Factors Controlling the Germination Date of Winter Annuals Author(s): E. I. Newman Reviewed work(s): Source: Journal of Ecology, Vol.

51, No. 3 (Nov., 1963), pp. 625-638 Published by: British Ecological Society Stable URL: http://www.jstor.org/stable/2257751 . Accessed: 25/02/2012 19:07
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625

FACTORS

CONTROLLING THE GERMINATION WINTER ANNUALS

BY E. I. NEWMAN Botany School,Cambridge* INTRODUCTION

DATE

OF

A winter annual is a plant whichgerminates the autumn,passes the winter the in in vegetative state,and flowers, seed and dies in thefollowing sets spring summer. or Thus the seeds are normally liberated late springor summer, theydo not germinate in but untilthe autumn.This paper is concerned withthereasonsforthisfailure germinate to in the summer, and withthe factors controlling precisedate of germination the the in autumn. Severalworkers have conducted laboratory experiments thegermination winter on of annualspecies, often though without particular any interest thegermination natural in in In conditions. mostspeciesinvestigated thereis a changein ability germinate the to as seed ages: aftera period of storagethe seeds give a higher total germination and/ora faster ratethando fresh seedsunderthesame conditions. mostspeciesthischangein In germination abilityis related to physiologicalchanges in the seed (after-ripening), but in some Leguminosae is due to the softening a hard seed coat. In some species it of the germination at ability some germination temperatures changesmorethanat others, so thatas a result after-ripening of a change(alwaysa rise)occursin theoptimum and/or themaximum for temperature germination. willbe referred as changein temperaThis to tureresponse withstorage. can be illustrated thegermination thedarkofBromus It by in tectorum (data fromHulbert1955). The total germination freshseed at 100 C was of 53 %, at 20? C 1%; after weeks'storage 7 germination about 95 % at either was temperabut at ture, faster 20? C. Amongthe specieswhichhave been studied, fivesortsof changewithstoragecan be distinguished. 1. In thefollowing speciesgermination fresh of seedsis low becauseofhardseedcoats: T. T. Trifolium glomeratum, procumbens T. campestre), reflexum, resupinatum, (= T. T. subterraneum (Toole & Hollowell 1939); T. hirtum, incarnatum T. (Williams& Elliott 1960); Lupinusdigitatus, Medicago tribuloides (Quinlivan1961). Some of thesespecies also showafter-ripening 2 changes (see section below,where conclusions Trifolium the on spp. are based on experiments withscarified naturally or softened seed). For severalof thesehard-seeded of speciesit has been shownthat softening the testais hastenedby and highconstant temperatures, evenmorebydailyalternations highand low temperof ature(LoftusHills 1942; Williams& Elliott1960; Quinlivan1961). 2. The following with speciesshowa changeintemperature response storage: Lepidium lasiocarpum (Barton1936); Trifolium glomeratum, reflexum, resupinatum T. T. (Toole & Hollowell 1939); T. subterraneum (Loftus Hills 1942, 1944); Bromusbrizaeformis, B. japonicus,B. tectorum Anisantha (= tectorum) (Hulbert1955); Arabidopsis thaliana. Draba muralis, verna Erophila (Ratcliffe 1957).
*

Present address: Department Botany, of University College Wales, of Aberystwyth.

626

Germination winter of annuals

3. In the following species storageproducesan increaseof germination abilityof approximately the same amount in all germination temperatures: Daucus pusillus, Plantagofastigiata,Streptanthus arizonicus(Barton 1936). Any hard-seededspecies (section1) whichdo not showafter-ripening also be placed in thisgroup. could 4. The following speciesshow an increaseof germination ability withstorage, but it is not knownwhether thereis a changein temperature response, since onlyone temperature was used: Holosteum umbellatum, perfoliatum (Ebner 1924); Arenaria Thlaspi serpyllifolia, Cardaminehirsuta, Hornungia petraea, Saxifraga tridactylites, Veronica arvensis (Ratcliffe 1957,1961). 5. One of the winter annual races of Arabidopsis thalianastudiedby Laibach (1951) showedno changein germination ability with storage;twoother racesdid showa change, as did therace studied Ratcliffe section by (see 2). These results suggest three explanations germination for occurring theautumn, in but notintheprevious spring summer. or 1. In some speciesfreshseed gives littleor no germination underany temperature condition;but by autumn,owingto after-ripening and/orsoftening the seed coat, of can germination occurin a widerangeoftemperatures. fresh seedgivesgermination at temperatures 2. In somespecies only belowthoseoccurin and summer. after-ripening ringin thefield late spring As proceeds, optimum the and maximum temperatures germination for rise,untiltheyoverlapthose occurring the in field. 3. In specieswherethere no changein germination is withstorage, field the temperain are tures summer above themaximum optimum germination. lowertemperor for The This explanation offered Went and his coaturesin autumnallow germination. is by for of of workers thecontrol germination winter-germinating annualsin theCalifornian desert(Went 1948, 1949; Went & Westergaard Went & Phillips1956). 1949; Juhren, withstorage. Theydid notinvestigate changein germination ability tentative most cases, sincefewworkers in Explanations2 and 3 mustbe somewhat records from naturalhabitats. the Toole & Hollowell(1939) providea givetemperature soil but temtable of dailymaximum temperatures, giveno reasonwhythe maximum thanthe minimum the mean. Resultspresented shouldbe moresignificant or perature for and laterin thispapersuggest that, somespeciesat anyrate,theminimum meanarein than the maximum. Ratcliffe factmoreimportant (1957, 1961) and Went and his coand minimum temperatures. air workers give graphsof maximum They are the only in whohavebeeninterested theprecise date ofgermination, theonlyonesto and workers in conditions. giveanydata on germination natural in soil moisture be of primary to considers Ratcliffe importance controlling germinaand to between tiondate. However,his attempts showa direct relationship germination in inconclusive. Field observations Went and his soil moisture the fieldare largely by in dateofgermination showthat thedesert, where rainis spasmodic, precise the co-workers a come.The amountofrainoccurring in winter dependson whentherainshowers during the particularshowerinfluences amount of germination (this is confirmed Tevis by minimum thatforeach speciesthere a certain is rainfall 1958).Thereis evidence required will before germination occur. any

