A phenological scale for the development of Gladiolus

Annals of Applied Biology ISSN 0003-4746

RESEA RCH A RTI CLE

A pheno log ical scale f o r t he developm ent of Glad io lusN.T. Schwab, N.A. Streck, C.C. Becker, J.A. Langner, L.O. Uhlmann & B.S.M.R. Ribeiro

Departamento de Fitotecnia, Centro de Ciências Rurais, Universidade Federal de Santa Maria (UFSM), Av. Roraima 1000, 97105-900 Santa Maria, RS, Brazil

Keyw ordsdevelopmental scale; developmental stages;floriculture; Gladiolus × grandiflorus;morphological criteria; phenology.

CorrespondenceN.A. Streck, Departamento de Fitotecnia, Centrode Ciências Rurais, Universidade Federal de SantaMaria (UFSM), Av. Roraima 1000, 97105-900,Santa Maria, RS, Brazil. Email:[email protected],[email protected]

Received: 20 January 2014; revised versionaccepted: 17 December 2014; published online:5 February 2015.

doi:10.1111/aab.12198

Abst ract

A staging system for developmen t of gladiola (Gladiolus × grandiflorus) that relieson simple, visual, non -destructive criteria is proposed. Four field trials wereconducted during the spring 2010, autumn/win ter 2011 and win ter 2011 atSan ta Maria, RS, Brazil, with differen t gladiola cu ltivars, in order to observethe developm en tal stages of the above-ground parts and their dry m atter. Thedevelopmen tal cycle, wh ich starts at dorm an t corm and ends with plan t senes-cence, is divided in to four developmen tal phases: dormancy phase, sprou tingphase (from filiform roots appearance to sheaths appearance), vegetative phase(from em ergence of the first leaf tip to emergence of the final leaf tip on thestem ) and reproductive phase (from heading to plan t senescence). The develop-men tal stages that were iden tified during the dormancy phase and during thesprou ting phases are coded as S stages: S0 = dorman t corm, S1 = appearance ofroots, S2.1 = first sheath , S2.2 = second sheath and S2.3 = th ird sheath . Vegeta-tive phase is coded as V stages: VE = emergence of the sheaths above ground,V1 = first leaf, V2 = second leaf, Vn = nth leaf and VF = flag leaf. Leaf tip is themarker for V1 –VF. The developmen tal stages du ring the reproductive phasesare coded as R stages: R1 = heading, R2 = blooming, R3 = onset of flowering,R4 = end of anthesis, R5 = end of florets senescence and R6 = plan t senescence(leaves and floret axis are brown). Sub-stages have also been assigned betweenR1 and R2 and between R3 and R4. Illu strations (photographs) of each develop-men tal stage taken from field pot-grown plan ts are provided and the proposedscale was tested with field observations. These criteria are straigh t forward andallow for qu ick determination of developmen t stage. Th is system can be usedby both farmers and for experimen tal trials.

Int roduct ion

Gladiola (also gladiolus) or sword lily (Gladiolus × gran-diflorus Hort.), Iridaceae fam ily, is an importan t cu t flowerpropagated from corms. Gladiolus is considered the genuswith in the largest known num ber of species of thepetaloid monocots, occu rring natu rally main ly in theMediterranean and Sou thern Africa regions, where thereare more than 100 wild species of Gladiolus (Greving,1987; Tombolato et al., 2005; Riaz et al., 2010). The m ar-ketable flower of gladiola is botanically a one-sided spikewith many florets. The flowers of cu ltivars come in avariety of colou rs. In addition to a cu t flower, the beau-tifu l blossom of gladiola may also be used in flowerbedsto create colou rfu l gardens (cottage-style) such as in the

reconstructed Monet’s garden at Giverny, France (Willery,2010).

Even though gladiola are grown in m any tropical, sub-tropical and temperate regions worldwide (Ahm ad et al.,2011), detailed studies on the phenology of gladiola arescarce. Previous studies on gladiola phenology is dedi-cated prim arily to describing below-ground developmen t(Trinklein , 2005), whereas above-ground developm en t isdescribed with fewer details (Cuevas, 1999). A detaileddescription of the above-ground development of glad-iola is importan t for basic studies on the biology andphenology of the species as well as for practical pu r-poses, such as the timing of field m anagem en t practicessuch as n itrogen side-dressing, disease and insect con -trol and harvest schedu ling (Greving, 1987; Smith , 2006).

496 Ann Appl Biol 166 (2015) 496–507© 2015 Association of Applied Biologists

Schwab et al. Staging system for describing the development of gladiolus

Therefore, a better understanding of gladiola phenologyhas the poten tial to improve flower quality and min imiseenvironmen tal effects on commercial production systems.

Phenology is the study of developm en t (Hodges, 1991).Plant developmen t can be defined as a process by whichindividuals or organs go th rough several identifiablestages during their life cycle (Wilhelm & McMaster, 1995),and includes cell differen tiation and organ in itiation andappearance, and may extend th roughout the plan t lifecycle including senescence (Hodges, 1991; Wilhelm &McMaster, 1995). Meier et al. (2009a) defined phenologyas the study of the even ts in the life cycle of an imals andplants, and these even ts are influenced by environmen-tal factors. A developm en tal stage is usually characterisedby the appearance (morphogenesis) of an organ , whereasthe in terval of time between two stages is defined as adevelopmen tal phase (Streck et al., 2003). An organ canbe identified using magn ification (hand lens or micro-scope) or in some cases by the naked eye.

