Phenological behaviour of Parthenium hysterophorus in response to climatic variations according to the extended BBCH scale: Phenology of Parthenium hysterophorus under varying climate

Abstract

Considering the importance of ecological and biological traits in imparting invasive success to the alien species, the phenological behaviour of an alien invasive weed Parthenium hysterophorus was documented according to the extended BBCH scale in four different seasons. A phenological calendar was prepared using both two- and three- digit coding system, precisely describing the developmental stages of the weed. The phenological documentation is further supplemented with the dates corresponding to a particular growth stage, pictures of the representative growth stages and meteorological data of all the four seasons. Results revealed that the phenology of the weed altered in response to the changing temperature and humidity conditions but no apparent climatic condition could inhibit its germination or flowering. However, the emergence of inflorescence was highly sensitive to the temperature/photoperiodic conditions. Variations in the phenological traits of P. hysterophorus with changing environmental conditions explain the acclimatisation potential of the weed permitting its vast spread in the non-native regions. Since the given phenological illustrations are accurate, unambiguous and coded as per an internationally recognised scale, they could be exploited for agronomic practices, weed management programmes, and research purposes.

Full text

Annals of Applied Biology ISSN 0003-4746
RESEARCH ARTICLE
Phenological behaviour of Parthenium hysterophorus in
response to climatic variations according to the extended
BBCH scale
A. Kaur1, D.R. Batish1,S.Kaur
1,H.P.Singh
2& R.K. Kohli1,3
1 Department of Botany, Panjab University, Chandigarh, India
2 Department of Environment Studies, Panjab University, Chandigarh, India
3 Central University of Punjab, Mansa Road, Bathinda, India
Keywords
BBCH growth stages; BBCH scale; Parthenium
hysterophorus; phenology; plant invasion.
Correspondence
D.R. Batish, Department of Botany, Panjab
University, Chandigarh 160 014, India. Email:
daizybatish@yahoo.com, daizybatish@pu.ac.in
Received: 10 April 2017; revised version
accepted: 30 May 2017; published online: 12
September 2017.
doi:10.1111/aab.12374
Abstract
Considering the importance of ecological and biological traits in imparting inva-
sive success to the alien species, the phenological behaviour of an alien inva-
sive weed Parthenium hysterophorus was documented according to the extended
BBCH scale in four different seasons. A phenological calendar was prepared
using both two- and three- digit coding system, precisely describing the devel-
opmental stages of the weed. The phenological documentation is further sup-
plemented with the dates corresponding to a particular growth stage, pictures
of the representative growth stages and meteorological data of all the four sea-
sons. Results revealed that the phenology of the weed altered in response to the
changing temperature and humidity conditions but no apparent climatic con-
dition could inhibit its germination or flowering. However, the emergence of
inflorescence was highly sensitive to the temperature/photoperiodic conditions.
Variations in the phenological traits of P. hysterophorus with changing environ-
mental conditions explain the acclimatisation potential of the weed permitting
its vast spread in the non-native regions. Since the given phenological illustra-
tions are accurate, unambiguous and coded as per an internationally recognised
scale, they could be exploited for agronomic practices, weed management pro-
grammes, and research purposes.
Introduction
Phenology is a scientific discipline dealing with the
dynamics of the periodic events in the life cycle of
a species. In biological sciences, the core phenologi-
cal research addresses the timing of switches between
recurrent developmental or behavioural phases (Badeck
et al., 2004). Phenological dynamics is an outcome of
the complex interactions between genetic and envi-
ronmental factors (Ruml & Vuli´
c, 2005). Being one of
the reliable bio-indicators of global change, as proposed
by European Environmental Agency (Menzel, 2013),
phenological studies have received due attention in the
recent decades. Inter-relating the phenological traits with
environmental variables may supplement the research
advancements in the field of climate change, biodiversity,
agriculture and forestry.
Plant invasion, a key contemporary issue in the bio-
logical sciences, is closely inter-linked with phenology.
