Plant Cuttings

This image, entitled “Diagram briefly covering pollination”, by YJaredY is made available under the Creative Commons Attribution-Share Alike 4.0 International license.

A few posts ago I wrote about the impact of airborne-pollution on the photosynthetic capacity of plants. The pollutants responsible for that weekday photosynthetic depression were aerosols, liquid droplets or small solid particles. But, aerosols are not the only pollutants in the atmosphere; many gaseous pollutants are amongst the [enormous] cocktail of compounds present within the air that surround us all. This post looks at a pollutant gas that affects the plant-pollinating activities of insects. This deleterious impact is all the more surprising because the main element concerned – nitrogen – is essential for the proper structure, growth and development of plants (Karen DeFelice et al.) (and of animals (Ethan Shaw) such as pollinating insects).

This post therefore highlights the double-edged nature of a chemical element that is both life-enhancing and life-impairing. That pollutants affect both plants’ capacity to photosynthesise, and to be pollinated must rank amongst the most concerning of botanical ‘double-whammies’. Why? Because of its direct impact upon the productivity of plants, which underpins all terrestrial ecosystems – and human agriculture (Peter Hazell) (hence civilisation as we know it…).

The wrong kind of nitrogen…

Nitrogen is one of – at least – 17 chemical elements that are essential to higher plants (Melissa Ha et al.), which means that it is needed for the plant to grow and develop properly so that it can complete a full life-cycle, from seed-germination to seed-set. Although nitrogen makes up/accounts for approx. 78% of the atmosphere (Alan Buis), it is not directly usable by plants in that form, so-called diatomic nitrogen, N₂. To be useful to plants, N₂ needs to be converted into other nitrogen-containing entities such as nitrate (Melissa Ha et al.), nitrite [NO₂^–] (Anne Bernhard), and ammonium [NH₄⁺] (Melissa Ha et al.). Of those three, nitrate is the principal form in which plants’ acquire nitrogen from the environment (Scott Killpack & Daryl Buchholz; Chiara Muratore et al., Plants 2021, 10, 681; https://doi.org/10.3390/plants10040681).

Represented in chemical symbol short-hand, nitrate is shown as NO₃^–, which indicates that it’s a combination of one nitrogen atom and three oxygen atoms, and has an overall single negative charge [because it has a ‘superfluous’ electron]. As an important plant nutrient, that four-atom combination is the ‘good’ quartet. However, if the nitrate ion loses that electron, it becomes NO₃ [nitrogen trioxide], which has no overall charge. Although electrically-neutral, it’s highly reactive; nitrogen trioxide is therefore radically different to the nitrate ion. Known as the nitrate radical, it’s very much the ‘bad’ version of the four atom combination.

The nitrate radical is naturally created in the atmosphere by the interaction of nitrogen dioxide (NO₂) [which is released into the atmosphere from – amongst other sources – anthropogenic activities such as the combustion of fossil fuel] with ozone (O₃) [produced when ultraviolet radiation from the sun interacts with ‘normal’ diatomic oxygen (O₂) in the atmosphere] (Nga Lee Ng et al., Atmos. Chem. Phys. 17: 2103–2162, 2017; https://doi.org/10.5194/acp-17-2103-2017), and anthropogenically]*. Formation and accumulation of NO₃ takes place principally in the atmosphere at nighttime due to its rapid breakdown by sunlight (Ng et al., 2017).

Once formed, NO₃ can produce significant amounts of secondary aerosols (Gunnar Myhre et al.) in the atmosphere, which can affect climate and harm human health (Yuhang Wang et al., Environ. Sci. Technol. 57: 21306–21312, 2023; https://doi.org/10.1021/acs.est.3c09259). One of the ways NO₃ produces aerosols is by reacting with so-called volatile organic compounds [VOCs] (Ng et al., 2017). Amongst the broad category of VOCs are scent compounds produced by plants (Salma Mostafa et al. (2022) Front. Plant Sci. 13:860157; doi: 10.3389/fpls.2022.860157; Matteo Caser & Valentina Scariot, Horticulturae 2022, 8, 1049; https://doi.org/10.3390/horticulturae8111049; Mame-Marietou Lo et al., Plants 2024, 13(3), 417; https://doi.org/10.3390/plants13030417). And it’s their interaction with NO₃ that was investigated by Jeremy Chan et al. (Science 383: 607-611, 2024; doi: 10.1126/science.adi0858)**.

