soil interfaces in terrestrial ecosystems

Agriculture, Ecosystems and Environment, 24 ( 1988 ) 117-134 Elsevier Science Publishers B.V., Amsterdam - - Printed in The Netherlands

117

Section 2. Interactions B e t w e e n Invertebrates and Organisms Associated with Plant Rhizospheres

Interactions of Organisms at Root/Soil and Litter/ Soil Interfaces in Terrestrial Ecosystems DAVID C. COLEMAN 1'2,D.A. CROSSLEY Jr. 1'2,M.H. BEARE 2 and P.F. HENDRIX 2

~Department of Entomology and 2Institute of Ecology, University of Georgia, Athens, GA 30602 (U.S.A.)

ABSTRACT Coleman, D.C., Crossley D.A., Jr., Beare, M.H. and Hendrix, P.F., 1988. Interactions of organisms at root/soil and litter/soil interfaces in terrestrial ecosystems. Agric. Ecosystems Environ., 24: 117-134. Invertebrates and micro-organisms have numerous interactions in soils. Because resource qualities and quantities are more often optimal in root/soil and litter/soil interfaces, our studies have been focused on mineralization and nutrient-cycling processes in these microhabitats. We address general aspects of resource qualities and interfaces, and then some specific results from our research in agro-ecosystems in Colorado and in the Georgia Piedmont. The paper concludes with suggestions for possible directions of new research in soil ecology.

INTRODUCTION T h e r e are n u m e r o u s aspects of t e m p o r a l a n d spatial r e l a t i o n s h i p s which affect soil processes a n d o r g a n i c - m a t t e r p r o d u c t i o n a n d t u r n o v e r in soil systems. In this review, we e x a m i n e t h e wide a r r a y o f scaling factors w h i c h are involved, a n d e x a m i n e t h e physical, c h e m i c a l a n d biological ( p a r t i c u l a r l y i n v e r t e b r a t e / m i c r o b i a l ) processes of i n t e r e s t to soil biologists a n d ecologists. Several m a j o r soil processes are associated p r i n c i p a l l y with aspects of prod u c t i o n a n d d e c o m p o s i t i o n , a n d t h e s e are, in t o r n , i n t e r l i n k e d with t h e import a n t processes of i m m o b i l i z a t i o n a n d m i n e r a l i z a t i o n . T h e s e subjects h a v e b e e n reviewed e x t e n s i v e l y b y S t o u t et al. (1981), C l a r k a n d Rosswall (1981) a n d C o l e m a n et al. ( 1983, 1984). As n o t e d b y C o l e m a n et al. (1983), t h e a r r a y of soil-forming factors o p e r a t i n g via various processes over t i m e leads to m a j o r e c o s y s t e m p r o p e r t i e s (Fig. 1 ). W e will review some of t h e p a s t l i t e r a t u r e r e g a r d i n g biotic influences on soil processes a n d t h e n p r e s e n t some new d a t a w h i c h have b e e n o b t a i n e d in this i n t e r e s t i n g area o f roots, b i o t a a n d o r g a n i c - m a t t e r d y n a m i c s .

0167-8809/88/$03.50

© 1988 Elsevier Science Publishers B.V.

118 CONTROLLING FACTORS Climate

Parent material

Vegetation

Relief

~ e s t $

Rangealnd

Cultivation Fallow Crop selection Residue management Nutrient inputs Water management Fire Harvest (removal)

Grazing Species Nutrient input Fire

,.o

Seeding and Planting Site preparation Watershed management Fire Harvest

PROCESSES Energy inputs and transformations Radiation --Primary production --Decomposition --Nutrient cycling Immobilization Mineralization Weathering Translocation --Transport Erosion Gaseous Leaching -

uJ

p.

