The mutualism between plants and their pollinators provides globally important ecosystem services, but it is likely to be disrupted by global warming that can cause mismatches between both halves of this interaction. In this review, we summarise the available evidence on (i) spatial or (ii) phenological shifts of one or both of the actors of this mutualism. While the occurrence of future spatial mismatches is predominantly theoretical and based on predictive models, there is growing empirical evidence of phenological mismatches occurring at the present day. Mismatches may also occur when pollinators and their host plants are still found together. These mismatches can arise due to (iii) morphological modifications and (iv) disruptions to host attraction and foraging behaviours, and it is expected that these mismatches will lead to novel community assemblages. Overall plant–pollinator interactions seem to be resilient biological networks, particularly because generalist species can buffer these changes due to their plastic behaviour. However, we currently lack information on where and why spatial mismatches do occur and how they impact the fitness of plants and pollinators, in order to fully assess if adaptive evolutionary changes can keep pace with global warming predictions.

Introduction

The effects of a warming climate on species fitness and persistence are becoming more apparent, with an increasing number of studies demonstrating its multiple impacts on biodiversity year on year [1–3]. This global change can directly affect the fitness of species across their current ranges but it can also alter, perhaps more subtly, their ecological interactions [4]. In terrestrial ecosystems, one crucial ecological interaction is the pollination of plants by animals, an interaction largely dominated by insects [5], representing 9.5% of global food production [6]. Global warming has the potential to disrupt this mutualism, leading to potential mismatches (i.e. a failure to achieve an efficient interaction) hence putting plant and pollinator species at risk of extinction [7]. The number of studies demonstrating this effect is growing, and many different methods have been described to assess it empirically ([8], reviewed in [9]).

First, mismatches in plant–pollinator interactions can occur through reduced co-occurrence of the interacting partners in a shared habitat; this reduction may be temporal or spatial. These kinds of mismatches have received growing attention [10,11], particularly those of temporal mismatches between plants and pollinating insects [12]. These mismatches can be driven by a change in the flowering period of the plant [13] and/or the phenology of the pollinator [14], either of which can be advanced or delayed. The co-occurrence of plants and pollinators, essential for the interaction to occur, can also be spatially disrupted. The geographic overlap between interacting partners may decrease or increase under global warming [15–16] depending on the plasticity, adaptability and life-history traits of the species in question [17].

In addition to temporal or spatial mismatches, global warming also has the potential to impact plant–pollinator interactions that are mediated by physiological and/or morphological traits. The mechanical fit of the interaction can be affected, as pollination success can be dependent on morphological traits such as tongue length or overall body size in order to have access to plant resources, as well as plant morphology [18]. For example, increasing average temperatures have been shown to negatively affect body size in many organisms [19]. Moreover, temperature increases can impact the foraging behaviour of the pollinator [20], the attractiveness of the plant [21], as well as the quality and quantity of plant resources [22].

Here, we summarise the current knowledge about the effects of global warming in driving mismatches between plants and pollinators (Figure 1, Table 1). Though other climatic variables such as precipitation frequency, ozone (O3) concentration or carbon dioxide (CO2) concentration can also affect these interactions [23], we restrict our review to the impact of global warming as it is the most extensively studied. Within this framework, we first explore the way in which (i) spatial and (ii) temporal mismatches can affect plant–pollinator interactions before assessing the impact of (iii) morphological mismatches and (iv) modification of foraging behaviours and host attraction. Finally, we assess the likely ecological and evolutionary consequences, as well as factors that may buffer against the potential mismatches between plants and pollinators.

Wrong time, wrong place: phenological and spatial mismatches

Global warming can have a strong impact on the activity pattern and life cycle development of organisms [9]. Many phenological shifts have already been reported at the species level for the insect emergence (e.g. [24,25]) or blooming time of flowering plants (e.g. [13]). Most of the studies showed a simultaneous advance in the phenology of pollinators and plants over the studied period in parallel with increasing average temperatures, but alternative patterns (i.e. simultaneous delays or opposite shifts) have also been described [25,26]. Mismatches between the emergence of bee species and the blooming of their main resources have been specifically recorded [26]. However, as far as we know, there is no study on the direct impact of these mismatches on pollinator individual fitness or population trends. In contrast, plants that flower earlier can miss part of the activity window of their main pollinators [27] and show a decrease in seed production [28]. Moreover, as these phenological shifts tend to be species specific for each species of the pollinator network, ecological communities are also disturbed. Duchenne et al. [25] recently demonstrated that non-random phenological shifts of European pollinators reduce the redundancy and the functional complementarity of their assemblages. Such a decrease in redundancy might alter the robustness of plant–pollinator networks to ongoing pollinators’ extinctions [10]. Additionally, the decrease in functional complementarity can decrease the provision of pollination services [29] with fewer visits to a lower diversity of plants [30], probably resulting in a negative feedback for pollinators. These modifications in species community phenology can, therefore, potentially impact the performance of one of the most important ecosystem services for agriculture [26].

If a plant species and the insects that pollinate it occupy slightly different climatic niches, a warming climate has the potential to cause a spatial mismatch between the two if their distributions diverge. There are multiple examples of range shifts in pollinators that are probably driven by climate change (e.g. [31]), with the changes in bumblebees (Bombus spp.) particularly well documented. Bumblebees are cold-adapted species, and have shifted to more northern latitudes and to higher altitudes over the last 100 years [32,33]. Likewise, many plant species are also predicted to undergo similar changes [34]. However, there are few studies that have considered spatial changes in plant and pollinator communities at the same time or have observed this phenomenon in the field.

