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Soil Biology & Biochemistry 32 (2000) 489±496
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Litter quality in¯uences on decomposition, ectomycorrhizal
community structure and mycorrhizal root surface acid
phosphatase activity
Christine Conn, John Dighton*
Rutgers University Pinelands Field Station, P.O. Box 206, New Lisbon, NJ, 08064, USA
Accepted 24 September 1999

Abstract
The in¯uence of litter quality on root growth, ectomycorrhizal communities and decay processes was investigated through a
litter bag experiment. Litter bags containing either pine needles, oak leaves or oak+pine mix were placed within the O horizon
of a lowland pitch pine (Pinus rigida ) forest in the New Jersey Pinelands. Upon retrieval, ingrown pine roots were removed and
quanti®ed for total length and percent ectomycorrhizal colonization by morphotype. Phosphatase activity was determined for
dominant morphotypes. In addition, litter decay rates and N and P litter content were measured. Mixed litter (oak+pine) had
highest total pine root ingrowth. Dominant ectomycorrhizal morphotypes di€ered in response to litter type. A tuberculate form
dominated (35%) in pine litters while distinctly di€erent nontuberculate morphotypes dominated in oak and mixed litters. High
phosphatase activity of morphotypes was correlated with high phosphorus immobilization during oak leaf decay. Results
indicate that a mix of forest litters (oak and pine) optimizes retention of scarce nutrients such as nitrogen and phosphorus. The
diverse chemical environment of these di€erent litter types induces di€erent ectomycorrhizal community development which

show functional di€erences in the way phosphorus is likely to be cycled. The in¯uence of litter type on diversity and function of
ectomycorhizae is an important step in identifying linkages between biodiversity of this group and ecosystem functions. 7 2000
Elsevier Science Ltd. All rights reserved.
Keywords: Litter decay; Oak+pine forest; Phosphorus cycling; Mycorrhiza

1. Introduction
The development of mycorrhizae increases the ability of roots to absorb nutrients and water from the
soil environment. The degree to which this ability is
enhanced depends both on the extent of mycorrhizal
colonization and the unique functional attributes of
the mycorrhizal fungal species involved. Community
structure of ectomycorrhizas on a root system may be
related to nutrient uptake eciency if di€erent mycorrhizal species have di€ering abilities to sequester nutri-

* Corresponding author. Tel.: +1-609-894-8849; fax: +1-609-8940472.
E-mail address: dighton@crab.rutgers.edu (J. Dighton).

ents from the soil solution (Dighton, 1995). The
structure of the ectomycorrhizal community is in¯uenced by competitive interactions between the colonizing mycorrhizal fungi and, possibly, between
mycorrhizal and saprotrophic fungal species (Shaw et

al., 1995). Edaphic factors, such as anthropogenic pollution, also have been shown to in¯uence mycorrhizal
abundance and community structure. Dighton and
Skengton (1985) showed that acidifying pollutants
altered ectomycorrhizal community structure by reducing abundance of species producing large amounts of
extramatrical mycelium. Other e€ects of acidifying pollutants on mycorrhizal communities are reported in
Jansen et al. (1988) and are modeled in Dighton and
Jansen (1991). Nitrogen amendment in a spruce forest
produced di€erent ectomycorrhizal species composition

0038-0717/00/$ - see front matter 7 2000 Elsevier Science Ltd. All rights reserved.
PII: S 0 0 3 8 - 0 7 1 7 ( 9 9 ) 0 0 1 7 8 - 9

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C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

and decreased root tip number in relation to an unamended community as observed by mycorrhizal morphology (Alexander and Fairley, 1983) and molecular
taxonomy (KaÊreÂn and Nylund, 1997). Increased soil
nitrogen and phosphorus can also reduce ectomycorrhizal development (Brun et al., 1995) and increase
root growth (Pregitzer et al., 1993; Weber and Day,

