bethlenfalvay and schuepp. arbuscular mycorrhizas and agrosystem stability -curso

7/30/2019 Bethlenfalvay and Schuepp. Arbuscular Mycorrhizas and Agrosystem Stability -CURSO

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Arbuscular mycorrhizas and agrosystem stability

GJ. B e t h l c n f a l v a y a n d H . S c h e p p 1U S Dep. ofAgriculture, Agrie. Research Service, Horcitltitral Crops Research Lab, Corvalts, OR 97330, U S ASwiss Federa! Research Stalion. CH-8820 Wdenswil, Switzerland

Introduct ionA n a g r o s y s t e m c o n s i s t s o f p l a r o o t s , t h e s o i l m i c r o f l o r a , t h e s o l f a u n a a n d t h e a b i o l icg c o c h e m i c a l so i l m a l r i x . P l a n t shoots, as i t s s o u r c e o f e n c r g y , a lso fo rm a n i n t e g r a l p a r o f t h es y s t e m . In k e e p i n g w i t h th e ro le o f p l a s a s p r o v id e r s o f f ood a n d f i b e r, f u n c t i o n s o ' f u n d a m e n t a lsocietal i m p o r t a n c e , m e ag r osys t e m h a s b e e n t r a d i t i o n a l l y u scd , t r e a t e d a n d e v a l u a t c d f rom aphylocen t r i c a n d e d aph i c p o i n l o f v i cw in ag r i cu l t u r e . O n a sca le o f pr ior i t ics , th e soil h a s a l w a y sl a k e n s e c o n d p l a c e , w i i h i t s f u n c l i o n o f s u p p o r t s u b o r d n a t e l o m a l o f ih e p l a , t h e p r i m a r yp r o d u c e r . T h i s p e r c e p t i o n i s u n d e r g o i n g r a d i c a l c h a n g e i n o u r t i me s . W e n o w r e c o g n i z e ih ei m p o r l a n c e o f soi l n o t o n l y a s a n a g r i c u l t u r a ! ' r e so urc e base' (Stewart e t al . , 1991), b u l a s ac o m p l e x , l i v i n g , an d f r ag e sys te m i ha t m u s b e pro lec ted ( R e gan o l d et al. , 1990) a n d m a n a g e d fo ri t s o w n sake ( P i e r cc a n d La l , 1991) to g u a r a n i e e i t s l o n g - t e r m s t a b i l i t y a n d p r o d u c t i v i t y .Arliculated sc en t i f i ca l ly in ihe ear ly 1980s ( Bezd ic ek and P o w e r , 1984; J a c k s o n , 1980; R o d a l e ,1983), s u s t a i n a b i l i t y has a l o n g h i s t o r y in a g r i c u l t u r e ( H a r w o o d , 1990), a n d h a s d e e p r o o t s insoc ie la l con se i ou sn e s s a l so .

In agriculiural research, th e goals o f sus ta inab i l i t y m a y b e s u m m a r i z e d in their briefest form as' m x i m u m p l a p r o d u c t i o n w i th a m n i m u m of so i l loss'. W i t h i n t h i s c o n t e x t o f b a l a n c e da g r o s y s te m i n p u t s a n d o u t p u t s (Horn ick and Par r , 1987) , th e ro le o f t h e a r b u s c u l a r - m y c o r r h i z a lf u n g i ( A M F ) h a v c b c e n describcd as t h a l of a f u n d a m e n t a l l i n k belween pla and soil( B e t h l e n f a l v a y a n d Li n d e r man , 1 992 ; M i l l e r a n d J a s l r o w , 1994; O'Neil el a l . , 1991). In k e e p i n gw i t h i ts i m p o r t a n c e , th e s y m b i o c as soc i a l i on b e t we e n A M F an d t h e i r h o s l p l a s a n d h o s l soils,an d its i m p a c t on agrosystem stability, is c ur r en t ly subject lo intensive investigalion. This w o r k hasbeen r e v i e w e d w i l h f o c u s on : ( 1 ) p l a g r o w i h a n d p l a n t e c o l o g y ( Bar e a a n d Jeffr ies, 1994;Be t h l e n fa l vay , 1 992 ; S i e ve r d i n g , 1991), (2) p l an t he a l t h a n d b i o c o n t r o l ( L i n d e r m a n , 1992, 1994;


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S c h o n h e c k a nd De h n e , 19 89 ), a nd (3) c u l t u ra l ( Jo h n so n a nd P f l eg e r , 19 92 ; Ku r l e a nd P f l e g e r ,19 94 ; M i l l e r a n d J a s tr o w , 1 99 2a ) a n d c n v i r o n m e n t a l ( S y l v i a a n d W i l l i a m s 19 92 ; W r i g h t a n dM i l l n e r 1994) p lant s t ress . R e c e n t l y , p e r h a p s i n s p ir e d b y th e i m p a c t o f s u s t a i n a b i l i ty , t h e A M Fh a v e a lso c o m e t o l i fe i n t h e r e v i e w l i t e r a t u r e a s soif s y m b i o n t s a n d a g r o s y s l e m s t a b i l i z e r s( B c l h l e n f a l v a y a n d Svejcar , 1991; F inlay a n d S o n d e r s t r ' m , 1992; Miller a n d Jastrow, 1992b;Tisda l l , 1991) . But no a t lempt had becn m a d e so fa r to in tg ra te the i n f o r m a c i n a v a i l a b l e o n t h einteractions b e l w e e n spec i f i c AMF i so la t e s and specif ic groups o f soil biota w i t h agrosystemstablity.

