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Early resources lead to persistent benefits for bumble bee colony dynamics
Abstract
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.
... Because bumble bee colonies are long-lived, the continuous availability of flowers during colony establishment and growth is thought to be critical to colony success (Hemberger et al., 2020;Kevan & Baker, 1983;Schellhorn et al., 2015). For example, worker production in colonies of B. terrestris Linnaeus and B. vosnesenskii Radoszkowski are positively linked to early-season resource availability, suggesting that shortfalls in these resources could negatively impact growing colonies, limiting their ability to produce reproductive individuals (gynes) later in the season (Crone & Williams, 2016;Malfi et al., 2021;Westphal et al., 2009;Williams et al., 2012). Additionally, late-season mass-flowering crops benefit queen production in B. terrestris by eliminating a late-season resource gap (Rundlöf et al., 2014). ...
... This was evidenced by the observed increased foraging rates for field colonies near Phacelia. Such increases in early-season resources are known to elevate colony growth and worker production (Malfi et al., 2021), but the availability of late-season resources may have a more direct impact on drone and gyne production (Rundlöf et al., 2014). This carry-over effect of early-season resource exploitation exhibited by B. impatiens, also seen with B. vosnesenskii (Malfi et al., 2021), may help explain the ability of this species to exploit modern agricultural and human-dominated landscapes in which resources are temporally heterogeneous. ...
... Such increases in early-season resources are known to elevate colony growth and worker production (Malfi et al., 2021), but the availability of late-season resources may have a more direct impact on drone and gyne production (Rundlöf et al., 2014). This carry-over effect of early-season resource exploitation exhibited by B. impatiens, also seen with B. vosnesenskii (Malfi et al., 2021), may help explain the ability of this species to exploit modern agricultural and human-dominated landscapes in which resources are temporally heterogeneous. ...
Centuries of landscape changes associated with agriculture have dramatically reduced the amount and increased the temporal variability of the floral resources that support key pollinating insects such as bumble bees. Adapting to these novel resource conditions is important to ensure the persistence of bumble bee species. While several species appear to be in decline in modern agricultural landscapes, others have thrived, suggesting adaptation to exploit highly variable floral resources. Bombus impatiens , the common eastern bumble bee, is a prime example of such a species.
We designed an experiment to compare how free‐foraging colonies of B. impatiens performed adjacent to areas with either temporally continuous or variable (pulsed) patches of purple tansy ( Phacelia tanacetifolia ) plantings.
We found that colonies in Phacelia landscapes grew faster, had gained more mass, and produced more gynes than did colonies in reference landscapes with no Phacelia .
Comparing colony responses between pulsed and continuous flowering resources showed that total mass gain at the end of the experiment was greater with continuous flowering resources. In contrast, colony growth rate and total gyne production were comparable for colonies adjacent to Phacelia plantings that were continuous versus pulsed.
While low in statistical replication, given the scale of the experimental manipulation, our experiment shows that although B. impatiens colonies can exploit periods of resource discontinuity and gain mass, these continuously available floral resources appear important for colony growth and benefit gyne production.
... foraging time) is likely to have detrimental effects on bumblebee colony growth and reproduction. Although we did not measure microcolony growth due to the temporal scope of each trial, reduced resource intake to bumblebee colonies limits growth Malfi et al. (2022). Most bumblebee colonies maintain only a few days of food reserves and an extended heatwave could exacerbate food limitation and create resource bottlenecks (Maron et al., 2015;Schellhorn et al., 2015), especially in landscapes with limited resources (Samuelson et al., 2018). ...
... Such events may lead to local extinctions or rapidly advancing climate envelopes(Marshall et al., 2020) Whether insect benefits and detriments to a hotter climate will balance, however, is an open question(Lehmann et al., 2020; but also seeJackson et al., 2022).The expected increases in heatwaves suggest several possible options for bumblebees. First, they could reduce foraging efforts during heatwaves, relying on existing food stores in the colony.For many species, minimal food stores may not bridge extended or back-to-back heatwaves resulting in resource shortfallsMalfi et al. (2022). Second, bumblebees might adjust daily foraging windows to early and later in the day when temperatures are more aligned to their physiological constraints. ...
Heatwaves are an increasingly common extreme weather event across the globe and are projected to surge in frequency and severity in the coming decades. Plant‐pollinator mutualisms are vulnerable due to interacting effects of extreme heat on insect pollinator foraging behaviour and their forage plants.
We designed an experiment to parse the impact of extreme heat on bumblebee foraging mediated directly through air temperature and indirectly through changes in plant rewards.
Temperatures simulating a moderate heatwave negatively impacted foraging bumblebees reducing the proportion of successful foraging bouts, foraging bout duration and plant and flower visitation and indirect stress through reduced nectar production that limited foraging bout duration.
Our experimental results provide a mechanistic link between climate, plants and pollinators and suggest in situ conditions from heatwaves could have profound negative consequences for bumblebee colony persistence and maintenance of pollination services.
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... workers (M ± SD 20.7 ± 3.0) and brood in all stages, were placed at each site ( Figure 1) 18 April-10 May 2017 (see Malfi et al., 2022 for details). The four colonies at paired flower planting and control sites were placed on the same day, with random allocation of colonies. ...
... The four colonies at paired flower planting and control sites were placed on the same day, with random allocation of colonies. Colonies were raised from wild queens caught near Monterey, California during March 2017 (Permit #SC-13698; for details see Malfi et al., 2019Malfi et al., , 2022Williams et al., 2012). No other permits or licences were needed for the study. ...
Sustainable agriculture relies on pollinators, and wild bees benefit yield of multiple crops. However, the combined exposure to pesticides and loss of flower resources, driven by agricultural intensification, contribute to declining diversity and abundance of many bee taxa. Flower plantings along the margins of agricultural fields offer diverse food resources not directly treated with pesticides.
To investigate the potential of flower plantings to mitigate bee pesticide exposure effects and support bee reproduction, we selected replicated sites in intensively farmed landscapes where half contained flower plantings. We assessed solitary bee Osmia lignaria and bumble bee Bombus vosnesenskii nesting and reproduction throughout the season in these landscapes. We also quantified local and landscape flower resources and used bee‐collected pollen to determine forage resource use and pesticide exposure and risk.
Flower plantings, and their local flower resources, increased O. lignaria nesting probability. Bombus vosnesenskii reproduction was more strongly related to landscape than local flower resources.
Bees at sites with and without flower plantings experienced similar pesticide risk, and the local flowers, alongside flowers in the landscape, were sources of pesticide exposure particularly for O. lignaria . However, local flower resources mitigated negative pesticide effects on B. vosnesenskii reproduction.
Synthesis and applications . Bees in agricultural landscapes are threatened by pesticide exposure and loss of flower resources through agricultural intensification. Therefore, finding solutions to mitigate negative effects of pesticide use and flower deficiency is urgent. Our findings point towards flower plantings as a potential solution to support bee populations by mitigating pesticide exposure effects and providing key forage. Further investigation of the balance between forage benefits and added pesticide risk is needed to reveal contexts where net benefits occur.