1996).
Heterogeneity of resource units in soil as an in¯uencing factor has been less well documented. Pregitzer et
al. (1993) have shown that patchiness of nutrient addition to soil altered root growth patterns and Baar et
al. (1994) showed that removal of litter and humus
from the forest ¯oor altered the pattern of distribution
of Laccaria bicolor sporophore production. This e€ect
could be manifest through altered nutrient availability
or as a result of the in¯uence of leaf litter extracts on
fungal growth. Soluble litter extracts have been shown
to stimulate or inhibit mycorrhizal fungal activity
(Baar et al., 1994; Michelsen et al., 1995; Koide et al.,
1998).
Di€erences in ectomycorrhizal eciency have been
suspected, but not clearly demonstrated in the ®eld.
Dighton et al. (1990) found di€erent phosphorus
uptake rates from soil pools to the tree canopy among
various ectomycorrhizal communities. In addition,
mycorrhizal enzymes may be able to directly in¯uence
nutrient cycling by acquiring both nitrogen and phosphorus from complex organic forms (Dighton, 1991;
Read, 1991).

Plant communities of the New Jersey pine barrens
have a nearly total reliance on mycorrhizal associations to obtain and conserve limiting nutrients and
water. We have speci®cally addressed the role litter
quality has on root growth and ectomycorrhizal development and how these factors integrate to a€ect ecosystem nutrient cycling. Speci®c null hypotheses were
(i) leaf litter decomposition rate is the same between
leaf litter species, (ii) leaf litter type does not a€ect
root growth into that litter and (iii) leaf litter type
does not in¯uence ectomycorrhizal species composition
and their enzyme expression.

2. Material and methods
2.1. Site description
The New Jersey Pinelands are located on the southeastern coastal plain of New Jersey, USA. Soils are
sandy and oligotrophic (total N: 0.5±3 g kgÿ1, Olson
extractable P: 70±140 mg kgÿ1); see Tedrow (1979) and
Markley (1979). Pinelands communities consist of
upland forests dominated by pitch pine (Pinus rigida )
and various oak species (Quercus alba, Q. velutina, Q.
ilicifolia, Q. marilandica, etc.) with lowland stands

dominated by pitch pine forests, red maple swamps
(Acer rubrum ) or Atlantic white cedar swamps (Chamaecyparis thyoides ). Understory ¯ora is primarily ericaceous,
represented
by
various
huckleberry
(Gaylussacia ) and blueberry (Vaccinium ) species
(McCormick, 1979). Mycorrhizal regulation of nutrient
cycles is considered very important in this nutrient
poor ecosystem, where interception of mineralized
nutrients in the organic horizons is of great importance. The study site was located in a lowland pitch
pine forest. Soil pH ranged from 3.4 to 3.8 with a 5±
10 cm deep organic horizon over sand.
2.2. Litter decomposition experiments and root ingrowth
Oak and pine litter was gathered from the forest
¯oor in January 1995, dried at 708C for 48 h and
placed in 1 mm mesh nylon litter bags. Bags contained
a total of 5 g of leaf material comprised of either pine
needles (pure pine), oak leaves (pure oak) or a mix of
oak and pine (2.5 g oak, 2.5 g pine). The mixed species

bags were included because these two litters do cooccur extensively and it was hypothesized that important interactions may be present that could not be
quanti®ed by the single species approach. Seven 2.25
m2 plots were located in close proximity to mature
pine trees in order to maximize encounters between
pine roots and litter bags. Equal numbers of bags for
each litter treatment were randomly located in each
plot. Half of the bags were placed on the forest ¯oor
and the remaining half were buried at the interface
between the organic and mineral horizon on 23 February 1995. Subsets of bags were recovered on 25 May,
17 August and 9 November (13, 27 and 41 weeks, respectively). A total of seven replicate bags were harvested on each sampling occasion. For each sampling
event, we only retrieved the number of bags on a daily
basis that could be processed that day in order to
reduce any experimental error due to root aging in the
phosphatase enzyme assay. The entire sampling e€ort
lasted for less than 1 week.
Extracted litter bags were brie¯y rinsed with tap
water to remove any adhering sand. Roots that had
grown into bags were removed by careful dissection of
the litter after opening the bags. Litter was dried at
708C for 48 h and weighed to determine percent mass

