Aquatic Botany 120 (2014) 283–289
Contents lists available at ScienceDirect
Aquatic Botany
jou rnal homepage: www.elsevier.com/locate/aquabot
Phenotypic plasticity: Cause of the successful spread of the genus
Potamogeton in the Kashmir Himalaya
a,∗ a a b
Aijaz Hassan Ganie , Zafar A. Reshi , B.A. Wafai , Sara Puijalon
a
Department of Botany, University of Kashmir, 190 006 Jammu & Kashmir, India
b
Université de Lyon, UMR 5023 “Ecologie des hydrosystèmes nature lsetanthropisés”, Université Lyon 1, CNRS, ENTPE, 69622 Villeurbanne Cedex, France
a r a
t i b s
c t
l e i n f o r a c t
Article history: Morphological variations observed for a given species according to habitat conditions are generally asso-
Received 29 January 2014
ciated with plant adaptation to local conditions enhancing the plants ability to occupy a wide range of
Received in revised form
environments, and hence ecological niche breadth. Morphological variations can result from genetic dif-
18 September 2014
ferentiation or from phenotypic plasticity in response to environmental conditions. The present study
Accepted 19 September 2014
was undertaken to assess phenotypic variations in the most widespread, as well as one of the largest,
Available online 28 September 2014
aquatic genera of the Kashmir Himalaya. The study was conducted in 10 species of Potamogeton across
habitats with different water flow types and a common garden experiment was carried out to test for the
Keywords:
plastic origin for the morphological differences observed under natural conditions. Significant differences
Morphological characters
were observed in morphological characters such as the leaf dimensions, spike and peduncle length; and
Phenotypic plasticity
Potamogeton number of spikes, flowers, fruits and turions/tubers per ramet in both lentic and lotic waters. The results
Ecological niche breadth of the transplantation experiments revealed that when plants of the same species collected from different
habitats (standing and running waters) were grown under similar conditions, the differences in the mor-
phological traits were no longer observed at the end of the transplantation period. These results suggest
that the morphological differences observed between the plants sampled under different conditions are
due to phenotypic plasticity and not to genetic differentiation. The capacity of these species to colonise
a wide range of environmental conditions may rely on this high level of morphological variation.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction research on phenotypic plasticity has largely attempted to disen-
tangle these three factors, focusing on the genotype–environment
Two different adaptive mechanisms that improve the survival, interaction (DeWitt and Scheiner, 2004).
reproduction and dispersal of plant species are phenotypic plas- Potamogeton, one of the largest genera of aquatic angiosperms,
ticity and local adaptation. Phenotypic plasticity is the capacity is ecologically diverse and distributed in various freshwater
of a given genotype to express different phenotypes in different (lakes, marshes, ponds, rivers, etc.) and brackish water habitats
environments (Sultan, 2000; Riis et al., 2010). Phenotypic plastic- (Hutchinson, 1975; Kadono, 1982). Residing in aquatic habitats,
ity leads to rapid changes of plant phenotypic characters induced by the species of the genus display, as in many aquatic plant species
environmental conditions in the habitat, and adaptive phenotypic (Santamaria, 2002), a high degree of variability (Wiegleb, 1988;
plasticity can support the spread of plants into a range of habi- Kaplan, 2002, 2008). There are both phenotypic variations in
tats (Riis et al., 2010). In response to environmental stress, many response to environmental conditions (phenotypic plasticity) and
plant species display adaptive plastic responses in developmen- genotypic variations as a result of isolation and predominant
tal, morphological, physiological, anatomical or reproductive traits vegetative reproduction (Wiegleb, 1988). The origin of the morpho-
that can support functional adjustments, possibly compensating logical variations (phenotypic plasticity or genetic differentiation)
for the detrimental effect of stress (Sultan, 2000, 2003). The extent reported to occur in this genus has not been studied system-
of ‘niche breadth’ may reflect physiological tolerance, local adap- atically; transplantation experiments conducted by Fryer (1890)
tation and/or adaptive phenotypic plasticity (Dudley, 2004). The were repeated for several seasons and revealed that the difference
between the states of species and varieties were only temporary.
The species of the genus Potamogeton have been demonstrated
∗ to display morphological variations in response to various environ-
Corresponding author. Tel.: +91 09622493652; fax: +91 01942421357.
E-mail address: [email protected] (A.H. Ganie). mental factors. The effects of light conditions and water chemistry
http://dx.doi.org/10.1016/j.aquabot.2014.09.007
0304-3770/© 2014 Elsevier B.V. All rights reserved.
