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Arsenic Hyperaccumulation in the Chinese Brake ( vittata) Deters () Herbivory Author(s): Bala Rathinasabapathi, Murugesan Rangasamy, Jason Froeba, Ronald H. Cherry, Heather J. McAuslane, John L. Capinera, Mrittunjai Srivastava and Lena Q. Ma Source: New Phytologist, Vol. 175, No. 2 (2007), pp. 363-369 Published by: Wiley on behalf of the New Phytologist Trust Stable URL: http://www.jstor.org/stable/4641054 . Accessed: 10/02/2014 12:51

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Arsenic hyperaccumulationin the Chinese brake fern (Pteris vittata) deters grasshopper (Schistocerca americana) herbivory

BalaRathinasabapathi', Murugesan Rangasamy2, Jason Froeba2, Ronald H. Cherry3,Heather J. McAuslane2,John L. Capinera2,Mrittunjai Srivastava4 and LenaQ. Ma4 1HorticulturalSciences Department, University of Florida,Gainesville, FL 32611-0690, USA; 2Entomology and Nematology Department, University of Florida,Gainesville, FL 32611-0620, USA; 3Everglades REC-Belle Glade, Belle Glade, FL 33430-4706, USA; 4Soil and Water Science Department, University of Florida,Gainesville, FL 32611-0290, USA

Summary

Authorfor correspondence: * Brakefern, Pterisvittata, not only toleratesarsenic but also hyperaccumulatesit BalaRathinasabapathi in the frond.The hypothesisthat arsenichyperaccumulation in this ferncould func- Tel:+1 352 3921928 x323 tion as a defense againstinsect herbivory was tested. Fax:+1 352 3925653 * Email:[email protected] Frondsfrom controland arsenic-treatedferns were presentedto nymphsof the grasshopperSchistocerca americana. Feeding damage was recorded by visual Received:24 January2007 observationand quantificationof the freshweight of frondleft uneatenand number Accepted:21 March2007 of fecal pellets producedover a 2-d period.Grasshopper weight was determined beforeand after5 d of feeding. * Grasshoppersconsumed significantly greater amounts of the frondtissue, pro- duced morefecal pelletsand hadincreased body weight on controlplants compared with grasshoppersfed arsenic-treatedferns. Very little or none of the arsenic-treated fernswere consumed indicating feeding deterrence. In a feedingdeterrent experiment with lettuce, sodium arsenite at 1.0 mM deterred grasshoppersfrom feeding whereas0.1 mmdid not. Ina choiceexperiment, preferred to feed on lettucedipped in watercompared with lettucedipped in 1.0 mmsodium arsenite. * Our resultsshow that arsenichyperaccumulation in brakefern is an elemental defense againstgrasshopper herbivory. Keywords: arsenite, arsenic hyperaccumulation,elemental defense, herbivory, grasshopper,pteridophytes, Pteris vittata, heavy metals. New Phytologist (2007) 175: 363-369 ? The Authors(2007). Journalcompilation ? New Phytologist(2007) doi: 10.1111/j.1469-8137.2007.02099.x

As in itsfrond tissue. Introduction Pterisvittata, hyperaccumulated Following this report, there was great interest in using this fern as a Arsenic(As) is widely distributedin natureand is associated cost-effectivegreen technology for the remediationof As- with the oresof metalssuch as copper,lead and gold. It also contaminatedsoil andwater (Tu et al., 2002; Rathinasabapathi enters into the environmentas a result of anthropogenic et al., 2006a). Severalother fernshave also been reportedto activitiessuch as the use of arsenicalsas pesticides,dyes and be capableof As hyperaccumulation,including Pityrogramma chemicalweapons (Oremland & Stolz,2003). Becauseof its calomelanos,Pteris cretica, P longifolia and P umbrosa carcinogenicity,As contaminationof soil and water is an (Visoottivisethetal., 2002; Zhao etal., 2002) but no fern environmentalhealth issue of globalproportions (Smith et al., accumulatessuch high levelsof As as 1Pvittata (up to c. 2% of 1992). Ma et al. (2001) reportedthat the Chinesebrake fern, theirdry weight). Work in severallaboratories is beginningto www.newphytologist.org 363

