Phenotypic Plasticity: Cause of the Successful Spread of the Genus

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

Department of Botany, University of Kashmir, 190 006 Jammu & Kashmir, India

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.

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

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-

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

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

– – – – 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

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

water and

the

species

scale of

Lake Lake Lake

Lake

features

1:50,000

valley valley valley

valley

Potamogeton on

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)

(Srinagar) (Srinagar)

Sundoo

capital

Tangmarg Lake canal

(Srinagar) rivulet stream

rivulet

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

± ± ± ± ± ± ± ± ± ±

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

± ± ±

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

± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ± ±

same ns ns 0.00 ns ns ns ns ns ns

± ± ± ± ± ±

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).

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

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

(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

different

leaves

* * * * either

0.09 0.05

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

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

± ± ± ± ± ± 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

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

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

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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