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World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop and Systems Laboratory U.S.Department of Agriculture "- Building 001, Room 323,10300Baltimore Avenue Beltsville, MD 20705 USA e-mail: [email protected] Keywords: AJlersieI. carbon dioxide, herbicide usage, nutrition, phano~uticals, raaweed. toxicology ABSTRAcr In addition to being the principle greeDhoUse gas,carbon dioxide (COV is also the principle sourceof carbon for photosynthesis. Although the stimulation of plant growth by rising C~ is usually viewed as a positive aspect of climate change, the rise in C~ is indiscriminate with respectto the stimulation of both anthropogenically important and deleteriousplant species. Here we present laboratory and in SJ'tu data from studiesthat have examined the response of undesirable(weedy) plants to C~ increases during the 20th century (i.e., from 290 to 375 parts per million by volume, ppmv), as well as that projected for the mid 21st century (SOO-l(xx) ppmv). Data from these studiesindicated a number of potential indirect effects(e.g.,changes in nutritional content of foods, increased useof herbicides) as weDas potential direct effects(e.g.,increased ragweed pollen) on public health. Theseinitial resultsregarding C~ and/or temperature-induced changes in plant biology suggest a number of potentially unfavorable and somefavorable consequences in human systems. However, these resultsare based on a small number of experiments and additional data are crucial to reduce the biological and economicuncertaintiesassociated with CO2-induced changes in plant biology and human health. 0 m w«w~arm. Alr.-~ 271

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Page 1: World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT ...€¦ · World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop

World Resource Review Vol. 15 No. J

CLIMATE CHANGE, PLANT BIOLOGYAND PUBLIC HEAL m

Lewis H ZiskaAlternate Crop and Systems LaboratoryU.S. Department of Agriculture "-

Building 001, Room 323,10300 Baltimore AvenueBeltsville, MD 20705 USAe-mail: [email protected]

Keywords: AJlersieI. carbon dioxide, herbicide usage, nutrition, phano~uticals, raaweed.

toxicology

ABSTRA crIn addition to being the principle greeDhoUse gas, carbon dioxide

(COV is also the principle source of carbon for photosynthesis. Although thestimulation of plant growth by rising C~ is usually viewed as a positiveaspect of climate change, the rise in C~ is indiscriminate with respect to thestimulation of both anthropogenically important and deleterious plant species.Here we present laboratory and in SJ'tu data from studies that have examinedthe response of undesirable (weedy) plants to C~ increases during the 20thcentury (i.e., from 290 to 375 parts per million by volume, ppmv), as well asthat projected for the mid 21st century (SOO-l(xx) ppmv). Data from thesestudies indicated a number of potential indirect effects (e.g., changes innutritional content of foods, increased use of herbicides) as weD as potentialdirect effects (e.g., increased ragweed pollen) on public health. These initialresults regarding C~ and/or temperature-induced changes in plant biologysuggest a number of potentially unfavorable and some favorable consequencesin human systems. However, these results are based on a small number ofexperiments and additional data are crucial to reduce the biological andeconomic uncertainties associated with CO2-induced changes in plant biologyand human health.

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INTRODUcnONDocumented and projected changes in the concentration of

atmospheric carbon dioxide [CO2J and other gases suggest potential changesin temperature and global climate that could negatively impact human health.Public health concerns related to climate stability include changes in the rangeof insect or rodent borne diseases, (e.g., malaria, yellow fever, dengue)(Gubler et aI., 2001); changes in waterborne and seafood-borne diseaseoutbreaks (Rose et aI., 2001); increasing ground-level ozone and respiratoryailments (Cifuentes et al., 2001, Bransford and Lai, 2002); contamination ofdrinking water due to increased flooding (Schelling, 1995); and, heat-relateddeaths (e.g., stroke) (McGeehin and Mirabi1li, 2001). At present, there is aconcerted effort among academic and government institutions to bothrecognjze the degree of health risk and to fomlulate strategies to minimi~adverse impacts (for reviews see Bums, 2002; Epstein, 21XX>; Patz and Kovats,

2002).The implications of a changing climate with respect to floods, storms,

range of disease vectors, etc., are well recognized. However, less attention hasbeen given to potential associations between climate, plant biology and humanhealth. Plant biology is directly affected by rising C~ since C~ is the solesupplier of carbon for photosynthesis. Because 96% of all plant species aredeficient in the amount of C~ needed to operate at maximum efficiency,recent increases in CO2 and future projections have already, and will continue,to stimulate plant growth (e.g., Poortcr, 1993), with the degree of stimulationbeing at least, potentially, temperature dependent (Long. 1991). Critics of therole of carbon dioxide as a greenhouse warming gas have stressed that C~-induced stimulation of plant growth will result in a lush plant environment(Idso and Idso, 1994); indeed, much of the literature has focused onanthropogcnical1y beneficial species (see Ainsworth et al., 2002; Curtis andWang. 1998; Kimball, 1993, iDter alia). However, it should be emphasizedthat C~ docs not discriminate between desirable (e.g., wheat, rice) andundesirable (e.g., ragweed, poison ivy) plant species (Patterson, 1995).

How would changes in plant biology impact public health? How have.past or projected atmospheric C~ levels mediated such changes? In thispaper we will provide a number of specific examples of potential direct andindirect effects on public health associated with CO2-induced changes in plantbiology. While these initial examples arc limited, we hope to emphasize the

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potential scope and impact of such effects and to highlight areas whereadditional data are needed.

