Ecology, 86(7), 2005, pp. 1737±1743 ᭧ 2005 by the Ecological Society of America

PREY ADDITION ALTERS NUTRIENT STOICHIOMETRY OF THE CARNIVOROUS PURPUREA

AMY E. WAKEFIELD,1 NICHOLAS J. GOTELLI,1,3 SARAH E. WITTMAN,1 AND AARON M. ELLISON2 1University of Vermont, Burlington, Vermont 05405 USA 2Harvard University, Harvard Forest, P.O. Box 68, Petersham, Massachusetts 01366 USA

Abstract. The carnivorous receives nutrients from both captured prey and atmospheric deposition, making it a good subject for the study of ecological stoichiometry and nutrient limitation. We added prey in a manipulative ®eld experiment and measured nutrient accumulation in pitcher-plant tissue and pitcher liquid, as well as changes in plant morphology, growth, and photosynthetic rate. Prey addition had no effect on traditional measures of nutrient limitation ( morphology, growth, or pho- tosynthetic rate). However, stoichiometric measures of nutrient limitation were affected, as the concentration of both N and P in the leaf tissue increased with the addition of prey. Pitcher ¯uid pH and concentration did not vary among treatments, although dissolved levels decreased and ammonia levels increased with prey addition. Ratios of N:P, N:K, and K:P in pitcher-plant tissues suggest that prey additions shifted these carnivorous from P limitation under ambient conditions to N limitation with the addition of prey. Key words: carnivorous plants; ®eld experiment; K:P ratio; N:K ratio; N:P ratio; ; nutrient limitation; phosphorus; Sarracenia purpurea; stoichiometry.

INTRODUCTION many species alter production or morphology of car-

nivorous organs in response to nutrient input (Knight Reports Ecological analyses of relationships between essen- and Frost 1991, Ellison and Gotelli 2002). tial nutrients and energyÐecological stoichiometry Because pitcher plants are sensitive to N:P input ra- (Sterner and Elser 2002)Ðcan provide important in- tios, we expect them to respond differently to two dif- sights into processes that control patterns of species ferent forms of nutrient input: captured prey and at- distributions, abundances, and population dynamics. mospheric deposition. Captured prey (mostly arthro- For example, if nutrient availability limits growth (Aerts and Chapin 2000), then ratios of nitrogen and pods) include N, P, K, Ca, and other nutrients that po- phosphorus (N:P) (Koerselman and Meuleman 1996, tentially enhance plant growth, but cannot be used by Bedford et al. 1999) or nitrogen, phosphorus, and po- the plant until they are released by and tassium (N:P:K) (Olde Venterink et al. 2002, 2003) in feeding activities of the specialized invertebrate com- plant tissue can predict nutrient limitations of both in- munity that inhabits Sarracenia pitchers (Heard 1994). dividual plants and entire communities (Aerts and Atmospheric deposition (NO3 and NH4) does not in- Chapin 2000). By these criteria, many European wet- clude other essential elements, but does provide a lands and North American tend to be N limited, source of biologically active nitrogen that is immedi- but other North American wetlands tend to be P limited ately available for plant uptake (Ellison and Gotelli (Bedford et al. 1999). 