E. I. NEWMAN GERMINATION OF AIRA PRAECOX AND TEESDALIA NUDICAULIS

627

withthe germination two speciesof winter of of The remainder thispaper is concerned their germination (L.) AirapraecoxL. and Teesdalianudicaulis R. Br. It describes annual, on Heath,westSuffolk. habitat Thetford and temperatures, also in a natural in controlled in I have shown(Newman1961)thatin boththesespeciesa smallvariation germination of size and seed production the matureplant. the affect subsequent date can markedly was therefore, to discoverhow muchthe mean geraim of thisresearch, The primary influence and conditions, whichfactors date variesfrom yearto yearin natural mination in date ofgermination anyyear. theprecise on by suggested previousworkto be important, This paperconcentrates the factors change in temperature for requirements germination, temperature namelydormancy, will be mentioned Otherfactors requirements. responsewithageing,and soil moisture and darkness light. between in differences germination briefly, including weremade,the soil is a coarse,flinty sand of In the habitatwherefieldobservations of content, especially subjectto rapidfluctuations moisture capacity, low water-holding wheremostof the seeds of Aira and Teesdaliaprobablylie. in the top fewmillimetres, withthe timeand equipment available,to make a recordof the It seemedimpossible, completeand accurateto be in layerwhichwould be sufficiently moisture this surface in of the Therefore approachhas beento study germination conditions continuous useful. and withfieldgermination and in regimes, by comparison moisture knowntemperature and of soil to importance temperature, moisture fieldtemperatures deduce the relative of in changes theresponse theseed.It has to be assumedthatthesearetheonlysignificant whichvaryas theyearproceeds. factors AIRA PRAECOX Details oftechnique the in heads werecollected 1958and 1959from same area, about 30 x 30 Ripe fruiting whichwerekeptin Theywerestoredin envelopes, m, on Foxhole Heath, westSuffolk. the laboratory usually 17-20?C), exceptfromNovember1958 to April (temperatures about 6-10? C in winter, rising werekeptin a glasshouse (temperatures 1959,whenthey to 10-20?C in April). weremade, Cladoniasylvatica Heath wherefieldobservations In the area of Thetford by mat coversabout 400% of the area, and is interspersed small patchesof Dicranum of and tussocks Higher plantcoveris sparse;it consists scattered scoparium bare ground. and Rumextenuifolius, of canina,A. tenuis of Festucaovina,and open growth Agrostis Aira occursin thelichen withAirapraecox and Teesdalianudicaulis. Although together growing and moss cover,it is muchmoreabundantin thebare patches.Since seedlings data presented all are hereare from plots on bare ground moreeasilyrecorded, thefield size on bare ground.To obtain areas of sufficient forthe plots, areas dominatedby In wereclearedofall vegetation. theseareasnumerous plots10x 25 cm Cladoniasylvatica weremarkedout. In 1958and 1959seedsweresownon theplotsin late August.In 1960 plantsgrownin themtheprevious no seeds weresown,but seeds fellon theplotsfrom in Aira plantsin the occurring year(thishad been prevented 1959). Each yearnaturally beforetheyset seed,in orderto prevent theirseed,whichmight wereremoved vicinity on thatsown,from from falling theplots.(The 'seed' of Aira is in fact differ genetically surrounded lemmaand palea.) fruit a one-seeded by

