Updated: Oct 19, 2020
· Anthropogenic influence has led to climate change that is threatening worldwide bee populations that are widely important in a number ecological and industrial aspects.
· Climate warming not only has direct negative implications on bees but indirect ones through interruption in pollinating relationships.
· Climate warming has led to alterations in weather conditions and patterns that have the potential cause bee declines.
· Certain aspects of bees being might act as a buffer against climate change impacts, additionally family level differences might lead to intraspecific variations.
· Monitoring and research must be conducted, and actions carried out to understand and prevent climate impacts on bees.
Anthropogenic impacts on the Earth’s climate, land, ocean and biosphere are so severe that a new ‘epoch’ was established in 2002 to mark the period – the Anthropocene (Zalasiewicz et al., 2011). An epoch is usually defined through differential footprints left on the earth’s geology and where there is still debate as to whether the elevated anthropogenic release of CO2 has left a significant impact as to deserve this label (Steffen et al., 2011; Zalasiewicz et al., 2008) , the Anthropocene has been informally adopted into geological literature and in wider scientific literature as an acceptance and acknowledgement of the period where human influence has been highly impactful upon a host of key worldwide processes. The host of abiotic changes created though anthropogenic means has led to what many believe to be the sixth max extinction (Anthony et al., 2011; Ceballos et al., 2015). Although invertebrates are generally neglected in favour of larger and more charismatic organisms in conservation efforts, bees have received disproportionately more interest. Their declines have been formally recognised by the convention of biological diversity (Biesmeijer et al., 2006), many charities have been established and ‘Save the bees’ is a slogan that has been widely spread and adopted. In addition to this, the international initiative on the conservation of sustainable use of pollinators (IPBES) work continuously with countries, communities and higher bodies such as the United Nations and have devised a worldwide action plan to safeguard wild and managed pollinators (Aizen et al., 2018). Despite these efforts, bee numbers continue to decline and 9% are currently classed as threatened (Potts et al., 2016).
How is climate change affecting bees?
Although there are many reported stressors that can partially explain for worldwide bee population
declines, namely: agricultural intensification methods, agrochemicals, habitat loss and habitat fragmentation (Goulson et al., 2015; Potts et al., 2010), this review will assess climate change particularly as a driver for change in bees. Despite climate change encompassing a wide range of prolonged weather conditions, the breadth of wider literature suggests the most influential climate change factor affecting bees to be climate warming. In 2014 the Intergovernmental panel on climate released information on previous, current and predicted climate changes in the most conclusive and in depth report we have on the topic yet. In this they predicted the average global temperature would rise between 1.1- 5.4 °C by 2090-2099 (Pachauri and Meyer, 2014). The period 1983-2012 was likely the warmest 30 year period on the earth’s surface in the last 1400 years (Stocker et al., 2014) and the rate at which this increase is occurring shows no suggestion of slowing down.
Figure 1 - A map representing global surface temperature increase from 1901-2012. The boxes represented with a ‘+’ are where the trend is significant at the 10% level, boxes without a colour represent areas with less than 70% complete temperature records. This figure was taken directly from the IPCC climate change 2014 synthesis report (Pachauri and Meyer, 2014).
Many insects are small bodied ectotherms and are particularly dependent on specific temperatures to optimise a host of physiological processes (Chown, 2004). Bees are no exception to this rule and have been observed to demonstrate heightened sensitivity to climate warming that interrupts these physiological and metabolic processes (Nooten et al., 2014). Each bee species might be considered firstly to have a climatic optimum and secondly a climatic tolerance (Williams et al., 2007). If neither of these two criteria are met bees might be expected to survive with lowered fitness, migrate, die or adapt in response.
For bees who have been documented to endure warmer temperatures, there have been a handful of responses noted. Thermal limits have been found to dictate behavioural patterns in bumblebees who choose to forage earlier in mornings and later in evenings to avoid optimum daily heat levels (Willmer, 1983), this demonstrates temperature as a dictator of behavioural patterns. In honeybees it has been found that when thermal limits have been reached (40°C), foraging behaviour has ceased completely (Cooper et al., 1985) showing that climate change has the ability to change behaviour in a disadvantageous manner, directly reducing fitness of bees by restricting nutritional intake. In addition to behavioural changes, a warmer temperature has been found to directly decrease the lifespan of bees in a few examples. In Sgolastra et al., 2011 it was found that temperature rises at the end of winter, similar to those that might occur at the start of spring caused premature ejection of juvenile bees from overwinter dormancy. This premature emergence was found to result in unnatural rates of nutrient catabolism and female infertility (Fliszkiewicz et al., 2012), reducing not only lifespan but reproductive potential. In addition to juveniles, temperature rises above optimal levels in adult bees was found to cause stress and reduce their lifespan also (Bosch et al., 2000). Lastly, temperature rises have also been found to cause elevated growth speed but reach smaller mature sizes, a phenomenon also observed in other ectotherms (Kingsolver and Huey, 2007).