2002). The purple pitcher plant Sarracenia purpurea L. (see In this study, we used a controlled ®eld experiment Plate 1) is a model system for studying ecological stoi- to test for the effect of prey addition on the morphol- chiometry because the production of carnivorous pitch- ogy, stoichiometry, and photosynthetic rates of Sar- ers and ¯at photosynthetic (phyllodes) is altered racenia purpurea. We hypothesized that pitcher plants by nutrient inputs (Ellison and Gotelli 2002). Carniv- would respond to additional prey by increasing leaf orous plants grow commonly in nutrient-poor , photosynthetic rate, and nutrient absorption. such as ombrotrophic bogs (Givnish et al. 1984), and We further predicted that because of the difference in rely in whole or in part on captured prey to supply nutrient content between prey and atmospheric depo- essential nutrients (Chapin and Pastor 1995). Growth sition, plant morphology (pitcher vs. phyllode produc- and reproduction of most carnivorous plants are limited tion) would not be altered in prey-fed plants. Last, we by available nitrogen (Ellison and Gotelli 2001) and compared N:P:K ratios in tissues of control and treat- ment plants to extend our understanding of pitcher- plant stoichiometry and to evaluate evidence for N, P, Manuscript received 3 November 2004; revised 4 February and K (co-)limitation in this species. 2005; accepted 1 March 2005. Corresponding Editor: D. A. Spiller. In agricultural systems, traditional measures of plant 3 Corresponding author: E-mail: [email protected] responses to nutrient additions include shifts in plant 1737 Reports tihoer htas niaentin limitation nutrient 2002). indicate Elser ecological and also (Sterner in ac- shifts that nutrient document tissue stoichiometry to of measures in photosyn- as cumulation well and as measured biomass, rate, have thetic growth, we study, morphology, this In plant 1986). al. best et communities the (Chapin natural in be limitation nutrient always detect to not way may measures rate. these photosynthetic However, or biomass, growth, morphology, 1738 ie ta.18) nieteohrseisof species other the Unlike (Ju- 1989). leaf the al. by et absorbed niper is from are nutrients prey and decomposing The pitchers, the the 2001). in Gotelli drowns and and trapped Ellison and (Chapin 1995, brightly nectaries Pastor the extra¯oral to and attracted pitchers prey colored nutrients their from of obtained bulk the are and 1989) sys- al. et developed (Juniper al. tems weakly et have (Ellison plants Columbia Pitcher At- British 2004). from to and west States, Canada United lantic the of fen mid-west and poor upper England, the New occasional plain, coastal the eastern nutrient-poor the and throughout sunny, swamps, seepage in bogs, grows that plant nrsos oeprmna ryadtos ht rdt .J Gotelli. J. N. credit: Photo additions. prey experimental to response in P arcnapurpurea Sarracenia LATE .I h anvru plant carnivorous the In 1. M TRASAND ATERIALS td species Study sarstefrigperennial rosette-forming a is M ETHODS arcnapurpurea Sarracenia M .WKFEDE AL. ET WAKEFIELD E. AMY Sarra- h ocnrto fla-isentoe n hshrsincreases phosphorus and nitrogen leaf-tissue of concentration the , cenia rpat rwn tBlieeBg n2h ee level 2-ha an Bog, Belvidere at growing plants er ie r ns(oel n lio 2002 Ellison and (Gotelli study ants our at rate are prey but sites capture insect primary affect variable, The generally 1991). highly (Cresswell not is does density pitchers cap- of pitcher between biomass total prey The 1978). pitcher tured Hall a and after (Fish capture weeks opens four and within 1998), decreases Nastase ef®ciency and (Newell captured are ryi h aa eorefrti odwb which web, by nutrients food capture available Prey this 1994). the (Heard mineralizes for and resource prey the basal shreds the is Captured prey 1994). (Heard and invertebrates, protists with specialized along of community associated an .ElsnadN .Gotelli, J. N. and Ellison M. inef®cient: utn narltvl osatnme fpthr per 1978). pitchers Hall of and re- number (Fish produced, constant plant the are relatively leaves a over new in as sulting senesce summer the they of the course season, into persist growing leaves some subsequent Although 1978). (Fish annually