Arthropod-Plnt Interctions DOI 1.17/s11829-11-9125-8 ORIGINAL PAPER The effect of nitrogen dditions on rcken fern nd its insect herivores t sites with high nd low tmospheric pollution Michele Etough Jones Mrk E. Fenn Timothy D. Pine Received: 4 August 21 / Accepted: 3 Jnury 211 Ó The Author(s) 211. This rticle is pulished with open ccess t Springerlink.com Astrct The impct of tmospheric pollution, including nitrogen deposition, on rcken fern herivores hs never een studied. Brcken fern is glolly distriuted nd hs high potentil to ccumulte nitrogen in plnt tissue. We exmined the response of rcken fern nd its herivores to N fertiliztion t high nd low pollution site in forests downwind of Los Angeles, Cliforni. Folige from the high pollution site hd higher totl N nd nitrte thn the low pollution site. Brcken fern iomss, folir N nd herivore undnce were ll ffected y fertiliztion tretments. Biomss nd herivore responses were gretest during yer of high precipittion. N dditions t the low pollution site were primrily ssocited with decresed fern iomss, nd with trnsient impcts on herivore undnce. N dditions significntly ffected rcken fern nd its herivores t the high pollution site where folir N nd nitrte decresed in response to N ddition tretments, while iomss nd herivore undnce incresed. High tmospheric deposition nd fertiliztion were oth ssocited with incresed herivore richness. Herivore undnce ws most impcted y fertiliztion during the erly expnsion of fern fronds. The most undnt chewing herivore, swfly, ws positively ssocited with plnt nitrogen t the low pollution site, ut negtively ssocited Hndling Editor: Joseph Dickens. M. Etough Jones (&) T. D. Pine Deprtment of Entomology, University of Cliforni, Riverside, CA 92521, USA e-mil: michele.etough@ucr.edu M. E. Fenn Forest Service, Pcific Southwest Reserch Sttion, Forest Fire Lortory, USDA, 4955 Cnyon Crest Drive, Riverside, CA 9257, USA with plnt nitrogen t the high pollution site, where concentrtions of oth totl N nd nitrte were high. While overll growth nd herivore impcts in this xeric loction were limited, the vrile response we oserved ssocited with rinfll, my indicte impcts could e lrger in more mesic environments. Keywords Nitrogen deposition Pteridium quilinum Brcken fern Insect herivore Sn Bernrdino Mountins Introduction Brcken fern (Pteridium quilinum vr. puescens Underw.) is widely distriuted in temperte zones throughout the world. Becuse of its invsive nture, it my ecome serious weed prolem in response to environmentl chnges due to pollution nd climte chnge (Gordon et l. 1999; Werkmn nd Cllghn 22; Whitehed et l. 1997). The ojective of our reserch ws to exmine the response of rcken fern nd its insect herivores to tmospheric pollution in southern Cliforni. Atmospheric pollutnts, prticulrly nitrogenous compounds nd ozone re trnsported inlnd from urn res of the Los Angeles sin, long the western slopes of the Sn Bernrdino Mountins y previling wether ptterns (Miller 1992). In forests of estern North Americ nd Europe, N sturtion hs een ssocited with forest decline (Aer et l. 1995). In these mesic ecosystems, tmospheric deposition effects re elieved to e primrily driven y se ction depletion, soil cidifiction nd ssocited impcts (Fenn et l. 26). In contrst, in Cliforni soils re not s highly leched ecuse of the Mediterrnen climte nd se ction supplies re reltively high. Only
M. Etough Jones et l. in the most polluted sites hs severe soil cidifiction een oserved. However, even in these instnces se ction levels re still severl fold higher thn in polluted forests of Europe nd estern North Americ (Fenn et l. 26). Becuse of the higher uffering cpcity nd se sturtion of mixed conifer forests in Cliforni, nutrient effects of N deposition re of much greter concern thn cidifiction effects (Fenn et l. 21; Tkemoto et l. 21). Brcken fern hs high potentil to ccumulte nitrogen (N) in plnt tissue compred to other plnts in the sme hitt. Gerloff et l. (1966) found rcken fern hd higher concentrtions of N compred to other plnts growing in northern dry forests. Stms nd Schipholt (199) found higher concentrtions of nitrte in rcken folige compred to other plnts in forests impcted y tmospheric N pollution. In the Sn Bernrdino nd Sierr Nevd Mountins, totl folir N nd nitrte were higher in rcken fern from