Kate Singer '24

e E ects of Climate Change on PlantPollinator Communication

BY KATE SINGER '24

Cover Image: European honeybee extracts nectar.

Image Source: Wikimedia Commons Introduction

It is common knowledge that the global climate is changing due to anthropogenic in uences. Increased CO2 levels in the atmosphere will lead to an increase in the global average temperature (Ekwurzel et al., 2017) which will have many negative impacts on the environment and its inhabitants. e timing of the biological cycles of many species is o en correlated with environmental cues that are being a ected by climate change. However, when the cycles of two interacting species are correlated with di erent cues, there can be a misalliance of interconnected biological processes. is phenomenon of timing discrepancies of biological cycles is known as phenological mismatch. is process is largely driven by climate change and a ects species across taxa (Visser & Gienapp, 2019). Mismatched phenological processes can also impede interspecies communication, particularly communication between plants and pollinators. Plants normally communicate with their pollinators through modalities such as olfactory, visual, or electric signaling. ese signals allow pollinators to locate the ower and its pollen stores (Sun et al., 2018), as well as determine whether that ower has previously been visited by another pollinator and has consequently been depleted of its resources (Clarke et al., 2013). e changing climate is also altering the visual and olfactory signals produced by the owers. While it is clear that these changes are occurring, the broader implications are still unknown.

Phenological Mismatch

e timing of many organisms’ life history activities, or phenology, is dependent on environmental cues such as temperature or day length. Should these cues cease to be reliable due to changes in the climate, these processes will not occur at the optimal time and the overall tness of the organism will decrease (McNamara et al., 2011). Hutchings et al. (2018) illustrate the phenomenon of decreased plant and pollinator tness due to phenological mismatch through observation of the spider orchid, Ophrys sphegodes, and the solitary mining bee, Andrena nigroaenea. Optimal pollination relies on male bees emerging from hibernation right before the orchids bloom, and females emerging a er the bloom. is is because these orchids create a scent bouquet which mimics the mating pheromones of a female bee. Since the orchid blooms before the female bees emerge and

Image 1: Spider orchids. Image Source: Wikimedia Commons

give o the true mating pheremone, the males are attracted to the owers, which allows for pollination. While the timings of orchid bloom and the emergence of male and female bees are all dependent on temperature, they are not equally a ected by changes in this factor. For every 1°C increase in the average spring temperature, the date of emergence of female solitary mining bees advances by 15.6 days, the date of emergence of male bees advances by 9.2 days, and the date of orchid bloom only advances by 6.4 days (Robbirt et al., 2014). is means that the warming temperatures have a greater e ect on female bee emergence than they do on the date of owering. If female bees emerge at the same time as or before the orchids bloom, the males are less likely to be deceived by the ower, and pollination rates decrease (Hutchings et al., 204). is study shows how instances of temporal discrepancy have increased over time in correlation with the increasing global temperature which has led to a decline in populations of spider orchids. e trend of phenological mismatch caused by climate change prohibiting plants from e ectively communicating with their pollinators is seen in many other plant pollinator relationships as well (Kudo, 2019; ompson, 2010). is process can be detrimental to plant species with specialized pollinators as is the case with the spider orchid and the solitary mining bee since they do not have other pollinators who can make up for this timing discrepancy if their primary pollinator is absent (Hutchings et al., 2018). erefore, the plants experience low rates of pollination which ultimately leads to a decrease in the populations of the plants and potentially the pollinators as a result.

Changes in Visual Signaling

Species not experiencing phenological mismatch will also encounter di culties in communicating with their pollinators because of climate change. Temperature can a ect owers’ visual displays, used to attract pollinators from far away, in multiple ways. Sullivan and Koski (2021) found that levels of anthocyanin, a oral pigment associated with blues, pinks, and purples, decreased in response to higher temperatures. is means that as temperatures increase due to anthropogenic causes, many ower species will be less pigmented and therefore will be less attractive to their pollinators which will likely lead to a decrease in pollination. Conversely, the team found that plants experiencing droughtlike conditions, but not necessarily increased temperatures, will experience higher levels of pigmentation. Since climate change will a ect di erent regions in di erent ways, it is important to note how the e ects described in this paper will not a ect every species equally (Sullivan & Koski, 2021). e pattern of varied responses to climate change across ower species is also depicted in the paper by Koski et al. (2020) examining the change in the UV absorption of owers in response to climate change. Flowers with exposed anthers, or pollen stores, have increased levels of UV absorbing pigmentation when exposed to increased UV levels due to ozone depletion. is pigmentation absorbs the radiation in the petals, so it does not damage the exposed pollen. e opposite is true for owers with anthers concealed by petals. In response to increased temperatures,

" is phenomenon of timing discrepancies of biological cycles is known as phenological mismatch."

