Studies on the Ecological and Physiological Significance of Amphicarpy in Gymnarrhena
micrantha (Compositae)
Author(s): Dov Koller and Nurit Roth
Source: American Journal of Botany, Vol. 51, No. 1 (Jan., 1964), pp. 26-35
Published by: Botanical Society of America
Stable URL: http://www.jstor.org/stable/2440059
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Amer.Jour.Bot. 51(1): 26-35. 1964.
STUDIES ON THE ECOLOGICAL AND PHYSIOLOGICAL SIGNIFICANCE
OF AMPHICARPY IN GYMNARRHENA MICRANTHA (COMPOSITAE)'
Dov
KOLLER
AND NURIT
ROTH
The HebrewUniversity,
Jerusalem
and
The NegevInstituteforAridZone Research,Be'er Sheva,Israel
ABSTRACT
The 2 typesoffruit(aerialan7dsubterranean)
borneby the dwarfdesertannualGymnarrhena
micrantha
werecomparedwithregardto theirresponsesto factorsaffecting
theirformation,
disand seedlingmortality.The 2 typesof fruitdiffered
persal,germination
markedlyin several
respects.In comparison
withthesubterranean
fruits,
the aerialonesare muchsmallerand more
in whichtheydevelopis moredependenton a
numerous,
but theformation
ofthe inflorescence
favorablesupplyofsoilmoisture.
The aerialfruitsaredispersed
bywind,afterbecomingdetached
by a complexseriesofhygroscopic
movements
whichinvolveseveralorgansand tissues,whilethe
subterranean
fruitsneverleave the dead parentplant,germinating
rightthroughits tissues.
ofthesubterranean
Germination
fruits
startsaftera shorter
incubation
periodandis lesstemperain bothlightand dark.Lightstimulatedgermination
of both typesoffruit,inture-dependent
ratesand finalpercentages,
but not affecting
creasingtheirgermination
the durationof the incubationperiod.In the subterranean
the rate of germination
was equallystimulatedby
fruits,
lightovertheentiretemperature
range,witha well-defined
optimumat 15 C in bothlightand
dark. In the aerial fruits,the same optimumwas foundonly in the light,rates in darkness
withdecreasing
In the aerialfruits,
increasing
temperatures.
alternations
of lightand darkwere
morefavorableto germination
thaneithercontinuous
lightor dark,thefulleffect
beingobtained
witha single8-hror 16-hrlightperiod,providedit was precededby 16 or8 hrofdarkness,
respecoflightand darkwerenotobservedin thesubterranean
tively.Similarreactionsto combinations
fruits.
Seedlingsdeveloping
fromthesubterranean
fruits
weremuchlarger,butgrewat a relatively
muchslowerratethanthosefromaerialfruits.The former
weredistinctly
moretolerantofunfavorablesoil-moisture
regimes,such as low moisturesupplyand drought.It was concluded
that the 2 typesof fruitserve2 distinctfunctions
in the biologyof the plant.The aerialfruits
are adaptedto thefunction
ofincreasing
ofthespecieswithinsuitablehabitats,
the distribution
whilethesubterranean
fruits
areadaptedtoincreasing
theprobability
ofthesurvivalofthespecies.
THE
PHENOMENON
of amphicarpy,where the
same plant bears both aerial and subterranean
fruits,is knownin quite a fewspecies.Therehave
been several suggestionsregardingthe ecological
ofthisphenomenon.One suggestionis
significance
that seedlingsgerminating
fromthe subterranean
fruits are provided with a better chance for
subsequentsurvival,since their micro-habitatis
that which provided the parentwith conditions
adequate forcompletionof the lifecycle (Zohary,
1937). Anothersuggestionis thatthesubterranean
fruitsare betterprotectedfromthe extremesof
the climate and fromforaginganimals than are
the aerial fruits(Engler,1895; Warburgand Eig,
1926), but this suggestionis opposed by Zohary
(1937). Yet anothersuggestionis that the very
fact that the subterraneanfruitsare already in
1 Received forpublication April 1, 1963.
This study was carried out at the Negev Institute for
Arid Zone Research, Be'er Sheva, and at the Hebrew
University,Jerusalem,under Grant No. FG-Is-1 15 from
the U.S. Department of Agriculture.The authors wish to
express their gratitude to their colleagues, D. Sitton and
M. Sachs, fortheirhelp, suggestionsand discussions.
26
the soil providesthem with a betterchance for
germinationand, therefore,presumablywith a
betterchance forsurvivalof the plants to which
theygiverise (Engler,1895). All thesesuggestions
are based mostlyon observations,and much less
on directexperimentalevidence.
The studies describedbelow were aimed at a
more detailed investigationof the physiologyof
the seeds and seedlingsof a typical amphicarpic
plant, in orderto determineany possible differences whichmightbe relatedto the value of this
particular adaptation to the survival of the
species. Gymnarrhenamicranthawas selected
becauseit has aerialand subterranean
fruitswhich
are very distinctfromeach other and because
intermediateformsof fruitare lacking.