Theories explaining the success of invasive exotic species
suggest that phenology, directly or indirectly, regulates
the phenomenon of invasion (Wolkovich & Cleland,
2014). An analysis of the traits associated with invasion
revealed that the flowering and reproductive biology is
significantly related with the invasion success (Küster
et al., 2008). Invasive species are far more opportunistic
with better phenological sensitivity, by virtue of which
they may alter their phenologies in response to the sea-
sonal variations (Wilsey et al., 2011; Fridley, 2012; Throop
et al., 2012). This allows certain species to expand their
invasion range with the shifting of favourable growth
conditions and others to adjust with the changing envi-
ronment. Either way, they gain a competitive advantage
316 Ann Appl Biol 171 (2017) 316– 326
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A. Kaur et al. Phenology of Parthenium hysterophorus under varying climate
over the natives. Coming decades may witness more of
such phenological shifts under the projected seasonal
catastrophes resulting from global warming and climate
change. Temperature dependent changes in the phenol-
ogy of exotic species have recently been noticed in North
America (Wolkovich et al., 2013). It is, therefore, perti-
nent to explore the phenological patterns exhibited by
invasive exotic species in order to predict their responses
in the future scenario and to devise better management
strategies for their mitigation.
BBCH (Biologische Bundesanstalt, Bundessortenamt
and CHemishe Industrie) scale is a simplified, standard-
ised and widely accepted phenological coding system. It
was first proposed by Bleiholder et al. (1989) to describe
growth stages of the plants, taking into consideration the
decimal code published by Zadoks et al. (1974). Later on,
it was adopted by Lancashire et al. (1991) to design spe-
cific scales of some cultivated plants. More recently, Hack
et al. (1992) and Hess et al. (1997) proposed an ‘extended
BBCH scale’ for crop and weed species with necessary
improvements. The scale is a systematic description of the
entire life cycle of a plant using a two- or three- digit dec-
imal code. First and the second digit of the two-digit code
represents ‘principal growth stages’ (PGS) and ‘secondary
growth stages’ (SGS), respectively, both described by ordi-
nal numbers, 0 to 9. Principal growth stages explain the
broad and long-term developmental processes, generally
common to a specific group of plant species, whereas
SGS correspond to the characteristic short-term develop-
mental steps that may be specific for genera or species.
Further, the three-digit code allows the introduction of
intermediate ‘mesostages’ for a detailed and better inter-
pretation of each growth stage (Hack et al., 1992). The
scale is being extensively used to describe the develop-
mental stages of cultivated plants and weed species, since
it was first proposed in 1989 (Meier et al., 2009). Earlier,
its use was limited to the agricultural purposes, but lately
it is being exploited for tracing the phenology of invasive
alien plants (Jaryan et al., 2014). The BBCH scale has been
recognised as a standard system for describing phenologi-
cal stages of a plant by European Phenology Network (van
Vliet et al., 2003) and European and Mediterranean Plant
Protection Organization (EPPO) (Meier et al., 2009).
Parthenium hysterophorus L. (Asteraceae) is an obnox-
ious invasive weed indigenous to the tropical and
subtropical Americas. It is posing a serious threat to the
natural- and agro-ecosystems in more than 50 coun-
tries worldwide (Belgeri & Adkins, 2015), by virtue of
its high reproductive ability, wide range of ecological
adaptation and allelopathic properties (Kohli & Rani,
1994). It is a weed of nearly 42 crop species, including
staple food crops, commercial crops, oil seed crops, veg-
etables and pulses (Shi et al., 2015). Also, the invasion
of P. hysterophorus has altered the vegetation patterns
and soil nutrient composition of the grassland commu-
nities due to its allelopathic interference (Nigatu et al.,
2010; Timsina et al., 2011). Recent studies reveal that the
invasion potential of P. hysterophorus is expected to be
increased under climate change scenario (Shrestha et al.,
2015). The recent reports of its occurrence from previ-
ously un-invaded countries (Mahmoud et al., 2015) and
possibility of its further spread in parts of southeast Asia,
sub-Saharan Africa, temperate northern hemisphere and
high elevation equatorial regions (McConnachie et al.,
2011; Kriticos et al., 2015; Mainali et al., 2015) shows
that P. hysterophorus has a considerable potential for rapid
adaptation with the changing environmental conditions.