... For example, recent laboratory studies have found that stressors such as a lack of pollen dietary diversity and pesticide exposure (Wu-Smart and Spivak, 2016; have strong negative effects on queen nest initiation and development. Additional work suggests that lack of dietary diversity negatively affects larval development and egg production in small, artificial, queenless colonies (Tasei and Aupinel, 2008;Moerman et al., 2016), and poor resources early in the season have persistent, negative effects on late colony growth rate and queen production Malfi et al., 2020). ...
This dissertation presents a deep dive into the behavior and physiology of spring
queen bumble bees. Bumble bee queens emerge from diapause and initiate new nests
independently in spring. As they lay eggs and subsequently rear offspring to adulthood, queens undergo a dramatic transition from a solitary, to subsocial, to eusocial lifestyle, which presents a unique opportunity to investigate phenotypic plasticity and life history transitions. This colony founding stage of their life cycle may also represent a particularly important demographic for bumble bee populations, many of which are experiencing dramatic declines. An improved understanding of this life stage may help inform conservation strategies and predict bumble bee responses to a changing world.
In this dissertation, I investigate behavioral and physiological plasticity in bumble
bee queens across the spring colony founding stage. In Chapter One, I show that queen ovary development and nest searching and occupation occur simultaneously, which may enable rapid nest initiation. In Chapter Two, I show that the emergence of workers in incipient nests increases queen survival and reproduction, suggesting that the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories, and ultimately nesting success. In Chapter Three, I show that queens respond to the emergence of workers in young nests by performing fewer brood care and food collection tasks, suggesting that queen maternal care behavior is tightly regulated by the number of helpers in the nest. And finally, in Chapter Four, I show that wild queens spend most of each day foraging via short, frequent trips, which highlights the heightened demands placed on early season queens.
Collectively, this work has yielded three major insights into spring queen bumble
bee biology. First, it suggests that queens are highly plastic in the incipient stages of
colony founding and have the capacity to change dynamically in response to social and environmental fluctuations. Second, it suggests that starting nests earlier in the season may be advantageous for bumble bees. Lastly, it underlines the importance of
conservation interventions that support the early nesting period and facilitate the
production and maintenance of workers in incipient nests
... While our analysis highlights how competition between different larval generations can affect optimal egg-laying schedules, the colony growth patterns and switch points of optimal strategies predicted by our model and the Macevicz and Oster (1976) model respond similarly to variation in model parameters. Our model also predicts an overall pattern of growth followed by a decline in worker number matching previous theory (e.g., Macevicz and Oster 1976;Hovestadt et al. 2019) as well as empirical observations (Crone and Williams 2016;Malfi et al. 2022). Further, our predictions regarding egg-laying patterns are at least partially consistent with the study by Mitesser et al. (2017) who showed that solitary insects with overlapping generations, e.g., multivoltine species, obtain a higher geometric population growth rate when the queen lays temporally separated broods and feed these progressively rather than laying one mass-provisioned egg after another. ...
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.
... Peak colony weight was not affected by sunflower abundance or other metrics of floral resource availability. Colonies were mature when placed in the field (as evidenced by the rapid switch to reproduction), and their earlier resource 'environment' in the laboratory likely determined ultimate growth [84]. Overall, it appears that sunflowers as a medicinal resource outweighed costs of potentially low-quality pollen. ...
Community diversity can reduce the prevalence and spread of disease, but certain species may play a disproportionate role in diluting or amplifying pathogens. Flowers act as both sources of nutrition and sites of pathogen transmission, but the effects of specific plant species in shaping bee disease dynamics are not well understood. We evaluated whether plantings of sunflower (Helianthus annuus), whose pollen reduces infection by some pathogens when fed to bees in captivity, lowered pathogen levels and increased reproduction in free-foraging bumblebee colonies (Bombus impatiens). Sunflower abundance reduced the prevalence of a common gut pathogen, Crithidia bombi, and reduced infection intensity, with an order of magnitude lower infection intensity at high sunflower sites compared with sites with little to no sunflower. Sunflower abundance was also positively associated with greater queen production in colonies. Sunflower did not affect prevalence of other detected pathogens. This work demonstrates that a single plant species can drive disease dynamics in foraging B. impatiens, and that sunflower plantings can be used as a tool for mitigating a prevalent pathogen while also increasing reproduction of an agriculturally important bee species.
... Seasonally, shifts in diet are necessary because the long duration of the colony life cycle exceeds the blooming period of most flower species (e.g., Fussell & Corbet, 1992). Foraging choices may also reflect the colony demand for pollen or nectar, itself a function of colony ontogeny and floral environment (Crone & Williams, 2016;Lanterman & Goodell, 2018;Malfi et al., 2022;Roulston & Goodell, 2011). Interspecific or intraspecific competition for flowers may further influence flower choice (Brian, 1957;Heinrich, 1976;Inoue et al., 2008). ...
Regionally specific flower preference data are needed to optimize conservation habitat plantings for at‐risk pollinators such as bumble bees (Bombus spp.). Current tools for selecting flowers for plantings rely on raw bee flower visits, which can be biased toward abundant flowers. To assist in planning habitat enhancements for bumble bees, we quantified genus‐ and species‐level floral preferences using a selection index that accounts for floral availability. Through 477 h of observation in Ohio, USA during the summers of 2017 and 2018, we recorded 22,999 observations of eight Bombus species visiting 96 flowering plant taxa. As a genus, Bombus selected flowers nonrandomly; the most strongly preferred plants included Asclepias spp., Cirsium spp., Convolvulaceae, Dipsacus spp., Echinacea purpurea, Monarda fistulosa, Penstemon digitalis, and Silphium spp. Only a few Fabaceae were highly selected (Baptisia spp., Trifolium pratense, and Vicia spp.), while some were preferred only during their peak bloom (Securigera varia), and others were not preferred by bumble bees (T. hybridum and Melilotus spp.). Diets differed among habitats, and in restored meadows, bumble bees selected for native planted species such as Monarda fistulosa, Asclepias syriaca, Echinacea purpurea, Penstemon digitalis, and Silphium spp. Diets and preferences shifted over the season, largely driven by changes in plant phenologies (e.g., in June, Penstemon was strongly selected, in July, Asclepias, and in August, Verbena). For the three most common Bombus (B. impatiens, B. griseocollis, and B. bimaculatus), rarefaction analysis indicates that we were able to detect almost all plants in their summer diets. However, for five less common species, even our extensive sampling was insufficient to fully characterize their diets. The common Bombus species differed in their feeding niches, perhaps reducing interspecific competition. In contrast, we found high diet overlap between three rarer species—B. vagans, B. fervidus, and B. pensylvanicus, suggesting that these at‐risk species might benefit from different floral communities than would the common species. Five of eight species (including one that is currently under review for federal listing) most strongly preferred one or another non‐native plant, presenting managers with a conservation conundrum concerning how to balance the needs of bees with the preservation of native plants.