-

DEVELOPMENT OF ECOSYSTEM PROPERTIES

V~ +

Vegetation Consumers Soil --Base status --Texture --Organic matter --Phosphorus --Sulphur Nitrogen --Salinity -

-

Fig. 1. Soil-forming factors, and major processes, over time, lead to development of ecosystem properties (from Coleman et al., 1983). MAJOR PROCESSES OF INTEREST TO BIOLOGISTS AND ECOLOGISTS WORKING WITH SOIL SYSTEMS

F r o m a global ( T u c k e r et al., 1985) or e c o s y s t e m p e r s p e c t i v e , t h e r e are a v a s t a r r a y of p r o c e s s e s w h i c h m u s t be u n d e r s t o o d to c o n t r a s t a n d m a n a g e n a t -

119

Roots and hyphae ( medium -term organic)

Root Hypha

200 M.m

Aggregates or particles

Plant and fungal debris encrusted with inorganics (persistent organic)

,

~. - i

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Amorphous aluminosilicates oxides and o~anic polymerl sorbed on cloy surfaces and electrostatic bonding, flocculation [permanent inorganic) 0.2/J.m

Clay

plates

Cement

Fig. 2. Soil microaggregates, across five orders of magnitude, beginning at the level of clay particles, through plant and fungal debris, up to a 2-mm diameter soil crumb (from TisdaU and Oades, 1982).

ural and agroecosystems. Below the soil surface there are ample opportunities for studying dynamics over short time periods, hours-days-weeks, and longer times, over centuries and millennia. At a finer level of resolution, there are important effects of the physical and chemical milieu on organic-matter dynamics. The organic matter is associated with clay particles, clay plates and microbial debris growing in association with the sand, silt and clay matrix

120 (a)

Jlj!l . . . . . . . . .

•

Cb)

oeo

o g ~ g

i

i

n

(c)

Fig. 3. Schematic representation of hypothetical development of depletion zones for a poorly diffusibleion around (a) non-mycorrhizal root with root hairs; (b) vesicular-arbuscular mycorrhizal root with root hairs and extra-matrical hyphae; (c) ectomycorrhizal root with fungal sheath, hyphae and mycelial strands (absence of root hairs). Uppersection in (a) and (b) repesents suberized root where mycorrhizal hyphae may be functional (from Coleman et al., 1983). which comprises the soil milieu (Fig. 2 ). Extending over three orders of magnitude from 0.2 to 20/~m and then an additional order of magnitude to 200/lm, brings one to the scale of roots and hyphae growing through soil pores and aggregate formation (Tisdall and Oades, 1982). These aggregates, of the size of a 2-mm sized macroaggregate, have ample pore space and solid material for diffusion of gases and liquids, as well as the important movement of microbes and fauna into and out of these ubiquitous sand, silt, clay associations. One of the important problems we have in studying soil systems is to reach the level of resolution where the processes are occurring. Foster (1981, 1986)

121

I ROOT TRANSECT A RHIZOSPHERE

, k 3'

BULK SOIL

Z

.~.'co~

..........

TRANSECT B

MINEI~ALIZFO

NUTRIFNT

POOl

Fig. 4. Conceptual diagram of root and bulk soil, showing organisms and principal processes. Rhizosphere, from left to right: root cap and region of elongation, showing sloughed root cap cells, region of root-hair growth, then maturation and sloughing of root cortex. Microfauna and meiofauna grazing on microbes affect nutrient availability, for uptake by root and mycorrhizae. Activity of root grazers and deposition of root debris, shown on right-hand side of the diagram {from Trofymow and Coleman, 1982). TABLE 1 Distribution of organic-matter production (g m -2 year-l), in four natural ecosystems and one agroecosystema Production

Deciduous forest (Tennessee)

Lightly grazed shortgrass prairie (Colorado)

Cooldesert, Atriplex shrub complex

Arctic tundra (Barrow, Alaska)

Irrigated alfalfa field (Minnesota)

