test using B. impatiens showed that colony performance, but not degree of variation in size, increases with mean worker size (Herrmann, Haddad & Levey, 2018). If production costs and lifespan are taken into account, intermediate-sized workers were shown to have the highest net resource contribution (Kerr, Crone & Williams, 2019). The question of how natural selection maintains size polymorphism in Bombus workers remains unresolved. ...
In a much-cited 1964 paper entitled "Reproductive efficiency in relation to colony size in hymenopterous societies," Charles Michener investigated the correlation between a colony's size and its reproductive efficiency-the ability of its adult females to produce reproductives, measured as per-capita output. Based on his analysis of published data from destructively sampled colonies in 18 species, he reported that in most of these species efficiency decreased with increasing colony size. His conclusion that efficiency is higher in smaller groups has since gained widespread acceptance. But it created a seeming paradox: how can natural selection maintain social behaviour when a female apparently enjoys her highest per-capita output by working alone? Here we treat Michener's pattern as a hypothesis and perform the first large-scale test of its prediction across the eusocial Hymenoptera. Because data on actual output of reproductives were not available for most species, Michener used various proxies, such as nest size, numbers of brood, or amounts of stored food. We show that for each of Michener's data sets the reported decline in per-capita productivity can be explained by factors other than decreasing efficiency, calling into question his conclusion that declining efficiency is the cause of the pattern. The most prominent cause of bias is the failure of the proxy to capture all forms of output in which the colony invests during the course of its ontogeny. Other biasing factors include seasonal effects and a variety of methodological flaws in the data sets he used. We then summarize the results of 215 data sets drawn from post-1964 studies of 80 species in 33 genera that better control for these factors. Of these, 163 data sets are included in two meta-analyses that statistically synthesize the available data on the relationship between colony size and efficiency, accounting for variable sample sizes and non-independence among the data sets. The overall effect, and those for most taxonomic subgroups, indicates no loss of efficiency with increasing colony size. Two exceptional taxa, the halictid bees and independent-founding paper wasps, show negative trends consistent with the Michener hypothesis in some species. We conclude that in most species, particularly those with large colony sizes, the hypothesis of decreasing efficiency with increasing colony size is not supported. Finally, we explore potential mechanisms through which the level of efficiency can decrease, be maintained, or even increase, as colonies increase in size.
... Morphometrics is a method for identifying species by representing them through measurements, calculations, or giving values or scores [13]. Aspects of bee morphometry determine the growth of bee species concerning pollen and nectar collection [14]. In addition, body size can describe environmental conditions because it is related to the provision of resources and the abundance and composition of resources [15]. ...
This study aims to determine the morphometric characteristics of the bee Trigona sp. in the Sustainable Food House Area (KRPL) Central Lombok. The research sample consisted of 28 samples of worker bees Trigona sp. taken from 14 colonies in KRPL. The study was conducted in October-November 2020. The morphological characters of each worker bee were observed and 33 morphometric characters were measured. The results of species identification based on morphological and morphometric characters showed that there were two species of Trigona sp. Those in KRPL are Trigona fuscobalteata and Trigona clypearis. The morphological differences that are quite clear between the two species are the structure of the hairbands on the meso scutum, the color of the abdomen, and the color of the wing venation. The color of the abdomen of Trigona fusco balteata is brownish yellow while the color of the abdomen of Trigona clypealis is blackish brown. Wing venation color the structure of the hairbands is more pronounced in Trigona fuscobalteata. Variations in the measured morphometric characteristics can be seen from the standard deviation values. The highest standard deviation values inspecies Trigona fuscobalteatawerehindwing found in length (SDñ0.26), body length (SDñ0.23), forewing length of tegula (SDñ0.19), and forewing length (SD). ñ0.18). Meanwhile, in the species, Trigona clypealis the highest standard deviation values were found in body length (SDñ0.20), forewing length of tegula (SDñ0.15), and forewing length (SDñ0.27).
... terrestris foragers were on average smaller when sampled in wildflower plantings embedded in agricultural landscapes dominated by arable land (e.g., cereal cultures lacking floral resources; see also Persson & Smith 2011). Colonies with small workers produce less queens, so the observed reduction in worker size may also have consequences for the long-term persistence of bumblebee populations (Kerr et al. 2019). In contrast, greater local resource abundance of wildflower plantings resulted in an increase in the mean corbicula area of workers as well as their functional diversity, which may promote pollen collection and resource contributions to colonies. ...
Wildflower plantings are an important mitigation tool within agri-environmental schemes to counter insect decline in resource-scarce agricultural landscapes. Effectiveness of wildflower plantings for insect conservation is typically studied at the community or species level. It is the individual, however, that is subject to changing abiotic and biotic conditions, not the species per se. Accordingly, functional traits of individuals, i.e., the intraspecific functional diversity within species, likely mediate responses to wildflower resources and landscape context. Here we focused on the ecologically and economically important wild insect pollinator Bombus terrestris to study its intraspecific functional diversity and plant-pollinator individual interactions in wildflower plantings. We found considerable trait variation among flower-visiting B. terrestris workers. Locally, this variation could be attributed to flowering plant traits, with larger workers visiting larger inflorescences and individuals with longer tongues preferentially feeding on zygomorphic but not radial symmetric flowers. In addition, wildflower plantings with high floral abundance attracted individuals with larger pollen baskets. At the landscape scale, increasing proportion of arable land resulted in smaller B. terrestris individuals in wildflower plantings, and a decrease in the overall size diversity of workers. These findings highlight the so far little considered role of intraspecific variation in functional traits of wild pollinators, which can mediate the trait-matching between plants and pollinator individuals. Landscape simplification from agriculture threatens intraspecific pollinator diversity, with potential harmful effects for pollinator fitness and plant reproduction. Tailored wildflower plantings can thus serve as an important tool to increase intraspecific variation in simplified landscapes. When designing seed mixtures for these plantings, high complementarity in plant traits is key for promoting high intraspecific trait diversity of bumblebees and potentially of other associated insect species.
... Our results suggest that a workforce consisting of a higher proportion of larger-bodied workers would benefit a colony under cold conditions. However, producing larger workers can come at a cost to a colony as they are more energetically expensive to rear and maintain, and larger workers have been reported to exhibit lower longevity and be less resistant to starvation than their smaller sisters Kerr et al., 2019). Furthermore, in hot conditions, large workers may be more at risk of overheating during flight (Dudley, 2000;Harrison & Roberts, 2000;Rubalcaba & Olalla-Tarraga, 2020). ...
The effects of environmental temperature on components of insect flight determine life‐history traits, fitness, adaptability and, ultimately, organism ecosystem functional roles. Despite the crucial role of flying insects across landscapes, our understanding of how temperature affects insect flight performance remains limited.
Many insect pollinators are considered under threat from climatic warming. Quantifying the relationship between temperature and behavioural performance traits allows us to understand where species are operating in respect to their thermal limits, helping predict responses to projected temperature increases and/or erratic weather events.
Using a tethered flight mill, we quantify how flight performance of a widespread bumblebee, Bombus terrestris , varies over a temperature range (12–30℃). Given that body mass constrains insect mobility and behaviour, bumblebees represent a useful system to study temperature‐mediated size dependence of flight performance owing to the large intra‐colony variation in worker body size they exhibit.
Workers struggled to fly over a few hundred metres at the lowest tested temperature of 12℃; however, flight endurance increased as temperatures rose, peaking around 25℃ after which it declined. Our findings further revealed variation in flight capacity across the workforce, with larger workers flying further, longer, and faster than their smaller nestmates. Body mass was also positively related with the likelihood of flight, although importantly this relationship became stronger as temperatures cooled, such that at 12℃ only the largest workers were successful fliers. Our study thus highlights that colony foraging success under variable thermal environments can be dependent on the body mass distribution of constituent workers, and more broadly suggests smaller‐bodied insects may benefit disproportionately more from warming than larger‐bodied ones in terms of flight performance.
By incorporating both flight endurance and likelihood of flight, we calculated a simple metric termed ‘temperature‐mediated foraging potential’ to gain a clearer understanding of how temperature may constrain colony foraging. Of our tested temperatures, 27℃ supported the highest potential, indicating that for much of the range of this species, higher mean daily temperatures as forecasted under climate warming will push colonies closer to their thermal optimum for flight. Subsequently, warming may have positive implications for bumblebee foraging returns and pollination provision.
A free Plain Language Summary can be found within the Supporting Information of this article.
... In that study, commercial bumble bees weighed 20-70% more than wild workers (depending on the study site location), compared to a 9% difference of average IT span (3.35 vs. 3.63 mm) in our study. Kerr et al. (2019) observed essentially no change in the probability that larger B. vosnesenskii workers would carry pollen over this size range, although very large workers (4.5 mm IT span) were more likely to forage for pollen, and carried slightly more pollen per trip. In our data, IT span was not a significant predictor of the probability workers would carry pollen, after accounting for colony origin (Appendix 3). ...