T h e p u r p o s e o f th is c o n t r i b u t i o n is to d i s cus s th e c u r r e n t c o n c e p t o f m y c o r rh i z a l e f f ec t i v enessan d lo r e f ocus i t by m a k i n g it applicable n o t o n l y to the host p lan t bu l to t he entire agrosystem,w i t h i n the contex t o f sus ta inab i l i ty in agr i cu l ture .Mycorrhizal effciency and benefts to the agrosystem: changing viewsT h e c o n t r i b u t i o n s o f A M F i n n a t u r a l o r d i s t u r b e d e c o s y s t c m s a n d i n e x p e r i m e n t a t i o n u n d e rcontrolled cond i ti ons have been t radi t ionally measured by plant response (Asai, 1943; G e r d e m a n ,1968; Jeffr ies , 1987; Peger an d Li nderm a n , 19 9 4 ; S c h l i c h t , 1889; S t a h l , 1900). Th e m o r e anA M F w a s able to i m p r o v e p l a n t g r o w t h r e l a t i v e to o t h e r i sola tes u n d c r a g i v e n s e t o f c o n d i t i o n s ,th e m o re ' e f f ec t i v e ' i t w a s said t o be . I n t u r n , th e be t t e r a n a rb usc u la r m y c o r rh i z a l p l a n t coulda p p r o x i m a t e g r o w t h b y a n o p t i m a l l y f e r t i l i z e d n o n - a r b u s c u l a r - m y c o r r h i z a l p l a n t ( A b b o t a n dRobson, 1991) , th e m o re ' bene f i t s ' i t w a s said to der ive f rom its s y m b i o t i c s ta tus . These benef i t s( m y c o t r o p h y , o r m y c o r r h i z a l d e p e n d e n c e ) w e r e e v a l u a t e d in t e r m s o f g a i n s d e r i v e d f romm y c o t r o p h i c P i m p o r t a g a i n s t th e p r i c e p a i d in r e d u c e d c a r b n b y t h e p l a n t to s u p p o r t i t sobl iga to r iJy b i o t ro p h i c e n d o p h y t e (Fi t ter, 1991; Koide, 1991).

Suc h a n a na ly s i s o f cos t -benef i t r e l a t i o n s h i p s f rom t h e p l a n t ' s p o i n t o f v ie w c o n t i nes t o be o fi n t e r e s t to a g r ic u l t u r e a nd a bo v e-g ro und ec o lo g y , a nd i s p a r t i c u l a r ly a p p l i c a b l e t o a d e mon s t r a t i ono f h o s t - e n d o p h y t e r e l a t i o n s h i p s u n d e r th e c o n d i t i o n s o f t w o - c o m p o n e n t a g r os y st em s t h a t cons i s lo n ly o f t h e m y c o r r h i / . a a nd t h e s l e r i l ized so i l u sed i n m o s t m y c o r rh i / . a e x p c r i m e n t s . In the f ie ld ,h o w e v e r , th e r e l a t i o n s h i p b e t w e e n h o s t p l a s a n d A M F is a l t ered by the other b io t i c c o m p o n e n t eof the agrosystem {Fitter, 1985; Het r i ck et al. , 1988; Saf i r , 1994), w h i c h p e r m i t measurablebenef i ts to accrue to the p lant on ly un de r par t i cula r con di t ion s o f g row th (F i t t e r , 1986) .

T h e c x t en t t o w h i c h t h e c o nc ep t o f m y c o r rh z a l b e n e f i t i s i n f luenc ed by phy toce n t r i c th inking isi l luslratcd by t w o i mpo r tan t recent studies. Hetrick et al . (1992) f o und t h a t a decline in d ry weightw as related to a loss o f m y c o r r h i z a l d e p e n d e n c e in m o d c m w h e at (Triticum aesvum L.) culvars .These a u t h o r s s u g g e s t e d t h a t m y c o r r h i z a l d e p e n d e n c y s h o u l d b e c o n s id e r e d i n b r e e d in g p r o g r a m s(Hetrick et al ., 1993). In d o i n g so , t h ey eq ua i ed m y c o r rh i z a l bc ne f i t w i t h m y c o r r h i z a l d e p e n d e n c eo f t h e h o s t p l a n t , a s if m y c o r r h i z a l c o n t r i b u t i o n s t o t h e so i l in w h i c h t h a t p l a n t g r o w s w e r e


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119i r r e l e v a n t . In th e s e c o n d s t u d y , J o h n s o n ( 1 9 9 3 ) sug g es t ed t h a t an u n d e r s l a n d i n g of themc c h a n is ms th a t le t A M F c n h a n c e or i n h i b i t p l a g r o w t h is necessary f o r m a n a g i n g ecosystcms.This vicw was based on f indings t h a t cul tura l pra c t ices se lec t AM F tha t a re i n fer io r mu t u a l i s t s( J oh n s on e t al., 1992) . Johnson (1993) recommended a m a n i p u l a o n o f A M F c o m m u n i t i e sf a v o u r i n g prol i fe ra t ion of the m o s t bene f i c i a ! isolates w i th re ga rd lo p l a yield insiead of theinfer ior ones Ihat c on t r i b u te lo yie ld dec l ine . Aga in , the suggestion does not consider that yie ld, inth e long r u n , depends on the qu a l i t y of the soil .

