Download Mycorrhizae and succession in plantings of beachgrass in sand dunes

Mycorrhizae and Succession in Plantings of Beachgrass in Sand Dunes
Author(s): R. E. Koske and J. N. Gemma
Source: American Journal of Botany, Vol. 84, No. 1 (Jan., 1997), pp. 118-130
Published by: Botanical Society of America
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AmericanJournalof Botany 84(1): 118-130. 1997.
MYCORRHIZAE AND SUCCESSION IN PLANTINGS OF
BEACHGRASS IN SAND DUNES1
R. E. KOSKE2 AND J. N. GEMMA
Departmentof Biological Sciences, Universityof Rhode Island, Kingston,Rhode Island 02881-0816
A survey of arbuscularmycorrhizalfungi (AMF), arbuscularmycorrhizae(AM), and hyphal networksof AMF was
carriedout in sand dune sites of different
successional stages in the Province Lands Area of Cape Cod National Seashore,
Massachusetts.The studyfocused on large-scaleplantings(each of 12-20 ha) of Americanbeachgrass (Ammophilabreviligulata) aged 0-7 yr and fiveadjacent naturaldune areas. Sample sites rangedin vegetativecover frombarrento forested.
Spores of 17 species of AMF were recoveredfromthe dunes. Over the successional sequence, therewere increases in the
richnessand spore populationsof the AMF community,the extentof colonization of A. breviligulataroots, and the mycorrhizalinoculum potentialof the soil. Unvegetatedsites lacked propagules of AMF, but roots of planted culms of A.
breviligulata(which carriedpropagulesof AMF) became mycorrhizalin <1 yr afterplanting.Spores were recoveredfrom
previouslyAMF-free sites thathad been planted with beachgrass for47 wk, and five species of AMF sporulatedin sites
<6 yr old. Significanthyphalnetworkswere not presentin any of the planted areas (<6 yr old at the time of sampling),
but did occur in naturalareas. The rate of invasion of areas plantedto A. breviligulataby later successional plant species
may in partdepend upon the establishmentof a vigorousnetworkof hyphaeof AMF in a site.
Key words: Ammophilabreviligulata;arbuscularmycorrhizae;hyphalnetwork;plant succession; Poaceae; sand dunes.
Since 1959, the possible importanceof arbuscularmy- inhabitantsof Cape Cod for more than threecenturies.
Prior to the arrivalof European colonists in the 1600s,
corrhizalfungi(AMF) in sand dune succession has been
recognized,and numeroussurveyshave shown AMF to
the area consisted of foresteddunes. Destructionof the
forestand damage by grazinglivestockin the following
be routineinhabitantsof temperateand tropicaldune sites
centurypermittedthe formerlystabilized dunes to bein coastal and inland dunes throughoutthe world (e.g.,
Nicolson, 1960; Koske and Polson, 1984; Giovannetti, come mobile again and led to the currentproblemswith
drifting
sand (McCaffreyand Leatherman,1979). Human
1985; Puppi and Riess, 1987; Rose, 1988; Read, 1989;
uses of the mobile dunes for recreationhave prevented
Koske and Gemma, 1990, 1992, 1996; Sturmerand Bellei, 1994; Al-Agely and Reeves, 1995). In these primary re-establishmentof sufficientvegetation to slow the
successional sites, AMF arriveearly,oftenwiththe first movementof the sand. Inundationof roads, buildings,
and adjacent forestsand the fillingin of Provincetown
plant colonizers (Nicolson, 1960; Sylvia and Will, 1988;
Harbor and PilgrimLake by wind-blownsand are longGemma and Koske, 1989, 1992; Koske and Gemma,
standingproblemsin the area.
1990).
Vegetation is an effectivemeans of slowing sand
The developmentof the belowgroundAMF commumovementin dunes (e.g., Jagschitzand Bell, 1966; Rannity is closely linked to aboveground vegetational
changes duringcolonizationand succession. In a variety well, 1972; Woodhouse, 1982), and large plantingshave
been made on Cape Cod for this purpose since at least
of naturalsites,AMF have been foundto play a vitalrole
1825 (Thoreau, 1865; Strahler,1966). The most recent
in plant succession, affectingthe success not only of obmajor plantingshave been made in the Province Lands
ligatelymycotrophicspecies, but also of species thatare
Dunes Area of Cape Cod National Seashore (CCNS).
Defacultativelymycotrophicand even nonmycotrophic.
75 ha of American beachgrass (Ammopending on the level of disturbanceand existingplant Since 1985,
phila breviligulataFern.) have been planted (in 1985,
populationin a site,the abilityof plantspecies to become
1988, 1989, and 1990) in a programadministeredby the
establishedafterdispersalto the site is determinedin part
National Park Service (NPS).
by thepopulationof AMF in the soil (Miller,1979, 1987;
Careful record keeping of the historyof plantingsin
Reeves et al., 1979; Janos,1980; Grimeet al., 1987; Read
clearly identifiableareas by the NPS in The Province
and Birch, 1988; Gemma and Koske, 1990, 1992; Koske
Lands Dunes site of CCNS offereda unique opportunity
and Gemma, 1990; Gange, Brown, and Sinclair, 1993;
to studythe dynamicsof primarysuccession in the earFrancis and Read, 1994, 1995).
Stabilizationof large,mobile dune fieldshas concerned liest seral stages (spanning 7 yr) in large plantingsof
beachgrass.The purposeof the studiesreportedhere was
1
to documentthe species of AMF presentin thedunes and
Manuscriptreceived 5 January 1996; revision accepted 22 July
1996.
to identifychanges occurringin the AMF communityas
The authorsthankMr. JimKillian and Dr. Charles Roman forlogiswell as theinoculumpotentialof the dune soil duringthe
tical support,advice, and encouragementforthestudy;Dr. Eric Roberts,
early stages of primarysuccession of the plant commuDr. David Berlinsky,Dr. Noel Jackson,Dr. Paul Godfrey,Dr. Alison
nity.
Roberts,ChristinLambiase, Rachel Maher,Ronnie LaBarbera, and Tom
Bellohusen for assistance; and Dr. Keith Killingbeckfor assistance in
the plants.This researchwas supportedby a grantfromthe
identifying
CooperativePark Studies Unit of the National Park Service.
2
Authorforcorrespondence.
MATERIALS AND METHODS
Study site-Studies were performedin an area measuring -4 X 1
km in the ProvinceLands Dunes regionof CCNS (70?8.5'W, 42?4.0'N)
118
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January
1997]
KOSKE
near Provincetown,MA. The vegetationand ecological processes occumng in theCape Cod dunes are similarto those in dunes along much*
of the NorthAtlanticseaboard of the U.S. (Godfrey,1977; Godfrey,
Leathermanand Zaremba, 1979; Woodhouse, 1982). The geology of
the area is described by Strahler(1966). The Province Lands Dunes
comprise a varietyof dune systemsin various stages of succession.
Large mobile dunes up to 32 m high are interspersedamong smaller,
more densely vegetatedareas (Strahler,1966). In the mobile dunes,the
dominantplant species is A. breviligulata.Early invadersof A. breviligulata-dominatedsites are Polygonella articulata(L.) Meisn. and Solidago sempervirensL. Later successional sites are characterizedby the
grass Deschampsia flexuosa (L.) Trin.,the shrubsMyricapensylvanica
Loisel. and Prunus maritimaMarsh., the trees Pinus rigida Mill. and
Quercus ilicifolia Wang., and otherspecies (Svenson and Pyle, 1979;
Whatley,1988). A forestof mixed deciduous trees and shrubs is the
most advanced successional stage in the area.
