•r llll.l~-lli5C 16~9-of>ft-{>-lSOJ.tMl/O ''"111 \(1l'lh.'.l' L•'r'ni:ht <' 1?'17 bv W1l11Jm< & W1ll1ru Pnrm:~ u. L' " -\ DYHAMICS OF CARBON AND NITROGEN MINERALIZATION, MICROBIAL BIOMASS, AND NEMATODE ABUNDANCE WITHIN AND OUTSIDE THE BURROW WALLS OF ANECIC EARTHWORMS (LUMBRICUS TERRESTRIS) Josef H. Gorres, Mary C. Savin, and Jose A. Amador We conducted a laboratory study using soil cores to determine whether anecic earthworm (Lumbricus terrestris) burrow linings (the drilosphere) are sites for enhanced carbon and nitrogen mineralization and increased m.i crobial biomass and nematode abundance. We compared m.icrobial bio mass C, C mineralization rates, metabolic quotient, levels ofi norganic N (NO; and NH:), and nematode abundance over the course ofll weeks in soil &om earthworm burrows, bulk soil away &om burrows, and a con trol soil in cores to which no earthworms were added. Significant differ ences were observed in inicrobial biomass carbon, which was 38 to 84% lower, and carbon mineralization and metabolic quotient, which were 2.3 to 7 .5 and 5 .6 to 17.4 times, respectively, higher in burrow than in control soil. No significant differences were observed in these variables between bulk and control soil. In addition, nematodes were 3.7 to 6.5 times more abundant, and inorganic N levels 21 to 78% higher in burrow than in con trol soil, with no significant differences observed between bulk and con trol soil. Dynamics ofm icrobial biomass carbon and inorganic N followed the same general pattern in burrow, bulk, and control soil. By contrast, dynamics ofn ematode abundance, carbon m.ineralization, and metabolic quotient differed between burrow and both bulk and control soil, with peak values observed at 5, 7, and 11 weeks for nematode abundance, C rnineralization, and metabolic quotient, respectively. Our results suggest that earthworms may have an indirect effect on soil C and N dynamics by stimulating the activities of nematodes and their interaction with m.icro bial biomass in the drilosphere to a greater degree than is observed in soil that has not come in direct contact with earthworms. E ARTHWORMS increase rhe rare of nument re has been arrribured ro compematory microbial lease from bulk soils (Marinissen and de growrh resulrmg from earrhwom1s gr.1zi11g on Ruiter 1993) and affect the growth rates of plants microAora (Mannissen and de Rutter 1993) al in both agricultural and forested ecosystems though mucus excretions (Scheu 1991) a11J aera (Haimietal.1992;Woltersandjoergensen 1992). tion of burrows may also stimulate nucrobial ac Earthworms may contribute direcrly to nutrienl riviry. Direcc mechanisms are generally regarded mineralization through respiration and digestion as minor (Haimi er al. 1992), whereas mdirecr (Andren et al. 1990) and mixing litter wirh min mechanisms are believed to be rhe major compo eral soil (Cheshire and Griffiths 1989), or indi nent of rhe effect of earthwom1s on minerahza recrly by controlling the growth rare of microor cion (Marinissen and de Ruiter 1993). g:misms (Marinissen and de Ruiter 1993). The Earthworm burrow walk known as the stimulation of microbial activity by earthwom1s drilosphere, have phrsical and chemical proper c1e~ rhar are discinct from those ofrhe bulk soil Jnd D<pt of Ndlurdl Rnou""' So<nc<, Unrv<1S1tyolRhod< l•l•nd, Kin9•lon, RI0288t airer the manner Ill which water. soluces. and Dr Gouts 1i counpondmg duthor E·me1L [email protected] biora interact w1rh bmrow soil. l3urrow lmings Con1ubuuon # 5923 from 1he Rhod< l•l•nd As,,cultur•I bcP<nm<nl Sr.t,on. have been found ro have a narrowt·r range of pH R<t<>V<d F.b 7, 1997; OCC<pt<d M.iy14, 1997 and clay content than bulk soil, wirh le\·els of to- VOL. 162 - No. ') E:\ll TH\\.