The description of plan t developmen tal stages hasbeen of in terest for cen tu ries with records dating startingin A.D. 750 for the flowering period of cherry trees inJapan (Morais et al., 2008). Once the relevan t devel-opm en tal even ts in a plan t’s life cycle are determined,their sequence can be assembled in to a developmen-tal or phenological scale with stages designating thoseeven ts. Developm en tal staging systems are usefu l toolsto standardise communication am ong those involvedin agricu ltu ral activities such as farm ers, consu ltan ts,extension agents, crop insu rers, educators and scien tistsand are an aid in providing crop m anagemen t practices(Counce et al., 2000). Developmen tal scales have fourmain parts: the name of the developmen tal phases, thename of the developmen tal stages with in each devel-opm en tal phase, a code (a number, a set of letters or acombination of letters and numbers) and a description(criteria) of each developmental stage (Zadoks et al.,1974; Feh r & Caviness, 1977; Counce et al., 2000).

Developmental scales have been proposed for severalagricu ltu ral crops, including annual grain crops such assoybean (Fehr & Caviness, 1977), maize (Hanway, 1966;Ritch ie et al., 1993), wheat (Large, 1954; Zadoks et al.,1974) and rice (Counce et al., 2000), and fru it crops suchas persimm on tree (Garcia-Carbonell et al., 2002), olivetree (Sánz-Cortés et al., 2002), coffee tree (Morais et al.,2008) and mango tree (Delgado et al., 2011). Some floralcrops also have phenological scales such as Rosa sp. (Meieret al., 2009b) and Zinnia elegans (Gonçalves et al., 2008).The BBCH (Biologische Bundesanstalt, Bundessorte-namt, CHemische Industrie) system includes a scale forbu lb vegetables bu t not for bu lb flowers (Feller et al.,1995). Bu lb vegetables (on ion and garlic) are bienn ials,whereas bu lb flowers, including gladiola, are perenn ials

and they differ greatly in developmen t, so the BBCHscale for bu lb vegetables is not su itable for gladiola. Weare unaware of a com prehensive and adaptive stagingsystem for gladiola, wh ich constitu ted the rationale fordeveloping a phenological scale for th is floral crop.

With regard to the coding approach , we presen t astaging system for gladiola where the code is com prised bya letter and a number, following the widely used codingsystem s of maize (Ritch ie et al., 1993), soybean (Fehr &Caviness, 1977) and rice (Counce et al., 2000), whereletters represen t the developmental phase and num bersrepresent the developm en tal stage. Th is approach is easierfor end users such as extension agen ts and growers thana system coded only with numbers such as the Zadoks’scale (Zadoks et al., 1974) and the BBCH system (Meieret al., 2009a).

The objective of th is study was to create a stagingsystem for describing the developm en t of gladiola thatrelies on simple, visual and non-destructive criteria thatare easy-to-use.

Materials and methods

A plan t developmen t system needs fou r main featu res(Counce et al., 2000): (a) dichotomous criteria based onplan t morphogenesis (i.e. discrete m orphological criteriawh ich are either presen t or absen t) to iden tify develop-men tal stages and phases; (b) a basis on actual even tsrather than indications; (c) a wide range of geograph icalapplication and (d) visible criteria or markers readily iden -tifiable with a sm all hand lens (abou t 10× magn ification).Fu rther, a staging system shou ld have vegetative develop-men t based on cumulative leaf number (CLN), wh ich is abiologically sound way to express plan t age (Counce et al.,2000). The Haun ’s system (Haun , 1973) was the first stag-ing system to formally incorporate CLN as a con tinuousdevelopm en tal stage for wheat. Feh r & Caviness (1977)incorporate CLN as V stages (vegetative stages) in theirsoybean system recogn izing that the vegetative develop-men t can overlap the reproductive developmen t. We con-sidered all the above requiremen ts in the developmen t ofou r system for gladiola.

We followed the approach proposed by Counce et al.(2000) for developing a rice staging system. In laboratoryand field experimen ts, we observed the developmen tof gladiola corms and plan ts, and recorded progressionof phenological even ts. We also studied the literatu reand discussed with scientists in biology and floricultu rein order to determine the appropriate developmen talphases and stages. As the developmen tal stages weredefined, at least two individuals made observations onthe plan ts in the experim en ts. If the criteria were notclear (dichotomous and objective), difficu lt to see or were

Ann Appl Biol 166 (2015) 496–507 497© 2015 Association of Applied Biologists

Staging system for describing the development of gladiolus Schwab et al.

in terpreted differen tly by other observers, we discussedthe criteria un til consensus was reached.

Gladiola morphogenesis was divided in to fou r phases:corm dormancy, bud sprou ting, vegetative and reproduc-tive. The developmen tal stages of the sprou ting phasewere observed in five commercially vernalised corms ofcu ltivar Jester, kept in a laboratory, in dark conditions andtemperatu re of 25 –30∘C, which were laid on a wet cottonmesh (January 2012). As the developm en tal stages werereached, the corms were photographed.

For documen ting each of developmen tal stages of thevegetative and reproductive phases, commercially ver-nalised corms of cv. Jester were plan ted in 3.5-L potsand the potted plan ts grew in open field conditions atSan ta Maria, RS, Brazil (latitude 29∘43 ′ 23′ ′ S, longitude53∘43 ′ 15 ′ ′ W and altitude 95 m ), from Ju ly 2011 to Febru -ary 2012. When the developmen tal stages were reachedon these potted plan ts, they were immediately pho-tographed.