Gymnarrhena
micranthaDesf. is a dwarfcomposite, belongingto the Saharo-Sindianphytogeographicelement (Eig, 1931-32). The plant
is a winter-growing
annual ofwide occurrencein
the steppe and desert regions of the Negev
(Israel). In thisregionit is conspicuousby having
habitat requirementsfar less strict than the
majorityof otherwinterannuals,since its distri-
January,19641
KOLLER
AND ROTH-AMPHICARPY
IN GYMNARRHENA
27
This behavioroccurredalso
butionis as abundanton slopes,plainsand "ham- aerial inflorescences.
mada" (gravelpavement)as in gullies,drywater- in experimentswith controlled water supply,
or as simulatedrainfall.
courses,depressions,etc.,whichreceiveadditional eitheras floodirrigation,
water.
runoff
Dispersal-The achenes formedin the subterremainenclosed withinthe
MATERIALS AND METHODs-Germination tests ranean inflorescences
werecarriedout in Petridishes,on a singlelayerof dead lignifiedtissues of the motherplant, and
Whatman's No. 1 filterpaper, moistenedwith when they germinate,the radicle penetratesthe
5 ml deionized predistilledwater. Incubators surroundingtissues and the seedling becomes
operatingwithin?0.5 C of the preset tempera- establishedin the identicalpositionof the parent
tureswereused. These incubatorswereilluminated plant. This may repeat itselfin successivegenerwith a mixtureof incandescentand fluorescent ations,leadingto the formationof a dense colony
was pre- of live and dead plants (Fig. la, b).
white light. Temperaturestratification
vented by a forcedair circulation.Dark germiThe achenesformedin the aerial inflorescences
tins. are dispersedmostcommonlyall at thesame time,
nation tests were carriedout in light-proof
The course of germinationwas followedby fre- leaving the receptacle bare. The mechanismof
quent counts, at which time the germinated dispersalwas studied under both fieldand conseedlingswere removed. Dark germinationwas trolledconditions.These studieshave shownthat
countedat the same time,by use of a dim green dispersalis operated by a formof hygrochastic
light(greenfluorescent
lamp wrappedwithseveral mechanism, respondingto repeated cycles of
layers of greenand blue cellophane),which was moisteningand drying.The responseswere the
of same whetherthe moisteningagent was liquid
found to have no effecton dark-germination
this species.
water,dew, or saturatedwater vapor. Details of
Soil for tests of survival was loess fromthe the mechanismwere studied by dissectingthe
natural habitat of this species. Before use, the inflorescenceas well as by microscopicexamsoil was cleanedof stonesand plant debris.These inationof mediansectionsthroughthe receptacle.
tests were carriedout in an exposed location in Dry sectionswere mountedin paraffinoil. The
Be'er Sheva. Detailed climatologicaldata forthis followingorgans and tissues were found to pararea are available fromtheMeteorologicalService, ticipate in the mechanismof dispersal,by perIsrael Ministryof Transport.
forminghygroscopicmovements,or by underRESULTS-AMorphology
and biology-A detailed going other changes, upon being moistenedor
deseriptionoftheplantis givenby Zohary(1937). dried. (1) The uppermostlayers of the domeThe followingdescriptionis based on our own shaped receptacleforma thintissue,composedof
observations,whichwere made over a period of collenchymatouscells, which becomes nearly
severalyears,on the morphology
of the plant and transparentwhen wet. The mechanicalstrength
bondingthe cellstogetheris apparentlyweakened
on its behaviorin the field.
has a compressedstem, thereby,sincethe tissueis easily disruptedin this
micrantha
Gymnarrhena
bearing a rosette of leaves. The aerial inflor- condition.(2) A second collenchymatoustissue,
eseences produce numerous,small achenes in a which underlies the above-mentionedsurface
compact capitulum,and each is borneat the end layer of the receptacle,swells very rapidlyupon
of a shortbranch.The subterraneaninflorescences being moistened.(3) The dry bract subtending
are sessile,borne in leaf axils whichare situated the achene is elongatedand lanceolate,with the
10-15 mm below the soil surface. Each inflor- edges slightlyrolled inwards. When it is first
but its edgesrollfurther
escence produces only 1-2 large achenes. The moistened,it straightens,
numberof aerial inflorescences
may vary between inwards.When it is subsequentlyredried,it coils
none and several (see below),whilethe numberof and becomes hook-shaped,and this coiling bethe subterraneaninfloreseences
is usuallybetween comes more pronounced upon furtherdrying.
1 and 3. The corolla tubes of the subterranean (4) The pappus ofthe dryacheneis in theformof
floretsopen on the soil surface. The achenes a paint-brushand the entireachene is enclosed
formedin the aerial inflorescences
are small and withinthe rolled edges of the subtendingbract.
are equipped with a well-developed pappus, When it is moistened,the hairsbend outwardsat
whereasthose formedin the subterraneaninflor- theirbase and the pappus opens up as the ribsof
escences are much larger and lack a pappus, or an umbrella.This movementis not reversibleby
bear onlya vestigialone. Duringthe summer,the drying.These featuresare shown in Fig. 2-5.
dead plants are sometimesgrazed by animals,
Some simplehistochemicaltestswere made, in
which pull the plants out of the groundin their orderto obtain moredetailedinformation
on the
search for the subterraneanachenes,whichthey nature of the receptacle.Freehand median secremove by chewingrthe entire plant. Zohary's tionswerecut throughthe receptacleand stained
findings(1937) that the formationof the sub- with Genevois Reagent2 and Cl-Zn-I Reagent,
terranean inflorescencesprecedes that of the respectively.These stains showed that whereas
aerial ones were confirmed.It was furthernoted
that in years with low rainfall,the plant can
2 GenevoisReagent = 2.5%
Chrysoidin+ 2%oCongo
wither and die without altogetherformingthe Red,inammoniated
aqueoussolution.