\)ll \I UURllO\\. .., -\='-P '\iLl!U[;-.;T ()y'\, \\\ICS tal and water soluble carbon two to e1ghr nmes The m~s wJter ..:oment of the soil (detemm1ed higher in burrow walls than in the :idJacenr bulk gra\·imemc.11Jv .lt I 05 C) at sJmplmg nme ranged soil (Stehouwer et al. 1993). Earchworrns may af from 0.27 co ll.3H g per g soi.I m·er the course of foct nutrient mineralization through the creation che expenment. correspond.mg to 60'"u and ~11" . of moist, nutrienr-rich microhabitats for smaller respectively. of the \\·acer-holding capac1ry or-rht• microbivorous organisms, such as nematodes. soil. which in turn stimulate microbial processes, en Sa111plh1,!! hancing mineralization. A laborarory study was conducted to deter The soil mixture was analyzed (in mplicuel mine whether carbon and/or nirrogen mineral for nematode abundance. soil resp1ranon ....o il ization is enhanced in earthworrn burrows and moisture, microbial biomass C, and morg:a111c 111- whether the burrows are sites of increased nema trogen (NOj -N and NH; -N) levels at the on,cr tode and microbial biomass density. The study of the experiment. Three earchworn1 and thrt'<" was conducted using anecic earthworrns (L11111bri control cores were sampled destructively after 111- ws terrestris) and packed, forest soil cores under cubation for 3. 5. 7. 9, and 11 weeks. The num conrroUed temperature and moisture conditions. ber of worrns and burrows in each core w.is We hypothesized that C and N mineralization recorded before sampling. In order to get \·aluc ... would be greater in burrow linings than in soil nor representative of rhe whole core. soil sample, affected by earchwom1 burrowing and that nema were obtained ar depths of0-5 cm, 5-15 cm. and rode numbers and microbial biomass would be J 5-25 cm. In cores conraining earthworms. s01I higher in burrow soil. was raken from rhe burrow walls, wirhin 11.5 un of the inside of the waJl (burrow so1l):and from Jt MATERIALS AND METHODS least 2 cm away from the burrow walls (bulk soil I A total of three samples per core (one from e.ich E:xpen·lllr111al Des(1?11 depth) were analyzed for soil moisture. C 1111ner Forest soil (Ap and C horizon) was collected alizarion, biomass C. and inorganic nitrogen. \nil in January 1996 from a maple-oak forest on a samples from different burrows \\·1th111 J pamcu Hinkley sandy loam soil (sandy-skeletal, mixed, lar core and depth wen: pooled for a1ulym. Tlw mesic, Typic Udorchent) at the Peck11am Fann quantity of burrow soil was !muted, Jnd tlw Research Facility of the University of Rhode Is amount ofs oil required for nematode .1bund.inct land, Kingsron, Rl. Ap and C horizon soils were determinations was large (20-25 g).Thus. for ne mixed {1:1, vol/vol) in the laboratory, stored in marode analysis. an equal amount ofs oil (burrm\. ·c the dark at 4 for 3 weeks. and subsequently bulk, or control) from each depth w1th111 a um: equilibrated at21-23"C for 1 week before rhe be was pooled for deterrninarion of nemarode abun ginning of the experiment. Mixing the soils was dance. necessary to ensure the physical stability of soil cores during the experiment. The soil mixture il1Cl/.!!,111ir .\'itn~!!Cll had an organic matter conrenr of7.8%, as deter lnorgaruc N (NH; and NO;) levels 111 sod mined by loss-on-ignition at 550 C for 4 h. were detem1ined by extracnon of I g (wet Thirty cores (30 cm long, 15 cm diameter) were weight) of soil \\ith 10 ml of2.\J KCl solution. prepared by packing the soil mixture into PVC tilcenng (Keeney and Nelson 1982). and colori cores to a bulk density ofl .1 g/cm3• A 5-crn layer metric analysis of the filrrarc usmg an automated of oak-maple licter collected from the same area nutrient analyzer (model RFA 300, AJpkem). of the forest from which soil was obtained wa5 placed on cop ofche soil 111 all 30 cores. Two adult C<1rbo11 .