Phenotypic plasticity: Cause of the successful spread of the genus Potamogeton in the Kashmir Himalaya

Aquatic Botany 120 (2014) 283–289

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Phenotypic plasticity: Cause of the successful spread of the genus Potamogeton in the Kashmir Himalaya Aijaz Hassan Ganie a,∗ , Zafar A. Reshi a , B.A. Wafai a , Sara Puijalon b a b

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 t i c l e

i n f o

Article history: Received 29 January 2014 Received in revised form 18 September 2014 Accepted 19 September 2014 Available online 28 September 2014 Keywords: Morphological characters Phenotypic plasticity Potamogeton Ecological niche breadth

a b s t r a c t Morphological variations observed for a given species according to habitat conditions are generally associated with plant adaptation to local conditions enhancing the plants ability to occupy a wide range of environments, and hence ecological niche breadth. Morphological variations can result from genetic differentiation or from phenotypic plasticity in response to environmental conditions. The present study was undertaken to assess phenotypic variations in the most widespread, as well as one of the largest, 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 plastic origin for the morphological differences observed under natural conditions. Significant differences were observed in morphological characters such as the leaf dimensions, spike and peduncle length; and number of spikes, flowers, fruits and turions/tubers per ramet in both lentic and lotic waters. The results 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 morphological 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 Two different adaptive mechanisms that improve the survival, reproduction and dispersal of plant species are phenotypic plasticity and local adaptation. Phenotypic plasticity is the capacity of a given genotype to express different phenotypes in different environments (Sultan, 2000; Riis et al., 2010). Phenotypic plasticity leads to rapid changes of plant phenotypic characters induced by environmental conditions in the habitat, and adaptive phenotypic plasticity can support the spread of plants into a range of habitats (Riis et al., 2010). In response to environmental stress, many plant species display adaptive plastic responses in developmental, morphological, physiological, anatomical or reproductive traits that can support functional adjustments, possibly compensating for the detrimental effect of stress (Sultan, 2000, 2003). The extent of ‘niche breadth’ may reflect physiological tolerance, local adaptation and/or adaptive phenotypic plasticity (Dudley, 2004). The

∗ Corresponding author. Tel.: +91 09622493652; fax: +91 01942421357. E-mail address: [email protected] (A.H. Ganie). http://dx.doi.org/10.1016/j.aquabot.2014.09.007 0304-3770/© 2014 Elsevier B.V. All rights reserved.

research on phenotypic plasticity has largely attempted to disentangle these three factors, focusing on the genotype–environment interaction (DeWitt and Scheiner, 2004). Potamogeton, one of the largest genera of aquatic angiosperms, is ecologically diverse and distributed in various freshwater (lakes, marshes, ponds, rivers, etc.) and brackish water habitats (Hutchinson, 1975; Kadono, 1982). Residing in aquatic habitats, the species of the genus display, as in many aquatic plant species (Santamaria, 2002), a high degree of variability (Wiegleb, 1988; Kaplan, 2002, 2008). There are both phenotypic variations in response to environmental conditions (phenotypic plasticity) and genotypic variations as a result of isolation and predominant vegetative reproduction (Wiegleb, 1988). The origin of the morphological variations (phenotypic plasticity or genetic differentiation) reported to occur in this genus has not been studied systematically; transplantation experiments conducted by Fryer (1890) 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 environmental factors. The effects of light conditions and water chemistry

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on the leaf shape of P. perfoliatus were studied by Pearsall and Hanbay (1925), and this study revealed that in addition to other factors, light intensity was operating to produce leaf variations in this species. Recently, several studies have described changes in response to environmental conditions. The influence of planting depth on tuber size in P. pectinatus was studied by Ogg et al. (1969) and Spencer (1987); the influence of planting depth on tuber weight in P. gramineus was studied by Spencer and Ksander (1990). At greater depths, individuals of P. gramineus exhibited a decrease in the shoot elongation, rhizome length and the number of flowers, ramets, leaves and floating leaves. Morphological responses to sediment and above-sediment conditions were observed by Kautsky (1987) and Idestam-Almquist and Kautsky (1995) for several morphological traits (e.g., biomass allocation to roots, rhizome length and branching). Water movement has long been considered as one of the primary factors that determines the growth and distribution of submerged aquatic plants in streams and rivers (Chambers, 1991). As early as the 1920s, Butcher (1933) recognised that changes in water flow altered the biomass and species composition of submerged plant communities. The role of water movement in regulating the growth of riverine plants is not as well understood (Chambers, 1991), and very little is known about the plastic responses of aquatic plants with respect to flow conditions (Puijalon and Bornette, 2006; Puijalon et al., 2008). In the present study, phenotypic variation was studied in response to a major environmental factor in aquatic habitats: water movement. Ten species of the genus Potamogeton were studied, forming two sets of species according to their ecological range: Potamogeton crispus, Potamogeton nodosus, P. pectinatus and P. wrightii are widespread (inhabiting both running and standing waters, water bodies with different trophic levels and depths), where as Potamogeton amblyphyllus, Potamogeton berchtoldii, Potamogeton lucens, Potamogeton natans and Potamogeton pusillus are less widespread (with restricted distribution in terms of flow conditions and trophic levels; Ganie et al., 2012). Both sets of species were examined in a common garden growth experiment to assess whether differences in phenotypic characters across different habitats would disappear after transplantation in common conditions, suggesting a plastic origin for the morphological differences observed under natural conditions. We tested the following specific hypotheses: (1) widespread species of the genus Potamogeton (P. crispus, P. nodosus, P. pectinatus and P. wrightii) display larger variations for morphological traits than species with restricted distribution (P. amblyphyllus, P. berchtoldii, P. lucens, P. natans and P. pusillus), (2) these morphological variations observed under natural conditions are due to phenotypic plasticity.