Chan et al. discovered that NO₃ rapidly degraded compounds within floral scents, specifically so-called monoterpenes (Jette Knudsen et al., Bot. Rev 72: 1-120, 2006; https://doi.org/10.1663/0006-8101(2006)72%5B1:DADOFS%5D2.0.CO;2; Haofei Zhang et al., PNAS 115(9): 2038-2043, 2018; https://doi.org/10.1073/pnas.1717513115; Karolina Wojtunik-Kulesza et al., Chem. Biodiversity 2019, 16, e1900434; https://doi.org/10.1002/cbdv.201900434; Wiktoria Potocka et al., Molecules 2023, 28(20), 7178; https://doi.org/10.3390/molecules28207178), produced by Oenothera pallida (pale evening primrose). This concerning case of ‘chemical-camouflage’ effectively made the flowers undetectable by night-flying, scent-following hawkmoths [Hyles lineata and Manduca spp.], with a 70% decrease in flower visitation.

Although Chan et al. specifically investigated night-time pollinators, they do consider the study’s relevance to day-time pollinators, such as bees, more generally by because it illustrates “the potential impact of field-relevant concentrations of NO₃ and O₃ [it should be mentioned that Chan et al. (2024) also found chemical degradation of the floral scent by ozone***, but that NO₃ caused the most severe effect] on plant-pollinator interactions”. Not only is that a problem for the pollinators – who miss out on food foraged from the flowers, it’s also an issue for the plants that lose valuable pollination services provided by the insect, the consequences of which deprivation include predicted reductions in fruit set, and plant fitness****.

But, how significant is this investigation – of NO₃-affecting scent-detection for a single plant species, by one group of night-time pollinators, in a very specific habitat [“the North American Deserts ecoregions”] – to any bigger picture appreciation of pollutant effects on pollination? Chan et al. (2024) considered that question and also presented an analysis of global meteorology and chemical emissions. From that study they concluded that the impact of anthropogenic pollutants [recall that NO₃ has origins from human activities] on an animal’s olfactory ability indicate that such pollutants may be critical regulators of pollination world-wide, particularly in regions such as North America, Europe, Central Asia, the Middle East, and southern Africa.

In other words, pollutant-impairment of pollination is a matter of global relevance. And that matters because an estimated 75% “of the leading global food crops is dependent upon animal pollination” (Alexandra-Maria Klein et al., Proc Biol Sci. 274(1608): 303–313, 2007; doi: 10.1098/rspb.2006.3721), which include flies, wasps, beetles, and butterflies (Romina Rader et al., PNAS 113: 146-151, 2015; https://doi.org/10.1073/pnas.1517092112), birds, mammals (James Rodger), and bats . Although, only 35% of global production volumes comes from crops that depend on pollinators (Klein et al., 2007) *****, that is a significant fraction of calories, nutrition, and variety for the human diet and not something we can afford to lose. And that’s just from a rather narrow human perspective. On a global, plant-wide, basis, it is estimated that “animal pollinated angiosperms … is 87.5% of the estimated species-level diversity of flowering plants” (Jeff Ollerton et al., Oikos 120: 321–326, 2011; doi: 10.1111/j.1600-0706.2010.18644.x). That 87% won’t all be down to insects, but the great majority will be, and that’s potentially an enormous number of flowering plants whose pollination is potentially at risk from olfactory-disruption from NO₃ or chemicals that act in a similar way.

Whilst the great majority of those insect-pollinated plants will not be of economic importance to humans, they will be components of a wide range of natural ecosystems where they will be primary producers whose photosynthetic activities underpin the function and stability of those habitats and communities. Chan et al’s work therefore adds to existing concerns about decline in numbers of pollinating insects (Nicola Gallai et al., Ecological Economics 68: 810-821, 2009; https://doi.org/10.1016/j.ecolecon.2008.06.014; James Rodger et al., Sci. Adv. 7,eabd3524, 2021; doi: 10.1126/sciadv.abd3524; Navkiran Kaur & Amritpal Singh Kaleka), and those more widely about the threats to pollination from air pollution (Laura Duque et al., Frontiers in Ecology and Environment Early View 2024; 0(0): e2701; doi:10.1002/fee.2701https://doi.org/10.1002/fee.2701).