Additionally, developmental stages of the vegetativeand reproductive phases were observed in th ree fieldtrials conducted at the Departamento de Fitotecnia ofthe Universidade Federal de San ta Maria in San ta Maria,RS, Brazil. The first trial was carried ou t from 8 Septem-ber 2010 to 29 December 2010 with seven cultivars:T704 (pu rple), Traderhorn (red), Sunset (yellow), Jester(yellow and red), Priscilla (pink and white), Peter Pears(orange) and Rose Supreme (pink). The seven gladiolacu ltivars are com monly grown and represen tative of thewide range of colou rs and developmen tal cycles of glad-iola cu ltivars used in Brazil. The second trial was carriedout from 30 March 2011 to 31 December 2011 usingth ree cu ltivars: Traderhorn , T704 and Jester. In thesetwo trials, observations were made on five plan ts of eachcu ltivar. The th ird trial was carried ou t from 5 August2011 to 8 April 2011 using th ree cultivars (Peter Pears,T704 and Jester) and observations were performed on24 plan ts of each cu ltivar. All th ree trials with plan tingsat differen t times of year allowed for evaluation of thecriteria and ensu red consistency for each developmen talstage of the scale.

In these field trials, commercially vernalised cormswere plan ted in beds with two rows, 40 cm among rowsand 20 cm am ong plan ts with in the rows. There were 10corms per cultivar in the first two trials and 40 corms percu ltivar in the th ird trial. Agronomic practices used bylocal growers were used during the trials, wh ich includedfertilisation , weed con trol by hoeing, irrigation and sup-porting plan ts vertically with individual bam boo stakesin the first and second trials and with plastic net in theth ird trial. Plan ts were observed daily and the dates ofoccu rrence of the developmen tal stages were noted. Thecriteria selected to the identification of the developmen tal

stages had to be straigh t-forward and quick in the field.While observing the plan ts, researchers made notes abou tthe difficu lties in applying the criteria to each stage ofdevelopm en t.

A fourth trial with Jester corm s planted on 14 Septem-ber 2012 was conducted in San ta Maria, RS, Brazil, inorder to determine dry matter accumulation at eachdevelopm en tal stage of the developmen t cycle of glad-iola. Corms were plan ted in a 10 m bed in the sam eplan t spacing and management practices used during theprevious trials. Plan ts were observed daily and five plan tswere random ly sam pled when they reached each devel-opmental stage. The soil was removed from the corm androots by wash ing them with tap water. Sam pled plan tswere separated in to leaves, old corm , new corm , cormels,filiform roots, con tractile roots and floral stem, whichwere then oven dried at 60∘C. Dry matter distribu tionamong the differen t parts was calcu lated as a percen tageof total dry matter at each developmental stage.

Results

The developmen tal scale for Gladiolus is presen ted inTable 1. Images of each developmen tal stage are presentedin Figs 1 –7.

The dorm ancy phase is visible as a dorman t corm whichis not yet sprou ted (Stage S0, Fig. 1A). There are fou rstages with in the sprou ting phase: S1 (Fig. 1B), S2.1(Fig. 1C), S2.2 (Fig. 1D) and S2.3 (Fig. 1E). In the field,the developmen tal stages of the sprou ting phase occu r inthe soil.

The vegetative phase starts when the shoot (usuallycom posed of th ree sheaths) emerges from the soil su r-face. Vegetative developmental stages are designated asV stages, beginn ing at VE (emergence of the sheathsabove the ground) and extend un til the last leaf (herecalled the flag leaf as in other m onocots) is visible. AfterVE, the number in the code denotes the num ber of true(foliage) leaves above the last sheath , i.e. the CLN, sothat a plant at V1 has one leaf, V2 two leaves and so forthun til the final (flag) leaf is visible (VF). The marker forV1 –VF is when the leaf tip is visible to the observer, i.e.the leaf tip appearance. Images of plan ts at VE, V1, V2,V3, V6 and VF are in Fig. 2A, 2B, 2C, 2D, 2E and 2F,respectively.

The reproductive phase starts in the proposed stagingsystem when the spike is first visible at the whorl andends when the whole plan t senesces. Developmen talstages are denoted as R stages. Heading (when the tipof the spike is visible at the whorl), blooming (whenflorets show the colou r of the corolla), an thesis (floretsare open ing and an thers are visible) and florets senes-cence (when the corolla dehydrates and dies) are major



Table 1 The developmental staging system for Gladiolus

Phase Stages Code Description

Dormancy Dormant corm S0 Buds and root nodules are at rest and covered by the husks that overlap eachother covering the corm and meeting at the top of the corm

Sprouting Appearance of roots S1 Roots start growing from root nodules at the base of the cormFirst sheath S2.1 The first sheath that grew from the apex is visible at the top of the corm pushing

up the husksSecond sheath S2.2 Sheath continues its growth through the husks and the second sheath is visible

at the top of the cormThird sheath S2.3 Third sheath is visible at the top of the corm

Vegetative Emergence VE Shoot is first visible above the groundFirst leaf V1 First true leaf tip is visible at the shoot whorlSecond leaf V2 Second true leaf tip is visible at the shoot whorlThird leaf V3 Third true leaf tip is visible at the shoot whorl. Florets differentiation starts at the

apex (R0)Nth leaf Vn Nth true leaf tip is visible at the shoot whorlFlag leaf VF Last leaf tip is visible at the shoot whorl