W e fully agree w i th ihese au thors t h a t p l a n t growth response to AMF is important in agricultura ,b u l wish to emphas ize ihat there is more to mycorrh iza l benef i t ihan j us l th e yield mercase derivedfrom r ny co t r o ph y . Stribley's verdic t (1989): "my co r r h i za l i nocu l an t s have fai led to fulfi l the rpromise because currenlly the re s l i t t le promise to fulfi l" w as apparently based on the assumpt iontha t p lan t growth e n h a n c e m e n t is a ll thai A M F affect in the agrosyslem. H o w e v e r , the full range ofthe promise is far from b e i n g e l u c i d a t e d , for m a n y of the bcnef i ts a re h idde n b e l o w - g r o u n d . It isour hope tha t our d iscuss ion here w i l l contr ib ute lo a beiier unders tand ing of both the p rom ise andthe benef i t s , since th e l a t t e r c l e a r ly fill a c ur re n t c on c e p tua l as w e l l as a p rac t i c a ! n i c h e insus t a i nab l e agr icul lure . These e x t ra b e n e f i t s m a y b e s u m m e d up as 'agrosyslem slabi l i ly' . Theyaccrue to p lan t and soi l al ike a n d c a n n o t b e w e igh e d a t h a rv es t on a scale of dry wcights . Theyresul t f rom the inseparab le , com ple x processes tha l u n i t e a ll c o m p o n e n l s of ih e agrosystem, andrepresen! a new agenda fo r agricullure (Board on Agricu l tu re , 1993).

AMF and soil structure

Sh i f t in g th e focus f rom th e plant to the agrosystem A messagc to a g r i c u l t u r e fifty yearsago advised that " the presence of an effect ive m ycor rh iza l symb ios is is essen t ial to p lan t hea l th"(H ow a rd , 1943). N o w , look in g b a c k on h u n d r e d s of research reports and an extensive collectionof myc or rh iz a books , i t scems t h a t th e t ime to ful ly a p p re c ia t e th is message h a s come, if onlybecause th e challenge posed by t he c omp le x i ty of i n t e r a c t i n g , i n t e r dependen t fac tors ihal h a v e abea r ing on rhizosphere research is now more c lea r ly dc l inea tcd (L inderman and Paultz, 1990;Schroth and W e i n h o l d , 1986). Plan t hea l th and p r o d u c t i v i t y are rooted in the soil, and the qua l i tyof soil dep ends on the divers it y and v iab il i ty of i ts b iota (Doran and Lin n, 1994; Visser, 1985)w hi ch shape the structures that support a s tab le and hea l th y agrosys tem.

The in te res t shown b y increas ing numb ers of mycorrh iza workers in the in te rac t ions of AM Fw i t h th e soil and its b io ta is therefore not so m u c h a sign of masochis t 's de l ight in gra p p l in g w i thu n m a n a g e a b l y c omp le x s yste ms (Sc h ro th a n d W e in h o ld , 1986), b u l s t em s f rom the needs andpr ior i t ies of th e agr i cul tu re of our t imes . In th is scnse, tha l the inc lus in of so i l s t ruc ture in tomy corrh iza resea rch is a necess ty w h os e t ime has f inal ly arr ived. Since Tisdall and Oades (1979)f i rs t reported that aggregate s tabil i ty a n d A M F s ta lus are re la ted in a gr ic u l tu ra l soils, w o r k has


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a d v a n c e d a l three l ev i s : ( 1 ) co l l cc l i on of e v i d e n c c fo r the r c l a t i o ns h i p , (2 ) e l u c i d a t i o n o f ilsmechan i sms , an d ( 3 ) t he i n l e g r a t i o n ot" its process i n t o agr i cu l t u r a ! concep ts . W h a t i s l a rge lylacking is a real izat ion ofthcory in practice.

I mp a c t of my co rrh i za s on soil aggregation The roster o f repor t s o f A M F effects o nagr i eu l t u r a l soils is still m i n u s c u l e c o m p a r e d to the we a l th o f i n f o r m a t i o n a va i l a b le o n p l a n tresponses. It starts w i t h the pioneering w o r k of Tisdall and Oades (1979, 1980a) on therelat ionships betw cen crop ro ta t ion , fa l lowing and soil stabili ty, showing a co nne ct ion between th ec x t e n i o f the soi l m y c e l i u m a n d m a c r o a g g r e g a t e f o r m a t i o n a n d s t ab i l i / . a t i on b y a r b u s c u l a rmycorrhizal roots (Tisdall and Oades 1980b). Umoves on to Miller's extensive ficld studies (1984,1987) o n prairie r e c o n s t r u c l i o n . Mi l l e r , in c o l a b o r a l i o n w i th Jas t r o w, r e p o r t e d in a series o fi m p o r t a n t p ap c rs h o w the a f n i t y b e t w een m y c o r r h iza s a n d soi l aggregates vanes with rootcharacter i s t ics , with the intensi ty of root c o lo n iza t io n , and wi th the am o u nt of so il mycel iumassociated wi th the roois. They f u r t he r e l u c i d a t cd , o r co n t r ib u t ed to t he u n d e rs t an d i n g o f , t heme chanisms o f the fo rmat ion of water-slahlc aggregates (Jastrow, 1987; Miller and Jastrow, 1990;Mil l e r and Jas t row, 1992a and b ; Mi l le r and Jas t row, 1994). Thomas et al. (19 86, 1993)e x pe r im e n te d o n ef fec t s of AMF on soil in pot cu l t u re s . They f o u n d that root an d f u n g u s effectsa re di f f i cu l t to sepra te , but that the soil m y c e l i u m a l on e is cap ab l e to br ing about soi l e f fec t sequiva len! to those of roots, whi l e roots and fun g i together affect soil aggregation synergistically.Mycorrh izas and the mechanism of aggregate formation Artcles discussng the con cep tof mycorrh iza contr ibut ions to soil s t ruc ture are as nu m erou s as those offering empir ica l data. Them a j o r rece rev iew s (Fin l ay and So nde rs tom, 1992; Mi l le r and Jas trow, 1992a and b , 1994;Tisda ll , 1991) agree tha t a ll of the biotic c o m p o n e n t s of the agrosystem interact in the forming ofits abiotic malrix from the pare nt materials (Robe rt and Berthelin, 1986; Emerson et al., 1986), butthere are few f i nd ings , if an y, tha t show in terac t ion s be tween specif ic g r o u p s o f soil organismsand AMF isolates in the aggradave process (Jastrow and Miller, 1991). While each soil organismm ay hav e a necessary f unc t ion in soil struc ture fo rmat ion , f ung i and f i lamentous ac t inomycetes hadbeen show n to be m ost e f fec t ive in b in d in g soil par t ic les in to c r u m b s (Hars e l al.. 1966), evenbefore Tisdall and Oades (1982) developed their concept of aggregate organization with itsim po r t a n t niche fo r AMF.