\/111crali.::-atit>11 R111c earthworrns (L11111briws tcrrestris) were placed in To detem1ine C mineralization rates . •1 each of 15 cores, with the other 15 cores serving known amount ofs oil (I g wet wt) was placed into as controls. Earthworm density was approxi a 20-ml glass serum \·ial, the \·ial stoppered with mately 110 wom1S/m2, within the range observed a rubber septum and cnmped wHh an alum.in um for temperate forest soils (Edwards and Bohlen collar. The sealed vials were incubated for 7 d.1y' 1996). The cores were placed on pbscic saucers in the environmcmal chamber 111 which the cort•, and incubated in che dark ac 18-20"C. The cores were scored. W c have shown previously rhac in received about 500 ml of water per week: half cubation of soil samples under these condit1011\ was applied to the bottom by fillmg the saucer, do~·' not result 111 J sig:mfic:rnc Jecline of oxygen with other half applied LO the top of each core. levels in the head,pace of rhe \"1Jls (Corre~ et .tl. 661'\ GORRES. S-\\"11'. .. \ND A.\Hl>OR Su1L Sl tE:--.:CE 1997). At the end of the mcubation period a 1.0- I3onferrom 1 test. All st:mmcal tests were e\·alu mL sample of the gas in the headspace oi the Vlal aced at the 95'\i, contide1Ke lt'\·el. was removed by displacement using an automated headspace sampler (model 7000, Tekmar). The RESULTS concentration of CO, m the headspace gas sam ple was measured \,.;ith a gas chromatograph Earchwom1s suf\;ved well dunng the first 3 (model 14A, Shimadzu) fitted with a Porapak Q weeks of the study, \\,;th all of the added wonns column (80/100 mesh, 10 ft). Carbon dioxide (six) recovered alive from the cores after incuba was converted to methane using a heated (- W0°C) tion for 3 weeks (first samplmg date). Four womlS Ni catalyst and an H, gas stream, and the resulting were recovered from all three cores after mcuba methane was meas~red with a flame ionization tion for 5, 7. and 9 weeks. and after 1 I weeks onlv detector. Injector, column, and detector temper one adult wonn (presumably a worm added 1m atures were 150°, 60, and 300°C, respectively. rially) and one juve11il<' \\'ere recovered. T\\'O Peak areas for CO~ were detennined by elec eanhwonn burrows per core \\'ere presem at 3 tronic integration. Conversion of peak area to and 5 weeks, after which four or more burro\\s mass ofc arbon dioxide was made by comparison were found per core .. indicating greatt'r worm JC with vials containing a known concentranon of tivity. C02• The soil had a relaavely low inmal microb1::il biomass C content, undoubtedly the result ot.. J\1icrobial Biomass Carbo11 mixing soil from Ap and C horizon (Fig. I). Mi Microbial biomass carbon was detennined crobial biomass C declint'd \\'ith time mall tn:at using the fumigation-incubation method Qenk ments throughout the expt'nment. S1g111ticanrh inson and Powlson 1976) using 1-g (wet wt.) soil lower microbial biomass C was found in burrO\\ samples in 20-mL glass serum vials. Following than 111 control soil on weeks 5. -. 9, and 11. The evacuation to remove chlorofom1 residues. the lowest biomass levels \\'ere ob~ef\·cd on \\ eek I I . ·c vials were sealed and incubated at 25 in the dark and these were 8..J.% of control \·alues. No \1~1111:.. for 10 days. At the end of the incubation period icant differences \\'t're observed between bulk and (0-10 days), the concentration of CO, in the control soil on any sampling date. headspace of the vial was measured as d~scribed The rate of carbon mineralization 111 burrm\ above. The air in the headspace of the vials was soil peaked afi:er incubation for 7 \\·eeks (fig. I subsequently evacuated and replaced with fresh and was 7 .5 times high<'r than m the control soil .. air five tin1es before incubation resumed for an \\'hereas carbon m111eralizanon rates 111 bulk Jnd other I 0 days. The concentration of CO! in the control soil \\'Cre constanr for the duranon ot the headspace of the vial was measured again at the experiment. Rates \\'er<' s1g111ficamly higher 111 end oft he second incubation period (10-20 days). burro\v than m control soil at 3, 5, 7. and 9 \\ eeks. The C0 -C produced during the second incuba Significant differences in C mi111::ralizarion r::ire 2 tion period (10-20 days) was subtracted from that were observed berween bulk and control soil only produced during the initial incubation period on week 3. The microbial metabolic quonent (0-10 days), and the difference was used to calcu (qCO,, i.e., the rate otCO. evolved per u1m n11- late microbial biomass C using a kF.c value of 0.