Thus, understanding the phenological behaviour of P.
hysterophorus may help in tracking its establishment,
proliferation and invasion in novel habitats as well as in
deciding the management options. A study was there-
fore, planned with an objective of (a) documenting the
phenological traits of P. hysterophorus according to BBCH
scale, and (b) understanding the phenological responses
of the weed with changing environmental conditions.
Materials and methods
Variations in the phenological traits of P. hysterophorus
were studied under different climatic conditions. The
study was divided into four seasons with respect to tem-
perature (T) and relative humidity (RH), that is S1 (Low
T high RH); S2 (High T low RH); S3 (High T high RH);
S4 (Low T low RH). On the basis of required variations in
T(
∘C) and RH (%), 4 months, December (12∘C; 93.1%),
May (30.3∘C; 55%), July (30.2∘C; 90.5%) and October
(25.1∘C; 57%) were selected representing S1, S2, S3 and
S4, respectively.
The experiment was established under partially nat-
ural conditions of experimental dome in the Depart-
ment of Botany, Panjab University, Chandigarh, India
(30∘45′38′′N; 76∘45′55′′ E; 348 m above sea level) dur-
ing 2014–2016. Wildly growing stands of the weed in
Panjab University campus served as the seed stock for
the experiment after a short period of dry storage as
suggested by Tamado et al. (2002). One hundred mature
seeds [weight: 0.06 ±0.005 g (df-4); percent viability:
94.35 ±0.113 (df-4)] were sown in earthenware pots
(diameter: 25 cm; depth: 22 cm) during S1, S2, S3 and
S4. The pots were kept free from the growth of any other
weed and maintained properly for water requirement.
After germination, 30 individuals were tagged for doc-
umenting the phenological stages, which were reduced
to 10 after the appearance of inflorescence. Each individ-
ual was carefully observed and photographed at regular
intervals. A phenological calendar for P. hysterophorus was
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Phenology of Parthenium hysterophorus under varying climate A. Kaur et al.
prepared according to the extended BBCH scale (Hack
et al., 1992; Hess et al., 1997). When 50% of the tagged
individuals reached a particular phenological stage, date
corresponding to the given stage was recorded and pre-
sented as DAS (days after sowing) describing the nth
day after the seeds were sown. Data pertaining to daily
temperature and relative humidity was obtained from
India Meteorological Department, Chandigarh, India.
Data for day length has been compiled from Chandigarh
Tribune (daily newspaper) available online at http://
epaper.tribuneindia.com/t/299.
Results
The phenology of P. hysterophorus was described using
both two- and three-digit BBCH coding system (Table 1).
Description was based on the external morphological
traits that can be easily observed, counted or measured
and can be presented in ordinal or percentage values.
However, the major developmental stages of the plant
did not proceed in the defined series and may be unse-
quential or coinciding. Wherever necessary, three-digit
coding may be taken into consideration for a better
understanding of the phenological stages. The pictorial
representation of the significant growth stages has been
provided in Fig. 1.
Life cycle began with the hypogeal germination of
the seeds (achene, 1 –3 mm long and 1 –1.5 mm wide)
(stage 000; Fig. 1) and emergence of seedling through
thesoilsurface,asdescribedbyPGS0(germination).
This process took place beneath the soil, hence cannot be
photographed or recorded. During S1, seed germination is
delayed and took 14 days, whereas during S2, S3 and S4,
seeds germinated in 3–4 days. The percent germination
recorded during S1, S2, S3 and S4 was 76%, 81%, 96%
and 83%, respectively. The average temperature was 12∘C
and humidity was 93% during S1. S2 and S3 witnessed
similar temperatures (30∘C) but varying humidity levels
(55% and 90%, respectively). During S4, the average
temperature recorded was 25∘C and humidity was 57%
(Fig. 3).