The c o n t r i bu t i o n of AMF h y p h a e to soi l aggregat ion was summarized by Mi l le r and Jastrow(1994) as cons i s t ing of three related stcps. First, hypha l growth in to th e soil matrix crales th eskele ta l s l ru c t u re t ha t ho lds th e pr im a r y soil particles together th r o ug h physica l en tanglement .Second, roots and hyp ha e together crale the physical and chem ical co nd io ns and p roduce organicand a m o r p h o u s m a t e r ia l s ( G u p t a an d Germida, 1988; Tisdall , 1991) for the b i n d i n g o f particles.Third , hyp ha e and roots enmcsh m icroaggregates in to ma croaggregate structurcs. Once f o r m e d ,


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(h e aggr ega te s enhance ca rbn and n u t r i e n t storage (E l l io t t , 1986; G u p t a and Gcrmida , 1988;Cambardc l l a and Elliott, 1993, 1994) and prvido micro hab i t is for soil microorganisms (Foste r ,1994; Tisdall, 1991). The quality and size distribuon of the aggregates affects pore sizedis t r ibu t ion (E l l i o t t and Coeman, 1988) and the pores offcr i m p r ov e d access to the h y p h a e forg raz ing by so il i nve r tebra te s ( In gh am , 1992). A l t h o u g h t he rc i s cons ide r ab le ev idencc t h a tin terac t ions between the soi l b iota and A M F m ay h a v e negativo effects on plas (Hctrick e t al.,1988; Ing h am , 1988; Ra bat in and St inn er , 1991; Ross , 1980), com ple m entary e f fects of theseinte ract ions on the soil and ils stabilily are little-known. One may speculate tha t these soilresponses are largely positive, since t h ey i nvo lve enhanced carbn i n p u t (Finlay and Snders trm,1992; Hepper, 1975; Lynch and W hi p p s , 1991; W r i g h t and Millner , 1994) from p l a n t to soil.U l t i m a t c l y , h o w e v e r , th is loss of c a r bn by the p l a n t no l only improves soil q u a l i t y , b u t alsobenef i l s p l an t growth (Bu rns and Dav ies, 1986).

Mycorrhiza l ef fect iveness measured by soil responses Because of i ts i m p o r t an c e toboth plant and soil, aggregate stability has been suggested as a measure of AMF effectiveness inagrocco logy ( B e t h l e n f a l v a y e t al., 1988; B e t h l e n f a l v a y and N c w t o n , 1991). Th i s i dea w asexpanded by T i sda l l ( 1991) , who descr ibed th e charac ter i s t ics of e f f ec t i ve AM f u n g a l soils tabi i ze rs as (1) the p rod u ct ion of greate r qua nt i t i es of more p ers i stenl and s t icky m uci lag e , (2)b o n d in g by h y r o p h o b i c bonds and poly valen t ca t ions to clay plate le ts , (3) preferenta l interactionswith plants, mcroorganisms and animis, (4) effective orientation of clay particles, (5) vigoroussoil pen e tra t ion, and (6) tlic produ c t i on of a p rofuse so il m y c e l i u m . Tisdall 's list supp l ements th ese lect ion guide for AMF effect ive in promot ing p l an t gro wth (Abbott and Robson, 1984a, 1991)an d refocuses priorities of mycorrhiza research in sustainable agriculture.AMF and the soil biota

Different eTects on plant and soil? Much e f for t h as gone dur ing th e past te n years into th eintegration of the combined effects of specif ic plant -fungus com bina t i on s and spec i f ic g roups ofsoil biola with bas ic and a p p l i e d aspects of p l a n t science (A z c n- A gu i l a r and Barea, 1992;Bagyara j , 1984; Hendrix e t al., 1990; Ingham, 1992; Miller, 1990; Paulitz and L i nd e r m a n , 1991;Reid, 1990; Tinker , 1984). At the same t ime , soil biota effects on mycorrhiza format ion have alsoreceived attention (Azcn et al., 1990; Linderman, 1992; Rabatin and Stinner, 1991). Much less sknown, how eve r , abou t th e inte ract ion s be tween speci f ic A M F isolates and distinct groups of soilo rgan i sms as i t re lates to soi l s t ructure , even though these inte racl ions h ad been conceptual izedt h o r o u g h l y in genera l t e rms ( B u r n s and Davies, 1986; N e w m a n , 1985; Oades, 1984; Tisdall,1991). W e f ce l t h e r e for e conf i den t in pr ed i c t i ng tha t m a n y expe r imenta l de s igns of f u t u r emycorrh iza research will include evaluatons of soil responses as routinely as they now report


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d e t e r m i n a t i o n s o f roo t c o l o n i / a i i o n . I f s l i m u l a t i o n o " t h e r h i z o s p h e r e h i o t a a n d ih e r c s u l t i n gi m p r o v e m e n t o f s o i l s t r u c l u r e i s in f a c t an e v o l u t i o n a r y m e c h a n i s m t h a t i m p a r t s c o m p e t i t i v ea d v a n t a g c s l o p l a n t s ( B u r n s a n d D a v i e s , 1 9 8 6 ) , t h c n a h o l i s t i c a p p r o a c h l o t h e j o i n t s t u d y o fa r b u s c u l a r m y c o r r h i z a l p l a n t an d soi l r esponses is indc ed a n a b s o l u t e necess i ty .