Hall sea- produced growing and are the leaves ®ve during average days on 14 son; to 10 every produced eeprmnal aiuae rylvl npitch- in levels prey manipulated experimentally We nNwEgad e ef(ice rpyld)is phyllode) or (pitcher leaf new a England, New In , .purpurea S. Ͻ %o h oeta ryta ii pitcher a visit that prey potential the of 1% xeietlmethods Experimental icesacmlt anae and rainwater accumulate pitchers nulse data unpublished .purpurea S. clg,Vl 6 o 7 No. 86, Vol. Ecology, a n is(A. ¯ies and ) srelatively is ). July 2005 STOICHIOMETRY OF SARRACENIA 1739 in Vermont, USA (44Њ N, 72Њ W), in order to determine TABLE 1. Dissolved oxygen and NH4-N in the ¯uid of Leaf I as a function of number of ¯ies added to the pitcher. the effect of prey addition on morphology, photosyn- thetic rate, water chemistry, and stoichiometry of S. No. ¯ies Dissolved oxygen purpurea. In May 2002 we haphazardly chose 200 non- added per week (mg/L) NH4-N (mg/L) Ն ¯owering adult plants (rosettes 10 cm) in the open 0 2.9 Ϯ 1.00 0.4 Ϯ 1.03 area of the bog. A distance of at least 50 cm separated 2 2.6 Ϯ 0.73 0.8 Ϯ 0.98 all experimental plants. Each plant was randomly as- 4 1.9 Ϯ 1.11 1.4 Ϯ 1.61 Ϯ Ϯ ϭ 6 1.8 0.81 1.4 1.49 signed to one of eight treatment levels (N 25 plants 8 1.7 Ϯ 1.19 2.3 Ϯ 1.8 per treatment), corresponding to 0-7 frozen house¯ies 10 1.4 Ϯ 0.83 2.7 Ϯ 1.69 (mean dry mass ϭ 1 mg; 103 mg N/g; 7.6 mg P/g; 9.2 12 1.1 Ϯ 1.09 3.1 Ϯ 1.76 Ϯ Ϯ mg K/g; 1.7 mg Ca/g; 1.4 mg Mg/g) fed twice weekly 14 0.6 0.62 3.5 1.48 to each pitcher throughout the summer. Because house Note: Values are means Ϯ SD; N ϭ 25 plants/treatment. ¯ies are heavier and have less chitin than most natural prey, these additions represented substantial On 15 August 2002 we measured maximum photo- increases over background levels of prey intake. Flies synthetic rates of the Leaf I on two randomly selected were added only to pitchers produced during the 2002 plants from each treatment level. These plants were all growing season; prey addition began when the ®rst new harvested at the fourth harvest (2 September). Photo- pitchers were produced (24 June 2002) and continued synthesis measurements were made in full , between until 12 September 2002. We added distilled water as 09:00 and 14:00 hours, using a LI-COR 6200 photo- necessary to maintain pitcher ¯uid at half of the leaf synthesis system (LI-COR, Lincoln, Nebraska, USA) volume (5±10 mL). Pitchers on each plant were num- and custom built 4-L chamber (Ellison and Gotelli bered sequentially in order of opening date (Leaf I, 2002). During all measurements, ambient solar radia- Leaf II, Leaf III, etc.) and each leaf was fed until they tion exceeded the saturating photosynthetic photon ¯ux were harvested for analysis. density of Sarracenia (PPFD Ͼ 800 ␮mol´mϪ2´sϪ1). At approximately two-week intervals (10 and 29 Statistical analyses

July, 13 August, 2 and 15 September), all fed pitchers Reports were harvested from each of ®ve randomly chosen We used two-way analyses of variance (ANOVA) plants from each treatment group. Immediately before using S-Plus 6.1 (Insightful Corporation, Seattle, each harvest, dissolved oxygen content of the pitcher Washington, USA) to compare mean responses of Leaf ¯uid (milligrams per liter and percentage saturation) of I to different feeding treatments at the different harvest each leaf designated for that harvest was measured in dates. Both numbers of ¯ies added and harvest date situ using a YSI-58 dissolved oxygen meter (YSI in- were treated as random variables in this ANOVA, so struments, Yellow Springs, Ohio, USA). Each pitcher the appropriate error term for these main effects in the was then cut off at the base; pitcher ¯uid was poured ANOVA is