Abstract
Global warming is now universally acknowledged as being responsible for dramatic climate changes with rising sea levels, unprecedented temperatures, resulting fires and threatened widespread species loss. While these effects are extremely damaging, threatening the future of life on our planet, one unexpected and paradoxically beneficial consequence could be a significant contribution to global iodine supply. Climate change and associated global warming are not the primary causes of increased iodine supply, which results from the reaction of ozone (O3) arising from both natural and anthropogenic pollution sources with iodide (I−) present in the oceans and in seaweeds (macro- and microalgae) in coastal waters, producing gaseous iodine (I2). The reaction serves as negative feedback, serving a dual purpose, both diminishing ozone pollution in the lower atmosphere and thereby increasing I2. The potential of this I2 to significantly contribute to human iodine intake is examined in the context of I2 released in a seaweed-abundant coastal area. The bioavailability of the generated I2 offers a long-term possibility of increasing global iodine status and thereby promoting thyroidal health. It is hoped that highlighting possible changes in iodine bioavailability might encourage the health community to address this issue.
Background
The crisis affecting all life on our planet, brought about as a consequence of global warming, has understandably instilled widespread fear (1). The Intergovernmental Panel on Climate Change (IPCC) has reported most of the consequences, such as melting of the polar ice caps with rising sea levels, unprecedented temperatures, resulting fires and threatened species loss, concentrating the minds of individuals and governments towards methods of alleviating the potential effects by reducing greenhouse gas emissions (2).
However, one potential consequence of climate change leading to global warming, which would fall into the category of unexpected consequences, at least for the health community, is the many ways global warming can contribute to increased worldwide iodine supply (3, 4). The authors are aware that when referring to human intake, the biologically important speciation is iodide (I−) when referring to other speciations; the collective term iodine is used. Climate change in itself does not result in increased iodine, which is a consequence of increased tropospheric ozone (O3) resulting from anthropogenic emissions of nitrogen oxides (NOx) reacting with marine iodide (I−) to release volatile iodine into the atmosphere (3, 4). Thus, the ocean provides a buffer to anthropogenic O3 production, providing a natural feedback mechanism regulating I2 production (5, 6). Although the reaction of O3 with I− at the ocean surface is the main abiotic source of generation of volatile iodines such as I2 and hypoiodous acid (HOI), producing approximately 80%, the remaining 20% is the result of biotic production of methylated iodines produced by photolytic degradation of organic matter and primary production by phytoplankton (3, 6, 7).
Different scientific communities develop their own special niche interests, even when dealing with the same subject (8, 9). Iodine researchers in the Health Sciences community direct their efforts to the study of iodine deficiency disorders (IDD) and their contribution to thyroid health (10). Perhaps less well understood by the thyroid community is the importance of iodine in marine and atmospheric chemistry. Studies of the marine atmosphere leave little doubt that the crisis of global warming has, through a variety of pathways, increased the bioavailable global iodine pool (3). We have previously drawn attention to the potential increase in global iodine status arising from global warming (11). Although it is unfortunately becoming less difficult to predict the course of climate change associated with global warming (2), it is not easy to extrapolate the influence of increased global iodine of various speciations on human or animal iodide (I−) intake (12, 13). These various iodine sources would include foodstuffs enriched by increased deposition in rainfall, iodine-richer drinking water or respiratory inspiration. Of course, the effect of increased iodine intake on human or animal thyroidal health would depend on the anionic I− content capable of being concentrated by the thyroid (14). Although no immediate change in population thyroidal health can be anticipated from climate-based alterations in global iodine status, this communication hopes to raise consciousness in the thyroid community about possible longer-term consequences and perhaps stimulate studies on the consequence of changes in atmospheric iodine on human and animal iodine intake.
Iodine in the marine environment
The marine environment is the most important source of global iodine supply as oceans make up 70% of the surface of the earth. Although seawater is not particularly rich in iodine, approximately 50 µg/L (8, 9, 10), its abundance makes it the most important iodine source, and organisms of marine origin, such as algae (seaweed), fish or other seafood, are correspondingly iodine-rich (9). The principal speciations of iodine in seawater are inorganic iodide (I−) which predominates in surface waters and iodate (IO3 − ) which is the major speciation in the deep (4, 12, 13). In addition to ocean depth, the partition of iodine between I− and IO3 − is dependent on temperature and the degree of oxygenation of seawater (4). The concentration of I− in surface water also depends on phytoplankton primary productivity, ocean circulation and vertical mixing, pH and oxygen levels (4, 7, 15, 16, 17, 18, 19). Geography and seasonal factors play a large part in higher concentrations of I− being present in warmer tropical waters or in subtropical gyres (rotating ocean currents) (3, 4, 5, 16, 18, 19). Seaweed (macroalgae) abundant areas in coastal regions are an important source of marine iodine with I− the major speciation (20, 21, 22, 23). I−-rich macroalgae normally covered by surrounding seawater, become stressed when exposed at low tides to atmospheric ozone (O3), which reacts with I− to produce volatile HOI and gaseous iodine (I2). This process is enhanced by global warming as the warmer surface seawater contains more I− (3, 4). Some species of seaweeds, particularly kelps such as Laminaria, have the ability to concentrate to 30,000 times that of the surrounding seawater (21, 24, 25). In contrast, the human thyroid concentrates iodide up to 20–40 times that of the bloodstream (26). I− and indeed other halides produced by the ocean surface as well as by organic sources such as algae both exert a negative feedback action by diminishing atmospheric O3 (5, 6, 19).