Reproductive Heading R1.0 Spike tip first visible at the shoot whorlR1.1 Half of the spike emerged. The tip of the spike is level with the tip of the last leafR1.2 Emergence of spike completed. The peduncle of the spike is visible. After R1.2,

the rachis elongates and florets grow apartBlooming R2 First three florets at the bottom of the spike show the colour of the corolla. This

is the marketable harvest pointOnset of anthesis R3 The corolla of the first floret at the bottom on the spike is open with visible

anthersHalf of anthesis R3.4 The corolla of the floret located at the middle portion of the spike is open with

visible anthersBeginning floret senescence R3.5 First floret at the bottom of the spike starts senescence (corolla of the first floret

is dehydrated)Half of florets senesced R3.6 Floret at the middle of the spike starts senescenceAnthesis completed R4 The corolla of the last uppermost floret on the spike is open with visible anthersEnd of floret senescence R5 Last uppermost floret on the spike senesced. Corolla of all florets are deadPlant senescence R6 Above ground parts of the plant (leaves and floral axis) are brown (dead plant)

developmen tal stages, with som e divisions with in them(Table 1). Images of plants at R1.0, R1.1 and R1.2 are inFig. 3A, 3B and 3C, and at R2 and at R3 are in Fig. 4Aand 4B, respectively. As the florets con tinue to openupwards on the spike after R3 and when the floret at themiddle position of the spike is open , the plan t is at R3.4(Fig. 5A). When the first floret at the bottom of the spikestarts to senesce, the plan t is at R3.5 (Fig. 5B). When thefloret at the middle position of the spike senesces, theplant is at R3.6 (Fig. 5C). Floret open ing con tinues onthe spike un til the last floret opens (R4, Fig. 6A) and thefloret senescence con tinues un til the last floret senesces,at R5 (Fig. 6B). At the end of the developmental cycle,the whole plant has senesced, i.e. all leaves and floralaxis are brown . Th is is the stage R6 (Fig. 6C).

The total developmental sequence is presented inFig. 7. The m orphological criteria for R1.0, R1.1 and R1.2stages and the florets differen tiation stage (R0) at V3are shown in detail in Fig. 7. However, its identificationis on ly possible by dissecting the plan t and observing it

under a magn ification of 14× with a hand lens, as theapex is on ly about 6 mm in length (Sh illo & Halevy, 1976).

The number of days after plan ting to reach each devel-opmental stage of the vegetative phase (V stages) and thereproductive phase (R stages) in plan ts of the field trialsare in Tables 2 –4. In the first trial (plan ting on 8 Septem-ber 2010), the stages R1.1, R1.2, R3.4, R3.5, R3.6, R5 andR6 were not observed (Table 2). In the second trial (plant-ing on 30 March 2011), the stages R1.1, R1.2, R3.4, R3.6,R5 and R6 were not observed (Table 3) and in the th irdtrial (planting on 5 August 2011) on ly the R3.6 stage wasnot observed (Table 4). The missing stages in the trialswere because, at that time, we were constructing the scaleand those developm en tal stages had not been defined yet.

The time (in days) from plan ting to each developmen talstage varied with cu ltivar (Tables 2 –4). For instance, themarketable harvest time (stage R2) varied from 81 daysfor cu ltivar Priscilla to 97 days for cu ltivar Jester in the firsttrial (Table 2). Among plan ting dates, for cu ltivar Jester,the R2 was the shortest (95 days after plan ting) in theth ird trial (Table 4) and the longest in the second trial



A B C

D E

Figure 1 Developmental stages during the dormancy and sprouting phases in Gladiolus: S0 = Dormant corm (A), S1 = appearance of roots nodules at the baseof the corm (B), S2.1 = first sheath (C), S2.2 = second sheath (D), S2.3 = third sheath (E). The circles indicate the root nodules (B) and the sheaths (C–E). Thearrow in the insets of panels (D) and (E) indicates the fi liform roots at the base of the corm.

(122 days after plan ting) (Table 3), indicating strong effectof temperatu re on the rate of developmen t.

Dry matter distribu tion among differen t plan t parts (oldcorm, new corm, roots, leaves and spike) changed withdevelopmen t stage (Fig. 8). From emergence to V3, abou t80% of the plan t dry matter is in the old corm (7.7 gcorm −1) and from V4 forward the reserves in the oldcorm have all been used. Florets differentiation and spikegrowth starts at V3, spike starts an intense linear growthat V7 and leaf dry matter is maximum at VF (V8 in Fig. 8)(15.4 g plan t−1). At R3 –R4, spike dry matter is maximum(17.3 g plan t−1) and abou t 80% of the total plan t drymatter (43.1 g plan t−1) is in leaves and spike. Filiformroots are active un til V4 and con tractile roots start togrow from that stage. Corm els usually start their growthat R1 (it may vary among genotypes) and represen t abou t2% of the total plan t dry matter at R5. The new cormstarts to grow at V1 bu t its growth is sm all un til R5 (2.6 g

plan t−1). After R5, the growth of the new corm increases(18.6 g plan t−1) because all photoassimilates produced byleaves are translocated to below ground parts, un til leavessenescence (R6).

Discussion

During the dormancy phase (S0, Fig. 1A), the cormrem ains dorman t due to growth inh ibitors, such asabscisic acid (ABA). Th is strategy allows the su rvival ofthe structu re under adverse field conditions, such as coldtemperatu res and low soil moistu re (Tom bolato, 2004).The corm dormancy in gladiola can be broken by coldstorage (5∘C) or by applying growth regu lators (Castroet al., 1970; Vidalie, 1990).

The sprou ting phase in itiates when the corm is plantedin the soil and filiform roots start to grow from rootnodules at the base of the corm (S1, Fig. 1B). Then ,



A B C

D E F

Figure 2 Developmental stages during the vegetative phase of Gladiolus: VE= emergence (A), V1 = first leaf (B), V2 = second leaf (C), V3 = third leaf (D)(the detail in V3 is the floret differentiation – R0), V6 = sixth leaf (E) and VF= flag leaf (F).

sprou ting takes place in the upper part of the corm, andthe root growth con tinues, concu rrently with the sheath(incomplete leaves or bracts) growth (in sets of Fig. 1Dand 1E). Leaf primordia differen tiate at the apex of thebud and usually th ree leaf sheaths grow from the budto protect the growing true leaf. It is possible that someplants m ay have a fou rth sheath and in this case the stagewou ld be coded as S2.4.