2. Materials and methods 2.1. Study sites The genus Potamogeton represents one of the largest aquatic genera and inhabits a wide variety of habitats in Kashmir Himalaya. Aquatic habitats in the Kashmir valley, India, were extensively surveyed and explored for the collection of Potamogeton plant material. The material was collected in 12 different aquatic habitats. All the study sites were located in the Valley of Kashmir, which is situated on the northern fringe of the Indian sub-continent (33◦ 22 to 34◦ 50 N and 73◦ 55 to73◦ 33 E) and covers an area of approximately 16,000 km2 . The valley is surrounded by the girdling chain of the Himalayan Mountains, namely the Pir Panjal in the south and the Great Himalayan range in the southeast, northeast and west. The climate of the Valley is predominantly temperate, changing from subalpine to alpine in the higher mountains. The Kashmir Valley, called the angler’s paradise, is characterised by a network

of glaciated streams and rivers, as well as alpine, sub-alpine and Valley Lakes that support arich diversity of aquatic vegetation. The details of the exact geographical location of the selected sites and their characteristic features are summarised in Table 1. The study sites can be grouped into two sets according to the overall current conditions: A. Standing water: Anchar Lake (AL); Dal Lake (DL); Manasbal Lake (ML) and Nigeen Lake (NL). B. Running water: Aarpath rivulet of Anantnag (ARRA); Achabal stream, Anantnag (ACSA); Bal-kol, Baramulla (BLBK); Irrigation channel of Sundoo, Anantnag (ICSA); Nagrad stream, Anantnag (NGSA); Nambal stream, Anantnag (NBSA); Spring stream of Sundoo, Anantnag (SSA) and Spring stream of Thajiwara, Anantnag (STA). The water flow of the running water study sites (Table 1) was measured by float and cross section methods following the methods of Kuusisto (1996). 2.2. Species sampled Ten Potamogeton species were sampled: P. lucens L., P. natans L., P. pusillus L., P. amblyphyllus C.A. Meyer (=Stuckenia amblyphylla C.A. Meyer), P. berchtoldii Fieb., P. crispus L., P. nodosus Poir., P. pectinatus L. (=Spartina pectinata (L.) Börner), P. perfoliatus L. and P. wrightii Morong. Not all species could be collected at all the sites; on average, each species was sampled in three or four sites. Three species were sampled only in standing water (P. lucens, P. natans, and P. pusillus), two only in running water (P. amblyphyllus and P. berchtoldii) and five in both habitats (P. crispus, P. nodosus, P. pectinatus, P. perfoliatus, and P. wrightii). Only the well identified individuals of each Potamogeton species were sampled for use in this study. For each species, 25 fully developed individuals (the clonal unit consisted of complete unit of ramets connected by rhizomes) were sampled in each sampling site. These individuals were randomly collected from 10-m2 quadrats (8 quadrats at each site, approximately 20 m apart). 2.3. Measurement of morphological traits The following morphological traits were measured on the sampled individuals: - leaf traits: number of leaves, petiole length, length and breadth of leaf blade were measured on five leaves per ramet of a clonal unit. - flower traits: peduncle length and number of flowers per spike, dimensions of flowers, fruit morphology and number of fruits per spike and per flower. - number of turions per ramet. 2.4. Transplantation experiment For each species, rhizomes were collected from three or four sites depending on the species. For each site and species, three replicate sets of five rhizomes were collected (representing a total of 45 and 60 rhizomes for species collected in three and four sites, respectively) and all the rhizomes were transplanted in 37.5 cm × 30 cm × 30 cm aluminium containers containing 3 kg of sediment (wet mass). The sediment used for all the transplantations was collected from a single water body to provide uniform conditions. For the same reasons, to ensure uniform conditions tap water was used to fill the containers and the water level was maintain at 25 cm above the sediment. The containers were housed at the Kashmir University Botanical Garden (KUBG) for 5 months (1st

Table 1 Salient features of some aquatic sources of Potamogeton species in Kashmir Valley J&K – India. Site (district)

Nature

Location

Altitude (m.a.s.l.)

