Functional
Ecology 1993
7, 236-241
Seed size and shape predictpersistencein soil
K. THOMPSON,
S. R. BAND
and J. G. HODGSON
Unitof ComparativePlant Ecology (NERC), Departmentof Animal and Plant Sciences, The University,
Sheffield
SJO2TN, UK
Summary
1. An understandingof seed persistencein the soil is importantto vegetation
managementand weed control,but experimentalcollectionof seed bank data is
tedious and expensive. We report a rapid, simple method for predictingseed
persistenceinthesoil. The methodis testedon a rangeofBritish,mostlyherbaceous,
species.
2. Diaspore (seed or fruit)weightis plottedagainstvariance of the three linear
dimensionsof the diaspore. All diasporeswithinan area of the graphdefinedby a
maximumweightand variance are persistentin the soil. The criticalweightis the
same forfruitsand seeds, but the criticalvarianceof diaspore dimensionsappears
slightly
higherforfruits.The greatmajorityofdiasporesoutsidethisregionare short
fewambiguouscases can be resolvedbyreferenceto habitat.
lived,and therelatively
3. The generalityof the suspectedunderlying
mechanismsuggeststhatthe method
can also be applied to florasoutsidenorth-west
Europe.
Key-word:seed bank
FunctionalEcology (1993) 7, 236-241
Introduction
Informed
vegetation
management
requiresaccurate
of
and reliableinformation
on the characteristics
of
manyplantspecies.One of themostimportant
in the soil. An
theserelatesto seed persistence
seedbanksis thekeyto
understanding
ofpersistent
for
manyaspectsof practicalland management
and to the effective
agriculture
or conservation,
conservation
ofmanyrarespecies.Theworld'smost
pernicious
arableweedsallpossessa persistent
viable
persistenceofseeds in thesoil are availableforonlya
minority
ofspeciesand are oftenofuncertainquality.
Outside Europe even less informationis available,
but to offsetthese deficienciesexperimentallyis a
formidabletask. Collection of original seed bank
data, eitherby germinatingor extractingthe seeds
contained in soil samples, is prohibitivelylabour
intensive and expensive, the results of a single
investigationare frequentlyinconclusive,and excavation of soil frombeneath rare species is clearly
undesirable.
seed bank (Holm et al. 1977). Furthermore,in the
The observationhas frequentlybeen made that
increasingly
disturbedenvironment
created by
there
is a connectionbetweenpossessionof a persismodernland use, soil seed banksare of growing
tent
seed
bankand seed size and shape (Thompson&
importance
in themanagement
of
and restoration
Grime
1979;
Thompson 1987; Leck 1989). For
vegetation
(Keddy& Reznicek1982;Jefferson
&
reasons
which
are almost certainlyconnectedwith
Usher1987;Bakker1989;Hodgson& Grime1990),
the
of burial,persistentseeds tend to be
probability
anditissometimes
to
the
of
possible predict response
small and compact, while short-livedseeds are
vegetation
to varioustypesof management
froma
ofthecomposition
oftheaccompanying normallylarger and either flattenedor elongate.
knowledge
However, a previousattemptto predictseed persisseedbank(Marks& Mohler1985;Van Der Valk&
Verhoeven
whichpermits
inter- tence required informationon germinationphysi1988).Management
ology as well as size and shape (Grime 1989). This
mittent
froma persistent
seed bankis
regeneration
crucialto the survivalof manyrare or declining paper reportsa rapid method of predictingpersistencein thesoil frommeasurementsof seed size and
species(Keddy& Reznicek1982;Rowell,Walters&
shape alone.
Harvey1982).A persistent
seedbankoftenconfers
a
236
in thefaceofmodernintensive
degreeofresilience
landuse;specieswhicharecurrently
increasing
their
abundancein Britainare twiceas likelyto have a
persistent
seed bankas thosewhichare declining
(Hodgson& Grime1990).Yet eveninthecomparativelywell-studied
European flora,data on the
Materialsand methods
Plantdiasporesare usuallyreferredto as seeds, even
though many of them are in fact fruits.Here we
analysedata on seeds and indehiscent,single-seeded
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237
Predictingseed
persistencein soil
fruitsseparately. Size is quantifiedas the air-dry
weightof 100 diaspores.In orderto givequantitative
expressionto therelationshipbetweendiasporesize,
shape and persistence,a quantityis requiredwhich
expresses the extent to which shape differsfrom
sphericity.The quantity we have chosen is the
varianceof diaspore length,widthand depth,after
firsttransforming
all values so that lengthis unity.