150 100 0.40

920 560 0.38

(Utah) Aboveground Belowground Belowground/total

700 (370) b 900 0.56 (0.71)b

118 576 0.83

120 270 0.69

~Modified from Coleman et al. {1976). bFigures in parentheses indicate increments other than woody tissue.

and Foster et al. ( 1983 ) have studied inputs of organic materials, particularly the more labile forms. The enhanced surface area of root plus mycorrhizal hyphae vs. root alone, for absorption of various inorganic minerals is very important. Thus, an uncolonized root has fewer depletion zones than a vesicular-arbuscular mycorrhizal (VAM) root and the more extensive ectotrophic mycorrhizal structures (Fig. 3). Processes associated with mycorrhizal function have been reviewed for natural systems by Coleman et al. (1983), St. John and Coleman (1983) and Fogel (1985). In addition to the spatial pattern, from the roots and root-associated organisms into the soil, there is a temporal progression of processes which occur

122

along the root, from the root cap and the root-cap cells to the older, more proximal regions. As the root grows, root-cap mucilage remnants and cap cells are sloughed, and the root hairs grow out from individual cells (Fig. 4). Proceeding downward to Zone A, there are various fibrous secondary wall layers which then break down and are colonized by bacteria and in turn provide food for associated other microbes and fauna (B and C). Farther up the root, the secondary walls break down gradually and show further wear. It should be noted that older cells, even some in decorticated zones of roots, are still able to take up water and nutrients. Extensive studies of root activity using a variety of radioisotopes and vital stains have been attempted and have met with varying success (BShm, 1979). Primary production going belowground into root production, as a fraction of total net primary production, can be as much as 60-80% of the total (Table 1 ). In a range of grassland, shrub-desert, coniferous-forest and deciduous-forest habitats these percentages are always greater, than 50%; only the arctic tundra contribution was less than 50%. Even these estimates may be slightly low because only now are some researchers (e.g. Persson et al., 1980; Fogel and Hunt, 1983; Fogel, 1985) making adequate measurements of fine root production and mycorrhizal production and turnover on an intra- and inter-seasonal basis. The interrelationships of organic-matter production and turnover in nutrient cycles are presented diagrammatically in Fig. 5 (McGill and Cole, 1981 ). ~ N2 a ~

Residues

Prints

\

Soli~

Inorganic

\ co I

P..-

.

~

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, j i Fig. 5. Schematic illustration of interrelations of C, N, S and P cycling within soil-plant systems (from MeGill and Cole, 1981 ).

123 STRUCTURAL C

STRUCTURAL N (C/N = 80)

METABOLIC

METABOLIC

C

N (C/N = 5)

ACTIVE

ACTIVE SOIL N (C/N" B )

SO~C (lO yr.)

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SOIL N

C ( 50 yr,~

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SOIL

C ( ~JO0 y,.)

N (C/N" II )

Fig. 6. Flowsof structural,metabolicand soil N and C in a soil organicmattermodel.Note faunalmicrobialinteractions,representedby Xfrom"metabolic"and "active"N boxes. I = immobilization and M= mineralizationprocesses (modifiedfromPartonet al., 1984). This conceptual model shows inputs of plant residues to microbes and subsequent production of microbial residues. The implicit impact of faunal feeding activity as well as release of carbon dioxide from growth and maintenance respiration, and then the formation of ester-linked phosphorus and sulfur (C-OP, C-O-S), and the production of various humified materials are also shown. The small bowties show the breakdown of these materials either by biological mineralization (for energy) or biochemical mineralization (cleavage of ester bonds), to release nutrients which can be taken up by plants, thus beginning the cycle all over again. Only a small fraction of the total organic material may be turning over very rapidly. Thus, the microbial population may be only 2-4% of the total soil ganic matter yet be turning over at a considerably faster rate, as shown in the conceptual model from Parton et al. (1984) showing active, slow and passive organic fractions (Fig. 6). There is an array of labile and non-labile organic and inorganic forms of mineral nutrients, e.g. phosphorus (Stewart and McKercher, 1982) and sulfur. There are complexities in physio-chemical aspects, and the biochemical and biological activity plays a central role in turnover of labile compounds.