Table 1 shows a simple illustration of the reaction of marine I− with atmospheric O3 to produce volatile iodine oxides HOI, I2 and IO−. This can occur in the open ocean or as a result of production by algae in coastal areas (3, 4, 7, 12, 23). The amount of volatile iodines released depends on the seaweed species and length of exposure (22, 27, 28). The duration of gaseous I2 and HOI in the atmosphere depends on the degree of photolytic degradation, and thus nighttime values tend to be higher than those sampled in daylight (12, 18, 29). Iodine released into the atmosphere can be of both inorganic origin (formed because of the reaction of seawater I− with O3, or of biogenic origin (I−) released from algae (macroalgae or microalgae/phytoplankton), which also reacts with O3. In coastal areas, the contribution of either pathway depends on the abundance of algal growth, particularly macroalgae, which predominates in certain but not all coastal waters as it requires sheltered areas to flourish (21, 23).
Reaction of marine iodide (I−) with atmospheric ozone (O3) leading to the production of highly reactive iodine oxides (IO−), gaseous iodine (I2) and hypoiodous acid (HOI). I− is in aqueous form in seawater while HOI and I2 can exist in gaseous or aqueous format (2). These reactions serve to increase volatile iodines while diminishing tropospheric O3 (4, 5, 12, 19).
| O3 + H+ + I– → HOI + O2 + IO– |
| IO−+ H+ → HOI |
| H+ + HOI + I− → I2 + H2O |
Iodine and the atmosphere
Sea-to-air emissions depend upon volatile organic iodine compounds (VOC) such as HOI and I2 being released into the atmosphere. Iodine so released can come from the ocean surface or marine algae but can also be released from land sources such as volcanoes or desert dust carried in sandstorms (30). Marine iodine emissions can be organic (CH3I, CH2ICl, CH2I2) or inorganic (HOI and I2). The contribution of organic iodine speciation has been assessed as being approximately 20% compared to the dominant role (approximately 80%) of inorganic HOI and I2 (2, 20, 21). An exception is CH3I which, in contrast to the short lifetime of other organic iodines, is longer lived (30, 31). The sources of iodine and emission pathways in the marine environment are shown in Fig. 1. The oceans provided the most important source of iodine which is released into the marine boundary layer (MBL), that part of the atmosphere, roughly the lowest 1 or 2 km, that has direct contact and, hence, is directly influenced by the ocean. The released I2 and HOI are photolysed to yield highly reactive iodine oxides IO− which initiate catalytic O3 destroying cycles in the atmosphere (3, 5, 16, 19). As shown in Fig. 1, I− released from oceanic or in coastal areas, algal sources, reacts with atmospheric O3 to produce gaseous I2 and HOI which remain in the gaseous or aqueous form before being available for inspiration through breathing or deposited in rainfall onto soil where it is recycled in foodstuffs consumed by humans and animals (9).
Atmospheric ozone (O3) arising from anthropogenic generated pollutants reacts with marine iodide (I−) to produce volatile iodines (HOI and I2). These iodines form cloud condensation nuclei (CCN) leading to aerosol and cloud formation opposing radiative forcing and global warming. Solubilised iodine is returned to Earth in rain with gaseous iodine being available for respiratory intake. Troposphere: lowest level of atmosphere (average 13 km above Earth’s surface); cloud condensation nuclei (CCN): particles that can form cloud droplets at a defined water supersaturation (relative humidity above 100%); marine boundary layer (MBL): 2–3 km above sea level); biotic: produced from organic compounds including macroalgae/phytoplankton; abiotic: inorganic compounds produced directly from the ocean.
Citation: European Thyroid Journal 13, 2; 10.1530/ETJ-23-0200
The reaction of O3 with I− accomplishes two major results. It is the major source of volatile iodine at the sea surface and, in turn, reduces potentially harmful O3 in the lower atmosphere (troposphere) up to 14 km above sea level (3, 32). This tropospheric O3 should not be confused with O3 in the stratosphere, which protects against solar UV radiation. Atmospheric iodine has been shown to drive new marine particle formation, leading to cloud condensation nuclei (CCN) increases and aerosol formation (33). Ozone and other tropospheric aerial pollutants such as nitrogen oxides (NOx) act to provide a barrier to heat escape from the Earth, causing cloud brightening and ultimately higher cloud reflectance. The heat energy is trapped within the atmosphere causing it to warm up, termed radiative forcing (3, 34). The reduction of O3 by I− is an important factor in opposing global warming (7, 32). Although currently of lesser significance than tropospheric iodine, recent reports have shown that anthropogenic iodine emissions have resulted in stratospheric iodine contributing to the diminution of the Antarctic O3 hole, particularly during spring and summer (35).
Effects of climate change on global iodine
Since seawater provides the iodine source for marine organisms, both plant and animal, anything that influences sea levels affects the iodine supply. Melting of the polar ice caps as a result of global warming raises sea levels, as occurred in previous global warming episodes (36). Studies measured seasonally from Alpine ice cores since the 1950s show evidence of a threefold increase in iodine content (37). The authors concluded that iodine’s impact on the northern hemisphere atmosphere accelerated over the 20th century and showed a coupling between anthropogenic pollution and the availability of iodine as an essential nutrient to the terrestrial biosphere. Similar studies on Greenland ice cores also showed a tripling in iodine from 1950 to 2010, which was also attributed to anthropogenic O3 production (38). An additional factor promoting global warming is the melting of the white ice, which reflects the heat from the sun, and thus thinning or eventual disappearance of the polar ice caps allows more penetration of sunlight and enhances radiative forcing (7, 38). Thawing of the ice caps also permits sunlight to irradiate frozen phytoplanktons, which acts via halperoxidases to release stored I− which in contact with O3 produces volatile iodines (21, 38). When the ice cap refreezes, the thinner ice is also more permeable to iodine formation and release (7, 21, 38).