Our studiesfocused on areas plantedin 1985, 1988, 1989, and 1990
(Figs. 1-4). Each plantingcovered 12-20 ha, and had been free of
vegetationfor >5 yr priorto planting.Vegetationin the planted areas
had a highlyregulardistribution.During NPS-supervised plantingon
the dunes, threecleaned culms (tillerswith roots and dead leaves removed) of A. breviligulatacv. Cape were insertedin a hole 20 cm deep,
and the soil was packed aroundthe culms. Such a groupof threeculms
is termeda "hill." Hills in the dunes were planted46 cm apartin rows.
The rows run in an east-westdirection(parallel to the shore) and are
spaced 46 cm apart.Hills in adjacent rows were staggered.At thecom-*
36 kg/haof a pelletizedIO:10: IOV
pletionof eachoftheNPS plantings,
119
IN SAND DUNES
AND GEMMA-MYCORRHIZAE
. -w.
_
a
__
t
ii
iL.
j
1
-
F
'
't
_
"'
0iW+ f.4
^
5_aS
.2
was add-Y
fertilizer
were applied by broadcasting.No additionalfertilizer
pet
of each of th N
ed.
The ProvinceLands plantingsare located 0.5-1.3 km fromthebeach,
and separated fromit by a series of dune ridges. Movement of sand
fromthe beaches inland to the plantingsites is uneven,and most sites
appear to receive very little sand deposition (Godfrey,Fowler and
Stack, 1991), resultingin a gradualdecline in the vigorof theplantings
(Eldred and Maun, 1982; Disraeli, 1984; Godfrey,Fowler,and Stack,
j'At
J4
X
*.
.
i
v
..
2
1991).
I
In addition to the plantingsof 1985-1990, we also sampled some
seralstages
nearbynaturalareasof thedunes(Sites 1-5) in different
forcomparison.These areas were naturallyvegetated,but had not been
plantedby the NPS. Site 1 (Fig. 5) was a vigorous stand of A. breviligulata located between NPS plantingareas of 1988 and 1989. This
area had been previously identifiedby Godfrey,Fowler, and Stack
(1991) as a native stand of beachgrass.Sand accretionwas high at this
site,organicmatterwas low, and invadingspecies were veryrare.Sites
2 and 3 (Fig. 6) were dominatedby decliningstandsof A. breviligulata
and representedslightlylatersuccessional stages. In additionto A. brev-
_
3
iligulata,areas2 and 3 wereverysparselycolonizedbyAchilleamil-
lefoliumL., Aster linariifoliusL., Deschampsia flexuosa, Myrica pensylvanica,Prunus maritima,Polygonella articulata,Quercus ilicifolia,
Rosa rugosa Thunb., Solidago nemoralis Ait., S. odora Ait., and S.
sempervirens.Site 4 (Fig. 7) had 98% cover by A. breviligulataand
numerousvigorouslyinvadingspecies (e.g., Myricapensylvanica,Rosa
rugosa,Artemisiaborealis Pall., Deschampsia flexuosa,Daucus carota
L., Hieracium canadense Michx., and Kalmia angustifoliaL., Pinus
rigida,and Q. ilicifolia).Site 5 was forestedwithAcer rubrum,Quercus
spp., Sassafras albidum, and an understoryof shrubs (e.g., Clethera
.4
r
-
s
4
.'_-',
4
S
it
.
3
'
'4w
-
.
i
.
4>
A
f
.
j4
r
'.
--
WK+f:#
_
t
=
-
_
Figs. 1-4. Plantingsof Ammophilabreviligulataon ProvinceLands
Dunes. 1. 1990 planting(age 1 yr). Sparse area near centerwas planted
withone culm per hill insteadof the usual threeper hill. 2. 1989 plant-'Jc
ing (age 2 yr). This plantingsufferedextensivewinterkilla few months_i
afterplanting.Note manydead individualsin some rows. 3. 1988 plant- ^ - :
ing (age 3 yr). 4. 1985 planting(age 6.5 yr). Note low vigorand cover 4,.
in thisdecliningstand. 3 - ;Lw
trlt
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120
AMERICAN JOURNAL OF BOTANY
[Vol. 84
Sampling-Sampling for AMF, arbuscularmycorrhizae(AM), vegwas carriedout in 1990 and 1991 using
etation,and soil characteristics
randomsamplingtechniques(Mueller-Domboisand Ellenberg,
stratified
1974; Koske and Gemma, 1992). The most extensive sampling was
carriedout in the planted areas thatwere of known age. Sampling of
natural areas was less comprehensive,and those data were gathered
mainlyforcomparisonto resultsfromthe plantedsites.
To ensure thatany changes in vegetativecover, vigor,etc. were not
the resultof pathogensor pests, we had Dr. Noel Jackson,a plant pathologistat the Universityof Rhode Island, examine A. breviligulata
plantsfromthe NPS plantingsand fromsome naturalareas in November 1990, February 1991, March 1991, and August 1991. He looked
specificallyforchinchbugs, rootcystnematodes,stripedsmut,and root
aphids. No significantoccurrencesof any of these pests were found.
~~~~~~
.
F
I
-'V
7~
Soil characteristics-Most soil samples were collected in October
1990 forphysicalanalysis. Samples at the 1990 plantingsite were collected a few days beforeplanting(October) and just afterplantingand
fertilization(November). The upper 15 cm of sand at each sampling
point was scraped away, and a sample (- 1 L) was collected by insertinga clean trowelto a depthof 15 cm and removingthe soil. Thus
the sample includedonly soil thatoccurredin the zone between 15 and
30 cm below the originalsoil surface.Soil pH was measuredin a soil:
waterslurry(1:2) witha pH meteraftera 20-minequilibration,organic
at 400?C for6 h, and theother
matterwas measuredby loss-on-ignition
parameterswere measured by the Soil Testing Service, Universityof
Rhode Island CooperativeExtensionService.
AMF community-The AMF communitypresentin the soil at the
time of sampling was assessed by directcounts of spores fromeach
area in the dune system. Fifteen soil samples were collected on 12
October 1990 fromeach of the four plantingsites (1985-1990) and
h'h
fromarea 2. The collections fromthe 1990 plantingarea were taken
beforethe plantingoccurred.In October 1991 additionalsamples were
collected fromthefollowingsites: 1990 plantingarea (12 samples), site
'1~~~~~~~~~~~~~~~~~~1
3 (eightsamples), site4 (13 samples), and site 5 (fivesamples). Samples
were collected in the fall because spore populations in New England
(Gemma and Koske,
dunes typicallyreach theirmaximumin fall/winter
1988; Gemma, Koske and Carreiro,1989).