Bumble bees (Bombus spp.) have been commercially propagated for over three decades. As the environmental conditions experienced by commercial bumble bees differ greatly from those experienced by wild bumble bees, commercial rearing of bumble bees may cause phenotypic changes. Here, we compare the foraging behavior and size of worker bumble bees (Bombus impatiens) from commercial and wild colonies. For this experiment, we measured worker body size, recorded if the workers returned with pollen, and examined the contents of pollen loads via microscopy. We found that, while commercial and wild bumble bees foraged on similar communities of flowers, wild bumble bees returned to colonies with purer pollen baskets (higher proportion of the most common species) and were more likely to return to the colony with pollen than their commercial counterparts. Commercial bumble bees were also smaller than wild bees. Our work highlights differences between commercial and wild bumble bees, in addition to raising important unanswered questions about the mechanism and drivers of these differences.
... Diet-dependent variation in worker body size can have implications for both individual and colony functioning. Kerr and Hebling (1964) found that worker weight can affect the age at which worker honeybees make the transition from in-hive tasks to foraging, and in bumblebees and other bees, body size has been shown to correlate positively with foraging range (Greenleaf et al., 2007) and the weight of pollen and nectar loads that can be collected and transported back to the nest (Goulson et al., 2002;Kerr et al., 2019;Ramalho et al., 1998). Smaller bees have also been shown to be less effective at pollinating flowers (Jauker et al., 2012;Willmer and Finlayson, 2014). ...
Resting metabolic rate (RMR) is a fundamental physiological measure linked to numerous aspects of organismal function, including lifespan. Although dietary restriction in insects during larval growth/development affects adult RMR, the impact of the nutritional composition of larval diets (i.e. diet quality) on adult RMR has not been studied. Using in vitro rearing to control larval diet quality, we determined the effect of dietary protein and carbohydrate on honeybee survival to adulthood, time to eclosion, body mass/size and adult RMR. High carbohydrate larval diets increased survival to adulthood and time to eclosion compared with both low carbohydrate and high protein diets. Upon emergence, bees reared on the high protein diet were smaller and lighter than those reared on other diets, whilst those raised on the high carbohydrate diet varied more in body mass. Newly emerged adult bees reared on the high carbohydrate diet showed a significantly steeper increase in allometric scaling of RMR compared with those reared on other diets. This suggests that the nutritional composition of larval diets influences survival to adulthood, time to eclosion and the allometric scaling of RMR. Given that agricultural intensification and increasing urbanisation have led to a decrease in both forage availability and dietary diversity for bees, our results are critical to improving understanding of the impacts of poor developmental nutrition on bee growth/development and physiology.
... The weight of pollen loads carried by bees is positively correlated with body mass (Giejdasz, 1998;Ramalho et al., 1998;Goulson et al., 2002;Kerr et al., 2019) with larger females carrying heavier loads than their smaller conspecifics. The maximum load that an animal can lift during take-off flights is positively correlated with body mass (Marden, 1994). ...
Body size is related to many aspects of life history, including foraging distance and pollination efficiency. In solitary bees, manipulating the amount of larval diet produces intraspecific differences in adult body size. The goal of this study was to determine how body size impacts metabolic rates, allometry, and flight-related morphometrics in the alfalfa leafcutting bee, Megachile rotundata. By restricting or providing excess food, we produced a range of body sizes, which allowed us to test the effect of body size on allometry, the power required for flight, and amount of energy produced, as measured indirectly through CO2 emission. The power required during flight was predicted using the flight biomechanical formulas for wing loading and excess power index. We found larger bees had higher absolute metabolic rates at rest and during flight, but smaller bees had higher mass-specific metabolic rates at rest. During flight, bees did not have size-related differences in mass-specific metabolic rate. As bees increase in size, their thorax and abdomens become disproportionately larger, while their wings (area, and length) become disproportionately smaller. Smaller bees had more power available during flight as demonstrated by flight biomechanical formulas. Smaller body size was advantageous because of a reduced power requirement for flight with no metabolic cost.
... Indeed, the environmental differences between our free-foraging colonies and the lab-confined colonies in the B. impatiens experiments [49,53] may explain some of the different results. Additionally, the limited sample sizes of these studies, including our own (which is difficult to improve given practical considerations), make it challenging to elucidate the advantage of size-based specialisation under different environments, and this is not yet fully understood [34,[71][72][73]. Nonetheless, we may speculate that, for example, the advantage of body size diversity would be more pronounced under conditions of colder and shorter days, in which large bees may be more efficient than small bees when foraging outside [38,74]. ...
Specialisation and plasticity are important for many forms of collective behaviour, but the interplay between these factors is little understood. In insect societies, workers are often developmentally primed to specialise in different tasks, sometimes with morphological or physiological adaptations, facilitating a division of labour. Workers may also plastically switch between tasks or vary their effort. The degree to which developmentally primed specialisation limits plasticity is not clear and has not been systematically tested in ecologically relevant contexts. We addressed this question in 20 free-foraging bumble bee (Bombus terrestris) colonies by continually manipulating colonies to contain either a typically diverse, or a reduced (“homogeneous”), worker body size distribution while keeping the same mean body size, over two trials. Pooling both trials, diverse colonies produced a larger comb mass, an index of colony performance. The link between body size and task was further corroborated by the finding that foragers were larger than nurses even in homogeneous colonies with a very narrow body size range. However, the overall effect of size diversity stemmed mostly from one trial. In the other trial, homogeneous and diverse colonies showed comparable performance. By comparing behavioural profiles based on several thousand observations of individuals, we found evidence that workers in homogeneous colonies in this trial rescued colony performance by plastically increasing behavioural specialisation and/or individual effort, compared to same-sized individuals in diverse colonies. Our results are consistent with a benefit to colonies of large and small specialists under certain conditions, but also suggest that plasticity or effort can compensate for reduced (size-related) specialisation. Thus, we suggest that an intricate interplay between specialisation and plasticity is functionally adaptive in bumble bee colonies.
... This allowed workers to forage freely by leaving the laboratory building via the entrance/exit tube. We monitored worker activity at this entrance using a 2-reader radio-frequency identification (RFID) system (Kerr et al. 2019;Nunes-Silva et al. 2019). We randomly selected 130 workers, measured their body size (intertegular distance; ITD), and affixed an RFID chip (mic3-TAGv, 64-bit RO, iID2000 13.56 MHz system, 1.9 mm × 1.6 mm × 0.5 mm, Microsensys, Erfurt, Germany) to the thorax of each bee under brief CO 2 anaesthetization. ...
Recent bumble bee declines have prompted the development of novel population monitoring tools, including the use of putatively non-lethal tarsal clipping to obtain genetic material. However, the potential side effects of tarsal clipping have only been tested in the worker caste of a single domesticated species, prompting the need to more broadly test whether tarsal clipping negatively affects sampled individuals. To determine if tarsal clipping reduces queen survivorship and colony establishment, we collected wild queens of Bombus vosnesenskii and clipped tarsi from a single leg of half the individuals. We reared captive queens and estimated survivorship and nest establishment success. We also clipped tarsi of workers from a subset of colonies across a range of body sizes. We found no consistent negative effect of clipping on queen survival. In the first year, clipped nest-searching queens suffered heavy mortality, but there was no effect on foraging queens. The following year, we found no effect of clipping on queen survival or establishment. Clipping did not reduce overall worker survival but reduced survivorship for those in the smallest size quartile.
Implications for insect conservation
Our findings suggest tarsal clipping does not have consistent negative effects on individual survival. However, our results varied with queen behavioral state, year, and worker size, suggesting differences within and among species and interactions with landscape stressors warrant further study. In the interim, we recommend researchers and conservationists minimize the use of tarsal clipping for sensitive species, populations, or small workers except in cases of exceptional scientific need.
... Therefore, it may be expected that pollinators with large body sizes are able to avoid some of the negative impacts caused by invasive plants by covering longer distances (Greenleaf et al., 2007) and foraging in uninvaded areas in their home range. Also, because pollinators' body size is a good predictor of crops' fruit set (Garibaldi et al., 2015), larger pollinators might be effective pollinators of invasive plants' flowers, if they gather more pollen and transport it over longer distances (Kerr et al., 2019). ...
Aim
Mutualistic interactions between alien plants and native pollinators are needed to enable plant invasions. Although the increasing abundance of invasive plants in a habitat causes a dramatic decline of native pollinators, pollination services received by invaders are often sustained. This invader–pollinator paradox might be attributed to differences in pollination effectiveness and varying vulnerability to invasion among pollinators with different life history traits. In an experimental study, we explored the relationships between pollinator body size, pollination effectiveness and abundance of invasive species.
Location
Kraków area, Poland.
Methods
We placed a pair of potted invasive goldenrods (Solidago gigantea) at 25 sites differing in goldenrod abundance (cover: 0%–100%). Floral visitation rate of the potted goldenrods, as well as seed set and viability, was noted.
Results
Species richness of pollinators visiting inflorescences decreased with the increase of the goldenrod cover, whereas the floral visitation rate remained unchanged. However, the seed set was positively related to the goldenrod cover. Body size of floral visitors was structured along with the goldenrod cover so that pollinators' size increased with the cover. Also, the seed set of the potted plants, as well as goldenrod seed viability, depended positively on the body size of visiting pollinators.