The catalytic effect of haloperoxidase in the reaction of I− with H2O2 is analogous to the role of thyroid peroxidase TPO in converting I− to I2 in the presence of H2O2 in thyroid hormonogenesis.
A review of glacial cycles over the Arctic Ocean demonstrated that climate change involving sea ice retreat and anthropogenic O3-induced iodine emissions will produce greatly increased biogenic gaseous iodine emissions (36). These findings were calculated based on changes in biogenic iodine release in previous Earth warming cycles, which in preindustrial times did not involve the additive effects of anthropogenic O3, resulting in an even greater change (36). Similar patterns of iodine emissions have been reported from the Southern Ocean, and a contribution of VOCs to the Antarctic stratospheric O3 hole has also been noted (35), although values in the northern hemisphere tend to be higher than those in the southern hemisphere (17). Another contributor to global iodine is its presence in dust carried into the atmosphere from deserts or volcanic eruptions (30). The consequence of such increases in global iodine levels, both atmospheric and deposited in rain, remains unknown. It has been found that O3 within dust layers has been diminished by 75%, with iodine levels highest where O3 is lowest (30). The lowering of ocean pH because of increases in the greenhouse gas CO2, which when dissolved in seawater forms H2CO3, also contributes to gaseous iodine release (39), as acid pH favours the reduced I−over the oxidised IO3 − speciation. Not all climate-related changes favour increased iodine emissions. Although increased ocean temperature and acidification can promote iodine release, they also have the opposite effect by destroying kelp forests (40). An example of this phenomenon is provided by the Tasmanian experience, where under the influence of the East Australia Current (EAC), ocean waters off Tasmania are warming, resulting in the decline of the giant kelp (Macrocystis pyrifera) around Tasmania by 95% overall from the middle of last century. This decline removes a large source of iodine from the coastal environment and will have the effect of diminishing the I2 buffering effect on O3 (40, 41). It is feared that this may be part of a worldwide trend (42). This may be a local effect caused by the increase in ocean temperatures resulting from the EAC (40) and may have opposing consequences, as it has been demonstrated that ocean acidification markedly stimulates growth of certain seaweed species and enhances their iodide accumulation (43). These workers concluded that ocean acidification was more important than increased temperature in promoting iodide accumulation and postulated that this might present a risk of excess iodine intake in populations consuming seaweed as a staple diet (43).
Pathways of potential increased iodine intake
Iodine in foodstuffs
An excess in atmospheric iodine will be returned to Earth in rainfall, thus increasing soil and therefore food iodine. The rate of deposition of soluble iodines will depend on local climatic conditions and geography (44). It is generally believed that coastal areas are richer in iodine than those inland (8), but this is more likely to be evident in larger land masses where distance from the sea assumes greater importance (8, 12). Iodine in the soil is generally associated with organic matter and is not readily soluble. The magnitude of iodine deposition is unlikely to make a significant contribution to populations in which universal salt iodisation (USI) of 20–40 mg prevails (10). The only possible significance would be in areas of iodine deficiency, borderline iodine intake or low iodine dietary preferences, particularly relevant in European countries with a recent history of iodine deficiency (10). The manner in which climate change might influence terrestrial pathway through which iodide enters the diet will depend on geographical location as well as local agricultural practises. The major consequences of climate change (i.e. increased global temperatures and rainfall patterns) will affect iodine status. It is estimated that rainfall increases by 1–3% for every 1° increase in temperature (45). However, this is not a universal finding, as studies have shown both increased drought (dry zones) as well as wet zones associated with anthropogenically associated global warming (46). Increases in atmospheric iodine will be returned to Earth in the shape of rainfall. This will include the solubilised gaseous fraction (I2 and HOI−) as well as aerosol and particles incorporated in clouds (47, 48). Nonetheless, it is highly unlikely that any improvements in global iodine status, in terms of diminishing IDD with associated benefits such as population infant neuropsychological development, will outweigh the increasing adverse effects of global warming (2). In many cases in the northern hemisphere, dairy milk and milk products are the major sources of dietary iodine intake (49, 50). This shows seasonal variation, being greater in winter where dairy cattle are housed indoors and fed dietary supplements, including added iodide (51). In the event of climate change-induced increases in iodine deposition this summer, milk iodine content might be expected to increase.
Consequences of increased global iodine
The consequences of increased temperatures, including increased rainfall and melting of polar ice caps, would by raising sea levels, have the potential to increase iodine deposition on newly inundated land (36, 38). In the event of changes in land use, efforts to reclaim such land for use in agriculture have been shown to increase local soil iodine, with knock-on effects on drinking water iodine concentration in Denmark (52). Crops grown on such land would have increased iodine content. Another consequence of climate change is desertification. Dust storms have been shown to be iodine enriched and can be readily deposited (30).