This variance has a minimumvalue of zero in
perfectlysphericaldiaspores, a maximumvalue of
about 0 3 in needle- or disc-shapeddiaspores, and
variesverylittlebetweenindividualseeds ofthesame
species. Five replicatediasporeswere measuredfor
each species. In most cases measurementswere
carriedout on the dispersule,ratherthanthe germinule. Thus'mostgrasscaryopsesweremeasuredwith
the persistentlemmasand awnswithwhichtheyare
normallydispersed,althoughthe nutof Carexflacca
was measured withoutits utricle.Medicago fruits
rather than seeds were measured for the same
reason. The achenes of Compositae,however,were
measuredwithoutthepappus. In thefewexamplesof
species with fleshyfruits(Arum maculatum and
Hedera helix),measurementsweremade on isolated
seeds.
Seed persistencein the soil is frequently
classified
withrespectto both longevityand size of the seed
bank relativeto annual seed production(Thompson
& Grime1979), butforthepurposesofthispaper we
have adopted a simplerschemeproposedbyBakker
(1989), and describedin Thompson (1992). In this
classification
threeclasses of seed persistencein the
soil are described:transient,
persistingin thesoil for
less than 1 year; short-term
persistent,
persistingfor
more than 1 but less than 5 years; and long-term
forat least 5 years.In practice,
persistent,
persisting
the boundarybetweenthe firsttwo classes is often
ratherblurred,and in thispaper we attemptmerely
to distinguish
thethird,longpersistent,
classfromthe
firsttwo. Seed persistencedata employed in this
paper were abstractedfroman unpublished(and as
database ofthesoil seed banksofthe
yetunfinished)
north-westEuropean flora in preparation by K.
Thompsonand J.P. Bakker. This database presently
contains data abstracted from c. 200 published
sources,and infersseed persistencebothfromdirect
estimationof seed longevityand fromthe depth
distributionof seeds in the soil (Thompson 1992).
The classification
ofspeciesintopersistencecategories in Table 1 mustthereforebe regardedas provisional,althoughwe are confidentthatveryfew,if
any, species will eventuallyturnout to have been
misclassified.
Measurements were made for 97 species (44
speciesofseeds and 53 speciesoffruits,Table 1). All
species are Britishnativesor naturalizedaliens, and
almostall areherbaceous.The specieswerechosenin
order to provide approximatelyequal numbersof
fruitsand seeds and of transientand persistent
100
(a)
x
x
10
X
X
*
x
,
-'
01 S-
>(t
01
et
0-01 -
E
cm
F3
0*001 0
x
{
01
0-05
02
0.15
I
0.3
025
035
ofseed dimensions
Variarnce
100-
?
(b)
x
10 - x
- - - - - - - ->-
-1
1 -
"
|
**
0*1 -*
0'01
X
X
X%
0
I
0
x
X
---
0.05
'I
I
01
015
02
I
I
025
03
0.35
dimensions
Varianceoffruit
andvariance
diasporeweight
between
Fig.1. Relationship
in(a) 44speciesofseedsand(b) 53
ofdiasporedimensions,
speciesof fruits.Data fromTable 1. (X) Specieswith
in thesoilforat least5 years;(x)
diasporeswhichpersist
inthesoilfor<5 years;
whichpersist
specieswithdiaspores
at
(#)specieswhoseseedbanktypecannotbe determined
data. The
or contradictory
presentowingto insufficient
whichall diaspores
dashedlineenclosestheregionwithin
arelonglived.
examined
diaspores, togetherwith a wide range of families,
seed sizes and shapes. An additionalconstraintwas
that seeds had to be available fromthe collections
held at UCPE.