SIMULA TI ON OF PAST AND FUTURE CLIMATESApplicability of data regarding plant biology and potential health

effects to a larger population is detennined in 'part by the experimentaltechniques used to obtain plant responses to past and projected atmosphericcarbon dioxide, Simulation of changing C~ and/or temperature utilizes awide range of indoor and outdoor methodologies, Here we provide a briefoverview of the means by which plant responses to C~ and/or temperatureare assessed (for a detailed review, see Moya et al. ,1997),

. Environmental Growth Chambers (EGCs). Althoughoutdoor in Sl'W systems are almost always preferred. such systems cannotsimulate pre-industrial atmospheric carbon dioxide levels over a 24 hourperiod (e.g., Mayeux et aI., 1993). Rather,' cloSed growth chambersystems with high C~ scrubbing capacity must be utilized, Such systemsallow precise control of edaphic factors, humidity, light, CO2,temperature, nutrients, pest control, etc. However, because of spaceconsiderations, the response of individual plants is usually evaluated,

. Gr=nbouses(GHs). Similar to growth chambers withrespect to control ofmicro-climate and C~, However, larger spacemay allow multi-species comparisons; in addition, natural light can beutilized or supplemented with an artiftciallight source for greatercontrol,

. OpeD-top chambers (OTCs). Usually field-based plexiglasschambers enclosing a small (2-6 m~ area. This method does allowspecies comparison of growth and physiology under in situ conditionsof soil, water, light, etc. while simulating future (but not past) levelsof atmospheric C~. However, most OTCs modify the abiotic microenvironment around the plant community with a subsequent effect onenergy flow, bioproccsses and plant growth, although the degree ofmodifICation depends on the system used.

. Free-Air CO2 Enn"chment(FACE). It was partly to negatethe induced micro-climatic changes of OTCs that the FACE systemwas introduced in the early 90s (Hendrcy and Kimball, 1994). FACEis an in situ system consisting of a large metal ring surrounding an

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experimental plot. The ring allows injection of CO2 at high velocitiesinto the center of large plots (100-500 m~ in order to simulate futureC~ values. FACE reduces micro-climate effects and provides themost realistic assessment of future C~ levels. However, operatingcosts for FACE systems can be high. In addition, only C~ can besupplemented in a FACE system, simul~eous increases in CO2 andtemperature over large areas are not pos$ible.

. Rural-Urban Transects(RUTS). It is clear that the twoprinciple environmental parameters expected to increase with globalclimate, ambient air temperature and CO2, also increase in response

to urbanization (Ids,? et al., 1998; 2001; Ziska, 2000). Experimentalplots which are located within urban, suburban and rural areas haverecently been used as an in situ means to simulate future climates(e.g., Ziska et al., 2003). Although this transect does not allowseparation of CO2 from temperature effects, it would provide a meansto assess concurrent increases in CO2 and temPerature over large

areas.

0 2003 WcxkI Resounz Review. AU riIbIJ~. 274

PUBLIC HEALTHWhile we generally think of plants in positive terms, there are a

number of species whose presence is considered undesirable or evendangerous. We call such plants "weeds" as a means to denote theirundesirability with respect to human activity. Although weeds are oftenassociated with cultivated situations (gardens, farms), they may also impacthuman health. Weeds are generally recognized as affecting human health inone of four ways: through allergenic reactions, skin irritations (contactdermatitis), mechanical injury, or internal poisoning.

AUCFgJ"es. At present it is estimated that approximately 100/0 of theU.S. population-or 30 million people-suffer from hay fever or allergenicrhinitis (Gergen et al., 1987). Symptoms include sneezing, inflammation ofnose and eye membranes, and wheezing. Complications such as nasal polypsor secondary infections of the ears, nose and throat may also be common.Severe complications, such as asthma, permanent bronchial obstructions, anddamage to the lungs and heart can occur in extreme cases. Although there are

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over four dozen plant species that produce allergic reactions, commonragweed (Ambrosia .7rtemJSiifolia L.), a ubiquitous weed, causes moreproblems tha.n all other allergenic pla.nts combined (Wodehouse, 1971),

Figure I Seasonal cban~ in ragw=d pollen prodoctioo in 2OOlalong an urbao-rural trao.ut. Soiland seed source were the same at each site. Average dally Caz concentrations were + I 0, + 112 and + 122

ppmv and a~ daily air tem~tures were +0.6, + 1.1 and + 1.9.C for the semi-rural, suburban and

urban locations relative to the rural control. No other measured climatic or air quality characteristicdiffered along the transect. Pollen counts were detennined by roto-rod sampling. Data were regressed

by ubest-fit" quadratic equation. Additional details are given in Ziska et aI., 2003.

EGC studies of common ragweed indicated that exposure toconcentrations of current CO2 (ca 370 ppmv) and that projected for the mid21st century (ca 600 ppmv) increased ragweed poDen productivity by 131 and32(1'/0 respectively, compared to ragweed grown at pre-industrial C~ levels(ca 280 ppmv) (Ziska and Caulfield, 2000). The finding regarding the responseof ragweed pollen to future C~ (relative to current levels) was later confirmedby a different group in a GH study (Wayne et al., 2002).