polluted sites compred to less polluted sites (Fenn et l. 1996, 23). Folir nitrte of rcken fern ws lso much higher thn for ok nd pine in the Sn Bernrdino Mountins. (Fenn et l. 1996). Nitrogen enrichment through tmospheric deposition hs een shown to ffect herivore performnce on vriety of plnts (Throop nd Lerdu 24). When rcken fern herivores from severl sites long the pollution grdient in the Sn Bernrdino Mountins were exmined, herivore communities t high pollution sites were chrcterized y higher undnce of chewing insects (Etough Jones nd Pine 26). The ojective of this study ws to further exmine the role of incresed N deposition on rcken fern nd its herivore communities. We simulted incresed N deposition through N dditions t sites in the Sn Bernrdino Mountins with different tmospheric pollution inputs. This is the first study to our knowledge to exmine the effects of N mendments on herivores of rcken fern. We expected tht fertiliztion tretments would increse folir nitrogen in rcken fern t oth the high nd low pollution sites. Incresed folir nitrogen ws expected to ffect rcken fern herivores. If differences in the undnce of chewing herivores previously oserved t these sites were ssocited with tmospheric nitrogen inputs, fertiliztion tretments should increse the undnce of chewing herivores, prticulrly t the low pollution site. Methods Sites nd nitrogen ddition tretments Brcken fern plots were estlished in the fll of 1997 t two loctions in the mixed conifer zone of the Sn Bernrdino Mountins (Sn Bernrdino County, CA) long west/est grdient for N deposition nd ozone. The western-most site t Cmp Pivik (HIGH; 34 14 5 N, 117 19 25 W) hs een impcted y high levels of N deposition while the more estern site t Brton Flts (LOW; 34 1 1 N, 116 54 25 W) hs received lower input from tmospheric N (Tle 1). The dominnt overstory species t the high pollution site re ponderos pine (Pinus ponderos Lws.), Cliforni lck ok (Quercus kellogii New.) nd incense cedr (Clocedrus decurrens (Torr.). The overstory t the low pollution site is dominted y ponderos pine nd the closely relted Jeffery pine (Pinus jeffreyi Grev. & Blf.), Cliforni lck ok nd white fir (Aies concolor Gord. & Glend.). The prent mteril of soils in oth res is prtilly wethered or decomposed grnite. Three 1 m 9 1 m rcken fern plots t ech site were mrked with stndrd metl fence post t ech corner nd fertilized with NitroformÒ (BFC Chemicls, Wilmington, Delwre) slow-relese fertilizer (38--) t rte of 15 kg N h -1 yer -1. This is grnulr ureformldehyde fertilizer designed for dry ppliction. Fertilizer ws pplied with hnd held spreder once ech fll, eginning in 1997 nd continued for the durtion of the study. The slow relese fertilizer ws pplied in utumn or erly winter to simulte the pulse of N input s winter rins wsh summer deposition off lef surfces into the soil. Corners of three unfertilized control plots of rcken fern were lso mrked with stndrd metl fence posts. Fern plots were chosen in reltively open res with prtil shde from nery trees, ut not directly under tree cnopies. Smple collection Folir insects nd folige were collected four times during ech growing seson (1998 through 2). Smpling dtes were determined y plnt phenology. The first smple ws collected s fern stems were elongting nd fronds were uncurling (My). The second smple for fern ws collected during mid expnsion, fter the min stem ws elongted, ut while fronds were still expnding (lte My to erly June; 1999 nd 2 only). A third smple ws collected in midsummer t full lef expnsion (June to erly July). The fourth smple ws collected in summer t the first sign of yellowing s senescence egn (August to erly Septemer). The ove ground growth of rcken fern ws gged nd removed for ll stems growing within four.5 m 9.5 m res rndomly selected within ech plot, for totl of 12 fern smples for ech tretment. Collected folige ws stored on ice for trnsport nd stored in n ultrcold (-65 C) freezer in the lortory. Insects were mnully removed from the folige, nd identified to