284 A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289
on the leaf shape of P. perfoliatus were studied by Pearsall and of glaciated streams and rivers, as well as alpine, sub-alpine and
Hanbay (1925), and this study revealed that in addition to other Valley Lakes that support arich diversity of aquatic vegetation. The
factors, light intensity was operating to produce leaf variations details of the exact geographical location of the selected sites and
in this species. Recently, several studies have described changes their characteristic features are summarised in Table 1.
in response to environmental conditions. The influence of plant- The study sites can be grouped into two sets according to the
ing depth on tuber size in P. pectinatus was studied by Ogg et al. overall current conditions:
(1969) and Spencer (1987); the influence of planting depth on tuber
weight in P. gramineus was studied by Spencer and Ksander (1990). A. Standing water: Anchar Lake (AL); Dal Lake (DL); Manasbal Lake
At greater depths, individuals of P. gramineus exhibited a decrease (ML) and Nigeen Lake (NL).
in the shoot elongation, rhizome length and the number of flow- B. Running water: Aarpath rivulet of Anantnag (ARRA); Achabal
ers, ramets, leaves and floating leaves. Morphological responses stream, Anantnag (ACSA); Bal-kol, Baramulla (BLBK); Irrigation
to sediment and above-sediment conditions were observed by channel of Sundoo, Anantnag (ICSA); Nagrad stream, Anantnag
Kautsky (1987) and Idestam-Almquist and Kautsky (1995) for sev- (NGSA); Nambal stream, Anantnag (NBSA); Spring stream of
eral morphological traits (e.g., biomass allocation to roots, rhizome Sundoo, Anantnag (SSA) and Spring stream of Thajiwara, Anant-
length and branching). Water movement has long been consid- nag (STA).
ered as one of the primary factors that determines the growth
and distribution of submerged aquatic plants in streams and rivers The water flow of the running water study sites (Table 1) was
(Chambers, 1991). As early as the 1920s, Butcher (1933) recog- measured by float and cross section methods following the meth-
nised that changes in water flow altered the biomass and species ods of Kuusisto (1996).
composition of submerged plant communities. The role of water
movement in regulating the growth of riverine plants is not as well 2.2. Species sampled
understood (Chambers, 1991), and very little is known about the
plastic responses of aquatic plants with respect to flow conditions Ten Potamogeton species were sampled: P. lucens L., P. natans L.,
(Puijalon and Bornette, 2006; Puijalon et al., 2008). P. pusillus L., P. amblyphyllus C.A. Meyer (=Stuckenia amblyphylla C.A.
In the present study, phenotypic variation was studied in Meyer), P. berchtoldii Fieb., P. crispus L., P. nodosus Poir., P. pectina-
response to a major environmental factor in aquatic habitats: tus L. (=Spartina pectinata (L.) Börner), P. perfoliatus L. and P. wrightii
water movement. Ten species of the genus Potamogeton were Morong. Not all species could be collected at all the sites; on aver-
studied, forming two sets of species according to their ecologi- age, each species was sampled in three or four sites. Three species
cal range: Potamogeton crispus, Potamogeton nodosus, P. pectinatus were sampled only in standing water (P. lucens, P. natans, and P.
and P. wrightii are widespread (inhabiting both running and stand- pusillus), two only in running water (P. amblyphyllus and P. berch-
ing waters, water bodies with different trophic levels and depths), toldii) and five in both habitats (P. crispus, P. nodosus, P. pectinatus,
where as Potamogeton amblyphyllus, Potamogeton berchtoldii, Pota- P. perfoliatus, and P. wrightii).
mogeton lucens, Potamogeton natans and Potamogeton pusillus are Only the well identified individuals of each Potamogeton species
less widespread (with restricted distribution in terms of flow were sampled for use in this study. For each species, 25 fully
conditions and trophic levels; Ganie et al., 2012). Both sets of developed individuals (the clonal unit consisted of complete unit
species were examined in a common garden growth experiment of ramets connected by rhizomes) were sampled in each samp-
2
to assess whether differences in phenotypic characters across dif- ling site. These individuals were randomly collected from 10-m
ferent habitats would disappear after transplantation in common quadrats (8 quadrats at each site, approximately 20 m apart).
conditions, suggesting a plastic origin for the morphological differ-
ences observed under natural conditions. We tested the following 2.3. Measurement of morphological traits
specific hypotheses: (1) widespread species of the genus Potamoge-
ton (P. crispus, P. nodosus, P. pectinatus and P. wrightii) display larger The following morphological traits were measured on the sam-
variations for morphological traits than species with restricted dis- pled individuals:
tribution (P. amblyphyllus, P. berchtoldii, P. lucens, P. natans and P.
pusillus), (2) these morphological variations observed under natural - leaf traits: number of leaves, petiole length, length and breadth
conditions are due to phenotypic plasticity. of leaf blade were measured on five leaves per ramet of a clonal
unit.
- flower traits: peduncle length and number of flowers per spike,
2. Materials and methods dimensions of flowers, fruit morphology and number of fruits per
spike and per flower.
2.1. Study sites - number of turions per ramet.
The genus Potamogeton represents one of the largest aquatic 2.4. Transplantation experiment
genera and inhabits a wide variety of habitats in Kashmir Himalaya.