While intriguing, do these laboratory results have meaning underrealistic conditions? A recent two-year transect study of ragweed did, in fact.find that urbanization-induced increases in CO2 and temperature werenssociated with increased ragweed growth. poDen production and poDen

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allergenicity (Ziska et aI., 2003), suggesting a probable link between rising C~levels, global change and public health (Figure I). While most of the workregarding weeds. pollen production and climate have focused on commonragweed. rising C~ and/or temperature would also be expected to influenceseasonal pollen production of other allergenic plants. including tree and grassspecies. ,

.

Contact De1m8titis. Another common weed-induced health effect iscontact dermatitis which is associated with over 100 plant species. Thesechemical irritants can be present on all plant parts, including leaves, flowersand roots, or can appear on the plant surface when plant injury occun.Toxicity may vary with a range of factors including maturity. weather, soiland eco-type. Most reactions caused by these chemicals usually occur within afew minutes of exposure. The type of dermatitis produced is speciesdependent. For example. the milky sap in spurges can be chemically irritating.whereas some species such as the stinging nettle. (~rtica dioica L.) are bothmechanically and chemically irritating. One welt known chemical is urushiol,a mixture of catchol derivatives. This is the compound that induces contactdermatitis in the poison ivy group (ToxicodendronlRhusspp.). Sensitivity tourushiol occurs in about two of every three people, and amounts as small as Ing are sufficient to induce a rash. Over two million people in the UnitedStates suffer from annual contact with members of the poison ivy group:poison ivy (7: Toxicodendron (L.) Ktze.). poison oak (7: Toxicarium(Sa1isb.)Gillis), or poison sumac (7:vemix(L.) Ktze) (Resnick 1986)

Unfortunately. the growth and qualitative response ofToxicodendron species to increasing C~ and/or temperature is unknown.Other vines similar in morphology such as kudzu (Pueraria lobata. Ohwi),have shown relatively strong response to future CO2 levels in EGCexperiments (Sasek and Strain, 1990). GH data is available for stinging nettlehowever, showing a 3(1'/0 increase in biomass at projected C~ levels of 700ppmv (Hunt et aI., 1991). Data for leafy spurge showed a 85% stimulation ofvegetative biomass to past increases in C~ (285-380 ppmv) and a smallerincrease (3-ZO/0) to projected C~ (380-720 ppmv) in ~t EGC studies (Ziska.

2003).Physical Contact. Many weeds may also cause physical injury.

Spines, or other sharp appendages can puncture the skin. For the unwary,removing common garden weeds such as Canada thistle (Cirsium ~nse (I.)Scop.) by hand can be particularly painful. Physical wounding by thorns or

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spines cnn be p3inful. 3nd C3re must be t:lken in utilizing the proper protectivegear to nvoid injury.

As with cont3ct derrnntitis. few studies h3ve qu3ntified changes inphysical 3ppendages as a function of C~ and/or temperatures. One exceptionis recent EGC data for Cn.nadathistle showing an mcrease in the . C ad thO tl. ; an a IS enumber and length of leaf Spinesas C~ increased from 285 to 382ppmv and from 382 to 721 ppmv ..'

(Figure 2)(Ziskn. 2002).PoisonIT oxiCol°.v.

While physical injury can beannoying. ingestion of poisonousplants can result in serious illnessor death. There are over 700plant species that are known toinduce illness in humans. Similarto dermatitis. toxicology is related Ito specific plant organs (fruit. leaf, ~stem) as well as stage of growth, -g..soil and eco-type- Both edible -;

=and poisonous parts can exist on !the same plant (e.g. rhubarb 3.(Rheum rhabarbarum L., potato iSolanum lUwosa L.). Bracken, <

(Ptenaium aqu/1inum (L.) Kuhn)may represent a toxicologicalthreat due to production ofpotential carcinogenic spores orex;udates (Trotter 1990). Poisonhemlock (Conium macu/atum L.),oleander (Nerium oleander L.),jimsonweed (Datum strJ1moniumL.) and castor bean (Ricinuscommunis L.) are so poisonousthat tiny amounts can be f3tal ifeaten (e.g., ricin in castor bean has

';..!'-0Q..0c

"Q..'0'i.aE~z

- .. - - ~A!m~pherlc CO2 concentration (ppmv)

Figure 2 Chan~ in the nmnm and length (mm) of

leaf spiJa ~ for mature and immatureIea~ of Canada thistle grown at 285.382. and 721

ppmv carbon dioxide. These levels of carbon dioxide..aPJX"oximarc !hoc present at the beginning of the 20

century. the ~t concentration. and that pro~for the end of the 21" century. . indicates a '

significant diff~ at the P<0.05 le~ ~ Caztreatments for a given measurement date. Bars aretSE. See Ziska. 2002, for a complete description ofthe experimenlal details.

0 2tI)J w~ R~ RCYicw. AD ricks~.277

--

I-

,.I

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a greater potency than cyanide). For 2001, approximately 73,<xx> cases of ac:ci

dental plant ingestion were reported for children in the U.S. under theage of six (personal Communication, Dr. Rose Anne Soloway, AmericanAssociation of Poison Control Centers).