... We suspect that beekeepers moved hives near the faba bean field late in the season of 2018. As production of reproductive castes is mainly conditioned in the earlier part of the season (Malfi et al., 2020), we expected the low abundance of honey bees in early season at this site to have a greater effect on bumble bees than the higher numbers of honey bees observed later on in the season. We therefore excluded late season samples from this site when analysing the 2018 data, but we analysed and present 2019 data both with and without this site included, consistently classifying it as a control site with low numbers of honey bee hives. ...
Wild bee declines in agricultural landscapes have led farmers to supplement crops with honey bees. Simultaneously, environmental subsidy and conservation programmes have incentivized farmers to establish flower strips to support wild and managed pollinators. To find out if flower strips enhance, and competition from honey bees suppresses, wild bees in the landscape and across seasons, we surveyed bumble bee and honey bee abundances in 16 sites in Sweden in summer 2018. The centre of each site (2 km radius) was with or without an annual flower strip, and with or without added honey bee hives. We surveyed bees in each flower strip and in linear habitats in the landscape around each site, such as field edges and road verges. In the following spring, we surveyed bumble bee queen abundance in each site. We show that adding flower strips benefits bumble bee queen abundance the following year, but this effect is diminished if honeybee hives are added. In sites with flower strips, added honey bee hives reduced male bumble bee abundance. Our relatively small flower strip areas bolstered bumble bee population growth across seasons, probably by relieving a resource bottleneck. Adding honey bee hives in combination with flower strips to landscapes with few floral resources should be avoided as it cancelled the positive effect of flower strips.
Agricultural practices and intensification over the past two centuries have dramatically altered the abundance and temporal continuity of floral resources that support pollinating insects such as bumble bees. Long‐term trends among bumble bees within agricultural regions suggest that intensive agricultural conditions have created inhospitable conditions for some species, while other species have maintained their relative abundances despite landscape‐level changes in flower availability. Bumble bee responses to spatiotemporal resource heterogeneity have been explored at the colony and behavioral level, but we have yet to understand whether these conditions drive community structure and ultimately explain the diverging patterns in long‐term species trends. To explore the relationship between landscape‐level floral resource continuity and the likelihood of bumble bee occurrence, we mapped the relative spatial and temporal availability of floral resources within an intensive agricultural region in the US Upper Midwest and related this resource availability with bumble bee species relative abundance. Across the bee community, we found that relative bumble bee occurrence increases in landscapes containing more abundant and more temporally continuous floral resources. Declining species, such as Bombus terricola , exhibited the strongest, positive responses to resource abundance and continuity whereas common, stable species, such as B. impatiens, showed no statistical relationship to either. Together with existing experimental evidence, this work suggests that efforts to increase spatiotemporal flower availability, along with overall flower abundance at landscape scales may have positive effects on bumble bee communities in the US Upper Midwest.
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Abstract Many bumble bee species are declining globally from multiple threats including climate change. Identifying conservation priority areas with a changing climate will be important for conserving bumble bee species. Using systematic conservation planning, we identified priority areas for 44 bumble bee species in Canada under current and projected climates (year 2050). Conservation priority areas were identified as those that contained targeted amounts of each species predicted occurrence through climate envelope models, while minimizing the area cost of conserving the identified conservation priority areas. Conservation priority areas in the two periods were compared to established protected areas and land cover types to determine the area of current and future priority sites that are protected and the types of landscapes within priority areas. Notably, conservation priority areas were rarely within established protected areas. Priority areas were most often in croplands and grasslands, mainly within the mountain west, central and Southern Ontario, Northern Quebec, and Atlantic Canada under all climate scenarios. Conservation priority areas are predicted to increase in elevation and latitude with climate change. Our findings identify the most important regions in Canada for conserving bumble bee species under current and future climates including consistently selected future sites.
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.
Many species of bumble bee (Bombus) have declined in range and abundance across Europe, the Americas, and Asia, whereas other species have persisted and remain common and widespread. One explanation as to why some species have declined, based primarily on studies of the European bumble bee fauna, is that declining species have relatively narrow pollen-foraging niches and are less able to use alternative host plants in the absence of their preferred hosts. Though extensively explored in Europe, this hypothesis has not been investigated in North America, in part due to incomplete information on the foraging niche of many species. We selected 12 bumble bee species found in Michigan and quantified their pollen diets using museum specimens. We also extensively resurveyed the state to understand their contemporary status and distribution. Compared to a pre-2000 baseline, six species remain relatively common and widespread, whereas six species show range contractions of over 50%. There was a significant relationship between dietary breadth and distributional range change, with declined or declining species collecting around one-third fewer pollen types than stable species. Though there were significant compositional differences, we found no differences in the number of pollen types collected by species with differing tongue lengths. Overall, these results support the hypothesis that species with narrower dietary niches are at greater risk of decline. However, it is not clear if narrow dietary niches are a cause of declines, or if both are driven by an underlying factor such as proximity to the edge of climatic niches. Further research is needed to improve our understanding of dietary niche in bumble bees, and how it interacts with other factors to influence population trajectories of stable and at-risk species.
1. Prior studies suggest that both the mean and variation of worker size predict the performance of bumble bee colonies. The ‘variation hypothesis’ posits that colony performance increases with variation of worker body size due to more efficient division of labour within colonies. The ‘mean size hypothesis’ posits that colony performance increases with mean bumble bee size, as each individual's efficiency tends to increase with body size.
2. The present study tested these non‐mutually exclusive hypotheses by establishing 62 Bombus impatiens Cresson (Hymenoptera, Apidae) nest boxes in 32 semi‐natural savanna fragments within large‐scale experimental landscapes in South Carolina (U.S.A.).
3. Based on measurements of > 24 000 individuals and on colony growth over ∼7 weeks, our results support the mean size hypothesis, not the variation hypothesis.
Workers of social insects, such as bees, ants and wasps, show some degree of inter-individual variability in decision-making, learning and memory. Whether these natural cognitive differences translate into distinct adaptive behavioural strategies is virtually unknown. Here we examined variability in the movement patterns of bumblebee foragers establishing routes between artificial flowers. We recorded all flower visitation sequences performed by 29 bees tested for 20 consecutive foraging bouts in three experimental arrays, each characterised by a unique spatial configuration of artificial flowers and three-dimensional landmarks. All bees started to develop efficient routes as they accumulated foraging experience in each array, and showed consistent inter-individual differences in their levels of route fidelity and foraging performance, as measured by travel speed and the frequency of revisits to flowers. While the tendency of bees to repeat the same route was influenced by their colony origin, foraging performance was correlated to body size. The largest foragers travelled faster and made less revisits to empty flowers. We discuss the possible adaptive value of such inter-individual variability within the forager caste for optimisation of colony-level foraging performances in social pollinators.
Context
Abundance and diversity of bumblebees have been declining over the past decades. To successfully conserve bumblebee populations, we need to understand how landscape characteristics affect the quantity and quality of floral resources collected by colonies and subsequently colony performance.