The situation is complicated further because pollination systems tend towards generalisation, with pollinators visiting multiple plant species and plant species being visited by multiple pollinator species [35]. Examples of individual plant species pollinated almost entirely by a single insect species that is, in turn, almost completely dependent on it for its own survival are the exception, rather than the rule (e.g. [36]). A simulation model incorporating different scenarios of species co-extinction and capacities for partner switches showed that projected plant extinctions under climate change are more likely to trigger animal co-extinctions than vice versa, with specialist pollinators being the most sensitive [37]. This contrasts with, for example, herbivory in butterflies (Lepidoptera) in which the majority of species are much more tightly bound to specific host plants [38]. A spatial divergence between the two is, therefore, more straightforward to model because a reduced area of overlap has clear negative fitness implications for the butterfly that cannot reproduce without its host plant [17,39]. Because pollinators may be generalised and therefore able to use different host plants across their range, and plants may also be variably dependent on pollination itself across their range [40], diverging spatial ranges will not necessarily have any fitness impacts on either group.

Examples of potential spatial mismatch come from models that predict the spatial distribution of plants and their pollinators separately under climate change scenarios, and then measure the extent to which these diverge (e.g. [41]). However, because these are predictions about the future, these models have necessarily not yet been verified. Where empirical observational studies have been conducted at a small spatial scale, though bumblebee pollinators moved to a higher altitudinal elevation over a 50-year period at a faster rate than flowering plants, the magnitude of this change was not great enough that they ceased to come into contact with the same suite of plant species [33]. Although, to date, climate-induced spatial mismatches between plants and pollinators have not been observed [9,11], marginal changes of a lower magnitude could occur which would reduce, but not eliminate, spatial co-occurrence. Studies that compare bee and plant interactions in the same region using a historic dataset and comparing it to the present day offer the opportunity to detect lost interactions and to attribute these to a lack of spatial or temporal co-occurrence. One such study [42] found that, of the lost interactions that were not caused by the extirpation of pollinator species, 41% were caused by a lack of spatial co-occurrence and 53% by a lack of temporal co-occurrence. However, because the environment in which this study was carried out has been highly fragmented between the two time periods it is unclear to what extent these changes can be attributed to climatic factors.

Right time, right place but…

Morphological mismatches

The response of insect body size to global warming is generally consistent: It has largely been observed that it decreases at higher ambient temperatures, probably because of higher metabolic rate and accelerated development (i.e. following the temperature-size rule [19,43,44]). This decrease can subsequently impact the thermoregulatory activity of pollinators. For example, it has been shown that larger bees are better able to thermoregulate than smaller ones [45], even if hair colour and thickness also impact this ability [46]. The responses of flower size and plant height to global warming seem to be far less consistent and very species-specific. At higher temperatures than the optimum level for a species (which can additionally be different for vegetative or reproductive parts [47]), a decrease in flower diameter [48] or in plant height [49] can be observed, but there is no consensus that global warming will systematically affect plant morphology or resource accessibility [50,51] as the converse pattern has also been observed [52].

Floral morphology is partly linked to the natural selection exerted by pollinator morphology and vice versa [35,53]. If the degree of morphological matching is high, it potentially implies a strong reciprocal selection because any change to this matching could result in fitness impacts for either or both partners [53]. However, if the level of matching is low, it potentially implies a low reciprocal selection because of the high variability of the phenotypes involved in the interaction [53]. Nonetheless, in many plant–pollinator interactions, morphological matching requires precision and a consistent mechanistic fit between the two actors to ensure the contact between the sexual parts of the flower (i.e. pollen and stigma) and the body of the pollinator and therefore efficient pollination [54]. Floral morphology is thus linked to the pollinator taxa that they attract, notably because of the relationship between the length of nectar spurs, corolla tubes and the proboscis of the pollinator (e.g. [54,55]). The relationship between proboscis length and corolla depth has been investigated in various groups like euglossine and solitary bees [54] and butterflies [18]. In most of these studies, species with longer proboscises visit a wider range of flowers, and all of the studies highlighted a positive relationship between proboscis length and the depth at which nectar is produced.

As an example of a potential morphological mismatch, two bumblebee species have evolved shorter tongue lengths over the last 40 years while their associated flowers have not become shallower [57]. This tongue size matching is particularly crucial as it has been showed recently to be a strong driver of foraging efficiency in multi-species assemblages [58]. The overall size matching will also determine the efficiency of pollen transfer: smaller pollinators (with on average shorter tongues) can have lower pollination efficiency (e.g. [59] but see [60]) through reduced pollen delivery, therefore, having a lower single-visit pollen deposition rate and seed set while large- or middle-sized species are, most of the time, more likely to have greater contact with anthers and stigma and therefore have a greater pollination efficiency [61]. Most of the studies have focused on pollen deposition and the pattern is largely constant. However, with regards to pollen removal from anthers, results are less consistent and some of them indicate that pollen removal efficiency is independent from body size [62]. Indeed, many other morphological features from both partners are driving pollination efficiency, notably hair characteristics (e.g. size and density) [58,59] which can also be impacted by temperatures during development [60]. Overall, morphological mismatches between plants and pollinators are most likely to occur within plant species displaying specialised flower morphologies as their morphological fit with pollinators is most restricted [51].

Disruption to host attraction and foraging behaviours

Like most phytophagous insects, pollinators are known to rely on olfactory cues (specific volatile organic compounds [VOCs] in a specific ratio) to recognise host plants at a distance [63,64]. A modification in the composition or the perception of the VOCs can, therefore, lead to the breakdown of the recognition process. It has been shown that changes in ambient temperature can affect volatile emissions from flowers, altering the quality of the signal [65]. Warming not only increases rate and abundance of floral VOC emissions, but also changed the ratios among compounds that constituted the floral scents. This response of floral emissions to temperature differed among species and among different compounds within species [65]. Such species-specific modification of the volatile blend emitted may impair plant–pollinators interactions if pollinators become confused with a more fragrant atmosphere, or are no longer attracted to their host-plant floral cues. Moreover, visual stimuli displayed by plants also appear to play a major role in host selection [66]. Several studies have already shown that the stress of high temperatures affects both vegetative and floral morphological traits, and higher temperatures can reduce plant height [67], cause flower deformity (i.e. floral organ malformation; [68]), lead to lighter flower colours [69], reduce the number of flowers as well as flower size [70], advance the timing of the anthesis [71] and limit the production of floral resources [72].