Where thermal limits being reached in certain examples has led to reduced fitness, some bee species have been found to track their climate to avoid this. Evidence of migration in bees has been documented in Europe and South America with populations moving upwards in latitude and altitude to areas resembling pre-warming climates (Hofmann et al., 2018; Kerr et al., 2015). Despite lack of a worldwide report on this, these trends are likely occurring elsewhere and have been recorded in a handful of other species including butterflies (Hill et al., 2002). Although in the short-term migration might seem like a suitable response to climate warming, northward and upward movement might not continue to be a viable response as mountainous areas and Northern lands may run out leaving no climate to track.
As well as bee species being documented to leave their native ranges, alien species, pests and pathogens’ elevated invasive ability and virulence might have increased in areas where warming has occurred, affecting functional dynamics of the bees who remain rather than migrate (Walther et al., 2009). If climatic change creates conditions similar to those in an alien species’ native range we can expect to see invasion (Walther et al., 2009), If drastic temperature increases that are currently forecasted occur, a complete change in the community structure might take place (Macdougall and Turkington, 2005), shifting abundances and distributions of bees in certain environments. While non-commercially used alien pollinators are little studied (Schweiger et al., 2010), more research has been done on the honeybee (Apis mellifera) and its spread. It is a lover of warmer climates due to its historical origin in Africa (Whitfield et al., 2006) and possesses a range of thermoregulatory behaviours to combat extreme heat (Kovac et al., 2014) many native bees in temperate and colder climates do not. In addition to this It is a generalist species (Schweiger et al., 2010) and has been widely domesticated, propagated and protected by humans worldwide, leading to an unnatural invasion advantage and leading to population declines for local bees (Roubik and Wolda, 2001; Thomson, 2004; Thomson, 2016).
In addition to alien species, diseases and pathogens might also alter bee native ranges in response to climate warming by colonising previously unattractive regions. This has been seen in the Varroa destructor mite, an agricultural pest to the honeybee which has infected native species causing declines (Thomson, 2016) and might occur in the future with the Tropilaelaps mite, originating from Asia that may move to Europe and North America with a warmer climate and cause widespread population declines (Grünewald, 2010). Warmer climates not only benefit invaders but disadvantage native bees that may fall victim to the beneficial acclimation hypothesis (Tobin et al., 2019), where they are now less suited towards the warmed temperatures and have reduced resistance to infection.
Most bee species are solely reliant on floral resources for nutrition and survival, nectar is consumed by adult’s and pollen consumed by larvae (Petanidou and Vokou, 1990). Reduced interaction between bees and plants therefore would reduce adult numbers but also larval numbers, reducing populations but also slowing the reproductive rate and speed at which dead adults are replaced (Memmott et al., 2007b; Minckley et al., 1994;Pyke et al., 2016). The idea of coextinction has been explored in Dunn et al., 2009, with hypotheses about reductions and extinctions in one species creating the same such result in the other. Examples of this have been seen in parasite species and their hosts (Thacker et al., 2006) but also in pollinator relationships, where angiosperm and floral population dynamics have had corresponding effects on bee community abundances and diversities (Banaszak, 1996; Knight et al., 2009; Potts et al., 2003; Pyke et al., 2016; Thomson, 2016). Climate warming not only has the potential to create temporal mismatches through alterations in phenological patterns but spatial mismatches through alterations in abundance and distribution (Memmott et al., 2007b; Tylianakis et al., 2008). These mismatches may lead to significant reductions in resource availability to bees and consequently lead to population stress and declines.
Figure 2 – How climate warming affects the phenology and distribution of plants (left) and pollinators (right), how these mismatches reduce interactions between the two (middle) and how these mismatches might adversely affect plants and pollinators respectively. This figure was taken from Hegland et al., 2009.
Temporal mismatches have been found to most notably affect bees through increased advancement of spring from winter (Sparks and Menzel, 2002). Anthophilia being small, poikilothermic organisms, means great dependence on the external environment to regulate their desired optimal temperature, this not only affects metabolism and many physiological processes but also means temperature change can affect and dictate seasonal patterns. Bees have been documented to emerge earlier in warmer springs due to reduced juvenile hormone release, the release of this hormone is dictated through temperature and higher temperatures illicit lesser releases that stimulate premature emergence from hibernation (Fliszkiewicz et al., 2012). Where bees have heightened temperature sensitivity (Gordo and Sanz, 2006), plants are thought to be generally less thermally responsive (Willmer, 2012), this has led to relative delayed floral emergence. This difference in seasonal emergence between the two has created a time lag between plants flowering and bees emerging thus reducing pollination interactions and leaving the bees who emerged earlier with less food resources.