Fi.
-3-Fg.l.
olnyofdadplnt
o
ymarhea
zrath
wthsedins
f uteraea
thog
hi ises-i.l.Snl
da
ln,wt
f t utraenfrisgriaigthog
Fig
2.Mdaoetorhog
r eetceo
h nlrecnemutdi
aafnolFg3Mda
through moistened
receptacle.~~~~~~~~~~~~~~~~~~~~~~~~~Ji
futsgemiatn
t
ise.
eto
January,1964]
KOLLER
AND ROTH-AMPHICARPY
both the uppermostlayer of the receptacleand
swellinglayerare bothcomposedof
theunderlying
collenchymatouscells, cell walls of the former
layer do not stain as cellulose,while those of the
latter layer do. The presence of hemicelluloses
in the cell walls of the uppermost layer was
indicated by the fact that this tissue was completelymaceratedin 3% HCl, during12-hrsoaking of the inflorescence,by dissolution of the
primarywalls. The achenes were thereby detached.A similarsoakingin watercaused none of
these changes. The suspected presence of hemicellulosesin this tissue was furtherconfirmedby
the pink stain obtained in the cell walls after
accordingto
treatmentwith Phloroglucinol-HCl,
Johansen(1940).
The dispersal mechanismapparentlyinvolves
the participation of all the above mentioned
tissues and organs (Fig. 7). The ripe, dry inflorWhen
escenceis compactand strawberry-shaped.
it is wet, the expansionof the receptacleand the
straighteningof the bracts bring about a distendingof the entirecapituluminto the formof a
lk~
IN GYMNARRHENA
29
hedgehog.The pappus opens up. At this stage
none of the achenesis released.When the head is
redriedthereceptaclecontractsand the capitulum
regainsmore or less its originalshape. However,
the irreversibleopeningof the pappus is evident
by the protrusionof its hairs betweenthe bracts.
Further cycles of moisteningand dryingbring
about the curlingof the bracts,and theyare thus
extractedfromtheir insertionin the receptacle,
whichby this timethe moisteninghad weakened.
This movementofthe bractspullsout the achenes
which they subtend. Very frequentlyall the
achenes are thus loosened at the same time,and
are easily dispersed by wind. The pappus is
permanent(at least up to germination)and serves
as an aid to dispersal. Achenes from aerial inflorescences
have been observedto come to restin
crevicesin the soil and at the bases of stonesand
rocks.
Germination-Thegerminationbehaviorof the
2 types of achene was investigatedby studying
the effectsof light and temperatureon their
germinationresponses.M\Iaterial
of different
ages
~~~~~
4 4
Fig. 4-7.-Fig. 4. Disintegration
of top layerof receptaclein moistenedcapitulum(mediansection).-Fig. 5. Top:
Moistenedfloralbract.Bottom:Bractscoilingat different
stagesofre-drying.-Fig.
6. The 2 typesoffruitofG. micrantha
and 6-dayold seedlingsproducedfromthem.At top,2 subterranean
achenesand 2 oftheirseedlings.At bottom,2 aerial
achenesand 2 oftheirseedlings.Dry acheneson left,moistenedand redriedacheneson right.Note absenceofpappuson
subterranean
achenes,unopenedpappusin unmoistened
aerialachene,and irreversible
openingof thepappusin moistened,redriedaerialachene.-Fig. 7. FruitingheadsofG. micrantha.
Dry-on left,moist-on right,and afterdispersalin center.Divisionsat bottomofFig. are 1 mmapart.
30
AMERICAN
JOURNAL
OF BOTANY
[Vol. )I
(fromripening)and fromcollectionsof different
years was compared. Only minor quantitative
differenceswere observed and qualitative responses were the same, so that when an experiment was repeated at different
times the results
could be treated as replicationsand combined.
The responsesof the 2 types of achene to the
conditionswerecomplex.In orderto
experimental
facilitate an analysis, the results were plotted
graphically.The germinationcurveswere almost
perfectlysigmoidal. The values "P" (final percentages), "S" (time in days until germination
reached P/6) and "R" (rate of germinationin
percentper day, between P/6 and 5P/6) were
computed fromthe germinationcurves (Koller,
1957). The relationshipbetweenthesevalues and
0~~~~
in lightand in darkness,respectively,
temperature,
are presentedin Fig. 8. These resultswere combined from4 separate experiments,with 3 replicates of 25-50 achenesin each.
The resultsin Fig. 8 show that the 2 types of
achenebehavedsimilarlyin thefollowing
respects:
In continuouslight,finalpercentageswere consistentlyhigherthanthosein continuousdarkness,
N.~X.
30'A
The depressingeffectsofhigh
at all temperatures.