Regarding the direct effect on pollinators, we only can speculate that higher temperatures might denature key proteins in olfaction (i.e. odorant-binding proteins and olfactory receptors [73]). It is already known that proteotoxic stressors (e.g. heat stress) can cause proteins to misfold and denature, resulting in a loss of biological function [74,75]. However, such heat denaturation of proteins involved in olfaction remains unlikely since they are particularly stable to thermal denaturation [76]. Exposure of pollinators to high temperatures may nevertheless induce serious damages such as denaturation of non-antennal proteins, disturbance of the nervous and endocrine systems, damage to DNA but also the alteration of the liquid-crystalline fluidity of the membrane, which could disrupt the whole organism and lead to death ([77], reviewed in [78]).

Elevated temperatures can also alter resource nutritional quality for pollinators as pollen appears to be particularly sensitive to heat (e.g. [79]). High temperatures can lead to a decrease in pollen viability, which is associated with changes in several metabolites [80]. For instance, heat stress can decrease the concentration of soluble carbohydrates [81] and proline [69] as well as alter the phospholipid content of pollen [82]. Moreover, plants may produce a repertoire of secondary metabolites in response to temperature rises [83]. Such increases in secondary metabolites as well as the accumulation of reactive oxygen species are likely to occur in pollen and may be detrimental to pollinators [84]. All these changes in pollen composition might decrease its suitability to pollinators, reducing their performance and health status [85,86]. Finally, these changes in pollen development and viability could also affect plant fitness as they could disrupt plant fertilisation and lead to a reduction in fruit and seed sets [87,88].

In addition, nectar chemical composition (i.e. sugar concentration) can also be affected by an increase in temperature, but to a lesser extent than pollen composition and nectar volume [79,89]. However, these modifications in nectar sugar concentration can compromise pollinator attractiveness and flower visitation rate [89], as bumblebees are able to discriminate between small differences in nectar concentration and prefer sugar concentrations higher than 40% [90]. In the same way, pollen quality can drive host selection and flower visitation [91,92]. Effects of global warming on pollen and nectar quality are, therefore, expected to affect pollinators as well as plant reproductive fitness.

Another cue that pollinators, especially bees, can use to recognise flowers is floral temperature. By using thermal detectors in their antennae and tarsi, bees can detect differences in overall flower temperature [93]. Previous studies have shown that bees prefer to collect warm nectar from flowers at low ambient temperatures [94]. However, this preference for warmer flowers may be context-dependent as shown by Australian stingless bees (Trigona carbonaria) that preferred warmer nectars at lower air temperatures (from 23 to 30°C), but changed their behaviour and selected ambient temperature nectar over warmer nectar when the air temperature reached 34°C [95]. While some plant species appear to modulate their temperature in a way consistent with bee preferences, other appear to lack a cooling mechanism, suggesting that they may be less attractive to bee pollinators under higher temperatures [96]. Regarding all these effects on sensory cues used by pollinators for host attraction, global warming is probably already disrupting the interactions between plants and pollinators since all these modifications might alter the attractiveness of flowers to pollinators and impact their foraging behaviour [89]. On the other hand, global warming may also alter foraging behaviour from the pollinator point of view. Learning abilities (i.e. association between floral traits and rewards [97]) of some pollinators such as bumblebees could be affected, therefore, impacting discrimination between sensory cues. This could impede the plasticity of pollinator behaviour (i.e. modification of their foraging behaviour as a response of altered floral traits) and threaten the plant–pollinator interactions.

Conclusions and perspectives

Mismatches in the interactions between plants and pollinators will lead to the emergence of new biological networks and communities (e.g. [98]). Though some communities will experience the loss of existing interactions, other communities could gain novel interactions [98,99]. Some communities could be more severely impacted. For example, stresses such as more frequent and intense heatwaves could predominantly impact summer-flowering communities through decreasing nectar production (particularly in Mediterranean regions where the temperatures are already very high) because the optimal temperature of nectar production is more likely to be exceeded. On the other hand, spring-flowering communities could be more severely impacted by phenological mismatches with their host plants that to date have been more frequently observed during the spring [100,101].

A certain level of variation in matches and mismatches is thought to be common in networks subject to co-evolutionary dynamics [53]. Based on ‘the most effective pollinator’ principle [102], floral traits should evolve to attract and match with the most abundant and effective pollinators. We may expect, therefore, when plant–pollinator interactions are predominantly generalist in nature, pollinators will show plasticity and be able to adapt to changes. In contrast, specialised pollinators will show limited plasticity in their response and therefore be less resilient to climate warming ([103] but see [23]). Indeed, generalist species are mostly less affected or even favoured by changing communities while species with narrower niches tend to be at higher risk of extinction [16]. Under changing conditions, this core of generalist species could partly sustain the plant–pollinator network, buffering the effects of climate change. Plant–pollinator networks are expected to be more stable and resilient to changes than host–parasitoid networks because of their nested and dynamic structures which act as a buffer against perturbations or cascading effects of species loss [10,11]. However, as such networks may be disrupted at both spatial and temporal scales and synergistic effects of additional detrimental factors (e.g. agricultural changes, pesticides, resource availability [104]), there is the potential for the resilience of the plant–pollinator network to be substantially weakened [51]. Whereas pollinators can offset local limitation of floral resources or nesting sites through their flight ability, plant populations are more threatened at the local scale by the reduction in the abundance of effective pollinators and soil nutrients limitation [11]. However, even if plants are sessile, simulation models incorporating different scenarios of species extinction and abilities to switch from host plant or associated pollinators showed that under climate change, the impact of host plant extinction could have a higher chance of causing the co-extinction of their pollinators than the converse scenario, thus the more likely extinctions cascades would come from plants to pollinators [37].