628

annuals of Germination winter

were made duringthe threeautumns 1958-60. At about Records of germination The in Airaseedling eachplotwas recorded. charts of intervals position every the 3-weekly in curves Fig. 1. progress thedata forthegermination thusmadeprovide and then of dry seed experiments was stored forvariouslengths time, In thelaboratory paper in Petridishes.The age of the seed whenplaced on moist put on to moistfilter filter paper is taken as the lengthof timesince collection.Table 1 showsthe dates at seed paper,and the corresponding ages. The filter whichseed was put on to moistfilter waterwas added and waterat thestart, moredistilled withdistilled paperwas saturated Each dishwas covered the to if at each recording, necessary, return paperto saturation. loss. bag in a with lid and enclosed a polythene to reducewater in in used The temperatures were: 5, 10, 15,20 and 25? C constant; addition, August, The (about 12 h at each temperature). experiments 6-15? C and 16-25?C alternation in wereconducted bothdarkand light. in started Augustand October seed in had temperatures been available forfresh lightnor alternating Since neither near collected in was experiment conducted 1962,usingseed freshly June1959,a further were 10, 15 and wereused,and thetemperatures Both Aberystwyth. lightand darkness (16 and 20? C constant, 10-20?C alternation h at 100 C, 8 h at 20? C). dates Table 1. Aira praecox:seedage on various
Date when placedon moist filter paper 22 August 7 October
(1959) 19 June

collection) from Seedage (weeks Seed Seed collected collected

1959 1958
-

10 16

2I

59 65

exceptin the 6-15? C and 16-25?C in The lightused was continuous all experiments, temperature). withthehigher it where was on for12 h daily(coinciding alternations, in but seeds per treatment, in thosestarted June therewerefifty In mostexperiments were100pertreatment. 1959there Results conditions in Germination natural Heath in 3 years.In each on Fig. 1 showsthe germination bare groundon Thetford of to two oftheplotsare shown, givesomeindication therangeof variayeardata from as in the tionbetween plotsin thatyear.Germination each plotis expressed a percentage of not recorded, as a percentage theseedssown.During of of thetotalnumber seedlings Heath or neighwereobservedon any part of Thetford these3 yearsno Aira seedlings seed shedand late August. bouringheathsbetween at occurred about thesame timein 1958and 1960, The graphshowsthatgermination in earlier 1960; butin 1959it was about 7 weekslater.The succeeding perhapssomewhat of the the controlling timing germination with factors of sections thispaperareconcerned in observed these3 years. in temperatures Germination controlled in of of The progress germination seeds of fourages is shownin Fig. 2 (germination to Each ofthe fourgraphsrefers seeds of a in light)and Fig. 3 (germination darkness). day); each curveshowsthe paperon a particular age particular (i.e. put on to moistfilter

E. I.

NEWMAN

629

regime.Recordingwas normally in temperature of progress germination a particular to but no further germination, in order untilat least2 weekshad elapsedwith continued Whereno gerhas been omitted. finalperiodwithout change the simplify graphsthis the werecontinued at least 6 weeks,before experifor observations occurred, mination was abandoned. ment relatedto seed age, in The graphsshow differences the finaltotals of germination later. of and temperature lightor darkness.The importance these will be considered whichprimarily concernus. These will be it At themoment is the ratesof germination 22 seed (b, started first 10-week-old the to discussedwithreference Fig. 2, considering occurs the between seeds: all thegermination is August).At 50 C there greatuniformity thereis greatvariationbetweenthe seeds: a few during2 weeks.At 10? C, however, is othersin laterweeks,and germination still within14 days fromthe start, germinate 100
z

80

1958

0~

AUG.
6IG.

SEPT.

OCT.

NOV.

DEC.

JAN

FEB

in 1. Aira germination fieldplots.

continuous threetypesof germination: simultaneous, Salisbury (1929) distinguished as and discontinuous. fairly corresponds closelyto Abruptgermination, just defined, to and Salisbury'ssimultaneous germination, prolongedgermination his continuous. However,abruptand prolongedare not consideredas absolute terms:therecan be and intermediates betweenthem and prolongedness, different degreesof abruptness occur. at On the graphjust considered 10-week-old seed) thegermination 5? C is abrupt; (b, On at 6-15? C it is nearly abrupt;at 10, 15 and 16-25?C it is prolonged. thenextgraph the at seed) the germination 5? C is virtually same as before.However, (c, 16-week-old 20? there and at abrupt. C, at which germination IO' C has becomeabrupt, at 15?C nearly Withseed 59-65 weeks now no was formerly germination, givesprolonged germination. C and old,(d) 5, 10, 15,20 and 6-15? C all giveabruptgermination,251 givesprolonged, 16-25FC givesintermediate. Thus the seeds show a progressive changein temperature responsewithincreasing temgive higher onlylow temperatures abruptgermination, lengthof storage.Ast peri still and germination, higher none at all. As after-ripening progiveprolonged peratures Oncethegermination a in germination. and ceeds,higher higher give temperatures abrupt no becomesfully changein rateoccurs. abrupt, further temperature given

the a be on thegraph giving abrupt germination; germination (e.g. at 5? C), will called be germination. prolonged slope(e.g. at 10?C) will called gentle

to It in continuing the last periodof recording. will be convenient givenamesto these a confined a short to The germination two typesofbehaviour. period,giving steepslope