Main conclusions
Invasive goldenrods did not suffer from pollinator shortage and ineffective pollination, especially in habitats densely covered by the invader, due to the presence of large‐bodied pollinators. Our study highlights that pollination and reproduction of invasive plants might be sustained through ecological filtering, affecting the composition of pollinators with traits increasing pollination effectiveness.
... Because body size and colony size are positively correlated and lead to opposing predictions in our study species, we cannot distinguish if the lack of relationship seen here is due to neither trait having an effect on exploration or instead both having similarly sized effects that lead to a net impact that is negligible since they work against each other. In addition, it is possible that particularly large or small body sizes might lead to risks or mortality costs that bee species with intermediate body sizes such as A. cerana and A. mellifera are buffered from (Müller et al. 1996;Chole et al. 2019;Kerr et al. 2019). Further research on species that exhibit more variation in body size and colony size in both open-and cavity-nesting species is therefore necessary to disentangle the potentially interacting influences of nest architecture, body size, and colony size on the exploitation-exploration trade-off. ...
Foraging animals continually face the decision of whether to exploit known resources or explore for new ones, a decision with large implications for their fitness. Though animal foraging decisions have been extensively studied, we currently lack a deep understanding of how the exploitation-exploration trade-off has evolved, including how it is shaped by divergent selection pressures between species. As a first step towards examining how the exploitation-exploration trade-off has been adaptively tuned by natural selection, we compared the exploratory behavior of four honey bee species that differ in traits such as nest architecture, body size, and colony size. In a common behavioral context—exploratory behavior triggered by a decrease in quality of a known food resource—we found species differences in exploratory behavior that are consistent with selection arising from evolved differences in nest architecture, though the behavioral differences were also strongly influenced by the magnitude of the reward decrease. We had expected that species that build their nests in the open, and hence face a higher fitness cost of worker attrition compared with species that inhabit protective cavities, would be less likely to prolong unrewarded search when food declines in quality. The behavioral data were partially consistent with this expectation. However, at times, the environmental context strongly modulated species differences in behavior that would be expected based on nest architecture. Overall, our results suggest that the resolution of the exploitation-exploration trade-off has been adaptively tuned between species by a number of interacting selection pressures.
Significance statement
Foraging animals must constantly decide whether to exploit known resources or explore for new, potentially better, ones. How animals resolve this trade-off is likely to have a cumulative effect on their fitness, so natural selection should shape it according to species-specific differences in life history. Using an experimental approach comparing four honey bee species, our results suggest that the tendency to engage in costly search is shaped by multiple interactions among selection pressures differing between honey bee species. We found a correlation between search and how species build their nests, with species nesting in the open generally searching less than those nesting in cavities. However, past experience with a reward can sometimes interact with or overshadow the patterns expected based on nesting behavior. These patterns highlight the complicated effects of life history and ecology on the evolution of behavior.
... 24,25 Taken together, these attributes mean that large bumblebees are predisposed to be the main contributors to a colony's store of nectar, thus outweighing the costs to the colony of raising them. 26 The data presented here argue that large bees learn the locations and features of highly rewarding flowers but tend to ignore less profitable ones. In contrast, small bees learn equally well about flowers of varying profitability but expend less effort when doing so than large bees. ...
Honeybees¹ and bumblebees² perform learning flights when leaving a newly discovered flower. During these flights, bees spend a portion of the time turning back to face the flower when they can memorize views of the flower and its surroundings. In honeybees, learning flights become longer when the reward offered by a flower is increased.³ We show here that bumblebees behave in a similar way, and we add that bumblebees face an artificial flower more when the concentration of the sucrose solution that the flower provides is higher. The surprising finding is that a bee’s size determines what a bumblebee regards as a “low” or “high” concentration and so affects its learning behavior. The larger bees in a sample of foragers only enhance their flower facing when the sucrose concentration is in the upper range of the flowers that are naturally available to bees.⁴ In contrast, smaller bees invest the same effort in facing flowers whether the concentration is high or low, but their effort is less than that of larger bees. The way in which different-sized bees distribute their effort when learning about flowers parallels the foraging behavior of a colony. Large bumblebees⁵,⁶ are able to carry larger loads and explore further from the nest than smaller ones.⁷ Small ones with a smaller flight range and carrying capacity cannot afford to be as selective and so accept a wider range of flowers.
... However, a stable increase of resources from flower strips may rather translate to a higher number of workers. In addition, worker size may be adaptive rather than constrained (Goulson et al., 2002;Malfi et al., 2019), with worker size affecting survival and foraging capacity in opposite ways (Kerr et al., 2019). Since worker size seems to be a function of a variety of interacting short-term and long-term factors (Chole et al., 2019), any positive effect of higher food availability on worker size may be offset by a smaller optimal size when food is more proximate. ...
Bumble bees are important crop pollinators but are negatively impacted by agricultural intensification and concomitant loss of floral resources. Flower strips can increase the abundance and sometimes the diversity of bumble bees at local scales, but the importance of flower strips for bumble bee populations at larger scales remains poorly understood. We investigated the effect of flower strips on bumble bee colony growth and reproduction at landscape scales. Commercial bumble bee colonies of a native species (Bombus terrestris) were placed and monitored at different distances from flower strips that were sown on existing ecological focus areas (European Common Agricultural Policy) in southern Sweden. Both the average colony growth (weight) and the production of reproductives (drones and queens) were highest for colonies adjacent to flower strips and declined with increasing distance. Colonies close to the flower strip also produced more reproductives per colony weight. Colony foraging activity was negatively related to the distance to flower strips whereas worker size was not affected. Annual flower strips in ecological focus areas benefit bumble bee colonies by increasing foraging success, colony growth and finally boosting sexual reproduction, demonstrating potential benefits for pollination within and between seasons. These effects were spatially limited but extended to foraging ranges of bumble bees. However, effects of increased colony growth on the abundance of foraging bees in the landscape may extend to larger distances because of forager movements within seasons and queen dispersal between seasons, suggesting that voluntary or incentivised collaboration between farmers may be needed to achieve optimal implementation of flower strips.
... A major benefit of larger workers is their performance while foraging (Spaethe & Weidenmüller, 2002), where works may have foraging ranges miles in diameter and have to negotiate complex floral landscapes (Greenleaf, Williams, Winfree, & Kremen, 2007;Osborne et al., 1999Osborne et al., , 2008. Natural foraging conditions also come with an increased risk of mortality, particularly for larger bumble bees (Kerr, Crone, & Williams, 2018;Müller, Blackburn, & Schmid-Hempel, 1996). Therefore, our experiment may not have captured all of the costs and benefits of size variation within a colony. ...
Complex systems (e.g. eusocial insect colonies) exhibit emergent behaviours as a result of the interactions of their components. These components often vary in several traits. Such variation may improve system performance by increasing its efficiency or its robustness to environmental change. These two outcomes, efficiency and robustness, are often thought to be in opposition. Therefore, variation may be beneficial only under certain environmental conditions. Here we aim to understand why variation evolved in a particular system, bumble bee (Bombus impatiens) colonies. Workers in these colonies vary in body size, which affects the tasks they perform as well as their starvation resistance, suggesting potential impacts on efficiency and robustness, respectively. We examine how this variation affects colony performance under different environmental conditions and how colonies respond physiologically to these conditions. We maintained colonies of equal biomass but with either variable or less variable worker body sizes using targeted worker removal. We found that colonies with variable body sizes did not produce more brood (i.e. did not show evidence of increased performance) under predictable or unpredictable food environments. However, workers that developed under the unpredictable environment were smaller relative to their weight at eclosion. This effect was due in part to an increase in stored lipids, particularly in smaller workers. These physiological changes may explain why mortality rates did not differ between the predictable and unpredictable environment. Therefore, our finding that size variation did not affect colony performance suggests that size variation may be a neutral trait, present because selection is not acting against it. Our results also suggest that workers respond physiologically to differences in environmental conditions, which is important to consider when testing system robustness.
... It has most successfully been used to follow workers entering and leaving captive nests or feeders (Gill et al. 2012, Hemberger and Gratton 2018, Malfi et al. 2018 but not for direct observations across a large landscape array. For example, it can be used to measure time away from a colony for many individuals, yielding an estimate of the time spent foraging and a proxy for landscape-scale foraging effort (Hemberger and Gratton 2018; for an example without RFID, see Westphal et al., 2006) and colony-wide activity patterns and potential task allocation (Kerr et al. 2019). Like RFID technology, optical tags with QR codes can be used to detect and track individuals within a photographable distance (Crall et al. 2015). ...
Understanding animal movement is critical for conservation planning, habitat management, and ecological study. However, our understanding is often limited by methodological constraints. These limitations can be especially problematic in the study of ecologically and economically important pollinators like bumble bees, where several aspects of their biology limit the feasibility of landscape-scale studies. We review the methods available for the study of bumble bee movement ecology, discussing common limitations and tradeoffs among several frequent data sources. We provide recommendations on appropriate use for different life stages and castes, emphasizing where recent methodological advances can help reveal key components of understudied parts of the bumble bee life cycle such as queen movement and dispersal. We emphasize that there is no one correct method and encourage researchers planning studies to carefully consider the data requirements to best address questions of interest.