As the pace of climate change is fast compared with the historical baseline, if species are to persist then species adaptation has to be equally fast, and the phenomenon of rapid evolution is known to be a crucial ecological process for species persistence [1]. The asynchrony resulting from spatial and/or temporal mismatches will be subject to selection and the ability of plants and pollinators to adapt remain unclear. To address this current knowledge gap, we need ambitious strategies for monitoring plants and their pollinators, not only to detect shifts in their temporal and spatial distribution (Table 1), but also in their phenotypic distribution [105]. So far only a limited pollinator diversity has been studied in these contexts; in detail, evidence for phenological mismatches as a result of microevolutionary responses has already been observed [106], thus a critical challenge is now to assess if the pace of adaptive evolutionary changes will be fast enough the track climate warming and prevent species extinctions [107]. Moreover, host shifts due to climate warming could also be observed, which could buffer the detrimental effects of changing conditions for pollinators [108]. Nevertheless, the last decade has seen much progress in the description and understanding of global warming and its impact on complex plant–pollinator networks even if responses in the field have been documented far less than responses under laboratory conditions. These advances should help us to mitigate the effects of global changes to sustain pollinator communities and pollination services.

Summary

  • Global warming is a major threat for biodiversity, impacting both species and their interactions. A fundamental interaction in terrestrial ecosystems is the mutualism between pollinators and their host plants.

  • Global warming can induce spatial and temporal mismatches when species fail to co-occur. While spatial mismatches are still poorly observed, there is growing evidence that temporal mismatches can reshape interactions within pollination networks.

  • Mismatches can also occur between species that still co-occur. These can be due to morphological modifications, disruption to host attraction and foraging behaviours, as well as shifts in the quality of floral resources.

  • Our understanding of the effects of global warming on this mutualism has advanced substantially and the resilience of plant–pollinator networks to changing conditions seems to be high. However, we still require field-realistic results based on ambitious datasets to assess to which extent the mismatches do occur.

Competing Interests

The authors declare that there are no competing interests associated with the manuscript.

Author Contribution

M.G., M.V., T.W. and D.M. conceived the ideas. M.G. lead the writing of the manuscript. M.G., M.V., T.W. and D.M. were each responsible of the redaction of one or several sub-chapters.

Acknowledgements

This work was partly supported by the ‘Fonds de la Recherche Scientifique — FNRS’ and the Fonds ‘Wetenschappelijk Onderzoek — Vlaanderen (FWO)’ under EOS Project (n°3094785) and the Belgian Science Policy (project BR/132/A1/BELBEES). MV is supported by the ARC project ‘METAFLORE’.