630

annuals of Germination winter

(Fig. in responseis shownwithgermination darkness The same trendin temperature in totalsof by is the darkness position complicated changes thefinal 3). In bothlightand whichare not always relatedto changesin rate. It will also be noticed germination, in betweenthe two lots of freshseed (the 1959 thereare differences germination that betweenseed populationsmerit Fig. and 1962 experiments, 3 (a, b)). Such differences investigation. further in changesin rate of germination relationto age and temperature Somewhatsimilar B. brizaeformis, japonicusand B. tectorum. have beenfoundbyHulbert(1955) in Bromus
100 8060 z 40 0 -

(a)

(b)

z
LU

20 -_
e

(9

C0
L

7 (C)

14

21 (d)

28

35

42

67

88

oL80-

6040 -~

20 0 7 14 21 28
DAYS

36

14

21

28

36

in variousseed ages,and of comparing curves Aira germination light, FIG. 2. Progress 10 23 seed (a) regimes. Started June, 0 daysold; (b) 22 August, weeks various temperature old; (c) 7 October,16 weeksold; (d) 59-65weeksold. 50 C (o), 100 C ([), 15? C (x),
200 C (+), 250 C (A), 6-150 C (A), 16-250 C (A).

moistened seeds of Effect redrying just behaviour of the In orderto understand ecologicalsignificance the germination for moisture gerthe continuous to it described, is necessary knowwhether seedsrequire out in a glasshousein February this An investigating was carried mination. experiment paper Seeds wereplaced on damp filter 1960,usingseed collectedthe previousspring. dishes2, from 6 seedsin each dish.After daystheseedswereremoved in fourdishes, fifty After lengths Petridishesin thelaboratory. varying uncovered 3 and 4 and placed in dry, to paper. The seeds in dish 1 were moist of timethe seeds were returned damp filter was Germination recorded daily. throughout. was In everydish the finalgermination over 90 %. Table 2 showsthe lengthof time in to frommoistening 500% germination; the case of the redriedseeds this means the the timefrom secondmoistening. somewhat after remoistening It appearsthattheseed whichwas driedout germinated and moist seed.Thisrequires confirmation, thematter thanthecontinuously morequickly to at It further. is moreimportant themoment notethat11 h drying is beinginvestigated the to (equivalent one dryday in the field)is enoughto return seed almostto the state

E. I. NEWMAN

631

almostas longin moistconditions ifit had as it was in before moistening; it requires i.e. neverbeenpreviously wetted. other In or moisture words,continuous almostcontinuous for is required germination.
100
80 6040200
z
Z

(a)(b

. 20 I -7 14 22 (c)