Results
Diaspore weight,varianceand persistenceare shown
in Table 1, whileweightis plottedagainstvariancein
Fig. 1. It is apparent that persistent diaspores,
whetherseeds or fruits,occupy more or less the
same, unique region of the size/shape space.
Compactdiasporeswhichweighless than3 mgare all
inthesoil. For moreflattenedor elongated
persistent
diaspores,persistenceappears to be determinedby
shape, and all diasporesabove a criticalvarianceare
shortlived. This criticalvariance was identifiedby
eye fromFig. 1, and is verymucha workinghypothesis at thisstage.The exactlocationofthelinedividing
transientfrompersistentdiasporesin the lowerpart
of Fig. 1(a) is particularlyuncertain.Nevertheless
thereis some evidence that the criticalvariance is
higherforfruitsthanforseeds; thepersistent
slightly
fruitswitha moderatelyhighvariance[whichwould
place themin the transientregionof Fig. 1(a)] are
mostly grasses in the genera Poa, Agrostis and
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Table 1. Diaspore weight,varianceofthreediasporedimensions(transformed
so thatlongestdimensionis unity)and persistencein the
and 53 speciesoffruits.NomenclaturefollowsClapham,Tutin& Warburg(1981). Persistenceclasses: (p) specieswithdiasporeswhichpe
years; (t) species withdiasporeswhichpersistin the soil for<5 years;(u) species whose seed bank typecannotbe determinedat prese
data
contradictory
Seeds
Species
Family
Fruits
Weight
Persistence Species
Variance (mg)
0*020
Araceae
Arummaculatum
0-084
Araliaceae
Hedera helix
Balsaminaceae 0-063
Impatiensglandulifera
Campanulaceae 0-119
Campanula rotundifolia
Arenariaserphyllhfolia
Caryophyllaceae 0-041
Cerastiumfontanum
Caryophyllaceae 0-038
Silene dioica
Caryophyllaceae 0-026
Silene nutans
Caryophyllaceae 0-048
Silene vulgaris
Caryophyllaceae 0*066
Spergulaarvenis
Caryophyllaceae 0-022
Stellariamedia
Caryophyllaceae 0-076
Chenopodiaceae 0-062
Chenopodiumalbum
0*051
Helianthemumnummularium Cistaceae
Convolvulaceae 0-039
Convolvulusarvensis
04132
Cruciferae
Alliariapetiolata
Cruciferae
0-069
Arabidopsisthaliana
Cruciferae
0-094
Capsella bursa-pastoris
04132
Cruciferae
Cardaminehirsuta
04127
Cruciferae
Erophila verna
0-092
Cruciferae
Thlaspiarvense
Droseraceae
0-248
Drosera rotundifolia
0-236
Ericaceae
Ledum palustre
0*089
Juncaceae
Juncuseffusus
0.100
Labiatae
Origanumvulgare
0-117
Leguminosae
Anthyllisvulneraria
0-089
Leguminosae
Cytisusscoparius
4.540
20-430
7-320
0-067
0-061
0-120
0.646
0*298
1.199
0-449
0-327
0*560
1-280
10-420
3-451
0.020
0-123
0.101
0-032
1.163
0-018
0-020
0-010
0-098
3-529
6-734
t
t
t
p
p
p
p
p
p
p
p
p
p
p
u
p
p
p
p
p
u
t
p
p
t
p
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Achillea millefolium
Carlina vulgaris
Centaureascabiosa
Matricariamatricarioides
Erigeroncanadensis
Gnaphaliumuliginosum
Hieraciumpilosella
Leontodonhispidus
Senecio vulgaris
Coronopusdidymus
Carexflacca
Agrostiscapillaris
Anthoxanthum
odoratum
Arrhenatherum
elatius
A venulapratensis
Brachypodiumpinnatum
Brachypodiumsylvaticum
Bromuserectus
Bromussterilis
Dactylisglomerata
Deschampsiaflexuosa
Desmazeria rigida
Festucaovina
Festucarubra
Holcus lanatus
Koeleria macrantha
Family
Va
Compositae
Compositae
Compositae
Co'mpositae
Compositae
Compositae
Compositae
Compositae
Compositae
Cruciferae
Cyperaceae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
Gramineae
0*
00.