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unravelthe mechanismsof planttolerance ofAs and its hyper- Total arsenic (AsV and AsIIl) and arsenite (AsII) were accumulationin 1Pvittata (Wang et al. 2002; Poyntonet al., determined by using an atomic absorptionspectrometer 2004; Srivastavaetal, 2005a;Ellis etal, 2006;Rathinasabapathi (Varian240Z Zeeman;Varian, Walnut Creek, CA, USA) et al., 2006b; Singh et al., 2006). (Chen & Ma, 1998). Despitethe potentialutility of As hyperaccumulatingferns and their unusual biochemistry,the reason(s)why certain Grasshoppers evolvedAs hyperaccumulationis not known. Meharg (2002) suggestedthat toleranceto As and hyperaccu- A laboratorycolony of grasshopper(Schistocerca americana mulation could be primitivetraits in earlyland that (Drury))was startedfrom a field collection made at Dade evolvedin As-richenvironments and were retained because of City (FL,USA) in 1991. Nymphswere maintained on a diet a selectiveadvantage (Meharg, 2002). Alternatively,As hyper- of Romainelettuce (Lactuca sativa) in a cageat 30'C and 80% accumulationmight have evolved late in differentfern taxa as relativehumidity. Before their use in the experimentwith fern a convergentadaptation (Meharg, 2002). Althoughan eco- leaves,third instar grasshopper nymphs were starved for 24 h logical advantagefor As hyperaccumulationhas not been and randomlyassigned to treatments.Preliminary observations demonstratedin ferns,Martens & Boyd(1994) proposedthat indicatedthat grasshoppersate fernleaves well when starved. hyperaccumulatedmetals can provide elemental defense against Grasshoppernymphs used in the two lettuce experiments herbivoresand pathogens. Elementaldefenses differ from werenot starved. secondarychemical defenses because their toxic principle is an elementtaken up from the soil ratherthan one derivedfrom Grasshopperfeeding on fern- no-choiceexperiment photosynthate(Boyd, 2004). Studies on nickel (Ni), zinc (Zn) and selenium (Se) hyperaccumulatingplants showed For each replicate,a starved nymph was placed inside a that these hyperaccumulatedelements could have roles in transparentcircular plastic box (17 cm diameterand 7.5 cm plantdefense, either by toxicityor deterrenceor both (Pollard high) closedwith a lid containingtwo wire mesh (1 x 1 mm & Baker,1997; Boyd etal., 2002; Vickermanet al., 2002; meshsize) circular windows of 3 cm diametereach. A layerof Boyd, 2004; Hanson et al., 2004; Boyd & Jhee, 2005; Jhee moistpaper towel was laid on the floorof the box.A glassvial et al., 2005; Noret et al., 2007). with a smallamount of wet cottonholding a frondfrom either Our objectivewas to test the hypothesisthat As hyperaccu- a controlor arsenic-treatedP vittatawas placedin the plastic mulationin PIvittata has a role in defenseagainst her- box. Fronds and grasshopperswere weighed before the bivory.We chose the grasshopperSchistocerca americana for experiment.The experimentwas carriedout at 27-30'C. this study becauseof its wide host range and preliminary Every24 h for 2 d the numberof fecalpellets per insectand observationsindicated that it could eat 1Pvittata fronds. the weight of the tissue left uneatenwere measured.These same grasshopperswere confined for an additional3 d on or treated and theirmass at the end of Materialsand Methods eitheruntreated plants the 5-d periodwas measured. Plants Sodiumarsenite for deterrence- Uniform2-month-old vittataL. with fourto sixfronds grasshopperfeeding 1P plants no-choiceexperiment each were grown hydroponicallyin half-strengthHoagland nutrient solution in a controlled environment room as Romaine lettuce leaf segments (of 50-60 cm2), weighing describedin Tu et al. (2004). Plants treatedwith As were between6 g and 9 g freshweight each,were dippedfor 10 s suppliedwith 0.16 mM(50 mg kg-') sodium arsenatein the in water (control)or sodium arsenitein waterat 0.1 mMor nutrient solution for 1 wk before harvestingof the fronds. 1.0 mM.The treatedlettuce leaf segmentwas placedon a wet Frondswere used immediatelyafter harvest. papertowel and presentedto a starvednymph in a plasticbox as describedabove for 48 h. The amountof leafarea eaten was Arsenicdetermination scoredusing a scaleof 1-10, with 10 representing100% of the surfacearea of the leafsegment consumed. The numberof Samplesof arsenic-treatedand untreated control fern tissue (c. fecalpellets was also recorded 24 and48 h afterthe beginning 0.5 g each,n= 3) werehomogenized three times in 3 x 1 ml of of the experiment.Unlike the experimentswith fernswhere 50% (v :v) methanolin water,using a glassrod. The pooled the weightof the tissueuneaten was recorded, the surfacearea extractfrom each samplewas clarifiedby centrifugationat of lettuce eaten was quantifiedhere becausethis was more 10 000 g for 5 min. The supernatantwas analysedfor total accuratethan the wet weight, which was affected by the arsenic and arsenite.Arsenate and arsenitewere separated moisturebecause of the dippingtreatment. Arsenite in lettuce usingan As speciationcartridge (Metal Soft Center, Highland dippedin 0.1 mMand 1.0 mMsodium arsenite solutions was Park,NJ, USA), which retainsarsenate (Meng et al., 2001). determinedfollowing extraction of the tissuein 50%methanol.