124 EXPERIMENTAL INVESTIGATIONS OF ROOTS, BIOTA AND SOIL ORGANICMATTER PROCESSES

Many studies have been made to measure respiration and nutrient-cycling 3.0

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(~g NH~-N q-l~o'} Fig. 7. The percent N of dry shoots, grown in soil in flasks with bacteria alone (B) or with amoebae (AB) at three initial soil N H : - N concentrations. *Significant at P<0.05 (from Elliott et al,, 1979). 4000

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Fig. 8. Mineralization of N, and facilitated uptake, in the presence of bacterial or fungal grazers ( . . . . ) vs. plant alone ( - - ) . © =Plant; • =plant + bacteria; [] =plant + bacteria + fungus; @=plant + bacteria + bacterial-feeding nematode; • =plant + bacteria + fungus + fungalfeeding nematode. (From Ingham et al., 1985).

125 TABLE 2a Numbers of nematodes within the pbn ~ treatment in the rhizosphere and nonrhizosphere of chitin-amended soil (mean and 95% confidence interval) from Ingham et al. (1985). Day

7 21 49 77 105

No. Pelodera per gram dry soil Nonrhizosphere

Rhizosphere

132 30.5_+16.5 63.8_+ 29.6 44.8 _+24.9 49.5 _+36.8

132 94.1_+ 59.0 535.5 -+543.9 429.6 _+259.3 912.2 _+699.0

lpbnb=plant (Bouteloua gracilis ), bacteria (Pseudomonas stutzeri) and bacterial-feeding nematode (Pelodera sp.). 2Values for Day 7 represent inoculum level. Replicate sampling to determine confidence intervals was not attempted. TABLE 2b Numbers of nematodes within the nonplant (bfn/) treatment and in rhizosphere and nonrhizosphere soil within the pbfn~ treatment (mean and 95 To confidence interval) modified from Ingham et al. {1985). Day

7 21 49 77 105

No. Aphelenchus per gram dry soil Nonrhizosphere

Rhizosphere

93 61.0_+ 41.9 42.2 _+20.6 7.2_+ 2.6 13.1-+ 9.6

93 154.6_+ 125.0 311.5 _+145.2 121.5_+ 59.4 142.4_+ 59.8

'bfnf=bacteria ( Pseudomonas paucimobilis ), fungus (Fusarium oxysporum ) and fungal-feeding nematode (Aphelenchus avenae ). 2pbfn[= plant (Bouteloua gracilis), bacteria, fungus and fungal-feeding nematode. 3Values for Day 7 represent inoculum level. Replicate sampling to determine confidence intervals was not attempted.

activity in controlled microcosm conditions ( B ~ t h et al., 1978, 1981; Coleman et al., 1983; Ingham et al., 1985). More recent work incorporates plant growth into the microcosm and enables us to measure carbon inputs and transformations over longer time spans as labile carbon is introduced continually via the root system. The following discussion reviews the results of several research projects in the U.S.A. and Europe. For both microfauna (protozoa) and mesofauna such as nematodes, significant nutrient returns were measured in several different research studies by Cole et al. (1978) and Woods et al. (1982).

126

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~..EarthwormsII Ench~rae,]_ldsM,cro,~,ropodsl I, c~o,3, oI~0, No Tillage Fig. 9 A and B. Conceptual models of detritus food webs in conventional-tillage (A) and no-tillage (B) agro-ecosystems. Boxes=nutrient storages; clouds=nutrient sources or sinks; arrows = nutrient transfer pathways. Valve symbols on arrows indicate that nutrient transfers are influenced by factors connected with dotted lines (from Hendrix et al.,1986).