Iodine intake through respiration
There is no doubt that increased pollution, particularly tropospheric O3, has resulted in a significant increase in atmospheric iodine and iodine oxides. The contribution to respiratory intake of increased atmospheric iodine is more difficult to assess, although higher urinary iodine (UI) levels occurred in those communities living adjacent to abundant seaweed growth, where higher volatile iodine levels were observed (12). An example of a possible pathway whereby gaseous iodine could contribute to human iodine intake is shown in Table 2, with data points selected from various study sites in a seaweed-rich environment on the west coast of Ireland (12, 22, 23). These findings utilise seaweed as a source of gaseous iodines and assume a daily respiratory intake of 15,000 L of air (53). High tide readings reflect the fact that the seaweed is below sea level and therefore protected from atmospheric O3. At low tide, the seaweed is exposed, and the reaction I− + O3 → I2 can take place. The Coastal Range represents the presumed steady state of atmospheric iodine remote from the seaweed-abundant site and shows a low (2.7 μg) potential I− uptake. This value might apply to populations not living adjacent to a seaweed-abundant site. The higher values of 58 μg, including the maximum (81 μg) over an iodine-rich Laminaria bed, were recorded at nighttime when removal of I2 by sunlight photolysis was not an issue (12, 22, 23). Potential I2 inspired is based on μg I2 in 6–16 L/min air, resting/normal activity (~15,000 L of air/day) (53). It is unlikely, even with global warming, that atmospheric volatile iodine levels will reach the values recorded over seaweed (12). Also, it should be noted that photochemical destruction of iodine is a rapid process, taking about 10 s, but, despite this, a mixing ratio of 567 ppt iodine over the seaweed beds was observed at 5 min of exposure and remained at 239 ppt after 15–20 min (22). Emissions from the seaweed beds, consisting of the macroalgae Ascophyllum nodosum and Fucus vesiculosus, increased gradually from 2 to 300 ppt as the tide receded and was maintained for 6 h of the half tidal cycle (22).
Mixing ratios of I2 at different sites on the West Coast of Ireland (12, 22, 23, 29, 37). Readings were taken directly over and 150 m downwind of the seaweed bed. Nighttime values suggest longer survival of volatile iodines excluding their destruction by photolysis. Potential I2 inspired was based on an arbitrary 24 h intake of 15,000 L of air (53).
| Time of observation | Site | Iodine, pg/L | Potential daily I2 inspired |
|---|---|---|---|
| Day high tide | Seaweed bed | 1860 | 27 |
| Day high tide | Downwind | 230 | 35 |
| Night low tide | Seaweed bed | 3930 | 58 |
| Night low tide | Downwind | 1240 | 18 |
| Coastal range | Various | 155–180 | 2.7 |
| Over seaweed | Different sites | 1145–3132 | 46 |
| Maximum recorded | Laminaria bed | 5470 | 81 |
Skin absorption
Water-soluble iodine (povidone iodine, Betadine) is frequently used as a skin disinfectant. Apart from its germicidal action on the skin surface, iodine can be both absorbed into and excreted from the skin (54). The increasing popularity of seaweed baths showed modest uptake of iodine, probably through a combination of skin absorption and respiration following such treatments (55). In view of the current very low levels of I− in sea spray, it is unlikely that deposition of I− on the skin, even in an iodine-enhanced ocean, would make a significant contribution to iodine intake. Unlike iodide (I−), which is actively taken up by the thyroidal basolateral sodium iodide symporter (NIS), I2 deposited on the skin is believed to be passively absorbed and excreted (54).
Discussion
There is little doubt that the current climate crisis provoked by global warming has the potential, in the immediate to middle-term future, to greatly increase global iodine supply. Whether this increase implies increased bioavailability in terms of inorganic I− remains uncertain, but it is reasonable to assume that increased atmospheric iodine resulting from continuing greenhouse gas pollution, including O3, will result in increased iodine deposition through rainfall in soil and on grasslands, resulting in foodstuffs richer in iodine. Milk iodine would be expected to increase, which would be particularly relevant in populations without the benefit of USI, whose dietary iodine intake is principally milk or dairy-product based (49, 50) In a majority of countries, the policy of USI has removed or almost corrected the problems associated with IDD (10). In such countries, the bioavailability of the relatively small increase in atmospheric iodine might not, at least in the short term, be expected to produce significant effects in population thyroid status. Increased iodine intake through respiration or absorption through the skin remains a possibility but remains unproven. The higher nighttime values for gaseous iodine emissions would only be relevant in populations living adjacent to a seaweed-abundant site. This uptake could be particulate or gaseous in form (56). Although the evidence for respiration making a significant contribution to human iodine uptake is inconclusive, the observations over a seaweed mass and in populations residing in seaweed-abundant regions may serve as a template for an iodine-enriched environment (12, 23). The overall levels of atmospheric iodine may never reach the values recorded over seaweed beds, but the reports of a tripling of deposited iodine in the Alps and in Greenland, together with the observation that current iodine deposition may in the near future lead to the greatest observed in 127,000 years (36), must at least raise consciousness among the thyroid community of the potential for significant changes in global iodine status and perhaps encourage the health-care community to address this issue. What remains unclear is the potential contribution to global iodine status of the observed threefold increase in atmospheric iodine, mainly arising from the consequence of anthropogenic pollution (37, 38). This increase was noted between 1950 and 2010 and would be of a much higher order if compared to preindustrial times and is likely to continue into the 21st century despite societal efforts to mitigate factors leading to global warming (36). From historical data, these workers hypothesised a near-future scenario with the highest iodine levels in 127,000 years on the basis of lower Arctic ice core iodine values 3.8 and 5.1 μg m−2 year−1 in the last glacial cycle increasing to a maximum of 9.6 μg m−2 year−1 when the sea ice retreated (36).
The increased volatile iodine emissions evident in the marine atmosphere as a result of the effects of global warming will create a more iodine-rich environment with the potential for increased human or animal uptake. The hypothetical daily iodine intake shown in Table 2, calculated for individuals living beside or remote from a seaweed-abundant coastal area, shows a wide variation (2.7–81.0 μg) but illustrates a source for the potential intake that might arise from greatly increased iodine emissions. Changes in iodine bioavailability because of seaweed loss resulting from ocean warming/acidification remain unknown (40, 42). Obviously, very few populations live in seaweed-rich coastal areas, but the potential for greatly increased iodine deposition as a result of oceanic production of gaseous iodines (I2 and HOI) arising from O3 at the ocean surface or biotic sources (bacteria and photolytic destruction of organic iodines) has the potential to give rise to increased iodine deposition (37, 38).