Aquatic habitats in the Kashmir valley, India, were extensively For each species, rhizomes were collected from three or four
surveyed and explored for the collection of Potamogeton plant sites depending on the species. For each site and species, three
material. The material was collected in 12 different aquatic habitats. replicate sets of five rhizomes were collected (representing a total
All the study sites were located in the Valley of Kashmir, which is of 45 and 60 rhizomes for species collected in three and four
◦
situated on the northern fringe of the Indian sub-continent (33 22 sites, respectively) and all the rhizomes were transplanted in
◦ ◦ ◦
to 34 50 N and 73 55 to73 33 E) and covers an area of approxi- 37.5 cm × 30 cm × 30 cm aluminium containers containing 3 kg of
2
mately 16,000 km . The valley is surrounded by the girdling chain sediment (wet mass). The sediment used for all the transplanta-
of the Himalayan Mountains, namely the Pir Panjal in the south tions was collected from a single water body to provide uniform
and the Great Himalayan range in the southeast, northeast and conditions. For the same reasons, to ensure uniform conditions tap
west. The climate of the Valley is predominantly temperate, chang- water was used to fill the containers and the water level was main-
ing from subalpine to alpine in the higher mountains. The Kashmir tain at 25 cm above the sediment. The containers were housed at
Valley, called the angler’s paradise, is characterised by a network the Kashmir University Botanical Garden (KUBG) for 5 months (1st
A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289 285 waters
water water water water water water water water water water water water
Standing Standing Standing Standing Running Running Running Running Running Running Running Running Running/standing water
of
– – – – 70.20 97.26 74.66 69.73 72.36 73.66 874 277 (litres/second) Flow 10 51 26 55 12 04 40 31 04 31 15 31 48 52 41 52 13 11 25 11 11 11 12 11 ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ 74 74 74 74 75 75 74 75 75 75 75 75 Longitude (east) 48 26 03 09 00 09 00 18 00 55 50 34 08 10 15 08 41 43 03 42 43 42 42 42 ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ ◦ 34 34 34 34 33 33 34 33 33 33 33 33 Latitude (north)
1600 1590 1610 1950 1605 1605 1605 1605 1605 Altitude (m.a.s.l.) 1595 1595 1595
India. a
–
J&K
Srinagar Srinagar
Srinagar Srinagar Srinagar Srinagar
Srinagar Srinagar Srinagar Srinagar Srinagar of of
of of of of
of of of of of Valley SE SE
Srinagar
study. NW NW SE SE NW of SE SE SE of NW
of
km km km km km km km km km km km
body km
Kashmir
Location 12 3 25 10 58 56 25 56 55 56 57 56 present
in
water and
the
species
scale of
Lake Lake Lake
Lake
features
1:50,000
valley valley valley
valley
Potamogeton on
of
Stream Rivulet Stream Salient Nature Urban Urban Rural Urban Stream Stream Stream Stream Stream (1971)
India. sources
state,
aquatic
Toposheets
J&K
spring
of Brakapor Sundoo
ThajIwara some
India (Anantnag) and of of
of (Bandipora)
of Sundoo of
(Anantnag)
of
(Srinagar) (Srinagar)
Sundoo
capital
Tangmarg Lake canal
of
(Srinagar) rivulet stream
rivulet
of
stream Lake Lake
stream stream
Survey
features
(district) 1 Lake
(Baramulla) (Anantnag) (Anantnag) Barakapora (Anantnag) stream (Anantnag) (Anantnag) Summer a Site Anchar Dal Manasbal Nigeen Achabal Aarpath Bal-Kol Irrigation Nambal Nagrad Spring Spring Salient Table Source:
286 A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289
April–31st August) with proper care. The duration of the exper- did not vary significantly under similar conditions (Table 3). Only
iment was designed to enable transplants to develop fully into two species (P. crispus and P. pectinatus) produced fruits after trans-
mature individuals. The quantitative data on morphological traits plantation, and the number of fruits produced under transplanted
were measured at the end of experiment. conditions did not vary significantly (Table 3).
2.5. Statistical analyses
4. Discussion
The variation in morphological characters in standing and run-
ning waters and across standing and running waters were analysed 4.1. Morphological differences between habitats of Potamogeton
using one-way ANOVA. Tukey tests were performed to determine species
post hoc differences between treatment means. All the statistical
analyses were performed using SPSS (10) software. During the present study, we observed that species of the genus
Potamogeton inhabit different habitats: standing water, running
3. Results water and both standing and running waters, depending on the
species. The species occurring in both standing and running waters
3.1. Variation in morphological traits in species between habitats showed high levels of phenotypic variability across the sampled
sites corresponding to contrasting habitat conditions. The species
Among the species colonising only habitats with one current developed distinct morphological traits in response to different
condition (standing or running water), P. lucens, P. natans and environmental conditions, particularly the leaf dimensions and
P. pusillus grew only in standing water (Kashmir valley). The petiole, mature spike and peduncle length as well as the num-
quantitative morphological traits of each of these species did not ber of spikes, flowers, fruits and turions per ramet. These observed
vary significantly across different sites of standing water habitats morphological differences possibly support adaptation to different
(Table 2, P ≥ 0.05). Likewise, the species inhabiting only running habitat types.