The effect of nitrogen dditions on rcken fern Tle 1 Site comprison for LOW nd HIGH mient ir pollution LOW HIGH Elevtion (meters) 1,9 1,6 Long-term verge nnul precipittion (mm) 641 963 Yerly precipittion (mm) 1998 1,55 1,259 1999 317 392 2 582 74 Averge nnul temperture (8C) 1.6 12.9 Ozone (pp) c Summertime 24-h hourly verge 6.9 67.5 Summertime verge pek vlues 91.3 11.6 Throughfll nitrogen deposition d :kgnh -1 yer -1 8 71 Precipittion from PRISM Climte Group, Oregon Stte University, http://www.prismclimte.org. Averge nnul precipittion clculted from 1895 to 27 From (Fenn et l. 25) c Summer ozone concentrtions were otined from continuous ozone monitors t Crestline (Cliforni Air Resources Bord, pulic informtion) nd Brton Flts (Atmospheric Deposition Group, USDA PSW Reserch Sttion) for June through Septemer 22 d N deposition dt were otined from ulk ion exchnge throughfll collectors (Fenn nd Poth 24). Dt ws collected for 2 5 yers from 2 to 25 (Fenn et l. 28) fmily nd morphotx. Morphotx were ssigned sed on visully distinct ppernces. Herivore undnce for ech smple ws recorded s individuls per.5 m 2 lnd re. This collection method emphsized the more sttionry components of the herivore community, nd likely missed mostly highly moile feeders, especilly fter fern fronds were fully expnded. However, comprison with sweep smples nd visul inspections in the field indicted the most undnt herivores were more sedentry feeders nd present in the sme reltive proportions (Etough Jones, unpulished dt). Herivore morphotx were pooled for ll smpling periods for 1998 through 2 within ech site nd N ddition tretment for richness estimtes. This minimized the effects due to clumped species distriutions nd the smll numer of smples. Species richness ws clculted using EcoSim (Gotelli nd Entsminger 1997). Richness estimtes were clculted sed on rrefction curves generted y EcoSim, with 1 itertions of Monte Crlostyle simultions from the pooled herivore communities. To stndrdize smpling intensity mong tretments, herivore richness ws compred t the level tht corresponded to 8% of the undnce for the tretment with the fewest herivores for ech smpling period. Significnt differences etween tretments were ssessed from the 95% confidence intervls determined from Monte Crlo itertions. Herivore dmge ws estimted quntittively. Individul leves were selected rndomly fter insects hd een extrcted from the collected folige. Enough leves were chosen to fill 2 cm 9 27 cm grid. Folige ws lid out nd covered with 4 mm 9 4 mm squres printed on cler cette sheets. Ten rndom trnsects were selected, nd ech grid point over folige ws scored s dmged or undmged. Dmged points were points where there ws evidence of feeding from chewing herivores nd miners. Plnt chrcteristics Folir nlyses were conducted using plnt tissue collected during insect smpling. Immeditely fter insects were removed from folige, ll leves from ech smple were weighed to determine fresh smple weight. Plnt smples were dried t 5 C for 3 dys nd weighed gin to clculte dry weight. Oven-dried plnt tissue ws ground with Wiley mill to pss through 6 mesh screen. Smple nlyses performed y the Division of Agriculturl nd Nturl Resources Anlyticl Lortory t the University of Cliforni, Dvis for totl N ws y Crlo Er comustion (Pell 199). Anlysis for nitrte ws y queous solvent extrction with 2% cetic cid nd quntittive determintion y flow injection nlysis (Crlson et l. 199; Wendt 1999). Totl N ws determined for smples collected during erly expnsion, mid expnsion nd during the period when leves reched full expnsion. Nitrte ws determined for smples collected during the period when leves reched full expnsion ut not for erlier smpling periods due to limited plnt mteril. Differences in herivore undnce nd plnt chrcteristics mong tretments nd yers within ech site were tested y ANOVA with N ddition tretment nd yer s min effects using SAS (23). Contrsts within ech site nd smpling period hd 12 smples collected t ech of 2 levels of nitrogen fertiliztion for 3 yers for totl of 72 oservtions. Smples were not collected during 1998 t mid expnsion, so there were totl of 48 oservtions in