All these pathways depend on the concentration of iodine reached because of the consequences of atmospheric pollution. In their publication comparing Arctic iodine over different glacial periods, Corella and his colleagues point out that anthropogenic ozone-induced iodine emissions may lead to the highest iodine levels of the last 127,000 years (36). They noted that iodine fluxes have doubled from the preindustrial era in 1750 to 2010 and tripled from 1950 to 2010. The anthropogenic component is further emphasised by the greater increase in greenhouse gas and consequential iodine emissions in the northern hemisphere (37). The acceleration in the disappearance of the polar ice sheets, together with unprecedented increases in global land and sea temperatures, can only add to iodine emissions. Recent increases in sea temperatures in the North Atlantic, termed the North Atlantic warming hole (57), and in the Southern ocean (58) also have the potential to increase dissolved iodine. Of course, the authors are not unaware that the iodine story is dwarfed by the real threat posed by global warming to current human existence (2). It is highly unlikely that any improvements in global iodine status, in terms of diminishing IDD with associated benefits such as population infant neuropsychological development, will ever outweigh the increasing adverse effects of global warming (2, 10). It may be that governmental and societal responses to these potential catastrophes may succeed in diminishing greenhouse gas emissions and therefore lessen the potential iodine increases. In any event, it is hoped that the realisation of the possibility of a significant increase in global iodine will stimulate studies on the subject.
The potential contribution of possible increases in mammalian thyroidal iodine uptake to thyroid physiology or pathology must remain speculative. A decrease in goitre and hyperthyroidism, mainly toxic nodular goitre, has been shown in Denmark following iodisation of table salt, but a small increase in hypothyroidism was noted (59). However, a report from China suggested that hyperthyroidism prevalence remained stable two decades after USI (60). The Danish authors observed that even small systematic increases in iodine supply can significantly increase both the presentation and risk of thyroid disease and emphasised the importance of increasing iodine intake to the level where IDD are prevented and not higher (59, 61). Studies in China of high-iodine containing groundwater enhanced by land overuse and intensive anthropogenic overexploitation showed an increased prevalence of subclinical hypothyroidism (62). The increased intake brought about by climate change would, by its nature, be of a long term. Undoubtedly, the human thyroid can adapt to different iodine intakes, as demonstrated by the Japanese experience where daily dietary intakes of approximately 1 mg (63), orders of magnitude greater than western intake, can be readily tolerated, perhaps by resetting an iodostat as suggested (64).
In the absence of previously largely unsuccessful attempts to reduce atmospheric pollution, the contribution of volatile iodines, by reducing atmospheric O3 pollution, may not be sufficient to alleviate the damaging effects of global warming but could paradoxically have a beneficial consequence of improving iodine status and thyroidal health.
Declaration of interest
The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the study reported.
Funding
This work did not receive any specific grant from any funding agency in the public, commercial or not-for-profit sector.
Acknowledgement
The authors are grateful to Christopher Murphy, BDes, for design advice.
References
- 1↑
IPCC. Climate change 2022: impacts, adaptation and vulnerability . Working group II contribution to the IPCC sixth assessment report. 2022.
- 3↑
Carpenter LJ, Chance RJ, Sherwen T, Adams TJ, Ball SM, Evans MJ, Hepach H, Hollis LDJ, Hughes C, Jickells TD, et al.Marine iodine emissions in a changing world. Proceedings. Mathematical, Physical, and Engineering Sciences 2021 477 20200824. (https://doi.org/10.1098/rspa.2020.0824)
- 4↑
Wadley MR, Stevens DP, Jickells TD, Hughes C, Chance R, Hepach H, Tinel L, & Carpenter LJ. A global model for iodine speciation in the upper ocean. Global Biogeochemical Cycles 2020 34 e2019GB006467. (https://doi.org/10.1029/2019GB006467)
- 5↑
Sherwen T, Evans MJ, Carpenter LJ, Schmidt JA, & Mickley LJ. Halogen chemistry reduces tropospheric O3 radiative forcing. Atmospheric Chemistry and Physics 2017 17 1557–1569. (https://doi.org/10.5194/acp-17-1557-2017)
- 6↑
Saiz-Lopez A, Fernandez RP, Li Q, Cuevas CA, Fu X, Kinnison DE, Tilmes S, Mahajan AS, Gómez Martín JC, Iglesias-Suarez F, et al.Natural short-lived halogens exert an indirect cooling effect on climate. Nature 2023 618 967–973. (https://doi.org/10.1038/s41586-023-06119-z)
- 7↑
Benavent N, Mahajan AS, Li Q, Cuevas CA, Schmale J, Angot H, Jokinen T, Quéléver LLJ, Blechschmidt A, Zilker B, et al.Substantial contribution of iodine to Arctic ozone destruction. Nature Geoscience 2022 15 770–773 . doi:10.1038/s41561-022-01018-w.