-ttJ crob1a-I biomass C) 111 both -bulk and conrrol soils (Sparling and West 1988). was constant for the first 7 \\'eeks. 111creasing for the subsequent ..J. weeks (Fig. I). By contrast, 1Ve111c11ode E1111111erativ11 qC0 in burrow soil appeared to increase d1spro 2 Nematodes were extracted from the soil us porcionally with time, with a 7-fold increase after mg rhe sugar flotation method (Ingham 199..J.). 5 weeks and a I 00-fold increase after 11 weeks. At The extracted nematodes were stored ar ..J. C in week I I. metabolic quoriem was more tlun 17 the dark and counted using a dissection micro times higher in burrow than in control soil. scope within I week of extraction. No attempt Nematode abundance 111 burrow soil peaked was made to classify nematodes into trophic after 5 weeks and was signific:mtly higher in bur groups. row than in control soil throughout the expen ment (Fig. I). with values in burrow soil 3. 7 to Ci.5 Statistical A11alysis times higher than 111 control soil. NenlJtode Statistical comparisons with the conrrol soil abundance 111 bulk and control soil remained rel were made usmg a one-way analysis of variance. atively constant during the t•xperiment. with no Meam separation was accomplished using the significant difference~ observed bt'tween the'e VnL. 162 - No. 9 E:\R 11-1\n1R "1 BuRRn\t·~ >.:-..n NL'TR1E:-.. T rll :-.. \.\Ill .. , rnenr for ,111 treatments (Fig. I). Burrow soil h.1d significantly higher le\·els of inorga111c N than ·.c.; .30 control soil on weeks J. 5. 7. and 9. Values for 111- organic N \\·ere 21 to 90% higher in burrow than ~ 20 u in ~omrol soil. Significant differences in inorganic :":'t 10 N levels bet\\·een bulk and control mil were ob served onh- on week 5. The mean (::!:::S.D.) per ,, 0 centage or" morganic N accounted for by ammo ~·c..; 4 c min nium was 13.6 ::!::: 5.0, 9.0 ± 4.1. and 7.0 ::!::: 3.5 for burrow, bulk, and control soil. respectively . .."....'. 3 + u I 2 DISCUSSION "' u0 • "' The presence of eanhworrns in soil has been ::t 0 shown previously to reduce nucrobial biomas~ C .'..O.... 2.0 qC0 and increase C nuneralizacion a~ weU as le\"els of .! I 2 E inorganic Nin soil (e.g .. Wolters andjoergensen u 1.5 0 Burrow 1992: Ruz-Jerez t:t al. 1992; Bohlen and EdwJrds ...O:.:..t.' 1.0 e Bulk 1995: Dediegher and Verstraete 1996: Zh.111~ u 'i1 Control I and Hendrix 1995). Our results are generalh- m 0 "' 0.5 u good agreement with previous studies. These "::'t 0.0 studies, hm\"e\·er. did nor differenci:ite between 40 " Nematode burrow and bulk soil. The results of the present 30 abundance study indicate th.1t the effects of L. rcrrcscns on 1111J ·c; crobi:il biomass and C mineralization are re "' * ::":-' 20 micted to the drilosphere. Others (e.g. . Sce houwer et al. 1993) have shown chat the 10 drilosphere differs in pH. wacer soluble: orga111c 0 carbon, and clay content from :idjacent. bulk soil. 120 Inorganic The differences in dvnamics ofC and N mineral ·.c,; ization and fauna pr~vide further evidence ofc he + unique characcerisrics ofs oil thac has come in con "' 80 ....... z tact wich eanhworrns. O::t' It is worth noting th:it at the earrl1\\·om1 den 40 sity used m this study ( 1 10 individuals per m1). enluacion oft he effects ofe archwom1s on the en 0 2 4 6 8 10 12 nre soil (i.e. bulk + burrow soil) would not ha\·e Time (weeks) revealed any significant differences from che con rral soil. We evaluaced this by combining soil property \"Jluc:s for the sampling rime on which Fig. 1. Microbial biomass carbon (C-=), carbon mineral the greatest differences in nemacode abund.111ce itzoadteio anb ruanted a(Cnmcoen>, , amnde tianboorgliacn qicu ontitireongte (nq C(N002), +n eNmHa; l between control and earthwom1 creatmenrs wen.