~0/
Z
temperatureson finalpercentageswere stronger
in continuousdarknessthan in continuouslight,
the declinein darknesssettingin alreadyat 15 C,
while in light the decline set in only at 25 C.
was the most rapid between
Start of germination
in
both
and
20
C,
15
lightand darkness,and was
10.
.
not affectedby continuouspresenceor absence of
was increasedby light,
light.Rate of germination
and light
but theinteractionbetweentemperature
in the 2 types, as will be
or dark was different
describedbelow.
Except for these 2 similarities,the types of
achene differedmarkedlyin several important
respects. Final germinationpercentagesof the
aerial achenes were much more temperaturedependentthan those of the subterraneanones.
This differencein sensitivitywas apparent in
bothlightand dark. Thus in darkness,"P" of the
aerialacheneswas reducedalmostlinearlyby 78%
was increased
(from82 to 4%) as the temperature
A~ \0
O 4
from10 to 25 C, while that of the subterranean
achenes was reduced only by 44% (from74 to
30%) under the same conditions.In light, this
2
$
zA
temperaturesensitivityis evident only at the
higher temperatures(between 20 and 25 C),
causingthe reductionof "P" by 8% (from95 to
87%) in the subterraneanachenes,and by 50%
(from88 to 38%) in the aerial ones. Start of
ofthesubterraneanacheneswas more
germination
TEMP. 0C
rapid than that of the aerial ones. The differences
Fig. 8. Effectsof lightand temperature
on start "S", are small, but consistentat all temperaturesin
rate "R" and finalpercentages"P" of germination
of both light and darkness. Rate of germination
aerial and subterranean
fruitsof Gymnarrhena
micrantha. presentsa complexinteractionbetweenlightand
Descriptionand details in text. (Results at all temps.,
effects.In the subterraneanachenes,
except 5 C, are means of 4 separateexperiments,
with temperature
3 replicatesof 25-50 fruitsin each. Resultsat 5 C are of a clear optimumis evidentat 15 C in both light
and darkness,and lightis nearlyequally effective
only1 suchexperiment.)
in increasinggerminationat all temperatures.In
Light
Dark
0
Aerial fruits
0
the aerial achenes,the rate of dark germination
*----a
X- - - X
Subterranean fruits
decreases almost linearlywith increase of temA
A-
80
Z60
1f40
r201a
i20
,9
410
|
op.
8
6-
<
A
5
lb i
2b 25
January,1964]
KOLLER
AND ROTH-AMPHICARPY
31
IN GYMNARRHENA
1. Theeffects
oflight(L)/dark(D) regime
on start A-S"
"P" of
(days),rate"R" (percent
perday) and finalpercent
germination
(on8thday) ofaerialachenesofG. micrantha
at 20 C and 25 C, respectively.
Threereplicates
of50 achenes
each.Explanationin text
TABLE
20C
P
Lightregime
12
Continuous D
ContinuousL
8 hrL, alternation
16hrD
16 hr D
8 hr L --cont.
S
D.
5.0
98
2.6
perature3),while in light a clear peak is evident
at 15 C. At temperaturesabove this optimum,
light seems to stimulate germinationequally,
since Rdark is parallelto Rlight.
Under natural conditions,the seeds are not
exposedto continuouslight,but to alternationsof
lightand dark. The stimulatingeffectsoflighton
germinationwere, therefore,studied with reference to such alternations.However, scarcityof
subterranean achenes permitted extensive experimentationonly with aerial achenes, and
rather limited ones with subterraneanachenes.
Germinationof the aerial achenes was tested
several times at 20 and at 25 C, in continuous
light, continuous dark, diurnal alternationsof
8 hr light with 16 hr dark, and darknessinterrupted after 16 hr incubationby a single 8-hr
light period. The course of germinationwas
plotted graphicallyand analyzed as described
above. The resultsin Table 1 are typical.
The resultsin Table 1 showed that combinations of light and darknesswere more favorable
for germinationthan either uninterruptedlight
or dark. Work with Plantago coronopusshowed
that the sequence of light and dark was of importancein the controlofgermination(Kollerand
Roth, unpublisheddata; see Koller, 1962). It was
thereforedecided to extendthese experimentsby
testingthe effectsof such sequences on germination of G. micrantha.The results in Table 2
show the responsesof the aerial achenes.
I It must, however, be rememberedthat the values for
5 C are based on a single experiment.
P
R
4.2
3.2
85
99
25C
3
3
18
19
31
52
28
43
S
R
5.0
5.1
6
14
4.3
11
The resultssummarizedin Tables 1 and 2 show
that treatmentswhich incorporatedL were invariably more favorable for germinationthan
those carriedout in continuousD. At the same
time,it is clear that treatmentsin whicha period
of L was precededby D weremorefavorableeven
than those carriedout in continuousL, or in D
whichwas precededby an initialL-period.
These stimulatoryeffectsmanifestthemselves
in different
ways, in the temperaturestested. At
15 C, "P" and "S" are the same in all treatments,
but "R" is increasedin all treatmentsincorporating both L and D, irrespectiveof sequence.At
20 C, the optimaltreatmentsin all respectswere
those in whicha periodof L was precededby an
initial D period. However, "P" in continuousL
was as high. Highest "S" values (slowest start)
were obtainedin continuousL and in continuous
D. At 25 C, the values of "S" and "R" do not
differsignificantlybetween the various treatments,but "P" values are highestin treatments
wherea period in lightis precededby an initial
dark-period.