Objectives
We therefore investigated how amount and composition of pollen collected by buff-tailed bumblebee Bombus terrestris colonies was affected by the surrounding landscape (i.e. the proportion of forest, urban, semi-natural habitats) and how they were related to colony growth.
Methods
Thirty B. terrestris colonies were placed at grassland sites differing in surrounding landscape. Colonies were established in spring when availability of flowering plants was highest, and their weight gain was monitored for 1 month. We additionally recorded the quantity and compared plant taxonomic composition and nutritional quality (i.e. amino acid composition) of pollen stored.
Results
Bumblebee colonies varied little in the pollen spectra collected despite differences in surrounding landscape composition. They collected on average 80 % of pollen from woody plants, with 34 % belonging to the genus Acer. Early colony growth positively correlated with total amount of woody pollen and protein collected and decreased with increasing proportions of semi-natural habitats and total amino acid concentrations.
Conclusions
Our results suggest that woody plant species represent highly important pollen sources for the generalist forager B. terrestris early in the season. We further show that colony growth of B. terrestris is predominantly affected by the quantity, not quality, of forage, indicating that several abundant plant species flowering throughout the bumblebees’ foraging season may cover the colonies’ nutritional needs.
For many species living in changing environments, processes during one season influence vital rates in a subsequent season in the same annual cycle. The interplay between these carry-over effects between seasons and other density-dependent events can have a strong influence on population size and variability. We carry out a theoretical study of a discrete semelparous population model with an annual cycle divided into a breeding and a non-breeding season; the model assumes carry-over effects coming from the non-breeding period and affecting breeding performance through a density-dependent adjustment of the growth rate parameter. We analyze the influence of carry-over effects on population size, focusing on two important aspects: compensatory mortality and population variability. To understand the potential consequences of carry-over effects for management, we have introduced constant effort harvesting in the model. Our results show that carry-over effects may induce dramatic changes in population stability as harvesting pressure is increased, but these changes strongly depend on whether harvesting occurs prior to reproduction or after it.
The dynamics of structured plant populations in variable environments can be decomposed into the ‘asymptotic’ growth contributed by vital rates, and ‘transient’ growth caused by deviation from stable stage structure.
We apply this framework to a large, global data base of longitudinal studies of projection matrix models for plant populations. We ask, what is the relative contribution of transient boom and bust to the dynamic trajectories of plant populations in stochastic environments? Is this contribution patterned by phylogeny, growth form or the number of life stages per population and per species?
We show that transients contribute nearly 50% or more to the resulting trajectories, depending on whether transient and stable contributions are partitioned according to their absolute or net contribution to population dynamics.
Both transient contributions and asymptotic contributions are influenced heavily by the number of life stages modelled. We discuss whether the drivers of transients should be considered real ecological phenomena, or artefacts of study design and modelling strategy. We find no evidence for phylogenetic signal in the contribution of transients to stochastic growth, nor clear patterns related to growth form. We find a surprising tendency for plant populations to boom rather than bust in response to temporal changes in vital rates and that stochastic growth rates increase with increasing tendency to boom.
Synthesis. Transient dynamics contribute significantly to stochastic population dynamics but are often overlooked in ecological and evolutionary studies that employ stochastic analyses. Better understanding of transient responses to fluctuating population structure will yield better management strategies for plant populations, and better grasp of evolutionary dynamics in the real world.
For many species, geographical ranges are expanding toward the poles in response to climate change, while remaining stable along range edges nearest the equator. Using long-term observations across Europe and North America over 110 years, we tested for climate change–related range shifts in bumblebee species across the full extents of their latitudinal and thermal limits and movements along elevation gradients. We found cross-continentally consistent trends in failures to track warming through time at species’ northern range limits, range losses from southern range limits, and shifts to higher elevations among southern species. These effects are independent of changing land uses or pesticide applications and underscore the need to test for climate impacts at both leading and trailing latitudinal and thermal limits for species.
Bucking the trend
Responses to climate change have been observed across many species. There is a general trend for species to shift their ranges poleward or up in elevation. Not all species, however, can make such shifts, and these species might experience more rapid declines. Kerr et al. looked at data on bumblebees across North America and Europe over the past 110 years. Bumblebees have not shifted northward and are experiencing shrinking distributions in the southern ends of their range. Such failures to shift may be because of their origins in a cooler climate, and suggest an elevated susceptibility to rapid climate change.
Science, this issue p. 177
1.Growing evidence for declines in wild bees calls for the development and implementation of effective mitigation measures. Enhancing floral resources is a widely accepted measure for promoting bees in agricultural landscapes, but effectiveness varies considerably between landscapes and regions. We hypothesize that this variation is mainly driven by a combination of the direct effects of measures on local floral resources and the availability of floral resources in the surrounding landscape.
2.To test this, we established wildflower strips in four European countries, using the same seed mixture of forage plants specifically targeted at bees. We used a Before-After Control-Impact (BACI) approach to analyse impacts of wildflower strips on bumblebees, solitary bees and Red List species, and examined to what extent effects were affected by local and landscape-wide floral resource availability, land-use intensity and landscape complexity.
3.Wildflower strips generally enhanced local bee abundance and richness, including Red Listed species. Effectiveness of the wildflower strips increased with the local contrast in flower richness created by the strips, and furthermore depended on the availability of floral resources in the surrounding landscape, with different patterns for solitary bees and bumblebees. Effects on solitary bees appeared to decrease with increasing amount of late-season alternative floral resources in the landscape, whereas effects on bumblebees increased with increasing early-season landscape-wide floral resource availability.
4.Synthesis and applications. Our study shows that the effects of wildflower strips on bees are largely driven by the extent to which local flower richness is increased. The effectiveness of this measure could therefore be enhanced by maximizing the number of bee forage species in seed mixtures, and by management regimes that effectively maintain flower richness in the strips through the years. In addition, for bumblebees specifically, our study highlights the importance of a continuous supply of food resources throughout the season. Measures that enhance early-season landscape-wide floral resource availability, such as the cultivation of oilseed rape, can benefit bumblebees by providing the essential resources for colony establishment and growth in spring. Further research is required to determine whether, and under what conditions, wildflower strips result in actual population-level effects.
There is compelling evidence that more diverse ecosystems deliver greater benefits to people, and these ecosystem services have become a key argument for biodiversity conservation. However, it is unclear how much biodiversity is needed to deliver ecosystem services in a cost-effective way. Here we show that, while the contribution of wild bees to crop production is significant, service delivery is restricted to a limited subset of all known bee species. Across crops, years and biogeographical regions, crop-visiting wild bee communities are dominated by a small number of common species, and threatened species are rarely observed on crops. Dominant crop pollinators persist under agricultural expansion and many are easily enhanced by simple conservation measures, suggesting that cost-effective management strategies to promote crop pollination should target a different set of species than management strategies to promote threatened bees. Conserving the biological diversity of bees therefore requires more than just ecosystem-service-based arguments.