Prior to collection of root zone samples, the upper 20-25 cm of
:s~~~~~~~~~~~~~~~~~~~~~soil in which few roots occur were removed and discarded. A trowel
was thenused to excavate soil (- 1 L) and roots fromthe bottomof
the hole. Spores of AMF were recovered fromsoil samples by wet(Walker,Mize, and McNabb, 1982). All the
sieving and centrifugation
spores containedin an 85-mL soil sample were placed on a 5.5 cm filter
paper -aftercentrifugationand then transferredto glass microscope
slides. Spores were mountedin a polyvinylalcohol mountingsolution
(Koske and Tessier, 1983) asndidentifiedat 400-1000X. Species idenspecimens.Vouchtitieswere confirmedby comparisonto authenticated
ers have been preservedin the authors' collections. All spore counts
were convertedto numberof spores per 100 mL soil.
Figs. 5-7. Naturaldune areas in the ProvinceLands Dunes. 5. Site
1. A vigorous, floweringstand of Ammophilabreviligulatais shown.
Lightband at top of dune indicatesthe numerousinflorescences.6. Site
2. Ammophilain decline, some invadingspecies present.7. Site 4. Note
high cover.Ammophiladominates,but otherspecies are common.
alnifoliaL., Gaylussacia baccata (Wang.) K. Koch). Soil organicmatter
and diversitywere high. The naturalsites were ranked 1, 2, 3, 4, and
5 fromearliestto latest in a successional sequence on the basis of soil
organic matter,incidence of invadingspecies, and vigor of A. breviligulata (Koske and Gemma, 1992).
Mycorrfiizalstatus of plants-The extentof mycorrhizalcolonization in plantingsof A. breviligulataand in invadingspecies of plants
was measured.Four fieldsurveyswere carriedout to assess the extent
of AM in A. breviligulatain sites of different
ages and to determine
when plantingsformmycorrhizae.The firsttwo studies included only
established plants, and the second two focused on seedlings. On 12
October 1990, fiveroot samples were collected fromeach of the 1985,
1988, and 1989 plantingareas and fromnativearea 2. At each sampling
point,a root sample (50-80 cm long) was collected at a depthof 25
cm beneaththe surface.The second surveywas carriedout at the 1990
plantingsite on 18 October 1991 (47 wk afterplanting).Ten rootsamples were collected.
In the seedling surveys,tenplants(3-5 cm high) were collectedfrom
the 1988 area in October 1990, and ten fromthe 1990 plantingsite in
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January 1997]
KosKE AND GEMMA-MYCORRHIZAE IN SAND DUNES
samples were collected
June 1992. Because seedlings were infrequent,
randomsampling
haphazardlyfromthe areas and not by the stratified
procedure.
Root samples were cleared in hot (65?C) 2.5% KOH and stainedin
an acidic glycerolsolutionof trypanblue (Koske and Gemma, 1989).
Extentof arbuscularmycorrhizae(AM) developmentin the roots was
quantifiedby calculating a MycorrhizalIndex (MI), in which colonization was assessed at 30-60X on a scale of 0-3, where 0 = no colonization,1 = up to 25% of the root lengthcontaininghyphae,arbuscules, vesicles, or coils of AMF, 2 = 25-50% colonized, and 3 = >50%
of length colonized. Portions of each root system were observed at
400X. Roots were considered to have functionalvesicular-arbuscular
(VA) mycorrhizaeonly if arbusculeswere observed (Gemma and Koske, 1990).
To estimatemycorrhizaein invadingspecies, root samples were collected in April 1992 from13 species of plantsinvadingthe 1985, 1988,
and 1990 plantingsor occurringin naturalareas 3 and 4. Care was
takento ensurethatonly therootsof theinvadingspecies were assessed
forcolonization.Invading species were rare in the youngestplantings,
and the collectingreflectedthis.Roots were treatedas describedabove.
Ectomycorrhizaewere ratedvisually only forpresenceor absence.
Mycorrhizalinoculum potential of soils and assessment of the hyphal network-An assay of mycorrhizalinoculum potential (MIP)
(Moorman and Reeves, 1979; Gemma and Koske, 1988) was employed
to assess the relativepopulationof infectiveunits(i.e., spores,hyphae,
pieces of mycorrhizalroots) in soils fromvarious sites.
Assay of 1990 plantingarea prior to planting-A MIP assay of the
soil fromthe 1990 plantingarea was performedto check forthe presence of viable propagulesof AME Fifteensoil samples were collected
randomsamplingplan. At each
on 12 October 1990 using a stratified
collection point,the upper 15 cm of soil was removed and a 1-L soil
sample (- 6 cm diameter)was collected. Soil samples were returned
to thegreenhouseat theUniversityof Rhode Island, and 70 mL of each
sample were mixed withan equal amountof Terra-Green?,a calcined
clay (Oil Dri Corp., Chicago, IL 60611), and the mix was placed in a
Cone-tainer?(a tapering,cylindricalplasticgrowthtube,20.5 X 4.0 cm
of 150 mL capacity,Stuewe and Sons, Corvallis,OR 97331). Two seeds
of Zea mays L. were sown in each of the 15 Cone-tainers,and the
materialwas placed in a heated greenhouse(avg. 26?C). Sunlightwas
Sodium vapor lamps giving
supplementedfor 16 h/dwithhigh-pressure
an intensityat theleaf surfaceof 350-1375 p1molphotons.m-2.s-2. After
seed germination,Cone-tainerswere thinnedto containa single plant.
Plants were wateredas required,but not fertilized,and harvestedafter
60 d. Roots were cleared, stained,and assessed forcolonizationby the
method(Giovannettiand Mosse, 1980).
line-intercept
Assay of soils from vegetatedsites-Undisturbed soil samples (see
below) were used for the MIP assays, and disturbedand undisturbed
samples were used to estimatethe extentof the hyphalnetworkin the
different
sites. Soil samples were collected on 3 September1991 from
plantingsof A. breviligulata(1985, 1988, 1989, and 1990 sites) and
fromsites 1 and 4. Samples were collectedby drivinga PVC (polyvinyl
chloride) tube (20 cm long X 5.1 cm inside,diameter;the top of the
tube covered witha piece of fiberglasswindow screen glued to it) into
the soil. The tube was thencarefullywithdrawn,withthe core of sand
remaininginside. Before the tube was drivenintotheground,theupper
8 cm of soil had been removed.Aftertheirremoval fromthe soil, the
tubeswere inverted(screennow at bottom)and used as potsforgrowing
plantsin the greenhouse(see below). At each of the six collectingsites,
fivehills (in the plantedareas) or locations(sites 1 and 4) were selected
randomly,and two cores were taken.The distancebetween the center
of the plant and the cores was 15-20 cm, so thatportionsof the root
zone were included in each sample. The contentsof one memberof
each pair of cores were emptied into a plastic bag. When five cores
121
froma site were in the bag, the bag was shaken vigorouslyfor 30 s,
back intothefiveoriginalPVC tubes.These
and thesoil was transferred
shaken samples were the "disturbed" cores. The intact cores were
termed"undisturbed."Thus, ten cores were obtainedfromeach of the
six sites,and halfof thecores were undisturbedand halfwere disturbed.
Disturbed and undisturbedcores were placed on the mist bench in
the greenhouse,and one pregerminatedseed of Z. mays was added to
each tube. After 1 wk, tubes were removed from the mist bed and
transferred
to the greenhousebenches and grown as described above.
At 8.5 wk aftersowing,the entireroot systemwas removedfromeach
tube,cleared,stained,and assessed formycorrhizaeas describedabove.