T h e goal o f i m p r o v i n g o r r e s t o r i n g d i s t u r b e d a g r o s y s t e m s m a y b e a p p r o a ch e d b y s t u d y i n g t h ec o n d i l i o n s tha t p rov id e s t a b i l i t y in n a t u r a l s y s t e m s and use i t as a m o d e l to r ec ons t ruc t ( L i n d e r m a n ,1986) t h e d i s t u r b e d s y s le m . A l t e r n a t i v c l y , a m a n i p u l a t o n o f th e d i s t u r b e d s y s le m m a y b e ried loa c h i e v e s p e c i fi c , l i m i t e d e n d s . T h e se e n d s h a v e b e e n p r o d u c t i o n - o r i e n t e d in t h e pas t ( C o o k e ,1982; Ha t f i e l d a n d K a r l e n , 1 99 4 ). S o i l m i c r o b e s h a v e b e e n t r i e d , w i t h o r w i t h o u l A M F , t os u p p re s s p l a n t p a t h o g e n s , to c o n t r o l p l a n t pes ts , t o e n h a n c e p l a n t n u t r i t i o n , to p r o m o t e p l a n tgrowlh, or to rel ieve e n v i r o n m e n t a l s tress to p l a n t s . N o w , r c gard less o f i t s p romise fo r e n h a n c i n gp l a n t p r o d u c t i o n , a n e w a g e n d a fo r a g r i c u t u r e a d v i s es a n d prescr ibes t h a t e a c h n e w b i o t e c h n i q u eto be c m p l o y e d in a g r i c u l l u r e be also sc ru t in ize d as to i ts ef fec ts o n agrosystem s t a h i l i l y (Board o nA g r i c u l t u r e , 1993). This w i l l takc s o m e r e t h i n k i n g of the p r e m i s e s , fo r the use o f b e n e f i c i a ! soilm i c ro o r g a n i s m s a s tools fo r the c on t ro l o f dc le te r ious onc s i s e v a l u a t c d b y p l a n t effecls (Sc h ipper set al., 1987). Let us speculatc here, if only to s l imulate controvcrsy, t h a t favorable p l a n t responsesto rh izosphere m a n i p u l a t i o n m ay n o l a l w a y s be a c c o m p a n i c d b y benef ic ia l soil r esponses , and tha tc o n v e r s e l y , c o n d i t i o n s m a y e x i s t w h e r e processes f a v o r a b l e to so i l s tab i l i ty may be u n f a v o r a b l e top l a n t g r o w t h , a t least in i t ia l ly .

W h a t a re s o m c o f thcse processes in a g r o s y s t e m b i o l o g y i ha t m a y a f ec t p l a n t p r o d u c t i o n a n dso i l s tab i l i ty di f fe r en t l y? A m o n g m a n y , w e wil l s ing le o u t three e x a m p l e s : (1 ) m i c r o b e - m e d i a t e dn u t r i e n t u p t a k e a n d so i l p H , (2 ) s t i m u l a t o r y o r a n t a g o n i s t i c r e l a t i o n s h i p s b e t w e c n A M F a n d soi lmic robes , and (3) soi l f a u n a ef fec ts o n t h e m y c o r r h i z a a n d i ts mic robia l as soc ia tes .Nutr i ent uptake an d soil p H L o n g - k n o w n a s e n h a n c e r s o f s y m b i o t i c N T f i x a l i o n in P-d e c i e n t soi ls (Asai, 1948; Mosse e t al. , 1976; Barca an d Azc n-Agui la r , 1982) , A M F have alsobeen s h o w n to affec t N up take f r o m soil ( A m e s e t al., 1983; A z c n ct al ., 1991; J o h a n s e n e t al.,1992), al though a prefe renc e for the form of N has no t ye t b e e n c o n c l u s i v e l y d e m o n s t r a t e d (Bareae t al, 1987; Azcn e t al . , 1992; Vaast an d Zasoski , 1992). Frey a n d Sc h e p p (1993a) showed , ina c u v e t t e s y s t e m w i t h r o o t - fr e e s o i l c o m p a r t m e n t s , s e p a ra t e d f r o m th c c o n f i n e d rh i z o sp h e r e o fm a i z e p la n t s , t h a t 15N w a s taken u p b y t h e soil m y c e l i u m o f A M F a f te r a d d i o n o f ( I 5NF4)2SO4to the soil to be transponed in considerable a m o u n t s to plant roots being several centimctres apartf rom th e site of app l ic a t ion . Sim i la r ly N also c an be t ransponed v a m y c o r r h i z a l h y p h a e f rom p l a n tto pla n t (Frey and Sc h epp , 1993b). The so i l m yc e l iu m o f A MF a lso prov ide c h ann els fo r t rans fe ro f f i x e d N f r o m l e g u m e t o n o n - l e g u m e p l a n t s ( F r e y a n d Sc hepp , 1992) . This c o u l d b ed e m o n s t r a te d i n a c u v e tt e s y s t e m s e p a r a t i n g th e n o d u l a t e d roots o f Trifoliutn alexandrinum f romth e rh izosphere o f m aize . Fur ther s tud ies a re needed to e luc da te the im pac t o f AM F in N cycl ing in


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relat ion lo N f i x a t ion . T he f u n c t i o n of A M F c o n c e r n in g the N c y c l e s h o u l d not be r c d u c e d to th e Nn u t r i t i o n of t he p l a b y h y p h a l N u p t a k c o r N t r a n s p o n . A M F m u s b e regarded in the d y n a m i cprocesses resulling in the temporary immobilizaon of N with in its biomass and the Nminera l i s a t ion at phases of deco m po s i l ion of a rbuscu la r mycor rh iza l myce l ium. N losses from theroot sys lem and froni th e soil t o t h e g r o u n d w a t e r m a y b e r e d u c e d o r e n h a n c e d b y m y c o r r h i z a lac t ivi ty.