Although quantification of particular compounds such as ricin havenot been determined. the response of a number of poisonous/toxicologicalplant species to rising C~ and/or temperature have been reported. Forbracken, GH studies indicated a significant stimulation of photosynthesis withan increase in C~ concentration 200 ppmv above current ambient at twolevels ofnitrogCD supply, although, curiously, no significant effect on growthwas observed (Capom etaJ., 1999). For castor bean in EGCs, the net gain ofcarbon per leaf was approximately double at projected C~ concentrations of700 ppmv (Grimmer and Komor, 1999). For jimsonweed, a 300 ppmvincrease in CO2 resulted in a 2-3x increaSe-in seed capsules and dry weight inGH experiments (Garbutt and Ba-zzaz. 1984);~d ~ C~ increase from pre-industrial levels (-280 ppmv) to 460 ppmv in EGC trials resulted in anapproximate doubling of dry mass (Bunce, 2001). Lambsquarters( Chenopodium album) which prod~ nitrates and soluble oxalates, withsubsequent photosensitization in humans, has shown an 115% increase inabove ground biomass with a 75 ppmv increase in C~ and 3.3°C increase intemperature along a rural-urban transect (Ziska, unpublished data). Overall,it is clear that for both laboratory and field, a number of poisonous specieswill show significant growth increases in response to C~ and temperature.

INDIRECT EFFECTS OF C~rrEMPERA TURE ON PLANTBIOLOGY AND POTENTIAL CONSEQUENCES FORPUBLIC HEALTH

The direct effect of CQitemperature on specific weedy species whosebiology directly impacts human health is straightforward. Less evident are themeans by which plant biology can indirectly impact public well-being.Overall. indirect effects may include COrinduced changes in plant nutrition,plant-derived pharmaceuticals, plants needed for disease vectors, and pesticideuse.

Nutritionlfood quab"iy. With a global population exceeding 6 billion,agriculture relies on grain cereals as their principle source of calories. Twoprinciple cereals, wheat and rice, supply the bulk of the caloric intake for over

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4 billion people. Although wheat and rice have shown a positive growthresponse to increasing C~ yields may actually decline with concurrentincreases in both C~ and temperature due to greater sensitivity of floralsterility to temperature as C~ increases (e.g., Matsui et aI., 1997). Inaddition, increasing ~ may also affect food quality. In general, plants areanticipated to become more starchy, but protein poor, with a subsequentdecline in digestibility as C~ increases (H~. 2<XX». In rice, percentprotein decreased with both increasing air temperature and increasing C~concentration over a two year period in an OTC study conducted for tropicalpaddy rice in the Philippines (Ziska et aI., 1997). For wheat, increasing C~from pre-industrial to current levels resulted in decreased protein in bothSpring and Wmter wheat (Rogers et aI., 1998) in a GH experiment. FACEexperiments with wheat in Maricopa. Arizona showed signifICant effects onflour protein concentration. optimum mixing time for bread dough and breadloaf volume with increasing C~ (550 ppmv} which were exacerbated ifnitrogen was limiting (Kimball et aI.. 2001). Although qualitative changes inrice and wheat have been well documented. jess is known regarding nutritionalimpacts on other crops. Lu et aI. (1986) reported decreased protein content insweet potato (Ipomoea batatas L.) in response to C~. In contrast. Rogers etaI. (1983) reported no response of protein content of maize (Zea mays L.) toCO2 in GH experiments. Recent OTC data for strawberries. which are agood soUrce of natural anti-oxidants, showed a positive increase inantioxidant capacity and flavanoid content in response to increased C~ (300and 600 ppmv above current levels) (Jim Bunce. personal communication).Overall. these data indicate both positive and negative changes in the qualityof common food sources in response to CQitemperature.

MediCJi1e. The use of plants as herbal remedies for human ailmentsdates to the beginning of civili2ation. Modern plant biochemists have longrecognized that plant species synthesize a wide range of secondary metabolites.One of the most compelling explanations for the degree of chemical diversityis that plants have evolved toxicological strategies to protect themselves fromviral diseases. fungal pathogens. and herbivory. Interestingly, a number ofthese secondary metabolites also constitute a principle source for established ,

medicines and potential new drugs (fable 1). Although it is estimated thatthere are roughly 400,000 terrestrial plant species. at present, less than 1 % ofthese species have been examined in-depth for their possible pharmacologicaluse (Pitman and Jorgensen, 2002).

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Table 1 A partial list of plant«rived dru~, their ~mica1 strocture, actionor clinical use and botanical source.

Dna ~Usc Spec"a

CarcfiotoaM:

Rubefacient

Anf¥:botinagic

Ba1"Dary dysentery

Analgcsic, ID~LaxativeAnti-ParkinsonCardiotooEAntihistamineCholin~terase inhibitorTranquilimAntiocalM:a'. anti-tumor

CardiotonicAnti-malarialAnaIgcsicAnti-lumorCerebral stimulantAnti-leukemic agent

AcdykIilOxinAllyl isolhiocyanalcAtropineBrzba:incCodeineDanthron

lrDoJaDi&itoxin~GalanthamincKawainLaI*iIoIOuabainQuinineSaficinTaxolVasiciocVin~tinc

DigilaJ8l1D11a

Brassica nigra

Air. beDadonDa

BetberisvuJ~Papa\U somDiferum

Cassiaspp.M1K:1IDa spp.

DigjIaJD ~EpllcdrlsiDaLycorissquarnigeraPipcrmcthysticum

T ahcbaia spp.