M. Etough Jones et l. this period. Becuse of limited plnt mteril, nlysis for totl N nd nitrte ws not ville for ll dt points. Due to missing vlues, the numer of oservtions for totl N t the low pollution site were n = 34 (erly expnsion) nd n = 37 (mid expnsion) nd t the high pollution site n = 54 (erly expnsion) nd n = 36 (mid expnsion). Missing vlues for nitrte t full expnsion gve n = 7 t the low pollution site nd n = 66 t the high pollution site. We conducted 2 nlyses to evlute herivore response over the 3 yer durtion of the study. We determined the reltionship of plnt chrcteristics to undnt herivore groups t ech site using Person correltion coefficients. Significnt correltions were evluted t =.5. Herivores chosen for individul comprisons were present t ll sites nd tretments, nd were the most undnt herivore tx (over 5 individuls collected). For the two most common chewing herivores, we lso evluted overll undnce nd dmge cused for dt pooled cross ll 3 yers. Results Plnt chrcteristics Fern iomss ws significntly ffected y N dditions t the LOW site, nd y N dditions nd yer t the HIGH site (Tle 2). Overll there ws trend for decresed iomss for fertiliztion tretments t LOW nd trend for incresed iomss for fertiliztion tretments t HIGH (Fig. 1). In 1998, fern iomss (grms dry weight.5 m -2 lnd re) t the time of full expnsion for unfertilized fern t LOW ws significntly higher thn for fertilized fern, nd higher thn iomss collected in other yers. Fern iomss ws highest in 1998 t the high pollution site, nd higher for fertilized fern. There were never ny significnt differences in totl plnt N for fern t the LOW site (Fig. 2). Plnt nitrte ws higher for LOW fern in 1998 compred to 1999 nd 2, ut there were no differences mong nitrogen ddition tretments (Tle 2). Plnt N ws significntly ffected y N dditions t ll stges of expnsion t the HIGH site (Fig. 2). In generl, oth plnt N nd nitrte were decresed y fertiliztion. Yer of smple collection lso influenced plnt N t HIGH, prticulrly t full expnsion (Tle 2). Totl N for control nd fertilized fern ws significntly different during mid expnsion in 2 nd t full expnsion in 1998 nd 1999. Plnt nitrte t full expnsion ws lso higher for control fern compred to fertilized fern t HIGH, nd significntly higher in 2. Plnt N ws higher for HIGH plnts compred to LOW plnts for ll yers t mid expnsion nd t full expnsion (Fig. 2). Herivore richness nd undnce A totl of 54 herivore morphotx nd 1 24 individuls were collected on rcken fern. 11 tx were collected in ll tretment plots. HIGH hd 26 unique morphotx, while LOW hd 12 unique morphotx. The remining 5 tx were collected t oth sites, ut were not present in ll tretment plots. For oth HIGH nd LOW, [ 98% of ll individuls collected were from morphotx common to oth sites. Those herivores present in high undnce for ll tretments included thrips, mites, nectr-feeding nts, phids, rchis-mining Lepidopter (Gelechiide) nd folige feeding swfly (Tenthridinide). Throughout the growing seson, fern herivore communities were chrcterized y 2 or 3 dominnt herivores. Fern smples collected during erly expnsion were dominted y rchis miner (5% of individuls collected) nd nectr feeding nts (33%). The rchis miner (38%) nd Tle 2 ANOVA sttistics Stge Low pollution site High pollution site F P Effects F P Effects Biomss Full 5.7 \.1 N 9.9 \.1 N, yer, N*yer Totl N Erly 2.7.5 2.7.3 N Mid 2.1.12 7.1 \.1 N, N*yer Full 1.1.37 1.5 \.1 N, yer Nitrte Full 3.6.1 Yer 3.6.1 N, yer Aundnce Erly 7.4 \.1 Yer 6.3 \.1 N, yer Mid 3.9.1 Yer 6.9 \.1 Yer, N*yer Full 2.8.2 Yer 8.5 \.1 N, yer, N*yer Summer 1.9.1 Yer 2.2.6 Contrsts tested effects of level of N ddition (N), yer of smpling (yer) nd the interction of N dditions nd yer (N*yer). Overll F is shown nd significnt contrsts listed
The effect of nitrogen dditions on rcken fern Fig. 1 Folige iomss (men nd SE). Biomss (g dry weight folige.5 m -2 lnd re) of rcken fern ws mesured when fronds reched full expnsion for control nd nitrogen ddition tretments t sites with differing ir pollution (LOW on the left nd HIGH on the right). Within ech site, rs with different letters were significntly different t =.5 iomss 5 4 3 2 1 LOW: control LOW: N dded c c HIGH: control HIGH: N dded c c 1998 1999 2 1998 1999 2 swflies (16%) were common t mid expnsion. Free feeding swflies (1%) were lso common herivores t full expnsion. Aphids were lso undnt y mid-expnsion (38%) nd remined undnt (74%) through the rest of the growing seson. There were no differences in herivore richness mong sites nd tretments during erly expnsion or mid expnsion (Fig. 3). For smples collected t full expnsion, herivore richness ws significntly higher for the fertilized plots t HIGH compred to ll other tretments. For smples collected during the summer, herivore richness for