Thereafter, PGS 1 (leaf development) described unfold-
ing of the cotyledons (stage 100; Fig. 1) and the subse-
quent true leaves. A leaf was considered unfolded when
it attained the length of 1 cm. The first pair of true
leaves was simple, opposite and elliptical in shape (stage
101/102; Fig. 1), whereas the subsequent leaves were
simple but alternate, highly pubescent and runcinate in
shape with slightly or deeply lobed margins (stage 107;
Fig. 1). During S2 and S3, the cotyledons unfolded 3–7 h
after the plumule breaks through the soil surface, whereas
in case of S1 and S4, it took 20–38 h for the cotyle-
dons to unfold. A gap of maximum 20 days was observed
in the emergence of subsequent leaves during S1. On
the contrary, during S2, the minimum gap was recorded
in the appearance of subsequent leaves, which was as
little as a few hours in certain cases. Principal growth
stage 1 was completed in 112 days during S1 and 24, 58
and 68 days during S2, S3 and S4, respectively (Fig. 2).
The total number of true leaves produced also varied
seasonally with S4 producing the maximum number of
leaves [33.2 ±4.80 (df-29)] and S2 producing the mini-
mum [9.1 ±2.11 (df-29)]. The PGS 1 experienced an aver-
age temperature of 19∘C during S1, 22∘C during S4 and
29–32∘C during S2 and S3 (Fig. 3a). Humidity levels were
high during S1 and S3 (81–83%), optimum during S4
(69%) and very low in case of S2 (39%) (Fig. 3b).
During the initial vegetative growth of the plant, the
stem remained short and leaves adhered to the ground,
thus forming a rosette (stage 301–309; Fig. 1). The weed
may arrest its growth at this stage depending on the envi-
ronmental conditions. This stage was represented by PGS
3 (rosette growth) and described in terms of percentage of
maximum diameter attained. In this study, S1 and S4 wit-
nessed the rosette formation with a maximum diameter
of 35.2 ±1.821 (df-29) cm and 43.2 ±2.669 (df-29) cm,
respectively. The duration of the stage was more in case
of S4 (88 days) than S1 (52 days) (Fig. 2). The average
temperature and humidity during S1 was 18∘C and 78%,
respectively, and during S4 was 17∘C and 82%, respec-
tively (Fig. 3).
On the onset of favourable climatic conditions, the
plant resumed its vegetative and reproductive growth, lat-
ter preceding the former. Thus, the remaining develop-
mental stages were overlapping and occurred concomi-
tantly. Since the plant does not reproduce vegetatively,
PGS 4 (vegetative propagation) was omitted.
End of the rosette growth was marked by emergence
of inflorescence (capitulum/flower head with five ray
florets and numerous disc florets, 5–8 mm in diameter)
as described by PGS 5 (inflorescence emergence) (stage
501–505; Fig. 1). This stage was accompanied by PGS
2 (formation of side shoots) (stage 201–209; Fig. 1).