StropiIanthlG gratus

CilM:hooa Jedgeriana

Salixalba

PodopbyDum peitam

V~ minorCatharanthus roseus

How then has rising C~ and/or temperature altered the growth ofmedicinal plant species? A OTC study showed a significant increase in leafphotosynthesis and plant growth in Brassica nigra L. with increasing C~ (300ppmv above ambient), but the effect of C~ on allyl isothiocyanate was notdetermined (Mishra et al., 1999). Similarly, a doubling of atmospheric C~above current ambient resulted in a doubling of dry weight in Tabebwa roses,but the effect ofC~ on levels of Iapachol was unknown (Ziska et al., 1991).

At present, few studies are available which have assessed thequantitative or qualitative CO2 response of secondary metabolites ofpharmacological interest. Most secondary metabolites have been evaluated intenDS of plant-insect interactions with projected C~ levels either stimulating(e.g., Julkunen- Titto et al., 1993; Lincoln, 1993) or decreasing the productionof secondary compounds (e.g., Wllliams et aI., 1994). One exception has been

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wooly foxglove (Digitalis lansta Ehrh.), which produces digoxin, apharDlaceutical glycoside which helps the heart pump blood. In GHexperiments, plant growth and digoxin production were signifICantly increasedat 1000 ppmv relative to ambient C~ conditions (Stuhlfauth and Fock, 1990).

Interestingly, while the relative proportion of digioxin amongglycosides did not change, the relative amoun~ of digitoxigenin, anotherglycoside, was considerably reduced in respook to C~ (Stuhlfauth et aI.,1987). Similarly to digoxin in D. Lansta, projected C~ has also been shownto increase the growth of tropical spider lily (HymenocalJis littoralis (Jacq.), aplant whose bulbs may produce secondary compounds with potential anti-cancer and anti-viral activities (Idso et al., 2000). Although production ofthese pharmaceutical compounds may be positively effected by C~, C~ ortemperature-induced changes in the synthesis of narcotic compounds whoseabuse constitutes a significant health problem in North America and Europe(e.g., Nicotine in tobacco, Tetrahydrocannabinol (rHC) in Cannabisspp.,Cocaine Chlorohydrate in Erytbroxylum ~) havt not been reported in thescientific literature.

Disease Vectors and Plant Biology. Adult mosquitoes do not feed onblood. (although the female requires blood proteins in order to successfullylay eggs); rather, they rely on flower nectar, phloem, and decaying plantmatter for flight energy. Rodents also depend in large part on plant materialas a principle food source (e.g., seed). In general, plant growth and seedproduction are anticipated to increase in response to rising C~ (e.g., Kimball,1993). Potentially, because of COz-induced increases in their food sources,populations of these disease carrying vectors could be stimulated.

Htrbicide- EIlicacy and Usage. Any resource which affects thegrowth of an individual alters its ability to compete with individuals of thesame or different species (patterson and Flint, 1990). Differential inter andintra-specifIC responses to C~ have been observed for the increase inatmospheric carbon dioxide which has already occurred during the 20thcentury (Sage, 1995) and that projected for the end of the 21st century (e.g.,Poorter,I993). If differential responses to increasing C~ occur betweencrops and weeds, will crop losses due to weedy competition increase ordecrease? This will depend in part on photosynthetic pathway, but there are anumber of GH and OTC experiments indicating a greater response of weeds(see Bunce and Ziska, 2000 for a review). Such a response is consistent withthe suggestion ofTrehame (1989) that the physiological plasticity and greater

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genetic diversity of weed species relative to modem crops would provide agreater competitive advantage as atmospheric C~ increases.

But even if C~ stimulates the growth of agronomic weeds (or any ofthe undesirable species mentioned earlier), won' t we still be able to limitwhere and when such species grow? Current availability of chemicalmethodologies allow for cheap, effective cont~ol in agronomic production.Actually, a single herbicide, glyphoSate is so Wide-spread and effective thatmore than half of the current U.S. soybean and a third of the US com crophave been genetically modified to be glyphosate resistant (Gaskell et aI., 1999).

Table 2 Changes in effICaCY detemIined as changes in growth (g dai1 following herbicide applicationfor weeds grown at either current or projrA:ted future levels of carbon dioxide. Plants were followed for a

2-4 ~k. period. Data for Canada thistle is based on top (shoot) growth only. All weeds were sprayed

with manufacturer recommended levels of the herbicide.

Growth

gday-1

Hcrb"K:ideCOz

p.p.m.v.

EnvironmentSpecies(Common name)

o.~ (death)137

36S

mGHGH

glyphosatcglyphosatc

lam~quarters

0.04 (death)

0.18365m

OUou

giyphosate

giyphosatered-root pigweed

-0.05 (death)

1.14glypbosatcgiyphosatc

GHGH

388nl

q1iad:gr3SS

o.ss137

arcOTC

glyphosateglyphosate

Canada thistle 421

771

glufosinaleglufosinale

0.52

1.14arcarc

421

'"I

Canada thistle

This assumes however, that increasing C~ will not effect herbicideefficacy. Yet, there is increasing evidence from GH and OTC studies that CO2decreases chemical efficacy for annual and perennial weeds (Table 2). It canbe argued that COrinduced changes in herbicide tolerance are irrelevant given

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the rate of atmospheric C~ increase (i.e., other herbicides will be developedin the future). However, herbicide use can persist over decades (e.g., 2-4D)coinciding with significant increases in atmospheric CO2 (e.g., 300-372 ppmvsince the introduction of 2-4 D in the 1940s). Given the investment of largecompanies in genetically modified crops and their associated herbicides, itseems more likely that use of current herbicid~ will persist for longer periods.Obviously, chemical control can still be obtaiDed if additional sprayings occur,or if concentration increases, but this could, potentially, alter theenvironmental and subsequent health costs associated with pesticide usage.