water (P. amblyphyllus and P. berchtoldii) also did not show signifi- The present results demonstrate that the morphological traits of
cant variation in the quantitative traits (Table 2, P ≥ 0.05). species inhabiting both standing and running water habitats varied
The species inhabiting both standing and running waters dif- significantly across these habitats. The broad- and petiolated-
fered significantly in their quantitative traits across these habitats leaved species (P. nodosus and P. wrightii) produced narrower
(Table 2). They produced longer and narrower leaves in running and longer blades as well as longer petioles in running water
water and smaller and broader leaves in standing water (Table 2). compared with standing water. These results support the simi-
However, we observed that in the case of P. pectinatus, P. crispus lar observations of Kaplan (2002, 2008), who also reported that
and P. perfoliatus, the leaves were longer and broader instead of the broad- and petiolated-leaved species of Potamogeton produced
narrower in running water habitats (Table 2). The species with peti- narrower leaves in running water compared to standing water. In
olated broad leaves (P. nodosus and P. wrightii) produced longer a pond of the Kashmir University Botanical Garden, broad- and
petioles in running water compared with standing water (Table 2). petiolated-leaved species of Potamogeton produced narrow leaves
The mature spike length, peduncle length and number of spikes, when exposed to running water (supplying water by pipes) com-
flowers, fruits and turions per ramet were significantly higher in pared with other locations in the same pond with constant depth
standing water (Table 2, P ≤ 0.05). (3 m) and availability of light (author personal observation). Narrow
However, an exceptionally small population of P. natans was and small leaves are considered an adaptation to running water,
found near the inlet of Anchar Lake, which is a running water thus reducing the risk of damage and detachment of leaves from
habitat. The plants of this site produced longer and narrower the stem to which they are attached by a small petiole (Ganie et al.,
(9.16 ± 0.32 cm long and 2.75 ± 0.78 cm broad) leaves, whereas 2008, 2012). As drag (horizontal force acting on plants exposed
the plants of the species inhabiting standing water of the same to flow; Vogel, 1994) scales with plant size, a reduced plant size
lake produced shorter and broader leaves (7.37 ± 0.27 cm long, results in the plants partially escaping the mechanical forces caused
3.35 ± 0.09 cm broad). The petiole length of the inlet site was longer by flowing water. Puijalon and Bornette (2006) also observed that
(16.83 ± 0.48 cm long), whereas that of the standing water sites was plant height and leaf area were significantly lower in plants exposed
distinctly shorter (11.66 ± 0.51 cm long). The peduncle length and to water current stress. The main morphological traits that enable
spike length of both sites, however, were almost the same at both plants to reduce the drag forces that they experience include a
sites (inlet-running water and centre of lake-standing water) of reduced area exposed to fluid action and a shape that reduces the
Anchar Lake. forces encountered for a given area (Puijalon et al., 2011). Niklas
(1996) observed that Acer saccharum L. trees on windy sites pro-
3.2. Transplantation experiment duce fewer and smaller leaves than on sheltered sites, thus reducing
drag and damage. The broad- and petiolated-leaved species of the
The results of the transplantation experiments revealed that genus Potamogeton investigated in the present study also appear to
when the plants of the same species collected from different habi- present an avoidance strategy against water currents by reducing
tats (standing and running waters) were grown under similar the size of leaves, which possibly enables these species to colonise
conditions, the differences in the morphological traits were no such stressful environments.