- 8↑
Fuge R, & Johnson CC. The geochemistry of iodine: a review. Environmental Geochemistry and Health 1986 8 31–54. (https://doi.org/10.1007/BF02311063)
- 9↑
Smyth PPA. Iodine, seaweed and the thyroid. European Thyroid Journal 2021 10 101–108. (https://doi.org/10.1159/000512971)
- 10↑
Zimmermann MB, & Andersson M. Assessment of iodine nutrition in populations: past, present, and future. Nutrition Reviews 2012 70 553–570. (https://doi.org/10.1111/j.1753-4887.2012.00528.x)
- 11↑
Smyth PPA, & O'Dowd CD. Letter to the editor: the potential impact of the climate crisis on global iodine status. Thyroid 2023 33 997–998. (https://doi.org/10.1089/thy.2023.0151)
- 12↑
Ravera S, Reyna-Neyra A, Ferrandino G, Amzel LM, & Carrasco N. The sodium/iodide symporter (NIS): molecular physiology and preclinical and clinical applications. Annual Review of Physiology 2017 79 261–289. (https://doi.org/10.1146/annurev-physiol-022516-034125)
- 13↑
Truesdale VW, Bale AJ, & Woodward EMS. The meridional distribution of dissolved iodine in near-surface waters of the Atlantic Ocean. Progress in Oceanography 2000 45 387–400. (https://doi.org/10.1016/S0079-6611(0000009-4)
- 14↑
Smyth PP, Burns R, Huang RJ,Hoffman T, Mullan K, Graham U, Seitz K, Platt U, & O’Dowd C. Does iodine gas released from seaweed contribute to dietary iodine intake? Environmental Geochemistry and Health 2011 33 389–397. (https://doi.org/10.1007/s10653-011-9384-4)
- 15↑
Sherwen T, Chance RJ, Tinel L, Ellis D, Evans MJ, & Carpenter LJ. A machine-learning-based global sea-surface iodide distribution. Earth System Science Data 2019 11 1239–1262. (https://doi.org/10.5194/essd-11-1239-2019)
- 16↑
MacDonald SM , Gómez Martín JC, Chance R, Warriner S, Saiz-Lopez A, Carpenter LJ, & Plane JMC. A laboratory characterisation of inorganic iodine emissions from the sea surface: dependence on oceanic variables and parameterisation for global modelling. Atmospheric Chemistry and Physics 2014 14 5841–5852. (https://doi.org/10.5194/acp-14-5841-2014)
- 17↑
Gómez Martín JC, Saiz-Lopez A, Cuevas CA, Fernandez RP, Gilfedder B, Weller R, Baker AR, Droste E, & Lai S. Spatial and Temporal Variability of Iodine in Aerosol. Journal of Geophysical Research: Atmospheres 2021 126 e2020JD034410. (https://doi.org/10.1029/2020JD034410)
- 18↑
Luther GW III. Review on the physical chemistry of iodine transformations in the oceans. Frontiers in Marine Science 2023 10 1085618. (https://doi.org/10.3389/fmars.2023.1085618)
- 19↑
Prados-Roman C, Cuevas CA, Hay T, Fernandez RP, Mahajan AS, Royer S-J, Galí M, Simó R, Dachs J, Großmann K, et al.Iodine oxide in the global marine boundary layer. Atmospheric Chemistry and Physics 2015 15 583–593. (https://doi.org/10.5194/acp-15-583-2015)
- 20↑
Chance RJ, Tinel L, Sherwen T, Baker AR, Bell T, Brindle J, Campos MLAM, Croot P, Ducklow H, Peng H, et al.Global sea-surface iodide observations, 1967–2018. Scientific Data 2019 6 286. (https://doi.org/10.1038/s41597-019-0288-y)
- 21↑
Ku¨pper FC, Carpenter LJ, McFiggans GB, Palmer CJ, Waite TJ, Boneberg EM, Woitsch S, Weiller M, Abela R & Grolimund D et al.Iodiden accumulation provides kelp with an inorganic antioxidant impacting atmospheric chemistry. Proceedings of the National Academy of Sciences 2008 105 6954–6958. (https://doi.org/10.1073/pnas.0709959105)
- 22↑
Huang R-J, Thorenz UR, Kundel M, Venables DS, Ceburnis D, Ho KF, Chen J, Vogel AL, Küpper FC, Smyth PPA, et al.The Seaweeds Fucus and Ascophyllum seaweeds are significant contributors to coastal iodine emissions. Atmospheric Chemistry and Physics Discussions 2013 12 25915–25939. (https://doi.org/10.5194/acpd-12-25915-2012)
- 23↑
Huang R-J, Seitz K, Buxmann J, Po¨hler D, Hornsby KE, Carpenter LJ, Platt U, & Hoffmann T. In situ measurements of molecular iodine in the marine boundary layer: the link to macroalgae and the implications for O3, IO, OIO and NOx. Atmospheric Chemistry and Physics 2010 10 4823–4833. (https://doi.org/10.5194/acp-10-4823-2010)
- 24↑
Zava TT, & Zava DT. Assessment of Japanese iodine intake based on seaweed consumption in Japan: a literature-based analysis. Thyroid Research 2011 4 14. (https://doi.org/10.1186/1756-6614-4-14)
- 25↑
Leblanc C, Colin C, Cosse A, Delage L, La Barre S, Morin P, Fiévet B, Voiseux C, Ambroise Y, Verhaeghe E, et al.Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 2006 88 1773–1785. (https://doi.org/10.1016/j.biochi.2006.09.001)
- 26↑
Lazarus JH. The importance of iodine in publichealth. Environmental Geochemistry and Health 2015 37 605–618. (https://doi.org/10.1007/s10653-015-9681-4)
- 27↑