The vegetative phase contain s a set of V stages, startingat em ergence (VE), suggesting that vegetative develop-ment occu rs by the accumulation of one leaf after theother on opposite sides of the shoot (Fig. 2). At VE, usu-ally one or two bracts of the th ree are visible above thesoil su rface (Fig. 2A). Emergence is an importan t develop-mental stage in many phenological systems (Zadoks et al.,1974; Fehr & Caviness, 1977; Counce et al., 2000) becauseit represen ts the beginn ing of leaf area growth andtherefore the beginn ing of solar radiation interception bythe canopy for photosyn thesis.

During the vegetative phase, the period between theappearance of successive leaf tips upwards on the shoot isone phylloch ron and can be easily determ ined by nakedeye. Photoassim ilates du ring the vegetative phase areused to grow roots, the new corm and cormels, and thespike. An important field managemen t practice in gladiolaoccu rs at the V3 stage. Nitrogen is side-dressed at V3because floral differen tiation starts at this stage inside thewhorl and is a strong n itrogen sink in the plan t (Shillo& Halevy, 1976). Differen tiation of florets is acropetaland the spike is visible at the whorl, righ t before the lastuppermost leaf tip (flag leaf) is visible (Fig. 2F), when thefinal leaf number is defined, indicating that the vegetativephase has ended.

The reproductive phase is composed of a set of Rstages, starting with R1.0 (Fig. 3A). At th is stage, it isim portan t that plan ts are supported either with indi-vidual stakes (wood or bamboo-made) or with a plasticnet so that plan ts do not tilt or lodge as the peduncleof the spike elongates above the uppermost leaf (final



A B C

Figure 3 Development of the spike during the reproductive phase in Gladiolus: R1.0 = spike first visible at the whorl (A), R1.1 = half of the spike emerged fromwhorl (B), R1.2 = emergence of spike is completed (C).

A B

Figure 4 Development of the spike during the reproductive phase in Gladiolus: R2 = first three florets at the bottom of the spike show the colour of the corolla(A), R3 = the corolla of the first floret at the bottom of the spike is open with visible anthers (B).

leaf number) and becom es heavy. When gladiola arepart of flowerbeds (Willery, 2010), lodging is usuallynot a problem as neighbour plan ts support the gladiolaplan t.

Following heading, the rachis elongates, the distanceam ong florets increases and florets become obvious.Flowering occu rs acropetally and at some poin t in timethe corolla of the first floret shows colou r. In comm ercialcu t flower plan tations, the R2-stage (Fig. 4A) is the rec-ommended harvest poin t for the spikes as it allows longvase life during transportation and marketing. Whencustomers see the spikes, th ree florets are usually open-ing. In Brazil, a major holiday for gladiola consum ption isAll Sou ls’ Day (2 Novem ber). In order to have marketableflowers for this holiday, plan ting is usually carried ou t

du ring the second half of Ju ly, V stages occu r from endof August to mid-October and R3 has to occu r 2 –4 daysbefore the holiday.

When the corolla of the first floret at the bottom ofthe spike is open, the stage indicates the onset of an the-sis. In the Jester cu ltivar, the beautifu l yellow corollais irregu larly flam ed with red, and is first visible at R3(Fig. 4B). An thesis and senescence of the florets proceedupwards on the rach is un til the uppermost floret has itscorolla open with visible an thers (Fig. 6A) and bloomingends. When the corolla of the uppermost floret senesces(Fig. 6B, after R5), the vase life has ended bu t the plan thas green leaves, and photoassimilates are translocatedfrom the leaves to the new corm and cormels. A gladi-ola plan t reaches the end of the cycle when the leaves



A B C

Figure 5 Development of the spike during the reproductive phase in Gladiolus: R3.4 = the corolla of the floret located at the middle portion of the spike isopenwith visible anthers (A), R3.5 = first floret at the bottom of the spike starts senescence (B), R3.6 = floret at the middle of the spike starts senescence (C).

A B C

Figure 6 Development of the spike during the reproductive phase in Gladiolus: R4 = the corolla of the uppermost floret on the spike isopen with visible anthers(A), R5 = uppermost floret on the spike senesced (B), R6 = above ground parts of the plant have senesced (C).

Figure 7 Developmental sequence in Gladiolus. For description of developmental stages, see Table 1. The detail in V3 is the florets differentiation at the apex(R0), which is only possible to be seen under 14× magnification.



Table 2 Number of days from planting to developmental stages (DS) in seven Gladiolus cultivars planted on 8 September 2010 at Santa Maria, RS, Brazil. Eachvalue is the mean of five plants and value in parenthesis is one standard deviation of the mean

Cultivars

DSa Priscilla Peter Pears Trader Horn Sunset Rose Supreme T704 Jester

VE 21 (± 3.69) 29 (± 7.11) 28 (± 2.57) 28 (± 4.64) 20 (± 0.99) 27 (± 1.41) 31 (±3.33)VFb 78 (± 0.00) 78 (± 0.00) 94 (± 7.89) 86(± 0.00) 90(± 3.74) 91(± 5.29) 91(± 5.72)R1.0 72 (± 2.29) 78 (± 5.35) 83 (± 4.95) 82 (± 2.65) 87 (± 2.77) 85 (± 2.49) 88 (±5.32)R2 81 (± 3.51) 87 (± 5.19) 92 (± 4.95) 91 (± 1.15) 96 (± 2.95) 94 (± 2.19) 97 (±4.82)R3 85 (± 3.39) 89 (± 5.25) 95 (± 6.36) 91 (± 4.04) 98 (± 3.09) 96 (± 2.95) 100 (± 4.85)R4 93 (± 3.53) 102 (± 5.07) 107 (± 0.71) 105 (± 0.58) 111 (± 2.38) 106 (± 2.30) 109 (± 3.29)

aFor description of DS, see Table 1.b Priscila and Peter Pears cultivars had eight leaves and the other cultivars had nine leaves.