• 3 levels in burrow, bulk, and control soil as a function of observed. Values measurc:d for the bulk. x,. Jnd rtiomwe .a n('d) cinodnitcraotle sso isl;i g( n+i)f iicnadnict adtieffse sreignncifeic baenttw dieffeenre bnucre rhe drilosphere soil, x1• were weighed based on the cross-secnonal areas of che bulk and burro\\ between bulk and control soil. soil using che formula two treatments on any sampling date. Signifi cantly lower microbial biomass values co-oc where x is the :iverage property (or variance) for curred with significantly higher nematode abun che enc ire soil, .\.· i' the number ofe arrhwonm per dance in burrow soil relative co the conrrol soil in unit area. ris the r.i<lius ofburrcn\', and R 1s the d1\ weeks 5, 7. 9, and 11. ta11ce from che cemer of che burrow co che edge Levels of inorganic N (N03 + NH;) gener oft he visually affected are.1 (soil clearly darkened). ally increased for the first 5 weeks, remaining rel w1ch values of rand R of approxim.icely 0.3 .md atively constant for the remainder of the experi- 0.9 cm. re,pecnvely. Mean \·alues for all oft he 'oil variables calculated 111 rhis manner from earth mlr of dtsrurb.mce (e.g. . :\nderson .111d Dom5ch wom1 core dara are nor significandy differenr 1993). from control cores (P > 0.1 in all cases). This Dau on morganic.. d\·nJmtcs may also be m .inalysis messes further rhe localized effecr of rerprered JS supporting this .11rem:uive hvpothe e:mhwom1s on soil btora and nurrienr cycling. sis. Grazingornlicroorgamsn1S by nucrobi\·orou' The etfecrs of earthworms on soil C and N nemarodes in soil has been shown ro increase eh<'. mineralizacion are generally explained wirhin rhe release ofinorgaruc fom15 of Nin soil (e.g .. An conrexr of the "grazing" hyporhesis, which scares derson er al. 1981: Ingham et al. 1985) although char grazing of soil microorganisms by earth excretion of inorganic N by eanh\vOmlS c.rnnot worms scimulares compensatory growth, result be ruled our as a cause for enhanced levels of in ing in an increased metabolic quotient (e.g .. organic N in burro,,· soil. 1n the presem srudy. rht' Bohlen and Edwards l995; Wolrers and Joer enhanced release of inorganic N was obsen·ed gensen 1992: Marinissen and de Ruiter 1993). during the initial stages of rhe experiment when Our resulrs suggest thar an alternative version of nematode grazing was presumably decunatin~ rhe grazing hypothesis may be worth considering: the nlicrobiaJ communiry. Taken together. our char rhe creation of burrows by anecic earrh results suggest that nematodes grazing on micro wom1S resulrs in favorable conditions for nema bial populations in die drilosphere could be par rodes. and rhese members of the soil fauna are at tially controlling the dynamics of m1crob1al bio least partially responsible for grazing on microbial mass C and C and N mineralization. biomass and resulring increases in metabolic quo Although the e,·idence presented here rn!,! tient and inorganic N release observed in rhe gesrs indirect effects of earrhwom1s on C ~111d !'-. drilosphere. dynamics by altering the distribution of nema Involvement of nematodes is suggested by todes and rhetr grazing acnnrics in \Otl. our resulr dynamics of nemarode abundance, microbial bio are nor conclusive rcgardmg the mvokemem nr· mass. and C and N mmeralization observed in the nemarodes as grazer-. For example. although sig presem study. Increases in nemarode abundance nificant increases m total numbers of nem::irodt•, in burrow soil during rhe initial part of the exper were observed as microbial biomass decreased. 