Roleda MY, Skjermo J, Marfaing H, Jónsdóttir R, Reboursa C, Gietlf A, Stengel DB, & Nitschke U. Iodine content in bulk biomass of wild-harvested and cultivated edible seaweeds: inherent variations determine species-specific daily allowable consumption. Food Chemistry 2018 254 333–339. (https://doi.org/10.1016/j.foodchem.2018.02.024)
- 28↑
Dixneuf S, Ruth AA, Vaughan S, Varma RM, & Orphal J. The time dependence of molecular iodine emission from Laminaria digitata. Atmospheric Chemistry and Physics 2009 9 823–829. (https://doi.org/10.5194/acp-9-823-2009)
- 29↑
Tham YJ, He XC, Li Q, Cuevas CA, Shen J, Kalliokoski J, Yan C, Iyer S, Lehmusjärvi T, Jang S, et al.Direct field evidence of autocatalytic iodine release from atmospheric aerosol. Proceedings of the National Academy of Sciences of the United States of America 2021 118 e2009951118. (https://doi.org/10.1073/pnas.2009951118)
- 30↑
Koenig TK, Volkamer R, Apel EC, Bresch JF, Cuevas CA, Dix B, Eloranta EW, Fernandez RP, Hall SR, Hornbrook RS, et al.Ozone depletion due to dust release of iodine in the free troposphere. Science Advances 2021 7 eabj6544. (https://doi.org/10.1126/sciadv.abj6544)
- 31↑
Bell N, Hsu L, Jacob DJ, Schultz MG, Blake DR, Butler JH, King DB, Lobert JM, & Maier-Reimer E. Methyl iodide: atmospheric budget and use as a tracer of marine convection in global models. Journal of Geophysical Research: Atmospheres 2002 107 4340. (https://doi.org/10.1029/2001JD001151)
- 32↑
Pound RJ, Durcan DP, Evans MJ, & Carpenter LJ. Comparing the importance of iodine and isoprene on tropospheric photochemistry. Geophysical Research Letters 2023 50 e2022 GL100997. (https://doi.org/10.1029/2022GL100997)
- 33↑
O'Dowd CD, Jimenez JL, Bahreini R, Flagan RC, Seinfeld JH, Hämeri K, Pirjola L, Kulmala M, Jennings SG, & Hoffmann T. Marine aerosol formation from biogenic iodine emissions. Nature 2002 417 632–636. (https://doi.org/10.1038/nature00775)
- 34↑
Slingo A. Sensitivity of the Earth's radiation budget to changes in low clouds. Nature 1990 343 49–51. (https://doi.org/10.1038/343049a0)
- 35↑
Cuevas CA, Fernandez RP, Kinnison DE, Li Q, Lamarque JF, Trabelsi T, Francisco JS, Solomon S, & Saiz-Lopez A. The influence of iodine on the Antarctic stratospheric ozone hole. Proceedings of the National Academy of Sciences of the United States of America 2022 119 e2110864119. (https://doi.org/10.1073/pnas.2110864119)
- 36↑
Corella JP, Maffezzoli N, Spolaor A, Vallelonga P, Cuevas CA, Scoto F, Müller J, Vinther B, Kjær HA, Cozzi G, et al.Climate changes modulated the history of Arctic iodine during the last Glacial cycle. Nature Communications 2022 13 88. (https://doi.org/10.1038/s41467-021-27642-5)
- 37↑
Legrand M, McConnell JR, Preunkert S, Arienzo M, Chellman N, Gleason K, Sherwen T, Evans MJ, & Carpenter LJ. Alpine ice evidence of a three-fold increase in atmospheric iodine deposition since 1950 in Europe due to increasing oceanic emissions. Proceedings of the National Academy of Sciences of the United States of America 2018 115 12136–12141. (https://doi.org/10.1073/pnas.1809867115)
- 38↑
Cuevas CA, Maffezzoli N, Corella JP, Spolaor A, Vallelonga P, Kjær HA, Simonsen M, Winstrup M, Vinther B, Horvat C, et al.Rapid increase in atmospheric iodine levels in the North Atlantic since the mid-20th century. Nature Communications 2018 9 1452. (https://doi.org/10.1038/s41467-018-03756-1)
- 39↑
Baker AR, & Yodle C. Measurement report: indirect evidence for the controlling influence of acidity on the speciation of iodine in Atlantic aerosols. Atmospheric Chemistry and Physics 2021 21 13067–13076. (https://doi.org/10.5194/acp-21-13067-2021)
- 40↑
Butler C, Lucieer V, Wotherspoon S, & Johnson CR. Multi-decadal decline in cover of giant kelp Macrocystis pyrifera at the southern limit of its Australian range. Marine Ecology – Progress Series 2020 653 1–18. (https://doi.org/10.3354/meps13510)
- 41↑
Johnson CR, Banks SC, Barrett NS, Cazassus F, Dunstan PK, Edgar GJ, Frusher SD, Gardner C, Haddon M, Helidoniotis F, et al.Climate change cascades: shifts in oceanography, species' ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 2011 400 17–32. (https://doi.org/10.1016/j.jembe.2011.02.032)
- 42↑
Smale DA, Burrows MT, Moore P, O'Connor N, & Hawkins SJ. Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and Evolution 2013 3 4016–4038. (https://doi.org/10.1002/ece3.774)
- 43↑
Xu D, Brennan G, Xu L, Zhang XW, Fan X, Han WT, Mock T, McMinn A, Hutchins DA, & Ye N. Ocean acidification increases iodine accumulation in kelp-based coastal food webs. Global Change Biology 2019 25 629–639. (https://doi.org/10.1111/gcb.14467)
- 44↑
Roulier M, Bueno M, Coppin F, Nicolas M, Thiry Y, Rigal F, Le Hécho I, & Pannier F. Atmospheric iodine, selenium and caesium depositions in France: I. spatial and seasonal variations. Chemosphere 2021 273 128971. (https://doi.org/10.1016/j.chemosphere.2020.128971)