Scarcity of subterraneanachenes prevented
extensivecomparisonswiththe aerial achenes,on
the effectsof light-darksequences and combinationsupon germination.
Material was available
for only 1 sufficiently
detailed experiment.The
resultsofthisexperiment
are presentedin Table 3.
For a varietyof technicalreasons,experiments
with the 2 types of achene were carried out
at different
times. Direct comparisonsare, therefore,not justified.However,the data in Table 3
showthat in the subterraneanachenestherewere
2. The effects
of light(L)/dark (D) sequenceson start"S" (days), rate "R" (percentper day) and final percent"P'
of germination(on 14thday) of aerial achenesof G. micranthaat 15 C, 20 C and 25 C. (Expt. at 15 C not simultaneous
withothers.)Threereplicatesof 50 acheneseach. Explanation in text
TABLE
15C
Lightregime
P
Continuous D
83
16hrD -*8hrL
cont. D
8 hr D -16 hr L
cont. D
8 hr L -cont. D.
16 hrLL cont. D
24 hr L
cont. D
87
91
78
92
92
ContinuousL
85
S
1.9
1.9
1.8
1.9
1.7
1.7
2.0
20C
R
35
24
65
61
65
62
77
P
S
16
4.7
66
72
24
39
33
2.8
2.9
3.1
3.3
4.0
72
4.3
25C
R
4
24
21
17
3
6
6
P
6
31
53
47
32
39
42
S
2.7
2.9
3.0
2.8
2.5
3.2
R
4
9
10
6
6
12
32
AMERICAN
JOURNAL
[Vol. 51
OF BOTANY
TABLE 3. The effects
of light(L)/dark (D) sequenceson start"S" (days), rate "R" (percentper day) and final percent"P"
Three replicatesof
of germtnation(on 5th day) of subterraneanachenes of G. micranthaat 20 C and 25 C, respectively.
25-30 achenes. Explanation in text
25C
20C
Lightregime
ContinuousD
ContinuousL
8 hrL, alternation
16 hrD
8hrL 16hrD
8 hr D -*16 hr L
8 hr L -cont. 1)
cont. I)
16 hr L
24 hr L
cont. D
cont. D
cont. D
P
S
R
P
S
R
76
79
91
1.2
0.9
1.0
38
49
37
42
69
84
0.7
0.8
1.0
25
22
31
90
88
86
89
83
1.0
0.7
1.1
1.1
1.0
56
50
62
84
65
83
79
81
72
88
1.1
1.0
1.3
1.0
1.0
36
36
38
24
34
no strikingeffectsto treatmentsincorporating than those fromthe subterraneanachenes, the
both lightand darkness,over those carriedout in "growth" of the formerwas several times more
continuouslight. It must, however,be remem- rapid. Actual growthrates were not determined,
bered that subterraneanachenes are not as light- since these would have to be related to initial
sensitiveas the aerial ones, at the temperatures imbibedembryoweight.The relationshipbetween
tested, which would make it more difficultto this weightand the weightof the achene is differpick out small effectswith such a limitedexperi- rentin the 2 typesof achene,sincethe aerial ones
ment.
includefloralparts of considerablesize whichare
Seedling development-Sizeand weight differ- absent (or vestigial) in the subterraneanones.
encesbetweenthe2 typesofachenewereparalleled Endospermis absent in both. It is thus clear that
by differenices
between the seedlings to which the weightratio of embryoto entire achene is
theygave rise (Fig. 6). Air-dryweightof achenes lower in the aerial achenes than in the subterof the 2 types was determinedby averagingthe ranean ones. These considerationsindicate that
in actual growthrate betweenithe
weight of 10 individual achenes of each type, the difference
Growth of the seedlings was compared in the seedlingsfromthe 2 types of achene are much
followingmanner. Achenes of both types were largerthan indicatedby the "growth"figuresin
incubated at 15 C in the dark. After3 days, 10 Table 4.
achenes of each type were selected,in whichthe
Tolerance of seedlings towards adverse soilradicleof the seedlingwas just protruding.These moistureconditions-Two methodswere tried to
seedlingswereleftto growat 15 C in thedarkfor simulateadversesoil-moisture
conditions.One was
an additional 3 days, afterwhichthe total fresh b) withholdingirrigationforvarious periods,the
weight,and the freshweightof the shoots and otherwas by regularsupplyof different
levels of
roots was determined.The results are given in liinitedirrigation.
Table 4.
