Biochar amendment to soils impairs developmental and reproductive performances of a major rice pest Nilaparvata lugens (Homopera: Delphacidae)

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1 J. Appl. Entomol. ORIGINAL CONTRIBUTION Biochr mendment to soils impirs developmentl nd reproductive performnces of mjor rice pest Nilprvt lugens (Homoper: Delphcide) X. Hou 1, L. Meng 1,L.Li 2, G. Pn 2 &B.Li 1 1 College of Plnt Protection, Key Lortory of Integrted Pest Mngement in Crops in Estern Chin, Ministry of Agriculture, Nnjing Agriculturl University, Nnjing, Chin 2 College of Nturl Resources nd Environments, Nnjing Agriculturl University, Nnjing, Chin Keywords iochr ppliction, chrcol, herivorous insects, integrted pest mngement, life history, rice Correspondence Boping Li (corresponding uthor), College of Plnt Protection, Nnjing Agriculturl University, No. 1, Weigng Rod, Nnjing 2195, Chin. E-mil: lp@nju.edu.cn Received: Decemer 5, 214; ccepted: Ferury 1, 215. doi: /jen Astrct Biochr mendments to soils hd roused much interest for hving potentil for greenhouse gs mitigtion, soil improvement nd incresed crop productivity. However, little ttention hd een focused on the influence of iochr mendments on herivorous insect pests. This study investigted whether iochr mendment ffected developmentl nd reproductive performnces of the rice rown plnthopper (Nilprvt lugens) feeding on rice plnts. The iochr from the pyrolysis of whet strw ws used for tretments of soils (from fllow rice field), nd the treted soils were pplied to grow rice seedlings in smll vils, in which N. lugens life history ws oserved. The nymphl development time ws delyed nd nymph-to-dult survivl decresed with high level of 2 g/kg iochr ppliction. Herivore lifetime fecundity decresed with incresing mounts of iochr, from 256 eggs under the control down to 69 eggs under the high level (2 g/kg) of iochr ppliction. Egg-htching rte significntly decresed t the highest iochr level (2 g/kg), compred to the other lower iochr levels. Our results suggest tht iochr mendment to rice fields my hve negtive impcts on the rice rown plnthoppers when pplied t level of 2 g/kg of soil. Introduction Biochr is cron-rich coproduct resulting from pyrolysing iomss. Biochr ppliction to soils hs creted worldwide ttention during the lst few yers ecuse of its multiple potentil roles (Lehmnn nd Joseph 29; Sohi et l. 21; Woolf et l. 21). Recent met-nlyses show tht iochr mendments to soils not only improve soil structure (texture, ph nd density), intensify soil retention of nutrients nd wter, dd nutrients to soils nd promote mycorrhizl competence, ut lso increse oveground productivity, crop yield, soil microil iomss nd rhizoi nodultion (Atkinson et l. 21; Jeffery et l. 211; Powlson et l. 211; Biedermn nd Hrpole 213; Liu et l. 213), lthough the exct mechnisms for these improvements remin uncertin (Crne-Droesch et l. 213). Bsed on the chemicl, physicl nd microil improvements reported for iochr-mended soil nd incresing plnt uptke of key nutrients in response to iochr ppliction, it could e nticipted tht iochr ppliction would lso hve n indirect impct on pthogen nd pest orgnisms on the plnts in iochr-mended soils. However, scnt ttention hs een devoted to impcts of iochr ppliction on plnt pthogens nd herivorous insects. A few studies demonstrted tht iochr pplictions to soils reduced infection of crop plnts with soilorne pthogens, such s Fusrium (Mtsur et l. 22; Elmer nd Pigntello 211) nd cteri Rlstoni solncerum (Nerome et l. 25), nd nother study y Eld et l. (21) reports decresed infection of pepper nd tomto with folir fungl pthogens such s Botrytis cinere, s well s reduced dmge to pepper plnts y the rod mite pest (Polyphgotrsonemus ltus Bnks). 215 Blckwell Verlg GmH 1

2 Biochr mendment impirs rice pest life history X. Hou et l. But there hve een virtully no studies focusing specificlly on herivorous insect pests s ffected y iochr ppliction to soils. In this study, we conducted lortory experiments to specificlly exmine the impct of iochr mendment to soils on the life-history trits of the rice rown plnthopper (Nilprvt lugens). N. lugens is migrtory species in Asi nd persistent pest of rice (Sogw 1982; Cheng et l. 23). Its phloem-sucking ehviour vries depending on chemicls in rice plnts (Sogw 1982; Lu et l. 25). Chemicl contents in rice plnts cn chnge with iochr pplictions (Asi et l. 29; Zhng et l. 21; Liu et l. 214). We thus hypothesized tht N. lugens developmentl nd reproductive performnces my e ffected y iochr ppliction to soils. Mterils nd Methods