Abbreviations

     
  • VOCs

    volatile organic compounds

References

References
1
Parmesan
,
C.
(
2006
)
Ecological and evolutionary responses to recent climate change
.
Ann. Rev. Ecol. Evol. Syst.
37
,
637
669
2
IPBES (Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services)
(
2019
)
Summary for policymakers of the global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. S. Díaz, J. Settele, E. S. Brondizio E.S., H. T. Ngo, M. Guèze, J. et al. (eds.). IPBES secretariat, Bonn, Germany. 53 pp
3
United Nations
(
2015
)
Millennium Development Goals Report. United Nations. Accessed January 20th 2020. Available from: https://www.un.org/millenniumgoals/2015_MDG_Report /pdf/MDG%202015%20rev%20%28July%201%29.pdf
4
Ockendon
,
N.
,
Baker
,
D.J.
,
Carr
,
J.A.
,
White
,
E.C.
,
Almond
,
R.E.A.
,
Amano
,
T.
et al (
2014
)
Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects
.
Glob. Change Biol.
20
,
2221
2229
5
Ollerton
,
J.
,
Winfree
,
R.
and
Tarrant
,
S.
(
2011
)
How many flowering plants are pollinated by animals?
Oikos
120
,
321
326
6
Gallai
,
N.
,
Salles
,
J.M.
,
Settele
,
J.
and
Vaissière
,
B.E.
(
2009
)
Economic valuation of the vulnerability of world agriculture confronted with pollinator decline
.
Ecol. Econ.
68
,
810
821
7
Scheffers
,
B.R.I.
,
De Meester
,
T.C.L.
,
Bridge
,
A.A.
,
Hoffmann
,
J.M.
,
Pandolfi
,
R.T.
,
Corlett
,
S.H.M.
et al (
2016
)
The broad footprint of climate change from genes to biomes to people
.
Science
354
,
aaf7671
8
Scaven
,
V.L.
and
Rafferty
,
N.E.
(
2013
)
Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions
.
Curr. Zool.
59
,
418
426
9
Byers
,
D.L.
(
2017
)
Studying plant–pollinator interactions in a changing climate: a review of approaches
.
Appl. Plant Sci.
5
,
1700012
10
Memmot
,
J.
,
Craze
,
P.G.
,
Waser
,
N.M.
and
Price
,
M.V.
(
2007
)
Global warming and the disruption of plant–pollinator interactions
.
Ecol. Lett.
10
,
710
717
11
Hegland
,
S.J.
,
Nielsen
,
A.
,
Lazaro
,
A.
,
Bjerknes
,
A.L.
and
Totland
,
O.
(
2009
)
How does climate warming affect plant–pollinator interactions?
Ecol. Lett.
12
,
184
195
12
Monahan
,
W.B.
,
Rosemartin
,
A.
,
Gerst
,
K.L.
,
Fisichelli
,
N.A.
,
Ault
,
T.
,
Schwartz
,
M.D.
et al (
2016
)
Climate change is advancing spring onset across the US national park system
.
Ecosphere
7
,
e01465
13
Menzel
,
A.
,
Sparks
,
T.H.
,
Estrella
,
N.
,
Koch
,
E.
,
Aasa
,
A.
,
Ahas
,
R.
et al (
2006
)
European phenological response to climate change matches the warming pattern
.
Glob. Change Biol.
12
,
1969
1976
14
Roy
,
D.B.
and
Sparks
,
T.H.
(
2000
)
Phenology of British butterflies and climate change
.
Glob. Change Biol.
6
,
407
416
15
Pompe
,
S.
,
Hanspach
,
J.
,
Badeck
,
F.
,
Klotz
,
S.
,
Thuiller
,
W.
and
Kühn
,
I.
(
2008
)
Climate and land use change impacts on plant distributions in Germany
.
Biol. Lett.
4
,
564
567
16
Settele
,
J.
,
Kudrna
,
O.
,
Harpke
,
A.
,
Kühn
,
I.
,
van Swaay
,
C.
,
Verovnik
,
R.
et al (
2008
)
Climatic risk atlas of European butterflies
.
BioRisk
1
,
1
710
17
Schweiger
,
O.
,
Settele
,
J.
,
Kudrna
,
O.
,
Klotz
,
S.
and
Kühn
,
I.
(
2008
)
Climatic change can cause spatial mismatch of trophically interacting species
.
Ecology
89
,
3472
3479
18
Corbet
,
S.A.
(
2000
)
Conserving compartments in pollination webs
.
Conserv. Biol.
14
,
1229
1231
19
Gérard
,
M.
,
Michez
,
D.
,
Debat
,
V.
,
Fullgrabe
,
L.
,
Meeus
,
I.
,
Piot
,
N.
et al (
2018
)
Stressful conditions reveal decrease in size, modification of shape but relatively stable asymmetry in bumblebee wings
.
Sci. Rep.
8
,
15169
20
Willmer
,
P.G.
and
Stone
,
G.N.
(
2004
)
Behavioral, ecological and physiological determinants of the activity patterns of bees
.
Adv. Study Behav
34
,
347
466
21
Yuan
,
J.S.
,
Himanen
,
S.J.
,
Holopainen
,
J.K.
,
Chen
,
F.
and
Stewart
,
C.N.
(
2009
)
Smelling global climate change: mitigation of function for plant volatile organic compounds
.
Trends Ecol. Evol.
24
,
323
331
22
Pacini
,
E.
,
Nepi
,
M.
and
Vesprini
,
J.L.
(
2003
)
Nectar biodiversity: a short review
.
Plant Syst. Evol.
238
,
7
21
23
Minckley
,
R.L.
,
Roulston
,
T.H.
and
Williams
,
N.M.
(
2013
)
Resource assurance predicts specialist and generalist bee activity in drought
.
Proc. R. Soc. B
280
,
20122703
24
Dalin
,
P.
(
2011
)
Diapause induction and termination in a commonly univoltine leaf beetle (Phratora vulgatissima)
.
Insect Sci.
18
,
443
450
25
Duchenne
,
F.
,
Thébault
,
E.
,
Michez
,
D.
,
Elias
,
M.
,
Drake
,
M.
,
Persson
,
M.
et al (
2020
)
Phenological shifts alter the seasonal structure of pollinators assemblages in Europe
.
Nat. Ecol. Evol.
4
,
115
121
26
Bartomeus
,
I.
,
Ascher
,
J.S.
,
Wagner
,
D.
,
Danforth
,
B.N.
,
Colla
,
S.
,
Kornbluth
,
S.
et al (
2011
)
Climate-associated phenological advances in bee pollinators and bee-pollinated plants
.
Proc. Natl. Acad. Sci. U.S.A.
20
,
20645
20649
27
Kehrberger
,
S.
and
Holzschuh
,
A.
(
2019
)
Warmer temperatures advance flowering in a spring plant more strongly than emergence of two solitary spring bee species
.
PLoS One
14
,
e0218824
28