In addition to any direct effect of CO2 on efficacy, climatic changeper se can alter abiotic variables such as temperature, wind speed, soilmoisture, and atmospheric humidity. Alteration of such variables can alsoinfluence the efficacy of herbicide applications (reviewed in Muzik, 1976).These same environmental variables can affect crop injury due to herbicideapplication. A recent economic evaluation based on anticipated climatechange suggested that increasing temperature i~~d pesticide cost variancefor com, potatoes and wheat, while decreasing it for soybean (Chen andMcCarl, 2001). Overall, existing data suggest that C~ and potential changesin climate could reduce efficacy with a subsequent increase in sprayingfrequency or herbicide concentration. The overall consequences of such anincrease have not been specifically evaluated with respect to human health.

CONCLUSIONSPlant biology impacts every aspect of our lives. As carbon dioxide

continues to increase, we can anticipate fundamental changes in plant biologyeither from anticipated changes in temperature or, directly from C~ inducedchanges in physiology and growth. From the initial studies described here, itis evident that there are a number of potential means by which plant biologywill directly or indirectly affect human health. This includes changes inallergenic pollen. contact dermatitis, physical damage, and poisons; as well aspotential changes in nutrition, medicines, disease vectors and pesticide usage.

Unfortunately, there is much we still don' t know. If C~ and/ortemperature influence ragweed pollen production, are there qualitative(allergenicity) changes in the pollen? What other allergenic species areaffected? Will the level of urishiol, or other chemicals which cause contactdcnnatitis increase with increasing C~? Can we expect toxicological changes

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in poisonous plants? How will C~induced changes in proteins or anti-ox.idants alter human nutrition? Is the nutrient content of foods increasing ordecreasing in response to C~? Is the quality of medicines derived frombotanical sources improving? What will be the impact of CQitemperature onthe production of narcotic plants? If more food is made available willpopulations of disease carrying mosquitoes Ot; rodents increase? If weedgrowth is improved and herbicide usage increases, will the C~ inducedreductions in efficacy result in increased pesticide use? If so, what are thelong-term implications for human health? None of these questions have beenaddressed in depth. Few, if any field data are available which assess both C~and temperature concurrently in regard to these questions.

The potential consequences of a warmer planet with respect to diseaseoutbreaks, air and water quality, and respiratory disease are well recognizedby the health care community (e.g., Patz and Kovatz, 2002). Less recognizedor evaluated are the direct and indirect conseq~ences of C~ on plant biologyand human health. Yet, the environmental and' he8Jth costs of notunderstanding these consequences may be substantial. It is hoped that thisreview will both emphasize the critical nature of this issue and serve as a guidefor interested medical researchers and policy-makers in assessing the separateimportance of atmospheric CO2 to plant biology and public health.

ACKNOWLEDGMENTS. My thanks to Dennis Gebhard and David Frenzof Surveillance Data Incorporated for their input, and to Dr. Jim Bunce forallowing me to cite his anti-oxidant strawberry data.

REFERENCES

Ainsworth, B.A., PA Davey, C.J. Bemacd1i, O.C. Dennody, B.A. Heaton, D.J. Moore,P .B. Morgan, S.L. Naidu, H.S. Y., Ra, X.G. Zhu, P .S. Curtis and S.P. Long. A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield,Global Change Biology, 8, 695-709 (2002).

Bransford, K.J. and JA. Lai, Global climate change and air pollution: Common originswith common solutions, Journal of the American Medical Association, 287, 2285-2286

(2002).Bunce, JA. and L.R Ziska Weed/Crop Interactions, In: Climate Change and Global CropProductivity, K.R. Reddy and H.F. Hodges (cds.), New York, NY, CABI Publishing. pp.333-352 (2000).

. 2IJI3 WwWR_Retiew. ADr 284

Page 15: World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT ...€¦ · World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop

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Bunce, J.A., Are plant adapted to the current atmospheric concentration of carbon dioxide?International Journal of Plant Science, 162, 1261-1266 (2001).

Bums, W.C., Climate change and human health: The critical policy agenda, Journal of theAmerican Medical Association, 287, 2287 (2002).Capom, S.J.M., A.L. Brooks, M.C. Press and JoA Lee, Effects of long-term exposure toelevated CO2 and increasing nutrient supply on bracken (Pteridium aquilinum), FunctionalEcology, 13, 107-115 (1999). 1.

Chen, C.-C. and B.A McCart. An investigation of the relationship between pesticide usageand climate change, Climate Change, SO, 475-487 (2001).Cifuentes, L., V.H. Borja-Aburto, N. Gouveia, G. Thurston, and D.L. Davis, Hidden healthbenefits of greenhouse gas mitigation, Science, 293, 1257-1259 (200 I ).

Curtis, P .S. and x. Wang, A meta-analysis of elevated CO2 effects on woody plant mass,

form, and physiology, Oecologia, 1.13,299-313 (1998).Epstein, P .R., Is global warming harmful to health?, Scientific American. 283, 50-57

(2000).Garbutt, K. and F.A Bazzaz, The effects of elevated CO2 on plants, III, Flower, Flower,fruit and seed production and abortion, New PhytologiSt;98, 433-446 (1984).