I
0 7 14 23 28 35

0lOC

80

t9 60
z 40 -

~~~~/

u20
o 0
100

/
7

X 14 21 28 35 42 53
2

80
60 -

(d)

(e)

40 20 0 7 14 21 28 0

FIG. 3. Progress curves Airagermination darkness, of in seedages,and comparing various various temperature regimes. 19 June1959, 3 days old; (b) 23 June1962, 0 days old; (a) 50 C: no data; (c) 22 August, weeks 16 10 old; (d) 7 October, weeksold; (e) 59-65weeks old. 50 C (O), 100 C (O), 150 C ( x), 200 C (+), 6-150 C (e), 10-200C (a), 16-250C;(A).

DAYS

14

21

on Table 2. Aira praecox: effect rateofgermimoistened seeds nationof redrying

Dish No.
1 2 3 4

Periodofdrying (h)
11 24 48

50 % germination

Timeto reach (days)

10-5 9-2 9-4 9-6

Fieldtemperatures to it observedin the field, is necessary knowthe In orderto explainthe germination the and whichthe seeds wereexperiencing temperatures during summer autumn.Maxiwereplaced withtheirbulbs lyinghorizontally mumand minimum thermometers just

632

Germination winter of annuals

of below thesurface bare soil on Thetford Heath; thecentre thebulb was at about 5 of mm depth.Readingsweretakenapproximately weekly from June October1959,and to 5 the less frequently throughout following months.The figures givenby Newman are are withtheabsolutemaximum minimum tempera(1961),where they compared and air turesforthesame periods, recorded Elveden,less thana mileaway.This comparison at in showsthatthemaximum temperatures thesoil wereup to 15? C above thoseoftheair declinedduring the but during summer, thedifference September October,and was and small fromearly Novemberto late March. The minimum temperatures were about in 1-4? C higher thesoilthanin theairthroughout. data are not suitablefordirectuse, forseveralreasons.Weekly The soil temperature of whichwilloccurmainly readings pick out the days and nights extreme conditions, in In when the soil will be dry,and the seeds unable to germinate. clear, dryweather, whenreadings and of in werebeing addition, thesummer autumn 1959, the taken, weather are warmand dry.The soil temperatures onlydirectly was exceptionally relevant while meansof dailymaximum minimum Table 3. Monthly and air temperatures Elveden at (?C)
Maximum
1958 1959 1960 1958

Minimum
1959 1960

May June July August September October November

16-5 18-0 20-5 20-5 19-0 14-0 8-5

17-0 21-0 24-0 23-5 21-0 17-0 95

18-0 21-0 19-0 20-0 17-0 13-5 10-0

70 10-0 12-5 12-5 11-5 7.5 40

6-5 95 12-0 12-5 8-5 7.5 2-5

8-0 11-0 12-0 11-0 9.5 7.5 5-5

moist.This will only happen,in summerand early autumn, the soil is continuously is the whenthe weather predominantly cloudy.Under such conditions soil and air will be at about the same temperature. Duringsunnyspells,ifthe soil remainsmoistat the of it surface, evaporation waterwill reduceheatingof the surfacelayers.Therefore is as to proposedto taketheairtemperatures approximations thesoil temperatures, though becomerather warmer thanthe air in the bearingin mindthatthe soil maysometimes and air are Means ofmaximum minimum temperatures given Table 3. in day-time. in field Control germination the of the in and autumnin This sectionwillconsider germination each partof the summer whichmostcloselyapproximate the fieldtemperatures to at thecontrolled temperatures will sincetheseare thattime.Data from alternating temperatures be usedwhere possible, but sincethe data from to moresimilar the fieldtemperature temregimes; alternating those constant will are peratures insufficient, from temperatures have to be used as well. It willbe seenfrom Figs. 2 and 3 thattheratein a given alternating temperature usually which the or liesneartherateintheconstant temperature equals either minimum themean in For ofthealternation. example, Fig.2 (b, 10-week-old is seed)the6-15? C curve similar to the 50 C, and the 16-25?C to the 15? C. (However,thefinaltotalof germination is than often in higher alternating temperatures in any constant temperature.) Thus,when and when no data are available froma relevant rates of germination, considering the data nearest minimum the and alternating temperature, from constant temperatures will meanfield temperatures be used.

E. I.

NEWMAN

633

considerwhether not some germination or We shall first would be expectedat the in -temperature s occurring thefield. the In June,whenthe seeds are first liberated, fieldtemperatures approximate a to In 10-20?C alternation. Junein the controlledconditionsthe 1962 seed gave some in germination this temperature regimein the dark, but not in light.It is doubtful in the whether 1959seed would have givenanygermination thisregime. are In Augustthe fieldtemperatures usuallysomewhathigher:15? C constantand are controlled conditions. bothof thesesome In 16-25?C alternation the mostrelevant occurred, darkness in light. in and germination in in would allow somegermination August, Thus thetemperatures thefield and prowhichprevents effect temperature of bablyin June.It cannotbe the direct germination wouldbe expected whatratesofgermination the We during summer. mustnow consider at thetemperatures in occurring thefield. In at no will In June 10-20?C alternation germination occurin light. darkness germinso ationtakesmorethan2 weeksto commence; it will onlyoccurin the fieldif thereis moisture. morethan2 weeksofcontinuous in In August 15? C and 16-25?C give prolongedgermination both dark and light. showthatalthough weeksofcontinuous 2 in The ratesofgermination thesetemperatures couldgive10 or 20 % germination, 6 weekscouldnotgivemore in even moisture thefield and Augustifthere continucan Thus germination onlytakeplace during is June, July thismustbe an uncommon for ous soil moisture severalweeks.Although occurrence at cool thistimeof yearon thesesoils,periodssufficiently and wetto allow some germination mightbe expectedto occur in some summers.However,germination will be sincethe rates of germination so slow. Comparison are limitedto a smallpercentage, ofFigs.2 and 3 showsthattheratesand totalsin therelevant are temperatures somewhat The germination buriedseedis thusfavoured, of in higher thedarkthanin thelight. and to continuous it is buriedseed whichis morelikely experience moisture thenecessary for of lengthof time.Fig. 1 showsthatin 1960 a smallpercentage germination occur did and thiswas presumably to theparticularly weather due cool during August, that during month. conditionsallow only prolongedgerIn August,as we have seen, the temperature have fallen,and the seeds have aftermination.By early October the temperatures are ripenedfurther. C and 6-15? C alternation now the relevant 10? regimes. data No in are available on the germination 6-15? C in October(16-week-old seed), but we can assume that the curvewould lie betweenthe 6-15? C curvesfor 10- and 59-week-old seed. Thus we see thatby Octoberboth 10? C and 6-15? C giveabruptgermination, in in both darkand light, within weeks. 2 resulting a highpercentage germination is As Thus thegeneral picture as follows. thesummer proceedstheseeds' responseto at temperature changes,so that the maximum temperature whichabruptgermination can occurgradually the rises;but up to earlySeptember field temperatures remain high enoughto allow onlyprolonged and earlyOctoberthe germination. DuringSeptember fallin temperature the continued and changeof the seeds' temperature responseallows i.e. moreabruptgermination; theperiodof continuous progressively moisture required becomesprogressively fora highpercentage shorter. thistimetheperiods At germination moistare probably forwhichthesoil does remain And it continuously becoming longer. is in factduringSeptember and Octoberthatmostof the germination occurred the in of in field 1958and 1960.Hencethetiming germination thefield be attributed an in can to
than 20 or 30 %.

634

annuals of Germination winter

temperature and temperature, thechanging soil factors, moisture, of interaction thethree of response theseeds. mainly have of the In thisexplanation effects seed age and temperature beenconsidered It totalofgermination. was thanto thefinal rather to in relation therateofgermination in occurring possiblein the temperatures shownearlierthat the totals of germination in in Juneand Augustdo notexplaintheusual absenceofgermination thefield summer. the could affect date of changesin total germination We mustconsidernow whether of percentage seeds do notgerminin germination theautumn:it could be thata certain later.Considering in ate underfieldconditions October,but becomeable to germinate 5, again Figs. 2 and 3, it willbe seenthatin Octoberin light, 10 and 15? C all givemore was temperatures much at the In than90 % germination. darkness germination constant have givennearly1000%germination, would presumably lower;but 6-15? C alternation it sinceit did so withseed bothnewerand older(10 and 59 weeksold). Therefore seems in whichgive abruptgermination Octoberalso probablethatthose fieldtemperatures through is so give hightotal germination, thatno delay of germination to be expected low totalsofgermination. and soil factors as In mostyears, in 1958and 1960,thethree temperature, moisture the some timein September, tendto converge responseof the seed willprobably changing unusual: although day temperatures to rapidgermination begin.1959is clearly allowing it highin thatautumn, was cool enoughby earlyOctoberforrapid wereexceptionally occurredin the fielduntilNovember.The to germination occur. Yet no germination reason for this musthave been the exceptionaldroughtof that autumn; between14 on rain occurred 21 prolonged Augustand 16 Octoberonly2 mmof rainfell.The first did perhapsbecause the October.Even afterthis germination not take place rapidly, occurs. the germination were temperatures bythenbelowthoseat which fastest in date yearscouldbe causedbyvariation any in Smallvariations germination between But and soil factors temperature, moisture rateofafter-ripening. because one ofthethree to likely it to factors converge, seemsthattheonlycondition of ofthetendency all three in suchas occurred 1959. date in difference germination is drought, marked cause a very on can It is not knownhow muchtherateof after-ripening vary.The effect it of condiis the tionsduring summer beinginvestigated. TEESDALIA NUDICA ULIS to similar thoseused forAira,and need not used forTeesdaliawerevery The techniques be described. Heath in 3 yearsis shownin Fig. 4. It will on plotson Thetford The germination field to dates in the3 yearsis similar Aira: the between germination be seenthattherelation in earlier 1960; muchlaterin i.e. about the same in 1958 and 1960,or perhapsslightly thanAira. earlier 1959.In each yearTeesdaliagerminated to effect thaton Aira. Teesdaliaseedshas a similar of Redrying moistened in of temperatures thedark.The Fig. 5 showsthegermination Teesdaliain controlled in wereconducted 1959. It willbe seen The experiments in germination lightis similar. occur,and their typesof germination that,as withAira,boththeabruptand prolonged and to relation temperature seed age is muchthe same as forAira. Thereare, however, proceeds more rapidlyin Teesdalia. after-ripening differences. Firstly, two important whereaswithAira 15? C abruptgermination, For instance, August15? C givesfully by at at evenin October.Secondly, anytemperature does not givefully abruptgermination

E. I. NEWMAN

635

whichgermination abrupt,it occursabout twiceas fastwithTeesdaliaas withAira. is Boththesedifferences tendto makeTeesdaliagerminate will earlier thanAirain thefield. The germination Teesdaliain controlled of to temtemperatures approximating field peratures nowbe considered. June field will In the to temperatures approximate a 10-20?C
100

z60

1959

~40

/
. 15 1
SEPT.

<20 Z 100