The evolution of eusociality is regarded as a major evolutionary transition, where units that previously reproduced independently function as one complex entity. Advanced eusocial societies are characterised by morphologically differentiated castes and reduced conflict. We explore conditions under which morphological castes may arise and the factors constraining their evolution. Control over offspring morphology and behaviour may often be decoupled. Queens and provisioners can influence morphology directly, through the nutrition they provide, while offspring control their own behaviour as adults. Queens and provisioners may, however, influence worker behaviour indirectly, if offspring modify their behaviour in response to their morphology. Our results suggest that the evolution of a morphologically differentiated worker caste depends on the prior presence of a behavioural caste: specialist worker morphology will be mismatched with behaviour unless some offspring already choose to work. A mother's certainty about her offspring's behaviour should also be critical -less certainty results in greater mismatch. Decoupled control is important in maintaining a worker caste, and may result in reduced or no conflict between offspring and provisioners. We also show how worker productivity in the absence of a morphological trait can affect the likelihood of that trait being favoured by natural selection.
Conditions experienced early in development can affect the future performance of individuals and populations. Demographic theories predict persistent population impacts of past resources, but few studies have experimentally tested such carry‐over effects across generations or cohorts. We used bumble bees to test whether resource timing had persistent effects on within‐colony dynamics over sequential cohorts of workers. We simulated a resource pulse for field colonies either early or late in their development and estimated colony growth rates during pulse‐ and non‐pulse periods. During periods when resources were not supplemented, early‐pulse colonies grew faster than late‐pulse colonies; early‐pulse colonies grew larger as a result. These results reveal persistent effects of past resources on current growth and support the importance of transient dynamics in natural ecological systems. Early‐pulse colonies also produced more queen offspring, highlighting the critical nature of resource timing for the population, as well as colony, dynamics of a key pollinator.
Trait variation can have important consequences for the outcomes of species interactions. Even though some traits vary as much within species as across related species, models and empirical studies typically do not consider the role of intraspecific trait variation for processes such as disease transmission. For example, many pollinator species are in decline due to a variety of stressors including pathogens, but the role of intraspecific trait variation in mediating disease dynamics is rarely considered. For example, pollinator body size could affect pathogen transmission via differences in resistance, foraging behavior and physiology. We tested effects of body size on pollinator pathogen transmission using the common eastern bumble bee Bombus impatiens in field tents, introducing an infected ‘donor’ microcolony of large or small workers with an uninfected average‐sized ‘recipient’ microcolony and allowing bees to forage for 9‐16 days. Small donor bees had nearly 50% higher infection intensity (cells/0.02 µL) than large donor bees, but large donor bees were twice as likely to transmit Crithidia bombi to recipient bees. Both behavioral and physiological mechanisms may underlie this apparent paradox. Compared to small bees, large bees foraged more and produced more feces; simulations showed that foraging and defecation rates together had stronger effects on transmission than did donor infection intensity. Thus, effects of bee size on contact rates and pathogen supply may play significant roles in disease transmission, demonstrating the multifaceted impacts of traits on transmission dynamics.
Fire‐induced changes in the abundance and distribution of organisms, especially plants, can alter resource landscapes for mobile consumers driving bottom‐up effects on their population sizes, morphologies and reproductive potential. We expect these impacts to be most striking for obligate visitors of plants, like bees and other pollinators, but these impacts can be difficult to interpret due to the limited information provided by forager counts in the absence of survival or fitness proxies.
Increased bumble bee worker abundance is often coincident with the pulses of flowers that follow recent fire. However, it is unknown if observed postfire activity is due to underlying population growth or a stable pool of colonies recruiting more foragers to abundant resource patches. This distinction is necessary for determining the net impact of disturbance on bumble bees: are there population‐wide responses or do just a few colonies reap the rewards?
We estimated colony abundance before and after fire in burned and unburned areas using a genetic mark–recapture framework. We paired colony abundance estimates with measures of body size, counts of queens, and estimates of foraging and dispersal to assess changes in worker size, reproductive output, and landscape‐scale movements.
Higher floral abundance following fire not only increased forager abundance but also the number of colonies from which those foragers came. Importantly, despite a larger population size, we also observed increased mean worker size. Two years following fire, queen abundance was higher in both burned and unburned sites, potentially due to the dispersal of queens from burned into unburned areas. The effects of fire were transient; within two growing seasons, worker abundance was substantially reduced across the entire sampling area and body sizes were similar between burned and unburned sites.
Our results reveal how disturbance can temporarily release populations from resource limitation, boosting the genetic diversity, body size, and reproductive output of populations. Given that the effects of fire on bumble bees acted indirectly through pulsed resource availability, it is likely our results are generalizable to other situations, such as habitat restorations, where resource density is enhanced within the landscape.
Size polymorphism is common in bees, and is determined by environmental factors such as temperature, brood cell size, and the diet provided to developing larvae. In social bees, these factors are further influenced by intricate interactions between the queen, workers, and the developing brood which eventually determine the final size and caste of developing larvae. Environmental and social factors act in part on juvenile hormone and ecdysteroids, which are key hormonal regulators of body size and caste determination. In some social bees, body size variation is central for social organization because it structures reproductive division of labor, task allocation among workers, or both. At ecological scales, body size also impacts bee-mediated pollination services in solitary and social species by influencing floral visitation and pollination efficacy.
Foraging specialization allows social insects to more efficiently exploit resources in their environment. Recent research on honeybees suggests that specialization on pollen or nectar among foragers is linked to reproductive physiology and sensory tuning (the Reproductive Ground-Plan Hypothesis; RGPH). However, our understanding of the underlying physiological relationships in non-Apis bees is still limited. Here we show that the bumblebee Bombus terrestris has specialist pollen and nectar foragers, and test whether foraging specialization in B. terrestris is linked to reproductive physiology, measured as ovarian activation. We show that neither ovary size, sensory sensitivity, measured through proboscis extension response (PER), or whole-body lipid stores differed between pollen foragers, nectar foragers, or generalist foragers. Body size also did not differ between any of these three forager groups. Non-foragers had significantly larger ovaries than foragers. This suggests that potentially reproductive individuals avoid foraging.
Despite a presumed fitness advantage for individuals with well-developed cognitive abilities, learning performance is usually found to be highly variable within a population. Although little is currently known about the mechanisms responsible for maintaining such variation, there is correlative evidence to suggest that learning performance may be linked to reproductive physiology in the social insects. Bumble bee colonies naturally undergo an initial co-operative phase, when only the queen reproduces, and a subsequent competition phase when all colony members compete to produce male offspring. We experimentally induced these distinct phases by manipulating the presence/absence of the queen and assessed changes in sucrose responsiveness and learning performance. We found that nest-based workers upregulated their reproductive potential in queenless colonies, and correspondingly, these bees were more responsive to sucrose than their queenright counterparts, performing better in an olfactory learning task as a result. These findings suggest that differences in ovarian development are responsible for at least some of the remarkable variation in learning performance that can be observed among very closely related members of social insect colonies.
Significance statement
Cognitive abilities are often assumed to be inherently adaptive, so the question of why individuals vary in their learning ability has received relatively little attention. Here, we focus on reproductive status as a proximate cause of variation in learning ability in the social insects. We show that a significant proportion of the surprising variation that exists between genetically similar colony members can be explained by worker ovarian development; reproductively active workers are more sensitive to food rewards and thus learn more quickly. Learning ability may be one of a suite of correlated traits that are linked to reproductive physiology in social insects and therefore play an important role in the evolution of division of labour.
Synthesis:
We introduce the COMADRE Animal Matrix Database, a resource for animal demography. Its open-data nature, together with its ancillary information, will facilitate comparative analysis, as will the growing availability of databases focusing on other aspects of the rich animal diversity, and tools to query and combine them. Through future frequent updates of COMADRE, and its integration with other online resources, we encourage animal ecologists to tackle global ecological and evolutionary questions with unprecedented sample size.
Locomotion through structurally complex environments is fundamental to the life history of most flying animals, and the costs associated with movement through clutter have important consequences for the ecology and evolution of volant taxa. However, few studies have directly investigated how flying animals navigate through cluttered environments, or examined which aspects of flight performance are most critical for this challenging task. Here, we examined how body size, acceleration and obstacle orientation affect the flight of bumblebees in an artificial, cluttered environment. Non-steady flight performance is often predicted to decrease with body size, as a result of a presumed reduction in acceleration capacity, but few empirical tests of this hypothesis have been performed in flying animals. We found that increased body size is associated with impaired flight performance (specifically transit time) in cluttered environments, but not with decreased peak accelerations. In addition, previous studies have shown that flying insects can produce higher accelerations along the lateral body axis, suggesting that if maneuvering is constrained by acceleration capacity, insects should perform better when maneuvering around objects laterally rather than vertically. Our data show that bumblebees do generate higher accelerations in the lateral direction, but we found no difference in their ability to pass through obstacle courses requiring lateral versus vertical maneuvering. In sum, our results suggest that acceleration capacity is not a primary determinant of flight performance in clutter, as is often assumed. Rather than being driven by the scaling of acceleration, we show that the reduced flight performance of larger bees in cluttered environments is driven by the allometry of both path sinuosity and mean flight speed. Specifically, differences in collision-avoidance behavior underlie much of the variation in flight performance across body size, with larger bees negotiating obstacles more cautiously. Thus, our results show that cluttered environments challenge the flight capacity of insects, but in surprising ways that emphasize the importance of behavioral and ecological context for understanding flight performance in complex environments.