Abstract Most mammalian populations suffer from natural or human-induced disturbances; populations are no longer at the equilibrium (i.e., at stable [st]age distribution) and exhibit transient dynamics. From a literature survey, we studied patterns of transient dynamics for mammalian species spanning a large range of life-history tactics and population growth rates. For each population, we built an age-structured matrix and calculated six metrics of transient dynamics. After controlling for possible confounding effects of the phylogenetic relatedness among species using a phylogenetic principal component analysis and phylogenetic generalized least squares models, we found that short-term demographic responses of mammalian populations to disturbance are shaped by generation time and growth rate. Species with a slow pace of life (i.e., species with a late maturity, a low fecundity, and a long life span) displayed decreases in population size after a disturbance, whereas fast-living species increased in population size. The magnitude of short-term variation in population size increased with asymptotic population growth, being buffered in slow-growing species (i.e., species with a low population growth rate) but large in fast-growing species. By demonstrating direct links between transient dynamics, life history (generation time), and ecology (demographic regime), our comparative analysis of transient dynamics clearly improves our understanding of population dynamics in variable environments and has clear implications for future studies of the interplay between evolutionary and ecological dynamics. As most populations in the wild are not at equilibrium, we recommend that analyses of transient dynamics be performed when studying population dynamics in variable environments.
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.
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.
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Resilience is a component of ecological stability; it is assessed as the rate at which perturbations to a stable ecological system decay. The most frequently used estimate of resilience is based on the eigenvalues of the system at its equilibrium. In most cases, this estimate describes the rate of recovery only asymptotically, as time goes to infinity. However, in the short term, perturbations can grow significantly before they decay, and eigenvalues provide no information about this transient behavior. We present several new measures of transient response that complement resilience as a description of the response to perturbation. These indices measure the extent and duration of transient growth in models with asymptotically stable equilibria. They are the reactivity (the maximum possible growth rate immediately following the perturbation), the maximum amplification (the largest proportional deviation that can be produced by any perturbation), and the time at which this amplification occurs. We demonstrate the calculation of these indices using previously published linear compartment models (two models for phosphorus cycling through a lake ecosystem and one for the flow of elements through a tropical rain forest) and a standard nonlinear predator-prey model. Each of these models exhibits transient growth of perturbations, despite asymptotic stability. Measures of relative stability that ignore transient growth will often give a misleading picture of the response to a perturbation.
1. Matrix population models are tools for elucidating the association between demographic processes and population dynamics. A large amount of useful theory pivots on the assumption of equilibrium dynamics. The preceding transient is, however, of genuine conservation concern as it encompasses the short-term impact of natural or anthropogenic disturbance on the population.
2. We review recent theoretical advances in deterministic transient analysis of matrix projection models, considering how disturbance can alter population dynamics by provoking a new population trajectory.
3. We illustrate these impacts using plant and vertebrate systems across contiguous and fragmented landscapes.
4. Short-term responses are of fundamental relevance for applied ecology, because the time-scale of transient effects is often similar to the length of many conservation projects. Investigation of the immediate, post-disturbance phase is vital for understanding how population processes respond to widespread disturbance in the short- and into the long term.
5. Synthesis and applications. Transient analysis is critical for understanding and predicting the consequences of management activities. By considering short-term population responses to perturbations, especially in long-lived species, managers can develop more informed strategies for species harvesting or controlling of invasive species.
We studied worker longevity in two colonies of Bombus fervidus (F.) and two colonies of Bombus pennsylvanicus (De Geer). In 1981, adult life expectation for B. fervidus workers was 21.8 days. In 1982, mean expectation of life at adult emergence was 34.1 days for workers of B. fervidus and 33.0 days for workers of B. pennsylvanicus. The longevities observed in 1982 are the highest yet recorded for temperate bumble bee species, and are intermediate between the previously described extremes of short life-span in north temperate species and high longevity in a tropical species. This study suggests that bumble bee life expectancy tends to decrease as one progresses northward. However, variation in life expectancy within B. fervidus at a single location in two consecutive years was almost as great as previously described differences in longevity between tropical and temperate species. Shortened life-span may therefore be associated with increased intensity of foraging activity during periods of low forage availability as well as with latitude. In both years, survivorship of late-emerging worker cohorts was consistently low, possibly because a larger proportion of late-emerging workers become foragers.
Survivorship data were obtained for a cohort of 274 individually marked workers of the bumble bee Bombus terricola Kirby. The mortality rate was very nearly constant for the first 14 days of adult life, after which it increased sharply. Environmental hazards, including predation, are considered the most probable causes of death, supplemented by the effects of wear and tear as the insects grow old. The life expectancy for a newly emerged adult worker bee was estimated at 13.2 days. The results, together with those of other studies, are discussed with reference to differences in mortality rates between temperate and tropical bumble bee species.
The components of nest provisioning behavior (resources per cell, transport capacity, trip duration, trips per cell) are examined for a data set derived from the literature and various unpublished studies. While there is a trade-off between transport capacity and trips required per cell, the highest provisioning rates are achieved by bees carrying very large pollen loads at intermediate trip durations. Most solitary bees appear to be either egg or resource limited, so sustained provisioning rates over one cell per day are unusual.
1. 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 towards 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. 2. 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. 3. 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. 4. 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.
The loss of flower-rich habitat in agricultural landscapes is a key factor contributing to bumble bee declines across Europe and North America. Yet, agricultural intensification has not only altered flower abundance in the landscape, but also affected when flowers are available during the season (e.g., mass-flowering crops). While we know that both total pollen and nectar as well as temporal availability can impact bumble bee colony success (growth and reproductive output), we have yet to understand how these two factors combined might manifest. We designed an experiment to decouple the effects of total food abundance and its temporal availability on bumble bee microcolony development by exposing them to either constant or pulsed food availability at a high and low ration level. Microcolonies provided constant, high-rations of food grew the most, while those fed variable, but high rations gained less mass over the course of the experiment. Regardless of the temporal presentation of food, microcolonies fed low rations gained little mass over the experiment. Reproductive output was greatest in microcolonies fed high rations, regardless of the temporal availability of food, while those given low rations produced on average 27% fewer drones. This study highlights the importance of food abundance for both colony growth and reproduction, regardless of how food is presented (e.g., constantly or in a pulse). Together, these results indicate that increasing total food abundance will have the greatest, positive impact on colony fitness.
Mass-flowering crops provide forage for bees but also contain pesticides. Such pesticide exposure can harm bees, but our understanding of how this cost is balanced by forage benefits is limited. To provide insights into benefits and costs, we placed bumblebee colonies in 18 landscapes with conventional red clover fields treated with the neonicotinoid thiacloprid (flowers + pesticide), untreated organic red clover fields (flowers), or landscapes lacking clover fields (controls). Colonies grew heavier near thiacloprid-treated clover compared to controls lacking clover, while colonies near untreated clover did not differ from colonies in neither of the other landscape types. Thiacloprid treatment effectively controlled pests and increased bumblebee crop visitation. However, colony production of queens and males did not differ among landscape types. In conclusion, thiacloprid application in clover appears to be of low risk for bumblebees. More generally, neonicotinoids may not be equally harmful when used in flowering crops and effective low-risk pest control in such crops could potentially benefit bumblebees and crop pollination.