Glimmers of hope…

Some small comfort – that matters may not be as doom-and-gloom-laden as Chan et al(2024)’s study might suggest – may be gleaned from three other investigations. First, work by Ignasi Bartomeus et al. (2014. PeerJ 2:e328; https://doi.org/10.7717/peerj.328) on spring oilseed rape, field bean, strawberry, and buckwheat. For the four crops studied, they found that, although there is clear benefit delivered by pollinators on yield quantity and/or quality, it is not maximized under current agricultural intensification. It therefore appears that we’re not making full use of pollinators when they are available. Doing so may go some way to offset any under-performance by NO₃-impaired pollinators, and more general decline in numbers of pollinators. Second, another intriguing notion is that plants may adapt and cope with a change in frequency or degree of insect-pollination by becoming self-fertilising – as found by Samson Acoca-Pidolle et al. (New Phytologist 242: 717–726, 2024; https://doi.org/10.1111/nph.19422), working with field pansy (Viola arvensis) in Paris (France) [for the press release on this work, see here].

Third is the work of Brynn Cook et al. (J Chem Ecol 46: 987–996, 2020; https://doi.org/10.1007/s10886-020-01211-4). Very briefly, they found that atmospheric ozone affected the floral scent emitted from a type of tobacco – Nicotiana alata – to the extent that olfactory attraction to the plant by the tobacco hawkmoth was impaired (in a manner similar to Chan et al’s work with NO₃). However, Cook et al. discovered that the moths were able to use visual cues to target artificial flowers and associate the ozone-altered floral blend with a nectar reward. Recognising that insects may use a number of senses to get to the correct flowers, the workers concluded that “The ability to learn ozone-altered floral odors may enable pollinators to maintain communication with their co-evolutionary partners and reduce the negative impacts that anthropogenically elevated oxidants may have on plant-pollinator systems”.

But, these are only ways that could cope with the problems of pollution-promoted reduction in pollinator visits, or declining insect numbers, The real solution ought to be to reduce pollutant load in the atmosphere and halt reduction in pollinating insect populations. In other words, those ‘solutions’ only deal with the effects of the issues, not their causes; they’re more of a sticking-plaster rather than a cure. It’s the issues that create the problems that need to be addressed. Caused – or made worse – by human activity, it’s action by humans that must sort it out.

What goes around, comes around…

If this 2024 work by Chan et al. sounds a little but familiar that may be because it is. Almost 8 years ago Jose Fuentes et al. sounded the alarm bell with their paper entitled “Air pollutants degrade floral scents and increase insect foraging times” (Atmospheric Environment 141: 361-374, 2016; https://doi.org/10.1016/j.atmosenv.2016.07.002). To give some idea of their findings, here are the last few sentences of their Abstract, “Results indicate that even moderate air pollutant levels (e.g., ozone mixing ratios greater than 60 parts per billion on a per volume basis, ppbv) substantially degrade floral volatiles and alter the chemical composition of released floral scents. As a result, insect success rates of locating plumes of floral scents were reduced and foraging times increased in polluted air masses due to considerable degradation and changes in the composition of floral scents. Results also indicate that plant-pollinator interactions could be sensitive to changes in floral scent composition, especially if insects are unable to adapt to the modified scentscape. The increase in foraging time could have severe cascading and pernicious impacts on the fitness of foraging insects by reducing the time devoted to other necessary tasks”. Well, we can’t say we haven’t been warned…

* In researching for this post I found out quite a bit about the chemistry of NO₃, and it’s really rather interesting (and the following gleaned from Hejun Hu et al., Atmos. Chem. Phys. 23: 8211–8223, 2023; https://doi.org/10.5194/acp-23-8211-2023). For example, in the dark – i.e. at night – nitric oxide [NO] reacts with ozone to make NO₂ and oxygen. The NO₂ reacts with more ozone to give us the nitrate radical and some more oxygen. But, during the daytime, some of the NO₃ is broken down by sunlight [the process known as photolysis] to NO and oxygen, and some NO₃ reacts with NO to give NO₂.Which is why the nitrate radical is particularly ‘troublesome’ at night-time, in the absence of sunlight, and therefore potentially an issue for night-active pollinating insects who use scent clues to find their flower target. This series of reactions and interactions with various nitrogen compounds also remind us of the complexity of the nitrogen cycle (Miriam Aczel (2019) Front. Young Minds. 7:41; doi: 10.3389/frym.2019.00041), and how it interacts with the oxygen cycle.

** For scicomm items on the work of Jeremy Chan et al. (Science 383: 607-611, 2024), see here, here, and here, and articles by Isaam Ahmed, Saugat Bolakhe, Warren Cornwall, and Alex Mitchell.