longer observed (Table 3). The length of leaves in P. crispus were The narrow-, linear- and sessile-leaved species (P. crispus and
8.38 cm ± 0.17 and 8.47 cm ± 0.01 in the plants grown from the rhi- P. pectinatus) and broad-, sessile-leaved species (P. perfoliatus)
zomes of running and standing water habitats, respectively; the produced wider leaves in running water compared with stand-
trait did not differ significantly (P ≥ 0.05) when transplanted under ing water. The same pattern of response was observed by Kaplan
similar hydraulic conditions. Likewise, the leaf length did not differ (2002, 2008) in many Potamogeton species and by Van Vierssen
significantly in the other sampled species. In addition, the breadth and Van Wijk (1982) in Zannichellia. In these species, the leaf lam-
of leaves did not differ significantly (P ≥ 0.05) in all the sampled ina is directly attached to the stem. Consequently, the production
species when grown under similar environmental conditions in of broader leaves in running water increased the area of the leaf
standing water (Table 3). The reproductive traits (mature spike base attached to the stem, which could reduce the risk of leaf
length peduncle length, number of spikes and flowers per plant) detachment. For these species, increased leaf size corresponds to
A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289 287 per water
* * 0.65 0.69 0.45 0.45 0.27 0.25 0.09 0.09 0.16 0.20 0.19 0.15
1.27 0.89 0.04 0.33 0.23 0.21 0.21 0.15 0.90 0.16 0.00 turions
± ± ± ±
± ± ± ± ± ± ± ±
ns ns 0.00 ns ns
± ± ± ± ± ± ± ± ± ±
of
standing
– – – – – – – – – – – – – – – – 9.66 8.23 6.00 3.15, 6.26b 5.80b 0.40a 0.90a 40.66, 1.60a 1.40a 1.00a 1.00a 1.58, 3.00b 3.06b 0.13a 0.13a 27.9, 1.26 0.33 0.40 2.13, 1.58 1.46 1.13 1.13 0.58, No. ramet and
per
*
* * *
16.39 16.39 39.90 17
* 17.42 6.79 6.79 10.46 17.42 17.42 4.26 4.09
running 6.21 ± ± ± ±
2.02 6.51 0.0 0.0 0.00 0.00 0.00 0.00 0.00 0.00 0.00 0.00
± ± ± ± ± ± ± ±
0.51 0.47 0.47 0.000 0.00 0.00 0.00 ± fruits
± ±
± ± ± ± ± ± ± ± ± ±
ns ns 0.00 ns b
± ± ±
of
hoc).
across
153.73 153.73 144.73 0.73, 120.13 120.13 111.53 2.83, 1.70 1.66 1.63 0.04, – – – – – – – – 16.20b 17.40b 0.00a 0.00a 10.37, 197.20b 190.20b 0.00a 0.00a 19.94, 22.0b 28.3 0.00a 0.00a 8.40, 5.53b 0.00a 0.00a 32.13, 135.36b 119.33b 0.00a 0.00a 32.13, No. ramet post
per
for
species
* 1.90 3.07
1.36 *
3.07 1.51 1.40 8.01
± ±
6.25 5.03 16.26 6.63 9.21 3.00 3.70 10.74 6.87 6.79 5.26 0.98 12.85 3.36 4.41 10.34 10.34 5.90 0.98 1.03 2.21 ±
test
± ± ± ±
1.95 1.50 0.87 0.84 1.43 0.76 0.05 flowers
b
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
±
same ns ns 0.00 ns ns ns ns ns ns
± ± ± ± ± ±
of
the
60.13 56.80 54.66 0.22, 50.06 48.53 47.60 1.14, 9.66 8.30 8.27 0.22, 10.40 10.46 10.06 0.04, 7.33 6.23 5.40 1.28, 19.46b 18.40ab 9.93a 12.13ab 3.56, 85.53 74.20 66.53 65.45 1.16, 24.40 21.40 13.93 17.66 1.45, 21.66a 11.33 11.06b 16.02, 86.40 78.33 69.80 70.88a 0.85, No. ramet of Tukey’s
per
plants
* 0.62
ANOVA, 0.62 0.37 0.33
±
0.18 0.16 0.16 0.16 0.41 0.47 0.12 0.12 0.12 0.17 0.27 0.12 0.11 0.63 0.46 0.47 0.26 0.11 0.19 0.19 0.38 0.17 0.16 0.23 0.71 0.57 0.19 0.21 0.17 0.27 spikes the
±
± ±
ns ns ns ns ns 0.00 ns ns ns ns
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
of in
No. 1.66 1.60 1.60 0.41, 1.53 1.33 1.53 0.56, 2.44 2.27 2.20 0.83, 1.33 1.33 1.33 0.00, 1.80 1.58 1.40 1.31, 3.73b 3.33ab 1.73a 2.26a 4.09, 1.66 1.60 1.33 1.34 0.68, 3.66 3.40 2.31 2.80 1.26, 2.66 1.60 1.60 3.70, 2.00 2.13 1.80 1.79 0.83, ramet One-way
SE,
±
** * *
length * *
0.16 0.45 0.12 0.30 significantly
0.39 0.31 0.50 0.23 0.35 0.56 0.82 0.10 0.09 0.32 0.34 0.45 0.12 0.32 0.31
0.21 0.26 ± ± ± ±
0.21 0.23 0.01 0.42 0.39 0.90 0.91 0.12 0.14 0.13 0.14 0.39 0.82 0.00 0.00
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
ns ns ns ns 0.038 0.00 0.01 ns ± ±
± ± ± ± ± ± ± ± ± ± ± ± ±
2 2 very (Mean
Peduncle 6.92 6.87 7.43 2.19, 9.75 9.30 9.35 1.18, 7.86 8.04 8.13 0.02, 4.0 4.0 3.39 2.19, 2.14 2.77 2.33 3.18, 5.71b 5.20b 3.85a 3.76a 16.07, 7.42a 7.91a 5.62b 6.51ab 3.42, 7.60b 7.56b 5.45a 6.19ab 5.68, 3.35a 3.30b 3.32ab 16.02, 6.87ab 7.11b 5.87a 5.77a 4.67, (cm) Valley
** * * * characters
0.19
0.12 0.13 0.22 0.41 0.06 0.06 0.41 spike 0.01 0.01 0.18 0.15 0.22 0.23 0.04
± (cm)
0.13 0.13 0.13 0.08 0.10 0.09 0.09 0.09 0.10 0.19 0.10 0.15 0.13 0.08 0.07 0.001 0.008 0.005 0.004 0.00 0.00 0.00
± ± ± ± ± ± ± ± ± ± ± ± ± ±
ns ns 0.002 0.084 ns ns ns Kashmir
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
these
0.05).