Latitude (north)

Longitude (east)

Flow of water (litres/second)

Running/standing waters

Urban valley Lake Urban valley Lake Rural valley Lake Urban valley Lake Stream Rivulet

12 km NW of Srinagara 3 km of Srinagar 25 km NW of Srinagar 10 km NW of Srinagar 58 km SE of Srinagar 56 km SE of Srinagar

1595 1595 1590 1595 1610 1600

34◦ 10 55 34◦ 08 48 34◦ 15 26 34◦ 08 50 33◦ 41 03 33◦ 43 09

74◦ 48 10 74◦ 52 51 74◦ 41 26 74◦ 52 55 75◦ 13 12 75◦ 11 04

– – – – 97.26 874

Standing water Standing water Standing water Standing water Running water Running water

Stream

25 km NW of Srinagar

1950

34◦ 03 34

74◦ 25 40

70.20

Running water

74.66

Running water

◦





◦





Stream

56 km of SE of Srinagar

1605

33 42 00

75 11 31

Stream

55 km SE of Srinagar

1605

33◦ 43 09

75◦ 11 04

Stream

56 km SE of Srinagar

1605

33◦ 42 00

75◦ 11 31

◦





◦



277

Running water

69.73

Running water



Stream

57 km SE of Srinagar

1605

33 42 18

75 12 15

72.36

Running water

Stream

56 km of SE of Srinagar

1605

33◦ 42 00

75◦ 11 31

73.66

Running water

A.H. Ganie et al. / Aquatic Botany 120 (2014) 283–289

Anchar Lake (Srinagar) Dal Lake (Srinagar) Manasbal Lake (Bandipora) Nigeen Lake (Srinagar) Achabal stream (Anantnag) Aarpath rivulet of Brakapor (Anantnag) Bal-Kol of Tangmarg (Baramulla) Irrigation canal and spring stream of Sundoo (Anantnag) Nambal rivulet of Barakapora (Anantnag) Nagrad stream of Sundoo (Anantnag) Spring stream of ThajIwara (Anantnag) Spring stream Sundoo (Anantnag)

Salient features of the water body

Source: Survey of India Toposheets (1971) on 1:50,000 scale and present study. a Summer capital of J&K state, India.

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April–31st August) with proper care. The duration of the experiment was designed to enable transplants to develop fully into mature individuals. The quantitative data on morphological traits were measured at the end of experiment.

did not vary significantly under similar conditions (Table 3). Only two species (P. crispus and P. pectinatus) produced fruits after transplantation, and the number of fruits produced under transplanted conditions did not vary significantly (Table 3).

2.5. Statistical analyses 4. Discussion The variation in morphological characters in standing and running waters and across standing and running waters were analysed using one-way ANOVA. Tukey tests were performed to determine post hoc differences between treatment means. All the statistical analyses were performed using SPSS (10) software. 3. Results 3.1. Variation in morphological traits in species between habitats Among the species colonising only habitats with one current condition (standing or running water), P. lucens, P. natans and P. pusillus grew only in standing water (Kashmir valley). The quantitative morphological traits of each of these species did not vary significantly across different sites of standing water habitats (Table 2, P ≥ 0.05). Likewise, the species inhabiting only running water (P. amblyphyllus and P. berchtoldii) also did not show significant variation in the quantitative traits (Table 2, P ≥ 0.05). The species inhabiting both standing and running waters differed significantly in their quantitative traits across these habitats (Table 2). They produced longer and narrower leaves in running water and smaller and broader leaves in standing water (Table 2). However, we observed that in the case of P. pectinatus, P. crispus and P. perfoliatus, the leaves were longer and broader instead of narrower in running water habitats (Table 2). The species with petiolated broad leaves (P. nodosus and P. wrightii) produced longer petioles in running water compared with standing water (Table 2). The mature spike length, peduncle length and number of spikes, flowers, fruits and turions per ramet were significantly higher in standing water (Table 2, P ≤ 0.05). However, an exceptionally small population of P. natans was found near the inlet of Anchar Lake, which is a running water habitat. The plants of this site produced longer and narrower (9.16 ± 0.32 cm long and 2.75 ± 0.78 cm broad) leaves, whereas the plants of the species inhabiting standing water of the same lake produced shorter and broader leaves (7.37 ± 0.27 cm long, 3.35 ± 0.09 cm broad). The petiole length of the inlet site was longer (16.83 ± 0.48 cm long), whereas that of the standing water sites was distinctly shorter (11.66 ± 0.51 cm long). The peduncle length and spike length of both sites, however, were almost the same at both sites (inlet-running water and centre of lake-standing water) of Anchar Lake. 3.2. Transplantation experiment The results of the transplantation experiments revealed that when the plants of the same species collected from different habitats (standing and running waters) were grown under similar conditions, the differences in the morphological traits were no longer observed (Table 3). The length of leaves in P. crispus were 8.38 cm ± 0.17 and 8.47 cm ± 0.01 in the plants grown from the rhizomes of running and standing water habitats, respectively; the trait did not differ significantly (P ≥ 0.05) when transplanted under similar hydraulic conditions. Likewise, the leaf length did not differ significantly in the other sampled species. In addition, the breadth of leaves did not differ significantly (P ≥ 0.05) in all the sampled species when grown under similar environmental conditions in standing water (Table 3). The reproductive traits (mature spike length peduncle length, number of spikes and flowers per plant)