Where temporal mismatches address an explicit timescale, spatial mismatches between floral resources and bees might be regarded to address physiological factors excluding phenological influence that reduce floral resource availability. Climate change impacts in this regard have firstly been documented with reference to dry periods and lack of water provision to plants. In certain areas climate warming has led to lower precipitation levels and increased rates of evapotranspiration causing droughts (Aldridge et al., 2011; Devoto et al., 2009) which in turn has negatively affected floral resource provision (Grünewald, 2010; Thomson, 2016). In addition to this and with a greater amount of wider literature surrounding it, climate warming has directly been found to affect floral resource provision also. One way in which this has been observed is through temperature having the ability to affect a plant’s decision to flower. In Liu et al., 2012 it was found that an increase in temperature led to less flower production, in Aldridge et al., 2011 the same was found with flowering being disrupted by higher temperatures as well as increased aridity. Conflicting with the conclusions of these two studies, increases in floral production was seen in response to higher temperatures in Schauber et al., 2002, this suggests that certain plant species are more disadvantaged by temperature increases than others. Bee species more heavily reliant on flowering plants more aptly conditioned to endure temperature increases might benefit after a certain level of warming whereas those that rely on flowering plants that are poorly conditioned will be disadvantaged – particularly in specialists who have few alternative nutrition sources (Biesmeijer et al., 2006; Memmott et al., 2007a).
In addition to the influence temperature has been shown to have on a plant’s choice to flower, the richness of the resources found within these flowers has also been found to change after warming through differential nectar concentrations and pollen count (Pacini et al., 2003; Yuan et al., 2009). Also affected by temperature are floral scents via differential release of volatile organic compounds, which signal to pollinators their willingness to receive them. Temperature that deviates significantly from a plant preferred average in a host of studies has shown to reduce sugar concentrations and volumes. In Hoover et al., 2012 this was shown in pumpkin plants, in Petanidou and Smets, 1996 the Thymus capitatus, a Mediterranean shrub was found to give increased nectar volume and sugar concentration up to 38°C but fell after this point and in soybeans it was found that elevated temperatures reduced pollen production by 30-50% (Koti et al., 2005). The potential disruption of floral scent perception by bees and the reduction in nutritional reward will likely have negative consequences for bees resulting in population declines.
Figure 3 – A diagram representing direct physiological impacts of climate warming on both flowering plants and pollinators, the diagram is taken directly from Victoria L. Scaven, 2013.
Climatic weather extremes
Climate warming and its direct influence on bees has been addressed, what has not been addressed however is the effect this climate warming might have on various weather systems and how that might in turn affect bees also. Where the view on global climate warming is generally consensual and the effects more homogenous, the radiative effects warming has on weather are thought to be more unpredictable and variable (Trenberth, 2012).
This said, one way in which bees might be disadvantaged by climate warming induced weather change is with regard to more intense precipitation and storm events. Firstly, the melting of glaciers has led to a 4% increase in atmospheric water vapour since the 1970s (Trenberth, 2012). This increase in atmospheric water vapour is thought to have increased global precipitation by 5-10%. In addition to this the higher temperatures have led to greater atmospheric carrying capacity meaning more water vapour can be contained within the same area, magnifying hydrological cycle events (Trenberth, 2012). Atmospheric water vapour increases are also thought to have added buoyancy to air flowing in storms and has likely increased the intensity of them. This with the addition of climate warmings increase on sea surface temperatures and influence on temperature flows such as El Niño and La Niña have proved to increase storm and hurricane commonality and intensity (Trenberth, 2012). Although there are no in-depth studies on the effect of strong winds from storms and hurricanes on bee species, I expect them to have damaging effects. The average precipitation increases as well as more intense and common storm events will increase flooding likelihood and severity which will also negatively impact them. Many bees hibernate underground overwinter (Goulson et al., 2015) and additionally the bee families Andrenidae, Megachilidae and Melittidae are ground nesters all year round (Michener, 2000) and will have nests destroyed as a result of this flooding. In Fellendorf et al., 2004, Flooding was found to have devastating effects on the Andrea vaga bee which nested on flood plains near the river Rhine in Switzerland, similar effects can expect to be replicated in other areas – particularly in the middle Americas and Asia where increased precipitation rates and storm incidences are thought to be affected most distinctly (Trenberth, 2012).
Where in these areas storms and flooding might be considered a threat to bee populations, in other areas droughts are of major concern (Trenberth et al., 2003). Particularly these areas include Africa, Southern Europe, Central America, Central Pacific, the coasts of North America and parts of south America. In these areas climate warming has been documented to reduce precipitation rates and increase rates of evapotranspiration leading to land surface drying and drought (Dai, 2011) making these areas hostile for bee survival. Arid conditions in the areas mentioned above combined with higher temperatures has led to desiccation of plants and has not only led to less food and habitat for bees in certain areas (Giannini et al., 2012) but is thought to have contributed towards greater instances of wildfires with more intensity. These wildfires can be expected to have catastrophic impacts on bee populations that share native ranges with such events. For example, the ongoing Australian wildfires are likely to decimate the families Stenotridae, endemic to Australia and Colletidae who are found in abundance here (Michener, 2000).
Not all doom and gloom?