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Sodiumarsenite for grasshopperfeeding deterrence- choice experiment This experimentwas conductedsimilarly to the no-choice experimentexcept that two pieces of lettuce, one dipped in water and anotherdipped in 1.0 sodium arsenite,were mM (a)~ providedin each of the boxes.The amount of tissue eaten . u from both of these treatmentswas estimatedusing the 1-10 .b scale describedearlier. Both the experimentsusing lettuce weredone for 48 h.

Experimentaldesign and statisticalanalyses LN For all experimentsa completely randomizeddesign was followed.Data were analysed using PROC GLM (SAS Institute, (b) ~A~ 1997) and means were separatedusing Student'st-test or Tukey'sStudentized range test when treatmentand control meanswere comparedor Duncan'smultiple range test when morethan two meanswere compared at a significancelevel of a = 0.05.

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i--., I, Results R• • Westco. ... Pterisvittata plants grown in hydroponicsolution took up arsenatethat was suppliedin the medium.Fronds of arsenic- treatedplants had 46.4 ? 3.2 mg kg-' arseniccompared with 2.9 ? 1.6 mg kg-1 in the frondsof controlplants, the values indicatingmean and standarderror of the mean for three replicates.These meanswere significantly different from each other at alpha= 0.05. Of this arsenic 83 ? 0.03% of the arsenicfound in the arsenic-treatedplant was in the form of Fig.1 Feedingdamage on Pterisvittata fronds from either control As(III) whereasonly 65 ? 0.13% was in this form in the (a) or arsenic-treatedplants (b) by grasshopperSchistocerca controlplants (n = 3). Starvedgrasshoppers ate frondsfrom americananymphs. The arrows indicate examples of damageon the control the frond.Photographs were taken 48 h afterreleasing the insectsonto plants (Fig. la), damaging green pinnules. the test fronds. Occasionally,however, the insectsalso ate the rachisportion of the frond (datanot shown).When observedat 24 h and 48 h afterthe start, each insect had consumed,on average, When analysedfor arsenite,lettuce dipped in 0.1 mMand 100 mg tissued-1 and produced10-13 fecalpellets per day 1.0 mM arsenitesolutions contained2.3 ? 0.2 and 46.14 + (Fig.2a,b). By contrast,the insectsfed with arsenic-treated 22 mg kg-1FW (mean? SE, n = 3), respectively.The amount fernsdid not eat the leavesexcept for minor damageto leaf of leaf eatenwas measuredand the fecalpellets were counted marginsin one or two cases(Fig. lb). This feedingdeterrence after24 h and 48 h. Insectsconsumed significantly more of was corroboratedby dataon the amountof leafeaten and the the leaf dipped in water or 0.1 mM arsenite(Fig. 3a) than fecal pellets produced per insect per day; both variables those dipped in 1.0 mM arsenite,which almost completely being significantly lower for feeding on fronds deterredinsect feeding (Fig.3a). This was also corroborated fromarsenic-treated plants than for insectsfeeding on control by the numberof fecalpellets, which were significantly less in plants(Fig. 2a,b). the 1.0 mMarsenite treatment on day 1 andwere less, but not In the longer-durationfeeding study, the insectsfed control significantlyon day2 (Fig.3b). Figure4 illustratesthe feeding frondsfor 5 d increasedin mass by 11.1 ? 2.7 mg (mean+ damageof grasshopperson lettucedipped in water(a), 0.1 mM SE, n = 5). Insectsfed arsenic-treatedfern decreased in weight, arsenite(b) or 1.0 mMarsenite (c) 24 h afterbeginning the losing on average7.7 ? 3.9 mg (mean? SE, n = 5), with no experiment. obvioussigns of food consumptionexcept occasional minor In a choiceexperiment, where grasshoppers were presented damagesto frondmargins. These insectweight changes were with lettuce dipped in water and lettuce dipped in 1.0 mM significantlydifferent when analysedusing Tukey'sStuden- arsenitein the sameplastic box, the grasshopperspreferred to tized rangetest at a = 0.05. consumemore control lettuce than arsenite-treated lettuce, as

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120 4 aa a (a) S 3 100 - 4(a) 0 b 2- E 80- , c c a) E 1.