"What is clear, however, is that specialized plant pollinator relationships are more at risk and declines in their populations because of climate change hindering communication and pollination are already being observed."

Image 2: Raphanus sativus. Image Source: Wikimedia Commons owers with concealed anthers showed a decrease in pigmentation. For these owers, it is important to reduce heat absorption as the petals enclosing the anthers create a “micro-greenhouse” which can cause the pollen to experience heat damage (Koski et al., 2020). While di erent across taxa, climate change will impact visual signals plants use to communicate with pollinators. In some species, this will mean the owers will be more conspicuous and therefore have increased pollination rates, while the opposite may be true for others.

Changes in Olfactory Signaling

Visual signals are not the only way in which owers attract pollinators. Olfactory signals are used to attract pollinators that are close to the ower. ese signals are also being altered by the changing climate. Increased temperatures have been shown to decrease volatile emissions in some species of ower (Cna’ani et al., 2014), therefore making them less attractive to pollinators. Conversely, other studies have shown that volatile emissions increase as temperatures rise, until a temperature threshold is reached, and the plant begins experiencing major heat stress (Farré-Armengol et al., 2014). is temperature maximum is about 40°C meaning only species in particularly warm climates will express the trend shown in this paper. Since these studies used di erent test species and got di erent results, one can conclude that the change in release of volatile compounds will di er between species, as was the case with UV pigmentation levels discussed above. Additionally, each individual volatile compound, of which a ower’s scent bouquet is composed, reacts di erently to increased temperatures. is means that the composition of the scent bouquet is altered in addition to the change in volatility. e composition of a volatile scent bouquet aids pollinators in identifying plant species, meaning that any changes in the makeup of a ower's olfactory signal will decrease a pollinator’s ability to recognize the ower. As with phenological mismatch, this is particularly damaging to specialists who rely on speci c scent bouquets to locate the correct ower (Farré-Armengol et al., 2014). Failure to do so would result in decreased pollination, which, for specialized pollination relationships, could be detrimental to plant populations.

Flowers normally carry a negative charge relative to the atmospheric electric eld while honeybees and other ying pollinators tend to be positively charged. ese charges are naturally uctuating and di er between environments. When a bee lands on a ower, it transfers some of its positive change to the ower which makes the ower’s electric eld less negative. While this change is not permanent, it does remain altered for a short period of time. Additionally, the more bees that interact with the ower, the longer the altered charge will last. When a bee approaches a ower, it can sense its change using the hairs on its body. is means that if a bee encounters a ower with an altered electric eld, it can determine that the ower had previously been visited by other individuals and would likely have been depleted of its nectar and pollen. e bee can then use this information to decide to move to a di erent ower instead of wasting its time and energy at a ower that bears no reward (Clarke et al., 2017).

Conclusion

Given the wide body of literature on the subject, it is undeniable that climate change will alter how plants and animals communicate with one

another. However, further study is needed to ll many di erent gaps in the knowledge of this eld. Since the e ects of climate change will be so diverse, there is still much that is unknown about how communication between plants and pollinators will be altered. In fact, because new modalities through which species communicate are still being discovered, the ways in which climate change will alter these signals has yet to be explored. e electric eld through which bees and owers communicate was only discovered within the last decade (Clarke et al., 2013). If climate change does not a ect the charge itself, it would be interesting to examine whether climactic conditions impact a pollinator’s ability to detect the charge. Additionally, since climate change impacts each sensory modality di erently, it would be bene cial to examine how important each modality is for successful, and frequent pollination. What is clear, however, is that specialized plant pollinator relationships are more at risk and declines in their populations because of climate change hindering communication and pollination are already being observed (Hutchings et al. 2018). Furthermore, the greater impact of this change is still unknown. In the worst-case scenario, this could mean a decline in plant populations due to lack of successful pollination. If this decline is severe enough, then pollinator populations would also decline which would have major consequences for global ecology and food supply. Luckily, this outcome is highly unlikely since most plants do not solely rely on speci c pollinators. In the best-case scenario, the change in signal modalities would be insigni cant, and pollinators would be able to carry on pollination without hindrance. e true consequences of these changes in plant pollinator communications will likely lie somewhere in between. is is especially true considering not all changes in communication due to climate change will be negative. As discussed earlier, some owers will have increased pigmentation and some will produce stronger olfactory signals (Koski et al. 2020; Farré-Armengol et al. 2014), both of which make the owers more attractive to pollinators. With the variation in signal modalities and their responses to climate change across taxa, it is di cult to claim that we will see a signi cant decrease in most plant and pollinator populations due to changes in their communication. Continuing to monitor these changes and their e ects on populations will be important for better predicting the severity of anthropogenic climate change and understanding how to protect species potentially at risk.