4.1. Morphological differences between habitats of Potamogeton species During the present study, we observed that species of the genus Potamogeton inhabit different habitats: standing water, running water and both standing and running waters, depending on the species. The species occurring in both standing and running waters showed high levels of phenotypic variability across the sampled sites corresponding to contrasting habitat conditions. The species developed distinct morphological traits in response to different environmental conditions, particularly the leaf dimensions and petiole, mature spike and peduncle length as well as the number of spikes, flowers, fruits and turions per ramet. These observed morphological differences possibly support adaptation to different habitat types. The present results demonstrate that the morphological traits of species inhabiting both standing and running water habitats varied significantly across these habitats. The broad- and petiolatedleaved species (P. nodosus and P. wrightii) produced narrower and longer blades as well as longer petioles in running water compared with standing water. These results support the similar observations of Kaplan (2002, 2008), who also reported that the broad- and petiolated-leaved species of Potamogeton produced narrower leaves in running water compared to standing water. In a pond of the Kashmir University Botanical Garden, broad- and petiolated-leaved species of Potamogeton produced narrow leaves when exposed to running water (supplying water by pipes) compared with other locations in the same pond with constant depth (3 m) and availability of light (author personal observation). Narrow and small leaves are considered an adaptation to running water, thus reducing the risk of damage and detachment of leaves from the stem to which they are attached by a small petiole (Ganie et al., 2008, 2012). As drag (horizontal force acting on plants exposed to flow; Vogel, 1994) scales with plant size, a reduced plant size results in the plants partially escaping the mechanical forces caused by flowing water. Puijalon and Bornette (2006) also observed that plant height and leaf area were significantly lower in plants exposed to water current stress. The main morphological traits that enable plants to reduce the drag forces that they experience include a reduced area exposed to fluid action and a shape that reduces the forces encountered for a given area (Puijalon et al., 2011). Niklas (1996) observed that Acer saccharum L. trees on windy sites produce fewer and smaller leaves than on sheltered sites, thus reducing drag and damage. The broad- and petiolated-leaved species of the genus Potamogeton investigated in the present study also appear to present an avoidance strategy against water currents by reducing the size of leaves, which possibly enables these species to colonise such stressful environments. The narrow-, linear- and sessile-leaved species (P. crispus and P. pectinatus) and broad-, sessile-leaved species (P. perfoliatus) produced wider leaves in running water compared with standing water. The same pattern of response was observed by Kaplan (2002, 2008) in many Potamogeton species and by Van Vierssen and Van Wijk (1982) in Zannichellia. In these species, the leaf lamina is directly attached to the stem. Consequently, the production of broader leaves in running water increased the area of the leaf base attached to the stem, which could reduce the risk of leaf detachment. For these species, increased leaf size corresponds to

Table 2 Phenotypic variability in morphological traits of different species of the genus Potamogeton from various habitats and sites of Kashmir Valley (Mean ± SE, One-way ANOVA, Tukey’s test for post hoc). Species

Sites/F, P values

Species growing in standing water P. lucens Anchar Lake Dal Lake Mansbal Lake F, P

Morphological traits Length of leaves (cm)

Breadth of leaves (cm)

Length of apical leaves (cm)

Breadth of apical leaves (cm)

Petiole length (cm)

Mature spike length (cm)

Peduncle length (cm)

