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Production of Allergenic Pollen by Ragweed (Ambrosia Artemisiifolia

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Production of Allergenic Pollen by Ragweed (Ambrosia Artemisiifolia Production of allergenic pollen by ragweed (Ambrosia artemisiifolia L.) is increased in CO2-enriched atmospheres Peter Wayne, PhD*; Susannah Foster, BS*; John Connolly, PhD†; Fakhri Bazzaz, PhD*; and Paul Epstein, MD‡ Background: The potential effects of global climate change on allergenic pollen creased by 29% since preindustrial production are still poorly understood. times, and is expected to double again 13 Objective: To study the direct impact of rising atmospheric CO2 concentrations sometime between 2050 and 2100. on ragweed (Ambrosia artemisiifolia L.) pollen production and growth. Increased CO2 concentrations stimu- Methods: In environmentally controlled greenhouses, stands of ragweed plants were late plant net photosynthetic rate,14 in- 15 grown from seed through flowering stages at both ambient and twice-ambient CO2 crease water use efficiency, decrease levels (350 vs 700 ␮LLϪ1). Outcome measures included stand-level total pollen carbon loss to dark respiration,16 and production and end-of-season measures of plant mass, height, and seed production. alter phenology17 and allocation pat- 18 Results: A doubling of the atmospheric CO2 concentration stimulated ragweed- terns. The net result of these re- ϭ pollen production by 61% (P 0.005). sponses is that plants grown in CO2- Conclusions: These results suggest that there may be significant increases in enriched atmospheres generally grow exposure to allergenic pollen under the present scenarios of global warming. Further faster and are larger at maturity, al- studies may enable public health groups to more accurately evaluate the future risks though the magnitudes of growth and of hay fever and respiratory diseases (eg, asthma) exacerbated by allergenic pollen, physiologic enhancements vary con- and to develop strategies to mitigate them. siderably with environmental condi- Ann Allergy Asthma Immunol 2002;88:279–282. tions and species identity.19,20 Whereas significant CO2-induced changes to re- INTRODUCTION within the past 50 years and the phe- production have been documented,21,22 Global environmental change has re- nology and abundance of allergenic nearly all studies to date have focused ceived significant attention in the pollen released by a number of Euro- on the responsiveness of female repro- fields of conservation biology, agricul- pean tree species.6,7 However, only ductive structures (ie, flowers, fruits, and ture, and economics. Only recently, limited data are currently available to seed). In one recent study, Ziska and however, has research begun to ad- evaluate the direct effects of rising at- Caulfield8 found that exposing ragweed dress how a changing global environ- mospheric CO2 concentrations on pol- plants to the higher CO2 concentrations ment may affect public health.1 Out- len production by allergenic plants and predicted in the year 2100 doubled the breaks and expansion of diseases its potential impact on public health.8 quantity of pollen produced. transmitted by vectors sensitive to cli- Human allergic responses to the pol- Ragweed (Ambrosia artemisiifolia matic shifts (eg, malaria, dengue fever, len of certain plant species (hay fever, L.) is a plant common to roadsides and and equine encephalitis) have been allergenic rhinitis, pollinosis) is a seri- disturbed habitats throughout most of linked to environmental change.2–4 ous environmental health issue.9 the United States and Canada.23 It is Thinning of the ozone layer is ex- Aeroallergens, including pollen, also dioecious, with male and female flow- pected to increase the incidence of play a role in the exacerbation of asth- ers born on distinct axillary branches, melanomas.5 Recent studies have also ma.10 The prevalence of both hay fever allowing for independent control of al- shown a link between warming trends and asthma has increased significantly location to sexes.24 Throughout its dis- in recent decades.11,12 Little research tribution, ragweed pollen is one of the has been devoted to understanding most abundant aeroallergens in late * Department of Organismic and Evolutionary how various components of global en- summer and fall, and it is one of the Biology, Harvard University, Cambridge, Mas- sachusetts. vironmental change influence aller- primary causes of seasonal pollen al- 25 † Department of Statistics, University College of genic pollen production and, thus, the lergy in North America. Conse- Dublin, Dublin, Ireland. potential for pollen-related disease. quently, ragweed pollen and specific ‡ Center for Health and the Global Environment, An increase in the concentration of allergens extracted from it have been Harvard Medical School, Boston Massachusetts. Received for