The initial procedurewas the same in both
The results in Table 4 show that although methods. Seedlings from both types of achene
seedlingsfromaerial achenes were much smaller weregrowntogetherin drainedplastic containers
filledwithcleanedloess soil. The watercontentof
the soil in the containerswas maintainedat the
TABLE 4. Growthof G. micranthaseedlingsfromaerial and
same level (33 g water per 400 g soil in each) by
subterraneanachenes. Seedlings germinatedand grown
daily addition of water to restorethe original
at 15 C in the dark for 6 days. Means and S.E. of 10
gross
weight.When the seedlingsappeared estabseedlings or achenes. "Growth" expressed as percent
lished (10 days), the containerswere transferred
increase in freshweightfr-omachene to seedling
to an exposedlocationoutdoors,wherethe treatments were carriedout. The course of seedling
Aerial
Subterranean
mortalitywas then followedby frequentobserachenes
achenes
vations. Three identicalcontainerswere used in
each treatment,in each of which8 similarseedA. Fresh weight (mg)
lings fromeach type of fruitwere grown. The
Achenes
0.37?+0
0.05
6.5040.55
experimentswere repeated 3 times: in January,
Whole seedlings
4.414?0.49
February,and April, 1962. The resultsdid not
26.27?4-1.98
differqualitativelyin the 3 experiments.During
Seedling roots
1.56?i00.28
10.38?4-1.02
the February experiment,which is describedin
Seedling shoots
2.85?40.29
15.89?i 1.13
detail below, the minimal temperatureswere
between 1 and 10 C, and the maximal temperB. "Growth" (%7)
1029
304
aturesvaried between15 and 32 C.
1964]
January,
KOLLER AND ROTH-AMPHICARPY
IN GYMNARRHENA
33
as influenced successfully.The numerous aerial fruits borne
G. m crantha,
5. Seedlingmortalitljin
in irrigation.
Explanation by each plant are formedlaterin ontogeny.Their
by durationof interruption
in text
developmenttakes place at the soil-airinterface,
TABLE
where the environmentis rather specialized
Durationofinterruption (Geiger,1959). When ripe,theybecomedetached
(days)
fromthe receptacleby a complexseriesof move-
ments,whichinvolvevarious parts of the inflorescence and requireseveral cycles of moistening
and dryingfor completion.The detached fruits
24
21
17
7
Dead seedlingsfromaerial
are adapted to dispersal by wind, and become
achenes:
lodgedin soil crevices,usuallyfarfromthe parent
9
0
0
Dead seedlingsfromsub0
is available on the
plant. So far,no information
terraneanachenes
environmentalconditionswhich determinewhen
the plant would cease to produce the earlier
subterraneaninflorescencesand switch over to
HowIn the firstmethod,water was withheldfrom the productionof the aerial inflorescences.
different
groupsof containersforvarious periods ever, both field observationsand experimental
(1, 3, 5 and 7 days, respectively),whenirrigation workwith controlledirrigationhave shownthat
was much
was resumed,as before.The effectsof this treat- the productionof aerial inflorescences
ment on seedling mortality (number of dead more dependenton availability of soil-moisture
This
seedlings24 days afterplanting,or 14 days from than that of the subterraneaninfloreseences.
the start of interruption
in irrigation)are given may well be due to the factthat thelatterare the
firstto be formedin ontogeny,when a relatively
in Table 5.
In the second method, the treatmentscon- small part of the rain water which had caused
sisted of daily irrigationsin amounts bringing germinationhad been utilizedforgrowth.Whatthe watercontentofthe soil to 20, 25, 45 and 60 g ever the cause, the fact is that, as a result,the
waterper 400 g soil. The effectsof thistreatment subterraneanfruitshave a muchhigherprobabilon seedlingmortality(numberof dead seedlings ity of beingformedthan the aerial ones.
30 days fromplanting,or 20 days fromthe start
also
The data in Fig. 8 indicatethat differences
of the treatment)are givenin Table 6.
exist betweenthe germinationresponsesof the 2
All these experimentsshowed that in both typesoffruitto environmental
conditions.Taking
methods which were used to simulate adverse firstthe value of "S" as indicatingthe durationof
soil-moisturerelationships,the seedlings from the preparatoryprocesses before the start of
subterraneanachenes survivedto a much larger germination,
it appears that underall conditions
extent than did those fromthe aerial achenes. the subterraneanfruitswould germinateearlier,
DIscussIoN-Summarizing the observations and their embryo will consequentlyestablish
and the experimentaldata, we find that the 2 directcontactwith soil moisturesoonerthan the
types of fruitformedby G. micranthadifferfrom aerial fruits.Admittedly,the difference
is never
each other not only in morphology,but also in verylarge.It must,however,be remembered
that
ontogeny,ecology and physiology,despite their under field conditionsin the desert, favorable
beingsituatedwithina fewmmofeach other.The moisturerelationsin the soil aroundthe fruitare
fewsubterraneanfruitsformedby each plant are ephemeral,and the advantageofeven a fewhours
protectedby a layer of soil as well as by the may be decisive in determiningestablishment.
tissuesof the motherplant,fromflowerinitiation This effectis enhanced by the fact that the
until germination.The establishmentof the habitatin whichthe aerial fruitsgerminateis the
seedlingsof thesefruitsis offereda highdegreeof soil surface,whereasthe subterraneanfruitsare
securityby the fact that they germinatein the invariablysituatedunder the soil surface,where
exact habitat where their parent plant grew moistureis much better protectedfrom evaporative loss. This would account for the observation that in the field,seedlingsfromsubterin G. micrantha,
as influenced
TABLE 6. Seedlingmortality
ranean fruitsare much more commonthan from
bywatercontent
ofthesoil.Explanationin text
aerial ones, despitetheirrelativelysmall number.