Gaskell, G., M. Bauer, J. Durant and N. Allum, Worlds apart? The reception of geneticallymodified foods in Europe and the U.S., Science, 285,384-387 (1999).Gergen, P.J., P.C. Turkeltaub, M.C. Kovar, The prevalence of allergic skin test reactivity toeight common aeroallergens in the U.S .population: Results from the second NationalHealth and Nutrition Examination survey, Journal of Allergy and Clinical Immunology,

SO, 669-679 (1987).Grimmer, C. and E. Komor, Assimilate export by leaves of Ricinus communis L. Growingunder normal and elevated carbon dioxide concentrations: the same rate during the day, adifferent rate at night, Planta, 209, 275-281 (1999).Gubler, D.J., P. Reiter, K.L. Ebi, W. Yap, R. Nasci and J.A Patz. Climate variability andchange in the United States: Potential impacts on vector- and rodent-borne diseases,Environmental Health Perspective, 2, 223-233 (2001).Hendrey, G.R. and B.A. Kimball, The FACE program, Agricultural Forest Meteorology,

70,3-14 (1994).Hesman, T., Greenhouse gassed: Carbon dioxide spells indigestion for food chains, Science

News, 157,200-202.Hunt, R., D. W. Hand, M.A. Hannah and A.M. Neal. Response to CO2 enrichment in 27herbaceous species, Functional Ecology, 5, 410-421 (1991).

Idso, C.D., S.B. Idso and R.C. Balling Jr., The urban CO2 dome of Phoenix, Arizona,

Physical Geography, 19,95-108 (1998).Idso, C.D., S.B. Idso and R.C. Balling Jr., An intensive two-week study of an urban CO2dome in Phoenix Arizona, USA, Atmospheric Environment, 35, 995-1000 (200 I ).

Idso, C.D., B.A Kimball, G.R Pettit, L.C. Pettit, and R.A. Backhaus, Effects of

0 2003 World R- Rnft. AU richIs resmed. 285

Page 16: World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT ...€¦ · World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop

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atmospheric CO2 enrichment on the growt,h and development of Hymenocallis Linaralis(AmaryIlidJM:cac) and the concentrations ofscvcral antineoplastic and antiviral constituentsof its bulbs, American Journal of Botany, 87, 769-773 (2000).

Julkuncn-Titto, R.. J. Tahvanainen and J. Silvola, Increased CO2 and nutrient statuschanges affect phytomass and the produc tion of plant defensive secondary chemicals inSalix myrsinifolia (SaIisb.), Oecolagio. 95, 49S-498 (1993).

Kimball, B.A., C.F. Morris, P.J. Pincter, Jr., O. W. W,ail, D.J. Hunsaker, F.J. Adamscn. R.L.LaMorte. S. W. Leavitt, T .L. Thompson. A.D. Matthias and T J. Brooks, Elevated CD2,drought and soil8itrogen effects on wheat grain quality, New Phylologist, 150, 29S-303(2001).Kimball, B.A., Effects of increasing atmospheric CO2 on vegetation, Vegetatio,104/105:65- 7S (1993).

Lincoln, D.E., The influence of plant carbon dioxide and nutrient supply on susceptibilityto ins cct herbivores, Vegetatio. 104/105,273-280 (1993).

Long, S.P., Modification of the response of photosynthetic productivity to risingtemperature by atmospheric CO2 concentrations: Has its importance been underestimated?Plant, Cell and Environment, 14,729-739 (1991).

Lu, J. Y., P.K. Biswas, R.D. Pace. Effect of elevated CO2 growth conditions on thenutritive composition and acceptability of baked sweet potatoes, Journal ofF ood Science,51, 3S8-3S9 (1986).

Matsui. T., O.S. Namuco, L.H. Ziska and T .Horie, Effects of high temperature and CO2concentration on spikelct sterility in indica rice, Field CrOP" Research, 51, 213-219(1997)..Mayeux. H.S., H.B. Johnson. H. W. Policy, MJ. Dumcsnil and O.S. Spanci. A controlledenvironment chamber for growing plants across a sub-ambient CO2 gradient, Functional&oIogy, 7, 12S-133 (1993).

McGcehin, M.A. and M. Mirabeli, The potential impacts of climate variability and changeon temperature-related morbidity and mortality in the United States, Environmental HealthPerspective, 1, 18S-189 (2001).

Mishra, R.S., M.Z. Abdin and D.C. Uprcty, Interactive effects of elevated CO2 andmoisture stress on the photosynthesis, water relation and growth of Brassica species,Journal of Agronomy and Crop Science, 182, 223-229 (1999).

Moya, T.B.. L.R. Ziska. C. Weldon. J. Quilang and P. Jones, Micro-climate in open-topchambers: Implications for predicting climate change effects on rice production,TransactiOM of the ASAE, 97, 739-747 (1997).

Muzik. TJ., Herbicides: Physiology, Biochemistry, Ecology, LJ. Audus (ed.), New York,-NY, Academic Press (1976).

Patterson. D.T. and E.P. Flint, Implications of increasing carbon dioxide and climatechange for plant communities and competition in natural and managed ecosystems, In:Impact of carbon dioxide, trace gases, and climate change on global agriculture, ASASpecial Publication. No. 53, Madison. WI, USA. pp. 83-110 (1990).