~~~~~~~z

so
1

AUG.

15

1 5 13

OCT.

NOV.

15

D EC.

15

JAN

15

FIG. 4. Teesdalia germination field in plots.

(a)

80

(b)

X-X

60~~~~~~~~~~~~~
60 40
z

p
4 7 14 21 28 35 42 74

20 0 6 3 26o0

z 100

so ELLJ

15?C Q~~~~~~~~~~~~
-(C)0-

(x),

20?C

(+),

25?C

(A),

6-15?C

(-),

16-(d)

60 +-A
40-

20 20

~~
4 O7

~
14

~
3510

~
28

~ ~~/+
DAYS

+~

14

20

28

35

41

FIG. 5. Progress of in various seedages, curves Teesdalia germination darkness, comparing and varioustemperature 20 seed 4 weeksold; (b) 22 August regimes. Started June, (a) 19 13 weeksold; (c) 8 October, weeksold; (d) 62-68 weeksold. 50 C (0), 100C () 150C ( x), 200C (-I), 250C (A), 6-150C (@), 16-250 (A&). C

in C alternation. On 11 June 1962, 2-day-old seed was put to germinate 10-20O in as Therewas no germination any of alternation, wellas in 10, 15 and 200 C constant. between theseconditions, either in darkness light. or Thereappearsto be a discrepancy this resultand the resultsfor 4-week-oldseed startedin June 1959 (Fig. 5a). The difference be due to the 1962 seed beingfresher. the basis of the 1959 results, On may at the possibility cannotbe excludedthatin late Junetherecould be some germination moisture would probably fieldtemperatures, thoughmorethan a week of continuous