No. of spikes per ramet

No. of flowers per ramet

No. of fruits per ramet

No. of turions per ramet

17.75 ± 0.47 17.00 ± 0.56 16.76 ± 0.58 0.89, ns

3.19 ± 0.68 3.21 ± 0.04 3.15 ± 0.77 0.24, ns

– – – –

– – – –

– – – –

4.52 ± 0.13 4.42 ± 0.13 4.32 ± 0.13 0.52, ns

6.92 ± 0.21 6.87 ± 0.23 7.43 ± 0.01 2.19, ns

1.66 ± 0.18 1.60 ± 0.19 1.60 ± 0.19 0.41, ns

60.13 ± 6.87 56.80 ± 6.79 54.66 ± 6.25 0.22, ns

153.73 ± 17.42 153.73 ± 6.79 144.73 ± 6.79 0.73, ns

– – – –

Anchar Lake Dal Lake Nigeen Lake F, P

7.37 ± 0.29 7.40 ± 0.28 7.40 ± 0.28 0.79, ns

3.35 ± 0.09 3.35 ± 0.14 3.40 ± 0.13 0.24, ns

– – – –

– – – –

11.66 ± 0.51 11.48 ± 0.55 11.50 ± 0.54 0.24, ns

4.39 ± 0.08 4.44 ± 0.10 4.44 ± 0.09 0.69, ns

9.75 ± 0.42 9.30 ± 0.39 9.35 ± 0.39 1.18, ns

1.53 ± 0.16 1.33 ± 0.16 1.53 ± 0.16 0.56, ns

50.06 ± 5.90 48.53 ± 5.03 47.60 ± 5.26 1.14, ns

120.13 ± 17.42 120.13 ± 17.42 111.53 ± 10.46 2.83, ns

– – – –

P. pusillus

Anchar Lake Dal lake Mansbal Lake F, P

5.12 ± 0.12 5.12 ± 0.81 5.05 ± 0.13 0.13, ns

0.20 ± 0.15 0.20 ± 0.14 0.20 ± 0.14 0.00, ns

4.10 ± 0.15 3.64 ± 0.14 4.05 ± 0.14 0.00, ns

0.10 ± 0.00 0.10 ± 0.00 0.10 ± 0.00 0.00, ns

– – – –

0.32 ± 0.08 0.31 ± 0.07 0.33 ± 0.001 1.68, ns

7.86 ± 0.90 8.04 ± 0.82 8.13 ± 0.91 0.02, ns

2.44 ± 0.41 2.27 ± 0.47 2.20 ± 0.38 0.83, ns

9.66 ± 1.95 8.30 ± 1.43 8.27 ± 1.50 0.22, ns

1.70 ± 0.47 1.66 ± 0.51 1.63 ± 0.47 0.04, ns

– – – –

17.04 ± 0.32 17.28 ± 0.32 16.86 ± 0.36 0.39, ns 4.77 ± 0.11 4.80 ± 0.12 4.92 ± 0.12 0.43, ns

0.20 ± 0.00 0.20 ± 0.00 0.20 ± 0.00 0.00, ns 0.25 ± 0.01 0.25 ± 0.04 0.25 ± 0.01 0.35, ns

– – – – 3.75 ± 0.14 3.82 ± 0.14 3.75 ± 0.11 0.11, ns

– – – – 0.17 ± 0.00 0.16 ± 0.00 0.16 ± 0.00 0.24, ns

– – – – – – – –

1.39 ± 0.09 1.39 ± 0.09 1.43 ± 0.10 0.81, ns 0.30 ± 0.005 0.30 ± 0.004 0.32 ± 0.008 1.83, ns

4.0 2 ± 0.21 4.0 2 ± 0.26 3.39 ± 0.12 2.19, ns 2.14 ± 0.14 2.77 ± 0.13 2.33 ± 0.14 3.18, ns

1.33 ± 0.12 1.33 ± 0.12 1.33 ± 0.12 0.00, ns 1.80 ± 0.17 1.58 ± 0.17 1.40 ± 0.16 1.31, ns

10.40 ± 0.98 10.46 ± 0.98 10.06 ± 1.03 0.04, ns 7.33 ± 0.87 6.23 ± 0.84 5.40 ± 0.76 1.28, ns

– – – – – – – –

– – – – 9.66 ± 1.27 8.23 ± 0.89 6.00 ± 0.90 3.15, ns

0.72b ± 0.02 0.72b ± 0.02 0.85a ± 0.03 0.88a ± 0.03 20.17, 0.00*

4.11a ± 0.12 4.23a ± 0.10 5.70b ± 0.90 4.39b ± 0.10 20.17, 0.00*

0.46bc ± 0.00 0.43bc ± 0.10 0.55ab ± 0.01 0.59a ± 0.01 2.84, 0.00*

– – – – –

1.70b ± 0.06 1.70b ± 0.06 1.36a ± 0.01 1.37a ± 0.01 20.84, 0.00*

5.71b ± 0.39 5.20b ± 0.35 3.85a ± 0.10 3.76a ± 0.09 16.07, 0.00*

3.73b ± 0.62 3.33ab ± 0.62 1.73a ± 0.37 2.26a ± 0.33 4.09, 0.00*

19.46b ± 3.07 18.40ab ± 3.07 9.93a ± 2.21 12.13ab ± 1.90 3.56, 0.00*

16.20b ± 4.26 17.40b ± 4.09 0.00a ± 0.0 0.00a ± 0.0 10.37, 0.00*

6.26b ± 0.65 5.80b ± 0.69 0.40a ± 0.16 0.90a ± 0.20 40.66, 0.00*

Species growing in running water P. amblyphyllus Nambal stream Nagrad stream Achabal stream F,P P. berchtoldii Nagrad stream Achabal stream Bal-kol stream F, P

Species inhabiting both standing and running waters P. crispus Anchar Lake 9.04ab ± 0.28 Dal Lake 8.80a ± 0.28 9.65b ± 0.14 Nambal stream Aarpath rivulet 9.08b ± 0.13 F, P 77.38, 0.00* P. nodosus