Where climate change is negatively affecting bee species in the variety of manners addressed in the main body of this review, certain aspects of their being might act as a buffer to climate change and increase their resilience to it. One of these aspects is a bee’s ability to track its environment. Where many organisms such as plants are sessile in nature and must endure the effects of climate change and either survive at a lower level of fitness or die, bees are motile and are able to track their environment. Not only are they motile, they transport themselves through the air rather than land meaning any geographical barriers such as bodies of water or mountain ranges can be manoeuvred.
Secondly, bees in some cases have indicated a level of adaption towards the new and hotter climate. Bees generally have a short generation time and swift reproductive cycle which might lend itself to faster evolutionary adaption towards climate change over a much shorter time period than one might anticipate (Gordo and Sanz, 2006). For example in Miller-Struttmann et al., 2015 phenotypic and evolutionary adaption was observed where it was found that in response to a reduction in floral resources of up to 60%, species B. balteatus and B. sylvicola altered their behaviour to forage in a more generalist nature and on more plants. As a result of this, over only 40 years they adapted from having a longer corolla (tongue) and specialising on a few particular flowers to shorter corolla in order to maximise nutritional intake to suit this new generalist behaviour and take advantage of diminishing resources made so by climate change. This adaption is not exclusive to bees either, but has been observed in flowering plants who have been found to flower earlier in spring in order to match the advanced emergence of bee species (Primack et al., 2004; Pyke et al., 2016) and so temporal mismatches defined as a potential cause for bee declines might not be so distinct.
Figure 4 – Commonalities in traits and geography of each seven bee families and how these factors might benefit them with reference to climate warming ‘+’ or disadvantage them ‘-‘. Note that this table highlights any characteristics generally shared by each family and is no definitive evidence to refer all species within the families with. Additionally, much of the ‘Hypothesised climate change influence’ column is based on my personal opinions which are shaped through evidence defined within this review.
How can we ‘save the bees’?
Firstly, efforts to monitor bee populations must be increased in order to inform adaptive management and give conservation efforts to combat climate change impacts a greater degree of specificity. For many taxa, inadequate information and knowledge on a global, regional and local scale means in depth analysis on population sizes and ranges is difficult. A phenomenon known as Wallacean shortfall describes the increasing gaps in knowledge on organisms that get progressively smaller and less complex – this is partly due to smaller organisms being harder to find and count and less complex organisms being less distinguishable from others with similar morphological traits (Whittaker et al., 2005). Wallacean shortfall very much applies to bees and makes surveying and monitoring harder. A potential future direction to utilise further in order to fill gaps in knowledge is to make use of species distribution modelling (SDM) in replacement of other surveying methods. Species distribution modelling uses observed species environmental preferences and predicts species ranges off the basis of this (Martins et al., 2015). SDM modelling is now being widely used in decisions on native ranges and is increasingly being used to support conservation decision making on a range of organisms (Guisan et al., 2013; Loyola et al., 2012; Priscila and Rafael Dias, 2013). Despite it being criticised for its inaccuracy due to the predictive nature it is based upon, SDM modelling is a cost efficient and pragmatic predictor of current and future ranges that should be utilised in full to predict climate changes impact on bee populations and subsequently used in directed conservation initiatives.
Secondly, more research must be conducted to identify more accurately the true impacts of climate change on bees. Distinct lacks in research have created gaps in knowledge of these effects and the few that do exist are mostly with regard to the family apidae (Martins et al., 2015). Currently available literature on the topic leaves no consideration to intraspecific variation and responses. Additionally, research on non-bee taxa should be conducted, firstly on the strength of pollinator relationships between certain bee taxa and the flowers they visit to understand how plant declines might create corresponding declines in the bees that rely upon them. Secondly studies must be conducted on how climate change is destroying the natural ecosystems bees are part of which will additionally have corresponding effects. The knowledge gathered from these increased monitoring and research efforts must be presented to higher bodies and implemented in order to design management policies and formulate relevant protection measures (Aizen et al., 2018). Specific regions more harshly affected by climate change should be identified as areas where bee populations might suffer to a more significant degree and must therefore be paid more attention. Evidence for bees Importance to humans and widespread benefit to society must be spread and the information of their importance as well as negative impacts that would follow in response to their declines propagated in order to drive policy making as well as alter public attitudes.
This review has addressed many responses bees have been documented to exhibit in response climate change elevated through anthropogenic influence. Bees are generally perceived as important pollinators but have been taken for granted, their influence to human well-being via food security, agricultural livelihoods, Biodiversity and ecosystem stability under-appreciated (Potts et al., 2016). Widespread negative impacts are likely to continue in the future should change not occur and climate change impacts not be recognised and combatted through action. Where intraspecific variation may lead to differential climate change responses in bees, the climate change impacts mentioned within this review – climate warming, Pollination relationship interruption and climatic weather extremes can be considered to affect bees worldwide to some degree. Despite some evidence that bees might be partially resistant to the effects of climate change and may adapt towards the unnatural and accelerated climatic conditions pressed upon them, far more must be done by humans to prevent their declines and a host of other taxa alike.