In additionto the standardMIP assay whichmeasuresthe amountof
rootcolonization,two otherparameterswere measured.When theplants
were harvestedat 8.5 wk, the lengthof the longestleaf in each Conetainerwas recordedand shoot dry mass was determinedby dryingin
a 60?C oven for48 h.
Statistical methods-Data were analyzed using t tests,chi-squared
tests,and one-wayANOVA. Means were separatedwithScheffe'stest.
Spore count data and root colonizationdata typicallyare not normally
distributed(Sylvia, 1986; St. Johnand Koske, 1988) and were transby adding 0.5
formedpriorto analysis. Spore countswere transformed
to the abundance value and takingthe square root of the sum (Little
and Hills, 1978), and colonizationvalues underwenta log (x+ 1) transformation(St. Johnand Hunt, 1983). A confidencelevel of P = 0.05
was used to determinestatisticalsignificance.
RESULTS
Physical characteristics of soils-Soils in all sites
were nearlypure quartz sand. With few exceptions,all
soils had verylow levels of organicmatter,nitrate,phosphorus,and potassium,and were acidic (Table 1). In the
planted areas (of known age), organic matterand age of
the stand were positively correlated(organic matter=
0.51 X age in yr + 0.123, r = 0.56; P = 0.02). When
all sites were compared (planted and natural),organic
matterwas higherin site 5 and nitratewas higherin site
4 thanelsewhere.
AMF community-Spores of 17 species of AMF were
isolated fromthe 98 samples collected fromroot zones
(i.e., excludingthe 12 samples collected fromthe barren
1990 plantingarea beforethe plantinghad been made).
Five of the species apparentlyare undescribedand are
identifiedby numberand are informallydescribedbelow.
Terminology follows that recommended by Walker
(1983, 1986) and Morton(1986). No spores were present
in the 1990 plantingarea priorto planting.Frequencyof
occurrenceand spore abundance of the more important
species are shown for each site in Fig. 8. In the notes
thatfollow, referenceto the frequencyof occurrenceof
particularspecies in all of the samples does not include
the 12 samples collected fromthe 1990 plantingarea prior to planting.
1. Acaulospora lacunosa Morton
Spores of A. lacunosa were recovered significantly
in sites ' the 1985 plantingin age (P =
more frequently
0.01) (Fig. 8). They occurredin 15% of all samples. This
species is relativelycommonin dunes of theU.S. Atlantic
coast fromMassachusettsto Virginia(R. E. Koske, personal observation).Until its descriptionin 1986, spores
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122
TABLE
[Vol. 84
AMERICAN JOURNAL OF BOTANY
1.
Some physicaland vegetationalcharacteristics
of samplingsites.
Site
1990c
1990c
1989
1988
1985
I
2
3
4
5
Age of
planting(yr)
0
1
1
2
5
n.a.'
n.a.
n.a.
n.a.
n.a.
Cover
(%)
OEd
33C
15D
34C
26C
59B
28C
25C
98A
n.d.
(N),
pH
2
6
2
2
2
5
2
3
3
3
6.OA
5.4A
5.8A
6.1A
6.2A
5.8A
5.6A
5.8A
5.8A
5.2A
NO,
(mg/kg)
l.5B
2.11B
1.4B
1.5B
1.6B
1.4B
1.4B
3.9B
9.1A
3.0B
P
(mg/kg)
14.5A
24.5A
13.9A
14.3A
15.1A
22.8A
13.2A
22.6A
30.6A
22.8A
K
(mg/kg)
5.OA
5.4A
5.OA
5.OA
5.OA
1O.5A
6.3A
13.3A
13.3A
25.8A
Organic matter
(%)b
0.12B (N = 14)
n.d.c
0.12B (N
0.14B (N
0.15B (N
0.13B (N
0.13B (N
0.23B (N
0.38B (N
1.91A (N
=
=
=
=
=
=
=
=
15)
13)
13)
5)
13)
4)
12)
5)
N = no. of samples analyzed forpH, nitrate,phosphorusand potassium.
Mean percentageorganic matter.N = no. of samples analyzed fororganic matter.
c The 1990 area was plantedand fertilizedin November 1990. It was sampled immediatelyafterand I yr later.
d Mean of samples. Values in columns followed by the same uppercase letterdid not differsignificantly.
Not determined.
Age of the vegetationof the naturalareas was not determined.
a
b
of this species would have been identifiedas A. scrobiculata Trappe.
2. Acaulospora mellea Spain & Schenck
Spores of A. mellea were recoveredfrom 16% of all
samples. Like A. lacunosa, it was absent fromthe 19881990 plantings,but occurredin all otherareas (Fig. 8).
Maximumspore abundanceoccurredin the 1985 planting
(avg. 4.9 spores/100mL).
3. Acaulospora scrobiculata Trappe
A common species in dunes of the Atlanticcoast of
the U.S. including other areas of Cape Cod, A. scrobiculata (e.g., Bergen and Koske, 1984; Koske, 1987;
Gemma, Koske, and Carreiro,1989) was recoveredonly
fromsite 2 in this study.It was presentin 20% of the
samples fromthis site, averaging2.7 spores/100mL.
4. Acaulospora 3106A (Fig. 9)
This species is similarto A. lacunosa, but spores possess a more finelydimpled laminatedwall. Spores were
foundonly in threeof the samples fromsite C.
Spores globose, 72-88 ,um diameter,yellow-brown.
Spore wall structure
consistingof six walls. Wall 1 membranous,wrinkling,hyaline,0.5 ,umthick,appressed to
wall 2. Wall 1 was difficult
to observe in mostspecimens,
apparentlydisappearingduringexposureto the soil. Wall
2 laminated,yellow, 2.0-3.0 ,umthick,ornamentedwith
hemisphericaldepressions2-3 ,umdiameterX 1-2 ,um
deep, closely spaced, separatedfromeach otherby ridges
- 2 ,umwide. Walls 3 and 4 paired, membranous,hyaline,each 0.5-0.6 ,umthick.Wall 5 membranous,beaded,
0.5-1.0 ,umthick.Wall 6 amorphous,hyaline,attached
to wall 5, 1.5-2.0 ,umthick,up to 8 ,umthickin crushed
spores, stainingdark red-brownin Melzer's reagent.Circatrix 12 ,umdiameter.
Acaulospora 3106A is a a memberof the group of
small-sporedAcaulospora species that include A. lacunosa and A. mellea, whichhave a commonwall structure
of the laminatedwall
(Morton,1994). The ornamentation
is sufficientto distinguishA. 3106A fromother orna-
quantitiesof
mentedspecies in this group,but sufficient
materialand stages of developmentwere not available to
preparea formaldescription.
5. Acaulospora 7034 (Figs. 10, 11)
Spores of this species were common in the midsuccessional sites in our study,and were especiallyabundant
in the 1985 plantingand in site 2 (Fig. 8). Spores of A.
7034 were the most frequentlyrecoveredof any species,
occurringin 31 % of all the rootzone samples. No spores
were isolated fromthe 1-yr-old1990 plantingand sites
4 and 5 (i.e., the youngestand oldest sites).