Biochr nd soil The iochr used in the experiment ws commercil chrcol product otined from the pyrolysis of whet strw (Snli New Energy Compny, Shngqiu, Chin). Air-dried whet strw ws pyrolysed under no-oxygen conditions using ptented pyrolysis equipment (Chin ptent No. ZL ) t 4 C (PH = 9.9.5, percentge of totl N =.8%, totl sh content = 2.8%, C = 1%, Mg =.6%, Fe =.4%, nd K = 2.6%). The sndy lom soil, loclly known s red-rown soil, ws collected from fllow rice field in the estern suur of Nnjing, Chin (32 3 N, E). The soil contined.9% nitrogen nd 1.17% orgnic cron with ph of 7.3. The ph vlues of the soils nd iochr were mesured following the ntionl stndrds (Liu 1996). To confirm the tretment effects, we nlysed the soils in ll experiments for totl nitrogen, orgnic cron nd cron nitrogen rtios using C N nlyzer (Vrio EL, Elementr GmH, Hnu, Germny). Five replictes from ech treted soil were nlysed fter the smple ws dried nturlly. Biochr-mended soils were prepred y thoroughly mixing the soil with iochr y weight, t levels: (control), 1, 5 nd 2 g/kg, respectively. Rice plnt nd insect The rice vriety K You 818, supplied y the Shenzhou Seed Compny of Nnjing Agriculturl University, ws used in the experiments. Rice seeds were sown in plstic pots (15 cm in dimeter nd 12 cm in height; out 1 seeds per pot), ech of which ws filled with 1 kg of treted soil nd mintined in growth chmers (26 1 C, r.h. 6 7% nd 16/8 h light (12 LX)/drk). The plnts were wtered every 2 dys to e supplied with enough wter. After 3 dys, plnts (25 cm tll) were used in the experiments. To confirm the effect of iochr mendment tretments on the plnts, plnt smples from five pots (replictes) were tken for nlysis of totl nitrogen, orgnic cron nd cron/nitrogen rtio using C N nlyzer (Vrio EL, Elementr GmH). To prepre smples for nlyses the oveground potted plnts were cut t the se nd dried in n oven t 12 C for 2 h, followed y 85 C for 36 h. The N. lugens popultion used in this study ws otined from the Insect Toxicology Lortory (Nnjing Agriculturl University), where its collection hs een mintined for >8 genertions. Test insects were mintined in n incutor (26 1 C, r.h. 6 7% nd 16/8 h light/drk) on rice plnts for one genertion (25 3 dys) efore the tril. Newly emerged N. lugens nymphs (within 24 h) were used in ll tretments. Insect developmentl nd reproductive performnces Rice seedlings were individully trnsplnted into glss vils (3 cm in dimeter nd 18 cm in height), which contined 2 g of iochr-treted soils. A group of 1 neonte first instr nymphs ws relesed into the vil, which ws covered with guze net to prevent the insects from escping. The rice seedlings were replced every 3 dys to keep food plnts in good condition. The nymphs were exmined dily for development progress nd survivl until dult emergence. The sex of emerging dults ws recorded. Ech tretment ws replicted 1 times. To mesure the fecundity of N. lugens, we introduced emerging dults in pirs ( mle nd femle) into individul glss vils with growing rice seedlings. These plnts were replced every other dy nd exmined under stereo microscope for eggs lid, until the deth of femles. To mesure egg-htching rte, we trnsferred the individul seedlings with eggs into glss vils nd exmined dily for htching nymphs, until no nymphs emerged in three successive dys. The trils were performed in growth chmers (26 1 C, r.h. 6 7% nd 16/8 h light/drk). Ech tretment ws replicted 3 times. Dt nlysis One-wy ANOVA ws used to detect differences etween iochr tretments in soil properties nd Blckwell Verlg GmH

3 X. Hou et l. Biochr mendment impirs rice pest life history rice plnt nutrients. Proportion dt were rcsinetrnsformed to mke the distriution confirm to normlity nd homoscedsticity ssumptions. Nymphl time ws verged over individuls in vil nd then nlysed with ANOVA fter eing log-trnsformed. When significnt differences were detected, post hoc Tukey HSD test ws pplied to detect pirwise differences etween iochr tretments. Logistic regression ws used to nlyse nymph-to-dult survivl, sex rtio nd egg-htching rte, nd Poisson regression ws pplied to nlyse N. lugens fecundity. When significnt effect of iochr tretments ws detected using the likelihood rtio test sed on the chnge in devince etween models, Tukey s ll pirwise comprisons were performed using the multcomp pckge in R (Bretz et l. 21). Dt nlyses were performed with R sttisticl softwre (R Core Tem 214). Results Nutrients in rice plnts Soil ph, nitrogen nd cron content incresed with incresing mounts of iochr mendments. However, rice plnt nitrogen nd cron content