0.
0.
0.
0.
0.
0.
00.
0000000000000*
00-
Table 1. (Continued)
Seeds
Fruits
Weight
Variance (mg)
Persistence Species
Species
Family
Lathyruspratensis
Lotus corniculatus
Ononis repens
Trifoliumdubium
Vicia cracca
Vicia hirsuta
Allium ursinum
Hyacinthoidesnon-scripta
Nartheciumossifragum
Chamerionangustifolium
Epilobiumhirsutum
Oxalis acetosella
Plantagolanceolata
Pyrola minor
Digitalispurpurea
Euphrasia officinalis
Linaria purpurea
Viola arvensis
0-036
Leguminosae
0-040
Leguminosae
0-027
Leguminosae
0-053
Leguminosae
0-005
Leguminosae
0.017
Leguminosae
0.061
Lifiaceae
0.032
Lifiaceae
0-302
Lifiaceae
0.171
Onagraceae
04118
Onagraceae
04148
Oxafidaceae
Plantaginaceae 04150
0-216
Pyrolaceae
Scrophulariaceae 0-072
Scrophulariaceae 0-149
Scrophulariaceae 0-101
0-087
Violaceae
13-688
1V278
5-427
0-227
23-661
24190
4-270
64170
0.060
0-041
04138
1F0lO
1-891
0.001
0-072
0*130
0-133
0-400
u
p
u
p
t
p
t
t
u
t
p
t
p
t
p
t
u
p
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Family
Lolium perenne
Gramineae
Poa annua
Gramineae
Poa trivialis
Gramineae
Ballota nigra
Labiatae
Labiatae
Galeopsis tetrahit
Labiatae
Stachyssylvatica
Teucriumscorodonia
Labiatae
Labiatae
Thymuspraecox
Medicago lupulina
Leguminosae
Melilotusaltissima
Leguminosae
Polygonumaviculare
Polygonaceae
Rumexacetosella
Polygonaceae
Ranunculusrepens
Ranunculaceae
Rosaceae
Dryas octopetala
Potentillaerecta
Rosaceae
Rosaceae
Filipendulaulmaria
Galium aparine
Rubiaceae
Galiumsaxatile
Rubiaceae
Anthriscussylvestris
Umbelliferae
temulentumUmbelliferae
Chaerophyllum
Coniummaculatum
Umbelliferae
Daucus carota
Umbelliferae
Foeniculumvulgare
Umbelliferae
Heracleumsphondylium
Umbelliferae
Umbelliferae
Myrrhisodorata
Torilisjaponica
Umbelliferae
Urticadioca
Urticaceae
Va
0-2
0-1
0-1
0-1
0-0
0-0
0-0
0.0
0-1
0-1
0-0
0.0
0-1
0.2
0-0
0-1
0-0
0-0
0-2
0-2
0.1
0-1
0-1
0.2
0.2
04
0-1
240
K. Thompson
et al.
Holcus. While the regionof the graphwithinwhich
all diasporesare persistentis relativelywell defined,
itis nottruethatall diasporesoutsidethisregionare
shortlived.Large, moreor less sphericaldiasporesin
particularmay be either persistentor not. Here
habitatseemsto be thebestguide.Species withlarge,
round,short-liveddiaspores (seeds or fruits)are all
commonestin woodland, hedgerows or tall herb
communities(e.g. Vicia cracca, Hyacinthoidesnonscripta,Galium aparine),whilethosewithpersistent
diasporesare plantsofdisturbedarable (Convolvulus
arvensis, Galeopsis tetrahit)or fire-pronehabitats
(Cytisusscoparius) (Grime,Hodgson & Hunt 1988).
A strongphylogeneticeffectis also apparent in
Table 1. Familiesinwhichthediasporesare normally
small and compact (e.g. Caryophyllaceae,
whilefamiliesin
Cruciferae)are generallypersistent,
whichthe diasporesare largeand eitherflattenedor
elongated(e.g. Umbelliferae)are mostlyshortlived.