128

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DAY Fig. 10. T o t a l f u n g i (nag -1 dry soil) at depths of 0 - 5 , 5 - 1 3 a n d 13-21 cm at Horseshoe Bend ( H S B ) research site July 1 9 8 6 - J u l y 1987. Error bars are + 1 $ E ( f r o m P.F. H e n d r i x , unpublished data).

Other studies (e.g. Elliott et al., 1979; Clarholm, 1985) showed significant increases in percentage nitrogen of dry plant material in microcosms containing amoebae and bacteria vs. those with bacteria alone. All microcosms contained growing blue grama (Boutelouagracilis) seedlings. Figure 7 shows plant growth responses over a considerable range of soil inorganic N from 50 to 250/~g of ammonium per gram soil. The biotic interactions enhanced percentage N and

129

TotalFungi HSBSummer1986

Surface Litter

600

=

i

i

i

i

NT

-*-_

._} Q 400 E .=

~

200

Control Captan i

=

4~0 8'0 ' 120 ' DaysafterApplication BuriedLitterTotal Fungi

~

HSB Summer1986

I

i

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i

1

i

i

800

CT

.J 6oo {3 E 400

~

Control Coptan

200

'

4'o

'

8'o

'

,~o

DaysafterApplication

Fig. 11. Total fungi in control and captan-treated micro-plots (4 m 2) at HSB, summer 1986. Error bars are + 1 SE (from M.H. Beare, unpublished data).

dry plant material significantly at the 0.05 level. More recent studies (summarized in Coleman et al., 1984; Ingham et al., 1985) showed enhanced total shoot biomass and total shoot N in microcosms containing plants and bacteria, or plants and bacteria and bacterial-feeding nematodes over a time span from 20 through 80 days in a 105-day experiment. These effects were more marked for bacteria (Fig. 8) than for fungi, possibly owing to the fact that the fungal species employed in our microcosms was a more rapid mineralizer of inorganic N. An additional factor of considerable interest in biota and organic-matter interactions is the fact that many of the soil invertebrates in the top 10 cm, if they are microbe-feeding, will tend to congregate in the rhizosphere region. Thus, Ingham et al. (1985) found that 60-70% of the total bacterial-feeding nematode population was in the less than 4% of total soil material which was truly rhizosphere in nature (Table 2a,b) i.e. less than 2 m m away from the root

130

SurfaceRyeLitterDecomposition IO0 C

•¢- 80 0

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40

Q

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HSB Summer

1986

' NT Capton -.~.--o

Control

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'

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Time(days) BuriedRye LitterDecomposition HSB

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1986 i

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'

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,~o

200

Time(days) Fig. 12. Per cent dry weight remaining in surface or buried rye litter bags, in control or captantreated micro-plots (4 m 2) at H S B , s u m m e r 1986. Error bars are _+1 S E {from M . H . Beare, unpublished data }.

surface. This relationship also applies to root growth. If roots grew in a regular fashion into the soil matrix, they would exhibit a regularly-spaced growth pattern. In fact, however, roots seem to grow more or less at random through the soil and then proliferate locally in zones with higher amounts of organic matter. This follows the sort of pattern one would expect from first exploring at random and then proliferating locally in a profusion of fine roots, and is described by a negative binomial distribution (St. John and Coleman, 1983). Further work by St. John et al. (1983a,b) has shown that mycorrhizal hyphae have a similar sort of growth pattern. We now turn to a brief overview of research in agro-ecosystems. There are important biological, as well as chemical and physical, differences between conventional tillage (CT) and no tillage (NT) (Phillips and Phillips, 1984; House et al., 1984; Groffman et al., 1987). The structural, abiotic and biotic characteristics change considerably, with more marked amounts of organic C, N and possibly P in the top 5 cm of the soil profile below the litter-layer in no tillage (Hendrix et al,. 1986).