of
<
Mature 4.52 4.42 4.32 0.52, 4.39 4.44 4.44 0.69, 0.32 0.31 0.33 1.68, 1.39 1.39 1.43 0.81, 0.30 0.30 0.32 1.83, 1.70b 1.70b 1.36a 1.37a 20.84, 5.96a 5.92a 5.71b 5.66b 6.95, 3.77a 3.52a 3.42b 3.48ab 19.61, 1.17a 1.07b 1.13b 21.35, 4.72 4.41 4.24 4.31 2.55, length P
while, sites
test:
*
and
* 0.13
1.43 1.43 1.13
±
0.51 0.55 0.30 0.31 0.54 0.50 0.32
length
± ± ±
0.000 0.00
± ± ± ± ± ± ±
ns (Tukey
significantly habitats
Petiole – – – – 11.66 11.48 11.50 0.24, – – – – – – – – – – – – – – – – – 14.61ab 11.30a 17.85b 17.85b 16.95, – – – – – – – – – 6.28a 6.87a 9.58b 9.42b 19.12, (cm) vary species
a
various
not of
apical
*
* 0.01 0.00 0.10
of do
0.81 0.06
0.01 0.03
± ± ± (cm)
0.00 0.00 0.00 0.00 0.00 0.00 0.00
from
± ± ± ±
sites 0.00 ns ns
± ± ± ± ± ±
water
– – – – – – – – 0.10 0.10 0.10 0.00, – – – – 0.17 0.16 0.16 0.24, 0.46bc 0.43bc 0.55ab 0.59a 2.84, – – – – – – – – – – 1.00a 1.88b 1.89b 63.31, – – – – – Breadth leaves different
running Potamogeton
* *
apical
or 0.10 0.12 0.13 0.90
0.12 0.10 0.04
of
(cm) 0.14 0.14 0.14 0.11 0.15 0.14 0.00 0.00
among
± ± ± ± ± ± ±
ns ns
± ± ± ± ± ±
genus
– – – – – – – – 4.10 3.64 4.05 0.00, – – – – 3.75 3.82 3.75 0.11, 4.11a 4.23a 5.70b 4.39b 20.17, – – – – – – – – – – 1.58a 3.63b 3.58b 62.31, – – – – – Length leaves the
standing
of
different
*
leaves
* * * * either
0.09 0.05
of
0.11 0.09 0.02 0.02 0.13 0.07 0.00 0.00 0.00 0.09 0.03 0.03 0.08 0.03 0.32 0.31 0.00 0.00
species
± ±
0.68 0.04 0.77 0.09 0.14 0.13 0.01 0.04 0.01 0.15 0.14 0.14 0.00 0.00 0.00 0.00 0.00 0.00 0.00
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
ns ns ns ns ns
± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
significantly
3.19 3.21 3.15 0.24, 3.35 3.35 3.40 0.24, 0.20 0.20 0.20 0.00, 0.20 0.20 0.20 0.00, 0.25 0.25 0.25 0.35, 0.72b 0.72b 0.85a 0.88a 20.17, 3.85a 3.40a 3.04aa 3.05aa 11.54, 0.20a 0.20a 0.30b 0.40b 161.65, 1.90a 2.50b 2.63b 13.28, 2.60b 2.71b 2.08a 2.05a 11.57, Breadth (cm) inhabiting
different are
traits
of
*
that
* * * *
leaves
species 0.32 0.32 0.28 0.30 0.17 0.15 0.28
waters
0.47 0.58 0.32 0.36 0.14 0.17 0.32 0.13 0.15 0.56 0.00 0.81 0.20 0.40 0.41 0.06 0.37 0.25 0.28
of
± ± ± ± ± ± traits ±
0.29 0.12 0.81 0.11 0.12 0.28 0.28 0.13 0.12 0.00 0.00 0.00 0.00
± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±
ns ns ns ns ns the
± ± ± ± ± ± ± ± ±
means
of
running Morphological Length 17.75 17.00 16.76 0.89, 7.37 7.40 7.40 0.79, 5.12 5.12 5.05 0.13, 17.04 17.28 16.86 0.39, 4.77 4.80 4.92 0.43, 9.04ab 8.80a 9.65b 9.08b 77.38, 8.75a 8.68a 10.02b 11.63, 6.87a 5.52a 12.69b 12.20b 113.28, 3.25a 10.47, 9.86a 9.24a 13.28b 13.30b 49.00, 10.00b 4.13b 4.02b (cm)
significant.