1 iment may be the resulr of rwo processes: move more conclusi\·e case could be made if data nn menr and/or reproduction. Nematode move rrophic group distribunon of nematode popub menr and aggregation is driven by CO, gradients rions had been perfom1ed. ;howing .1 concomi 111 rhe soil (Dusenbu1y 1983. 1987) and bacteriv r:inr increase in populations ofmicrobivorous ne orou< nemarodes have been shown by Griffiths matodes with declining microbi::il hiom.1" Jnd Caul (1993) to migrate to decomposing plant Senapari ( t 9n) has shown th:ir the preSt"IKL' rhe residues. Enhanced C mineralization levels ob earrhwonn L111rpirn 1111111rirri (Kinberg) t'nhancc-. served in burrow soil in week 3 oft he study could the abundance of nucrob1\·orous nematodes Ill have atrracred nemarodes. AJremati\·ely. rhe pres soil. Additional organisms may be i1n-oh·ed in ence of litter {anecic eanhworms line their bur grazing along with the nematodes. For example. rows wirb plant materials brought from the sur numerous studies ha\·e shown that grazing ofbac race) and earthworms (dead or alive) and terial populariom by protozoa in soil can have ef associated exudates could have resulred in in fects on microbial biomass .ind C and N mineral creased reproduction oft he nematode population ization similar ro thme ob-;erved tll the pn:senr in burrow soil. In eirher case, increases in nema study (e.g .. Wrighr er JI. I 995; Woods er al. 198~: rode abundance require food resources, which Rutherford and Ju m a 199~: 1n gham et :ii. 1985). could have been provided by microbial biomass. [n conclusion, our resulrs indicate that nema The greater rate of microbial biomass loss in the todes may ha\·e an important role as indirecr me drilosphere and the concurrent enhancemenr in di::nors of rhe effects of earthworm> on C and J\. C mineralization when nematode abundance was mineralization in soil. increasing is consistent with the hypothesis that nematodes are grazing the microbial community. ACKNOWLEDGMENTS The metabolic quotienr of drilosphere soil in This research \\·as spomored. 111 part, by the creased dramaticalJy subsequent to peaks in ne R.hode Island Agriculrur:il Experiment Sunon lllJtode abundance and C mineralization. Such and by a grant from the USDA/Natinml Re mcreases in metabolic quoriem luve been inrer se.uch lniriari\·e Compertrt\"L' GrJm~ Program. pn:ted as reflecting rhe diversion of energy front \Ve thank the sruJe1m of" NR.S 492 (IC Conde. growth and reproduction to maintenance ;is ::1 re- S. Aubois) .md S. IJ~rron for technical help. VOL. 162 - No. 9 EARTHWORM BURROWS .-\ND NUTRIE:"<T 0Y'-'"u\llCS REFERENCES C. Cokman. 1985. Interactions of bactena. iiingi. and theu nematode grazers: Effect on numem c• Anderson, R. V., D. C. Coleman, C. V. Cole. and E. cling and plant growth. Ecol. Monogr. 55: 119-1-!ll. T. Elliott. 1981. Effect oft he nematodes :1crobe/oides Jenkinson. D.S. . and D.S. Powlson. 1' 176. The effern sp. and J\lesodiplogasrer i/1eririeri on substrate utiliza ofbiocicW treatments on merabohsm m soil-\' -\ tion and nitrogen and phosphorus mineralizaoon in method for measuring soil bionlJss. Soil Biol. soil. Ecology 62:549-555. Biochem. 8:209-213. Anderson, T.-H., and K. H. Domsch. 1993. The meta Keeney, D. R., and D. W. Nelson. 1982. Nitrogen - bolic quotient for C0 (qCOJ as a specific activity Inorganic forms. fo Methods of soil analysis. P.irt 2 2 parameter to assess the effects of environmental -Chemical and rrucrobiological properties, 2nd Ed. conditions, such as pH, on the microbial biomass of A. L. Page, R.H. Miller, and D. R. Keeney (t:d~.J. forest soils. Soil Biol. Biochem. 25:393-395. ASA-SSSA, Madison, WI, pp. 643-698. Andren, 0., T. Lindberg, U. Bostrom. M. Clarholm, Marinissen.J. Y. C., and P. C. de Ruiter. 