the harvest ϫ treatment mean square, and into sterile plastic tubes (50-mL centrifuge tubes) for the error term for the interaction term is the residual subsequent analysis and the pitcher itself placed into mean square (Gotelli and Ellison 2004). Observed re- a Ziploc plastic bag. All harvested material was kept sponses of Leaves II and III to the treatments were cool and returned to the laboratory for processing with- qualitatively similar to those of Leaf I, but because in4h. some plants had fewer than three leaves, we illustrate In the laboratory, the pitcher ¯uid was ®ltered using and discuss only the results for Leaf I. As measure- a Millipore Steri®l Aseptic system (Millipore Corpo- ments of were conducted only once, ration, Billerica, Massachusetts, USA). The pH of the these values were compared among treatment levels ®ltrate was measured with an Orion Model 290A por- using a one-way, random-effects ANOVA. Variables table pH/ISE meter (Thermo Corporation, were log10 transformed as necessary to normalize var- Waltham, Massachusetts, USA), and nitrogen (both iances and eliminate heteroscedasticity. NO -N and NH -N) and phosphorus (PO -P) concen- 3 4 4 RESULTS trations were determined spectrophotometrically using standard methods (Bledzki and Ellison 1998, Clesceri Characteristics of the pitcher ¯uid et al. 1998). The length, mouth diameter, and maximum With increasing number of ¯ies fed to the pitchers, width (Ϯ1 mm) of each harvested pitcher or phyllode dissolved oxygen concentration in the pitcher ¯uid de- ϭ Ͻ was measured, along with the width of its wing (keel); creased (F7,21 9.89, P 0.001; Table 1) and NH4-N ϭ Ͻ see Ellison and Gotelli (2002) for an illustration of content increased (F7,28 9.51, P 0.001; Table 1). these measurements. All leaves were dried at 70ЊC for Dissolved oxygen concentrations were similar across 3±5 days, and individually weighed and ground for harvests early and late in the summer (2 mg/L), but nutrient analysis at the University of Vermont Agri- decreased to 1.2 mg/L in midsummer at Harvest 3 (F3,21 ϭ ϭ cultural and Environmental Testing Laboratory (Bur- 10.8, P 0.03). NH4-N increased from an early lington, Vermont, USA). season low of 1.3 Ϯ 1.73 mg/L to a midsummer peak Reports ϭ 2.5 of 1740 ubr f¯e.Dt r o rtlae only; leaves ®rst for are Data ¯ies. of numbers ifrn ubr f¯e de rvre signi®cantly varied or added ¯ies of numbers different PO eee f t2.1 at off leveled fvria ie)adidvda ausbyn h pe and upper circles). the (ends (solid beyond deciles deciles values lower lower individual and and lines) upper vertical boxes), of of (edges low- quartiles and upper er Box line), harvests. horizontal (center ®ve median all illustrate across plots pooled are Values treatment. per F 6.2 4 IG P(0.69 -P .Ntin ocnrtosi icesfdvarying fed pitchers in concentrations Nutrient 1. . Ϯ Ϯ .0m/ ( mg/L 1.90 .6[ 1.06 Ϯ .7m/)cagdsgicnl with signi®cantly changed mg/L) 0.87 SD Ϯ ) NO ]), .0m/.Nihrp gadmean (grand pH Neither mg/L. 1.80 F 4,28 3 ϭ N(0.16 -N 4.60, P Ϯ ϭ .9m/) nor mg/L), 0.39 .0) n then and 0.006), M .WKFEDE AL. ET WAKEFIELD E. AMY N ϭ 5plants 25 al esrdi h ice ¯uid. pitcher inter- the in no var- any measured were for iable date There harvest summer. and treatment the between actions of course the over .3,bticesdsgicnl uigtegrowing the during ( signi®cantly season increased but 0.13), Mg: 0.001; ϭ F .)was 1.4) (overall treatments other the all plants 6.02, control in the plants either or than test) HSD Tukey's 0.05, P nrae ihicesn ubro isadd(N: added ¯ies of all number leaves increasing pitcher with in increased concentrations 1C) (Fig. tassium ubro iceso h lnsa ahhretdate harvest each at plants mean the (grand on pitchers of number e f¯e de ( num- added the ¯ies with of signi®cantly ber decrease not did plants fed avss(N:K harvests ( e 4¯e e ekwssgicnl ihr( higher signi®cantly was week per ¯ies 14 fed ramns( treatments eeso hog ie(eflnt:161 length: (leaf time through Individual or treatment levels treatments. among differ not across did variables morphological production pitcher of a osgicn ifrnei h : ai among ratio N:P the ( in harvests difference signi®cant no was F F F icn neato ewe ramn n avs date harvest ( and treatment between interaction ni®cant ihrta hto n ftefdpat ( plants fed the of any of that than higher measured nutrient tissue. between any pitcher interactions the for in no date harvest were and there treatment ¯uid, pitcher in itn ieto Fg E.NihrN( N Neither 1E). (Fig. direction sistent D i o ayaogtetet ( treatments among vary not did 1D) hog h rwn esn(K: season decreased growing both Mg the and K through but date, harvest with varied in®atitrcinaogtetet n harvests and ( treatments among interaction signi®cant in®atymr icesa ae avssta tear- ( at harvests than harvests lier were later there at treatments pitchers across more that signi®cantly surprising season, not growing was the it throughout produced are pitchers ue e plant; per duced efwdh 41 width: leaf epniua ot imtr:27 diameters: mouth perpendicular 7,28 K: m[mean mm 8 160 28, 4,28 155 28, irgn(i.1) hshrs(i.1) n po- and 1B), (Fig. phosphorus 1A), (Fig. Nitrogen hr a odfeec mn ramnsi the in treatments among difference no was There Ͻ .9 o ( P nor 0.79) F h : ai ftecnrlpat a signi®cantly was plants control the of ratio N:P The 7,28 ϭ .0;Tbe2.Hwvr h : aiso the of ratios N:P the However, 2). Table 0.001; ϭ P 15.19, ϭ ϭ ϭ uretcneto h ice tissues pitcher the of content Nutrient F Ͻ 16.37, ϳ F 4,28 1.12, 1.569, 4.34, 5 oe hnNKa h usqetfour subsequent the at N:K than lower 25% 4,28 .0) : lodfee mn harvests among differed also N:K 0.001). Ϯ F F ϭ 7,28 ϭ 4,28 F SD P ϭ rwhadmorphology and Growth ϭ Ϯ P 4,28 P F 17.82, P 2.9 Ͻ ϭ ]). ϭ P 2.35, 1.8). 05m;ke it:19 width: keel mm; 10.5 F 4,28 Ͻ ϭ ϭ P ϭ 4,28 .0;P: 0.001; 4.61, ϭ 16.52, Ϯ .2.TeNKrtoo h plants the of ratio N:K The 0.32). .0) : thret1(N:K 1 harvest at N:K 0.001); Ͼ ϭ .0) ansu aidacross varied 0.002). 35.510, .4)btn ossetpattern consistent no but 0.045) ϭ P . [mean 1.4 P .5 ue' S et.There test). HSD Tukey's 0.05; 1.25, P ϭ 0.515, Ͻ P ϭ .8,nrwsteeasig- a there was nor 0.08), .0) swt nutrients with As 0.001). F Ͻ P .0) u o nacon- a in not but 0.002), P 7,28 ϭ .0) acu (Fig. 0.001). Ͻ P clg,Vl 6 o 7 No. 86, Vol. Ecology, ϭ F Ϯ .1 nla tissue leaf in 0.31) Ϯ ϭ .1.Teewsa was There 0.01). 4,28 13.14, F SD . n 20 and 6.4 .1) Because 0.815). 7,28 F ϭ icespro- pitchers ] 4,28 Ϯ ϭ F 65.59, P Ϯ 7,28 ϭ 1.76, 84mm; 38.4 Ͻ . mm; 7.7 ϭ 0.42, F 0.001; Ϯ 7.28 5.98, P P P 5.1 ϭ ϭ Ͻ ϭ Ͻ P July 2005 STOICHIOMETRY OF SARRACENIA 1741

TABLE 2. Ratios of critical elements (N, P, K) in plant tissues of Sarracenia purpurea fed different numbers of ¯ies.

Element ratios (mg/mg) No. ¯ies added per week N:P N:K K:P 0 17.0 Ϯ 3.05 3.1 Ϯ 1.27 5.6 Ϯ 4.26 2 11.8 Ϯ 3.25 3.3 Ϯ 1.22 3.8 Ϯ 1.28 4 10.1 Ϯ 2.28 3.3 Ϯ 1.06 3.2 Ϯ 0.92 6 10.5 Ϯ 2.48 3.5 Ϯ 1.31 3.3 Ϯ 1.15 8 10.5 Ϯ 2.08 3.9 Ϯ 1.29 2.9 Ϯ 0.98 10 9.1 Ϯ 1.33 3.9 Ϯ 1.22 2.5 Ϯ 0.69 12 9.4 Ϯ 2.62 3.9 Ϯ 1.18 2.5 Ϯ 0.71 14 9.1 Ϯ 1.46 4.5 Ϯ 1.85 2.3 Ϯ 0.87 Threshold for limitation² 14.5 2.1 3.4

Notes: Values are means Ϯ SD; N ϭ 25 plants/treatment. If the observed ratio exceeds the threshold for limitation, the results suggest limitation of the nutrient in the denominator. If the observed ratio falls below the threshold, the results suggest limitation of the nutrient in the numerator. See Discussion for additional details. ² Threshold ratios are from Olde Venterink et al. (2003).

