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Limnologica

jou rnal homepage: www.elsevier.de/limno

Phenology of the aquatic natans (L.) All. in the Vistula Delta in the

context of climate warming

∗

Agnieszka Gałka, Józef Szmeja

University of Gdansk,´ Department of Ecology, 80-308 Gdansk,´ Wita Stwosza 59,

a r t i c l e i n f o a b s t r a c t

Article history: We determined the phenology and architecture of life stages by observing permanent

Received 20 November 2011

plots in the Vistula Delta (Baltic Sea Region, N Poland) biweekly from 2006 to 2010. Germination of

Received in revised form 25 June 2012 ◦

macro- and was initiated at 12.4 ± 0.2 C water temperature corresponding to early-April

Accepted 6 July 2012

water temperature in the Vistula Delta. Early development of the female gametophyte took place at

◦ ◦

14.2 ± 0.4 C, and late development, with fertilization, at 18.3 ± 1.5 C (April/May). Gametophyte devel-

Keywords:

opment required about 35 days. During the study years the density of early gametophyte populations

Aquatic fern 2 2

was 2522 ± 3327/0.25 m , but only 437 ± 326/0.25 m for late-stage populations. The drop in density was

Climate change

due to ground frost in April. Due to climate warming in the Baltic Sea Region, ground frost occurs less

Clonal architecture

frequently than previously, leading to the expansion of Salvinia natans in the Vistula Delta. Sporophyte

Expansive

Phenology life stages development required about 170 days. The early juvenile sporophyte (Ja) consists of a floating leaf and

◦

Spores a submerged leaf rudiment. Its development took about three weeks at 16.8 ± 1.2 C. The late juvenile

◦

±

sporophyte (Jb) has a fully developed submerged leaf and lasts about four weeks at 18.4 0.7 C. The

2 2

density of Ja populations was 432.7 ± 413.4/0.25 m , but only 9.6 ± 12.9/0.25 m for Jb populations. The

density drop in Jb populations was caused by spring ground frost. A mature individual consists of 2.1 ± 1.1

modules (structural units of a clone), 6.8 ± 4.5 modules for a -producing one. Senile individuals dis-

◦

±

integrated into modules and died at 2.0 1.1 C. For about 160 days from autumn to early spring, Salvinia

natans was found at the bottom of watercourses in the form of .

© 2012 Elsevier GmbH. All rights reserved.

∗

Corresponding author. Tel.: +48 58 520 16 89; fax: +48 58 341 20 16.

E-mail address: [email protected] (J. Szmeja).

0075-9511/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.

http://dx.doi.org/10.1016/j.limno.2012.07.001

Please cite this article in press as: Gałka, A., Szmeja, J., Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the

context of climate warming. Limnologica (2012), http://dx.doi.org/10.1016/j.limno.2012.07.001

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LIMNO-25289; No. of Pages 5 ARTICLE IN PRESS

A. Gałka, J. Szmeja / Limnologica xxx (2012) xxx–xxx 1.e1

Introduction ditches, which construction started in the 13th century and gradu-

ally extended since then (Majewski, 1993). Its fertile soils have long

Salvinia natans is an aquatic fern (Polypodiopsida) of the been exploited extensively for agriculture. The hydrological system

Salviniaceae, closely related to Marsyliaceae (incl. Pilulariaceae), of the delta is closely dependent on its proximity to the Baltic Sea,

which encompasses the genera and Pilularia (Smith et al., the Vistula and its tributaries.

2006). It is an annual pleustophyte consisting of structurally similar The watercourses of the delta are shallow (2.2 ± 1.5 m),

−1

± subunits, some of which are functionally autonomous, so-called slow-flowing (0.1 0.1 m s ), and rich in nitrogen

−3 −3

modules according to Preston and Ackerly (2004) and de Kroon (4.7 ± 4.2 mg TN dm ), phosphorus (0.7 ± 0.4 mg TP dm ) and

−3

et al. (2005). The modules remain connected by the shoot, which organic carbon compounds (3.8 ± 2.3 mg OC dm ). The water

−1 −3

± produces two floating leaves and one submerged leaf. The latter is brackish (53.8 21.3 mg Cl dm ), moderately calcium-

2+ −3

functions as a root (Jampeetong and Brix, 2009) and a fin preventing rich (97.7 ± 18.5 mg Ca dm ), and has high conductivity

−1

± ␮

the plant from capsizing. (828 212 s cm ) and neutral or alkaline pH (7.2–9.2). Most of