Kudo
,
G.
and
Cooper
,
E.L.
(
2019
)
When spring ephemerals fail to meet pollinators: mechanism of phenological mismatch and its impact on plant reproduction
.
Proc. R. Soc. B
286
,
20190573
29
Blüthgen
,
N.
and
Klein
,
A.
(
2011
)
Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions
.
Basic Appl. Ecol.
12
,
282
291
30
Fontaine
,
C.
,
Dajoz
,
I.
,
Meriguet
,
J.
and
Loreau
,
M.
(
2006
)
Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities
.
PLoS Biol.
4
,
e1
31
Bedford
,
F.E.
,
Whittaker
,
R.J.
and
Kerr
,
J.T.
(
2012
)
Systemic range shift lags among a pollinator species assemblage following rapid climate change
.
Botany
90
,
587
597
32
Kerr
,
J.T.
,
Pindar
,
A.
,
Galpern
,
P.
,
Packer
,
L.
,
Potts
,
S.G.
,
Roberts
,
S.M.
et al (
2015
)
Climate change impacts on bumblebees converge across continents
.
Science
349
,
177
180
33
Pyke
,
G.H.
,
Thomson
,
J.D.
,
Inouye
,
D.W.
and
Miller
,
T.J.
(
2016
)
Effects of climate change on phenologies and distributions of bumble bees and the plants they visit
.
Ecosphere
7
,
e01267
34
Dullinger
,
S.
,
Gattringer
,
A.
,
Thuiller
,
W.
,
Moser
,
D.
,
Zimmermann
,
N.E.
,
Guisan
,
A.
et al (
2012
)
Extinction debt of high-mountain plants under twenty-first-century climate change
.
Nat. Clim. Change
2
,
619
622
35
Waser
,
N.M.
,
Chittka
,
L.
,
Price
,
M.V.
,
Williams
,
N.M.
and
Ollerton
,
J.
(
1996
)
Generalization in pollination systems and why it matters
.
Ecology
77
,
1043
1060
36
Carvalho
,
A.T.
and
Schlindwein
,
C.
(
2011
)
Obligate association of an oligolectic bee and a seasonal aquatic herb in semi-arid north-eastern Brazil
.
Biol. J. Linn. Soc
102
,
355
368
37
Schleuning
,
M.
,
Fründ
,
J.
,
Schweiger
,
O.
,
Welk
,
E.
,
Albrecht
,
J.
,
Albrecht
,
M.
et al (
2016
)
Ecological networks are more sensitive to plant than to animal extinction under climate change
.
Nat. Commun.
7
,
13965
38
Forister
,
M.L.
,
Novotny
,
V.
,
Panorska
,
A.K.
,
Baje
L
,
Basset
Y
,
Butterill
,
P.T.
et al. (
2015
)
The global distribution of diet breadth in insect herbivores
.
Proc. Natl. Acad Sci. U.S.A.
112
,
442
447
39
Pelini
,
S.L.
,
Prior
,
K.M.
,
Parker
,
D.J.
,
Dzurisin
,
J.D.K.
,
Lindroth
,
R.L.
,
Hellmann
,
J.J.
et al. (
2009
) Climate change and temporal and spatial mismatches in insect communities. In
Climate Change Observed Impacts on Planet Earth
(
Letcher
,
T.M.
, ed.), pp.
215
231
,
Elsevier
,
Amsterdam
.
40
Hargreaves
,
A.L.
,
Weiner
,
J.L.
and
Eckert
,
C.G.
(
2015
)
High-elevation range limit of an annual herb is neither caused nor reinforced by declining pollinator service
.
J. Ecol.
103
,
572
584
41
Polce
,
C.
,
Garratt
,
M.P.
,
Termansen
,
M.
,
Ramirez-Villegas
,
J.
,
Challinor
,
A.J.
,
Lappage
,
M.G.
et al (
2014
)
Climate-driven spatial mismatches between British orchards and their pollinators: increased risks of pollination deficits
.
Glob. Change Biol.
20
,
2815
2828
42
Burkle
,
L.A.
,
Marlin
,
J.C.
and
Knight
,
T.M.
(
2013
)
Plant–pollinator interactions over 120 years: loss of species, co-occurrence, and function
.
Science
339
,
1611
1615
43
Kingsolver
,
J.G.
and
Huey
,
R.B.
(
2008
)
Size, temperature and fitness: three rules
.
Evol. Ecol. Res.
10
,
251
268
44
Oliveira
,
M.O.
,
Freitas
,
B.M.
,
Scheper
,
J.
and
Kleijn
,
D.
(
2016
)
Size and sex-dependent shrinkage of Dutch bees during one-and-a-half centuries of land-use change
.
PLoS One
11
,
e0148983
45
Bishop
,
J.A.
and
Armbruster
,
W.S.
(
1999
)
Thermoregulatory abilities of Alaskan bees: effects of size, phylogeny and ecology
.
Funct. Ecol.
13
,
711
724
46
Heinrich
,
B.
(
1974
)
Thermoregulation in endothermic insects
.
Science
185
,
747
756
47
Hatfield
,
J.L.
and
Prueger
,
J.H.
(
2015
)
Temperature extremes: effect on plant growth and development
.
Weather Clim. Extrem.
10
,
4
10
48
Hoover
,
S.E.R.
,
Ladley
,
J.J.
,
Shchepetkina
,
A.A.
,
Tisch
,
M.
,
Gieseg
,
S.P.
and
Tylianakis
,
J.M.
(
2012
)
Warming, CO2, and nitrogen deposition interactively affect a plant–pollinator mutualism
.
Ecol. Lett.
15
,
227
234
49
De Frenne
,
P.
,
Brunet
,
J.
,
Shevtsova
,
A.
,
Kolb
,
A.
,
Graae
,
B.J.
,
Chabrerie
,
O.
et al (
2011
)
Temperature effects on forest herbs assessed by warming and transplant experiments along a latitudinal gradient
.
Glob. Change Biol.
17
,
3240
3253
50
Willmer
,
P.G.
and
Corbet
,
S.A.
(
1981
)
Temporal and microclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pollen vectors and nectar robbers
.
Oecologia
51
,
67
78
51
Schweiger
,
O.
,
Biesmeijer
,
J.C.
,
Bommarco
,
R.
,
Hickler
,
T.
,
Hulme
,
P.E.
,
Klotz
,
S.
et al (
2010
)
Multiple stressors on biotic interactions: how climate change and alien species interact to affect pollination
.
Biol. Rev. Camp. Philos. Soc.
85
,
777
795
52
Rammig
,
A.
,
Jonas
,
T.
,
Zimmermann
,
N.E.
and
Rixen
,
C.
(
2010
)
Changes in alpine plant growth under future climate conditions
.
Biogeosciences
7
,
2013
2014
53
Nattero
,
J.
,
Cocucci
,
A.A.
and
Medel
,
R.
(
2010
)
Pollinator-mediated selection in a specialized pollination system: matches and mismatches across populations
.
J. Evol. Biol.