Table 3 Number of days from planting to several developmental stages inthree Gladioluscultivarsplanted on 30 March 2011 at Santa Maria, RS, Brazil.Each value is the mean of five plants and value in parenthesis is one standarddeviation of the mean

CultivarsDevelopmentalstagesa Jester Trader Horn T704

VE 24 (± 5.15) 19 (± 5.14) 21 (± 5.80)VFb 115 (± 5.47) 100 (±17.04) 78 (± 7.23)R1.0 110 (± 8.92) 90 (± 14.28) 117 (± 10.84)R2 130 (± 10.71) 109 (±13.50) 122 (± 18.61)R3 132 (± 10.89) 113 (±12.60) 126 (± 19.91)R3.5 139 (± 7.51) 122 (±13.67) 128 (± 17.79)R4 147 (± 8.08) 131 (±7.08) 143 (± 17.46)

aFor description of developmental stages, see Table 1.b Cultivar T704 had eight leaves and the other cultivars had nine leaves.

have completely died (leaves and floral axis are brown),coded as R6 stage (Fig. 6C). At th is stage, translocationof assimilates to the new corm and the cormels ceasesbecause there are no more photosyn thetically activeorgans. Thus, the maximum size of the corm and themaximum number of cormels are set at R6.

The period from about R3 to R4 is the vase life ofgladiola. The longer the R3 –R4 period the better forcustomers. Therefore, the search for cu ltivars with longerR3 –R4 period shou ld be in the portfolio of desirable traitsin gladiola breeding programm es. The data on durationof R3 and R4 in Tables 2 –4 are based on gladiola grownand left to flower in the field. As a cut flower, the spike isremoved from the plan t and kept in vase from abou t R3to R4, and florets open with the reserves accumulated inthe rach is before it was removed from the plan t. Thus, weexpect a close relationsh ip between the duration of theR3 and R4 phase in the field with its vase life, m odu latedby tem peratu re.

The staging system proposed in Table 1 and illu stratedin Figs 1 –7 was tested in the th ree field trails, wheregladiola plan ts of differen t cultivars grew in distinctmeteorological conditions. In the 2010 trial, vegetative

Table 4 Number of days from planting to several developmental of develop-mental stages in three Gladiolus cultivars planted on 5 August 2011 at SantaMaria, RS, Brazil. Each value is the mean of 24 plantsand value in parenthesisis one standard deviation of the mean

CultivarsDevelopmentalstagesa Peter Pears T704 Jester

VE 21 (± 4.24) 24 (± 3.74) 20 (± 3.95)V1 24 (± 1.82) 31 (± 3.47) 27 (± 1.71)V2 35 (± 1.11) 42 (± 2.64) 39 (± 3.54)V3 45 (± 1.12) 51 (± 3.95) 50 (± 3.17)V4 54 (± 1.18) 59(± 2.68) 57 (± 2.51)V5 62 (± 1.31) 68 (± 3.46) 66 (± 3.59)V6 69 (± 1.22) 73 (± 6.81) 73 (± 3.61)V7 75 (± 0.85) 79 (± 7.28) 75 (± 1.75)V8 80 (± 1.95) 85 (± 6.72) 80 (± 1.36)VF 80 (± 4.81) 92 (± 9.85) 86 (± 2.76)R1.0 85 (± 2.27) 86 (± 4.21) 84(± 2.34)R1.1 86 (± 2.37) 87 (± 5.52) 87 (± 2.96)R1.2 89 (± 1.76) 90 (± 5.51) 88 (± 2.44)R2 95 (± 2.14) 96 (± 4.10) 96 (± 2.05)R3 97 (± 2.13) 98 (± 3.56) 98 (± 1.98)R3.4 98 (± 1.11) 99 (± 2.29) 102 (±2.24)R3.5 99 (± 1.80) 99 (± 1.89) 102 (±2.20)R3.6 107 (± 2.67) 109 (± 1.72) 106 (±1.22)R4 106 (± 2.36) 108 (± 2.42) 109 (±0.71)R5 108 (± 0.76) 110 (± 2.03) 111 (±0.92)R6 216 (± 5.23) 189 (± 25.65) 210 (±14.35)

a For description of developmental stages, see Table 1.

developm en t occurred during mild temperatu res inSeptember and October (15 –25∘C) while reproductivedevelopm en t took place during warm tem peratu res(30 –37∘C) in Novem ber and December. In the 2011 trial,vegetative developmen t occu rred under m ild tempera-tures (20 –25∘C) during April, May and June, whereasreproductive developm en t occu rred under low temper-atu res (5 –15∘C), du ring Ju ly and August. In the th irdtrial, the vegetative development occu rred from Augustto October, when temperatu res were mild (15 –25∘C)and reproductive developm en t occu rred in November(25 –30∘C), except the period between R5 and R6, wh ich



Figure 8 Dry matter distribution among different parts of a Gladiolus plant (cv. Jester) as a function of developmental stage and days after emergence (DAE).Planting date was 14 September 2012. Each point is the mean of five plants.

occu rred from December to March , under elevatedtemperatu res (25 –35∘C). These trials provided a gooddata set to evaluate the criteria for iden tifying eachdevelopmen tal stage of the proposed staging system.