Although, the main stem as well as the lateral and higher
order branches terminated in a globular capitulum, it was
observed that their elongation succeeded the appearance
of inflorescence. In the beginning, primary inflorescence
appeared in the form of a terminal capitulum, enclosed
between the terminal leaf axils. As the terminal capitulum
developed, main stem began to elongate and secondary
inflorescences started appearing in the axils of the lower
leaves of the stem, producing lateral branches. Simi-
larly, with the development of secondary inflorescence,
lateral branch elongated and produced higher order
inflorescences and branches. Thus, the development of
terminal capitulum was accompanied by production of
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A. Kaur et al. Phenology of Parthenium hysterophorus under varying climate
Tabl e 1 BBCH scale for P. hysterophorus and DAS (days after sowing) recorded for a particular stage in S1, S2, S3 and S4
BBCH Scale DAS (Days After Sowing)
2 digit 3 digit Description S1 S2 S3 S4
Principal growth stage 0: Germination
00 000 Dry seed (achene) 0 0 0 0
01 001 Beginning of seed imbibition – – – –
03 003 Seed imbibition complete – – – –
05 005 Radicle emerged from seed – – – –
06 006 Elongation of radicle, formation of root hairs and lateral – – – –
roots
07 007 Hypocotyl with cotyledons or shoot breaking through – – – –
seed coat
08 008 Hypocotyl with cotyledons or shoot growing towards – – – –
soil surface
09 009 Emergence: cotyledons break through soil surface 14 3 3 4
Principal growth stage 1: Leaf development
10 100 Cotyledons completely unfolded 15 3 3 5
11– 12 101– 102 First pair of true leaves unfolded 35 7 6 9
13 103 Third true leaf unfolded 54 11 11 12
14 104 Fourth true leaf unfolded 57 15 15 15
15 105 Fifth true leaf unfolded 67 16 18 18
16 106 Sixth true leaf unfolded, small rosette developed 75 18 21 22
17 107 Seventh true leaf unfolded 82 19 27 25
18 108 Eighth true leaf unfolded 86 23 30 30
19 109 Ninth true leaf unfolded 89 26 33 34
110 Tenth true leaf unfolded 92 – 40 36
111 Eleventh true leaf unfolded 95 – 49 39
112 Twelfth true leaf unfolded 99 – 60 41
113 Thirteenth true leaf unfolded 103 – – 44
114 Fourteenth true leaf unfolded 106 – – 49
115 Fifteenth true leaf unfolded 110 – – 52
116 Sixteenth true leaf unfolded 115 – – 55
117 Seventeenth true leaf unfolded 119 – – 58
118 Eighteenth true leaf unfolded 122 – – 61
119 Nineteenth true leaf unfolded, rosette enlarged 126 – – 72
Principal growth stage 2: Formation of side shoots
21 201 First lateral branch on the main stem visible 132 32 74 169
22 202 Second lateral branch on the main stem visible 137 34 77 171
23 203 Third lateral branch on the main stem visible 146 37 79 175
24 204 Fourth lateral branch on the main stem visible 155 51 83 179
25 205 Fifth lateral branch on the main stem visible 168 57 95 198
26 206 Sixth lateral branch on the main stem visible 181 64 109 202
27 207 Seventh lateral branch on the main stem visible 195 77 136 227
28 208 Eighth lateral branch on the main stem visible 208 – – 235
29 209 Ninth lateral branch on the main stem visible 220 – – 244
210 Tenth lateral branch on the main stem visible – – – 249
211 Eleventh lateral branch on the main stem visible – – – 253
212 Twelfth lateral branch on the main stem visible – – – 255
Principal growth stage 3: Rosette growth
31 301 Rosette 10% of the maximum diameter 75 – – 39
35 305 Rosette 50% of the maximum diameter 92 – – 61
39 309 Maximum rosette diameter attained 126 – – 126
Principal growth stage 4: Vegetative propagation
(omitted)
Principal growth stage 5: Inflorescence emergence
51 501 Primary (terminal) inflorescence begins to appear, 128 31 72 160
indistinguishable from the developing leaves
55 505 Capitulum clearly visible in the terminal leaf axils, 129 32 74 161
beginning of stem elongation
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Phenology of Parthenium hysterophorus under varying climate A. Kaur et al.