W h i l e so i l b io logi s t s a re sa id to be m ore p reoccu p ied with the tr ipa r ti te l egu m e associal ion thanw i th any o ther b io log i ca l process (Ly nc h , 1987), an inc reas ing nu m be r of bac te r ia wi th N^fixingcap ab i l i ti es a re also b c i n g d i s c o v e r ed . This provides th e cha l l enge of s u p p l y i ng , p c rhap s by meansof A M F h y p h a e ( Ba rc a el al . , 1992) , nonlegumes w i t h bio logica l ly-der ived N (Dobere iner , 1989;Z u be re r , 1990). In add i l ion , an inc rcase in assoc ia t ive d i az o t r o p h p op u l a l i ons i n Ihe presence o fA M F (Bagyara j , 1984) m ay a lso im pro ve so il qua l i ty , since aggrcgate s tabi l i ty can be propor t iona lto the b i omas s of ce l l s p resen! (Lynch , 1987) .

B i o l o g i c a l l y - f i x e d N a l w a y s i m p r o v e s p r od u c t i v i t y , s in c e N ava i l ab i l i t y i s one o f t he m a j o rliming factors in a g r i cu l t u r e . H o w e v e r , w h e n N i n p u t is in the f o rm of NH4-N, as is the casewith N2 f i xa t ion , ex t ru s in of H+ and of organic ac ids i s preva len! and resul ts in an ac id i f i ca t ion o fthe g r o w th m d i u m no t o n ly in th e r h i z osp he re (M arsch n e r a n d R o m h e l d , 1983; Marschner et al.,1987) but a lso in the ent i re m y c o r r h i z o s p h e r e (Li e t al., 1991). Soil pH effecLs on AM F h a ve l ongb ee n k n o w n ( W a n g e t al., 1993), bu t i t i s l i t t le k n o w n to w h a t e x t e n t m y c o r r h i z a s an d t h e i rassoc ia ted m i c r o f l o r a m a y c ra te , cont ro l , a n d m a i n t a i n t h e pH o f t h e ir e n v i r o n m e n t t h r o u g he x u d a t i o n ( S c h w a b e t al. , 1991) an d CO2 levis ( K n i g h t e t al . , 1989) in the abs c nc e o f soi ld i s tu rbance . E leva ted so i l pH, however , af fects the s tabi l i ty of aggregates (Oades, 1984; Red andGoss, 1 9 8 1 ) as wcl l as the c o m p o s i t i o n of the soil m i c r o f l o r a (Harr i s e t al., 1966). In f a c t ,nega l ive e f f ec t s o n soi l aggregat ion b y l e g u m e c r o p p i n g h a v e b e e n d o c u m e n t e d (Alberts e t al. ,1985; Laflen and Moldenhauer , 1979) . Soi l loss, how eve r is determined by m a n y aggrcgat ing andd i s aggreg a t i ng to r c e s (G i s c h and B ro w ni n g , 1 94 8; St r i ck l ing , 1950), is i n f l u e n c e d by c l i ma t i c ,e d a p h i c , c rop p i ng and t i l l age f ac tors , an d c a e n o f these a f f e c t th e processes o f soil b i o l o g y . It isthe re fore n o t s u rp r i s i ng t h a t th e connec t ion bc tween so i l loss an d l e g u m e c r o p p in g is unreso lved(Alberts an d Wendt , 1985) , but the p h e n o m e n o n s e rv es as an e x a m p l e h o w m y c o r r h i z a - m i c r o b cr e l a t ionsh ips may a f f ec t cos t -bencf i t ratios in p rod u c t i on and co n se rv ao n .

Mycorrhiza-microbe in teract ions and their e f f e c t s on plant and soil A n i m p o r t a n !f u n c t i o n o f t he a r b u s c u l a r m y c o r r h i z a l soil m y c e l i u m i s t h e t r a n s p o n o f c a r b n t o m i c r o b i a lc o m m u n i t i e s (Jakobsen and R o s e n d a h l , 1990). Th is i s espec ia l ly s i g n i f i c a n ! when root dens i ty i slo w ( A b b o t t a n d R obson , 1 9 8 4 b) , since th e h y p h a e c an pent ra te s cvera l cen t imete rs o f soil( C a m e l e t a l . , 1 99 1) a n d r e a c h t h e m i c r o f a u n a o f t h e b u l k so i l ou t s i d e t he i n f l u enc e o f t herh i z osp he re (F i n l ay a n d S o n d e r s t r o m , 1992). In view of the i r ro le as med i a t o r s o f c a r b n f low


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( W h i p p s , 1990) , one w o u l d e xp e c t th c i n f l uence of AMF on soil microbcs lo be posi t ivo. This isno t a lw a y s th e case, h o w e v e r . Ma n y s tu d ic s h a v e s h o w n tha t A M F m a y alter th e soi l micro f lo ra(Ames, et al., 1984; Bagyaraj and Mengc, 1978; Christcnsen and Jakobsen, 1993; Mcycr andLind erman , 1986; Seci lia and B agy araj , 1987) by s t im ula t ing as wel l as i nh ib i t ing total bacterialcounts or se lected bacter ia l groups . Soi l microbes , in tum, may promote (Ames, 1989; Azcn ,1989. A z c n e t a l . , 1990; Azcn-Aguifar el al, 1986; Staley et al., 1992; Vejsadov et al., 1993)or antagonize (Azcn et al., 1990; Beth len fa lvay et al., 1985; D h i l l o n , 1992; Krishna et al., 1982)mycorrhiza developmenl.