Aizen, M., P. Basu, D. Buchori, L. Dicks, L. Vera, I. Fonesca, and L. Galetto, 2018, Conservation and sustainable use of pollinators, Convention on biological diversity.
Aldridge, G., D. W. Inouye, J. R. K. Forrest, W. A. Barr, and A. J. Miller-Rushing, 2011, Emergence of a mid-season period of low floral resources in a montane meadow ecosystem associated with climate change: Journal of Ecology, v. 99, p. 905-913.
Allaby, M., 2014, Apidae, Oxford University Press.
Anthony, D. B., M. Nicholas, T. Susumu, O. U. W. Guinevere, S. Brian, B. Q. Tiago, M. Charles, L. M. Jenny, L. L. Emily, C. M. Kaitlin, M. Ben, and A. F. Elizabeth, 2011, Has the Earth’s sixth mass extinction already arrived?: Nature, v. 471, p. 51.
Banaszak, B., 1996, Ecological bases of conservation of wild bees, The conservation of bees: Linnean Society symosium, London, Academic Press, p. 55-62.
Biesmeijer, J. C., S. P. M. Roberts, M. Reemer, R. Ohlemüller, M. Edwards, T. Peeters, A. P. Schaffers, S. G. Potts, R. Kleukers, C. D. Thomas, J. Settele, and W. E. Kunin, 2006, Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands: Science (New York, N.Y.), v. 313, p. 351.
Bosch, J., W. P. Kemp, and S. S. Peterson, 2000, Management of Osmia lignaria (Hymenoptera: Megachilidae) populations for almond pollination: Methods to advance bee emergence: Environmental Entomology, v. 29, p. 874-883.
Bryan, N. D., S. Sedonia, F. Jennifer, and G. B. Seán, 2006, The history of early bee diversification based on five genes plus morphology: Proceedings of the National Academy of Sciences, v. 103, p. 15118.
Ceballos, G., P. R. Ehrlich, A. D. Barnosky, A. García, R. M. Pringle, and T. M. Palmer, 2015, Accelerated modern human–induced species losses: Entering the sixth mass extinction: Science Advances, v. 1.
Chown, S., 2004, Insect physiological ecology mechanisms and patterns: Oxford, Oxford : Oxford University Press.
Cooper, P., W. Schaffer, and S. Buchmann, 1985, Temperature Regulation of Honey Bees ( Apis mellifera ) Foraging in the Sonoran Desert, Journal of Experimental Biology, p. 1-15.
Dai, A., 2011, Drought under global warming: a review: Wiley Interdisciplinary Reviews: Climate Change, v. 2, p. 45-65.
Devoto, M., D. Medan, A. Roig‐Alsina, and N. H. Montaldo, 2009, Patterns of species turnover in plant‐pollinator communities along a precipitation gradient in Patagonia (Argentina): Austral Ecology, v. 34, p. 848-857.
Dunn, R. R., N. C. Harris, R. K. Colwell, L. P. Koh, and N. S. Sodhi, 2009, The sixth mass coextinction: are most endangered species parasites and mutualists?: Proceedings of the Royal Society B, v. 276, p. 3037-3045.
Fellendorf, M., C. Mohra, and R. Paxton, 2004, Devasting effects of river flooding to the ground-nesting bee, Andrena vaga (Hymenoptera: Andrenidae), and its associated fauna: Journal Of Insect Conservation, v. 8, p. 311-322.
Fliszkiewicz, M., K. Giejdasz, O. Wasielewski, and N. Krishnan, 2012, Influence of winter temperature and simulated climate change on body mass and fat body depletion during diapause in adults of the solitary bee, Osmia rufa (Hymenoptera: Megachilidae): Environmental Entomology, v. 41, p. 1621-1630.
Giannini, T. C., A. L. Acosta, C. A. Garófalo, A. M. Saraiva, I. Alves-Dos-Santos, and V. L. Imperatriz-Fonseca, 2012, Pollination services at risk: Bee habitats will decrease owing to climate change in Brazil: Ecological Modelling, v. 244, p. 127-131.
Gordo, O., and J. J. Sanz, 2006, Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004: Ecological Entomology, v. 31, p. 261-268.
Goulson, D., E. Nicholls, C. Botias, and E. Rotheray, 2015, Bee declines driven by combined stress from parasites, pesticides, and lack of flowers: Science, v. 347.
Grünewald, B., 2010, Is pollination at risk? current threats to and conservation of bees: GAIA, v. 19, p. 61-67.
Guisan, A., R. Tingley, J. B. Baumgartner, I. Naujokaitis-Lewis, P. R. Sutcliffe, A. I. T. Tulloch, T. J. Regan, L. Brotons, E. McDonald-Madden, C. Mantyka-Pringle, T. G. Martin, J. R. Rhodes, R. Maggini, S. A. Setterfield, J. Elith, M. W. Schwartz, B. A. Wintle, O. Broennimann, M. Austin, S. Ferrier, M. R. Kearney, H. P. Possingham, and Y. M. Buckley, 2013, Predicting species distributions for conservation decisions: Ecology Letters, v. 16.