control plots t LOW ws significntly lower thn richness for oth HIGH tretments, nd richness for LOW fertilized plots ws significntly lower thn for HIGH fertilized plots (Fig. 3). There ws rrely ny difference in herivore undnce t the low pollution site in response to nitrogen ddition tretments (Fig. 4). Herivore undnce did vry mong yers t LOW (Tle 2). During erly expnsion, herivore undnce ws highest in 1998. Lter in the growing seson, herivore undnce ws highest in 1999. Brcken fern herivores showed more differences relted to fertiliztion tretments t the high pollution site, prticulrly during erly expnsion (Tle 2). Totl herivore undnce t HIGH ws higher on fertilized plots thn control plots during erly expnsion (Fig. 4). Lter in the seson there were few differences mong yers or tretments t HIGH. The one exception ws high undnce for control plots during 1999. We compred dmge to fern nd undnce of individul herivores for two of the most common herivores, the rchis mining Lepidopter nd the free-feeding swfly, pooled cross ll 3 yers of smple collection (Tle 3). Dt ws pooled for the period of pek undnce for ech herivore. The rchis miner ws most undnt during erly expnsion while the swfly ws most undnt s fern fronds reched full expnsion. While these herivores were oth present t mid-expnsion, nerly ll dmge to fern fronds ws mde y only one txon t erly nd full expnsion. Aundnce of oth the rchis miner nd the swfly nd dmge to fern were higher t the high pollution site compred to the low pollution site. There were no significnt differences in dmge or undnce of rchis miners nd swflies etween control nd fertiliztion tretments within either site. Reltionship etween plnt chrcteristics nd herivore undnce Aundnce of the rchis mining Lepidopter ws never correlted with plnt N t either site (Tle 4). Swfly undnce ws significntly positively correlted with plnt N t LOW during full expnsion, ut negtively correlted with plnt N during mid expnsion t HIGH. Aphid undnce ws significntly negtively correlted with plnt N t LOW during mid expnsion, ut never correlted with plnt N t HIGH. Aundnce of nectrfeeding nts ws positively correlted with plnt N t LOW during mid expnsion, ut negtively correlted with plnt N during erly expnsion t HIGH. Discussion We chose to study the response of rcken fern herivore communities to simulted tmospheric nitrogen deposition through N fertiliztion ecuse rcken fern hs shown strong cpcity to store excess N in folige (Fenn et l. 1996; Stms nd Schipholt 199). Fern iomss per lnd re nd fern herivore undnce were ffected y fertiliztion t oth low nd high pollution sites. In contrst, similr fertiliztion study t these sites found no response to fertiliztion for herivores on Cliforni lck ok t the low pollution site (Etough Jones et l. 28). Brcken fern herivores my e more responsive to smll chnges in N lloction within plnts or chnging ptterns of plnt
M. Etough Jones et l. Fig. 2 Folige N nd nitrte (men nd SE). Totl N ws mesured t erly, mid nd full expnsion. Solule nitrte (ppm) ws mesured t full expnsion. Ech site (LOW (left) nd HIGH (right) mient ir pollution) hd control nd nitrogen ddition tretments. Within ech site, rs with different letters were significntly different t =.5 N (erly) 6 4 2 LOW: control LOW: N dded HIGH: control HIGH: N dded 6 N (mid) 4 2 c c c 4 d N (full) 2 3 2 NO 3 (full) 1 4 2 1998 1999 2 1998 1999 2
The effect of nitrogen dditions on rcken fern Fig. 3 Brcken fern herivore richness nd 95% confidence intervls. Herivores were pooled within ech smpling period for ll smples collected 1998 through 2. Ech site (LOW nd HIGH mient ir pollution) hd control nd nitrogen ddition tretments. Within ech smpling period, rs with different letters re significntly different s determined y 95% confidence intervls Herivore richness 15 12 9 6 3 LOW: control LOW: N dded HIGH: control HIGH: N dded c c erly expnsion mid expnsion full expnsion summer Fig. 4 Fern herivore undnce (men nd SE). Totl herivore undnce for ech smpling dte nd ech yer during erly, mid nd full expnsion. Ech site (LOW (left) nd HIGH (right) mient ir pollution) hd control nd nitrogen ddition tretments. Within ech site, rs with different letters were significntly different t =.5 erly 2 15 1 5 LOW: control LOW: N dded c c c c HIGH: control HIGH: N dded c cd d d 8 Totl herivores mid 6 4 2 16 12 full 8 4 1998 1999 2 1998 1999 2