These trendsare also evidentwithinfamilies;small,
compact grass and composite fruitsare persistent,
whiletheirlargerrelativesare not.
Discussion
DIFFERENCES BETWEEN SEEDS AND FRUITS
Some interestingdifferencesbetween seeds and
fruitsemerge fromFig. 1. Seeds, whichuntilsheddingare enclosed withinthe protectivewalls of the
ovary,encompassa rathernarrowerrangeof shapes
than fruits.However, there are some important
exceptions.The fourspecies on therightof Fig. 1(a)
are all small-seededplantsof unproductive,infertile
habitats (Pyrola minor, Narthecium ossifragum,
Ledum palustre,Dorsera rotundifolia).The significance, if any, of elongated seeds in these typesof
habitatsis unknown.
The data illustratethatthelikelihoodofa diaspore
persistingin the soil is determinedto a large extent
not by its developmentalorigin(i.e. whetherit is a
seed or fruit),but by its size and shape. Withinthe
samplestudiedmoreseeds thanfruitsformedpersistent seed banks simplybecause seeds, on average,
are more compact than fruits.Size seems to differ
rather little between the two groups (Fig. 1),
althoughtheupperand lowersize limitsare occupied
by a fruitand a seed respectively.
PREDICTING PERSISTENCE
On the basis of the relativelysmall sample of the
British,mostlyherbaceous, floraexamined here it
seems thatseed size and shape can predictdiaspore
persistencein the soil. Additionalhabitatdata seem
capable of resolving those few cases where any
ambiguityremains.The mechanismunderlyingthe
relationshipinFig. 1 is almostcertainlyease ofburial,
linkedto the relativefreedomfrompredationconferred by burial (Thompson 1987). Most likely
mechanismsof burial (penetratingcracks in soil,
being washed into soil by rain, ingestion by
on small,
earthworms)will operate more effectively
compact diaspores. Exceptions include self-burial,
e.g. in Avena and Erodium (Stamp 1984), and ant
dispersal.Avenafatuais one conspicuousexampleof
a large, elongated diaspore with a persistentseed
bank whichfails to conformto the relationshipin
Fig. 1(b). Many genera with an elaiosome (e.g.
Luzula) have relativelysmall,roundseeds consistent
withFig. 1, whilesome withlarge,roundedseeds are
also persistent(e.g. Ulex). We are not aware of any
specieswhichcombinesantdispersalwitha transient
seed bank,butmoreworkis needed to determinethe
exact relationshipbetween ant disperal and seed
persistence.However, outside these small and perhaps atypicalgroups,the work of Peart (1984) has
demonstratedthatsmall diasporesnot onlybecome
buriedmore easily,but thattheyalso requireburial
forsuccessfulseedlingestablishment.
Of courseseed persistencein the soil is not wholly
determinedby seed size and shape. Germination
requirements,
dormancymechanismsand resistance
to pathogens also contributeto persistence. For
example, phenolic defence compounds are implicated in prolongedseed persistence(Kremer 1986;
C. Moss, G.A.F. Hendry, K. Thompson & P.C.
Thorpe, unpublished observations). Nevertheless
seeds do not persistfor long periods on the soil
surface,and burialis clearlyan essentialpreludeto
persistence.Artificialburial nearlyalways overestimates the potentialfor persistencein the soil. For
instancePons (1989) commentedon the resultsof a
seed burial experiment:'The resultsindicate that
Moliniacaeruleaseeds can surviveforlongperiodsin
the soil, but the author knows of no records of
persistentseed banksof thisspecies'. Under normal
circumstancesdiaspores of some species frequently
become buried,whileothersdo so onlyrarely.Those
diasporeswhichoftenbecome buried consequently
experiencedifferent
selectionpressuresfromthose
whichdo not,and thusprobability
ofburialhas come
to be associated witha suite of othercharacteristics
concerning germination,dormancy and defence
chemistry.Measurementsof seed shape and size,
whichadmittedly
affectonlythefirstessentialstepin
seed persistence,can perhaps thereforeprove a
surprisingly
good guide to subsequent seed persistence. It remainsto be determinedwhethermechanisms whereby seeds become incorporatedinto a
persistent
seed bankare similarworld-wide,butifso,
we anticipatethat this method of predictingseed
persistencecan be easilyextendedto otherflorasand
climates.