Salvinia natans reproduces by sexual and asexual (vegetative) the watercourses are insolated. They warm up quickly in spring

means. Sporocarps with micro- and macrosporangia are the organs and are often overheated in summer, while in winter only the

of sexual reproduction. Each macrosporangium produces 32 spores, shallowest might freeze to the bottom (Szmeja et al., 2012).

only one of which survives (macrospore 70–75 ␮m in diameter), Ground frost in the spring months (mid March to April) elim-

while the microsporangium contains 64 microspores, each about inates some of the already germinating spores and the youngest

20 ␮m in diameter (Lawalrée, 1964). The macrospore develops into development stages of Salvinia (Szmeja et al., 2012). March is the

the female gametophyte, and the into the male one. coldest and most thermally variable spring month (Table 1). In the

◦

Fertilization takes place on the water surface, producing a zygote study years March temperature ranged from −5.1 to +20.1 C; there

± ±

which becomes the sporophyte, which is clonal in structure. Vege- were 13.6 8.0 days with ground frost and 17.0 8.7 days with-

tative reproduction entails fragmentation of the mature clone. out. The highest number of days with sub-zero temperatures was

In the delta of the Vistula, which flows into the south of the Baltic recorded in March 2006 (26) and 2010 (17); in the other years

Sea, Salvinia natans (hereafter Salvinia) is an indigenous species there were 2 (2007), 12 (2008) and 13 (2009) sub-zero days. In

◦

occurring with varying abundance for at least 1500 years (Swi´ eta-˛ April the temperature range was narrower (−3.8–+25.3 C) and

Musznicka et al., 2011). From the mid-19th century to the end there were fewer days with ground frost (4.4 ± 2.2). May was

of the 20th century, the plant grew in few watercourses, where warmer and more thermally stable than April. Mean annual air

◦

it formed sparse populations. In the first decade of the 21st cen- temperature was 8.7 ± 7.2 C. The warmest years were 2007 and

tury it was already occurring in every watercourse and formed 2008, while 2009 and 2010 were slightly cooler. In every year the

very numerous populations. Between 1990 and 2004, simultane- spring and summer seasons were warm, and autumn was thermally

ously to the spread in the Vistula Delta, similar phenomena were quite stable. Frosty winters occurred only twice, in 2005/2006 and

recorded in other regions of Europe, such as the German federal 2009/2010.

states of Baden-Württemberg and Rhineland-Palatinate (Wolf and

Schwarzer, 2005). The plant rarely disperses beyond the hydrolog-

Population sampling and statistical analyses

ical systems it occupies. As a result, its principal mode of expansion

is to increase the abundance of its populations.

We examined the features of Salvinia development stages, their

According to Szmeja et al. (2012), the expansion of Salvinia in

life span and the phenology of clonal architecture in permanent

the Vistula Delta was caused by a rise of mean annual and seasonal

plots in the River Tuga. For five consecutive years (2006–2010) we

air (and water) temperature. Climate warming is associated with an

studied ten plots (0.5 m × 0.5 m quadrats) biweekly from the turn of

increase of the intensity and frequency of the positive phase of the

×

March/April to November. Each plot consisted of 25 0.1 m 0.1 m

North Atlantic Oscillation (NAO), during which warmer, moister

quadrats. The plots, interconnected and anchored, floated on the

air has been flowing from above the Atlantic to North-western

water surface. On each sampling occasion we counted sporophyte

Europe, Scandinavia and the Baltic Sea Region since 1989, especially

development stages (juvenile, mature, spore-producing, subsenile

in the colder seasons (Hurrell, 1995, 1996). Consequently, March

and senile) and measured the temperature at the water surface.

and April are warmer in the Vistula Delta, and temperature varia-

In other studies the same plots were used to record abundance,

tion in these months is lower (Szmeja et al., 2012). We hypothesize

survival rates and mortality in the population (Szmeja et al., 2012).

that these changes in weather conditions activates Salvinia spores

−3

We observed gametophyte development in 0.5 dm surface

earlier in the year, prolongs the growth season, and increases the

water samples taken every seven days from the River Nogat from

survival rate of individuals, especially in the early spring cohort.