23
,
1957
1968
54
Borrel
,
B.J.
(
2005
)
Long tongues and loose niches: evolution of euglossine bees and their nectar flowers
.
Biotropica
37
,
664
669
55
Anderson
,
B.
,
Ros
,
P.
,
Wiese
,
T.J.
and
Ellis
,
A.G.
(
2014
)
Intraspecific divergence and convergence of floral tube length in specialized pollination interactions
.
Proc. R. Soc. B
281
,
20141420
56
Kuriya
,
S.
,
Hattori
,
M.
,
Nagano
,
Y.
and
Itino
,
T.
(
2015
)
Altitudinal flower size variation correlates with local pollinator size in a bumblebee-pollinated herb, Prunella vulgaris
L. (Lamiaceae).
J. Evol. Biol.
28
,
1761
1769
57
Miller-Struttmann
,
N.E.
,
Geib
,
J.C.
,
Franklin
,
J.D.
,
Kevan
,
P.G.
,
Holdo
,
R.M.
,
Ebert-May
,
D.
et al (
2015
)
Functional mismatch in a bumble bee pollination mutualism under climate change
.
Science
349
,
1541
1544
58
Klumpers
,
S.G.
,
Stang
,
M.
and
Klinkhamer
,
P.G.
(
2019
)
Foraging efficiency and size matching in a plant–pollinator community: the importance of sugar content and tongue length
.
Ecol. Lett.
22
,
469
479
59
Howlett
,
B.G.
,
Walker
,
M.K.
,
Rader
,
R.
,
Butler
,
R.C.
,
Newstrom-Lloyd
,
L.E.
and
Teulon
,
D.A.J.
(
2011
)
Can insect body pollen counts be used to estimate pollen deposition on pakchoi stigmas?
N. Z. Plant Prot.
64
,
25
31
60
Adler
,
L.S.
and
Irwin
,
R.E.
(
2006
)
Comparison of pollen transfer dynamics by multiple floral visitors: experiments with pollen and fluorescent dye
.
Ann. Bot.
97
,
141
150
61
Solis-Montero
,
L.
and
Vallejo-Marin
,
M.
(
2017
)
Does the morphological fit between flowers and pollinators affect pollen deposition? An experimental test in a buzz-pollinated species with anther dimorphism
.
Ecol. Evol.
7
,
2706
2715
62
Zych
,
M.
,
Goldstein
,
J.
,
Roguz
,
L.
and
Stpiczynska
,
M.
(
2013
)
The most effective pollinator revisited: pollen dynamics in a spring-flowering herb
.
Arthropod–Plant Interact.
7
,
315
322
63
Bruce
,
T.J.
,
Wadhams
,
L.J.
and
Woodcock
,
C.M.
(
2005
)
Insect host location: a volatile situation
.
Trends Plant Sci.
10
,
269
274
64
Beyaert
,
I.
and
Hilker
,
M.
(
2014
)
Plant odour plumes as mediators of plant-insect interactions
.
Biol. Rev. Camb. Philos. Soc.
89
,
68
81
65
Farré-Armengol
,
G.
,
Filella
,
I.
,
Llusià
,
J.
,
Niinemets
,
Ü.
and
Peñuelas
,
J.
(
2014
)
Changes in floral bouquets from compound-specific responses to increasing temperatures
.
Glob. Change Biol.
20
,
3660
3669
66
Döttrel
,
S.
and
Vereecken
,
N.
(
2010
)
The chemical ecology and evolution of bee-flower interactions: a review and perspectives
.
Can. J. Zool.
88
,
668
697
67
Qaderi
,
M.M.
,
Kurepin
,
L.V.
and
Reid
,
D.M.
(
2012
)
Effects of temperature and watering regime on growth, gas exchange and abscisic acid content of canola (Brassica napus) seedlings
.
Environ. Exp. Bot.
75
,
107
113
68
Smith
,
A.R.
and
Zhao
,
D.
(
2016
)
Sterility caused by floral organ degeneration and abiotic stresses in Arabidopsis and cereal grains
.
Front. Plant Sci.
7
,
1503
69
Lai
,
Y.S.
,
Yamagishi
,
M.
and
Suzuki
,
T.
(
2011
)
Elevated temperature inhibits anthocyanin biosynthesis in the tepals of an oriental hybrid lily via the suppression of LhMYB12 transcription
.
Sci. Hortic.
132
,
59
65
70
Morrison
,
M.J.
and
Stewart
,
D.W.
(
2002
)
Heat stress during flowering in summer Brassica
.
Crop Sci.
42
,
797
803
71
Murcia
,
C.
(
1990
)
Effect of floral morphology and temperature on pollen receipt and removal in Ipomoea trichocarpa
.
Ecology
71
,
1098
1109
72
Mu
,
J.
,
Peng
,
Y.
,
Xi
,
X.
,
Wu
,
X.
,
Li
,
G.
,
Niklas
,
K.J.
et al (
2015
)
Artificial asymmetric warming reduces nectar yield in a Tibetan alpine species of Asteraceae
.
Ann. Bot.
116
,
899
906
73
Leal
,
W.S.
(
2013
)
Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes
.
Ann. Rev. Entomol.
58
,
373
391
74
Sørensen
,
J.G.
,
Kristensen
,
T.N.
and
Loeschcke
,
V.
(
2003
)
The evolutionary and ecological role of heat shock proteins
.
Ecol. Lett.
6
,
1025
1037
75
Mayer
,
M.P.
(
2010
)
Gymnastics of molecular chaperones
.
Mol. Cell
39
,
321
331
76
Pelosi
,
P.
,
Zhu
,
J.
and
Knoll
,
W.
(
2018
)
Odorant-binding proteins as sensing elements for odour monitoring
.
Sensors (Basel)
18
,
E3248
77
Martinet
,
B.
,
Lecocq
,
T.
,
Smet
,
J.
and
Rasmont
,
P.
(
2015
)
A protocol to assess insect resistance to heat waves, applied to bumblebees (Bombus Latreille, 1802)
.
PLoS One
10
,
e0118591
78
Neven
,
L.G.
(
2000
)
Physiological responses of insects to heat
.
Postharvest Biol. Technol.
21
,
103
111
79
Sato
,
S.
,
Kamiyama
,
M.
,
Iwata
,
T.
,
Makita
,
N.
,
Furukawa
,
H.
and
Ikeda
,
H.
(
2006
)
Moderate increase of mean daily temperature adversely affects fruit set of Lycopersicon esculentum by disrupting specific physiological processes in male reproductive development
.
Ann. Bot.
97
,
731
738
80
Paupière
,
M.J.
,
van Heusden
,
A.W.
and
Bovy
,
A.G.
(
2014
)
The metabolic basis of pollen thermo-tolerance: perspectives for breeding
.
Metabolites
4
,
889
920
81
Pressman
,
E.
,
Peet
,
M.M.
and
Pharr
,
D.M.
(
2002
)
The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrates concentration in the developing anthers