© 2015. Published by The Company of Biologists Ltd.
Carbon dioxide and cold narcosis have been found to have various effects on insect behaviour and physiology, ranging from changes in fecundity and memory to alterations in aggression and foraging. In spite of these potentially confounding effects, narcosis is repeatedly used to handle insects prior to experimental studies. To begin disentangling the unintended effects of narcosis from the effects of experimental manipulation, a better understanding is needed of how different types of narcosis affect insect behaviour, as well as the time frames of these effects. Here, we compare the effects of CO2 and cold narcosis relative to control animals regarding activity, foraging, brood care, aggression, and productivity of worker bumblebees, Bombus terrestris. We show that even a single narcosis event with either cold or CO2 affects these behaviours often in dissimilar ways, and these effects are maintained for at least 4 days following narcosis.
Eusocial insects undoubtedly evolved from solitary ancestors, but how this occurred is not well established. The Ground Plan hypothesis suggests that gene networks that once regulated the oviposition and foraging phases of an ancestral solitary insect's life cycle have been co-opted to establish the queen-worker dimorphism in extant eusocial insects; queens permanently express genes that were once expressed during the oviposition phase, whereas workers express genes that were once associated with foraging. An extension of the Ground Plan hypothesis, the Reproductive Ground Plan-forager hypothesis, proposes that foraging specialization by worker honey bees for either pollen or nectar is controlled by the same reproductive gene networks. According to the Reproductive Ground Plan-forager hypothesis, workers with more ovarioles forage early in life and specialize in pollen collection. Here we find that among workers of a highly reproductive honey bee subspecies, Apis mellifera capensis, there is a positive correlation between ovariole number and age at onset of foraging, and no association between ovariole number and foraging preference, thus contradicting key aspects of the Reproductive Ground Plan-forager hypothesis. We also find a negative association between ovariole number and ovary activation, suggesting that high ovariole number is not directly related to reproductive potential as previously assumed.
Summary
Schedules of survival, growth and reproduction are key life-history traits. Data on how these traits vary among species and populations are fundamental to our understanding of the ecological conditions that have shaped plant evolution. Because these demographic schedules determine population growth or decline, such data help us understand how different biomes shape plant ecology, how plant populations and communities respond to global change and how to develop successful management tools for endangered or invasive species.
Matrix population models summarize the life cycle components of survival, growth and reproduction, while explicitly acknowledging heterogeneity among classes of individuals in the population. Matrix models have comparable structures, and their emergent measures of population dynamics, such as population growth rate or mean life expectancy, have direct biological interpretations, facilitating comparisons among populations and species.
Thousands of plant matrix population models have been parameterized from empirical data, but they are largely dispersed through peer-reviewed and grey literature, and thus remain inaccessible for synthetic analysis. Here, we introduce the compadre Plant Matrix Database version 3.0, an open-source online repository containing 468 studies from 598 species world-wide (672 species hits, when accounting for species studied in more than one source), with a total of 5621 matrices. compadre also contains relevant ancillary information (e.g. ecoregion, growth form, taxonomy, phylogeny) that facilitates interpretation of the numerous demographic metrics that can be derived from the matrices.
Synthesis. Large collections of data allow broad questions to be addressed at the global scale, for example, in genetics (genbank), functional plant ecology (try, bien, d3) and grassland community ecology (nutnet). Here, we present compadre, a similarly data-rich and ecologically relevant resource for plant demography. Open access to this information, its frequent updates and its integration with other online resources will allow researchers to address timely and important ecological and evolutionary questions.
Maximum likelihood or restricted maximum likelihood (REML) estimates of the
parameters in linear mixed-effects models can be determined using the lmer
function in the lme4 package for R. As for most model-fitting functions in R,
the model is described in an lmer call by a formula, in this case including
both fixed- and random-effects terms. The formula and data together determine a
numerical representation of the model from which the profiled deviance or the
profiled REML criterion can be evaluated as a function of some of the model
parameters. The appropriate criterion is optimized, using one of the
constrained optimization functions in R, to provide the parameter estimates. We
describe the structure of the model, the steps in evaluating the profiled
deviance or REML criterion, and the structure of classes or types that
represents such a model. Sufficient detail is included to allow specialization
of these structures by users who wish to write functions to fit specialized
linear mixed models, such as models incorporating pedigrees or smoothing
splines, that are not easily expressible in the formula language used by lmer.
Hamilton's rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton's rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton's rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton's rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton's rule regarding conditions for social evolution and their causes.
Although models of colony organization in social insects often rely on the assumption that within-group variation increases group performance, empirical support for this is mostly confined to studies of genetic variation. However, workers in ant or bee colonies often vary in behaviour and morphology even when genetic variation is low. Bumblebees provide a unique opportunity to explore the consequences of such variation: colonies have a wide range of worker body sizes compared to other social bee species, and workers also vary in response thresholds (i.e. stimulus levels at which workers respond by performing a task), in spite of queens being singly mated (and thus, low genetic variation). Here we test how body size and response threshold diversity affect colony performance in two unrelated in-nest tasks (thermoregulation and undertaking). We manipulated worker diversity using worker removals to restrict threshold or body size variation within the colony. We also quantified the degree of intracolony variation across colonies and related this to colony performance. In general, colonies took longer to cool the nest after bees were removed, but there was no significant effect of treatment on fanning or undertaking success. Furthermore, when intracolony variation was analysed as a continuous variable, we found no effect on colony-level thermoregulation or undertaking performance. Instead, average threshold was a more useful predictor of thermoregulation success, and colonies with a narrower range of size variation had more success at undertaking. These results emphasize the importance of understanding how different types of variation (e.g. behavioural, morphological, etc.) contribute to colony performance.
Individuals in many types of animal groups show both reproductive and task-related division of labour. In some social insect species, such division of labour may be related to the spatial organization of workers inside the nest. We examined colonies of bumblebees and found that (1) 11-13% of workers maintained small spatial fidelity zones inside the nest, and all workers tended to remain at a specific distance from the colony centre independent of their age; (2) smaller individuals maintained smaller spatial zones and tended to be closer to the centre; and (3) individuals that were more likely to perform the in-nest task of larval feeding tended to remain in the centre of the nest, whereas foragers were more often found on the periphery of the nest when not foraging. Individuals that performed other tasks did not maintain a predictable distance to the centre, and there was no evidence that spatial preferences changed over time. Instead, spatial patterns may result from inherent differences between individuals in terms of activity level, and may be a self-organized sorting mechanism that influences division of labour among workers.
Current bee population declines and colony failures are well documented yet poorly understood and no single factor has been identified as a leading cause. The evidence is equivocal and puzzling: for instance, many pathogens and parasites can be found in both failing and surviving colonies and field pesticide exposure is typically sublethal. Here, we investigate how these results can be due to sublethal stress impairing colony function. We mathematically modelled stress on individual bees which impairs colony function and found how positive density dependence can cause multiple dynamic outcomes: some colonies fail while others thrive. We then exposed bumblebee colonies to sublethal levels of a neonicotinoid pesticide. The dynamics of colony failure, which we observed, were most accurately described by our model. We argue that our model can explain the enigmatic aspects of bee colony failures, highlighting an important role for sublethal stress in colony declines.
ln the seed beetle, Staler limbatus, the fitness consequences of egg size vary substantially among host plants. There is intense selection for laying large eggs when larvae will develop on seeds of Cercidium floridum (caused by high mortality penetrating the seed coat) but selection for laying small eggs when larvae will develop on seeds of Acacia greggii (caused by very low mortality penetrating the seed coat and an egg size/egg number trade-off). We test the hypothesis that host-associated variation in egg size within populations of S. limbatus represents an adaptive maternal effect in which females adjust egg size in response to host species. In laboratory experiments, S. limbatus females laid significantly larger and fewer eggs on C. floridum than on A. greggii. When switched between hosts, females readjusted egg size, producing progressively larger eggs on C. floridum and smaller eggs on A. greggii. When conditioned to lay either small eggs (on A. greggii) or large eggs (on C. floridum), and then forced to lay on C. floridum, females conditioned on C. floridum laid eggs that had substantially higher survivorship than eggs laid by females conditioned on A. greggii, These experiments demonstrate that egg size is an adaptively plastic character in S. limbatus.