Dal Lake Mansbal Lake Irrigation Channel Spring stream sundoo F, P

8.75a ± 0.81 8.68a ± 0.20 10.02b ± 0.17 10.00b ± 0.15

3.85a ± 0.09 3.40a ± 0.08 3.04aa ± 0.09 3.05aa ± 0.05

– – – –

– – – –

14.61ab ± 0.13 11.30a ± 1.13 17.85b ± 1.43 17.85b ± 1.43

5.96a ± 0.18 5.92a ± 0.15 5.71b ± 0.12 5.66b ± 0.13

7.42a ± 0.32 7.91a ± 0.34 5.62b ± 0.31 6.51ab ± 0.16

1.66 ± 0.27 1.60 ± 0.23 1.33 ± 0.12 1.34 ± 0.11

85.53 ± 16.26 74.20 ± 12.85 66.53 ± 6.63 65.45 ± 9.21

197.20b ± 39.90 190.20b ± 17 0.00a ± 0.00 0.00a ± 0.00

1.60a ± 0.27 1.40a ± 0.25 1.00a ± 0.19 1.00a ± 0.15

11.63, 0.00*

11.54, 0.00*

–

–

16.95, 0.000*

6.95, 0.002**

3.42, 0.038**

0.68, ns

1.16, ns

19.94, 0.000*

1.58, ns

P. pectinatus

Anchar Lake Dal Lake Nambal stream Aarpath rivulet F, P

6.87a ± 0.40 5.52a ± 0.41 12.69b ± 0.32 12.20b ± 0.28 113.28, 0.00*

0.20a ± 0.00 0.20a ± 0.00 0.30b ± 0.00 0.40b ± 0.00 161.65, 0.00*

– – – – –

– – – – –

– – – – –

3.77a ± 0.22 3.52a ± 0.23 3.42b ± 0.22 3.48ab ± 0.19 19.61, 0.00*

7.60b ± 0.56 7.56b ± 0.50 5.45a ± 0.45 6.19ab ± 0.45 5.68, 0.00*

3.66 ± 0.63 3.40 ± 0.71 2.31 ± 0.46 2.80 ± 0.57 1.26, ns

24.40 ± 3.36 21.40 ± 4.41 13.93 ± 3.00 17.66 ± 3.70 1.45, ns

22.0b ± 6.51 28.3 b ± 6.21 0.00a ± 0.00 0.00a ± 0.00 8.40, 0.00*

3.00b ± 0.45 3.06b ± 0.45 0.13a ± 0.09 0.13a ± 0.09 27.9, 0.00*

P. perfoliatus

Mansbal Lake Spring stream Sundoo Spring stream Thajiwara F, P

3.25a ± 0.06 4.13b ± 0.17

1.90a ± 0.03 2.50b ± 0.13

1.58a ± 0.04 3.63b ± 0.12

1.00a ± 0.03 1.88b ± 0.81

– –

1.17a ± 0.04 1.07b ± 0.41

3.35a ± 0.12 3.30b ± 0.82

2.66 ± 0.47 1.60 ± 0.19

21.66a ± 1.40 11.33 b ± 1.36

5.53b ± 2.02 0.00a ± 0.00

1.26 ± 0.04 0.33 ± 0.15

4.02b ± 0.15

2.63b ± 0.11

3.58b ± 0.13

1.89b ± 0.06

–

1.13b ± 0.41

3.32ab ± 0.12

1.60 ± 0.21

11.06b ± 1.51

0.00a ± 0.00

0.40 ± 0.16

10.47, 0.00*

13.28, 0.00*

62.31, 0.00*

63.31, 0.00*

–

21.35, 0.00*

16.02, 0.00*

3.70, ns

16.02, 0.05*

32.13, 0.00*

2.13, ns

Dal Lake Mansbal Lake Nambal stream Aarpath rivulet F, P

9.86a ± 0.37 9.24a ± 0.25 13.28b ± 0.32 13.30b ± 0.30 49.00, 0.00*

2.60b ± 0.07 2.71b ± 0.09 2.08a ± 0.32 2.05a ± 0.31 11.57, 0.00*

– – – – –

– – – – –

6.28a ± 0.50 6.87a ± 0.32 9.58b ± 0.30 9.42b ± 0.31 19.12, 0.00*

4.72 ± 0.19 4.41 ± 0.10 4.24 ± 0.15 4.31 ± 0.13 2.55, 0.084

6.87ab ± 0.30 7.11b ± 0.23 5.87a ± 0.32 5.77a ± 0.31 4.67, 0.01*

2.00 ± 0.27 2.13 ± 0.26 1.80 ± 0.17 1.79 ± 0.11 0.83, ns

86.40 ± 10.34 78.33 ± 10.74 69.80 ± 10.34 70.88a ± 8.01 0.85, ns

135.36b ± 16.39 119.33b ± 16.39 0.00a ± 0.00 0.00a ± 0.00 32.13, 0.00*

1.58 ± 0.33 1.46 ± 0.23 1.13 ± 0.21 1.13 ± 0.21 0.58, ns

P. wrightii

287

Different letters (a, b and c) indicate means that are significantly different among different sites of a species (Tukey test: P < 0.05). N, 25; –, not applicable, ns, not significant. Note: The morphological characters of the species inhabiting either standing or running water do not vary significantly while, these characters very significantly in the plants of the same species across running and standing water habitats. * Significant at <0.001 level. ** Significant at 0.05 level.