loss. Phosphorus and nitrogen content of initial litter
and decayed litter were determined by the Kjeldahl
(N) and molybdate blue (P) methods (Allen, 1989).
Oak and pine fractions from mixed species bags were
analyzed separately in order to determine changes in
chemistry (nutrient loss or gain) in each leaf species
within the mixed litter bags.
Total length of ingrown pine roots from the litter
bags was measured using the line intersect method of
Tennant (1975). Ectomycorrhizal community structure

C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

was determined by morphotype identi®cation of all
root tips and expressed as a percentage of the total
number of root tips. Classi®cation was based on color
and gross sheath morphology, following the methods
of Agerer (1987) and Ingleby et al. (1990).
2.3. Acid phosphatase activity of ectomycorrhizas
Immediately following ectomycorrhizal classi®cation,

acid phosphatase activity of root tips of each of the
dominant ectomycorrhizal morphotypes were assayed
following the methods used by Dighton and Coleman
(1992). The phosphatase assay was used as an indicator for linkages between functional attributes of
mycorrhizae and their chemical environment. The
phosphatase assay measures the amount of phosphate
cleaved from an organophosphate ( p-nitrophenol
phosphate). Root tip volume (diameter and mycorrhizal unit length measured using an eyepiece graticule in
a steromicroscope) was measured in order to express
enzyme activity as mg nitrophenol per mm2 root tip
produced.
2.4. Litter decay measurements and fungal development
The decay dynamics of litter in bags placed aboveground were compared against bags of litter placed
below-ground under the assumption that fungal in¯uences on decay and nutrient ¯ux from litter would be
greater below-ground, especially within the mycorrhizal group. Subsamples of the decomposed litter were
analyzed for hyphal length. Fungal hyphal lengths
were measured by homogenizing a 1-g sample of leaf
material in a blender in 1 l of sterile water. Five 1-ml
aliquots were ®ltered through membrane ®lters (0.25
mm pore size), stained with Loe¯er's methylene blue,

mounted in immersion oil. Fungal hyphal length was
measured using a grid-line intersect procedure (Frankland et al., 1990). Litter hyphal length may suggest
how desirable these substrates were for fungal utilization.

491

3. Results
Analysis of variance (three-way ANOVA) showed
that leaf litter decomposition was signi®cantly greater
in leaf litter placed below-ground (P < 0.001; F ˆ
71:09† (Fig. 1). Overall, there was a signi®cant loss of
mass over time (P < 0.01; F ˆ 62:2). Although there
were no signi®cant di€erences between decomposition
rates of litter types overall (P > 0.05; F ˆ 1:52). The
presence of pine needles aboveground increased the
rate of oak leaf decomposition (mixed oak). The presence of oak leaves had no e€ect on the decay of pine
needles. However, the opposite pattern occurred
below-ground. Oak leaves increased pine needle decay,
while the presence of pine needles had no e€ect on the
decay of oak leaves. These di€erences in response

account for the signi®cant (P < 0.05; F ˆ 4:5† depth 
time interaction of the ANOVA.
Initial nitrogen content was higher (P < 0.01 by ttest) in oak leaves (1.61 2 0.22 mg gÿ1) than pine needles (0.2920.03 mg gÿ1). When changing nutrient content is coupled with decay rate, patterns of nutrient
immobilization or mineralization can be detected.
Nitrogen immobilization refers to a net increase in the
absolute amounts of nitrogen (>100% initial nitrogen
remaining). This generally occurs in litters that are

2.5. Statistics
All data were analyzed using three-way ANOVA or
GLM sequences of SAS (SAS, 1990). Pair-wise mean
separation was determined using Tukey's Honestly Signi®cant Di€erence Test. Data pertaining to leaf litter
mass loss and litter chemistry were separated into component litter species (i.e. oak, pine, oak in oak/pine
mixture and pine in oak/pine mixture) yielding a total
of 168 samples. Data regarding root length were analyzed on a per litter bag basis, yielding 126 samples
and phosphatase activity based on the number (variable) of root tips of each morphotype available within
any one litter bag.