Final germinationpercentagesprovide an indiWatercontent
cation of the total potentialof the seeds to ger(mlpercontainer)
complex.
minateunderthe specificenvironmental
The resultsshow2 facts.One is thatalthough"P"
60
20
25
45
in both types of fruitis favorablyaffectedby
withinthe rangetested,
light,at all temperatures
1
Dead seedlingsfromaerial
13
10
3
oflightwas relativelystronger
thepromotiveeffect
achenes
in the aerial fruitsthan in the subterraneanones.
Dead seedlingsfromsub3
2
0
0
The second is that the aerial fruitsare more
terraneanachenes
inhibitionof "P"
sensitiveto high-temperature
1
3
5
7
34
AMERICAN
JOURNAL
OF
BOTANY
[Vol. 51
thanthesubterraneanones,in bothlightand dark. significanceof the requirementfor darkness to
Rate of germination"R" is another parameter precedelightmust remainspeculativetintilsubwhichindicatesa difference
betweenthe2 typesof jected to experimentaltreatment.
fruit.In the subterraneanfruits,Rlight is equally
Seedlings produced fromthe 2 types of fruit
higher than Rdark at all temperatures,both also differedgreatlyin size, growthrate and in
reachingan optimumvalue at 15 C. In the aerial the ability to withstand adverse soil-moisture
fruits,Rlight values are very similarto those of conditions.It mustbe made clearthatno attempt
the subterraneanfruits,with an optimumvalue was made to determinesurvivalas affectedby the
at 15 C. However, Rdark values are inversely water-potentialof the soil. The 2 types of test
proportionalto temperature,
showingno optimum which were performedwere designedto present
withinthe range tested. Thus, between 15 and the seedlingswith 2 variationsof simulatedfield
25 C Rdark parallels R light, whereas below 15 C conditions.One oftheserepresented
a situationof
a regular distributionof rainfall, of different
Rdark increaseswhileR light decreases.
The experimentsreportedin Tables 1-3 were amounts. The other representeda situation of
duration.Under
designed to study the possibilitywhether the cessationof rainfall,of different
stimulatingeffectsof light on germinationwere both these experimentaltreatmentsthe seedlings
photoperiodic in nature. These results show produced fromthe subterraneanfruitssurvived
clearlythat at least the aerial fruitswere more muchbetterthanthosefromthe aerialfruits.One
is due
stimulated by some combinationsof light and possibleexplanationis that this difference
in growth-rate
betweenthe 2 types
darknessthan by continuouslight.In this,their to differences
behavior resemblesthat of seeds of Eragrostis of seedling(see Table 4), rapidlygrowingtissues
ferruginea(Isikawa, Fujii, and Yokohama, 1961) being more susceptibleto droughtdamage than
and of Lemna perpusilla (Posner and Hillman, tissueswhichgrowslowly(cf.Levitt,1956,p. 161).
1962). This indicates the possibilitythat the
Morphological heterocarpy,which expresses
action of light is photoperiodicin nature. The itselfalso in physiologicalbehaviorof the seeds,
factthat a single8-hrlightperiodwas as effective has alreadybeen describedin severalspecies,e.g.,
as several such periods repeated at intervalsof Xanthiumpennsylvanicum
(Shull, 1911), Atriplex
16 hr in no way detractsfromthis possibility, spp. (Beadle, 1952; Kadman-Zahavi,1955; Koller,
since the photoperiodicinduction of flowering 1957),Salsola volkensii(Negbi and Evenari,1961),
may also be satisfiedwitha singleinductivecycle Aelleniaautrani(Negbi,personalcommunication),
(Hamnerand Bonner,1938; Evans, 1960; Zeevart, Pteranthusdichotomus(Evenari, personal com1962). However,the resultsin Table 2 raise some munication) and several others (Becker, 1913).
doubts.Thus, a single8-hrlightperiodis no more There does not appear to be any evidernce
as to
effectivethan a single 16-hr one. Secondly, it whetherthe formationof 2 (or more) types of
would seem that the effectiveness
of the light- fruiton the same plant is determinedby the
perioddependson its beingprecededby darkness, physiologicalage of the plant or by its environwhich,in photoperiodicterms,would mean that ment at the time of fruitdevelopment.Possibly,
only dark processesand the secondhigh-intensityin species where transitionaltypes occur, as in
lightprocessare required(cf.Isikawa et al., 1961). Atriplexdimorphostegia
(Koller, 1957), the latter
The present results do not seem sufficientto possibilitymight be feasible, but where trandecide whetheror not the sensitivityof the aerial sitionaltypes are absent, as in G. micrantha,
the
fruitstowards light is photoperiodicin nature, formerpossibilityseems more likely.This raises
and moreworkis in progresson thisproblem.For another problem. In heterocarpicplants, the
the time being it can only be said that both at various types of fruitdevelop at different
stages
20 and 25 C some preparatorydark-requiring in the ontogeny of the mother plant. Conseprocesses are needed for full effectivenessof quently, their ripeningtakes place in different
lightin stimulatingthe germinationof the aerial seasons and thus under different
environmental
fruits.The resultssummarizedin Table 3 show conditions.Differencesin theirphysiologicalbethat the subterraneanfruits were also more haviormay thenbe caused eitherby geneticprefavorablyaffectedby combinationsof light and determination,or by environmentexisting at
darknessthan by continuouslight alone. How- time of ripening,as has been shown to occur in
ever,the effectsof such combinationsweremuch Chenopodiumamaranticolor(Lona, 1947), Rosa
less pronouncedand no requirementfordarkness spp. (Von Abrams and Hand, 1956) and lettuce
to precedelightis evident.This difference
between (Harringtonand Thompson,1952; Koller, 1962).