1993. Con A. C. Hannson, G.Johansson,J. Lagerlof, K. Paus tribution of earthwom1s to carbon and mrrogen n· tian,]. Persson, R. Petterson,J. Schnurer, B. Sohle cling in agro-ecosysrems. Agne. Ecosy>. Ennron. nius, and M. Wivsrad. 1990. Organic carbon and .\7:59-74. nitrogen flows. Ecol. Bull. 40:85-125. Rutherford, P. M., and N. G.Juma. 1992. Influence of Bohlen, P.J., and C. A. Edwards. 1995. Earthworm ef soil texrure on protozoa-induced mineralizanon oi fects on N dynamics and soil respiration in micro bacteria carbon and nitrogen. Can. J. Soil. Sci. cosms receiving organic and inorganic nutrients. 72: 183-200. Soil Biol. Biochem. 27:341-3.\8. Ruz-Jerez. B. E .. P.R. Ball. and R.. \V. Tillman. 19'12. Cheshire, M. V., and B. S. Griffiths. 1989. The influ Laboratory assessment of nutnem release from :i ence of earthworms and cranefly larvae on the de pasture soil receivmg grass or clon•r r.:s1Jue>. m the composition of uniformly 14C labeled plant mater presence or absence of L11111briw; mbcl/11s or L1.<c111.1 ial in soil.J Soil. Sci. 40:117-12.\. fr11d,1. Soil Biol. Biochem. 24: I 52'J-15.3.\. Devliegher, W., and W. Verstraete. 1996. L11111l>riws Scheu, S. 1991. Mucus excr.:non and carbon rurnm-.:r • rerrrstris in a soil core experiment: Effects of nurri of endogeic earrhworms. Biol. Fcml. Soils 12:21- ent-ennchment processes (NEP) and gut-associ 220. ated processes (GAP) on the availability ofp lant nu Sen:ipari. B. K. 1992. Interactions between soil ne11i.1- trients and metals. Soil Biol. Biochem. 28:.\89-496. rodt's and earthwonns. Soil Biol. l310chem 2.J: Dusenbury, D. B. 1983. Chemotactic behavior of ne 14.\ 1-1.\.\.\. matodes.]. Nematol. 15:168-173. Sparlmg. G. P .. and A. W. West. 1988. A direcr t'X Dusenbury, D. B. 1987. Theoretical range over which traction method to esmnate s01l microbi.11 C: C.1h bacteria and nematodes locate plant roots ming car braoon 111 sit11 using microbial resprranon .md "t; l.1- bon dioxide. J. Chem. Ecol. 13: 1617-1625. beled soils. Soil Biol. B1ochem. 2U:337-.3.\.3. Edwards, C. A., and P. J. Bohlen. 1996. Biology and Stehouwer, R. C., W. A. Dick, and '>.J. TrJmJ. 111•1_; ecology of earrhwonru, 3rd Ed., Chapman and Characterimcs of earthwom1 burrow hnmg afTcn Hall, London, UK. ing arrazine sorpcion. J. Environ. Qua!. 22: 1S1- Gorres, J. H., M.]. DiChiaro, J.B. Lyons. and J. A. 185. Amador. 1997. Spatial and temporal patterns ofs o.ii Wolters. V .. and R. G. Joergcnsen. 1992. Microbial b1ological activity in a forest and an old field. Soil carbon rumover m beech forest soils worked b,· Biol. Biochem. (In press) .Aporrecrodca caligi11os11 (Savigny) (Ohgochaeta: Lum Griffiths, B. S., and S. Caul. 1993. Migration ofbacte bricidae). Soil Biol. Biochem. 2.\: 171-177. rial feeding nematodes, but not protozoa, to de Woods, L. E .. C. V. Cole, E.T. Elhort. R. V. Ander composing grass residues. Biol. Fertil. Soils 15:201- son, and D. C. Coleman. 1982. Nitrogen rramfor 207. mations in soil as affected by bacterial-microfaun.11 Haimi, J., V. Huhta, and M. 13oucelham. 1992. imeracaons. Soil 13101. Biochem. 1.\:93-98. Growth increase ofbirch seedlings under the mflu Wright. D. A .. K. Killham. L. A. Glover, Jnd J. l. ence of earrhwonm-A laboratory study. Soil Biol. Prosser. 1995. R.ole of pore size looaon 111 dctt·r Biochern. 2.\: 1525-1528. mming bacterial acnvHy dunng predrnon by pro Ingham. R. E. 1994. Nematodes, ill Methods of soil tozoa in soil. Appl. Ennron. M1crobiol (,I: analysis, part 2: microbiological and biochen11cal 3537-3543. properties. R. W. Weaver, J. S. Angle, and P. S. Zhang, Q. L., and P. F. Hendrix. 1995. E:irrhworm Bottomley (eds.). SSSA Book Series, no. 5. SSSA. (L11111briws nibcllus and .-tporrccrod11 Cc1/(l/itrt1s11) efl~cc­ Madison, WI, pp. 459-490. on carbon flux 111 s01l. Soil Sci. Soc. Am. J. Ingham, R.. E.,J. A. Trofymow, E. R. Ingham, and D. 59:816-823.