131

As a result of the ideas presented in the review papers above, Holland and Coleman (1987) investigated the types and amounts of microbial populations which are present in the soil profile in the top 5 cm in CT and NT. Holland and Coleman (1987) found: (1) fungal biomass in surface-straw treatments ( NT ) was 144% of that in incorporated-straw (CT) treatments (Table 3 ); (2) using 14C-labelled wheat straw a greater proportion of added 14C was retained in the NT, than in the CT treatment; (3) maximum net N immobilization was higher and litter decomposition was slower in the surface straw than in the CT-straw treatments, even after one full year of field decomposition. The probable mechanism for gradual reduction of C:N ratio in the surface-applied wheat straw (C:N ratio 80:1 ) included transport of mineral N by fungal hyphae across hyphal "bridges", between the soil and the surface litter, as shown in Table 3. These results led Hendrix et al. (1986) to postulate two different types of food webs operative in various management regimes of row-crop agriculture, with CT more bacterially-dominated (Fig. 9a) and NT more fungally-dominated (Fig. 9b). Our results from experiments in 1986 show that, indeed, fungal populations (hyphal biomass) are higher in NT than in CT, in the top 5 cm, 5-13 and 13-21 cm (Fig. 10) (P.F. Hendrix, unpublished data). Several experiments are currently underway, in which we are experimentally manipulating key members of the biota. Our results with captan, as a general fungicide, are illustrative. M.H. Beare (unpublished data) found a 40-80% reduction in fungal hyphae (Fig. 11 ) and significantly decreased rates of litter decomposition (Fig 12). NEW AREAS OF RESEARCH IN SOIL ECOLOGY

There are several areas especially ready for new research in belowground ecology. The first of these includes tripartite associations such as roots, mycorrhiza and rhizobium or roots, mycorrhiza and actinorhiza (Rose and Youngberg, 1981). An additional area of research interest is the interaction between symbionts such as mycorrhiza or actinorrhiza and fauna which feed upon them. These feeding interactions may be positive or negative, although Warnock et al. (1982) and Finlay (1985) have demonstrated significantly reduced plant growth with presumed feeding by Collembola on VA mycorrhizae under field conditions. Recently, Moore et al. (1985) have shown that Collembola eat VA mycorrhizae hyphae and/or chlamydospores, as well. Recent studies by Read et al. (1985) and Chiariello et al. (1982) have also pointed out the community-level implications of between-species and between-family transfers of carbon and phosphorus between plants via mycorrhizal hyphae. It will be useful to ascertain whether transfers of nutrients other than C and P occur by the mechanisms noted above. There are three major conclusions to be drawn in this area of roots-microbes-fauna interactions and their impacts on organic-matter processes.

132 Firstly, a c o n s i d e r a t i o n of s o i l - p l a n t - m i c r o b i a l - f a u n a l assemblages a n d t h e i r i n t e r a c t i o n s in energy-rich, i.e. labile c a r b o n - c o n t a i n i n g zones, is i m p o r t a n t in e c o s y s t e m studies. Secondly, the s y s t e m a n d t h e feeding m o d e s of t h e various faunal groups affect n u t r i e n t t r a n s f o r m a t i o n s a n d rates of t u r n o v e r . T h i r d l y a n d finally, episodic p h e n o m e n a o c c u r r i n g at e n e r g y - r i c h zones of " t e n s i o n " such as roots a n d soil are i m p o r t a n t factors in s h o r t - t e r m d y n a m i c s over days to weeks a n d possibly have a significant i m p a c t on l o n g - t e r m s t r u c t u r a l characteristics o f soil systems. It will be b o t h i n t e r e s t i n g for basic scientific res e a r c h a n d useful for s u b s e q u e n t e c o s y s t e m m a n a g e m e n t to u n d e r s t a n d c o n s i d e r a b l y m o r e a b o u t t h e s e basic processes t h a t occur in this i n t e r e s t i n g a n d largely u n s e e n world of b e l o w g r o u n d ecology.

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