Hegland, S. J., A. Nielsen, A. Lázaro, A. L. Bjerknes, and Ø. Totland, 2009, How does climate warming affect plant‐pollinator interactions?, Oxford, UK, p. 184-195.
Hill, J. K., C. D. Thomas, R. Fox, M. G. Telfer, S. G. Willis, J. Asher, and B. Huntley, 2002, Responses of butterflies to twentieth century climate warming: implications for future ranges: Proceedings of the Royal Society B: Biological Sciences, v. 269, p. 2163-2171.
Hofmann, M., A. Fleischmann, and S. Renner, 2018, Changes in the bee fauna of a German botanical garden between 1997 and 2017, attributable to climate warming, not other parameters: Oecologia, v. 187, p. 701-706.
Hoover, S. E. R., J. J. Ladley, A. A. Shchepetkina, M. Tisch, S. P. Gieseg, and J. M. Tylianakis, 2012, Warming, C02, and nitrogen deposition interactively affect a plant‐pollinator mutualism: Ecology Letters, v. 15, p. 227-234.
Kerr, J. T., A. Pindar, P. Galpern, L. Packer, S. G. Potts, S. M. Roberts, P. Rasmont, O. Schweiger, S. R. Colla, L. L. Richardson, D. L. Wagner, L. F. Gall, D. S. Sikes, and A. Pantoja, 2015, Climate Change. Climate change impacts on bumblebees converge across continents: Science (New York, N.Y.), v. 349, p. 177.
Kingsolver, J., and R. Huey, 2007, Temperature, size, performance and fitness: Journal of Morphology, v. 268, p. 1093-1093.
Kluger, J., and K. Dell, 2006, The Buzz on Bees: Time, v. 168, p. 56.
Knight, M. E., J. L. Osborne, R. A. Sanderson, R. J. Hale, A. P. Martin, and D. Goulson, 2009, Bumblebee nest density and the scale of available forage in arable landscapes: Insect conservation and diversity., v. 2, p. 116-124.
Koti, S., K. R. Reddy, V. R. Reddy, V. G. Kakani, and D. Zhao, 2005, Interactive effects of carbon dioxide, temperature, and ultraviolet-B radiation on soybean (Glycine max L.) flower and pollen morphology, pollen production, germination, and tube lengths, v. 56.
Kovac, H., H. Käfer, A. Stabentheiner, and C. Costa, 2014, Metabolism and upper thermal limits of Apis mellifera carnica and A. m. ligustica: Official journal of the Institut National de la Recherche Agronomique (INRA) and Deutschen Imkerbundes e.V. (D.I.B.), v. 45, p. 664-677.
Liu, Y., J. Mu, K. J. Niklas, G. Li, and S. Sun, 2012, Global warming reduces plant reproductive output for temperate multi‐inflorescence species on the Tibetan plateau: New Phytologist, v. 195, p. 427-436.
Loyola, R. D., P. Lemes, F. V. Faleiro, J. Trindade-Filho, and R. B. Machado, 2012, severe loss of suitable climatic conditions for marsupial Species in Brazil: challenges and opportunities for conservation (Climate Change and marsupial Species in Brazil), v. 7, p. e46257.
Lucas, J., 1999, Insect-Plant Biology -- From Physiology to Evolution. L.M. Schoonhoven, T. Jerny and J.J.A. van Loon: An International Journal on Plant Growth and Development, v. 28, p. 217-218.
Macdougall, A., and R. Turkington, 2005, Are invasive species the drivers or passengers of change in degraded ecosystems?: Ecology, v. 86, p. 42-55.
Martins, A., D. Silva, P. De Marco, and G. Melo, 2015, Species conservation under future climate change: the case of Bombus bellicosus, a potentially threatened South American bumblebee species: Journal Of Insect Conservation, v. 19, p. 33-43.
Memmott, J., P. G. Craze, N. M. Waser, and M. V. Price, 2007a, Global warming and the disruption of plant-pollinator interactions: Ecology Letters, v. 10, p. 710.
Memmott, J., P. G. Craze, N. M. Waser, and M. V. Price, 2007b, Global warming and the disruption of plant–pollinator interactions: Ecology Letters, v. 10, p. 710-717.
Michener, C. D., 2000, The bees of the world: Baltimore, Md., Baltimore, Md. : Johns Hopkins University Press.
Miller-Struttmann, N. E., J. C. Geib, J. D. Franklin, P. G. Kevan, R. M. Holdo, D. Ebert-May, A. M. Lynn, J. A. Kettenbach, E. Hedrick, and C. Galen, 2015, Functional mismatch in a bumble bee pollination mutualism under climate change: Science (New York, N.Y.), v. 349, p. 1541.