Fig. 1. Leaf litter decomposition (expressed as percent mass remaining) of single and mixed pine and oak litter in litter bags placed on
the soil surface or buried in the organic horizon of New Jersey pine

barrens soil. Data points are means of seven replicates 2 standard
error.

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C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

nitrogen poor and can re¯ect nitrogen limited decay.
Mineralization refers to the net release of a nutrient
( 0.05;
F ˆ 2:18), but two-way analysis within the belowground litter bags showed that fungal hyphal colonization of pine litter alone was signi®cantly less than oak
or oak in oak/pine mix (P < 0.01; F ˆ 4:34). There
was signi®cantly greater fungal colonization of litter
decaying below-ground (P < 0.01; F ˆ 6:6), suggesting
greater fungal utilization of leaf substrate resources
below-ground than aboveground (Fig. 4). There were

Fig. 2. Nitrogen content of single and mixed pine and oak litter in
litter bags placed on the soil surface or buried in the organic horizon
of New Jersey pine barrens soil. Data points are means of seven
replicates2standard error.

Fig. 3. Phosphorus content of single and mixed pine and oak litter in
litter bags placed on the soil surface or buried in the organic horizon
of New Jersey pine barrens soil. Data points are means of seven
replicates2standard error.

C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

493

Fig. 5. Ectomycorrhizal morphotype categories associated with roots
colonizing single and mixed pine and oak litter in litter bags buried
in the organic horizon of New Jersey pine barrens soil after 41
weeks.

Fig. 4. Fungal hyphal length associated with single and mixed pine
and oak litter in litter bags placed on the soil surface or buried in
the organic horizon of New Jersey pine barrens soil. Data points are
means of seven replicates2standard error.

signi®cantly more hyphae in the ®nal harvest than
either of the ®rst or second (P < 0.001; F ˆ 83:98).
Discussion of pine root colonization and mycorrhizal classi®cation is necessarily con®ned to litter bags
placed below-ground since root ingrowth did not
occur aboveground. The root ingrowth data presented
is limited to the third sampling interval since root
ingrowth was universally absent during the ®rst
sampling date and absent from many litter bags for
the second sampling date. More root ingrowth
occurred in mixed species litter bags (425.02155.5 mm
per bag) than in single species litter bags (oak 218.6 2

59.0; pine 230.6 2 68.6 mm per bag), but this was not
statistically signi®cant …P ˆ 0:31; F ˆ 1:24). Of the
ectomycorrhizal morphotypes identi®ed, the ®ve most
abundant (90% of all ectomycorrhizae) are described
in Table 1. The other mycorrhizae were lumped
together in a ``miscellaneous'' category. Each litter
type was dominated by a di€erent mycorrhizal morphotype (Fig. 5). Types 2 and 3 dominated root tips
invading pure oak leaves while Type 10 dominated
root tips invading pure pine needles. Roots in mixed
oak and pine litter supported a mycorrhizal ¯ora
dominated by type 4.
Phosphatase activity measures the potential to cleave
inorganic phosphate from an organic molecule. Table 2
shows the phosphatase activity of the main mycorrhizal morphotypes. The highest rates of phosphatase activity were associated with the morphotypes (types 2, 3
and 4) most common on root tips in¯uenced by oak
leaves and, consequently, to litter that immobilized
phosphate in organic forms. Root tips associated with
pure pine needles, which show rapid losses of phosphorus, were dominated by type 10 mycorrhizae which
had signi®cantly lower phosphatase activity than type
4 and slightly less phosphatase activity than types 2
and 3. Type 1 was non-mycorrhizal and had the lowest
phosphatase activity. The in¯uence of rapid P mineralization from pine leaves on the phosphatase enzyme
production by roots is suggested by the signi®cant reduction in phosphatase production in oak/pine mixed