We quantified the relationships of colony-level factors (number of workers and colony age) with task performance by workers of the bumble bee Bombus bifarius. Worker’s age of first foraging decreased as their colonies aged, which may have caused the observed decrease in worker longevity with colony age. Daily variation in colony nectar foraging rates was related to the number of active foragers, while pollen foraging rates corresponded more strongly with variation in numbers of adult workers. Rates of brood care behavior decreased as the colonies aged, but rates of thermoregulatory behavior (incubation and fanning) did not decrease over time. We conclude that rates of performing some tasks (pollen foraging, brood care) were largely determined by changes in colony demography or correlated variables, while rates of performance of other tasks (nectar foraging, thermoregulation) depended more on external environmental conditions. Most workers switched between two foraging tasks (pollen and nectar collection) and among several in-nest tasks. However, some foragers specialized by focusing their effort on either nectar or pollen. Other workers specialized on in-nest tasks by performing thermoregulatory behavior (incubation and fanning) at significantly higher rates than their nestmates. The task specialists contributed disproportionate amounts of labor to their colonies. Task specialization indicates that workers were not identical in their responses to variation in colony need.
This is the second edition of a multi-author book first published in 1992. It deals with all aspects of plant regeneration by seeds, including reproductive allocation, seed dispersal and predation, longevity, dormancy and germination. All chapters have been updated, and four new chapters added on seed size, seedling establishment, the role of gaps, and regeneration from seed after fire.
Division of labor is a complex phenomenon observed throughout nature. Theoretical studies have focused either on its emergence through self-organization mechanisms or on its adaptive consequences. We suggest that the interaction of self-organization, which undoubtedly characterizes division of labor in social insects, and evolution should be further explored. We review the factors empirically shown to influence task choice. In light of these factors, we review the most important self-organization and evolutionary models for division of labor and outline their advantages and limitations. We describe ways to unify evolution and self-organization in the theoretical study of division of labor and recent results in this area. Finally, we discuss some benchmarks and primary challenges of this approach.
Analyzed egg number and egg size of 17 populations of coho salmon Oncorhynchus kisutch distributed over a latitudinal gradient in North America. A significant latitudinal increase in egg number is accompanied by a significant latitudinal decrease in egg size. Total biomass of eggs produced also declines with latitude. Thus, the positive latitudinal trend in egg number cannot be explained by latitudinal variation in the total investment in eggs. This suggests that local optima in egg size may result in latitudinal clines in egg number. This reasoning, that egg number evolves around selection for egg size, is in fact predicted by life history theory and may explain the clutch size patterns observed in many organisms. -from Authors
Bees may leave their nest in the event of an attack, but this is not their only response. Here, we examine the behavior of those individuals that remain inside the nest during a disturbance. Specifically, we test the hypothesis that bee workers usually exhibiting high levels of inactivity (i.e., 'lazy' bees) may function as defensive reserves that are more likely to respond when the colony is disturbed. We explore this hypothesis by simulating vertebrate attacks by vibrating or blowing carbon dioxide into two colonies on alternating days and measuring the movements and tasks performed by bees inside the nest. Our results show that regardless of the disturbance type, workers increase guarding behavior after a disturbance stops. Although pre-viously inactive bees increased their movement speed inside the nest when the disturbance was vibration, they were not more likely to leave the nest (presumably to attack the simulated attacker) or switch to guarding behavior for any disturbance type. We therefore reject the hypothesis that inactive Bombus impatiens bumblebees act as defensive reserves, and propose alternative hypotheses regarding why many workers remain inactive inside the nest.
1. Bumble bees exhibit worker size polymorphisms; highly related workers within a colony may vary up to 10-fold in body mass. As size variation is an important life history feature in bumble bees, the distribution of body sizes within the colony and how it fluctuates over the colony cycle were analysed.
2. Ten commercially purchased colonies of Bombus impatiens (Cresson) were reared in ad libitum conditions. The size of all workers present and newly emerging workers (callows) was recorded each week.
3. The average size of bumble bee workers did not change with colony age, but variation in body size tended to decrease over time. The average size of callows did not change with population size, but did tend to decrease with colony age. In all measures, there was considerable variation among colonies.
4. Colonies of B. impatiens usually produced workers with normally distributed body sizes throughout the colony life cycle. Unlike most polymorphic ants, there was no increase in worker body size with colony age or colony size. This provides the first, quantitative data on the ontogeny of bumble bee worker size distribution. The potential adaptive significance of this size variation is discussed.
The body size of the host insect in which a parasitoid develops can have important effects on its development and life history. Large and small host body size have both been suggested to be advantageous to parasitoids, depending on the life-history of the species concerned. We test field data on the bumblebeeBombus terrestris and its conopid parasitoids for evidence of differences in size between parasitised and unparasitised worker bees. Bees acting as hosts for conopid parasitoids are on average larger-bodied than unparasitised bees. This result holds for bees collected in two different years, and whether bees are collected while foraging or from the nest. The results we present demonstrate differential parasitism of hosts of different body sizes, but do not necessarily indicate active host choice by conopids. However, they are in agreement with independent evidence that conopids develop more successfully in large-than in small-bodied hosts.
In bumble bees (Bombus spp.), where workers within the same colony exhibit up to a tenfold difference in mass, labor is divided by body size. Current
adaptive explanations for this important life history feature are unsatisfactory. Within the colony, what is the function
of the smaller workers? Here, we report on the differential robustness to starvation of small and large worker bumble bees
(Bombus impatiens); when nectar is scarce, small workers remain alive significantly longer than larger workers. The presence of small workers,
and size variation in general, might act as insurance against times of nectar shortage. These data may provide a novel, adaptive
explanation, independent of division of labor, for size polymorphism within the worker caste.
KeywordsPolymorphism-Robustness-Social insects-Bumble bees-
Bombus impatiens
Some worker honey bees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. We use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and we propose that the non-guard defenders be called soldiers, due to their important role in colony defense.
1. Natural and anthropogenic stressors threaten the sustainability of bumble bees and evaluating their impact is essential to the stewardship of these valuable pollinators. Demographic modelling provides a framework for testing hypotheses about the impacts of stressors, but it has not previously been applied to bumble bees.
2. I therefore formulated a demographic model for a bumble bee colony and then quantified the impact of two stressors, pesticide exposure and spider predation, by perturbing it with their known effects.
3. By simulating a laboratory exposure of Bombus terrestris L. to dietary imidacloprid (a neonicotinoid insecticide), I tested whether the observed colony decline was explained solely by a toxic effect on the fecundity of the foundress queen. By simulating field observations of B. terricola Kirby, I tested whether predation by crab spiders reduced colony fitness sufficiently to provide an adaptive explanation for avoidance behaviours seen when bumble bees encounter spiders.
4. In B. terrestris, a dose‐appropriate decrease in fecundity predicted the observed colony decline, which implicates this as a principal mechanism of toxicity. In B. terricola, doubling the rate of spider predation reduced a colony's production of new queens by 11%, which implies that spider avoidance is highly adaptive.
5. These analyses illustrate the utility of demographic modelling for quantifying the impacts of stressors on bumble bees. In the future, models of this type could be used to investigate a wider range of stressors and to produce thereby knowledge and tools useful for safeguarding bumble bees and the pollination services that they provide.
We studied the allocation of total egg mass to size and number in the carabid beetle Notiophilus biguttatus F. at several temperature and day length regimes. Eggs increase in number and decrease in size with increasing (constant) temperature. Day length interacts with temperature: at short day the effect of temperature on size and number of eggs is weaker than at long day. In diurnally fluctuating temperature regimes, egg size is affected disproportionately by the high temperature period. All treatments, however, are similar in affecting number and size of eggs in an opposite direction. Consequently, egg size is explained to a high degree by egg production rate. The relationship between size and number of eggs among treatments is furthermore characterized by a decrease in egg size with an increase in total egg mass production. Within treatments, rate of egg production and egg size are negatively correlated among females in the low‐temperature groups but not in the high‐temperature groups; the correlations among females are also characterized by a decrease in egg size, with an increase in total egg mass production. Hence, possible trade‐offs between size and number of eggs are masked by phenotypic variation in reproductive effort. The observations enable us to propose a simple conceptual model that explains the within‐treatment correlation by the same causal factor as the negative relationship among treatment means.
Bumblebees are familiar and charismatic insects, occurring throughout much of the world. They are increasingly being used as a model organism for studying a wide range of ecological and behavioural concepts, such as social organization, optimal foraging theories, host-parasite interactions, and pollination. Recently they have become a focus for conservationists due to mounting evidence of range coBIOL15ANIB and catastrophic extinctions with some species disappearing from entire continents (e.g. in North America). Only by improving our understanding of their ecology can we devise sensible plans to conserve them. The role of bumblebees as invasive species (e.g. Bombus terrestris in Japan) has also become topical with the growing trade in commercial bumblebee nests for tomato pollination leading to establishment of non-native bumblebees in a number of countries. Since the publication of the first edition of the book, there have been hundreds of research papers published on bumblebees. There is clearly a continuing need for an affordable, well-illustrated, and appealing text that makes accessible all of the major advances in understanding of the behaviour and ecology of bumblebees that have been made in the last 30 years.