"0 0 0.1 mM 1.0 mM 0 0.1 mM 1.0 mM U- As(Ill) As(Ill) As(IIl) As(lll) As(Ill) As(llI)

20- 6a30 o 25 a - 2a (b) 0 C, 20 a Con. As Con. As (- 6=S5 015- 16 14 0 0.1 1.0 0 0.1 1.0 - - (b) As(Ill) mM mM As(ll) mM mM 12- As(ll) As(IllI) As(Ill) As(Ill) 10- Fig.3 Feedingof grasshopper(Schistocerca americana) on lettuce - (Lactucasativa) dipped in 0.1 mmand 1.0 arsenite(As) and water 8- mM control.(a) Amountof leaf eaten per day perinsect (scored using a 0 6- relativescale of 1-10, as describedin the Materialsand Methods and the meannumber of fecal 6 * section) (b) pelletsproduced per day C 4- per insect.Observations are for 24 h (tintedbars) and 48 h (closed 2- bars)from the beginningof the experiment.For each day,means shown with differentletters indicate significant difference by 0 Duncan'smultiple range test at alpha= 0.05 with n = 5. Con. As Con. As Fig.2 Feedingdeterrence of grasshopper(Schistocerca americana) by arsenic-hyperaccumulatingfern (Pterisvittata) fronds. (a) Fresh Pteris vittata ferns growing in uncontaminated sites (FW)of frondeaten insectand (b) the mean weight perday per (0.44-7.56 mg kg1) accumulated between 11.8 mg kg-1 and numberof fecal insectwhen fronds from pelletsproduced per day per 64 in its fronds(Ma et al., 2001). The concentration control(Con.) and arsenic-treated(As) were to mg kg-1 plants supplied found the frond that thereis for Schistocercaamericana. Observations are for 24 h (tintedbars) ranges in indicates potential and 48 h (closedbars) from the beginningof the experiment. this arsenicconcentration to act as a herbivoredeterrence. Barsdenoted by asteriskswere significantdifferent by the mean Data on tissue consumedand productionof fecal pellets separationtest at (x= 0.05, n = 5 for each treatment. both indicatedthat arsenic-treatedfern fronds were not con- sumedby S. americana(Figs 1 and 2) in no-choicetests. Like many generalistherbivores, the grasshoppersmade many test shown by the amount of leaf eaten between the two treat- bites beforerejecting the arsenic-accumulatedfronds (Pollard ments. Insects consumed a significantly greater area of the & Baker,1997; Behmeret al., 2005), suggestingthat olfac- controlleaf than the treatedleaf (Fig. 5). tion alonewas not sufficientto detectthe arseniteor arsenite- inducedphytochemicals if any. Pteris nativeto eastern is distributed Discussion vittata, , widely throughoutthe tropicsand subtropicsincluding South , Our resultsshow that As accumulatedin P vittatafronds at Madagascar,New Guinea, and partsof North and the concentrationaveraging 46 mg kg-' was sufficient to SouthAmericas (Jones, 1987). Schistocercaamericana is known deter grasshoppersfrom feeding. While this could be the to be distributedthroughout the easternUSA to the Great concentrationconsumed by the insect,the exactconcentration Plainsand south to Mexico (Thomas, 1991). However,it is of As is not known because of limited knowledge of highlyunlikely that S. americanais a naturalpest of ? vittata. subcellularand tissue-specificaccumulation of arsenitein the While our experimentssuggest that insectdamage could pos- fern.The X-rayabsorption spectroscopy and imagingstudies siblyhave been a selectionpressure for the evolutionof arsenic indicated that arsenicwas found in the upper and lower hyperaccumulationin ferns,it is not knownwhether arsenic epidermal layers of the frond, probably in the vacuoles hyperaccumulationtrait has that advantageunder natural (Lombiet al., 2002; Pickeringet al., 2006). Suchdistribution field conditions.Gould & Vrba(1982) coined the term exa- would be ideal for arsenicto play a role in insect feeding ptationto denoteadaptations that now enhancefitness of an deterrence. organismbut were not built by naturalselection for their

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7.0 (a) . 6.0- 5.0 ) 4.0 I r 3.0 i S 2.0