Tabl e 1 Continued
BBCH Scale DAS (Days After Sowing)
2 digit 3 digit Description S1 S2 S3 S4
59 509 Petals visible on the terminal capitulum 131 34 75 164
5 N1 Secondary inflorescence begins to appear on nth lateral – – – –
branch
5 N5 Capitulum clearly visible in the lateral leaf axils, branch – – – –
elongated
5 N9 Petals visible on the capitulum, higher order branches – – – –
produced
Principal growth stage 6: Flowering
60 600 Terminal capitulum completely developed 139 38 81 173
61 601 Beginning of flowering: 10% of capitula developed 162 55 105 194
63 603 30% of capitula developed, maximum stem length 183 66 119 215
achieved
65 605 Full flowering: 50% of capitula developed 192 81 137 232
67 607 Flowering finishing: majority of capitula developed 216 101 255 247
69 609 End of flowering 263 144 291 265
Principal growth stage 7: Development of seeds
71 701 Seeds begin to develop in the terminal flower head 141 45 85 175
79 709 Seeds completely developed in the terminal flower head 143 47 88 177
7 N1 Seeds begin to develop in the flower head on nth lateral branch – – – –
7 N9 Seeds completely developed in the flower head on nth lateral branch – – – –
Principal growth stage 8: Ripening of seeds
81 801 Seeds begin to ripen in the terminal flower head 143 48 89 179
89 809 Seeds fully ripened in the terminal flower head 144 49 91 180
8 N1 Seeds begin to ripen in the flower head on nth lateral branch – – – –
8 N9 Seeds fully ripened in the flower head on nth lateral branch – – – –
Principal growth stage 9: Senescence
97 907 Plant dead and dry 285 169 298 284
subsequent capitula progressively down the stem and lat-
eral branches, in a basipetal manner producing more and
more lateral and higher order branches. Thus, the events
were found to be co-occurring and cannot be recorded
separately. After prolonged rosette stage, inflorescence
in S1 and S4 was emerged 128 and 160 DAS (days after
sowing), respectively. On the other hand, the terminal
capitulum was observed 31 and 72 DAS in case of S2 and
S3 (Fig. 2). Temperature during PGS 5 varied between
23–29∘C, and it played a crucial role in deciding the time
of bolting (Fig. 3a). Humidity patterns (45–72%) varied
between different seasons but did not seem to influence
the emergence of inflorescence (Fig. 3b). Considering,
the importance of photoperiodic phenomenon in initia-
tion of flowering, the average day length (hh:mm:ss) was
observed 7 days prior to the emergence of inflorescence,
and it was recorded to be 13:13:22 during S1, 13:59:43
during S2, 12:08:24 during S3, and 11:40:21 during S4. It
took 7–13 days for the capitulum to develop completely
after its emergence, irrespective of the season.
PGS 6 (flowering) described the proportion of
fully developed capitula, beginning with the terminal
capitulum (stage 601 – 605; Fig. 1). A capitulum was
considered fully developed when all the five ray-florets
appeared. The entire plant development was taken into
consideration for PGS 6 and the reproductive growth
was measured in terms of capitula produced on the
main stem and all the branches. This is because main
stem/lateral branches produce a single capitulum and
give rise to higher order branches. Ray florets and disc
florets within a capitulum emerge simultaneously and
cannot be differentiated. Therefore, rather than applying
a 3-digit code separately for the main stem and lateral
branches, a 2-digit code was used to describe flowering of
the entire plant. The duration of PGS 6 was recorded to
be the longest in S3 (211 days) with 1236.6±92.88 (df-9)
number of capitula produced (Fig. 2c). In case of S1, S2
and S4, this duration was shorter (93–125 days) and the
number of capitula produced was 39–51% higher in the
former than latter (Fig. 2). The PGS 7 (development of
fruit) and PGS 8 (ripening or maturity of fruit and seed)
were overlapping with PGS 6. As soon as the terminal
capitulum became mature, it started developing seeds and
so was the case with the subsequent capitula. Time taken
by a fully developed capitulum in producing the seeds did
not vary significantly among different seasons. Within
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A. Kaur et al. Phenology of Parthenium hysterophorus under varying climate
Figure 1 Significant growth stages observed in the life cycle of P. hysterophorus.
a very short period of time the seeds in the capitula
developed, ripened (turned brown) and dispersed. In the
meantime, elongation and branching of the main stem
were also completed. The maximum plant height were
achieved during S4 [62.4 ±2.03 (df-9) cm], followed
by S1 [48.14 ±0.88 (df-9) cm], S3 [29.4 ±1.03 (df-9)
cm] and S2 [10.28 ±0.278 (df-9) cm]. Similar pattern
was observed for branching as well, with maximum
number of branching in S4 [12.8 ±0.08 (df-9)] and min-
imum in S2 [7.12 ±0.19 (df-9)]. Principal growth stage
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Phenology of Parthenium hysterophorus under varying climate A. Kaur et al.
