Variation in Microbial Biomass and Activity in Four ...

Reprlntcd fiorii the So11,YcrcJriceA'ocrc~!~ ofAtr~r~rrrtr.Joumu~ Volurnc 60, no 2, Marclr -Apr~l 1990 077 South Segoe Rd Madrson, WI 517 11 USA

.

Variation in Microbial Biomass and Activity in Four Different Wetland Types PHer M. CrcrRrnan,* Gay 6 . Hanson, Erik Kiviat, and Gretchen Stevens ABSTRACT Functional evaluation of wetlarrds iri nutrient cycling, water quality maintenance, and wetlarrd ssrrstruction and restoration contexts rcquires knowledge of diEerences in microbial ~ ~ r w e s sbetween es di&rent wetlarad t y p s arrd understanding o f the nature and extent of variation in these prwesses within a given wetland t y p . In this study, we measured a suite of microbial variables (micmbial bicbrnass C and N corntent, denitrification enzyme activity, ptential net N mineralization and nitrification, rand soil respiration) that are indices of wetland nutrier~t cycling arid water quality nnaintenance functions in four diEerent wetland t y p s (calcareous ferrs, red rnapIe swamps, woodland pmls, and wet clay meadows) in eastern New York state. Total soil C and N content, water content, pH, water-table levels, and groundwater NHZ , NO,, and electrical conductivity were also n~easured.The clay ~neadowwetlands were drier and bad lower lebels of orgarric matter and most ~nicrohialvariables than the other wetlarld typs. Site-to-site variation within tile fens was very high and was not strongly controlled by water-table levels. Organic tnatter cc~ntentand 16' status appear to be strong regulators sf microbial biomass and activit:, in fens, Red maple swanlps srrd woc~rdlandpools had similar levels of n~ost~nicrobial variables. Variation within these wetland t j p s was controlled by hydrology a ~ r dorgarlic matter quality. The suite of nricrobial variables that we meawlred identified ptential functirs~ralcliEerences between wetland t y p s and should be l~sefulfor casmparisoas sf the water quality mai~ttenalrcevahre s f difiiferent wetlands and for. Funrtional evaluation o f altered or restored sites.

ICROBIAL, PROCESSES

are critical to several aspects

of ecosystem structure and function. Microorganisms are responsible for the degradaticjn of organic mate-

rials and the cycling of nutrients csrltalned thereirr, and are therefcjre a critical cc~ntrollerof plant productivity irz wetlands (Mitsch and Gcosselink, 1986; Wetzel, 1992)Several microbial processes esntrihrlte to the water quality maintenance value of wetlands (Johnston, 1991). Denitrifieatlon i s thought to rnake wetlands an irnportant sink for excess N rnoving f'rorn intensive upland land uses toward streanls and groundwater (GroEman, 1994). Microbial populations can immobilize signlfieant quantities of a variety of nutrients as well as organic pesticides and industrial pctllutants (Smlith and Paul, 1990). Microbial populations can also be irnportant degraders of organic po1lut;;ants (Alexander, 1994). Variation in microbial processes within and between wetlarlds i s caused by a variety of factors including organic matter quality and quantity, hydrology, plant type and dynamics, and disturbance, both natural and anhrc~pogenic(Bowden, 1987; Findlay et al ., 1990; Verhoeven et al., 1990; Morris, 1991; Patrick and Jugsujinda, 1932; van Vuuren et al,, 1992; Bridgharrr and Richardson, 1993; Day and Megonigal, 1993; McKee and McKevlin, 1993; Borga et al . , 1994; Walbridge and P.M. G r o h a n and G C Hanssn, Inst of Ecosystem Studles, Box AB, Mrllbrook, NY 12545; E. K~viatand G Stevens. Hudsonra, Ltd., Bard College Field Sut~on,Annandale, NU 12504 Rccelved 17 May 1935 *Correspn,I~ng author (capg@vm marlst edu) hblished rn Soil Sci. Soc. Am. J . 60:622-629 (1996)