and
indicate
not
water
water c)
Channel morphological
characters level.
values
Lake Lake Lake Lake Lake
rivulet rivulet rivulet ns, stream stream
stream stream stream stream
stream stream Lake Lake Lake Lake Lake stream P Lake
stream stream stream standing in level. ,
F and
Lake Lake lake Lake Lake Lake Lake
b
standing running P P P P P P P P P
both
<0.001 0.05 , , , , , , ,
Sites/ Anchar Anchar Anchar Nambal Nagrad Anchar Dal Anchar Mansbal Dal sundoo Sundoo Thajiwara Dal Mansbal F Dal Nigeen F Dal Mansbal F Nagrad Achabal F,P Nambal Nambal F, F Dal Spring Dal Mansbal Irrigation Aarpath F Achabal Bal-kol Spring Mansbal Nambal Aarpath F Aarpath F, Spring F (a, in in
at at
applicable,
variability
morphological
letters
growing growing inhabiting not
–, 2
The
: Significant Significant lucens natans pusillus amblyphyllus berchtoldii crispus nodosus pectinatus perfoliatus wrightii
25; *
Species Species P. P. P. P. P. P. P. Species P. Species P. P. , ** Phenotypic Table Different Note N habitats.
288 A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289
Table 3
Morphological traits of the Potamogeton species from various habitats and sites when grown under similar environmental conditions (Mean ± SE, One way ANOVA, Tukey’s
test for post hoc).
Plants grown from the rhizomes collected from the standing water habitats Plants grown from the rhizomes F P
collected from the running water
habitats
Trait Species Sites Sites
± ± ± ±
Length of P. crispus 8.38 0.17 8.36 0.16 8.52 0.01 8.47 0.01 0.109 0.954
± ± ± ±
leaves (cm) P. nodosus 8.61 0.13 8.68 0.12 8.38 0.12 8.31 0.12 1.564 0.208
P. pectinatus 7.74 ± 0.25 7.82 ± 0.23 7.84 ± 0.24 7.68 ± 0.24 0.087 0.967
P. perfoliatus 3.12 ± 0.73 – 3.08 ± 0.68 3.26 ± 0.71 1.845 0.171
± ±
± ±
P. wrightii 9.12 0.12 9.08 0.12 9.22 0.12 9.24 0.12 0.308 0.820
±
± ± ±
Breadth of P. crispus 0.78 0.02 0.80 0.02 0.78 0.02 0.81 0.02 0.264 0.851
± ± ± ±
leaves (cm) P. nodosus 3.51 0.08 3.65 0.07 3.48 0.07 3.44 0.07 1.109 0.353
P. pectinatus 0.19 ± 0.01 0.18 ± 0.0009 0.18 ± 0.01 0.19 ± 0.01 0.339 0.754
P. perfoliatus 1.66 ± 0.43 – 1.68 ± 0.40 1.63 ± 0.41 0.356 0.702
P. wrightii 2.67 ± 0.05 2.68 ± 0.05 2.64 ± 0.05 2.70 ± 0.05 0.197 0.898
± ± ± ±
Mature spike P. crispus 1.65 0.04 1.65 0.04 1.70 0.04 1.68 0.04 0.599 0.618
± ± ± ±
length (cm) P. nodosus 5.52 0.15 5.53 0.17 5.54 0.18 5.53 0.14 0.623 0.593
P. pectinatus 4.06 ± 0.17 4.15 ± 0.16 4.05 ± 0.16 4.14 ± 0.16 0.095 0.962
±
P. perfoliatus 1.14 0.33 – 1.18 ± 0.30 1.16 ± 0.32 0.500 0.610
P. wrightii 3.90 ± 0.13 3.68 ± 0.12 3.61 ± 0.12 3.52 ± 0.12 2.237 0.093
Peduncle P. crispus 5.00 ± 0.19 4.99 ± 0.18 4.82 ± 0.18 4.88 ± 0.18 0.224 0.880
± ± ± ±
length (cm) P. nodosus 8.33 0.18 8.08 0.17 8.24 0.18 8.42 0.18 0.691 0.562
P. pectinatus 7.93 ± 0.20 7.08 ± 0.19 7.81 ± 0.20 7.42 ± 0.20 1.50 0.222
P. perfoliatus 3.06 ± 0.97 – 2.68 ± 0.91 3.03 ± 0.94 1.365 0.267
P. wrightii 6.03 ± 0.20 6.08 ± 0.18 6.00 ± ±0.20 6.06 ± 0.20 0.030 0.993
± ± ± ±
Number of P. crispus 2.29 0.24 3.00 0.27 2.86 0.28 2.46 0.28 0.706 0.525
± ± ± ±
spikes per P. nodosus 0.57 0.18 0.75 0.17 0.60 0.18 0.40 0.18 0.645 0.589
plant P. pectinatus 2.28 ± 0.45 2.68 ± 0.42 2.26 ± 0.44 2.13 ± 0.44 0.308 0.820
P. perfoliatus 0.42 ± 0.13 – 0.31 ± 0.12 0.40 ± 0.12 0.224 0.800
P. wrightii 0.42 ± 0.15 0.37 ± 0.14 0.46 ± 0.14 0.46 ± 0.14 0.072 0.975
± ± ± ±
Number of P. crispus 18.64 1.99 20.00 1.87 18.66 1.93 17.69 1.93 0.541 0.656
± ± ± ±
flowers per P. nodosus 15.35 6.17 18.28 5.77 18.73 5.96 16.53 5.95 0.311 0.817