636

Germination winter of annuals

were seen on Foxhole Heath on 13 July be required.In factthreeTeesdaliaseedlings out scratched by a rabbit(wherethe soil would perhapshave a 1960,in a depression moistthanon thenormalsoil surface). chanceofremaining greater to regimes consider. temperature In August,150 C and 16-25?C are the controlled in the between germination thesetworegimes. difference Unfortunately is a marked there and abrupt,but at 16-25?C it is stillprolonged, is At 15? C germination alreadyfully total and steepercurve,thoughnot fully thetotallow. (In light16-25?C givesa higher length by is complicated thefactthatwithincreasing abrupt.)The interpretationfurther at of storageafter13 weeks,the rateof germination 10? C actuallygetsslower,though comgermination is (i.e. any changein abruptness there a longerperiodbefore without (Boththese the mences, thecurveis stillas steep);whereas ratein 6-15? C increases. but not It changesare shownin lightas wellas in darkness.) is therefore clearwhatratesof how theywill changesubseare germination to be expectedin the fieldin August,.nor of on The mostusefulinformation thiscomes fromthe germination seeds on quently.
100 o80
z
E 60

/
-

z w

0 40

~20
00

7
DAYS

14

22 (n) in germination glasshouse. light,(m) dark,started August;(o) FIG. 6. Teesdalia

8 light, dark,started October. (@)

similar was fairly regime the in glasshouse which temperature filter paperin an unheated thatfairly rapidgermito thatofthesoil. The results, whichare shownin Fig. 6, suggest is in the though totalgermination darkness significantly in nation be expected August, can and owingto thefallin temperatures the (P<0 001). By October, lowerthanthatin light has and of response theseed,therateof germination increased, thetotalin the changing darkhas risen (P<0-01). significantly from of We can see from thatthefaster this after-ripeningTeesdalialeadsto a difference rapidgermination date. SinceTeesdaliacan givefairly of Airain thecontrol germination a which occur,it willrequire commonly to a hightotalin late Augustin thetemperatures at than Aira for germination thattime. much shorter period of continuousmoisture did And in fact in 1960 some germination occur in the fieldin August (see Fig. 4). between Augustand October, there some changein therateof germination is Although of will thanthatin Aira.So thetiming germination be thechangeis ofa muchlesserorder of as length, the autumnprogresses, the periodsof on mainlydependent the increasing will part. soil and temperature after-ripening play a smaller continuous moisture; Teesdaliaand Aira: in Augustthetotal germinabetween Thereis another difference lowerin thedarkthanin thelight. tionof Teesdaliaat mosttemperatures significantly is on of This willtendto favour germination theseeds lying the surface;but theseare the than buried seeds, so this reductionof less likelyto experience continuousmoisture the during summer. in germination thedarkmaytendto reduceoverallgermination

E. I.

NEWMAN

637

DISCUSSION This paperhas shownthatin seedsofAirapraecoxand Teesdalianudicaulis temperathe because of tureresponsechangesin a characteristic as the seed ages, presumably way In of in by after-ripening. Aira the timing germination the fieldis normally controlled an interaction soil moisture, of response. temperature this changing and temperature in In Teesdaliathe temperature responsein Juneand July will make germination these and nevermorethan a smallpercentage; monthsuncommon, but owingto the faster the by after-ripening, date of the main autumngermination be less affected temwill and rate of after-ripening in Aira, and will therefore relatively than more perature be It be affected soilmoisture. might expected from thatTeesdalia this by wouldshowgreater from variation yearto yearin thetiming germination; field of the data are notadequate this. to confirm I As mentioned in earlier, have shown(Newman1961)thata smalldifference germinaaffect subsequentsize and seed productionof the plant: the tion date can markedly the the thelaterthegermination, smaller plantand thelowertheseed production. Thus, selection other wouldbe expected favour to germination. things beingequal,natural early the the will However, earlier germination, greater riskthattheseedlings be killed the the byan autumn drought. it a When Teesdaliagerminates sendsdown a robustroot whichcan penetrate centiAira, on metreor more whilethe above-ground partsconsistonly of two cotyledons. in This difference the the otherhand, sends down onlya fewshort, fineroots at first. amountof rootproduction to size oftheAira seed. Sincethe maybe related thesmaller Teesdaliaseedling has a deeperroot,it is probablymoredrought-resistant (thoughthis If has not been testedexperimentally). so, selection the may have favoured somewhat earlier germination Teesdaliacompared of with Aira. The germination which bothspeciescan giveinAugustis ofinterest thisconnection. in These earlyplantshave a highchanceof beingkilledby autumndrought, iftheydo but survive gamble' they producea very largenumber seeds.Thus it maybe a 'worthwhile of imforthe speciesif some of the seeds germinate a cool, moistAugust.It is clearly in thatonlya smallpercentage seeds shouldgerminate August,so thatifall of in portant theseearlyseedlings thereare stillplenty seeds leftto germinate theautumn. die of in Aira appearsto have a morereliable onlya small mechanism thanTeesdaliaforensuring in percentage germination August. in Salisbury (1929)states thatall theviableseedsofRanunculusparviflorus germinate the September following shedding, withina period of about a fortnight. comments: He 'This speciesis a typicalexampleof a "winter germination, annual" withsimultaneous and this latterfeature may constitutes definite a dangersince almostall the seedlings be destroyed the same adversecondition.'However,it could be said for Aira and by Teesdalia(and it may be trueforotherwinter annual speciesas well) thattheyexhibit boththe continuous and simultaneous typesof germination, getthe advantagesof and both. ACKNOWLEDGMENTS I wishto thankDr A. S. Watt forvaluable advice duringthe course of thisresearch. Most of the research was performed whileI was the holder of a Nature Conservancy ResearchStudentship; am grateful the Nature Conservancy this support, I and to for fortheuse ofThetford HeathNatureReserve.