Lockaby, 1994). Different wetland types should exhibit distinctive patterns of microbial activk)., because wetland ecasy stcms are the integrated product o f rnultiple environmental factors, However, variation witlrin a given wetland type rnay also be quite high (Johnston, 16393: Brinson, 1993). Determining i f there are sy sternatic diRerences irr nricrobial processes between diRerent wetland types, and understanding the nature and extent of variation irr these processes within a given wetlalrd type, would be useful for functional evaluaticlr~of wetlands it] nutrient cycling, water quality maintetlance, and wetlanci esnstruction arrd restoration contexts. In this study, we measured a suite of ~nicrohialvariables that are indices of irnportarlt wetland nutrient eycling and water quality maintenance ft~nctions.We rneasured microbial biomass C and 16' contelrts, which are indices of the capacity o f an ecosystem to support rlutricr~t cycllng and biodegradation functions (Srrritk and Paul, 1990). We nreasured denitrificatlorr enzyrne activity as an index o f the denitrification capacity of di8itererrt sires. This activity has besrr found to be strongly related to the annual denitrification rare in soils (Groffl~ranand Tiedje, 1989). Additional variables rneasured included potential net N rnineralizativn and nitrification, and soil respiratio~z.The supply of N thrtough minerali~atiorris an important component of soil krtility arkd potential net nitrification is often used as an iriciicator of N availability ln ecosystems. Ecosystenss (including wetlands) with high net nitrification are thought to be snseeptit-sle to high N losses if disturbed by harvest, fire, blowdowns, or other perturbations (Vitousek et at., 1982: Pastor et a]., 1984; Aker et al., 1989). Sr~ilrespiration is a useft11 index o f overall soil biological activity (Paul and Clark. 1989). Our objectives were to: (i) determine if diRerent wetland types have distinctive patterns of microbial activity, (ii) quantify variation in rnricrobial biomass and activity within difirent wetland types, and (iii)tlnderstand the factors regulating variation witkin ~lrldarnong wetland types.

MATERIALS AND RIETHODS Study Slites 'The 12 wetlands (study sites) are in Dutchess County ( I I ) and southern Columbla County ( I ) , New Vcvk (Table 1). The study sltes represent four widespread wetland types: calcareous fens, red maple swamps, wet clay rneadows, and intermittent woodland pools. Mean annual precipitation averaged over five weather statiorls in Butchess County is .= 1M crn, ranging from 6.6 to 10.2 cm nrs-' ((Tho~nas,1985). Mean annual temperature at Poughkeepsie, .= 10 to 50 k r x l frorn our. study sites, is 9.5"C (Thomas, 1985). Calcareous .fens are here defined as groundwater-fed. often slop~ng,perenrlially saturated meadows that lack a closed tree canopy and coritaln calcicoles (Mo~kir;,1994).Although rnany investigators restrict their detinition of fens to peatlands, ather investigators, especially those in the U, S, Northeast, have found floristic and Functional similarities between calcareotls

(;KOI*EMAh f 1 21

623

t A R I A 1 ION I N Mrk,l'[ ,AND MICRQPDIAI. BIOMASS A N D ACTIVIT V

Table I. I)cscr.iption\ of the 12 wetlarrd \ile\ r~rcdfor tllin study.

Site

Soil seric\

Area

Soil

classification

ha

Fens 8

> 100

'100 24 21 .I00

Sun silt loam Carlisle muck Sun silt loam I.irnerick silt loam

Sun silt loa~rl Carlisle muck Carlisle muck

3

1%

I,ivirrgstorr silty clay loarrr Rnynham silt loam 1 i\ ingstorr silty clay loam Kingsbury-Wlrinebeck complex

1 2

79). Clay 111cadous clrfjer frorn fen\ 111 b e ~ n gsal~gcnou\ ( runof fed) r'lther than groundwater fcd and rn havrng ic\\ c~-rlcareou\\ o i l and water than fcns M.i)otllrrrrtl poc11.c ( somerlrnes called r~umalpool.r, c. g. , Reschke, 19963) are s n ~ a l l(often 1 blue method was used to quantlb NH r' arld a C'd reductioniN I -napthylethy lens d i a m ~ n edihydrochloride (NEDD) rl~ethod was used to quantify NO? plus NOz (Alpken1 Corporat~on, 1984).