the 2 types of fruitshould,however,be treated
The observeddifferences
betweenthe 2 types
withcaution,sincetheresultsin Table 3 are based of fruitmay be analyzed fromthe viewpointof
on a singlelimitedexperiment,whichwas more- the role which each plays in the successfulexisover carriedout at a much later date than the tenceof the speciesin theextremeenvironment
of
experimentssummarizedin Tables 1 and 2. It the desert.It would seem that whereasthe aerial
must also be rememberedthat the subterranean fruitsfunctionmainlyin increasingthe distribufruitsare less light-sensitive
at the highertem- tion of the species withinits habitat,the subterperaturesthan the aerial fruits.The ecological raneanfruitsservemainlyin ensuringits survival.
January,1964]
KOLLER
AND ROTH-AMPHICARPY
IN GYMNARRHENA
induction.Austral.Jour.
to photoperiodic
sensitivity
The formerare formedin habitats or years with
Biol. Sci. 13: 123-131.
favorable rainfall. Their germinationis more
and since GEIGER, R. 1959. The climatenear the ground.Harstrictlyinfluencedby the environment,
vard U. Press,Cambridge,Mass. 494 p.
theygerminateon the soil-surfaceand only after
1938. Photoperiodism
HAMNER, K. C., AND J. BONNER.
some delay, relative to the subterraneanfruits,
in relationto hormonesas factorsin floralinitiation
a favorablecombinationof environmental
factors
Bot. Gaz. 100: 388-431.
and development.
is a prerequisitefortheirformationas well as for HARRINGTON, J. F., AND R. C. THOMPSON. 1952. Effect
theirsubsequentgerminationand establishment.
of varietyand area of productionon subsequent
This fitsin well withthe relativelylow tolerance
germinationof lettuce seed at high temperatures.
Proc.Amer.Soc. Hort.Sci. 59: 445-450.
whichtheirseedlingsexhibittowardsunfavorable
soil-moistureregimes. The subterraneanifruits ISIKAWA, S., T. Fujii, AND Y. YOKOHAMA. 1961. Photoseeds.
ofEragrostis
periodiccontrolofthegermination
are formedin relativelysmall numbersper plant,
Bot. Mag. Tokyo74: 14-18.
but at the same time theyare a verysafe investD. A. 1940. Plant microtechnique.Mcment. They are formedeven with unfavorable JOHANSEN,
Graw-Hill,New York.
soil-moisturesupply. They start to germinate KADMAN-ZAHAvI, A. 1955. Noteson thegermination
of
relativ7ely
soon afterimbibition,and theirgermirosea.Bull. Res. CouncilIsrael4: 375-378.
Atriplex
nation is relativelyless sensitiveto variationsin KOLLER, D. 1957. Germination-regulatinlg
mechanisms
All thesecharacteristics
the environment.
tend to
Kar.
in some desert seeds. IV. A triplexdimorphostegia
et Kir. Ecology38: 1-13.
increase the probabilitiesfor germinationand
in lettuce
ofgermination
1962. Preconditioning
completion of the life cycle. They germinate
Amer.Jour.Bot. 49: 841-844.
at timeoffruitripening.
exactly where the conditionswhich sufficedfor
theirparentto completetheirlife-cycleare most LEvITT, J. 1956. The hardinessof plants. Academic
Press,New York.
likely to be duplicated. In addition,it has been
dellecondizioniambientali,
LONA, F. 1947. L'influenza
suggested(0. Stockerand M. Evenari, personal
del seme
sulla caratteristiche
durantel'embriogenesi,
communications)that this location is specially
e della pianta che ne deriva.Lavori Bot. (G. Gola
favoredby the fact that the undergroundtissues
JubileeVol.,Padova, Italy): 277-316.
of the motherplant, and the cavity left in the NEGBI, M., AND MI. EVENARI. 1961. The means of
soil by their shrinkage,may serve as vertical
survivalof some desertsummerannuals. AridZone
in arid and
Research.XVI. Plant-water
relationships
conduits for deeper penetrationof rain wvater.
Proc. MadridSymp.UNESCO,
semi-aridconditions.
Paris.p. 249-259.
POSNER, H. B., AND W. S. HILLMAN. 1962. Aseptic
of seeds of
BEADLE, N. C. W. 1952. Studieson halophytes.
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I. The
germination
ofseedsand establishment
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Lemnaperpusilla6746. Physiol.Plantarum15: 700in Australia.Ecology33: 49-62.
fivespeciesofAtriplex
708.
BECKER, H. 1913. Uber die Keimungversehiedenarti-SHULL, C. A. 1911. The 02 ininimum and the germinagenFrQlchte
und Samen bei derselbenSpecies.Beih.
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Bot. Zentralb.29: 21-143.
VON ABRAMS, G. J., AND M. E. HAND. 1956. Seed
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LITERATURE
CITED