Task specialization is one of the distinguishing features of social insect colony organization. Here we study the task of corpse removal (‘undertaking’) from the nest in three Bombus impatiens colonies. We determine (1) which task these bees perform when corpses are absent from the nest; (2) the degree to which worker body size relates to undertaking behavior; and (3) whether certain bees are more likely to completely remove corpses (i.e., are better undertakers)? We found that only ~ 31% of the workers in a colony participated in corpse removal even when corpses were abundant (and only ~ 12% participated in more than one trial, i.e., were “repeat undertakers”). Larger bees, and those that engaged in guarding tasks when corpses were absent, were more likely to perform undertaking. In addition, repeat undertakers, who were not necessarily larger than one-trial undertakers, were more successful at removing corpses and invested more effort per trial. Overall, our results are consistent with the interpretation that workers who are more likely to engage in guarding tasks (who also tend to be larger and patrol throughout the nest) may be more vigilant and sensitive to changes in the chemical nature of the nest, and so will also perform undertaking when it becomes necessary.
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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Floral resources and natural enemies are considered important drivers of wild bee population dynamics, yet there is little information on how these factors, either independently or in combination, influence the demographic performance of bees. Bumble bees (Bombus spp.), ecologically important social insects, have long colony cycles lasting many weeks. Food shortfalls during the colony lifetime can result in smaller colony sizes and lower reproductive output. Conopid flies (Conopidae, Diptera) are prevalent endoparasitoids of bumble bees, often infecting high percentages of free‐flying individuals. Conopids can reduce worker lifespan and foraging efficiency; consequently, they may negatively affect colony success. In this study, we evaluated how seasonal variability in food resources and conopid parasitism together influence the productivity of bumble bee colonies through construction of a simulation model. In addition to simulating colony performance in relation to a defined food environment and conopid‐induced worker mortality, we evaluated how daily background mortality risk and the timing of colony initiation affected growth and reproductive outcomes of colonies, as well as the degree of influence exerted by conopids. Model parameters were largely informed by field data collected from Bombus impatiens colonies at our study site (Blandy Experimental Farm, Boyce, VA, USA), including data on forager risk of conopid parasitism as assessed using radio frequency identification (RFID) technology. In spite of the high probability of parasitism (4% per hour of flight during seasonal peak) incorporated into our model simulations, lethal parasitism by conopids generally had a modest influence on colony productivity, reducing reproductive output by 15% or less across most tested scenarios. However, conopids were more influential under very low resource conditions, reducing reproductive output by 21‐28%. Inclusion of sublethal effects of conopids on foraging activity further reduced colony performance in all scenarios, but had a greater impact on colony performance under the poorest resource conditions. This work emphasizes that the importance of natural enemies to the demographic performance of bees can increase under certain environmental conditions and highlights the value of using models to consider multiple stressors that are difficult to evaluate simultaneously in field experiments. This article is protected by copyright. All rights reserved.
1. Acceptance of hosts for oviposition is often hardwired in short‐lived insects, but can be dynamic at the individual level due to variation in physiological state determinants such as ageing and prior oviposition. However, the effect of the oviposition history of resources together with time taken to accept less preferred hosts in ageing insects has rarely been investigated.
2. The time taken by parasitic fig wasps to accept resources with different oviposition histories was recorded in order to investigate the effect of wasp physiological state and resource oviposition history on oviposition behaviour. These wasps, which differ in life‐history traits, oviposit at specific developmental stages of enclosed fig inflorescences called syconia.
3. Behavioural assays were performed with naive wasps and wasps aged with and without prior oviposition experience. Syconia at the same developmental stage but differing in oviposition history were offered in no‐choice assays and the time taken to first oviposition attempt was recorded.
4. One short‐lived pro‐ovigenic galler species exhibited a decline with age in time taken to accept a syconium for oviposition. The exact timing of the transition from non‐acceptance to acceptance of less preferred syconia was determined in terms of the proportion of elapsed life span at the transition; this occurred at 25% of elapsed life span.
5. Longer‐lived parasitoids did not show any decline in specificity despite being aged for 50% of their life span. Therefore, host quality, trophic position, egg load and age may individually affect oviposition decisions or have interaction effects.
Agricultural intensification has led to a reduction in semi-natural areas and in the abundance of wild flowering plants, reducing the availability of floral resources upon which pollinating insects depend. This is widely accepted as one of the major drivers of pollinator declines, but few studies have directly addressed the effects of dietary restrictions on pollinator fitness. Here, we investigated the effects of restricting pollen and nectar supply on bumble bee (Bombus terrestris) colony growth, adult size and number. Colonies required up to 6 g pollen/1 g protein and 50 g sugar to establish a colony of 5 workers, and consumed in excess of 176 g pollen/31 g protein and 1,186 g sugar in their lifetime. Regardless of restrictions on pollen or nectar availability, colonies consumed a ratio of 1 g protein to ~43 g sugar, though free-flying colonies require proportionally more sugar to fuel foraging. Food-limited colonies from an early stage grew little with anything less than ad-lib nectar, while more-established colonies increased in weight even with low levels of nectar suggesting a shortage of resources in early spring may be most damaging to bumble bee colonies. Dietary restriction reduced the number of reproductives produced, but had variable effects on the size of workers and males. Nosema ceranae infection was included as a covariate in analyses and had a significant negative effect on colony growth. This study provides a base line for the developmental requirements of bumble bee colonies, and indicates the effects a resource deficit may have on their development and reproduction.
Insect pollinators such as bumblebees (Bombus spp.) are in global decline. A major cause of this decline is habitat loss due to agricultural intensification. A range of global and national initiatives aimed at restoring pollinator habitats and populations have been developed. However, the success of these initiatives depends critically upon understanding how landscape change affects key population-level parameters, such as survival between lifecycle stages, in target species. This knowledge is lacking for bumblebees, because of the difficulty of systematically finding and monitoring colonies in the wild. We used a combination of habitat manipulation, land-use and habitat surveys, molecular genetics and demographic and spatial modelling to analyse between-year survival of family lineages in field populations of three bumblebee species. Here we show that the survival of family lineages from the summer worker to the spring queen stage in the following year increases significantly with the proportion of high-value foraging habitat, including spring floral resources, within 250-1,000 m of the natal colony. This provides evidence for a positive impact of habitat quality on survival and persistence between successive colony cycle stages in bumblebee populations. These findings also support the idea that conservation interventions that increase floral resources at a landscape scale and throughout the season have positive effects on wild pollinators in agricultural landscapes.
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.
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.