Bumble bee (Bombus) species are ecologically and economically important pollinators, and many species are in decline. In this article, we develop a mechanistic model to analyse growth trajectories of Bombus vosnesenskii colonies in relation to floral resources and land use. Queen production increased with floral resources and was higher in semi-natural areas than on conventional farms. However, the most important parameter for queen production was the colony growth rate per flower, as opposed to the average number of available flowers. This result indicates the importance of understanding mechanisms of colony growth, in order to predict queen production and enhance bumble bee population viability. Our work highlights the importance of interpreting bumble bee conservation efforts in the context of overall population dynamics and provides a framework for doing so.
Interactions between nectar-seeking insects (primarily bumble bees Bombus spp. and honey bees Apis mellifera L.) visiting common milkweed (Asclepias syriaca: Asclepiadaceae) inflorescences and their commonest predator at the inflorescences, the crab spider Misumena vatia (Clerk) (Thomisidae), were recorded. Densities of Misumena were low. On average a given insect would only be attacked once each 4-6 d by a spider, and predicted periods until capture of the different species ranged from 21 to 109 d, far longer than any individual visited milkweed. Insects showed no sign of avoiding spiders. /// Регистрировали вэаимодействия между насекомыми, собирающими нектар (прежде всего шмели Bombus spp. и пчелы Apis mellifera L.) на соцветиях ваточника Asclepias syriaca: Asclepiadaceae и их обычным хищником на соцветиях - пауком-крабом Misumena vatia (Clerck), Thomisidae. Плотность Misumena ниэкая. В среднем данное насекомое могло бы подвергнуться нападению раэ в 4-6 дней, и предскаэанные периоды отлова определенного вида составляют 21-109 дней - гораэдо более длительные, чем посещения ваточника одной особью. у насекомых не обнаружено приэнаков иэбегания науков.
1. Energetic considerations of preflight warm-up in bees predict that bees should warm-up as fast as they can and that larger species should be able to warm-up more rapidly. Larger species should also be able to maintain higher thoracic temperatures during flight. These predictions are examined for 19 species in the solitary bee genus Anthopora (Hymenoptera; Apoidea; Anthophoridae). 2. The genus Anthophora has uniformly high warm-up rates and body temperatures in flight, and the highest warm-up rates measured in any heterotherm. 3. Under standard conditions, both warm-up rates and thoracic temperatures during flight increase with body mass in Anthophora, in keeping with the prediction that heterotherms should minimize the energetic cost of warm-up. 4. Having controlled for body mass effects, Anthophora species able to maintain flight activity at lower ambient temperatures have higher warm-up rates and body temperatures in flight, showing that even in the smallest endotherms there may still be room for selective modification within the limits imposed by body size. 5. Differences in warm-up rates between subgenera within Anthophora suggest that endothermic abilities have diverged in response to differences in the thermal environments which are the centres of diversity for the subgenera. 6. Similar importance of both body mass and the thermal environment in which the species is active is demonstrated over 40 bee species in six families. Because species over a wide taxonomic range do not constitute independent data points, phylogenetic effects in these analyses are controlled for using Grafen's phylogenetic regression. 7. The evolution of high levels of endothermy in Anthophora is discussed with reference to patterns of nectar secretion found in the arid environments which are current centres of diversity for the genus.
1. The behaviour of workers marked individually has been studied in four observation nests of B. agrorum. 2. Both large and small workers foraged and undertook house duties; the apparent division of labour previously noted results from the later age at which small workers begin to forage, about 15 days from emergence as against 5 days for the large workers. 3. By manipulation of colonies it was found that neither absence of foraging bees nor absence of nectar caused the small house-bees to begin foraging. It was therefore considered to be a matter of ontogeny. 4. The longevity of the workers was variable, 69 days being the maximum recorded. On the average 29% of the bees died every 5 days. House-bees lived slightly longer than foragers, particularly in a bad season. 5. About two-thirds of the total bee population were house-bees and one-third foragers at any particular time. 6. No trend in duties with age was observed in the house-bees, foragers, when in the nest, performing a variety of house duties. 7. The larger foragers collected pollen and nectar, 75% of pollen loads being accompanied by nectar. The smaller foragers tended to collect nectar only. 8. In all, 665 foraging trips were timed, the averages for two nests being 17.5 and 15.3 min. Pollen loads with or without nectar took longer to collect than nectar loads alone and loads were collected faster in damp weather than in dry. 9. Pollen loads from one nest were collected and identified. Out of 120 loads, sixty-seven were mixtures of from two to six plant species. The pollen collection of individual workers indicated moderately fixed foraging habits. 10. Normally the workers behaved indifferently towards each other but on a very few occasions attacks were observed in which the attacked bee was forced to disgorge liquid or leave the nest. The attacker was always a house-bee, the attacked a forager. A comparison with the dominance order in Polistes wasps is made.
In recent decades, several N orth A merican bumble bee ( Bombus spp.) species have undergone precipitous declines. It is suspected that a parasite or pathogen may be responsible, yet few studies have examined the extent of parasitism and the ecology of host–parasite relationships in U.S . bumble bee populations.
A season‐long survey of bumble bees in seven grassland meadows of the northern S henandoah V alley and P iedmont regions in V irginia was conducted in 2011 to ascertain the local prevalence and predictors of parasitism by the internal parasites Nosema and Crithidia , and by parasitoid conopid flies.
In total, 835 bumble bees representing six species were examined. Using visual detection methods, we determined that 25% of bees were infected with parasitoid larvae, 17.4% with Crithidia , and 7.3% with Nosema .
Nosema infections were more prevalent and intense in locally rare than locally common species, with the two rarest bumble bees [ B. fervidus (Fabricius) and B. auricomus (Robertson)], newly suspected to be in decline, having the highest frequencies of infection (11–17.8%).
Crithidia was generally more prevalent in common bumble bee species (11–35%). With fewer than 5% of individuals infected, the two rarest species had the lowest frequencies of Crithidia . Conopid fly larvae were more prevalent in common species.
Body size significantly influenced the probability of parasitism by conopids and Crithidia . Smaller bees were more likely to be parasitised by Crithidia . Larger bees were more likely to be parasitised by conopid flies, although the largest bee species ( B. auricomus ) was not infected by conopids in this study.
Adult body mass is a strong correlate of many important life history traits of bees, and thus, has been used as a proxy for these traits in ecological studies. However, body mass is difficult to measure on live specimens in the field, and impossible to measure non-destructively on dry museum specimens. For worker and male bumblebees, we evaluated the linear measures inter-tegular span (IT span) and head width as predictors of fresh and dry weight. For males, linear regressions best explained the relationship between fresh and dry weight and the linear size estimators, while for workers, exponential regressions best explained this relationship. We found that both IT span and head width are precise estimators of weights of bumblebees. Head width was a slightly better predictor of male weights, while IT span was a slightly better predictor of worker weights. IT span and head width changed little by drying. We discuss patterns of size variation in bumblebees, and highlight possible applications of the method in ecological studies.
The negative effect of agricultural intensification on bumblebee populations is thought to partly be caused by loss of food plants, for example because of increased field size and concomitant loss of non-crop field borders and their nectar and pollen plants. Earlier studies have focused on how loss of foraging resources affects colony growth and thereby abundance of workers and sexual reproduction. By comparing bumblebees in agricultural landscapes of different complexity in Southern Sweden, we here demonstrate that also the adult size of bumblebee foragers is significantly related to the availability of foraging resources. This effect was independent of both species identity and foraging habitat type. This suggests a shortage of flower resources in landscapes of lower complexity, which may also affect the reproductive success of colonies negatively.
Work load is analyzed as a heritable summary measure of individual activity, such that high work loads benefit the colony but increase the mortality rate of individuals. Thus, worker genotypes that adopt low work loads are expected to accumulate during colony growth at the expense of hard-working types if both occur in the same colony. When mature colony size is reached, this accumulation could, through nepotism, bias the production of sexuals toward the accumulated genotypes. A formal model shows that a gene coding for low levels of work load could indeed spread in a population of hard-working colonies, if colony workers are not always full sibs, that is, with polygyny or polyandry. The work load that is evolutionarily insensitive to slightly deviating mutants is predicted to decrease with the degree of polygyny (number of egg-laying queens), with polyandry (number of males contributing sperm), and with an increase in the degree of nepotism. Work load should also vary with ecological variables, such as the length of the colony's growth period before reproduction. To evaluate this hypothesis, several measures for work load (inactivity, self-grooming, brood care, risky tasks) are compared across species of ants. Average work load increases with reported colony size, but activity levels in colonies of monogynous and polygynous species are remarkably similar. -from Authors
I develop a general treatment of the effects of parental resource status on optimal offspring size. The model shows that even when there is a resource trade-off between size and number of offspring within individuals, positive correlations between size and number may occur among individuals due to individual variation in resources. Such positive correlations imply that parental resource status affects the fitness-maximizing offspring size, in contrast to the predictions of the standard Smith-Fretwell model. I show that parental resource status affects the fitness-maximizing offspring size whenever the size-number fitness function is nonhomogeneous in offspring number. This condition implies some sort of density-dependent interactions among offspring, although it is possible to have either positive or negative sib interactions in fitness functions that are homogeneous in offspring number. In the latter case offspring size should be insensitive to parental resource status. I explore several cases including linear (Smith-Fretwell), nonlinear but homogeneous, and nonhomogeneous seed-number functions with independent size and number effects, as well as models with interacting offspring size-number effects. I briefly review the plant literature on offspring density dependence and seed-size variation with parental resource status. Some suggestions for testing the ideas with plants and some alternative explanations of positive seed-size/plant-size and seed-size/seed-number correlations are discussed.