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241
Acknowledgements
peristencg n
so
This work was supportedby the Natural EnvironmentResearch Council.
References
Bakker, J.P. (1989) NatureManagementby Grazing and
Cutting.Kluwer,Dordrecht.
Clapham A.R., Tutin T.G. & Warburg, E.F. (1981)
ExcursionFlora of theBritishIsles, 3rdedn. Cambridge
University
Press, Cambridge.
Grime, J.P. (1989) Seed banks in ecological perspective.
Ecology of Soil Seed Banks (eds. M. A. Leck, V.T.
Parker& R.L. Simpson), pp. xv-xxii.Academic Press,
London.
Grime,J.P., Hodgson, J.G. & Hunt, R. (1988) ComparativePlantEcology. UnwinHyman,London.
Hodgson, J.G. & Grime,J.P. (1990) The role of dispersal
mechanisms,regenerativestrategiesand seed banks in
thevegetationdynamicsoftheBritishlandscape.Species
Habitats(eds. R.G.H. Bunce &
DispersalinAgricultural
D.C. Howard), pp. 65-81. Belhaven, London.
Holm, L.G., Plucknett,D.L., Pancho, J.V. & Herberger,
J.P. (1977) The World'sWorstWeeds.Hawaii University
Press,Honolulu.
R.G. & Usher, M.B. (1987) The seed bank in
Jefferson,
soils of disused chalk quarriesin the YorkshireWolds,
England: implicationsfor conservationmanagement.
Biological Conservation42, 287-302.
Keddy, P.A. & Reznicek, A.A. (1982) The role of seed
banksin the persistenceof Ontario'scoastal plain flora.
AmericanJournalof Botany69, 13-22.
Kremer, R.J. (1986) Antimicrobialactivityof velvetleaf
(Abutilontheophrasti)
seeds. WeedScience34, i17-622.
Leck, M.A. (1989) Wetland seed banks. Ecology of Soil
Seed Banks (eds. M.A. Leck, V.T. Parker & R.L.
Simpson),pp. 283-305. Academic Press, London.
Marks, P.L. & Mohler, C.L. (1985) Succession after
eliminationof buriedseeds froma recentlyplowed field.
Bulletinof the TorreyBotanical Club 112, 376-382.
Peart,M.H. (1984) The effectsof morphology,orientation
and position of grass diaspores on seedling survival.
Journalof Ecology 72, 437-453.
Pons, T.L. (1989) Dormancy,germination
and mortality
of
seeds in heathlandand inlandsand dunes.Acta Botanica
Neerlandica38, 327-335.
Rowell, T.A., Walters,S.M. & Harvey, H.S. (1982) The
rediscovery
of thefenviolet,ViolapersicifoliaSchreber,
at WickenFen. Watsonia14, 183-184.
Stamp, N.E. (1984) Self-burialbehaviour of Erodium
cicutariumseeds. Journalof Ecology 72, 611-620.
Thompson,K. (1987) Seeds and seed banks. New Phytologist106 (suppl.), 23-34.
Thompson,K. (1992) The functional
ecologyofseed banks.
Seeds: theEcologyofRegeneration
in PlantCommunities
(ed. M. Fenner), pp. 231-258. CAB International,
Wallingford,UK.
Thompson,K. & Grime,J.P. (1979) Seasonal variationin
the seed banks of herbaceousspecies in ten contrasting
habitats.Journalof Ecology 67, 893-921.
Van Der Valk, A.G. & Verhoeven,J.T.A. (1988) Potential
role of seed banks and understoreyvegetation in
restoring
quakingfensfromfloatingforests.Vegetatio76,
3-13.
Received11 March 1992; revised22 June1992; accepted2
July1992
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