Photosynthetic rate mg/g level (Fig. 1C), indicating that K could also limit The average photosynthetic rate measured for plants plant growth. However, N:K and K:P ratios (Table 2) in all treatments was 3.1 Ϯ 1.2 ␮mol CO ´mϪ2´sϪ1 suggest that K was not a signi®cant limiting nutrient, 2 given the low availability of N (Fig. 1A). [mean Ϯ SD]. We observed no signi®cant difference in ϭ Collectively, these data suggest that prey additions photosynthetic rate among treatments (F7,20 0.316, P ϭ 0.938), and no relationship between tissue nitrogen shifted plants from being P limited under ambient con- ϩ content and photosynthetic rate (r ϭ 0.17, P ϭ 0.4). ditions to being N limited (or N K co-limited) when

prey were added. Ratios of N:P, N:K, and K:P in plants Reports DISCUSSION receiving extra prey were strikingly different from the ratios observed in a complementary similar ®eld ex- In wetlands, if plant tissue P Ͻ 1.0 mg/g and N:P periment in which plants were fed soluble nutrients to Ͼ 16 mg/mg, phosphorus limitation is implied (Koer- pitchers (Ellison and Gotelli 2002); the latter was an selman and Meuleman 1996). If plant tissue N Ͻ 20 experiment designed to mimic the impact of nutrient mg/g and N:P Ͻ 14 mg/mg, then N limitation is sug- deposition from atmospheric sources on pitcher plants. gested (Koerselman and Meuleman 1996). Olde Ven- In the current experiment, S. purpurea shifted from terink et al. (2003) further assessed the importance of K limitation in wetland plants. They suggested K may being relatively more P-limited with ambient prey in- be limiting if its concentration in plant tissue is Ͻ8 puts to being relatively more N limited when prey were mg/g. Critical ratios indicating P or PϩN limitation are added (Fig. 2). Although pitcher plants accumulated N:P Ͼ 14.5 mg/mg and K:P Ͼ 3.4 mg/mg; for N lim- both N and P with prey additions (Fig. 1), P appears itation, N:P Ͻ 14.5 mg/mg and N:K Ͻ 2.1 mg/mg; and to have been taken up at a relatively faster rate, so the for K or KϩN-limitation, N:K Ͼ 2.1 mg/mg and K:P N:P ratio fell in the fed plants relative to the unfed Ͻ 3.4 mg/mg. Relatively high levels of nitrogen de- controls (Table 2). In contrast, as soluble N (as NH4Cl) position occur in the northeastern United States (Ol- was added to pitchers in the Ellison and Gotelli (2002) linger et al. 1993), which may lead to a shift in nutrient study, S. purpurea shifted from being N limited to be- limitation from N limitation to limitation either by P ing P limited (Fig. 2). Changes in pitcher-plant stoi- alone or jointly by N and P (Morris 1991). chiometry appear to be controlled by both the quantity In our study, prey additions signi®cantly altered tis- and form of nutrient inputs. sue nutrient content and stoichiometry of Sarracenia Prey addition had no obvious effects on plant mor- purpurea (Tables 1 and 2, Fig. 1). Traditional measures phology, photosynthetic rate, or growth within a single of nutrient limitation (plant morphology, biomass, growing season. This ®nding also contrasts with results growth, and photosynthesis) did not change with prey found when soluble nutrients were added to S. purpurea addition, although our measurements were restricted to pitchers, which resulted in dramatic reductions of within-season growth. The mean concentration of P in pitcher diameter, increases in keel size, and increases control (unfed) plants was Ͻ1 mg/g (Fig. 1B), and the in photosynthetic rate (Ellison and Gotelli 2002), all corresponding N:P ratio of 17 mg/mg (Table 2) sug- of which occurred within a single growing season. This gested that these plants were P limited. In contrast, the lack of a growth response when prey were added is N:P ratios in all the other (fed) treatments were Ͻ12 consistent with results of Chapin and Pastor (1995), mg/mg, suggesting N limitation (Table 2). Potassium who also reported no effect of fertilizer or prey addition concentrations in all treatments were well below the 8 on aboveground plant biomass, number of leaves pro- Reports Zmr ta.19) and 1997), al. et (Zamora of mass leaf average or season, per duced NaH and 1742 niaeNadPcnetain fntin ouinaddt h ln.Ntin-iiainbudre ntetraypo are colors plot (2002); ternary the Gotelli in (2003). and boundaries al. Nutrient-limitation Ellison et plant. Venterink from the Olde data to of added are criteria solution squares the nutrient of on Colored concentrations based ¯ies/week). P and (2±14 N treatments indicate ¯y-addition circles, open a emnrlzdb h odwbfse hni is it than faster web N food because the perhaps by 1), mineralized (Table be tissue may plant ab- entirely by being sorbed than rather treatment with increased a ail bobdb ice ise ncnrs,am- (NH contrast, In monium tissue. pitcher web by food absorbed the rapidly by was the mineralized the P harvest the within in or that level suggesting web treatment levels date, by differ food not did the 1994). ¯uid pitcher for (Heard also ¯uid but pitcher plant, the for reproduction. or for growth stored future and that accumulated suggest Kethley being results were our and nutrients and excess 1997), Plummer al. et 1906, Schulze 1964, (Shreve store years readily sub- sequent in plants reproduction especially Pitcher and growth 1989). for nutrients Evans 1986, Moo- and ney (Field content photosynthetic nitrogen and leaves between of of capacity relationship prey) because photosynthesis well-known (i.e., of the rate nutrients the increased increase should that al. et predicts Givnish of and (1984) model (Ellison cost±bene®t pitchers The to 2002). added it Gotelli was as N rate, soluble photosynthetic when pitcher did increase not did prey 1976). rae ln ims nsvrlohrcarnivorous other several including in plants, biomass in- plant have experiments creased prey-addition hand, other the On F IG rycpue ytepthri eorentonly not resource a is pitcher the by captured Prey of addition the that surprised somewhat were We .Traypo lutaigNPKtsu aisof ratios tissue N:P:K illustrating plot Ternary 2. . 2 PO 4 surs.Crlsaedt rmtepe-diineprmn cretsuy:sldcrls min rycontrols; prey ambient circles, solid study): (current experiment prey-addition the from data are Circles (squares). 4 N ocnrto ntepthrwater pitcher the in concentration -N) arcna¯ava Sarracenia Tu 1988), (Thum M .WKFEDE AL. ET WAKEFIELD E. AMY (Christensen .purpurea S. arcnapurpurea Sarracenia . ouprlmtt h bobneo NH of absorbance the to limit found who upper (1984) the no Creelman with and contrasts Bradshaw This of tissue. ®ndings pitcher the by absorbed yoyasmithii Wyeomyia o omnso h aucit h aucitwsim- was manuscript The manuscript. the on comments for eoiinhsbe rdce ola otelong- the to lead to of predicted decline term been has and deposition 1991), de- (Morris N N sources in atmospheric increases from continental position with consistent is tions eprlcagsi ryaalblt.Testoichiom- The of availability. etry by prey caused in limitation changes nutrient temporal in shifts any overwhelm n a eeltegoigiprac fatmospheric of importance inputs. growing the monitor- reveal continued may ing and sources, atmospheric and prey lio 2002 Ellison u ne cnrl lnswr iie,whereas N by limited, limited N were P prey or additional were received plants that plants criteria, (control) these unfed (Gu of critical species some our these individual by whether Nevertheless, to 2004). yet applied sewell clear be can not limits is Venterinkratio It Olde 2003). 1999, al. nutrient and al. et predict et (Koerselman Bedford to level 1996, used community Meuleman be the can at ratios limitations anal- N:P:K that of proposed have ysis wetlands in experiments tion ea aveta inhabit that larvae teran etakJmKrgtie n h V clg a group lab ecology UVM the and Karagatzides Jim thank We eetppr htrve tde fnutrient-addi- of studies review that papers Recent ϩ Tbe2.Plmtto ne min condi- ambient under limitation P 2). (Table K Sarracenia b e is(ice)o obntoso NH of combinations or (circles) ¯ies fed .Cniun eoiinas may also deposition N Continuing ). .purpurea S. A and CKNOWLEDGMENTS eet uretipt rmboth from inputs nutrient re¯ects eronmsknabi Metriocnemus .purpurea S. ouain Gtliand (Gotelli populations clg,Vl 6 o 7 No. 86, Vol. Ecology, pitchers. 4 xrtdby excreted w dip- two , 4 NO È- 3 July 2005 STOICHIOMETRY OF SARRACENIA 1743 proved by comments from Dave Spiller and two anonymous of carnivorous plants to sunny, moist nutrient-poor habitats. reviewers. This research was funded by NSF grants 02±34710 American Naturalist 124:479±497. and 02±35128 to N. J. Gotelli and A. M. Ellison, and NSF/ Gotelli, N. J., and A. M. Ellison. 2002a. Biogeography at a EPSCoR grant 00±82977 to N. J. Gotelli. regional scale: determinants of ant species density in bogs and forests of New England. Ecology 83:1604±1609. LITERATURE CITED Gotelli, N. J., and A. M. Ellison. 2002b. 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