Table 1
Mycorrhizal morphotype classi®cation
Morphotype

Description

Type
Type
Type
Type
Type
Type

non-mycorrhizal
cream mantle, white granular hyphae with clamp connections, outer sheath loosely woven
cream mantle, cream rhizomorphs, slightly granular hyphae with clamp connections, hyphal dia > type 2
Black mantle, black wirey hyphae, club shaped tip
rusty brown mantle, no hyphae, sheath loose prosenchyma
tuberculate, frosty white mantle, black non-granular hyphae

1
2
3
6
4
10

494

C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

litter compared to oak alone (226 2 125, 301 2 165 ng
p-nitrophenol mmÿ2 root surface, respectively, P <
0.05) and a lower, though not signi®cant, activity in
pine alone (2712194 ng p-nitrophenol mmÿ2 root surface). From the analysis of variance, there was a signi®cant litter  mycorrhizal interaction for
phosphatase activity. This could be explained by the
di€ering response of the same mycorrhizal type to
di€erent leaf litters. For example, type 1 showed similar enzyme activity between leaf litter types (125 2 52,
121256, 121277 ng p-nitrophenol mmÿ2 root surface
in oak, oak±pine and pine, respectively). Type 6 is a
mycorrhizal morphotype that occurred in low abundance in all leaf litter types. Type 6 showed highest
levels of activity when in the presence of oak leaves
alone (300 2 160, 135 2 49, 153 2 40 ng p-nitrophenol
mmÿ2 root surface in oak, oak±pine and pine, respectively). Type 4 exhibited lowest activity on oak±pine
mixed litter (4712115, 196236, 5642296 ng p-nitrophenol mmÿ2 root surface in oak, oak±pine and pine,
respectively).

4. Discussion
Our study has shown that, aboveground, decomposition of oak leaves is slower than that of pine needles
or of oak in combination with pine needles. However,
there is no di€erence below-ground in the decomposition rates. Pine needles represent a source of easily
mobilized phosphorus while oak leaves serve as a
phosphorus sink. Both litter types immobilize nitrogen,
but this immobilization is signi®cantly greater in pine
than oak. Litter quality di€erences in¯uence the turnover of organic matter in the Pinelands ecosystem.
Pure and mixed litters decompose at di€erent rates
and these patterns di€er in response to placement
above or below ground. It was hypothesized that faster
decay would be related to greater hyphal length.
Indeed there was a signi®cantly higher fungal biomass
on litter placed below ground, where decomposition
was accelerated, but there were no di€erences between
leaf litter types. Resources of di€ering nutrient content

have been shown to in¯uence fungal colonization
(Rayner, 1991; Ritz, 1995) by the in¯uence of di€erent
hyphal growth rates and branching patterns.
Although root growth into litter bags containing a
mixture of oak and pine was greater than single litter
species, the di€erence was not statistically signi®cant.
This enhanced root growth suggests that patches of
high resource diversity encourage root production.
Di€erential rates of root growth into patches of soil
with di€erent nutrient contents has been shown by
Pregitzer et al. (1993), Eissenstat and Van Rees (1994)
and Barber (1995). In the case of di€erences in root
growth into litter bags, a number of interacting factors
may be present, including availability of nutrients,
water relations, physical constraints on root growth
and allelopathic chemical leaching from the litter
(Michelsen et al., 1995).
We found that ectomycorrhizal community structure
also responds to patches of resource diversity. Ectomycorrhizal species composition was di€erent between
leaf litter types. J. Baar (unpublished Ph.D. thesis,
University of Wageningen, 1995) and Baar et al.
(1994) showed signi®cant e€ects of leaf litter and
humus on the ectomycorrhizal community structure of
Scots pine. Koide et al. (1998) has shown di€erential
response of ectomycorrhizal fungal hyphal growth to
leaf litter extracts, with growth of some species being
suppressed whilst being promoted in other species.
Michelsen et al. (1995) showed that leaf litter extracts
a€ected nutrient acquisition by mycorrhizal plants.
Ectomycorrhizal root surface acid phosphatase activity has been shown to di€er between fungal species.
In this study, we have shown that our morphotype 4
produced signi®cantly more phosphatase than types 1,
6 and 10. When combined with the distribution of
morphotypes within the di€erent litter types, a pattern
emerges of the presence of greater abundance of phosphatase producing morphotypes (especially type 4 in
oak litter and types 2 and 3 in the oak/pine litter mixture) where P immobilization is greatest. It is
suggested, therefore, that the greater amounts of organically-bound phosphorus in decaying oak leaves may
be a factor selecting for phosphatase producing ecto-