Spores globose to subglobose, 120-160 ,umdiameter,
brownish-yellow.Spore wall structurecomplex, consisting of six walls. Walls 1 and 2 evanescent,hyaline,adherentto each otherand to wall 3. Wall 1 0.5-0.8 ,um
thick;wall 2 1.5-2.0 ,umthick.Wall 3 laminated,colored,
ornamentedby craniformfolds, 5.6-7.5 ,umthick.Wall
4 membranous,wrinkling,hyaline,1.0 ,umthick.Wall 5
coriaceous, hyaline, 1.0-2.2 ,umthick.Wall 6 appressed
to wall 5, membranous,hyaline,0.5 ,umthick.Circatrix
12-14 pLmdiameter.
Spores of A. 7034 are similar to those of A. rehmii
Sieverding & Toro in their surface ornamentation,but
differin wall structure.
6. Entrophosporainfrequens(Hall) Ames & Schneider
Spores were foundin a single sample fromarea 4. This
species has not previously been recovered from sand
dunes of the Atlanticcoast of the U.S., although it is
known fromdunes in the west coast (Koske and Halvorson, 1989).
7. Gigaspora gigantea (Nicol. & Gerd.) Gerd. &
Trappe
Spores of G. gigantea were recoveredfromthe 5-yrold site and naturalareas 2, 3, and 4 (Fig. 8). Spores
were presentin 18% of all samples. The species is common in A. breviligulata-dominated
dunes of the Atlantic
coast of NorthAmerica fromQuebec to Virginia(Koske
and Halvorson, 1981; Bergen and Koske, 1984; Koske,
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AllSpeciesofAMF
1990 (O yr)
Y
1990(I yr)
1989(19(I
1988(2 yr)
1986(6y198
site2
Zt B
X _
...
site 4
site 5
I gm (O yr)
_0
It990 (0 yr)
y1 B
y B
Y B
Y- B
1990(I yr)
yr)
B
1988(2 yr)
1985(
yr)
site2
site3
-------------
B
XY
XY
X
site 4
B
AB
_
0
XY0
B
site 5 |X
0
10
.,
Y B
Y B
- 99(I
198(5(yr)
Y B
1990(1 yr)
1989(1 r
(2yYr)Y
1
2YrY-B18
g
o
^
Y
Y B
0.,
.
10
I1990(Oyr)
1990(1 yr)
yr
2Y)Y-B1988
1985(5yr)
fe2
i0sRe
FrequencyAbundance
AB
AB
margarita
Gigaspora
AB
AB
AB
site A
I 990(Oyr)|
1990(I yr)
1989(1 yr)
1988(1 yr)
1985(5yr)
site2
site3
4
site5
Y-A
XY
XY
_.
X
X
X
A
A
A
X
..
La
Y
Y
B
B
-B1989
---AB
AB
4 3 .........................
sfte
~~AB
I
Scutellosporaerythropa
calospora
Scutellospora
2y- ~~~~~~~~site
oRe
L
,
Yt B
Y B
y B
Y-- B
Y
y
1988(2 yr)
1985(5yr)
site2
site3
site4
5
7243
Glomus
_
C
site 4
8?,?''?
I 990(Oyr)
1990(I yr)
,.
I1990
(Oyr)
X B
X B
X B
X
A
X AB
AB
X
gigantea
Gigaspora
Y B
1990(Oyr)
Y B
1990( yr)
1989(19
(I
B
Y;
1988(2 yr)
1985(5yr) ---- y
s(te2
yE S B
site3
Y B
site4
B
site
YE
0b..
X--B
199 (I yr)
1989(1 yr)
1988(2 yr)
1985(5 yr)
site2
site3
site 5
7034
Acaulospora
)
meHea
Acaulospora
lacunosa
Acaulospora
B
?
'La
8
-~~~~~~~T
.
123
KosKE AND GEMMA-MYCORRHIZAE IN SAND DUNES
January 1997]
1990(Oyr)
1990(1 yr)
(1 yr)----1985(5yr)
site2
site45
sRO
FrequencyAbundance
X
Y
B
- -YA
---
FrequencyAbundance
Fig. 8. Plots of frequencyof occurrenceand average spore abundance (spores/100mL soil) of the species of AMF presentin ?15% of all
are not illustrated.Frequencyand abundanceof all 17 species are combined
samples. Nine additionalspecies were recovered,but theirdistributions
in the firstgraph.
1987; Gemma and Koske 1988; Gemma,Koske, and Carreiro, 1989; Dalpe, 1989) where it frequentlyis a codominantmemberof the AMF community.
8. Gigaspora margaritaBecker & Hall
Spores of G. margaritawere recoveredfrom26% of
all samples,includingthe 1-yr-old1989 plantingarea but
were not significantlymore abundant at any particular
site (Fig. 8). This was the second most frequently
recovered species.
9. Glomus clarum Nicol. & Schenck
This species was one of theearliestappearingpioneers,
showing up in the 1-yr-oldplanting(1989), apparently
originatingin theplantingstock(see below). Spores were
presentin only 6% of the samples and were absentfrom
the 1985 plantingas well as areas 3, 4, and 5. Glomus
clarum also is knownfromsand dunes of easternCanada
(Dalpe, 1989).
10. G. microaggregatumKoske, Gemma & Olexia
Anothercommoninhabitantof coastal dunes of eastern
NorthAmerica and theGreatLakes (Koske, Gemma,and
Olexia, 1986; Koske, 1987; Koske and Tews, 1987; Dalpe, 1989), G. microaggregatumwas recoveredonly from
the more advanced seral stages (sites 3, 4, and 5) in this
study,and its abundance never exceeded 2 spores/100
mL. Spores of this species typicallyformwithindead
spores of otherAMF, and we tended to findthemmore
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124
AMERICAN JOURNALOF BOTANY
[Vol. 84
abundantlyin areas of the dunes where the A. breviligulata was in decline and organic matterwas higherthat
near the dune crest(personal observation).
11. Glomus 7099
Spores of this undescribed species occurred in one
sample fromsite 3 and one fromsite 4.
Spores globose to subglobose,60-80 ,umdiameter,hyaline. Spore wall 2-3 pumthick,laminated. Spores surrounded by a hyaline peridium 10-30 ,um thick composed of loosely organized hyaline hyphae. Peridial hyphae 2-5 ,m broad,withwalls up to 1.0 ,umthick.Walls
of thickesthyphaeroughened.
12. Glomus 7243 (Fig. 12)
~~~:.
~
~
-,
^
This was anotherof the species that was limited to
more advanced seral stage, and spores were recovered
only fromsites 3, 4, and 5 (Fig. 8). In some samples,
spores occurredin greatabundance(up to 600 spores/100
mL in a sample fromsite 4).
Spores globose to subglobose, 80-90 (-115) ,umdiameter,red-brownto orange-brown.Spore wall relatively
thick,8-12 ,umthick,laminated.Attachmenthyphayellow-brown,10-12 ,umwide, constrictedto 4-6 ,umat
base of spore. The species is very similar to G. etunicatum Becker & Gerd. but differsin the smaller size of
the spores and the more robustattachmenthypha.Spores
of G. 7243 occurredonly in the soils withhigh organic
matterand frequentlywere found inside dead spores of
Gigaspora and Scutellospora spp.
^
13. Scutellospora calospora (Nicol. & Gerd.) Walker&
Sanders
12 4X!
Fg. 91.