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P. natans

288

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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 collected from the running water habitats

Trait

Species

Sites

Sites

Length of leaves (cm)

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

8.38 ± 0.17 8.61 ± 0.13 7.74 ± 0.25 3.12 ± 0.73 9.12 ± 0.12

8.36 ± 0.16 8.68 ± 0.12 7.82 ± 0.23 – 9.08 ± 0.12

8.52 ± 0.01 8.38 ± 0.12 7.84 ± 0.24 3.08 ± 0.68 9.22 ± 0.12

Breadth of leaves (cm)

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

0.78 ± 0.02 3.51 ± 0.08 0.19 ± 0.01 1.66 ± 0.43 2.67 ± 0.05

0.80 ± 0.02 3.65 ± 0.07 0.18 ± 0.0009 – 2.68 ± 0.05

Mature spike length (cm)

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

1.65 ± 0.04 5.52 ± 0.15 4.06 ± 0.17 1.14 ± 0.33 3.90 ± 0.13

Peduncle length (cm)

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

Number of spikes per plant

F

P

8.47 ± 0.01 8.31 ± 0.12 7.68 ± 0.24 3.26 ± 0.71 9.24 ± 0.12

0.109 1.564 0.087 1.845 0.308

0.954 0.208 0.967 0.171 0.820

0.78 ± 0.02 3.48 ± 0.07 0.18 ± 0.01 1.68 ± 0.40 2.64 ± 0.05

0.81 ± 0.02 3.44 ± 0.07 0.19 ± 0.01 1.63 ± 0.41 2.70 ± 0.05

0.264 1.109 0.339 0.356 0.197

0.851 0.353 0.754 0.702 0.898

1.65 ± 0.04 5.53 ± 0.17 4.15 ± 0.16 – 3.68 ± 0.12

1.70 ± 0.04 5.54 ± 0.18 4.05 ± 0.16 1.18 ± 0.30 3.61 ± 0.12

1.68 ± 0.04 5.53 ± 0.14 4.14 ± 0.16 1.16 ± 0.32 3.52 ± 0.12

0.599 0.623 0.095 0.500 2.237

0.618 0.593 0.962 0.610 0.093

5.00 ± 0.19 8.33 ± 0.18 7.93 ± 0.20 3.06 ± 0.97 6.03 ± 0.20

4.99 ± 0.18 8.08 ± 0.17 7.08 ± 0.19 – 6.08 ± 0.18

4.82 ± 0.18 8.24 ± 0.18 7.81 ± 0.20 2.68 ± 0.91 6.00 ± ±0.20

4.88 ± 0.18 8.42 ± 0.18 7.42 ± 0.20 3.03 ± 0.94 6.06 ± 0.20

0.224 0.691 1.50 1.365 0.030

0.880 0.562 0.222 0.267 0.993

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

2.29 ± 0.24 0.57 ± 0.18 2.28 ± 0.45 0.42 ± 0.13 0.42 ± 0.15

3.00 ± 0.27 0.75 ± 0.17 2.68 ± 0.42 – 0.37 ± 0.14

2.86 ± 0.28 0.60 ± 0.18 2.26 ± 0.44 0.31 ± 0.12 0.46 ± 0.14

2.46 ± 0.28 0.40 ± 0.18 2.13 ± 0.44 0.40 ± 0.12 0.46 ± 0.14

0.706 0.645 0.308 0.224 0.072

0.525 0.589 0.820 0.800 0.975

Number of flowers per plant

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

18.64 ± 1.99 15.35 ± 6.17 14.71 ± 2.92 3.50 ± 1.56 17.14 ± 5.99

20.00 ± 1.87 18.28 ± 5.77 17.75 ± 2.74 – 14.93 ± 5.60

18.66 ± 1.93 18.73 ± 5.96 14.80 ± 2.82 2.29 ± 1.46 15.66 ± 5.78

17.69 ± 1.93 16.53 ± 5.95 14.53 ± 2.82 3.51 ± 1.56 14.00 ± 5.61

0.541 0.311 0.260 1.819 0.086

0.656 0.817 0.854 0.175 0.967

Number of fruits per plant

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

2.57 ± 0.56 0 1.50 ± 0.43 0 0

3.31 ± 0.52 0 1.87 ± 0.40 – 0

2.93 ± 0.54 0 1.46 ± 0.42 0 0

2.73 ± 0.54 0 1.60 ± 0.42 0 0

0.353 – 0.201 – –

0.787 – 0.895 – –

Number of turions per plant

P. crispus P. nodosus P. pectinatus P. perfoliatus P. wrightii

1.14 ± 0.28 0.71 ± 0.20 1.57 ± 0.40 0.85 ± 0.22 0.78 ± 0.21

1.25 ± 0.26 0.93 ± 0.19 1.25 ± 0.38 – 0.68 ± 0.19

1.20 ± 0.27 0.66 ± 0.19 1.33 ± 0.39 0.87 ± 0.21 0.80 ± 0.20

1.06 ± 0.27 0.46 ± 0.19 1.33 ± 0.39 0.80 ± 0.21 0.80 ± 0.20

0.083 0.988 0.119 0.033 0.075

0.969 0.405 0.984 0.968 0.973

the strategy of increasing the resistance of plants to the detrimental effects of stress caused by running water by increasing the resistance to breakage. For these species, the morphological traits observed under running conditions could thus represent a tolerance strategy that maximises plant resistance to breakage (Bornette and Puijalon, 2011). The length of mature spikes and peduncles did not vary in the species inhabiting only standing (P. lucens, P. natans, and P. pusillus) or running (P. amblyphyllus and P. berchtoldii) water. However, among the species inhabiting both habitats, these characters varied significantly across these habitats. In floating broad-leaved species (P. nodosus, P. wrightii), the length of the mature spike and peduncle was slightly lower in running water than in standing water. Floating leaves in running water protect the spikes to some extent from the pressure of flowing water. This could explain why the difference in mature spikes and peduncle length was marginal in those species that grow in both running and standing waters. In submerged broad- (P. perfoliatus), linear- (P. crispus) and filiform- (P. pectinatus) -leaved species, the length of the mature spikes was smaller in running water plants compared