Global trends in pollinator-dependent crops have raised awareness of the need to support managed and wild bee populations to ensure sustainable crop production. Provision of sufficient forage resources is a key element for promoting bee populations within human impacted landscapes, particularly those in agricultural lands where demand for pollination service is high and land use and management practices have reduced available flowering resources. Recent government incentives in North America and Europe support the planting of wildflowers to benefit pollinators; surprisingly, in North America there has been almost no rigorous testing of the performance of wildflower mixes, or their ability to support wild bee abundance and diversity. We tested different wildflower mixes in a spatially replicated, multiyear study in three regions of North America where production of pollinator-dependent crops is high: Florida, Michigan, and California. In each region, we quantified flowering among wildflower mixes composed of annual and perennial species, and with high and low relative diversity. We measured the abundance and species richness of wild bees, honey bees, and syrphid flies at each mix over two seasons. In each region, some but not all wildflower mixes provided significantly greater floral display area than unmanaged weedy control plots. Mixes also attracted greater abundance and richness of wild bees, although the identity of best mixes varied among regions. By partitioning floral display size from mix identity we show the importance of display size for attracting abundant and diverse wild bees. Season-long monitoring also revealed that designing mixes to provide continuous bloom throughout the growing season is critical to supporting the greatest pollinator species richness. Contrary to expectation, perennials bloomed in their first season, and complementarity in attraction of pollinators among annuals and perennials suggests that inclusion of functionally diverse species may provide the greatest benefit. Wildflower mixes may be particularly important for providing resources for some taxa, such as bumble bees, which are known to be in decline in several regions of North America. No mix consistently attained the full diversity that was planted. Further study is needed on how to achieve the desired floral display and diversity from seed mixes.
Annual flowering schedules for heathland communities in Scotland were quite similar to published schedules for mediterranean-type shrubland communities at high elevations in Chile but were very different from schedules for mediterranean-type shrubland communities at lower elevations in Chile, Australia and South Africa. Air temperatures were lower at heathland and high elevation, mediterranean-type shrubland sites than at low elevation, mediterranean-type shrubland sites, which probably accounts for differences in the length and seasonal timing of the flowering period. Drought between June and September (= December and March in the Southern Hemisphere) at low elevation, mediterranean-type shrubland sites likely restricted flowering so that more species flowered before the month of peak flowering than afterwards. Drought would be less severe at heathland and high elevation, mediterranean-type shrubland sites because precipitation was more evenly distributed throughout the year and/or air temperatures were lower. Hence, flowering was more evenly distributed around the month of peak flowering. -from Author
A common suggestion to support ecosystem services to agriculture provided by mobile organisms is to increase the amount of natural and seminatural habitat in the landscape. This might, however, be inefficient, and demands for agricultural products limit the feasibility of converting arable land into natural habitat. To develop more targeted means to promote ecosystem services, we need a solid understanding of the limitations to population growth for service-providing organisms. We propose a research agenda that identifies resource bottlenecks and interruptions over time to key beneficial organisms, emphasising their resulting population dynamics. Targeted measures that secure the continuity of resources throughout the life cycle of service-providing organisms are likely to effectively increase the stock, flow, and stability of ecosystem services.
Copyright © 2015. Published by Elsevier Ltd.
Understanding the effects of neonicotinoid insecticides on bees is vital because of reported declines in bee diversity and distribution and the crucial role bees have as pollinators in ecosystems and agriculture. Neonicotinoids are suspected to pose an unacceptable risk to bees, partly because of their systemic uptake in plants, and the European Union has therefore introduced a moratorium on three neonicotinoids as seed coatings in flowering crops that attract bees. The moratorium has been criticized for being based on weak evidence, particularly because effects have mostly been measured on bees that have been artificially fed neonicotinoids. Thus, the key question is how neonicotinoids influence bees, and wild bees in particular, in real-world agricultural landscapes. Here we show that a commonly used insecticide seed coating in a flowering crop can have serious consequences for wild bees. In a study with replicated and matched landscapes, we found that seed coating with Elado, an insecticide containing a combination of the neonicotinoid clothianidin and the non-systemic pyrethroid β-cyfluthrin, applied to oilseed rape seeds, reduced wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Hence, such insecticidal use can pose a substantial risk to wild bees in agricultural landscapes, and the contribution of pesticides to the global decline of wild bees may have been underestimated. The lack of a significant response in honeybee colonies suggests that reported pesticide effects on honeybees cannot always be extrapolated to wild bees.
Spatiotemporal resource continuity promotes persistence of mobile animal populations. Current agricultural landscapes are poor in flowers resources for bumble bees. Available forage crops are predominantly early-season mass-flowering crops (MFC). It has been suggested, but not tested, that scarcity of late-season flower resources are limiting bumble bee populations. We examined whether addition of late-season flowering red clover affected worker, queen and male bumble bee densities. Bumble bees were surveyed in flower-rich uncultivated field borders across 24 landscapes (radius 2 km) with or without a clover field in the centre, varying in semi-natural grassland (SNG) and early MFC availability. Clover fields had over ten times higher worker densities compared to field borders, suggesting red clover as favoured forage. Five times more queens and 71% more males were found in landscapes with clover fields compared to control landscapes, despite these fields constituting less than 0.2% of the landscape area. Both MFC and SNG increased the density of males, but only in the presence of clover fields. Our results suggest that late-flowering red clover positively affects bumble bee reproduction, likely by increasing temporal resource continuity. Interventions such as flower strips can thus have mitigating effects if they release population regulation by late-season resource bottle-necks.
Captive colonies of Bombus terricola Kirby received pollen for 8, 14, or 24 h per day from the time of onset of second brood oviposition until colony decline. The pattern of change of worker body size over time, especially between the first and second broods, varied according to these experimental food regimes. The results indicate that conflicting results reported in the literature, with respect to changes in worker size over the course of colony development, probably can be regarded, at least in part, as the outcome of differences in food supply.
Most populations exist in variable environments. Two sets of theory have been developed to address this variability. Stochastic dynamics focus on variation in population growth rates based on random differences in vital rates such as growth, survival, and reproduction. Transient dynamics focus on short-term, deterministic responses to changes in the stage distribution of individuals. These processes are related: demographic variation shifts stage structures, producing transient responses, which then contribute to the overall variability of population growth rate. The relative contributions of vital rates vs. transient responses to stochastic dynamics, and the implications for transient analyses, are unclear. This study explores the role of transient responses in stochastic dynamics of nine perennial plant species. Across the species, transient responses contributed more on average to variability in annual population growth rates than did variation in vital rates alone. Transient potential of an average matrix was indicative of the contribution of transient dynamics, although these metrics varied greatly across years. Transient responses were often in the opposite direction as demographic variation, suggesting that transient dynamics may at times have a buffering effect on populations. Overall, transient dynamics had an important role in modulating environmental variation, with implications for both processes in understanding stochastic dynamics.
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.