624

SOIL, SC'I SOC AM J , VOI. 60. MARCH- APKII 1996

Soil Sampling and Analysis Six so11 samples &ere takcn at eaeh site on ~ U ' O siirrlpling dales. The first groui, of samples was takcn on 1 3 and 19 May and the scconcl grottp was taken on 12 and 14 July 1994. Two sanlples (0-15-cln depth) *ere taken within 1 rn of each ot the three wcater-table wells at each site, for a total of stx sarllples per site per date. Because "re sarnpling desrpn was keyecl to the locar~onof the water-table rnonitnring wells, we were able to explore relationsh~psbetween water-table levels and \oil varlablcs within each site ( n = 3) land within each \vetland tjpe ( n = 6); three sites pcr type, three wells per site). Sarnples were stored st 4°C hetween sarnplirlg and analysis (4 rnrn) and held at field moisture f o r all analyses, Sorl water content was determirred gravinretrica11y and sod pH was measured with ,a glass electrode In a 1 :2soili'water slurry. Soil total C ar-rdN csnterrts were nleasured using a Carlo-Erba NA 1500 CNS analyzer (Carlo Erba Strumentazione, Milan, Italy). All results arc expressed on a per grans of dry soil basis. Dearitrrlicat~onerazylne activitj w a s measured ustng rille shofl-term anaerobic assay cgescnbed by Sl~litlcrarrd Tiedjc (1979). Sicved soil% were arrrerrcled with NO, (100 nag N kg '1, dextrose (30rllg kg I ) , cklornmphenlcd ( 10 r~lgkg I ) , and acetqlene ( 10 kPa) arld were irrcub;tted urlder anaerobic condrbions for 90 min. Gas qaramples were taken at 30 and 90 mln, stored rn evacuated glass tut?es, and analy~edfor N,O by electron capture ga\ chrorraatc)g~aphy. Microbial biornass C and N conterrt was measured using the chlidrofornr I'urnigatiorr--inc~1bat1c~ia rrrethod (Jenkinson and Powlson, 1936).Soils were ft'umigaredto kill bznd lyse lllicroblal cells rn the canaple. 'The furnipatcd sample was roloculated wrth fresh soil, and rnicroorganisrrls frorrr the fresh soil grcw vigorously using the killed cells as substrate. The f'lushes of CO? anal 2 M KC1 extmctable ra~ineralN (NH6 and NO1 ) released by the actively growing cells during a 10-d incrabrat~on ;it field mt~isriurecontent were assmra~edtc:, be directly proportronal to the arrrount (sf C and N in the ~aaicnjbialbiomass of the orfgirral sanrplc. A proport~onalr(yconstant (0.45) was used to calculate $rla)~~las?; C fro111 the CO? Bus11 (Jenbnson 2nd Powlson. 1976)-Carbon dloxlde was measured by thermal conductivity gas chromatography. Maneral N ilush data were not corrccred wit11 a propar-tionality cconstirnt. Minerdl N and 602prtrducrion were also measured In u n h xrrignteai ""corrtrc~I'~ samples.. 'These incubations provided estimates of soil respiratron a~adpotential net N mineralization and nitrificatia3nz. Soil respiration was q~lantifiedfrom the arnount of Co, evolved during the 10-d incubation. Potential net N rrrrneralization and llitrificatisn were quantified from the acenmulatiorr of NHd plus NO3 and NO; alone during the 10-d incutoation. Anmma;;Pniu~rtand NC)? were arra:asured as described above.

Statistical Analysis Data were analyzed with tire analysis of variance (ANOVA) routine oftlne St~atisticalArlalysis System (SAS Institute, 1988). To test for diEerences among wetland types, wetland type, sampling date, a r ~ dtype x date interacticon were used as tnain eRects in an ANOVA model. Separate analyses for each date were used where type x date interactions were significant. To test for diRerenees between sites within each type, separate analyses were run for each type, with date, site. and date x site interaction us main eEects. Separate analyses for each date were used where dare x site interactions were significant. Significant type x date and date x site interactions were rare and are all explicitly indicated in the text, tables, and figures.