- 45↑
Ham YG, Kim JH, Min SK, Kim D, Li T, Timmermann A, & Stuecker MF. Anthropogenic fingerprints in daily precipitation revealed by deep learning. Nature 2023 622 301–307. (https://doi.org/10.1038/s41586-023-06474-x)
- 46↑
Xiong I, Guo S , Abhishek CJ, & Yin J. Global evaluation of the “dry gets drier, and wet gets wetter” paradigm from a terrestrial water storage change perspective. Hydrology and Earth System Sciences 2022 26 6476. (https://doi.org/10.5194/hess-26-6457-2022)
- 47↑
Suess E, Aemisegger F, Sonke JE, Sprenger M, Wernli H, & Winkel LHE. Marine versus continental sources of iodine and selenium in rainfall at two European high-altitude locations. Environmental Science and Technology 2019 53 1905–1917. (https://doi.org/10.1021/acs.est.8b05533)
- 48↑
Gilfedder BS, Petri M, & Biester H. Iodine speciation in rain and snow: implications for the atmospheric iodine sink. Journal of Geophysical Research 2007 112 D07301. (https://doi.org/10.1029/2006JD007356)
- 49↑
Andersen S, Petersen SB, & Laurberg P. Iodine in drinking water in Denmark is bound in humic substances. European Journal of Endocrinology 2002 147 663–670. (https://doi.org/10.1530/eje.0.1470663)
- 50↑
Bath SC, Combet E, Scully P, Zimmermann MB, Hampshire-Jones KH, & Rayman MP. A multi-centre pilot study of iodine status in UK schoolchildren, aged 8-10 years. European Journal of Nutrition 2016 55 2001–2009. (https://doi.org/10.1007/s00394-015-1014-y)
- 51↑
Smyth P, Burns R, Casey M, Mullan K, O’Herlihy C, & O’Dowd C. Iodine status over two decades: influence of seaweed exposure. Irish Medical Journal 2016 109 421.
- 52↑
Niero G, Visentin G, Censi S, Righi F, Manuelian CL, Formigoni A, Mian C, Bérard J, Cassandro M, Penasa M, et al.Invited review: iodine level in dairy products-a feed-to-fork overview. Journal of Dairy Science 2023 106 2213–2229. (https://doi.org/10.3168/jds.2022-22599)
- 53↑
Pleil JD, Ariel Geer Wallace M, Davis MD, & Matty CM. The physics of human breathing: flow, timing, volume, and pressure parameters for normal, on-demand, and ventilator respiration. Journal of Breath Research 2021 15 042002. (https://doi.org/10.1088/1752-7163/ac2589)
- 54↑
Westby T, Cadogan A, & Duignan G. In vivo uptake of iodine from a Fucus serratus Linnaeus seaweed bath: does volatile iodine contribute? Environmental Geochemistry and Health 2018 40 683–691. (https://doi.org/10.1007/s10653-017-0015-6)
- 55↑
Nesvadbova M, Crosera M, Maina G, & Filon FL. Povidone iodine skin absorption: an ex-vivo study. Toxicology Letters 2015 235 155–160. (https://doi.org/10.1016/j.toxlet.2015.04.004)
- 56↑
Harvey RP, Hamby DM, & Palmer TS. Uncertainty of the thyroid dose conversion factor for inhalation intakes of 131I and its parametric uncertainty. Radiation Protection Dosimetry 2006 118 296–306. (https://doi.org/10.1093/rpd/nci349)
- 57↑
Kusakabe Y, & Takemura T. Formation of the North Atlantic warming hole by reducing anthropogenic sulphate aerosols. Scientific Reports 2023 13 8. (https://doi.org/10.1038/s41598-022-27315-3)
- 58↑
Cai W, Gao L, Luo Y, Li X, Zheng X, Zhang X, Cheng X, Jia F, Purich A, Santoso A, et al.Southern Ocean warming and its climatic impacts. Science Bulletin 2023 68 946–960. (https://doi.org/10.1016/j.scib.2023.03.049)
- 59↑
Petersen M, Knudsen N, Carlé A, Andersen S, Jørgensen T, Perrild H, Ovesen L, Rasmussen LB, Thuesen BH, & Pedersen IB. Increased incidence rate of hypothyroidism after iodine fortification in Denmark: a 20-year prospective population-based study. Journal of Clinical Endocrinology and Metabolism 2019 104 1833–1840. (https://doi.org/10.1210/jc.2018-01993)
- 60↑
Laurberg P. DanThyr 20 years of iodine monitoring and research. Thyroid International 2015 2 1–25.
- 61↑
Wang C, Li Y, Teng D, Shi X, Ba J, Chen B, Du J, He L, Lai X, Li Y, et al.Hyperthyroidism prevalence in China after universal salt iodization. Frontiers in Endocrinology (Lausanne) 2021 12 651534. (https://doi.org/10.3389/fendo.2021.651534)
- 62↑
Ma R, Yan M, Han P, Wang T, Li B, Zhou S, Zheng T, Hu Y, Borthwick AGL, Zheng C, et al.Deficiency and excess of groundwater iodine and their health associations. Nature Communications 2022 13 7354. (https://doi.org/10.1038/s41467-022-35042-6)
- 63↑
Nagataki S. The average of dietary iodine intake due to the ingestion of seaweeds is 1.2 mg/day in Japan. Thyroid 2008 18 667–668. (https://doi.org/10.1089/thy.2007.0379)
- 64↑
Dworkin HJ, Jacquez JA, & Beierwaltes WH. Relationship of iodine ingestion to iodine excretion in pregnancy. Journal of Clinical Endocrinology and Metabolism 1966 26 1329–1342. (https://doi.org/10.1210/jcem-26-12-1329)