plant P. pectinatus 14.71 ± 2.92 17.75 ± 2.74 14.80 ± 2.82 14.53 ± 2.82 0.260 0.854
P. perfoliatus 3.50 ± 1.56 – 2.29 ± 1.46 3.51 ± 1.56 1.819 0.175
P. wrightii 17.14 ± 5.99 14.93 ± 5.60 15.66 ± 5.78 14.00 ± 5.61 0.086 0.967
± ± ± ±
Number of P. crispus 2.57 0.56 3.31 0.52 2.93 0.54 2.73 0.54 0.353 0.787
fruits per plant P. nodosus 0 0 0 0 – –
P. pectinatus 1.50 ± 0.43 1.87 ± 0.40 1.46 ± 0.42 1.60 ± 0.42 0.201 0.895
P. perfoliatus 0 – 0 0 – –
P. wrightii 0 0 0 0 – –
± ± ± ±
Number of P. crispus 1.14 0.28 1.25 0.26 1.20 0.27 1.06 0.27 0.083 0.969
± ± ± ±
turions per P. nodosus 0.71 0.20 0.93 0.19 0.66 0.19 0.46 0.19 0.988 0.405
plant P. pectinatus 1.57 ± 0.40 1.25 ± 0.38 1.33 ± 0.39 1.33 ± 0.39 0.119 0.984
P. perfoliatus 0.85 ± 0.22 – 0.87 ± 0.21 0.80 ± 0.21 0.033 0.968
P. wrightii 0.78 ± 0.21 0.68 ± 0.19 0.80 ± 0.20 0.80 ± 0.20 0.075 0.973
the strategy of increasing the resistance of plants to the detri- with standing water plants. The pressure of flowing water may
mental effects of stress caused by running water by increasing the have impaired the development of spikes (Ganie et al., 2008).
resistance to breakage. For these species, the morphological traits Pollux et al. (2006) observed a significantly higher proportion of
observed under running conditions could thus represent a toler- flowering individuals of Sparganium emersum in a low-velocity
ance strategy that maximises plant resistance to breakage (Bornette river. Strong currents generally have negative impacts on plant
and Puijalon, 2011). development (Nilson, 1987; Gantes and Caro, 2001; Flynn et al.,
The length of mature spikes and peduncles did not vary in the 2002) due to mechanical stress (Riis and Biigs, 2003). Kautsky
2
species inhabiting only standing (P. lucens, P. natans, and P. pusillus) (1987) observed that the floral number per m in P. pectinatus
or running (P. amblyphyllus and P. berchtoldii) water. However, was highest in sheltered populations, and the number decreased
−2
among the species inhabiting both habitats, these characters from 9 to 6 and 945 to 672 m , respectively, with increasing
varied significantly across these habitats. In floating broad-leaved exposure to waves. Puijalon et al. (2008) observed that flowering
species (P. nodosus, P. wrightii), the length of the mature spike and was negatively affected by flow in Mentha aquatica. A reduction
peduncle was slightly lower in running water than in standing in flower, seed and/or fruit production has also been observed for
water. Floating leaves in running water protect the spikes to some several terrestrial species encountering mechanical stress (Niklas,
extent from the pressure of flowing water. This could explain 1998; Cipollini, 1999). In running water habitats, all the species
why the difference in mature spikes and peduncle length was in this study produced a decreased number of fruits and axillary
marginal in those species that grow in both running and standing turions per ramet compared with the standing water habitats,
waters. In submerged broad- (P. perfoliatus), linear- (P. crispus) and the numbers varied significantly across these habitats. The
and filiform- (P. pectinatus) -leaved species, the length of the fast-flowing water impaired the development and maturation of
mature spikes was smaller in running water plants compared these structures (Ganie et al., 2008). Ecological studies conducted
A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289 289
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