'I'able 2. Summary water-Vdble data from 12 sampling dates betweerr 5 May aid 21 Sept. 1994. Wetland t y p s with digerenl codes are significantly didhierent at P < 0.85. Site

Mean

Standard errcar

Minimum

Maxinlurn

Range

cm IFrom ground surface

Red maple 1 2 3

A -3.7 I,O 0.3 A -- 32.6 - 19.9 12.3 B -26-8 -29.6 ---48.1 A 17.1 -- 14.4 15.0

A

0.9

1.2 0.7

- 21.7 - 5.0 - 4.4 B

2.0 3.7 1.7 4.5 4.5 5.9

2.1 5.1 3.2

-

0 - 57.5 --- 4.2 C - 92.0 - 93.5 - 103.5 AB

- 12.0 -- 63.5 - 17.8

BC

QI:

4-3

26.0

41.9

- 2.3

4A.9 10.3 B 41.5

19 45.7

76.5 49-9

5.9

B

C

A

5.0 -- 1.0 --8.3

97.0 92.5 303.2

A

B 52 .$ 104.1 70.3

40.6 40.6 53.3

Relationship3s alnong \~:lriakles within ancf among sltes were ar~aljrec% by conlputlng Pearson arrd Spearr.ra;in correlation coeficients (SAS Institute, 1988).

A surnmal3; of all the water-ttible data (7"ahle 2) shows that the clay rneadow wetlands had lower ( P < 0.05) !mean water tables than the other wetland types, which were not digerent fr'rorn each other. The clay me.a4 OW wetlands also had the largest ( P < 0.05) range of watcrtable levels, whereas the fens had the lowest ( P < 0-05) range. The hrgl-rest ( P < 0-05)rnaxlrarurnp water-table ievels w e r e observed in the order of woodland poejls ftsllswed by red nraple swannps, fens, and clay rrreadows. There was no significant diRerence in rnrraxir~~urn watertable levels between the red srraple swarnps and the fens and between the fens and the clay meadows, There were few consistent diRerences in water chemistry :aa.mong the sites (Fig, I ). Woodland pools had higher ( P < 0.05) levels of NH 3" in groundwater than the other wetland types, which were nor different from each sther. The red nraple swarnps had higher ( P < 0.05) NO1 levels than the clay rneadows and wc>udlandpsols, which were not dieerent a'rsm eaeh other. Fen NO? levels were not distinct Crcsm any of the other wetland types. Electrical conductivity was in the order fens > red nnaple swamps > woodland pools (all diRerenees P < 0.65). Clay meadows were not distinct from fens or red maple swamps but were higher ( P < 0.05) than woodland psols. There was signif cant variation in water elremistry an-rsng the sites within each wetland type (see superscripts on bars in Fig. I for specific sig~iifieantdigercnees). Analysis of basic soil properlies shows that the clay meadow wetlands diger from the other wetland types. Soil tohl C, total N,and water ccDntent were lower ( P < 0.05) in h e clay meadow wetlands than in the other wetland types, which were not diRsrent from each other (Table 3). In saturated sites, variation in soil water content is strongly ec~ntrolled by soil c3rganie matter content and is thus not as good an ir~dieatorof site

C i K O I ; I ~ M , l N F 1 (21

2.5

2.0

:5

1.5

Water

E 63 EE

Table 3. Soil C , K, water content, arld pH in three replicate sites of four diRerent 14etlanaA types. Values for C , N, and pH are the rnean of six replicate sarnples taken at each s i k in spring I994 (n = 6). Ytllues for soil water content are the rnean of six replicate sarrrples taken at each site at two sarrrple dates in sprillg and srrlllnner of 1994 (n = 12). Wetlsrld types, and speci6c sites within ;;a \zeCland type, with diKerent Letters are significantly diEerent at ED < 0.05. --

sz 4-

625

V A R I 4 1 ION IN W l * r L A N D MICRC)BIAI, BIOMASS AN13 AC'TlVITV

1.0

Sire - --

'Total C

Total -N

content -

g kg-' 0.5

8.0

Fens 1 2 3 Red nlaple I

A

S9.9b 52. l b 426.03

.4 4.2b

3.8b 24.8a

PEI

-

A

4Wb S2Ob

880a

A

A

A

109.2b

7.0b

590b

A 7.4b 7,Zb 7.7a

R 6.2~

Wmdland pool 1 7'

&

3

Fig, I. [;roundwater t.4) NElt , (BP) NOT ,arnd ( C )electrical corrtluctivity in three replicate sites of Four diEere~itwetland t y p s . Values are the rrlesrr (stksrrderd error) of three replicate samples taker1 at three sarnplirlg dates in llre fall of 1994, Wetland g y p s , srartl \pcific sites withirr 8 netls~rdtype, with diRerent snwrscripts are qigriificarrtl? diRerent st P i:0.05.