Spors o
nae
AFfo
roic
ad
Dunes
9. Surface
of spore of Acaulospora 3 106A. Bar = 40 p.m. 10. Surface
ofsoeo
cuopr
04
oefn-txueoranainad
Spores of S. calospora were presentonly in the older
sites (i.e., the 1985 plantingand in all of the naturalareas) (Fig. 8). Highestabundance and frequencyoccurred
in site 4. The species was recovered from 19% of all
samples.
Scutellospora calospora is a common memberof the
dune communityof the Atlanticcoast of NorthAmerica
and theGreatLakes (Koske and Halvorson,1981; Bergen
and Koske, 1984; Koske, 1987; Gemma, Koske, and Carreiro,1989; Gemma and Koske 1988; Dalpe, 1989).
14. S. erythropa(Koske & Walker) Walker& Sanders
Spores of S. erythropaoccurredin sites rangingfrom
the 1-yr-oldplantingof 1990 to site 5 (Fig. 8). It seldom
was presentin abundance,but was a consistentmember
of most sites. It was found in 16% of all samples. This
is anothercommon member of the sand dunes of the
Atlanticcoast of the U.S.
prominentcircatrix("C"). Bar = 60 ,um. 11. Spore of Acaulospora
7034. Walls 3-6 are indicated. Walls 1 and 2 are not visible in this
photograph.Bar = 30 ,um. 12. Spores of Glomus 7243. Note thick
laminatedwall of spore and stoutattachmenthypha.Bar = 50 ,um.
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All use subject to JSTOR Terms and Conditions
January 1997]
KOSKE AND GEMMA-MYCORRHIZAE
1990 (Oyr)
D
ffi
1988(2yrs)
A
G
0 60
BC
1985 (5 yrs)
BC
site2
B
site3
so
40t
0
INA
site4
site5
100
80
CD
CD
1989(1yr)
0L
o
?
CD
1990(1yr)
125
IN SAND DUNES
I
BC
16 14 12 10 8 6 4 2 0
Total
Richness
1
2
E06
3
4
5
6
Average
Richness
Fig. 13. Species richnessin different
successional sites. "Total richness" indicates the total numberof species recoveredfromeach site,
and "average richness" is a measureof the average numberof species
in each sample. The 1990 plantingwas sampled beforeplantingand 1
yr later.
15. S. pellucida (Nicol. & Schenck) Walker& Sanders
Spores of S. pellucida occurredin the 1-yr-old1990
plantingand in sites 3 and 4. It was recoveredfrom6%
of all samples and never in abundance. It is a common
species in maritimedunes of the easternU. S. and Canada.
16. S. persica (Koske & Walker) Walker& Sanders
This species was isolated only fromsites 3 and 4. It
occurredin 7% of all samples. Scutellospora persica is
anothercommonmemberof theAMF communityin sand
dunes of the easterncoast of the U.S.
17. S. reticulata(Koske, Miller & Walker) Walker&
Sanders
Spores of this species were isolated only fromfourof
the 13 soil samples collected at site 4. Its abundancewas
low (avg. 0.6 spores/100mL at this site). Scutellospora
reticulata is an infrequentlyrecovered species in U.S.
dunes (Koske, Miller, and Walker,1983; Koske, 1987),
and its spores seldom occur in abundance. Spores of S.
reticulatatypicallyare foundin dunes of the NorthAtlantic coast of the U.S. where organic matteris higher
thanin accretingareas (personal observation).
Increases in the richness and complexityof the AM
fungal communityaccompanied the development and
succession in the plant community.Spores were absent
priorto planting,but were recoveredfromareas thathad
been vegetatedfor <1 yr (Fig. 8). The species richness
(totalnumberof AMF species presentin a site) increased
with increasingstabilizationof the dunes and then declined in theoak/mapleforest(Fig. 13). Average richness
per sample at differentsites showed a similar pattern.
Maximum richnessoccurredin site 4, where spores of
14 species were isolated. In some individual samples
fromsite 4, spores of nine species of AMF were present.
B
1
0
80-J
2
3
4
B
5
4
0
0
C')
06
0
1
2
3
4
5
Ageofplanting
(yr)
Fig. 14. Changes in the populations of AMF in association with
plantingsof Ammophilabreviligulataover a 5-yr-period.The percentage of samples fromwhich spores were recovered(A) showed a significantlinear trendover the time period (r = 0.996, P = 0.003), and
sporesabundance(B) showed a significant
exponentialtrend(r = 0.964,
P = 0.008).
Average species richnessin site 4 was 5.3, a value significantlyhigherthan values fromothersites. Spores of
only five species of AMF were isolated fromthe 1-yrold sites. In the planted areas (for which the age was
known), the average species richness per sample was
highlycorrelatedwith age of the planting(r = 0.699, P
= 0.0001), as was the percentageof samples thatcontainedspores of AMF (r = 0.996, P = 0.003) (Fig. 14A).
The abundanceof spores of AMF in the different
sites
(Fig. 8) generally mirroredthe species richness data.
Youngest sites (1990, 1989, and 1988 plantings)had the
fewestspores per 100 mL, and site 4 had themostspores
(avg. 208.9 spores/100mL). In the planted areas, spore
abundance was significantlycorrelated with age (r =
0.964, P = 0.008) (Fig. 14B).
Based upon when their spores were firstrecovered
fromthe sites,two groupsof AMF were identified.Early
invaders(present1-2 yrafterplanting)includedA. 7034,
GI. clarum,Gi. margarita,S. erythropa,and S. pellucida.
Spores of the second group of species were isolated only
fromlater successional sites (the 1985 plantingarea or
older). This second groupincluded the majorityof AMF
species, includingA. lacunosa, A. mellea, Gi. gigantea,
GI. 7243, and S. calospora. Scutellospora erythropawas
unique in sporulatingin all seral stages.
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126
TABLE
2.
aged stands.
Mycorrhizaein Ammophilarootsfromdifferent
Mycorrhizal
index
Percentage
of samples
mycorrhizal
Site and age
of planting
Plant type
N
1990 (47 wk)
1990 (1.5 yr)
Mature
Seedling
9
10
I.OCa
O.OD
78A
OB
1989 (I yr)
1988 (2 yr)
Mature
Mature
Seedling
5
5
10
1.2B
1.9A
O.OD
80AB
IOOA
OB
1985 (5 yr)
Naturalarea 2
(age unknown)
Mature
Mature
5
5
1.8A
2.OA
IOOA
IOOA
a Values in columns followed by the same uppercase letterdid not
differsignificantly.
Mycorrhizalstatus of plantsA. breviligulata-Most plants became mycorrhizalin
the 1st yr afterplanting,and all matureplantswere mycorrhizawithin2 yrafterplanting(Table 2). Greatestcolonizationoccurredin the 1985 and 1988 plantingsand in
site 2 and least in the 1990 area (sampled 47 wk after
planting). No mycorrhizaewere presentin any of the
seedlings.
Invadingspecies-The incidenceof mycorrhizaein invading species appeared to increase withsuccession,but
numberof samples was recoveredto idenan insufficient
tifytrendsin theplantedareas (Table 3). The majorityof
species and specimensin naturalareas 3 and 4 were myTABLE
[Vol. 84
AMERICAN JOURNAL OF BOTANY
3.
corrhizal,and halfof thesix species fromthe 1985 planting were mycorrhizal.In the 1988 site,only one species,
the nonmycorrhizalPolygonella articulata, was found.