April to July in 2009 and 2010. In total, 24 water samples with about

In this study we investigated the species’ life cycle in relation to

1000 gametophytes were analyzed. The terminology of gameto-

temperature conditions, in particular the length of the winter dia-

phyte development stages follows Schneller (1976) and Schwarzer

pause, spore germination temperature in watercourses in spring,

and Wolf (2005).

features of the consecutive development stages of the gametophyte

The data from the permanent plots in the River Tuga was ana-

and sporophyte, water temperature at those stages, and the pattern

lyzed to reveal the phenology of clonal architecture. We assume

of clone formation and growth.

that a clone is made up of iterative structural subunits, so-called

Methods modules according to Preston and Ackerly (2004) and de Kroon

et al. (2005). A single module also consists of iterative subunits

called ramets. Each ramet is built of two floating leaves and one

Study area

submerged leaf and the spore-producing stage (). On each

observation day we counted the modules in a clone and the ramets

The studies were conducted in 2006–2010 in the delta of the

in the modules. In total, 200 clones, 600 modules and almost 2000

River Vistula (N Poland), which flows into the Baltic Sea (Fig. 1).

ramets were considered.

The delta was formed towards the end of the Pleistocene, under-

The expansion rate of modules was determined from observa-

went numerous transformations in the Holocene, and today is

2 tion of the permanent plots and by culturing 100 modules in a

wedge-shaped with a surface area of 1700 km . The area is char-

◦

thermostatic chamber on Streiber medium (pH 5.9) at 20 C and

acterized by a dense network of polders, canals and drainage

Please cite this article in press as: Gałka, A., Szmeja, J., Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the

context of climate warming. Limnologica (2012), http://dx.doi.org/10.1016/j.limno.2012.07.001

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Fig. 1. Location of the study area in the Baltic Sea Region (left) and outline of the Vistula Delta (right).

−1

light intensity typical of mid-July (89.6 ± 0.8 ␮mol s , 16D/8N). gametophytes are formed. The postponed formation of the gameto-

Newly formed modules were counted every five days during the phytes makes them less susceptible to freezing. The winters of 2008

experiment. These data were used to calculate the module growth and 2009 were fairly warm and consequently the gametophytes

coefficient: the ratio of the number of modules on a measurement appeared earlier than in 2010, when the winter was frosty.

day to the number of modules in the previous measurement. Female gametophyte development can be divided into two

The results for individuals, populations and habitat were ana- stages (Fig. 2): an early phase lasting from the beginning of

◦

±

lyzed by standard statistical methods, using Statistica for Windows April (water temperature 12.4 0.2 C) to the end of that month

◦ ◦

± ±

v. 7. The significance of differences at p < 0.05 was determined by (14.2 0.4 C), and a late phase (April/May, 18.3 1.5 C) last-

ANOVA with U Mann-Whitney test. ing about 15 days (Fig. 3). In the study years, the density of

2

late-gametophyte populations was 437 ± 326/0.25 m , an order

Results of magnitude lower than that of early-gametophyte populations

2

(2522 ± 3327/0.25 m ; p = 0.0046). The density drop in the late-

gametophyte populations was due to high mortality of the early

Life stages

development stages during April ground frost (Table 1). The male

In winter, Salvinia natans occurs in the form of macro- and gametophyte developed at the turn of April/May. The female game-

microspores lying on river bottoms, at first in sporocarps, from tophyte produces archegonia, and the male produces antheridia.

which they are released gradually as the sporocarp walls disinte- After fertilization a zygote is formed, which in turn gives rise to the

3

grate (7.8 ± 13.5 macrospores per 50 cm sediment sample). Winter sporophyte.

diapause lasts from autumn to early spring for about 160 days. The following sporophyte development stages were differenti-

As soon as the ice cover has melted (usually in the second half of ated: juvenile (J), mature (M), spore-producing (s-p), subsenile (SS)

March or first decade of April), spores emerge on the water surface and senile (S). In the first three the number of modules in a clone

◦

and germinate. Spore germination is initiated at 12.4 ± 0.2 C water increased, and in the last two it decreased. The early juvenile stage

temperature. Germinating macrospores give rise to female game- (Ja) consisted of a floating leaf and the bud of a submerged leaf;

tophytes, and germinating microspores to the male gametophytes. it appeared in the first half of May and lasted about three weeks

◦

±

From the beginning of April to mid-May, about 45 days, they are at 16.8 1.2 C water temperature (Fig. 3). The late juvenile stage

found in the surface water film, which is very susceptible to air (Jb) had a fully formed submerged leaf, appeared in mid-June and

◦ 3

±

temperature fluctuations. The timing of spore activation depends lasted about four weeks at 18.4 0.7 C. In 0.5 dm surface water

on temperature. The longer a river is covered with ice, the later the samples randomly collected for five consecutive years there were

Table 1

Mean and range of air temperature in 2006–2010 growth seasons in the Vistula Delta (data from the Polish National Hydrological and Meteorological Service).