1. Bumblebees are important pollinators in North America and are attacked by a range of parasites that impact their fitness; however, few studies have investigated the extent or causes of parasitism in North America.
2. This study used a 2-year multi-site survey of bumblebee parasitism to ask: (i) how common are parasitoid conopid flies and the internal parasites Crithidia bombi and Nosema bombi in Massachusetts; and (ii) what factors are correlated with parasitism?
3. Infection rates by all three parasites were higher in this study than previously documented in North America. Overall, conopids infected 0–73% of bees in each sample, C. bombi infected 0–82% of bees, and N. bombi infected 0–32%.
4. Conopid flies infected female bees more than males and intermediate-sized bees more than large or small bees. Crithidia bombi infection rates were higher in certain bee species and sites, and exhibited a unimodal pattern of prevalence over time. Nosema bombi parasitism was higher in male than female bees.
5. Infection by N. bombi in two rare bumblebee species was higher than expected based on parasitism rates of common bee species but C. bombi infection was lower.
If high prevalence of N. bombi in these bumblebee species is common, parasitism may be a potential cause of their decline.
6. Given the documented effects of these parasites, the high levels of infection may affect bee populations in Massachusetts and threaten the stability of their valuable ecosystem services.
The analysis of life history evolution includes any trait that impinges on the reproductive success of an organism. More specifically, life history evolution is typically concerned with the evolution of the age and size at first reproduction, reproductive effort, clutch size, and propagule size. While many analyses focus only on a single trait, it should be remembered that selection acts on fitness (as defined later) and not solely on single traits. Therefore, the appropriate framework for the analysis of life history evolution is the whole suite of traits that interact to determine the fitness of an organism. The analysis of components of fitness is appropriate in many circumstances but the limitations of such an analysis must always be remembered.
In contrast to other social bees, bumble‐bees exhibit considerable size variation within the worker caste. This size variation has not been adequately explained, although it is known that larger workers tend to be foragers and smaller bees spend more time in the nest. We quantify size variation and mean size for foragers of 22 bumble‐bee species inhabiting climates ranging from arctic and montane to the lowland tropics.
Mean size was larger in bee species from cold climates compared with temperate bumble‐bees. Within species, individuals from Scotland tended to be larger than those from southern England. However, tropical bumble‐bees (mostly belonging to the subgenus Fervidobombus ) were largest of all. We suggest that although a lower limit to size may be imposed by inhabiting cold climates, overheating does not constrain large size in bumble‐bees from hot climates, perhaps because they have efficient mechanisms for heat loss through shunting heat to their extremities.
Tropical bees had shorter thoracic setae than species from cooler climates, while B. terrestris from Greece had shorter setae than those from southern UK. Presumably shorter setae enhance heat loss in warm climates.
Larger workers of B. terrestris were found to have smaller extremities, in proportion to their size, than small workers. We suggest that heat retention is more important in large bees that spend more of their time foraging, than in small bees which spend much of their time in the nest where incubation of the brood requires them to lose heat.
In the temperate climate of southern UK, we found no evidence for ambient temperature having a differential effect on activity of workers of B. terrestris according to their size. We suggest that, at least in temperate climates, size variation in bumble‐bee foragers is probably not an adaptation to temperature variation. Instead it may improve colony foraging efficiency since foragers of different sizes are suited to, and tend to visit, different flower species.
1. The study tested the hypotheses that bumblebees have shorter foraging trips in environments that provide abundant resources than in environments that provide sparse resources, and that shorter foraging trips translate into greater colony growth.
2. Six even‐aged Bombus terrestris colonies were established in contrasting resource environments. Three colonies had access to abundant resources ( Phacelia tanacetifolia fields with high flower densities), and three colonies were placed in an environment with sparse resources (scattered semi‐natural habitats with food plants at lower densities).
3. A total of 870 foraging trips of 220 marked B. terrestris foragers were observed using automated camcorder recordings.
4. The duration of foraging trips was shorter in environments with abundant resources (66 ± 4.6 min) than in environments with sparse resources (82 ± 3.7 min). Within 34 days colonies that had access to abundant resources gained significantly more weight (129 ± 40 g) than colonies foraging on sparse resources (19 ± 7 g).
5. Thus, the spatial distribution and quality of resources at landscape level affected the duration of foraging trips and the colony growth. It was concluded that future conservation schemes need to improve the spatial and temporal availability of resources in agricultural landscapes to counteract the ongoing decline of bumblebees.
Abstract 1. Body weight is often used as an estimator of production costs in aculeate Hymenoptera; however, due to differences between sexes in metabolic rates and water content, conversion of provision weight to body weight may differ between males and females. As a result, the cost of producing female progeny may often have been overestimated.
2. Provision weight and body weight loss throughout development were measured in a solitary bee, Osmia cornuta (Latreille), to detect potential differences between sexes in food weight/body weight conversion.
3. Male O. cornuta invest a larger proportion of larval weight in cocoon spinning, and presumably have higher metabolic rates than females during the larval period; however, this is compensated by a slightly longer larval period in females.
4. Overall, body weight loss throughout the life cycle does not differ significantly between sexes. As a result, cost production ratios calculated from provision weights and from adult body weights are almost identical.
5. The validity of other weight (cocoon, faeces) and linear (head width, intertegular span, wing length, cocoon length, and cell length) measures as estimators of production costs is also discussed.
6. Valid estimators of production costs vary across species due to differences in sex weight ratio, cocoon shape, provision size in reference to cell size, and adult body size.
Bumblebees harbour a wide range of parasitic organisms that attack all stages of their life cycles (reviews in Postner, 1951; Pouvreau, 1973, 1974; Alford, 1975; Kistner, 1982). Among them, conopid flies (Conopidae, Diptera) are particularly interesting because they attack foraging bumblebees which are handling flowers, or even on the wing (Frison, 1926; Cumber, 1949; Postner, 1951; Howell, 1967; Askew, 1971). A single egg is attached to (Frison, 1926; Plath, 1934; Cumber, 1949) or inserted into (DeMeijre, 1904; Howell, 1967) the host's abdomen, where the larva hatches and feeds on haemolymph and internal organs. Within 6–10 days the larva passes through three recognizable stages (Pouvreau, 1974) before the fly pupates in situ within the abdomen. The host bee dies shortly before the parasite pupates (Postner, 1951; Smith, 1966) and the parasite overwinters in its puparium; the adult fly then emerges in early summer (Frison, 1926; Townsend, 1935; Cumber, 1949; Postner, 1951). Conopid flies as parasites of bumblebees are known from all major habitats where the hosts occur (e.g. Kröber, 1939; Smith, 1966). However, the effect of parasitism on distribution and abundance of bumblebees is not known. In this preliminary note we have estimated degrees of infestation and concomitant reduction of life span in affected workers. The results are compared with literature reports on infestation levels in Europe.
The effect of workers size frequency distribution on colony development was studied in 12 young colonies ofB. terrestris. By replacing the original workers with workers of determined size, colonies constituting small, large or mixed size nursing workers were created. The nursing workers size frequency distribution did not influence the average size of the newly emerged workers, nor their size frequency distribution. In contrast, the number of emerging workers and number of egg cells constructed by the queen in colonies with large workers were higher than in colonies with small workers. The small number of emerging workers is explained by prolonged duration of larval time in response to sub-optimal feeding in colonies of small workers. The higher number of egg cells constructed by the queens is supposed to be in response to the number of new cocoons available, or to better condition of the brood.
In the absence of predators, pollinators can often maximize their foraging success by visiting the most rewarding flowers.
However, if predators use those highly rewarding flowers to locate their prey, pollinators may benefit from changing their
foraging preferences to accept less rewarding flowers. Previous studies have shown that some predators, such as crab spiders,
indeed hunt preferentially on the most pollinator-attractive flowers. In order to determine whether predation risk can alter
pollinator preferences, we conducted laboratory experiments on the foraging behavior of bumble bees (Bombus impatiens) when predation risk was associated with a particular reward level (measured here as sugar concentration). Bees foraged in
arenas containing a choice of a high-reward and a low-reward artificial flower. On a bee’s first foraging trip, it was either
lightly squeezed with forceps, to simulate a crab spider attack, or was allowed to forage safely. The foragers’ subsequent
visits were recorded for between 1 and 4h without any further simulated attacks. Compared to bees that foraged safely, bees
that experienced a simulated attack on a low-reward artificial flower had reduced foraging activity. However, bees attacked
on a high-reward artificial flower were more likely to visit low-reward artificial flowers on subsequent foraging trips. Forager
body size, which is thought to affect vulnerability to capture by predators, did not have an effect on response to an attack.
Predation risk can thus alter pollinator foraging behavior in ways that influence the number and reward level of flowers that
are visited.
Keywords
Bombus impatiens
–Bumble bees–Foraging–Non-consumptive effects–Pollination–Predation risk