M. Etough Jones et l. Tle 3 Herivore undnce (individuls per.5 m 2 lnd re) nd ssocited dmge (%) to fern fronds for two common herivores t low nd high pollution site Site Tretment Rchis miners Dmge (erly) Swflies Dmge (full) Low Control.8 ±.2 3. ±.9 1.7 ±.5 8.4 ± 1. N dded.3 ±.1.7 ±.3.7 ±.2 7.3 ±.8 High Control 3.7 ± 1.1 6.2 ± 1.7 5.6 ± 1. 13.9 ± 2.6 N dded 3.9 ±.7 5.6 ± 1.2 5.1 ± 1.1 15.3 ± 2.5 F 7.83 4.8 9.76 4.35 P \.1.3 \.1.6 Dt were pooled cross yers within ech tretment. Rchis miners were present during erly expnsion. Swflies were present s rcken fern reched full expnsion. Contrst compred site (Low nd High mient ir pollution) nd level of N ddition. Significnt differences re indicted within ech column Tle 4 Person correltion coefficients for plnt N with herivore undnce Low pollution growth t the low pollution site. Both fern nd ok herivores showed responses to fertiliztion t the high pollution site, indicting tht further N pollution inputs will continue to lter plnt-insect interctions in southern Cliforni forests. Plnt nutrient response High pollution Erly Mid Full Erly Mid Full Rchis miner -.1.16 -.7 -.4.5 -.3 Swfly -.24.9.37* -.7 -.43*.1 Aphid -.4 -.46* -.5 -.1.12 -.1 Ant -.2.47*.15 -.27* -.23.2 LOW: n = 34 erly, n = 37 mid, n = 72 full. HIGH: n = 54 erly, n = 36 mid, n = 72 full. Correltions for herivores were performed cross ll yers nd within ech site. *P \.5 Contrry to our expecttions, we found tht oth totl N nd plnt nitrte were decresed in folige of fertilized plnts t the high pollution site. In 1998, when plnt iomss ws very high for fertilized fern, it is possile tht the common phenomenon of growth dilution my hve contriuted to lower plnt N for fertilized fern t the high pollution site. However, iomss responses t the high pollution site in 1999 nd 2 don t support this s mechnism to explin overll decreses in plnt N nd nitrte. Another possile fctor my e tht fertiliztion t the high pollution site incresed microil immoiliztion of N, nd consequently the N ville for ssimiltion y rcken fern my hve decresed. Although dt collected in this study cnnot conclusively demonstrte microil moiliztion, evidence from other studies conducted in the Sn Bernrdino Mountins suggests the possiility (Fenn et l. 25). There is much more litter in the forest floor nd higher orgnic mtter content in the A soil horizon t the high pollution site compred to the low pollution site (Fenn et l. 25). Litter nd soil orgnic mtter t the high pollution site my provide undnt C for microil immoiliztion of N. Tht, in comintion with the dded N, my stimulte microil growth resulting in less N ville for plnt uptke in fertilized plots t the high pollution site. It is common for lrge frction of dded N to e incorported into the orgnic horizon (Fenn et l. 1998), nd N immoiliztion cn e much greter in the orgnic horizon compred to minerl soil (Johnson et l. 2). Aer et l. (1998) reported from literture review tht two-thirds of N dded in N mendment studies ended up in the soil orgnic lyer without pssing through oveground plnt tissues. Although oth ok nd pine trees t the high pollution site showed incresed rdil growth in response to fertiliztion tretments (Fenn nd Poth 21), fern my tke much greter frction of N from the A horizon nd humus horizons thn do the forest trees. As result, microil immoiliztion my ffect N vilility for fern more thn for pine nd ok, which re deeply rooted in the minerl soil nd wethered edrock (Witty et l. 23). Neither net N minerliztion nor net nitrifiction in the minerl soil ws ffected y N dditions t the high pollution site (Fenn et l. 25). However, fertiliztion resulted in lower nitrte levels in forest soils t the high pollution site (Fenn et l. 25). Additionlly, high rtes of gross NH 4 immoiliztion in the orgnic lyer t the high pollution site (ME Fenn, unpulished dt), nd higher totl C in fertilized soils, lso suggest tht incresed microil immoiliztion of N my e tking plce in the upper minerl soil nd orgnic horizon of fertilized plots t the high pollution site. It is likely tht comintion of differences in ville C in the minerl soil, litter lyer depth, microil immoiliztion, understory plnt diversity nd precipittion ccount for the different responses of fern to fertiliztion t these two sites.