wetness as water-table level. Eaclr wetland type had sigrrific;intly (P < 0.05) distinct soil pH in the order of fens > rcd m:aplk: > clay meadows > wt~ocllarrd pools (Table 3)- Soil water conterrt was lower (B< 0-05) irr Ju1y tharl in M;ty. Tliere was sign~tiieant ~arlationin basic soil prop3er-ties arnong sites within ei1-3c.h wetland ty pc (see Titble 3 for specific sigrrihcant d~ffererlces). Among the N-cycle variables measrrred, ~nicrobial

kiornass N and tlenitrification showed coherent irnd sirnilar patterns arnorag the clifferent wetland types, whereas poternrial arer N mir1eralizati61aand nitrification were nlore variable. Dcnitrification enzynle r~ctivity(DEA.Fig. 2a) and ~r~icrobial bionnass N (Fig. 2b) were slrrnilar in red inaple and woodl;tntl pool wetlarld types and were greater (P< 0.05) in these wctlarrci types than in fens or clay nrneadows. 'rhlh pattern was con~isteratat both sampling date?, for kionrass N bur in July the pattern for DEA was woodland pools > red rr~aple--- fens > clay rneadows (all direrences Y < 0.05). B,evels of DEA werc higher ( P < 0-10) in 5t11y than in hlay , whereas hionlass N showed an opposite ternporal pattern (P < 0.10), Potential rret N rarinerallzation (Fig. 2a) was in the order of' clay nltladcaws > uoodlanci pools .= red r-rraple sbvalngas > fens (all diEcrerrces P < 0.051, but wrihin-type 1 ariation was quite high for this 1 ariablc. Potential net raitrificiirion (Fig. 3k) was in the order of woodland pools = red rllaple swa~-\lps > fcrrs .= clay i~leadctwsand was less variable within each metland type (all diEercnces P < O . 0 5 ) , Both ~nirieralizatlon(8"" < $9.05)alld nirrilication (F' < utchess County Dep. of Planning. Porrghkeepsie, NU. van Vuuren, M.M.I., R. Aens, F. Rerendse, and W. De Visser. L992. Nitrogen mineralization in heathland ecosysterns dominated by d~fferentplant spcies, Biogewhemistry 16:151- 166. van Wirciun.1, G . 1W3. An ecosystems approach to base-rlch freshwater wetlands, with spcial reference to fenlands. Hydrobiology 254: 129-.153. Verhoeven, J.T.A., E. Maltby, anc! M.B. Schmitz. 1WI. Nitrogen and phosphoms mineralization in fens ancP hogs. J . Ecol. 78:713726. Vcrhoeven, J.T. A., and M.B. Schmitz. 1991. Control of plant growth by nitrogen and grlrospborus irr ~nesotrophicfens. Biiogecxbem~stry 12: 115-148. Vitousek, P.M., J.W. Gosz, C.C. C'rrier, J.M. Melillo, W.A. Reiners. and W.L. T d d , 1982. A cc~mparatlveanalysis of ptential nitrification and niirrate mobility in forest ecosystems. Ecol. Monogr. 52: 155- 1'77. Walbridge, M . R . , and B.G. Lcxkaby . 1994. EEects of forest management on biogeochemical functions in southern forested walands. Wetlands 13: 10- 17. Wassen, M .J., and A. Barendregc. 1992. Toptjgraphic psition and water chen~istnyof fens in a Dutch river plain. J . Veg. Sci. 3:M7-456. Wetzel, R.G. 1992. Wetlands as nletabolic gates. J. Great I.akes Res, 18:529-532. Zak, D.R., and D.F. Grigal. l Wl . Nitrogen mineralization, nitnfication arld deniitrification in upland and wetland ecosystems. %culogia 88: 189--196. Zak, D.R., D.F. Grigal, S. Gleeson, and D. Tllmmn. 19W. Carbon and niitrc3gen cycling during rpld-field success~on:Constraints on plant and rnicroh~alblomass. Wiogecxlremisrrlc, 1 1 : 1 1 1 - 129.