No invaderswere located in the 1989 area, and a single,
nonmycorrhizalseedling of Prunus maritimawith red,
puckeredleaves was presentin the 1.5-yr-old1990 planting.
Mycorrhizal inoculum potential of soils-No AM
were observed in any of the 15 roots systemsexamined
from the MIP assays set up using soil fromthe 1990
plantingarea priorto planting,indicatingthatviable propagules of AMF were not presentin the samplingarea.
In the planted sites the MIP of dune soils showed a
significantlogarithmictrend(ln[x+ 1] = -0.308 + 0.526
x age in yr; r = 0.701, P = 0.0006), increasingwithage
(Fig. 15A). Greatest root colonization occurred in the
samples fromsite 4. Variationwas greaterforMIPs from
soil collected fromyoungestplantedareas thanfromthe
older, more established sites, indicatinga very uneven
distributionof AMF propagules in the former.For example, rootcolonizationvalues in the fiveMIPs fromthe
1988 plantingsitewere 7, 52, 39, 4, and 5%, while values
fromsite 4 were 33, 32, 30, 33, and 40%. The average
MIP from the native areas (26.4%) was significantly
higher(t test,P = 0.002) than the average MIP (8.6%)
of the 1985-1990 plantingsites.
Incidence of mycorrhizaein seedlingsof plant species invadingareas of the ProvinceLands dunes collected April 1992.'
Naturalareas
Plantingsof Ainit)ophzila
Species
1990 (1.4 yr)b
1988 (3.4 yr)
Asteraceae
Achillea millefolium
Artemisiaborealis
Asterlinariifolius
Solidago sempervirens
Solidago odora
Solidago nemoralis
1985 (7 yr)
0/2
0/2
2/2
1/3
Myricaceae
Myrica pensylvanica
Poaceae
Deschampsia flexuosa
3/5
Area 3
2/4
1/5
2/2
0/1
0/1
2/3
5/8
3/3
Polygonaceae
Polygonella articulata
0/4
Fagaceae
Quercus ilicifolia
Totals
specimensc
speciesc
O/lAB
0/lA
0/4B
0/lA
6/15B
3/6A
3/3
0/5
0/1
0/ld
All sites
0/3
0/2
2/4
1/7
4/4
1/3
0/3c
Pinaceae
Pinus rigida
Rosaceae
Prunus maritima
Rosa rugosa
Area 4
3/3
1/1
1/1
3/4
2/2
3/3
3/3
6/6
14/25AB
7/9A
7/7A
3/3A
Mycorrhizae,if present,were of the arbusculartypeexcept in Quercus and Pinus, which had ectomycorrhizae.
Age of plantingsite at time thatsamples were collected.
C Firstvalue indicateshow many samples possessed mycorrhizae;second indicatesno. of samples examined at a site.
dThis seedling had red, distortedleaves and appeared stunted.
c Values in rows followedby the same uppercase letterdid not differsignificantly.
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All use subject to JSTOR Terms and Conditions
27/52
9/13
January1997]
KosKE
AND GEMMA-MYCORRHIZAE
A
1990C
1989C
.
~root
1988
1985_
|
site 1
0
10
~~~
colonization
5;
2.5.$l$
X
2.|*
1990_
30
40
_.._. ..........................._..
la
length
......... . ......
50
Fig. 0.......
Efec
0
desrucio
we .....
00L
a
'
the
0 hypalnewok.n.
0ML
oo.
t0 ..
clo
Site
~~~~B
1989
_ _....._............_.....
........
shootmass
*~0.5......
20
ofroot
Percentage
length
colonized
C,)
3.5
2
site 4
127
IN SAND DUNES
Fig. 16. Effectof destructionof the hyphalnetworkon root colonizationand growthof Zea mays plants grownin soils fromdifferent
seral stages of the dunes. Y-axis values were calculated by dividingthe
response of plants grownin undisturbedsoil cores by the response in
disturbedcores. Values > 1.0 are indicativeof a hyphalnetworkpresent
in undisturbedcores. Bars markedby a starindicatesignificantdifferences betweencolonizationor growthin disturbedand undisturbed
samples.
198
site t
site 4
0
0.2
0.4
0.6
0.8
1
1.2
Shoot
mass(g)
dry
in disturbedsoil cores. Disturbance of cores from the
plantedareas did notresultin significant
reductionin root
colonizationor growthof plants.
DISCUSSION
1990
AMF are common membersof the biota of sand dune
systemsthroughoutthe world where theyappear to play
an important
role in thedevelopmentof plantcommunity
structure(e.g., Nicolson, 1960; Koske and Polson, 1984;
1988
Puppi and Riess, 1987; Dalpe, 1989; Koske and Gemma,
1985
1996). The simultaneousarrivalof AMF and plant colonists in primarysuccessional sites, representedby the
site 1
planted areas in this study,allows the fungito interact
with the developing plant communityfromthe earliest
site 4
seral stage (Nicolson, 1960; Sylvia and Will, 1988; Gemma
and Koske, 1989, 1992; Koske and Gemma, 1990).
0 5 10 15 20 25 30 35 40
In the Cape Cod dunes, most measures of mycorrhizal
presence (e.g., spore abundance, species richness,root
oflongest
leaf(cm)
Length
colonization,and MIP) increased fromthe 1st yr in the
plantedareas, and these increases generallycontinuedin
Fig. 15. Measurementsof MIP fromundisturbedsoil cores from
the later successional sites representedby naturallycolsites differing
in successional stage. Cores were collectedin September
1991. Three parameterswere measured: root colonization,shoot dry
onized areas 2-4. These increases in the early-and midmass, and lengthof the longest leaf. Narrow bars representstandard
successional sites and theirsubsequentdecline in thefordeviation. Note great variationin the data fromthe youngestplanted
ested site agree with previous studies of sand dunes in
areas. Bars in 15A sharinga commonletterdid not differsignificantly.
Scotland (Nicolson, 1960), the Pacific coast of the U.S.
No significantdifferenceswere detectedin the data forFig. 15 B, C.
(Rose, 1988), and Mexico (L. Corkidi and E. Rincon,
Universityof Mexico, personalcommunication).
Most of the species of AMF occurringin the Province
Shoot growthand leaf lengthwere not correlatedwith
the age of the site in the plantedsites,and no significant Lands have been previouslyreportedfromsand dunes of
the mid-Atlanticcoast of the U.S. (e.g., Koske, 1987).
differenceswere noted between growth made in soil
Values for species richnessand spore abundance in the
cores fromnaturalsites and plantedsites. (Fig. 15B, C).
natural areas and the 1985 plantingsite are similar to
Extent of the hyphal network-Soil disturbancerevalues reportedin earlier surveys of AMF in naturally
duced the MIP of the soil cores fromsites 1 and 4, invegetateddunes on or adjacentto Cape Cod (Bergen and
dicatingthatsignificanthyphalnetworkshad developed
Koske, 1984; Gemma, Koske, and Carreiro,1989).
only in these sites (Fig. 16). Similarreductionswere obThe identification
of early-and later sporulatingspeserved in shoot mass and the lengthof the longest leaf
cies of AMF in the dune sites suggestedan apparentsuc1989
.C
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128
AMERICAN JOURNAL OF BOTANY
cession of AME While thismay be, the evidence is confoundedby the possibilitythat not all species of AMF
presentin the roots had sporulatedat the time of collecof theoriginof thepioneerAME
tion and by uncertainty
Three of the fivespecies isolated fromtheyoungestsites
(Gl. clarum, S. erythropa,and S. pellucida) apparently
arrivedon theA. breviligulataplantingstock(Koske and
Gemma, 1992), a common occurrencewithrhizomatous
dune pioneers (Sylvia and Will, 1988; Gemma and Koske, 1989, 1992; Koske and Gemma, 1990). Because the
plantingstock was raised in a nurseryin sandy agricultural soil (Church's Garden Center,Cape May, NJ), it
cannotbe concluded thattheAMF species presenton the
stock are necessarilypioneer species, althoughtheyare
capable of sporulationin pioneer sites.