How do these complex interactons affect p lan t prod uction and soi l s labi l i ty? A s t im ula t io n ofplan t growth may be ach ieved by m a n i p u l a t i n g specif ic groups of organisms, such as p h o sp h a t es o l u b i l i z i n g ( A z c n - A g u i l a r et al. , 1986) o r d ia zo t r o p h ic ( P a u la e t al. , 1992) bacter ia , orrh izo bacter ia t h a t p r o m o te p l a n t g r o w th by v a r io u s m e c h a n i s m s ( B u r r a n d Caesar, 1984),How ever , when the arbuscular mycorrh iza l p lant is grow n in thc Field, subject to m a n y inf luencesat th e same t ime , growth s t imu la t ion b y A MF becomes e lu s iv e (Fit ter , 1991; Hetrick et al., 1988,Ross, 1980). This led some workers to conclude tha t t is the soil microflora that reglalesmycorrh iza formation and p lant grow th rcsponse , regardless of the AMF isolates present (Hetrickand W i l so n , 1991). One mus t keep in m i n d , however , tha t the 'g rowth responso ' is on ly one ofth e w a y s to e v a la te t h e A MF e f fec t on p la s ( K o i d e and Schreiner , 1992) , let a lone th eagrosys tem, of which the plant is but one componenl .

The absence of a plant growth response to AMF, or a negative one, was interpreted as a loss ofcarbn by the p la n t , w h ic h o u tw e igh s Ihe mutua l i s t i c a d v a n t a g e of e n h a n c e d P up take by thee n d o p h y t e (Fitter, 1991). This form of paras i t i sm h as been v iewed t rad i t iona l ly as a lack ofarbuscular mycorrh iza l efficiency, and in a w idcr sense, as a lack of applicaon potentia l for AMFin agr icu l ture (Stribley, 1989). From the poin t of v iew of agrosystem stabil i ty, on the other h a n d ,th e gain of carbn by the soil represents an increase in substrate availability, resulting in greatermicrobia aclivity (Kkch ner et al., 1993) and increased organic matter conten and soil stabilily.

Seen in th i s context , one may e v e n ascribe usefu l (agrosystem-stabilizing) f u n c l i o n s tomycoparasites: although th e parsitos m ay l imit A M F popu la t ions and thereby reduce plant growth(Pau l i tz an d Menge, 1986; Ross and Rut lencu t te r , 1977) , they m ay also s t i m u l a t e h y p h a lregrowth , thus fur ther increasing carbn f lux and microbia ac l iv i ty in the soil. Seen f rom thisang le , the u t i l i ty o f chemica l con l ro l o f myc oparas i te s (Sy lv ia and Schenck , 1983), may berevised, using so aggrcgation measuremcnts as an altrnate tool for the evaluation of mycoparasiteeffects. M icrobia biomass and activ i ty (Dinel e t al., 1992) play an impor tan t role in the format ionand s tabi l i ty of soil aggregates, and p remi so a wide range of app l i ca t ions fo r AMF and the irassociated microf lora .Mycorrhizas and the soil fauna Invertebrates and AMF are ubiquitous and abundant


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c o i n h a b i t a n t s o f th e s o il e n v i r o n m e n t . T o g e lh e r t hey f i l l i m p o r t a n f u n e t i o n s in processes w h i c hregla te n u t r i c n t a v a l a b i l i t y a n d m i n e r a l i z a t i o n ( I n g h a m , 1 992 ). I n te r a c t io n s b e twe e n th e m a j o rg r o u p s o f f u n g i v o r o u s so i l in v e r t c b ra te s ( n e m a lo d e s , sp r in g ta i l s , rni tes a n d m i c r o a r t h r o p o d s h a v ebeen rev iewcd (Fi t te r a n d Sanders , 1 992 ; Pa u l i t z a n d L i n d e r m a n , 1 9 9 1 ; R a b a t i n an d S l in n c r ,1991) a n d discussed in c c o lo g ic a l ( M c G o n i g l e a n d Fitter , 1988) a n d a g r i c u l t u r a l ( S y l v ia a n dWil l i a m s , 1 992 ) se t t i n g s . Gra z in g b y i n v e r te b ra te s o n t h e s o i l m y c e l i u m o f A M F m a y l i m i t i tsd e v e l o p m e n t o r d i s c o n n e c t t from tb e r o ot m y c e l i u m , bu t i t may also s t i m u l a t e i ts growth (Fi t te ra n d S a n d e r s , 1 992 ) . D a m a g e to the h y p h a l n e t w o r k w o u l d resu l l in an i m p a i r m e n t o f n u t r i e n tu p i a k e , a p r e p o n d e r a n c e o f root- over s o i l -myc e l i a l b io m a ss . S t i m u l a t i o n o f h y p h a e a n d sporep r o d u c t i o n , o n th e o t h e r h a n d , w o u l d b e b e n c f i c i a l lo the agrosys tem a n d t o p l a n t g r o w t h . S u chpo s i t i v e effects h a v e b e c n re po r t c d w i t h sp r in g ta i l s (Har r i s a n d B oe r ne r , 1990) and nematodes( I n g h a m , 1988) , a n d re lated to gra/.er d e n s i ty a n d g ra z in g in ten s i ly ( Mo o rc , 1 988). P l a n t g ro w thm a y hav e been af fected b y t h e increased m i n e r a l i z a t i o n o r m o b i l i z a t i o n o f n u t r i e n t s b y t h e grazers( F i n l a y , 1 985 ; I n g h a m et al . , 1985 ; Harr i s and Boermer , 1990). A l t e r n a t i v e l y , t h e re m o v a l o fsenesc ing so i l myee l ia b y t h e graze rs m a y have resu l ted in the e l i m i n a t i o n o f g r o w t h - i n h i b i t o r ys e c o n da r y m etahol i lcs (Mo ore , 1988).