Minckley, R. L., W. T. Wcislo, D. Yanega, and S. L. Buchmann, 1994, Behavior and Phenology of a specialist bee (Dieunomia) and Sunflower (Helianthus) Pollen Availability: Ecology, v. 75, p. 1406-1419.
Münster-Swendsen, M., 1970, The Nesting Behaviour of the Bee Panurgus banksianus Kirby (Hymenoptera, Andrenidae, Panurginae): Insect Systematics & Evolution, v. 1, p. 93-101.
Nooten, S. S., N. R. Andrew, L. Hughes, and M. Sears, 2014, Potential Impacts of Climate Change on insect communities: A transplant experiment: PLoS ONE, v. 9.
Pachauri, R., and L. Meyer, 2014, Climate Change 2014: Synthesis Report., Contribution of Working Groups I, II and III to the Fifth Assessment Report of the
Intergovernmental Panel on Climate Change, Geneva, Switzerland, IPCC.
Pacini, E., M. Nepi, and J. L. Vesprini, 2003, Nectar biodiversity: a short review: Plant Systematics and Evolution, v. 238, p. 7-21.
Petanidou, T., and E. Smets, 1996, Does temperature stress induce nectar secretion in Mediterranean plants?: New Phytologist, v. 133, p. 513-518.
Petanidou, T., and D. Vokou, 1990, pollination and pollen energetics in mediterranean ecosystems: American Journal of Botany, v. 77, p. 986-992.
Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W. E. Kunin, 2010, Global pollinator declines: trends, impacts and drivers: Trends in Ecology & Evolution, v. 25, p. 345-353.
Potts, S. G., V. Imperatriz-Fonseca, H. Ngo, M. A. Aizen, J. Biesmeijer, T. Breeze, L. V. Dicks, L. Garibaldi, R. Hill, J. Settele, and A. Vanbergen, 2016, Safeguarding pollinators and their values to human well-being: Nature, v. 540, p. 220-229.
Potts, S. G., B. Vulliamy, A. Dafni, G. Ne'Eman, and P. Willmer, 2003, Linking bees and flowers: How do floral communities structure pollinator communities?: Ecology, v. 84, p. 2628-2642.
Primack, D., C. Imbres, R. B. Primack, A. J. Miller‐Rushing, and P. Del Tredici, 2004, Herbarium specimens demonstrate earlier flowering times in response to warming in Boston: American Journal of Botany, v. 91, p. 1260-1264.
Priscila, L., and L. Rafael Dias, 2013, Accommodating species climate-forced dispersal and uncertainties in spatial conservation planning: PLoS ONE, v. 8, p. e54323.
Pyke, G. H., J. D. Thomson, D. W. Inouye, and T. J. Miller, 2016, Effects of climate change on phenologies and distributions of bumble bees and the plants they visit: Ecosphere, v. 7, p. n/a-n/a.
Rader, R., J. Reilly, I. Bartomeus, and R. Winfree, 2013, Native bees buffer the negative impact of climate warming on honey bee pollination of watermelon crops: Global Change Biology, v. 19, p. 3103-3110.
Roubik, D. W., and H. Wolda, 2001, Do competing honey bees matter? Dynamics and abundance of native bees before and after honey bee invasion: Population Ecology, v. 43, p. 53-62.
Schauber, E. M., D. Kelly, P. Turchin, C. Simon, W. G. Lee, R. B. Allen, I. J. Payton, P. R. Wilson, P. E. Cowan, and R. E. Brockie, 2002, masting by eighteen New Zealand plant species: the role of temperature as a synchronizing cue: Ecology, v. 83, p. 1214-1225.
Schweiger, O., J. C. Biesmeijer, R. Bommarco, T. Hickler, P. E. Hulme, S. Klotz, I. Kühn, M. Moora, A. Nielsen, R. Ohlemüller, T. Petanidou, S. G. Potts, P. Pyšek, J. C. Stout, M. T. Sykes, T. Tscheulin, M. Vilà, G. R. Walther, C. Westphal, M. Winter, M. Zobel, and J. Settele, 2010, Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination: Biological Reviews, v. 85, p. 777-795.
Sgolastra, F., W. P. Kemp, J. S. Buckner, T. L. Pitts-Singer, S. Maini, and J. Bosch, 2011, The long summer: Pre-wintering temperatures affect metabolic expenditure and winter survival in a solitary bee: Journal of Insect Physiology, v. 57, p. 1651-1659.
Smith, K., E. Loh, M. Rostal, C. Zambrana-Torrelio, L. Mendiola, and P. Daszak, 2013, Pathogens, pests, and economics: drivers of honey bee colony declines and Losses: One Health - Ecology & Health - Public Health | Official journal of International Association for Ecology and Health, v. 10, p. 434-445.
Soltis, P. S., and D. E. Soltis, 2004, The origin and diversification of angiosperms: American Journal of Botany, v. 91, p. 1614-1626.