In our team, we had a total of six personnel who wen tto the field and m ade the observations of the developmen-tal stages in the trials. In each visit, at least two individualsassessed the plan ts and independen tly evaluated the cri-teria. Overall, the personnel found that using the criteriawas easy and they cou ld qu ickly determine all develop-mental stages. These resu lts are importan t, as detailedexperiments where several developmen tal stages have tobe analysed can be very labour in tensive. Another impor-tan t featu re for a developm en tal scale is that the criteriamust be clear and objective. The personnel who did theobservations unan im ously agreed abou t clarity and theobjective natu re of the descriptions provided in Table 1.Th is allows for consistency am ong observations.

The different plan ting dates in the th ree trials resu ltedin differen t du rations of vegetative and reproductivestages (Tables 2 –4). The average length was 62, 77 and64 days for the vegetative (VE–VF) phase and 23, 40and 22 days for the reproductive phase (R1 –R5) in thetrials plan ted on 8 September 2010, 30 March 2011 and5 August 2011, respectively. The longer length of all thedevelopmen tal stages du ring the 30 March 2011 plan ting

was because plan ts grew during au tumn and win ter(April–August) when the air temperature varied from− 1.1∘C to 31.7∘C. Plan ts in the other two plan tings devel-oped during the warmest mon ths (September –March)when air tem peratu re varied from 1.2∘C to 36.3∘C. Theseresu lts indicate that air temperatu re has an importan teffect on the rate of the developmen t in gladiola, similarto other agricu ltu ral crops (Hodges, 1991; Wilhelm &McMaster, 1995; Streck et al., 2003).

The phylloch ron varied from 2 to 12 days per leaf(Table 4). The fou r V1 –V4 leaves required more tim ethan the V5 –V8 leaves. The difference was related totemperature. The first four leaves developed at meanair temperatu re of 16.3∘C, while the last fou r leavesdeveloped at mean air temperatu re of 19.6∘C. Similareffects of temperatu re on leaf appearance rate have alsobeen reported for other agricu ltu ral crops (Wilhelm andMcMaster, 1995; Streck et al., 2003).

Plan t growth (dry m atter accumulation and its parti-tion ing among plan t parts) is modu lated by developmen-tal stages (Fig. 8). As plan t developmen t progresses, som egrowth processes are connected to specific developmen-tal stages. For in stance, in gladiola during the vegetativephase, the majority of plan t dry m atter accumulates inthe leaves. At the V3 stage, the spike starts its growth andat the V4 stage the contractile roots start their growth ,



whereas corm els on ly start their growth at R1 (Fig. 8).This dynamic relationsh ip between growth and develop-men t is another exam ple of the importance of having adetailed phenological scale for gladiola. We expect the drymatter partition ing pattern in Jester (Fig. 8) to be con-sisten t with other commercial gladiola cu ltivars, as thevariability of the genotype-dependent traits of cormel drymatter and number of leaves per plant is small.

The developmen t scale proposed in th is paper is aneasy and practical field scale, su itable for use by farmers aswell as by extension personnel for research purposes. Thescale was tested with seven widely grown comm ercialgladiola cu ltivars in Brazil (Table 2–4). These cu ltivarshave similar colou rs and morphological featu res as thosegrown in Europe and North America. Consequently, thedevelopmen tal scale (Table 1) works for a wide rangeof gladiola cu ltivars (Gladiolus × grandiflorus). The scalecomprises stages du ring different developmen tal phases,from sprou ting, vegetative and reproductive phases,including the period of commercial in terest to producersof cu t flowers (VE–R2) and extends to plan t senescence(R6), based on discrete (dichotomously) naked eye mor-phological criteria. The vegetative developm en t is basedon CLN and the system can be expanded to includethe development of the spike inside the whorls beforeappearance (R1). Floret differen tiation (wh ich occu rs atV3, Fig. 2D) is coded as R0 so that early reproductivedevelopmen t (R0 –R1) overlaps part of vegetative devel-opm en t (V3 –VF). The partial overlap between vegetativeand reproductive developmen t also happens in other agri-cu ltu ral crops such as wheat (Zadoks et al., 1974), soybean(Fehr & Caviness, 1977) and rice (Counce et al., 2000).

Acknow ledgements

Authors thank Charles Patrick Oliveira de Freitas, Gio-vana Ghislen i Ribas and José Eduardo Wink for theirassistance with the field experimen ts and Patricio OrozcoCon treras for captu ring images of the plan ts. Th is workwas supported by the Conselho Nacional de Desen-volvimen to Cien tífico e Tecnológico (CNPq), Proc. no.302524/2011-8, and by Coordenação de Aperfeiçoa-men to de Pessoal de Nível Superior (CAPES).

ReferencesAh mad I., Khattak A.M., Ara N., Amin N.U. (2011) Effect

of plan tin g dates on th e growth of gladiolu s corm inPeshawar. Sarhad Journal of Agriculture, 27, 195 –199.

Castro P.R.C., Min am i K., Gil C.M., Demétrio C.G.B. (1970)Efeitos da vern alização e de fitoregu ladores n o desenvolvi-mento de Gladiolus grandiflorus. Anais da E.S.A. “Luis deQueiros”, 36, 153 –171.

Cou nce P.A., Keisling T.C., Mitch ell M.J. (2000) A un iform ,objective, and adaptative system for expressin g rice devel-opm en t. Crop Science, 40, 436 –443.

Cu evas R.H. (1999) Produccion de Gladiolo. Curso: Produc-cion de tulipan, lilium y gladiolo. In stituto de Investiga-cion es Agropecu arias – Centro Regional de InvestigacionCarillan ca, 70, 49 –65.