*** I had hoped to include something more about ozone in this piece with mention of research by Ben Langford et al. (Environmental Pollution 336 (2023) 122336; doi: 10.1016/j.envpol.2023.122336) entitled “Mapping the effects of ozone pollution and mixing on floral odour plumes and their impact on plant-pollinator interactions”. But, after the previous post’s mammoth read – on ligule structure-and-function – I thought all readers deserved a shorter piece this time. Anyway, for more on that ozone story – which, like Chan et al’s, is also about a gaseous pollutant’s impact on floral scents and their detection by pollinating insects – see these scicomm items here, and here, and for insights into the work by some of the investigation’s authors, see Ben Langford et al..

For more on the impacts of air pollutants on pollination – including specific impacts of ozone – see the review by Laura Duque & Ingolf Steffan-Dewenter (Front Ecol Environ 2024; 0(0): e2701; doi:10.1002/fee.2701) (and Robert Emmerich’s scicomm item about it here), the literature review by Hanna Francis, Maryse Vanderplanck et al. (Antioxidants 2021, 10, 636; https://doi.org/10.3390/antiox10050636), here, James Ryalls et al. (Environmental Pollution 297, 2022, 118847; https://doi.org/10.1016/j.envpol.2022.118847) (and its related scicomm item here), Fabien Démares et al. (Science of The Total Environment, 827, 2022, 154342; https://doi.org/10.1016/j.scitotenv.2022.154342), and James Blande (Current Opinion in Environmental Science & Health 19, 2021, 100228; https://doi.org/10.1016/j.coesh.2020.100228).

**** As an aside, the results of the investigation by Chan et al. (2024) isn’t the only bad news about that work. There’s a problem with its title, “Olfaction in the Anthropocene: NO₃ negatively affects floral scent and nocturnal pollination”. Sensibly-worded, and succinctly summarising the study’s findings, it was fine when the paper was submitted for consideration by the journal on 4^th April, 2023. But, it is probably already ‘out-of-date’, barely a month after its publication on 9^th February, 2024. Although it’s only an issue of ‘bad-timing’, it does illustrate that science is not a static thing. Why? What’s the problem? The term ‘Anthropocene’ (Liana Chua & Hannah Fair; Katie Pavid), which has been proposed to indicate a new period of time in the planet’s geological history, has been voted down by a panel of experts, as reported on 5^th March, 2024 by Raymond Zhong. [For more on this story, see items by Sigal Samuel, Erle Ellis, Alexandra Witze, and Richard Fisher.] But, and as bad as that news is for Chan et al., spare a thought for the team behind Anthropocene, “an interdisciplinary peer-reviewed journal answering questions about the nature, scale and extent of interactions between people and Earth processes and systems”, and devoted to that now-lost epoch. Will they have to change the periodical’s name..?

Or, is this all a lot of fuss over nothing? As reported by Alexandra Witze, “some are now challenging the vote, saying there were ‘procedural irregularities’”. One is therefore left wondering if this is all a bit like Mark Twain, reports of whose demise were “greatly exaggerated” (Emily Petsko)..?

***** Even wind-pollinated crops such as maize, rice, and wheat (which are amongst those that supply 65% of the needs of humans and their domesticated animals (Klein et al., 2007)) that don’t require insects for pollination (Hannah Ritchie), may still benefit from insect visits. For instance, Manu Saunders has documented numerous instances of insects collecting pollen from wind-pollinated plants (Insect Conservation and Diversity 11: 13-31, 2018; https://doi.org/10.1111/icad.12243). Whilst those visits may not be of great importance in terms of pollinating those plants, the nature of any interactions that may result between pollinator and plant probably remain to be fully investigated. And one such ‘ecological service’ that insect pollinators might possibly provide when visiting the flowers is transfer of insect-derived bacteria to the ovule and subsequently on to the seed that develops, and thence to the next generation of plants (Alberto Prado et al., Sci Rep 10, 3575 (2020); https://doi.org/10.1038/s41598-020-60591-5). Even though that possibility might not be of too much relevance to wind-pollinated wheat, rice and maize whose seeds are harvested and processed for consumption, this could be of great importance to anemophilous plants in natural ecosystems that may be insect-visited. For more on the fascinating area of pollinators, microbes, and plant reproduction, see Masayuki Ushio et al. (Sci Rep 5, 8695 (2015); https://doi.org/10.1038/srep08695), Rachel Vannette (Annual Review of Ecology, Evolution and Systematics 51: 363-386, 2020; https://doi.org/10.1146/annurev-ecolsys-011720-013401), Nevin Cullen et al. (Current Opinion in Insect Science 44: 48-54, 2021; https://doi.org/10.1016/j.cois.2020.11.002), and Massimiliano Cardinale & Sylvia Schnell ((2024) Front. Microbiol. 15: 1343795; doi: 10.3389/fmicb.2024.1343795).