Sparks, T. H., and A. Menzel, 2002, Observed changes in seasons: an overview: International Journal of Climatology, v. 22, p. 1715-1725.
Steffen, W., J. Grinevald, P. Crutzen, and J. McNeill, 2011, The Anthropocene: conceptual and historical perspectives: Philosophical Transactions of the Royal Society A, v. 369, p. 842-867.
Stocker, T. F., D. Qin, G. K. Plattner, M. M. B. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, 2014, Climate change 2013 the physical science basis: Working Group I contribution to the fifth assessment report of the intergovernmental panel on climate change, v. 9781107057999, 1-1535 p.
Thacker, J. I., G. W. Hopkins, and A. F. G. Dixon, 2006, Aphids and scale insects on threatened trees: co-extinction is a minor threat: Oryx, v. 40, p. 233-236.
Thomsett-Scott, B., 2017, Encyclopaedia of the History of Science, Technology, and Medicine in Non-Western Cultures: Reference Reviews, v. 31, p. 29-30.
Thomson, D., 2004, Competitive interactions between the invasive European honeybee and native bumble bees: Ecology, v. 85, p. 458-470.
Thomson, D. M., 2016, Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources: Ecology Letters, v. 19, p. 1247-1255.
Tobin, K. B., A. C. Calhoun, M. F. Hallahan, A. Martinez, and B. M. Sadd, 2019, Infection Outcomes are Robust to Thermal Variability in a Bumble Bee Host-Parasite System: Integrative and Comparative Biology, v. 59, p. 1103-1113.
Trenberth, E., A. Dai, M. Rasmussen, and D. Parsons, 2003, The Changing Character of Precipitation, Boulder, Colorado, The national center for atmospheric research.
Trenberth, K., 2012, Framing the way to relate climate extremes to climate change: An Interdisciplinary, International Journal Devoted to the Description, Causes and Implications of Climatic Change, v. 115, p. 283-290.
Tylianakis, J. M., R. K. Didham, J. Bascompte, and D. A. Wardle, 2008, Global change and species interactions in terrestrial ecosystems, Oxford, UK, p. 1351-1363.
Victoria L. Scaven, N. E. R., 2013, Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions: Current Zoology, v. 59, p. 418-426.
Walther, G.-R., A. Roques, P. E. Hulme, M. T. Sykes, P. Pyšek, I. Kühn, M. Zobel, S. Bacher, Z. Botta-Dukát, H. Bugmann, B. Czúcz, J. Dauber, T. Hickler, V. Jarošík, M. Kenis, S. Klotz, D. Minchin, M. Moora, W. Nentwig, J. Ott, V. E. Panov, B. Reineking, C. Robinet, V. Semenchenko, W. Solarz, W. Thuiller, M. Vilà, K. Vohland, and J. Settele, 2009, Alien species in a warmer world: risks and opportunities: Trends in Ecology & Evolution, v. 24, p. 686-693.
Whitfield, C. W., S. K. Behura, S. H. Berlocher, A. G. Clark, J. S. Johnston, W. S. Sheppard, D. R. Smith, A. V. Suarez, D. Weaver, and N. D. Tsutsui, 2006, Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera: Science (New York, N.Y.), v. 314, p. 642.
Whittaker, R. J., M. B. Araújo, J. Paul, R. J. Ladle, J. E. M. Watson, and K. J. Willis, 2005, Conservation Biogeography: assessment and prospect: Diversity and Distributions, v. 11, p. 3-23.
Williams, P. H., M. B. Araújo, and P. Rasmont, 2007, Can vulnerability among British bumblebee ( Bombus) species be explained by niche position and breadth?: Biological Conservation, v. 138, p. 493-505.
Willmer, P., 1983, Thermal constraints on activity patterns in nectar-feeding insects., Ecological entomology.
Willmer, P., 2012, Ecology: Pollinator–Plant Synchrony Tested by Climate Change: Current Biology, v. 22, p. R131-R132.
Willmer, P., 2014, Climate Change: Bees and Orchids Lose Touch: Current Biology, v. 24, p. R1133-R1135.
Yuan, J. S., S. J. Himanen, J. K. Holopainen, F. Chen, and C. N. Stewart, 2009, Smelling global climate change: mitigation of function for plant volatile organic compounds: Trends in Ecology & Evolution, v. 24, p. 323-331.
Zalasiewicz, J., M. Williams, A. Haywood, and M. Ellis, 2011, The Anthropocene: a new epoch of geological time?: Philosophical Transactions of the Royal Society A, v. 369, p. 835-841.
Zalasiewicz, J., M. Williams, A. Smith, T. L. Barry, A. L. Coe, P. R. Bown, P. Brenchley, D. Cantrill, A. Gale, P. Gibbard, F. J. Gregory, M. W. Hounslow, A. C. Kerr, P. Pearson, R. Knox, J. Powell, C. Waters, J. Marshall, M. Oates, P. Rawson, and P. Stone, 2008, Are we now living in the Anthropocene: GSA Today, v. 18, p. 4.