0.0 0 As(Ill) 1 mM 0 As(Ill) 1 mM As(Ill) As(Ill) Fig.5 Preferenceof grasshopper(Schistocerca americana) nymphs for lettuce(Lactuca sativa) dipped with 1 mmarsenite and controlin a choicetest. Amountof leaf eaten was scoredbased on a relative scaleof 1-10 as describedin the Materialsand Methodssection. Observationsare for 24 h (tintedbars) and 48 h (closedbars) from (b) the beginningof the experiment.Bars followed by asterisksindicate significantdifference between the controland the treatmentmeans by Student'st-test at a = 0.05 withn = 5 for eachtreatment/control.

is a byproductof otherphysiological processes in metalhyper- I accumulatingplants (Boyd & Martens,1998). (c In a studydone in CostaRica, Rowell et al. (1983) reported l that forestgrasshoppers Hylopedetes nigrithorax and Homeo- mastaxdentata ate ferns and preferredto eat certainspecies over others.In that study,a numberof chemicalparameters such as total phenolics,astringency and fibercontent of the I' ferns did not correlateto the grasshoppers'choice (Rowell et al., 1983). Heavy metal hyperaccumulationwas not con- (c) ,.? . ~. , ., sideredas a potentialdeterrent in that study.Our resultshere are consistentwith As hyperaccumulationhaving a role in insectdeterrence. It is possiblethat arseniteitself acts as a deterrent.Alterna- tively, secondaryproducts induced in responseto arsenite treatmentmight be the feeding deterrent.To distinguish between these possibilities,we tested arsenitesolutions for feedingdeterrence. Our resultsshowed that sodium arsenite actedas a deterrentat 1 3 and In 7, ' directly feeding mM(Figs 4). a choiceexperiment, grasshoppers preferred lettuce dipped in waterover lettuce dipped in 1 mMarsenite (Fig. 5). The con- centrationof arsenitein lettucedipped in 1 mMsodium arsen- Fig.4 Feedingdeterrence of grasshopper(Schistocerca americana) ite was comparablewith that found in arsenic-treatedfern nymphspresented with lettuce (Lactuca sativa) dipped into (a) water, fronds.Our resultsare consistent with the hypothesisthat the 0.1 mmor 1.0 sodiumarsenite. (b) (c) mM The arrowsindicate grasshopperssense arsenite test bitesand arseniteitself of on the frond. were taken24 h during examples damage Photographs can act as a deterrent.However, we did not determine if afterreleasing the insectsonto the test leaf. As-inducedP vittatanatural products also play a rolein insect feedingdeterrence. Plant resistancedue to allelochemicalsand heavy metals currentrole. The As hyperaccumulationtrait could be an exa- other than As has been investigatedin great detail (Boyd, ptation(Gould & Vrba,1982) as a characterevolved for other 2004; Hanson et al., 2004; Jhee et al., 2005). However,our currentlyunknown uses but later 'coopted'for their role in study is the firstexample where arsenite accumulated in the herbivoredeterrence. This idea is suggestedin 'inadvertent plant tissue is shown to have a role in feeding deterrence uptake hypothesis' of metal hyperaccumulationwherein againsta generalistherbivore. This is significantin designing metal hyperaccumulationhas no selectivevalue but the trait novelinsect deterrents because if arseniteis directlysensed by

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Tu C, Ma LQ, BondadaB. 2002. Arsenicaccumulation in the VisoottivisethP, FrancesconiK, SridokchanW. 2002. The potential hyperaccumulator.Chinese brake and its utilizationpotential for of Thai indigenousplant species for the phytoremediationof .Journal ofEnvironmental Quality 31: 1671-1675. arseniccontaminated land. EnvironmentalPollution 118: Tu S, Ma LQ, MacDonaldGE, BondadaB. 2004. Effectsof arsenicspecies 453-461. and phosphoruson arsenicabsorption, arsenate reduction and thiol WangJ, Zhao F, MehargAA, RaabA, FeldmannJ, McGrathSP. 2002. formation.Environmental and ExperimentalBotany 51: 121-131. Mechanismsof arsenichyperaccumulation in Pterisvittata. Uptake VickermanDB, YoungJK, TrumbleJT. 2002. Effectof selenium-treated kinetics,interactions with phosphate,and arsenicspeciation. Plant alfalfaon development,survival, feeding, and ovipositionpreferences of Physiology130: 1-10. Spodopteraexigua (Lepidoptera: Noctuidae). Environmental Entomology Zhao FJ, Dunham SJ, McGrathSP. 2002. Arsenichyperaccumulation by 31: 953-959. differentfern species. New Phytologist156: 27-31.

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? The Authors(2007). Journalcompilation ? New Phytologist(2007) www.newphytologist.org New Phytologist(2007) 175: 363-369

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