The effect of nitrogen dditions on rcken fern Plnt growth response Nitrogen fertiliztion studies with rcken fern hve often shown little positive effect on plnt growth (Gordon et l. 1999; Werkmn nd Cllghn 22; Werkmn et l. 1996; Whitehed et l. 1997). Our study suggests tht high N vilility my hve even decresed fern iomss. Although iomss ws higher for fertilized fern t the high pollution site, N in plnt tissues nd soil NO 3 (Fenn et l. 25) were ctully decresed y N dditions, so tht plnts from control plots t the high pollution site with higher folir N hd lower iomss production. Fern iomss from fertilized plots t the low pollution site ws consistently lower thn for control plots. This ws prticulrly evident during yer of high precipittion. There ws n El Niño event during the winter of 1997 1998. Rinfll for 1998 in the Sn Bernrdino Mountins ws much higher thn rinfll for 1999 nd 2 (Tle 1). Gordon et l. (1999) found tht drought hd greter impct thn N supply on fern growth, nd decresed oth frond density nd height. Our results lso suggest tht wter vilility is more importnt thn N vilility for fern iomss production. We would expect tht N fertiliztion nd dded precipittion from the El Niño would hve incresed fern growth (e.g. Wring nd Co 1992), prticulrly t the low pollution site. We cn only speculte tht the dditionl precipittion stimultes microil N immoiliztion. It is possile tht immoiliztion my e promoted y the slow relese fertilizer we used which depends on microil relese of the N, so tht t the N-poor site microes outcompeted the plnts for N. A negtive growth response to N fertiliztion ws lso found for trees t the low pollution site (Fenn nd Poth 21). Other studies of the effects of N fertiliztion on rcken fern hve used rtes equivlent to 5 kg N h -1 yer -1 (Gordon et l. 1999; Werkmn nd Cllghn 22; Werkmn et l. 1996; Whitehed et l. 1997) compred to the rte of 15 kg N h -1 yer -1 tht we used. Our high rte of fertiliztion my e why we oserved decresed iomss while other studies hve not. However, deposition in some res of southern Cliforni lredy exceed 5 kg N h -1 yer -1. The current rte of tmospheric deposition t our high pollution site is 71 kg N h -1 yer -1, nd verge nnul fluxes under pine cnopies s summer deposition is wshed off y winter rins re c. 13 kg N h -1 yer -1 (Fenn nd Poth 24). However, with vrile rinfll mong yers, different soil N chrcteristics etween our sites, nd possile interference from choosing fertilizer tht required microil relese, we cnnot confidently presume tht the oserved decrese in fern iomss ws due directly to N fertiliztion. The interctions etween rinfll nd tmospheric nitrogen deposition wrrnt further investigtion. Herivore responses We found evidence tht plnt N sttus does influence undnce for rcken fern insect herivores. Nitrogen deposition hs previously een shown to ffect herivore performnce (Throop nd Lerdu 24). Most insects respond positively to incresed plnt nitrogen (Kyto et l. 1996; Mttson 198; Wring nd Co 1992). Similrly, we found tht swfly undnce ws positively correlted with plnt N t the low pollution site, nd chewing dmge to fern s well s undnce of swflies nd rchis mining Lepidopter were oth higher t the high pollution site compred to the low pollution site. Brcken fern hs mny cron-sed defensive compounds including tnnins (Jones 1983). This my ffect swflies more thn rchis miners since tnnin concentrtions re low in expnding fronds while miners re ctive nd high in mture folige when swflies re present (Jones 1983; Tempel 1981). Fertiliztion my decrese concentrtions of tnnins, nd increse pltility for insect herivores (Feeny 197). However, undnce of swflies ws negtively correlted with plnt N t the high pollution site. Differences in the ssocition of plnt N nd herivore undnce for these two sites my e relted to the lrge difference in plnt N sttus etween sites nd the high nitrte concentrtions in fern fronds t the high pollution site. Totl plnt N nd plnt nitrte were positively correlted. Folir nitrte t the high pollution site ws nerly 2 orders of mgnitude higher thn nitrte t the low pollution site. High plnt nitrte cn e feeding