.
Ann. Bot.
2002
,
631
636
82
Djanaguiraman
,
M.
,
Prasad
,
P.V.V.
,
Boyle
,
D.L.
and
Schapaugh
,
W.T.
(
2013
)
Soybean pollen anatomy, viability and pod set under high temperature stress
.
J. Agron. Crop Sci.
199
,
171
177
83
Ramakrishna
,
A.
and
Ravishankar
,
G.A.
(
2011
)
Influences of abiotic stress signals on secondary metabolites in plants
.
Plant Signal. Behav.
6
,
1720
1731
84
Santiago
,
J.P.
and
Sharkey
,
T.D.
(
2019
)
Pollen development at high temperature and role of carbon and nitrogen metabolites
.
Plant Cell Environ.
42
,
2759
2775
85
Vanderplanck
,
M.
,
Moerman
,
R.
,
Rasmont
,
P.
,
Lognay
,
G.
,
Wathelet
,
B.
,
Wattiez
,
R.
et al (
2014
)
How does pollen chemistry impact development and feeding behavior of polylectic bees?
PLoS One
9
,
e86209
86
Roger
,
N.
,
Michez
,
D.
,
Wattiez
,
R.
,
Sheridan
,
C.
and
Vanderplanck
,
M.
(
2017
)
Diet effects on bumblebee health
.
J. Insect Physiol.
96
,
128
133
87
Hedhly
,
A.
(
2011
)
Sensitivity of flowering plant gametophytes to temperature fluctuations
.
Environ. Exp. Bot.
74
,
9
16
88
Snider
,
J.L.
and
Oosterhuis
,
D.M.
(
2011
)
How does timing, duration, and severity of heat stress influence pollen–pistil interactions in angiosperms?
Plant Signal. Behav.
6
,
930
933
89
Descamps
,
C.
,
Quinet
,
M.
,
Baijot
,
A.
and
Jacquemart
,
A.-L.
(
2018
)
Temperature and water stress affect plant–pollinator interactions in Borago officinalis (Boraginaceae)
.
Ecol. Evol.
8
,
3443
3456
90
Cnaani
,
J.
,
Thomson
,
J.D.
and
Papaj
,
D.R.
(
2006
)
Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration
.
Ethology
112
,
278
285
91
Somme
,
L.
,
Vanderplanck
,
M.
,
Michez
,
D.
,
Lombaerde
,
I.
,
Moerman
,
R.
,
Wathelet
,
B.
et al (
2014
)
Pollen and nectar quality drive the major and minor floral choices of bumble bees
.
Apidologie
46
,
1
15
92
Muth
,
F.
,
Francis
,
J.S.
and
Leonard
,
A.S.
(
2016
)
Bees use the taste of pollen to determine which flowers to visit
.
Biol. Lett.
12
,
20160356
93
Hammer
,
T.J.
,
Hata
,
C.
and
Nieh
,
J.C.
(
2009
)
Thermal learning in the honeybee, Apis mellifera
.
J. Exp. Biol.
212
,
3928
3934
94
Dyer
,
A.G.
,
Whitney
,
H.M.
,
Arnold
,
S.E.J.
,
Glover
,
B.J.
and
Chittka
,
L.
(
2006
)
Bees associate warmth with floral colour
.
Nature
442
,
525
95
Norgate
,
M.
,
Boyd-Gerny
,
S.
,
Simonov
,
V.
,
Rosa
,
M.G.
,
Heard
,
T.A.
and
Dyer
,
A.G.
(
2010
)
Ambient temperature influences Australian native stingless bee (Trigona carbonaria) preference for warm nectar
.
PLoS One
5
,
e12000
96
Shrestha
,
M.
,
Garcia
,
J.E.
,
Bukovac
,
Z.
,
Dorin
,
A.
and
Dyer
,
A.G.
(
2018
)
Pollination in a new climate: assessing the potential influence of flower temperature variation on insect pollinator behaviour
.
PLoS One
23
,
e0203153
97
Chittka
,
L.
and
Raine
,
N.E.
(
2006
)
Recognition of flowers by pollinators
.
Curr. Opin. Plant Biol.
9
,
428
435
98
Rafferty
,
N.E.
(
2017
)
Effects of global change on insect pollinators: multiple drivers lead to novel communities
.
Insect Sci.
23
,
22
27
99
Williams
,
J.W.
,
Jackson
,
S.T.
and
Kutzbacht
,
J.E.
(
2007
)
Projected distributions of novel and disappearing climates by 2100 AD
.
Proc. Natl. Acad. Sci. U.S.A.
104
,
5738
5742
100
Takkis
,
K.
,
Tscheulin
,
T.
and
Petanidou
,
T.
(
2018
)
Differential effects of climate warming on the nectar secretion of early- and late-flowering Mediterranean plants
.
Front. Plant Sci.
9
,
874
101
Wolkovich
,
E.M.
,
Cook
,
B.I.
,
Allen
,
J.M.
,
Crimmins
,
T.M.
,
Betancourt
,
J.L.
,
Travers
,
S.E.
et al (
2012
)
Warming experiments underpredict plant phenological responses to climate change
.
Nature
485
,
497
497
102
Stebbins
,
G.L.
(
1970
)
Adaptive radiation of reproductive characteristics in angiosperms I: pollination mechanisms
.
Annu. Rev. Ecol. Syst.
1
,
307
326
103
Forrest
,
J.R.K.
(
2015
)
Plant–pollinator interactions and phenological change: what can we learn about climate impacts from experiments and observations?
Oikos
124
,
4
13
104
Goulson
,
D.
,
Nicholls
,
E.
,
Botias
,
C.
and
Rotheray
,
E.L.
(
2015
)
Bee declines driven by combined stress from parasites, pesticides, and lack of flowers
.
Science
27
,
1255957
105
Gérard
,
M.
,
Martinet
,
B.
,
Maebe
,
K.
,
Smagghe
,
G.
,
Vereecken
,
N.J.
,
Rasmont
,
P.
et al (
2020
)
Shift in size of bumblebee queens over the last century
.
Glob. Change Biol.
26
,
1185
1195
106
Van Asch
,
M.
,
Tienderen
,
P.H.
,
Holleman
,
L.J.M.
and
Visser
,
M.E.
(
2007
)
Predicting adaptation of phenology in response to climate change, an insect herbivore example
.
Glob. Change Biol.
13
,
1596
1604
107
Skelly
,
D.K.
,
Joseph
,
L.N.
,
Possingham
,
H.P.
,
Freidenburg
,
L.K.
,
Farrugia
,
T.J.
,
Kinnison
,
M.T.
et al (
2007
)
Evolutionary responses to climate change
.
Conserv. Biol.
21
,
1353
1355
108
Thomas
,
C.D.
,
Bodsworth
,
E.J.
,
Wilson
,
R.J.
,
Simmons
,
A.D.
,
Davies
,
Z.G.
,
Musche
,
M.
et al (
2001
)
Ecological and evolutionary processes at expanding range margins
.
Nature
411
,
577
581
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