decresed with incresing mounts of iochr mendments (tle 1). Developmentl performnce of N. lugens Biochr mendments to soils hd significnt effects on nymphl development time (ANOVA: F 3, 36 = 26., P <.1), which ws longer t the highest iochr level (2 g/kg) thn t the lower levels nd the control, without significnt differences etween the lter tretment levels (fig. 1). The iochr mendments significntly ffected nymph-to-dult survivl (logistic model, log-likelihood rtio test: v 2 = 65.13, P <.1), which decresed under the high level (2 g/kg) of iochr ppliction compred to the lower levels of ppliction (fig. 2). Biochr mendments did not influence the sex rtio (logistic model, v 2 = 1.98, P =.58), which vried round 5%. Reproductive performnce of N. lugens Biochr mendments to soils significntly ffected fecundity (Poisson regression, log-likelihood rtio test: v 2 = 33.78, P <.1), which decresed sustntilly with incresing mounts of iochr ppliction, from eggs t the control down to eggs t the highest iochr level (2 g/kg) (fig. 3). Biochr mendments to soils significntly ffected the egghtching rte (logistic regression, v 2 = 21.43, P <.1), which ws lower t the highest iochr level (2 g/kg) thn t the lower iochr levels (fig. 4). Discussion Our results show tht 2 g/kg of iochr ppliction to soils hd negtive impcts on N. lugens, incresing its nymph development time, decresing its nymph survivl to dult emergence, nd reducing its life time fecundity nd egg-htching rte. The negtive effect on the developmentl nd reproductive performnces of N. lugens quite likely results from chnges in nutrients in rice plnts following the iochr mendment (tle 1). These nutrient chnges my inhiit Tle 1 Men (SE) content of min nutrients in iochr-mended soils nd ssocited rice seedlings in the experiments Biochr ppliction (g/kg) ph Per cent N Per cent orgnic C C/N rtio Soil c c c c d d Rice plnt c c d c Different lowercse letters indicte significnt differences (P <.5) sed on Tukey s HSD post hoc test for soils nd rice plnts, seprtely. Proportion dt were rcsine-trnsformed efore the nlysis. 215 Blckwell Verlg GmH 3

4 Biochr mendment impirs rice pest life history X. Hou et l. Nymph durtion (d) Biochr content (g/kg) Fig. 1 Men (SE) nymph development time of Nilprvt lugens under different iochr tretments. Different lowercse letters indicte significnt differences (P <.5) sed on Tukey s HSD post hoc test for different iochr tretments. Fecundity (eggs lid) Biochr content (g/kg) Fig. 3 Men (SE) lifetime fecundity of Nilprvt lugens under different iochr tretments. Different lowercse letters indicte significnt differences (P <.5) sed on Tukey s HSD post hoc test for different iochr tretments. 1 c Nymph-to-dult survivl (%) Biochr content (g/kg) Egg-htching rte (%) Biochr content (g/kg) Fig. 4 Men (SE) egg-htching rte of Nilprvt lugens under different iochr tretments. Different lowercse letters indicte significnt differences (P <.5) sed on Tukey s HSD post hoc test for different iochr tretments. Fig. 2 Men (SE) nymph-to-dult survivl rte of Nilprvt lugens under different iochr tretments. Different lowercse letters indicte significnt differences (P <.5) sed on Tukey s HSD post hoc test for different iochr tretments. N. lugens feeding ehviour. Multiple studies show tht while some key nutrients increse in iovilility nd plnt uptke in response to chrcol ppliction, others decrese (Lehmnn et l. 23; DeLuc et l. 29; Atkinson et l. 21; Mjor et l. 21, ). In our study, we found decresing nitrogen content in rice plnts with incresing mounts of iochr mendments. The similr finding s ours is lso reported in microcosm experiments in rice fields (Xie et l. 213). Another study showed incresing soil silicon vilility nd rice plnt uptke following iochr mendment to cid nd slightly cid rice soils (Liu et l. 214). Nitrogen nd silicon in rice plnts re criticl fctors for N. lugens feeding ehviour while the former is n ctive stylet-proing nd phloem-sucking stimulus (Sogw 197, 1982; Cheng 1971; Lu et l. 25), the lter strong sucking inhiitor (Yoshihr et l. 198; Sogw 1982). We therefore ssume tht decresed N nd incresed Si in rice plnts following iochr ppliction my impede N. lugens feeding ehviour, leding to poor developmentl nd reproductive performnces. Further studies re required to investigte how chnges in plnt secondry metolites in rice plnts, especilly those importnt for sucking herivores, re ssocited with feeding ehviour of N. lugens on the plnts following iochr ppliction Blckwell Verlg GmH