deterrent for mny insect herivores (Jnsson nd Smilowitz 1985; Mnglitz et l. 1976). This my e prticulrly importnt for chewing herivores such s swflies. High nitrogen vilility my lso e ssocited with n increse in nitrogen sed plnt defenses (Brynt et l. 1983). Brcken fern hs rod rry of secondry compounds ssocited with nti-herivore properties (Jones 1983) including the enzyme thiminse which my increse with high nitrogen vilility. Conversely t the low pollution site, where plnt nitrte is much lower thn t the high pollution site, higher plnt N my mke plnts more fvorle resource for swflies. Nectr feeding nts nd phids my e responding to differences in plnt growth, timing of nectr production or nectr qulity. Fertiliztion is known to ffect mino cid composition for some plnts (Grdener nd Gillmn 21) nd mino cids in nectr cn ffect nt ttrction (González-Teuer nd Heil 29). However, rcken fern hs not een shown to enefit from nt ttrction to extrflorl nectrines (Rshrook et l. 1992) nd the effects of fertiliztion on nectr of rcken fern re unknown. Aphids re likely voiding plnt nitrte, which is stored in the vcuole, y feeding directly from phloem. Aphids, which hve pek undnce lter in the seson, my e
M. Etough Jones et l. preferentilly colonizing lrger, more expnded plnts t the low pollution site. Further exmintion of chnges in mino cids nd secondry compounds of rcken fern my provide further insight for the reltionship etween chnges in plnt N sttus nd insect herivore responses. Conclusions In spite of rcken fern s glol distriution, common noxious weed sttus nd potentil to respond to environmentl chnge, the impct of tmospheric pollution on rcken fern herivores hs never een studied. We found indictions tht tmospheric N inputs hve impcted rcken fern herivores in the Sn Bernrdino Mountins of Cliforni. The response of swflies nd rchis mining Lepidopter to N dditions my wrrnt further investigtion. Rchis miners cn inhiit fronds from fully unfurling nd ffect lef surfce re in mture fern (Etough Jones, personl oservtion). Swflies were the only free-feeding herivore we oserved to hve mjor impct on removing lef re through herivory. We did not oserve dmge from herivory y mmmls during this study. These two insect herivores hve the gretest likelihood of cusing dmge to fern in the Sn Bernrdino Mountins, potentilly reducing frond surfce re nd impcting ground cover in fern stnds. While we did see effects of fertiliztion within ech site, there were much stronger differences in herivore undnce etween sites. Additionlly, environmentl differences from yer to yer hd stronger influence. We did see indictions tht rcken fern response to nitrogen inputs my vry depending on rinfll, with the strongest responses eing oserved in yer of high rinfll. Brcken fern hs rod geogrphicl distriution nd is noxious weed in mny res with more mesic climtes compred to southern Cliforni (Tylor 199). Our study suggests tht the impcts of tmospheric nitrogen deposition on rcken fern plnt N my e more pronounced in more mesic climtes. The interctions etween rinfll nd tmospheric nitrogen deposition wrrnt further investigtion. Acknowledgments We re grteful to Stephnie Wshurn, Chris Hnlon, Ktherine Lurhing, Sturt Wooley, Srh Allen, Idr Essien, nd Jocelyn Holt for their ssistnce in the field nd lortory. Funding ws provided in prt y the University of Cliforni Grdute Division through disserttion improvement grnt nd y grnt from the University of Cliforni Acdemic Sente. The support of the USDA Ntionl Reserch Inititive Competitive Grnts Progrm, Agreement No. 96-3511-3259 to Mrk Fenn, Mrk Poth nd Pul Miller ws instrumentl in estlishing the reserch plots for this study. Open Access This rticle is distriuted under the terms of the Cretive Commons Attriution Noncommercil License which permits ny noncommercil use, distriution, nd reproduction in ny medium, provided the originl uthor(s) nd source re credited. References Aer JD, Mgill A, McNulty SG, Boone RD, Ndelhoffer KJ, Downs M, Hllett R (1995) Forest iogeochemistry nd primry production ltered y nitrogen sturtion. 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