Determining the factors that influence migratory population abundance has been constrained by the inability to connect events in different periods of the annual cycle. Carry-over effects are events that occur in one season but influence individual success the following season and recent empirical evidence suggests that they may play an important role in migratory population dynamics. Using a long distance migratory shorebird as an example, I incorporate carry-over effects and changes in the relative amount of habitat quality into a density-dependent equilibrium population model. The model uses the example where the quality of habitat on the wintering grounds (nonbreeding season) influences breeding output the following summer (breeding season). Carry-over effects, however, may be manifested in a number of other ways that could influence population dynamics. In the simulations, population declines occur when habitat is lost on the wintering grounds. However, results show that carry-over effects can magnify these declines when a disproportionate amount of high quality habitat is lost the previous winter. Simulations also show that carry-over effects can have a relative, positive impact on population size when the majority of habitat that is lost in the previous season is low quality. In this case, the carry-over interacts with density-dependence the following season producing an additive and positive effect, buffering the population from severe declines. To predict changes in population size of migratory animals, it will be important to determine (i) which demographic factors in which season produce strong carry-over effects and, (ii) not just the amount, but the relative quality of habitat that is lost. If carry-over effects are significant, they could potentially mitigate'seasonal compensation effects'from density-dependence, leading to exacerbated population declines.
Four important points in colony development are distinguished: 1) start of egg laying by the queen, leading to the beginning of the eusocial phase, the emergence of the first workers; 2) the switch point, at which the queen switches from laying diploid eggs (producing workers or queens) to the laying of haploid eggs (producing males); 3) onset of queen production reared from diploid eggs; 4) loss of dominance by the queen, expressed by the beginning of aggression on the part of queen and workers, worker oviposition, oophagy and the functional elimination of the queen. -from Authors
North temperate bumble bee colonies produce workers for the first part of the summer, then, at some point, switch to rearing only reproductives. The first occurrence: of males and gynes (new queens) of one bumble bee (Bombus flavifrons) was used to estimate when the reproductive switch point occurred in colonies distributed among 20 discrete subalpine meadows. Occurrence of reproductives in meadows was correlated with forager and flower abundance: males and gynes appear earlier in meadows with high forager and flower densities. While males were observed in each of the 20 meadows, gynes occurred. in only 15. The five meadows where gynes were not observed had lower flower densities: and supported significantly fewer foragers relative to meadows producing gynes. Differences among meadows in phenological patterns of flower availability were not related to the temporal occurrence of reproductive switch points.
Evidence from wildlife and human populations indicates that conditions during early development can have marked effects on the subsequent performance of individuals and cohorts. Likewise, the effects of maternal and, more generally, parental environments can be transferred among individuals between generations. These delayed life-history effects are found consistently and suggestions have been made that they can be one source of both variability and of delayed density dependence in population dynamics. Assessments of several different time series indicate that population variability and delayed density dependence are common and that understanding the mechanisms giving rise to them is crucial for the interpretation and application of such models to basic and applied research. Therefore, it is necessary to assess the different ways in which history in the life history might give rise to variability and delayed density dependence in population dynamics. Here, we build on recent appraisals of the pervasive influence of past environmental conditions on current and future fitness and link the details of these life-history studies to classic features of population dynamics.
Pollination is a vital ecosystem service, which is endangered by the ongoing declines of pollinators. These declines also affect bumblebees ( Bombus spp.), which are important generalist pollinators in agricultural landscapes. Most studies focussing on the conservation of bumblebees have investigated the effects of local flower‐rich habitats on bumblebee density and diversity. However, bumblebee densities do not necessarily correlate with the colonies’ reproductive success (i.e. the presence or absence of males and/or queens).
We analysed the effects of landscape‐wide availability of mass flowering oilseed rape Brassica napus on the growth and sexual reproduction of Bombus terrestris colonies. Thirty‐two young colonies were established and monitored in different resource environments represented by 16 landscapes (circular study areas with 3000 m radius) with large or small amounts of oilseed rape. As an indicator of colony growth, we used weight gain, which was strongly correlated with the numbers of brood cells in the colonies.
The colonies gained significantly more weight in study areas with large amounts of oilseed rape particularly during early colony stages.
Despite early weight gain, the colonies in study areas with large amounts of oilseed rape did not reproduce more successfully. The frequencies of colonies that produced males and/or queens did not differ between the two resource environments.
Synthesis and applications . Early mass flowering oilseed rape has a beneficial effect on colony growth, which however, does not translate into a greater likelihood of colonies producing sexual offspring. This may be due to food plant scarcity later in the colony cycle. Conservation measures should enhance food plant availability in agricultural landscapes, particularly during the most critical phases of the colony cycle: the colony establishment in spring and the reproductive phase in mid‐ to late summer.
1. Bumble bees play a vital role in the pollination of many crops and wild flowers, and plans for their conservation require a knowledge of the dynamics and spatial scale of their foraging flights, which are, at present, poorly understood.
2. We investigated the foraging range and constancy of two colonies of bumble bees Bombus terrestris L. on a mixed arable farm using harmonic radar, which has a unique capability to record the trajectories of insects flying at low altitude in the field.
3. Foraging bees were fitted with lightweight radar transponders and tracked as they flew to and from the nest to forage. The resulting tracks gave information on length, direction and straightness of foraging routes. Superimposition onto a map of the foraging landscape allowed interpretation of the bees’ destinations in relation to the spatial distribution of forage.
4. Outward tracks had a mean length of 275·3 ± 18·5 m (n = 65) and a range of 70–631 m, and were often to forage destinations beyond the nearest available forage. Most bees were constant to compass bearing and destination over successive trips, although one bee was tracked apparently switching between forage patches. Both outward and return tracks had a mean straightness ratio of 0·93 ± 0·01 (n = 99). The bees’ ground speeds ranged from 3·0 m s–1 to 15·7 m s–1 (n = 100) in a variety of wind conditions.
5. The results support the hypothesis that bumble bees do not necessarily forage close to their nest, and illustrate that studies on a landscape scale are required if we are to evaluate bee foraging ranges fully with respect to resource availability. Such evaluations are required to underpin assessments of gene flow in bee-pollinated crops and wild flowers. They are also required when making decisions about the management of bees as pollinators and the conservation of bee and plant biodiversity.
Food availability is a major component of habitat quality. For bumblebee field colonies, it is unknown to what extent reproductive success is limited by food availability relative to other factors such as parasites. To assess the importance of food availability, we carried out a field experiment in the Quebec City area, Canada, in 1999 and 2000, using 45 colonies of Bombus impatiens and B. ternarius. Colonies whose nectar and pollen supplies were increased regularly throughout the season reached larger sizes (in number of workers) and had a higher reproductive success than controls, by 51% and 86% respectively. In particular, food supplementation increased the number of males produced and the probability of producing gynes (young queens). The sex ratio was highly skewed in favour of males overall, and the relative proportion of gynes increased with food supplementation in B. ternarius, but not in B. impatiens. These results suggest that colonies ensure reproduction by producing some males and, given the opportunity (sufficient food availability), will produce gynes. Possible reasons for the increased success of food supplemented colonies are explored. However, despite some clear advantages of having larger food supplies such as the build-up of larger worker populations, food supplementation did not appear to help colonies defend themselves against macroparasites because experimental and control colonies experienced similar levels of parasitism by Psithyrus, Fannia canicularis, Brachicoma devia and Vitula edmandsae.
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.