0 2003 W~R_~. AlricMll8f'ed.2R6

Page 17: World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT ...€¦ · World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop

World Resource Review Vol. 15 No.3

Patterson. D.T.. Weeds in a Changing Climate, Weed Science, 43,685-701 (1995).

Patz, 1.A. and RS. Kovats. Hot spots in climate change and human health. Briti.fh MedicalJournal, 315.1094-098 (2002).Pitman, N. and P. Jorgensen. Estimating the size of the world's threatened flora, Science,298, 989 (2002).

Poorter, H., Interspecific variation in the growth response of plants to an elevated ambientCO2 concentration. Vegetatio, 104/105,77-97 (1993).Resnick. S.D., Poison ivy and poison oak dermatitis, Clinical Dermatology, 4, 208-212

(1986).Rogers, G.S.. P. W. Gras.l.L. Batey, P.l. Milham. L. Payne and J.P. Conroy, The influenceof atmospheric CO2 concentration on the protein. starch and mixing properties of wheatflour, AlLftraiian Journal of Plant Physiology, 25, 387-393 (1998).

Rogers. H.H., G.E. Bingham, J.D. Cure. 1.M. Smith, K.A. Surano, Responses of selectedplant species to elevated carbon dioxide in the field, Journal of Environmt.ntal Quality, 12,569 (1983).

Rose, J.8., P.R Epstein. E.K. Lipp, B.H. Sherman. S.M. Bernard and J.A. Patz, Climatevariability and change in the United States: Potential impacts on water and food bornediseases caused by micro biologic agents, Environmental Health Pt.rspective, 2, 211-221

(2001).Sage, R.F., Was low atmospheric CO2 during the Pleistocene a limiting factor for theorigin of agriculture? Global Change Biology, 1,93-106 (1995).

Sasek, T .S. and B.R Strain, Implications of atmospheric CO2 enrichment and climaticchange for the geographical distribution of to introduced vines in the U.S.A., ClimateChange, 16,31-51 (1990).Scltelling. T.C., Global warming and health effects in the third world, Science, 268. 1264

(1995).Stuhlfauth, T. and H.P. Fock. Effect of whole season CO2 enrichment on the cultivation ofa medicinal plant, Digitalis lanala. Journal of AgrOllOmy and Crop Science, 16, 168-173(1990).Stuhlfauth. T., K. Klug and H.P. Fock, The production of secondary metabolites byDigitalis lanata during CO2 enrichment and water stress, Phytochemistry, 26, 2735-2739

(1987).Treharne, K., The implications of the 'greenhouse effect' for fertilizers and agrochemicals,In: The Greenhouse Effect and UK AgricrJture, R.C. Bennett (ed.). CAS Paper 19,Minjstry of Agriculture. Fisheries and Food, UK. pp. 67-78 (1989).

Trotter, W.R, Is bracken a health hazard? The Lanct.t. 336, 1563-1565 (1990).

Wayne. P., S. Foster, J. Connolly, FA Bazzaz and P.R. Epstein, Production ofallergcnicpollen by ragweed (Ambrosia artemisii/olia L.) is increased in C02-enriched aDnospheres.Annals of Allergy. Asthma and Immunology, SO, 669-679 (2002).

Williams. M. D.E. Lincoln and R.B. Thomas. LobIoUy pine grown under elevated CO2

G - W cxW a- ann. AI r.Mi---287

Page 18: World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT ...€¦ · World Resource Review Vol. 15 No. J CLIMATE CHANGE, PLANT BIOLOGY AND PUBLIC HEAL m Lewis H Ziska Alternate Crop

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affects early instar pine sawfly perfonnancc. Oecologia, 98, 64-71 (1994).

Wodebousc, R.P.. Hay/ever Plants. 2nd Edition, New York, Hamer Publishing (1971).

Ziska. L.H-. K.P. Rogan. AP. Smith. B.G. Drake. Growth and photosynthetic response ofnine tropical plant species with long-tenD exposure to elevated carbon dioxide, Oecologia.86.383-389 (1991).Ziska, L.H., O.S. Namuco, T. Moya and J. Quilang. Growth and yield response of field-grown tropical rice to increasing carbon dioxide and air temperature, Agronomy Journal,89,45-53 (1997).Ziska, L.H., O. Ghannoum. J.T. Baker, J. Conroy, JA Bunce. K. Kobayashi, M. Okada. Aglobal perspective of ground level "ambient" carbon dioxjde for assessing the response ofplants to abnosphcrlc CO2. Global Change Biology. 7. 789-796 (2000).

Ziska. L.R. and FA Caulfield, Rising carbon dioxide and pollen production of commonragweed. a known allergy-inducing species: Implications for public health AustralianJournal of Plant Physiology. 17, 893-898 (2000).

Ziska. L.H., D.E. Gebhard. D.A. Frenz, S. Faulkner. B.D. Singer and J.G. Straka, Cities asharbingers of climate change: Common ragweed. urbanization and public health. Journalof Al/ergy and Clinical Immunology, 111, 290-295 (2003). ..

Ziska. L.H.. (nflucnce of rising atmospheric CO2 since 1900 on early growth andphotosynthetic response of a noxious invasive weed. Canada thistle (Cirsium ~nse).Functional Plant Biology, 19,1387-1392 (2002).

Ziska. L.R., Evaluation of the growth response of six invasive species to past. present andfuture atmospheric carbon dioxide. Journal of Experimental Botany, 54, 395-404 (2003).

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