Figure 2 Variations in the life cycle of P. hysterophorus in S1 (A), S2 (B), S3 (C), and S4 (D).
6 continued for a very long duration and experienced an
array of climatic conditions in all the four seasons. Princi-
pal growth stages 7 and 8, on the other hand, immediately
followed the PGS 5 and therefore witnessed similar tem-
perature and humidity levels. As more of the seeds were
produced and ripened, vegetative growth decelerated
and symptoms of senescence started appearing.
The final stage of the scale was represented by PGS 9
(senescence) when yellowing and drying of leaves, main
stem and branches began from the base of the plant (stage
907; Fig. 1). Although the plant continuously shed the
older leaves throughout its life cycle, however, at this
stage, formation of new leaves impeded. Most of the
capitula were dried and the seeds had been dispersed.
With gradual reduction in the plant moisture content,
main stem and its ramifications were completely dead.
The average temperature (26–33∘C) as well as humidity
(38–74%) was variable during PGS 9 in all the four
seasons (Fig. 3). The shortest life cycle was witnessed by
S2 (169 days), whereas in other seasons it varied from 284
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A. Kaur et al. Phenology of Parthenium hysterophorus under varying climate
Figure 3 Average temperature (A) and average humidity (B) during different growth phases of P. hysterophorus in S1, S2, S3 and S4.
to 298 days. Vegetative phase was the longest in case of S4
(155 days), followed by S1 (113 days), S3 (69 days) and
S2 (28 days). Reproductive phase, on the other hand, was
the longest in S3 (228 days), followed by S1 (158 days),
S2 (139 days) and S4 (125 days) (Fig. 2).
Discussion
The present study was conducted to demonstrate the
acclimatisation potential of P. hysterophorus in response
to the climatic variations. The duration of the life cycle
varied with the changing environmental conditions, with
an average life span being 9 months. Previous studies,
however, reported that plant may complete its life cycle in
an average of 5 months (Kushwaha & Maurya, 2012) or
7months (Nguyen et al., 2017). Batish et al. (2012) sug-
gested that despite being an annual herbaceous weed, P.
hysterophorus possesses a tendency to be perennial. How-
ever, during the given study, only a single flowering spell
was observed in the entire lifetime of the weed and no
perennial behaviour was noticed. Life cycle of the weed
was completed within a year in all the four seasons, but in
view of a prolonged reproductive phase during S3, it can
be suggested that the life cycle may extend over a year, if
more favourable environmental factors are present.
Vegetative phase was prolonged during S1 and S4 and
short in case of S2 and S3, signifying the effect of cli-
matic conditions on the length of vegetative period and
initiation of the reproductive phase. Studies pertaining
to the germination ecology of the weed revealed that
no obvious climatic conditions can limit its germina-
tion (Tamado et al., 2002). Present study has also wit-
nessed that the germination of P. hysterophorus was not
restricted to any particular season, but extremely low
temperature conditions (12∘C) delayed the germination
of seeds during S1. Percent germination was highest dur-
ing S3 which might be a result of combination of high
temperature and high humidity conditions. Further, low
temperature conditions (19–22∘C) influenced the unfold-
ing of cotyledons during S1 and S4 and the appearance
of subsequent leaves during S1. The growth of the weed
was suspended at the rosette stage during S1 and S4,
as a strategy to escape the low temperature conditions
(8–24∘C). Earlier studies have also demonstrated that
plants grown in the temperature regime 22/15∘C stayed
in rosette stage (Tho et al., 2011). This attribute reflects its
remarkable adaptability to survive in the harsh environ-
mental conditions. On the contrary, the weed completed
its vegetative growth rapidly under high temperatures
(29–30∘C), that is during S2 and S3. Low humidity con-
ditions (39%) further shortened the vegetative phase in
S2. In a similar study, it was observed that the warmer
temperatures accelerated the growth of two Australian
biotypes of P. hysterophorus and resulted in a shorter life
span (Nguyen et al., 2017). Earlier studies reported that
the flowering of P. hysterophorus is usually insensitive to
photoperiod and thermal regimes (Mahadevappa, 1997;
Shabbir & Bajwa, 2006), but in the present study PGS
5 (inflorescence emergence) was identified as the most
sensitive stage, responding strongly to the prevailing tem-
perature/photoperiodic conditions. A study by Williams &
Groves (1980) suggested that generally 13 h day light with
warm temperature induces flowering in P. hysterophorus.