T h e c o n s e q u e n c c s o f s u c h t r o p h i c i n t c r a c l i o n s b e tw e e n t h e s o i l f a u n a a n d A M F o n soi la g g r e g a l i o n s p e c i f i c a l l y , a re l i t l l e - k n o w n . Ge n e ra l ly , h o we v e r , a l l b o t a f o u n d w i t h i n th ea g r o s y s t e m w e r e s h o w n to c o n t r i b u t e to the d e v e l o p m e n t o f so i l s t r u e t u r e ( Jas t row a n d Mil le r ,1 9 9 1) . In m y c o r r h i z a r es ea r ch , i t r e m a i n s to be seen h o w t h e soil f a u n a affects the cos t-benef i tra t io of p lan t o r so il d eve lopm ent as they re la te to agrosys tem s tab i l ily .Summary and c o n c l u s i o n sA n agrosystem is t ha t part of the larger ( n a t u r a l o r agr icu l tura l ) ag roecosys tem t h a t m a y b e s u b j e c tto exper imenta l con l ro! , and where roo ts , the so i l m i c r o f l o r a and the soil f a u n a i n t c r a c t t o suppo r tp l a n t g r o w t h a n d to fo rm a s l a b le so i l m a t r ix . A n agroecosys tem is s u s t a i n a b l e w h e n th e b io t iccom po nents o f the agrosys tem are in ba lance . In d is turbed ecosys tems , th is ba lance depends on thegoals o f l a n d m a n a g e m e n t : p r o d u c t i o n o r c o n se rv a t io n . T h e two goa ls m a y b e c o m b in e d if theagr icu l lu ra l m a n a g e r u n d e r s t a n d s t h e bio log ica l com plexi ty o f the land un der h is s tewardship .A m o n g th e m u l t t u d e o f o r g a n i sm s t h a t m a k c u p th e agrosys tem, A M F s t ands o u t because of i tsab i l i ty t o f o rm a b r id g e b e twe e n p l a n t and so i l . Thcse f u n g pe n t r a te a n d c o lo n i ze t h e cells o fho s t -p lan t roo is, w h i l e the i r so i l hy ph ae a re in i n t ma t e contad w i th th e m ic ro b io t a th a t inhbi l soilaggrega tes and co n t r ib ut e to so il s t rue ture f o r m a t i o n . B y m e d ia t in g n u t r i e n t f luxe s b e tw e en p l a n tan d so i l , the f u n g i n f l u e n c e b o t h p l a n t gr o w t h a n d hea l th and the d e v e l o p m e n t o f c o m m u n i t i e s o fs o i l o r g a n i s m s . In t he c o u r se o f e x p e r i m e n t a l m a n i p u l a t i o n of i he a g ro sy s te m , c o m p le xre l a t i o n sh ip s b e twe e n o rg a n i sm s m a n i f e s t t h c m se lv e s t h a t c a n b e s t i mu l a t o r y , an t agon i s t i c , o r


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126b o t h , d c p e n d i n g on t hc c i r c u m s t a n c e s . S u c h r e l a t i o n s h i p s may be real o r artefacts of ar t i f ic ia lenvironments, and their effecls m ay be beneficia! or delclerious lo p lan t and soil in divergen! ways,al leasi in i t ia l ly and in passing. It is o n e of the ch a l l en g es of ag r i cuk ur a l and ecolgica! rescarch todraw val id i n ferences from such t ransient effecls achicv ed unde r con t ro l l ed c o n d i o n s to the realityof thc f i e ld .In the field of agricul turc , sustainabi l i ty has become th e p a r a d i g m of our t ime, and in biolgica!research sus ta in ab i l i ty m e a n s p l a n t p r o d u c t i o n w i t h o u t soi loss. F o r m y c o r r h i z a research , thsm e a n s a r e t h i n k i n g of the c o n c e p t o f m y c o r r h z a l b e n c f i t . S y n o n y m o u s w i l h p l a n t g r o w t hcnhancement in thc past, in the context of sustainability i t may be redefmed in terms of agrosystems tabi l i ty , res t i ng o n soil biotic c o m m u n i t i e s i n h a r m o n y w i t h roois an d b a l an ce with each o therwithin a s trong, resil ient , l i fe-supportng soil matr ix .

T h u s , wc sec a closed chain of cause-effect re la t ionsh ips as ih c u l t mate b en c f i t of myco rrh iza lfu ng i in the ag r o s y s t em . T h e f ung i i m p r o v c p l a n t g r o w l h , h e a l t h , an d stress res is tance; th e p l a so s t reng th en ed i s a more a b u n d a n source of energy to the so i l, enc oura g in g the dev c lop me nt o fils biota; ih e organisms e n h a n c e soil aggregate forrnation; an d ih e l i fc-support ing so i l struclurc soformed pcrniils better pla growth, closing thc chain.Refe r en t e s

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