publication October 25, 2001. atmospheric CO2 is one of the most used in many clinical studies, and the Accepted for publication in revised form No- certain predictions of climate change biochemistry and genetics of ragweed vember 1, 2001. models. CO2 concentration has in- allergens and their impacts on the hu- VOLUME 88, MARCH, 2002 279 man immune systems are well under- of ethanol. To estimate pollen concen- reported an even greater magnitude of stood.26,27 tration, a 5-mL sample of well mixed pollen increase. Similarly, our ob- This study investigates the direct pollen-ethanol solution was transferred served CO2-induced enhancement to impact of rising CO2 concentrations on to a glass vial and dried for 24 hours in shoot biomass is similar to average pollen production in experimental pop- an oven. The dried pollen was then species enhancements values (54%) ulations of ragweed. The results will mixed with 4 mL of concentrated salt observed in surveys of fast-growing be used to more accurately evaluate the water (Instant Ocean, Mentor, OH) and wild plants.18 future risks of hay fever and respira- subsamples of this solution were ana- Detailed data on individual plant pol- tory disease exacerbated by allergenic lyzed for pollen particle number and len production and reproductive devel- pollen, and to develop strategies to size using a Coulter Z-series Particle opment were not investigated in this mitigate them. Count and Size Analyzer (Hialeah, study. Nevertheless, it is possible that in FL). Calibration for particle size was addition to increasing stand-level pollen MATERIALS AND METHODS conducted by using 50-␮m beads using production through increased plant size, To study pollen production by ragweed the protocol suggested by the manufac- high CO2 may have resulted in plants populations in elevated CO2 atmo- turer. Particle number was calibrated allocating proportionally more resources spheres, seeds of Ambrosia artemisi- against solutions of pure salt water. to pollen relative to seed or total shoot ifolia L. were grown to reproductive After pollen removal from plants, all mass. Previous studies with ragweed maturity in controlled-environment mature seeds were removed from each have shown that adding essential re- glasshouses. Seeds were initially col- shoot, and along with total shoot bio- sources to stands (eg, nitrogen) results lected from wild populations in Wood- mass, oven-dried and weighed to the in plants investing in proportionally stock, Illinois. Seed were sown into 12 nearest gϪ4. Shoot height was mea- more male versus female reproductive total 30-L growth containers (50 ϫ sured immediately before pollen re- structures.29 More generally, studies 40 ϫ 15 cm). Soil in each container moval. Persons responsible for pollen with ragweed and other wind-polli- was composed of a 4:3 mix of Pro-Mix collection and measurements of parti- nated species suggest that larger and compost (Red Hill, PA) and washed cle counts and plant size, were not taller plants within populations tend to 30,31 sand (Quickrete Co, Atlanta, GA). blinded as to which CO2 environments be male more often. Containers were fertilized weekly with plants were grown in. It will be challenging to accurately 500 mL of 20:20:20 NPK Peter’s So- For all traits, including total pollen predict the future threat to public lution (Allentown, PA), and watered production, mean pollen size, shoot health caused by CO2-stimulated pol- daily. Day/night temperatures were biomass, height, and seed weight, dif- len production. As with most environ- maintained at 26/21° C and ambient ferences between treatments were mental health issues, many factors are glasshouse light levels were approxi- evaluated with analysis of variance involved, and in the specific case of cli- mately 70% of full sun. that compared the effects of CO2 to the mate change, the future state of many of ϫ Containers were randomly assigned larger of Block CO2 and container- the factors themselves is uncertain. to two blocks, each containing two to-container variation. Based on previous climate change stud- modules maintained at either ambient ies evaluating the responses of plant 350 ␮LLϪ1) or double ambient (700 RESULTS AND DISCUSSION growth and yield, it is likely that plant ␮ Ϫ1 LL )CO2 concentrations (ie, three We found that stand-level pollen pro- pollen production will also be influenced containers per growth module). Thirty duction was 61% higher in elevated by factors expected to change in concert plants were established in each growth versus ambient CO2 environments with CO2, including temperature, precip- ϭ ϭ 15,32,33 container and arranged in a regular (F 15.16, P 0.005); however CO2 itation, and atmospheric pollutants. grid. This resulted in a density of 150 did not significantly influence the av- Over longer periods of time, these fac- plants mϪ2, a density commonly ob- erage
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