Our results corroborate the given statement as flowering
was observed only after an average temperature of 27∘C
and day length of 12:45:28 (hh:mm:ss).
Although, emergence of inflorescence required a
threshold temperature (22–25∘C), but once bolted, the
Ann Appl Biol 171 (2017) 316– 326 323
© 2017 Association of Applied Biologists

Phenology of Parthenium hysterophorus under varying climate A. Kaur et al.
flowering may continue independent of the temperature
and humidity. As a result, the weed can flourish luxuri-
antly throughout the year and this may provide a very
strong competitive advantage over the native species. The
average time interval between anthesis and seed shed-
ding was 15 days, similar to that reported by Kushwaha &
Maurya (2012). Reproductive phase of the weed contin-
ued for 4–8 months, thereby constituting the major part
of its life cycle. Differences in the duration of reproductive
phase were insignificant during all the seasons except
for S3, where reproductive phase was exceptionally
stretched. This could be a possible outcome of favourable
growth conditions at the time of seed germination. Simi-
larly, it was observed that the maximum plant height and
highest number of branches was achieved in S4, followed
by S1 which could be a result of prolonged vegetative
phase during the initial developmental stages.
The study holds significant applications in the field
of weed research and invasion biology. The periodicity
of various events in response to the climatic conditions
provides an estimation of the invasive potential of P.
hysterophorus. It can be concluded that the optimum
temperature and high humidity favours growth of the
weed, but it holds the capacity to survive in any sort
of climatic conditions. This observation is in accordance
with a number of earlier studies (Batish et al., 2012; Tho
et al., 2011; Kohli et al., 2006; Tamado et al., 2002). In
order to escape the temperature or moisture stress, the
weed either delays or paces up its reproductive growth.
In the scenario of climate change, this adaptive behaviour
of plant may prove beneficial. The present study supports
the view that predicted increase in ambient temperature
may enhance the growth and productivity of the weed as
suggested by some recent studies, provided suitable mois-
ture conditions are present (McConnachie et al., 2011;
Kriticos et al., 2015; Bajwa et al., 2016; Nguyen et al.,
2017). Description of the developmental stages in rela-
tion to time can also be utilised for comparing the patterns
of phenology across native and introduced ranges (Jaryan
et al., 2014). More of such studies across temporal and
spatial scales may acquaint the possible trends or shifts
in the invasive behaviour of the plants in response to the
environmental factors. In addition to this, the weak-links
identified in the phenological behaviour of the weed
can be exploited while designing the weed management
programmes. In agricultural fields, herbicidal treatment
is the most reliable strategy for the management of
weeds. Since the success of herbicide treatment protocols
depends on the correct timing of application, identi-
fication of most vulnerable growth stages may prove
effective. In case of P. hysterophorus, weed management
is needed at a pre-flowering stage in order to avoid its
persistent seed banks in the soil. Studies revealed that
most of the chemical treatments and biological control
measures are more effective at the rosette stage (Khan
et al., 2012; Dhileepan, 2003). During high temperature
conditions, the weed demands early control measures
owing to its quick leap to the reproductive phase. Thus, a
suitable period of treatment can be recognised, taking into
consideration the annual life cycle of the weed and pre-
vailing climatic conditions. Moreover, the phenological
documentation is based on long-term observations and is
coded as per a standardised scale therefore, can be utilised
for further research purposes at an international level.
Acknowledgements
A. Kaur is thankful to University Grants Commission,
India, for the financial support. Authors are grateful to
India Meteorological Department, Chandigarh, India, for
providing the meteorological data. Authors declare no
conflict of interest.
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