Delgado P.M.H., Aran gu ren M., Reig C., Galván D.F., MesejoC., Fu en tes A.M., Saúco V.G., Au gu stí M. (2011) Ph e-n ological growth stages of man go (Mangifera indica L.)accordin g to the BBCH scale. Scientia Horticulturae, 130,536 –540.

Feh r W.R., Caviness C.E. (1977) Stages of Soybean Development.Ames, IA, USA: Iowa State University of Science an dTech n ology (Special Report, 80).

Feller C., Bleih older H., Bu h r L., Hack H., Hess M., Klose R.,Meier U., Stau ss R., Van den Boom T., Weber E. (1995)Phän ologische Entwicklun gsstadien von Gemü sepflan zen :I. Zwiebel-, Wu rzel-, Kn ollen- u nd Blattgem üse.Nachrichtenblatt des Deutschen Pflanzenschutzdienstes, 47,193 –206.

Garcia-Carbon ell S., Yagü e B., Bleih older H., Meier U.,Augusti M. (2002) Ph en ological growth stages of th e per-simmon tree (Diospyros kaki). Annals of Applied Biology, 141,73 –76.

Gon çalves C., Jú nior M.J.P., Castro C.E.F. (2008) Fen ologia eestim ativa da du ração do ciclo da zín ia ’Profu sion Cherry’cultivada em vasos em am bien te protegido. Bragantia, 67,527 –532.

Greving A.J. (1987) Historical Materials from University ofNebraska-Lincoln Extension: G87-852 Growing Gladiolus. Un i-versity of Nebraska – Lin coln Extension , Paper 978, 1 –5.

Han way J.J. (1966) Growth stages of corn (Zea mays L.).Agronomy Journal, 55, 487 –492.

Hau n J.R. (1973) Visual quantification of wheat develop-m en t. Agronomy Journal, 65, 116 –119.

Hodges T. (1991) Introduction . In Predicting Crop Phenology,pp. 1 –2. Ed T. Hodges. Boston, MA, USA: CRC Press.

Large E.C. (1954) Growth stages in cereal – illustration of th eFeekes scale. Plant Pathology, 3, 128 –129.

Meier U., Bleih older H., Buh r L., Feller C., Hack H., HeßH., Lan cashire P.D., Schn ock U., Stau ß R., Van Den BoomT., Weber E., Zwerger P. (2009a) The BBCH system tocodin g th e ph en ological growth stages of plan ts – h istoryand pu blication s. Journal für Kulturpflanzen, 61, 41 –52.

Meier U., Bleiholder H., Bru mm e H., Bru ns E., Mehring B.,Proll T., Wiegan d J. (2009b) Phenological growth stagesof roses (Rosa sp.): codification an d description accord-in g to the BBCH scale. Annals of Applied Biology, 154,231 –238.

Morais H., Caram ori P.H., Koguishi M.S., Ribeiro A.M.A.(2008) Escala fen ológica detalh ada da fase reprodu tiva deCoffea arabica. Bragantia, 67, 257 –260.

Riaz T., Kh an S.N., Javaid A. (2010) Managem en t of Fusariumcorm rot of gladiolus (Gladiolus grandiflorus sect. Blan du s cv.



Aarti) by u sin g leaves of allelopath ic plants. African Journalof Biotechnology, 9, 4681 –4686.

Ritch ie S.W., Han way J.J., Ben son G.O. (1993) How a CornPlant Develops. Ames, IA, USA: Iowa State University ofScience and Tech nology, Cooperative Extension Service(Special Report, 48).

Sánz-Cortés F., Martín ez-Calvo J., Baden es M.L., Bleih olderH., Hack H., Llácer G., Meier U. (2002) Ph enologicalgrowth stages of olives trees (Olea europaea). Annals ofApplied Biology, 140, 151 –157.

Sh illo R., Halevy A.H. (1976) Inflorescence developmentof flowering and blasted gladiolu s plants in relation todevelopment of other plan t parts. Scientia Horticulturae, 4,79 –86.

Sm ith R.C. (2006) Giddy over Gladiolus. Fargo, ND, USA:North Dakota State Un iversity.

Streck N.A., Weiss A., Xu e Q., Baezin ger P.S. (2003) In corpo-rating a ch ron ology response fu nction into th e predictionof leaf appearan ce rate in win ter wh eat. Annals of Botany,92, 181 –190.

Tombolato A.F.C. (2004) Cultivo comercial de plantas ornamen-tais. In stitu to Agron ôm ico de Cam pin as (IAC): Campinas,Brazil.

Tombolato A.F.C., Castro J.L., Matthes L.A.F., Lem e J.M.(2005) Melh oramento genético do gladíolo n o IAC: novoscultivares ‘IAC Carmim ’ e ‘IAC Paran apanema’. Científica,33, 142 –147.

Trin klein D. (2005) G6620 Summer Flowering Bulbs: Gladiolus.Colu mbia, MU, USA: University of Missou ri-Colu mbia,1 –4.

Vidalie H. (1990) Les productions florales (Collection Agricultured’Aujourd’hui). Paris, Fran ce: Édition s Tec Et Doc/Lavoisier.

Wilhelm W.W., McMaster G.S. (1995) Im portan ce of th ephylloch ron in studying developm en t an d growth ingrasses. Crop Science, 35, 1 –3.

Willery D. (2010) The Garden of Claude Monet. Paris, France:Ulm er.

Zadoks J.C., Ch an g T.T., Kon zak C.F. (1974) A decim alcode for th e growth stages of cereals. Weed Research, 14,415 –421.


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A phenological scale for the development of Gladiolus