5 X. Hou et l. Biochr mendment impirs rice pest life history Induced plnt defences following iochr mendment is nother likely explntion for delyed development nd reduced reproductive chrcteristics of N. lugens in response to high levels of iochr mendments. Induced defences hve een found to e widespred in plnts (Krn nd Bldwin 1997; Johnson 211), nd severl iochemicl mechnisms nd signlling pthwys hve een confirmed for the induction process (Wlling 2). A study pplying wood nd greenhouse wste iochr to the potting medium of strwerry demonstrted suppressed diseses cused y three fungi with different infection strtegies nd oserved primed stte of defence-relted gene expression upon infection y two of the fungi (Hrel et l. 212). This study suggests tht iochr my stimulte rnge of generl defence pthwys in plnts. However, n lterntive explntion for plnt defence responses to iochr ppliction ws proposed y Viger et l. (214). Using the model plnt Aridopsis nd the crop plnt lettuce (Lctuc stiv L.), these uthors found incresed plnt growth in oth species following iochr ppliction, ut oserved downregultion of lrge suite of plnt defence genes. Such genes re criticl for plnt protection ginst insect nd pthogen ttck, s well s defence ginst stresses including drought. These studies suggest tht plnt defence responses to pest orgnisms following iochr mendments my vry widely depending upon multiple vriles in complex wys. For exmple, iochrs cn vry gretly in sored voltile orgnic compounds (VOCs) nd their chemicl dissimilrity could ply role in the wide vriety of plnt nd soil microil responses to iochr soil mendment (Spoks et l. 211). While some VOCs on iochr my inhiit plnt pthogens (Grer et l. 21), others cn increse soil iologicl community composition nd ctivity (Lehmnn et l. 211). Multiple studies show tht iochrs hve positive effects on the undnce of mycorrhizl fungi (Wrnock et l. 27). In fct, mycorrhizl sttus of the host plnt cn influence insect herivore performnce, ut the mgnitude nd direction of the effect depend upon the feeding mode nd diet redth of the insect nd the identity of fungi (Gehring nd Whithm 1994; Korichev et l. 29). Furthermore, induced defence responses in plnts often vries with the herivore species, the plnt species nd genotype within species, the environmentl conditions under which plnts re grown, the numer of herivore species ttcking the plnt nd feeding hits of the herivorous species (Wlling 2; Hre 22; Wu nd Bldwin 21; Bllre et l. 213). Future studies re required to chrcterize the iochemicl mechnisms nd signlling pthwys involved in induced plnt resistnce to herivore pests in response to iochr pplictions. Our study demonstrtes tht 2 g/kg of iochr mendment to rice soils cn hve negtive impcts on the development nd reproduction of the phloemsucking rice rown plnthopper (N. lugens). This negtive impct on plnt-feeding insect species my provide potentil dditionl enefit to iochr pplictions. Pddy field trils re required to evlute how the performnces oserved in this lortory study re displyed in the field, y exmining how iochr pplictions ffect N. lugens popultion nd its dmge to rice yields. Acknowledgements We thnk John Orycki for his comments on the mnuscript nd Yihn Xi, Shiwei Guo, Yongli Wen, Jili Hou nd Jing Nie for their help in the experiments. Moreover, we thnk two unknown reviewers for very vlule comments nd improvement of the mnuscript. The reserch ws funded y the Specil Fund for Agro-scientific Reserch in the Pulic Interest (2933 nd 21132). References Asi H, Benjmin K, Smson B, 29. Biochr mendment techniques for uplnd rice production in Northern Los 1. Soil physicl properties, lef SPAD nd grin yield. Field Crop Res, 111, Atkinson CJ, Fitzgerld JD, Hipps NA, 21. Potentil mechnisms for chieving griculturl enefits from iochr ppliction to temperte soils: review. Plnt Soil, 337, Bllre CL, Gross KL, Monson RK, 213. Zooming in on plnt interctions. Oecologi, 171, Biedermn LA, Hrpole WS, 213. Biochr nd its effects on plnt productivity nd nutrient cycling: metnlysis. GCB Bioenergy, 5, Bretz F, Hothorn T, Westfll P, 21. Multiple comprisons using R. Chpmn & Hll/CRC, Boc Rton, FL. Cheng CH, Effect of nitrogen ppliction on the susceptiility in rice to rown plnthopper ttck. Tiwn Agric Res J, 2, 21 3 (In Chinese, with English summry). Cheng XN, Wu JC, M F, 23. Reserch nd prevention of rown plnthopper. Chin Agriculture Pulishing Inc, Beijing. Crne-Droesch A, Aiven S, Jeffery S, Torn MS, 213. Heterogeneous glol crop yield response to iochr: met-regression nlysis. Environ Res Lett, 8, Blckwell Verlg GmH 5

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