References

Barragán-Fonseca KY, van Loon JJA, Dicke M, Lucas-Barbosa D (2019) Use of visual and olfactory cues of owers of two brassicaceous species by insect pollinators. Ecological Entomology. 45(1):45-55

Bryers KJRP, Bradshaw HD Jr, Ri ell JA (2014) ree oral volatiles contribute to di erential pollinator attraction in monkey owers (Mimulus). Journal of Experimental Biology. 217(4):614-623

Clarke D, Morley E, Robert D (2017) e bee, the ower, and the electric eld: electric ecology and aerial electroreception. Journal of Comparative Physiology A, Neuroethology, Sensory, Neural, and Behavioral Physiology. 203(9):737-748

Clarke D, Whitney H, Sutton G, Robert D (2013) Detection and learning of oral electric elds by bumblebees. Science. 340(6128):66-69

Image 3: Interactions between bee, ower, and atmospheric electric eld cannot be separated, as each of them in uence the other.

Image Source: Clarke et al., 2017

Cna’ani A, et al. (2014) Petunia x hybrida oral scent production is negatively a ected by hightemperature growth conditions. Plant, Cell & Environment. 38(7):1333-1346

Dunes, E. (2016). Spider Orchids [photograph]. Wikimedia Commons. https://commons. wikimedia.org/wiki/File:Spider-orchids_ (30733033192).jpg

Ekwurzel B et al. (2017) e rise in global atmospheric CO2, surface temperature, and sea level from emissions traced to major carbon producers. Climatic change. 144:579-590

Farré-Armengol G, Fillella I, Llusiá J, Niinemets Ü, Peñuelas J (2014) Changes in oral bouquets from compound-speci c responses to increasing temperatures. Global change biology. 20(12):3660-3669

Hutchings MJ, Robbirt KM, Roberts DL, Davy AJ (2018) Vulnerability of a specialized pollination mechanism to climate change revealed by a 356year analysis. Botanical Journal of the Linnean Society. 186(4):498-509

Koski MH, MacQueen D, Ashman TL (2020) Floral pigmentation has responded rapidly to global change in ozone and temperature. Current Biology. 30(22):4425-4431

Kenpei. (2007). Raphanus sativus [photograph]. Wikimedia Commons. https://commons. wikimedia.org/wiki/File:Raphanus_sativus3.jpg

Kudo G, Cooper EJ (2019) When spring ephemerals fail to meet pollinators: mechanism of phenological mismatch and its impact on plant reproduction. Proceedings of the Royal Society B. 286(1904)

McNamara JM, Barta Z, Klaassen M, Bauer S (2011) Cues and the optimal timing of activities under environmental changes. Ecology Letters. 14(12): 1183–1190.

Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) e e ects of phenological mismatches on demography. Philosophical transactions of the Royal Society of London. 365(1555): 3177–3186

Radchuk V, Reed T, Teplitsky C, van de Pol M, Charmantier A, Hassall C, et al. (2019) Adaptive responses of animals to climate change are most likely insu cient. Nature Communications. 10(3109) Robbirt KM, Roberts DL, Hutchings MJ, Davy AJ (2014) Potential disruption of pollination in a sexually deceptive orchid by climatic change. Current Biology. 24(23):2845-2849

Severns, J. (2006). European honeybee extracts nectar [photograph]. Wikimedia Commons. https://commons.wikimedia.org/wiki/ File:European_honey_bee_extracts_nectar.jpg

Solga MJ, Harmon JP, Ganguli AC (2014) Timing is Everything: An Overview of Phenological Changes to Plants and eir Pollinators. Natural Areas Journal. 34(2)227-234

Sullivan CN, Koski MH (2021) e e ects of climate change on oral anthocyanin polymorphisms. Proceedings of the Royal Society B. 288(1946)

Sun S, Leshowitz MI, Rychtář J (2018) e signalling game between plants and pollinators. Nature. 8(6686)

ompson JD (2010) Flowering phenology, fruiting success and progressive deterioration of pollination in an early- owering geophyte. Philosophical transactions of the royal society b. 365(1555):3187-3199

Visser ME, Gienapp P (2019) Evolutionary and demographic consequences of phenologicalmismatches. Nature Ecology & Evolution. 3(6):879-885