with standing water plants. The pressure of flowing water may have impaired the development of spikes (Ganie et al., 2008). Pollux et al. (2006) observed a significantly higher proportion of flowering individuals of Sparganium emersum in a low-velocity river. Strong currents generally have negative impacts on plant development (Nilson, 1987; Gantes and Caro, 2001; Flynn et al., 2002) due to mechanical stress (Riis and Biigs, 2003). Kautsky (1987) observed that the floral number per m2 in P. pectinatus was highest in sheltered populations, and the number decreased from 9 to 6 and 945 to 672 m−2 , respectively, with increasing exposure to waves. Puijalon et al. (2008) observed that flowering was negatively affected by flow in Mentha aquatica. A reduction in flower, seed and/or fruit production has also been observed for several terrestrial species encountering mechanical stress (Niklas, 1998; Cipollini, 1999). In running water habitats, all the species in this study produced a decreased number of fruits and axillary turions per ramet compared with the standing water habitats, and the numbers varied significantly across these habitats. The fast-flowing water impaired the development and maturation of these structures (Ganie et al., 2008). Ecological studies conducted

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by Van Wijk (1988) showed that successful flowering and achene production was not observed in running waters and no achenes were found in the sediments of these waters. Recently, Kaplan (2002, 2008) also reported that plants growing in running water frequently failed to accomplish sexual reproduction and did not produce fruits. However, as revealed during the present study, the production of below-sediment turions (winter buds) in P. nodosus, P. perfoliatus and P. wrightii was not affected by running water stress (did not differ between lotic and lentic conditions). In the case of P. pectinatus, the number of underground tubers produced was significantly higher in standing water compared with running water. This result may be attributed to the hard and stony substratum in the running water, where meristematic branches are the preferred mode of vegetative propagation in place of tubers. 4.2. Relationship between morphological variations and habitat range The results of the transplantation experiment revealed that the differences in morphological traits across different hydraulic conditions are mostly due to phenotypic plasticity and not to genetic differentiation: most traits (e.g., for leaf shape and size, inflorescence size and floral, fruit, turion and tuber number per ramet) did not differ significantly when plants were grown under similar conditions with respect to flow conditions. The plastic responses upon transplantation were also observed in different species of the genus Potamogeton (Kaplan, 2002, 2008). Puijalon and Bornette (2006) and Puijalon et al. (2008) also reported that upon transplantation, different morphological traits in several aquatic plant species with respect to flow did not differ significantly compared to field observations. As hypothesised, the species displaying high variations in morphological traits in response to flow stress, possibly due to phenotypic plasticity, have a diverse habitat range. For some traits, this plasticity may be adaptive and provide them with an advantage to colonise different types of habitats and physical conditions by adopting morphological traits adapted to the specific habitat conditions. During the present study, we observed that the species that are more plastic inhabit a wide range of habitats: for example, P. nodosus, which inhabits both standing and running waters, produced narrower and longer leaves in running water habitats compared with standing water habitats, and the species take on land-form in rice fields and marshy lands. The present study also revealed that the species of the genus Potamogeton exhibit a high level of plasticity in morphological characters, which may allow the fitness of these species to remain constant across diverse habitats and also enable them to inhabit a diverse range of habitats. Acknowledgements We are very thankful to the Head, Department of Botany, University of Kashmir, Srinagar, for providing the necessary facilities. We also gratefully acknowledge the kind help of Dr. Zdenek Kaplan, Institute of Botany, Academy of Science of Czech Republic, who authenticated the identification of several plant specimens. References Bornette, G., Puijalon, S., 2011. Response of aquatic plants to abiotic factors: a review. Aquat. Sci. 73, 1–14. Butcher, R.W., 1933. Studies on the ecology of rivers. I. On the distribution of macrophytic vegetation in the rivers of Britain. J. Ecol. 21, 58–91. Chambers, P.A., 1991. Current velocity and its effect on aquatic macrophytes in flowing waters. Ecol. Appl. 1, 249–257. Cipollini, D.F., 1999. Costs to flowering of the production of a mechanically hardened phenotype in Brassica napus L. Int. J. Plant Sci. 160, 735–741. DeWitt, T.J., Scheiner, S.M., 2004. Phenotypic Plasticity: Functional and Conceptual Approaches. Oxford University Press, Cary, NC.

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