638

Germination winter of annuals SUMMARY

Previouswork on the germination winter of annuals has suggested thatthe timingof germination variousspeciesis controlled dormancy, in by changesin the temperature responseof the seed withageing,temperature, moisture, some combination soil or of -these. This paper attempts account for the precisetimingof germination Aira to in praecoxand Teesdalianudicaulis. Recordsofgermination natural in conditions given, are and by comparisonwithgermination controlled in temperatures is shownthat the it germination Airais normally of controlled an interaction soil moisture, by of temperature and thechanging temperature response theseed. In Teesdalia, of becauseoffaster change in temperature response, moisture soil playsa relatively moreimportant role. REFERENCES
Barton, V. (1936).Germination somedesert L. of seeds. Contrib. BoyceThompson 8, 7-11. Inst. Ebner, (1924).Keimungsphysiologie Draba verna, H. von Holosteum umbellatum und Thlaspiperfoliatum, Veronica hederifolia. Ost.bot.Z. 73, 23-41. Hulbert, C. (1955). Ecologicalstudies Bromus L. of tectorum otherannualbromegrasses. and Ecol. Monogr. 181-213. 25, Juhren, Went, W. & Phillips, (1956).Ecology desert M., F. E. of plants. Combined andlaboratory field IV. work thegermination annuals theJoshua on of in California. Ecology, TreeNationalMonument, 37,318-30. Laibach,F. (1951). Ober sommer- winterannuelle und Rassen von Arabidopsis thaliana (L.) Heynh. zur der Ein Beitrag Atiologie Blutenbildung. Beitr. Biol.Pfl.28, 173-210. Loftus Hills,K. (1942).Dormancy hardseededness T. subterraneum. effect time harvest and in I. The of of andofcertain storage seed conditions.J. Coun. Industr. Aust. 275-84. Sci. Res. 15, Loftus Hills, (1944).Dormancy hardseedednessT. subterraneum. progress after-harvest K. and in II.The of ripening.J. Coun.Sci. Industr. Aust.17,186-90. Res. Newman, I. (1961).Population E. Studies Winter on Annuals the in Breckland. Ph.D. thesis, Cambridge. Quinlivan, J. (1961).The effect constant fluctuating B. of of and temperatures thepermeability the on hardseedsofsomelegume species. Aust. Agric. J. Res.12,1009-22. Ratcliffe, (1957).TheAutecology someAnnuals theDerbyshire D. of of Limestone. Ph.D. thesis, Sheffield. Ratcliffe, (1961).Adaptation habitat a group annual D. to in of plants. J.Ecol.49, 187-203. Salisbury, J.(1929).The biological E. equipment species relation competition. Ecol. 17,197of in to J. 222. a Tevis,L., Jr.(1958). Germination growth ephemerals and of induced sprinkling sandydesert. by Ecology, 681-8. 39, of Toole,E. H. & Hollowell, A. (1939).Effect different E. of temperatures thegermination several on winter annualspecies Trifolium. Amer. of J. Soc. Agron. 604-19. 31, TreeNational Went, W. (1948).Ecology desert F. of plants. Observations germinationtheJoshua I. in on Monument, California. Ecology, 29,242-53. on F. of of and Went, W. (1949).Ecology desert plants.II. The effect rainand temperature germination growth.Ecology, 1-13. 30, of F. Went, W. & Westergaard, (1949). Ecologyof desert M. plants.III. Development plantsin the Death Valley NationalMonument, California. Ecology, 26-38. 30, to W. of Williams, A. & Elliott, R. (1960).Ecologicalsignificance seedcoat impermeabilitymoisture J. incrimson, subterranean roseclovers i Mediterranean-type and in climate. Ecology, 733-42. 41,

1962) (Received27 November