Table 2
Acid phosphatase activity (ng p-nitrophenol mmÿ2 root surface area) of the main ectomycorrhizal morphotypes from litter bags and from litter
types. Means within columns sharing identical superscripted letters are not signi®cantly di€erent from each other p ˆ 0:05: (Tukey's Honestly
Signi®cant Di€erences test)
Mycorrhizal morphotype

Phosphatase mean2S.E.

Litter type

Phosphatase mean2S.E.

1
2
3
4
6
10

100211a
270215b
370238bc
420254c
204243ab
192228ab

oak
oak/pine
pine

301225a
226219bc
194230ac

C. Conn, J. Dighton / Soil Biology & Biochemistry 32 (2000) 489±496

mycorrhizal species. The di€erent litters of this experiment demonstrated very di€erent nutrient dynamics.
Pine needles are low in nitrogen and high in phosphorus. Phosphorus is rapidly lost, presumably as leachate, while nitrogen is conserved and accumulated via
immobilization. Oak leaves, initially higher in nitrogen
and lower in phosphorus, did not exhibit a net loss of
nitrogen and accumulated phosphorus. It may be that
decaying oak leaves represent a biological sink for
phosphorus leached from pine leaves. These varying
chemical environments are likely to select for di€erent
ectomycorrhizal species. Mycorrhizae with high phosphatase activity are better suited to utilize immobilized
phosphorus and were, therefore, associated more
strongly with oak litters.
In mixed species forest, the distribution of leaf litter
on the forest ¯oor is heterogeneous. The nature of litter patches may have e€ects on the soil biota below it.
In an unpublished study, we (Dighton et al.) have
found that the distribution of litter patches in the New
Jersey upland oak±pine habitats of the pine barrens is
related to litter dams created by stems of the ericaceous understory community. Litter patch size (area)
was positively correlated …r2 ˆ 0:908† with the density
of ericaceous stems. Small litter patches contained a
higher percentage contribution (by weight) of pine needles and large patches contained a higher percentage
contribution of oak leaves. Large litter patches were
also found to have a higher Simpson's diversity index
of ectomycorrhizal species than small patches. Our
results suggest one mechanism (selective chemical environment) by which litter patches of varying composition could in¯uence mycorrhizal diversity.
Forming links between biodiversity and function
was one of the main areas of perceived future research
in soil microbiology (Coleman et al., 1994). In this
paper we have shown that environmental factors can
signi®cantly a€ect ectomycorrhizal community structure. These micro-spatial changes in communities are
related to changes in physical and chemical properties
of the environment. We have also provided preliminary evidence of di€ering functional attributes of the
resultant ectomycorrhizal community developing
within leaf litter patches of di€ering resource quality.
This function has been expressed as root surface phosphatase enzyme production, but represents possible
wider overall physiological competence of di€erent
ectomycorrhizal communities (see also Dighton et al.,
1990).

Acknowledgements
We would like to thank The Victoria Foundation
for supporting Christine Conn's postdoctoral fellowship and Dennis Gray for his assistance with the

495

chemical analyses. We would also like to thank two
anonymous reviewers for their constructive comments
on the original draft of this paper.

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