Further,the primary vegetative succession on the
plantedsites differsconsiderablyfromnaturalsuccession
occurringin sand dunes that are not managed (Hewett,
1970; Ranwell, 1972). The very rapid and uniformcolonization of '12 ha of bare sand by a a single pioneer
species thatresultsfroma plantingof beachgrasshas no
parallel in nature.Thus, the rate of developmentand the
complexityof the AMF communitydescribed in this
studymay differfromthatoccurringin a naturalsuccession.
The formationof the AMF communityis closely
linked to changes in the aboveground vegetation.In a
varietyof naturalsites,AMF have been foundto play a
vital role in plant succession, affectingthe success not
only of obligatelymycotrophicspecies, but also of those
that are facultativelymycotrophicor nonmycotrophic.
Essentially,obligatelymycotrophicplantspecies are prevented fromcolonizing a site if the fungiare absent or
if theirabundance is below a criticallevel (Miller, 1979,
1987; Reeves et al., 1979; Janos, 1980; Grime et al.,
1987; Read and Birch, 1988; Gemma and Koske, 1990,
1992; Koske and Gemma, 1990; Miller and Jastrow,
1992; Gange, Brown, and Sinclair, 1993). The stunted
seedlingof Prunusmaritima(an obligatemycotroph[Koske and Gemma, 1992]) that was found in the 1990
CCNS plantingsite illustratesthis phenomenon.Some
nonmycotrophicand facultativelymycotrophicspecies
may be activelyexcluded when theinoculumpotentialis
greaterthan a minimal level (Francis and Read, 1994,
1995).
It is the hyphalnetworkof AMF thatfirstexertsthese
beneficialor antagonisticeffectson the seedlings of potentialinvaders.Studies in pasturesoils and mine spoils
have shown that the hyphal networkis responsiblefor
the preponderanceof initialcontactswithroots of seedlings (Evans and Miller,1988; Fairchildand Miller,1988;
Read and Birch,1988; Jasper,Abbottand Robson, 1989a,
b; Gange, Brown, and Sinclair,1993; Francis and Read,
1994, 1995). A similarrole for the hyphal networkappears to exist in the succession on the dunes of CCNS.
Of the two sites (1 and 4) in the CCNS studyarea that
had significanthyphal networks,widespread invasion
was occurringonly in the later succesional site (site 4).
However,as the failureof plantsto invade site 1 shows,
the formationof a hyphalnetworkis but one factorthat
is necessaryduringsuccession to permitcolonizationby
nonpioneer,obligatelymycotrophicplant species. Other
site changes accompanyingsuccession in dunes include
[Vol. 84
improved soil conditions (e.g., soil structure,organic
and a largerpopulationof soil mimatter,soil nutrients,
croorganisms) and an ameliorated microclimate(e.g.,
Oosting, 1954; Olson, 1958; Koske, Sutton,and Sheppard, 1975; Baldwin and Maun, 1983; Rose, 1988), and
to the high
these improvementscontributesignificantly
plant diversityin site 4. The lack of invadingspecies in
site 1 probablyresultsfromthe high rate of sand accretion in this area. Few plant species can tolerateburialby
sand, and rapidly accretingdune sites (such as site 1)
typicallyhave impoverishedsoils withvery low organic
matterand are dominatedby a single species (Ranwell,
1972).
The extentof of hyphalnetworksestimatedfromthe
"undisturbed"cores in the presentstudymay have been
underestimatedbecause of possible damage to the network when the cores were collected. However, the differencein root colonization between disturbedand undisturbedsamples fromsite4 were verysimilarto reports
fromothersoils (e.g., Read and Birch 1987; Evans and
Miller,1988), suggestingthatlittledisruptionoccurredin
the undisturbedcores. The lack of AM in seedlingsof A.
breviligulatacollectedfrom1- and 2-yr-oldplantingsites
also indicates that no significantnetworkis presentin
very young sites. All threeparametersused to assess the
extent of the hyphal network (viz., root colonization,
shootdrymass, and lengthof longestleaf) producedsimilar results.The lattertwo techniquespermita morerapid
study.
assessmentand warrantfurther
In contrastto the slow rate of invasion by obligately
mycotrophicspecies in highlydisturbedsecondary successional sites where the AMF populationhas been destroyed(Miller, 1979, 1987; Reeves et al., 1979; Allen,
1988; Miller and Jastrow,1992), dune sites are invaded
relativelyquickly.The differenceis explained by thecodispersal of AMF with the plantingor colonizing stock
(Gemma and Koske, 1989, 1992; Koske and Gemma,
1990) and the resultantrapid increase in populationsof
spores and otherinocula of AME
In the Cape Cod dunes, some of the earliestinvading
species of stands of A. breviligulata are incapable of
formingmycorrhizae(e.g., Polygonella articulata) or do
not require mycorrhizaebut may benefitfromthe symbiosis if the fungiare present(e.g., Solidago sempervirens, Deschampsia flexuosa,Achillea millefolium)(Koske and Gemma, 1992). An importantfunctionsuch facultativelymycotrophicspecies may be in maintainingand
increasingthe MIP in the dunes as the A. breviligulata
stands lose vigor. These species can establish in areas
where thereis a minimalhyphalnetwork(as seen in the
older,planted areas). In time, theirroots can supporta
populationof AMF, paving the way forlaterinvasion by
plant species thatrequiremycorrhizae.The role of such
mycorrhizal"facilitators"in secondarysuccessionalsites
has been describedpreviously(e.g., Miller, 1979, 1987;
Reeves et al., 1979; Janos,1980; Allen, 1988; Miller and
Jastrow,1992).
The great variationin the MIP data fromthe planted
areas reflectedthe very uneven (aggregated)distribution
of AMF propagules(e.g., Sylvia, 1986; Tews and Koske,
1986; St. Johnand Koske, 1988) in these young soils.
limitthe numberof sites
will further
Such a distribution
This content downloaded from 128.193.8.24 on Fri, 19 Jul 2013 16:33:39 PM
All use subject to JSTOR Terms and Conditions
January
1997]
KOSKE AND GEMMA-MYCORRHIZAE
thatare amenable to invasion by plantsthatrequireAM
(Allen, 1991).
Results fromthis studyagree withMiller's (1985) observationthatrestorationof the abovegroundplantcommunitymustincluderestoration
of thebelowgroundcomponentsof the site. In primarysuccession in sand dunes
AMF fungiare an importantcomponentof the complex
belowgroundsystem.
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