◦

Year Temperature [ C]

March April May spring summer autumn year

−0.9 ± 4.5 7.3 ± 2.3 13.3 ± 2.9 12.0 ± 4.6 18.3 ± 2.5 8.0 ± 2.6 8.8 ± 8.7

2006

−15.1–+14.0 −2.3–+17.3 2.1–24.4

7.1 ± 2.9 8.0 ± 3.9 14.3 ± 5.5 13.3 ± 5.0 16.3 ± 2.1 4.3 ± 4.0 9.3 ± 6.8 2007

−3.5–+16.7 −3.8–+23.3 −3.5–29.1

3.7 ± 3.3 8.2 ± 3.1 12.7 ± 2.6 12.0 ± 4.0 16.3 ± 2.9 5.5 ± 4.3 9.3 ± 6.1

2008

−6.8–+15.9 −0.3–+20.9 −0.7–24.7

2.4 ± 1.9 10.3 ± 4.3 12.4 ± 3.0 0.6–25.1 12.0 ± 2.0 17.2 ± 1.9 4.0 ± 4.4 8.4 ± 7.3 2009

−5.1–+12.7 −3.3–+25.3

3.0 ± 5.7 7.7 ± 3.0 11.2 ± 2.6 1.7–23.7 11.6 ± 4.3 16.6 ± 4.3 4.6 ± 3.9 8.7 ± 6.9 2010

−10.3–+20.1 −3.1–+25.0

Please cite this article in press as: Gałka, A., Szmeja, J., Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the

context of climate warming. Limnologica (2012), http://dx.doi.org/10.1016/j.limno.2012.07.001

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Fig. 2. Female gametophyte development stages: early (left) and late (right).

± ±

432.7 413.4 Ja stages in the first half of May, but only 9.6 12.9 Jb reproduction in the Vistula Delta generally lasted ten weeks, five

stages by mid-June (p = 0.0003). High mortality in cohort Ja, caused generations of such offspring were produced per year.

by ground frost in the first half of May was responsible for the huge The subsenile stage (SS) appeared in the third decade of

decline in Jb population density (Table 1). September. Its leaves were yellow, a symptom of ageing. From mid-

◦ ◦

The mature individual (M) had a simple clonal structure and October (6.7 ± 1.2 C) to the end of October (2.0 ± 1.1 C) the senile

± ◦ appeared from the beginning of July (19.6 1.4 C) to the end of stage (S), characterized by brown leaves, was dominant. During this

◦

August (19.9 ± 0.6 C). The stage that followed (spore-producing, period the gradually died off, and winter diapause, which

s-p) was a fully formed clone consisting of 6.8 ± 4.5 modules and generally lasts about 160 days, set in. Then Salvinia occurred as

15.8 ± 6.2 sporocarps. It was found from the end of August to the sporangia (SP) and spores (s) (Fig. 3).

end of September and reproduced asexually by division. Numerous

divisions and rapid growth of offspring could increase popula- Phenology of clonal architecture

tion abundance in August by as much as tenfold. Regardless of

Mature and spore-producing Salvinia was clonal in structure,

clone fragmentation, each mature module gave rise to 4.2 ± 3.7

formed in the process of adding new modules arranged radially

daughter modules which, having separated, intensified vegetative

around the central (oldest) part of the plant. The older the clone,

reproduction. In August and September a new generation of vege-

the more complex was its structure. The clone was net-like and

tative offspring formed every two weeks on average. As vegetative

consisted of modules that grew like lateral branches in vascular

plants. Each module was linear in structure and made up of subunits

called ramets. Clones expanded by increasing the number and size

of modules, as well as the number and size of ramets in the modules.

The process took about 130 days from mid-May to late September.

Clonal development was divided into three stages (early, sub-

optimal and optimal) and clonal disintegration into two stages

(subterminal and terminal) (Fig. 4). The early stage consisted of one

module composed of 2.6 ± 0.7 ramets. It appeared from mid-May

± 2

to the end of June and had a surface area of 1.0 0.3 cm . In the sub-

optimal stage the clone consisted of 2.1 ± 1.1 modules and 5.6 ± 4.1

ramets, lasted 7 weeks (from July to mid-August), and was larger

2

than the previous (3.3 ± 2.5 cm ; p = 0.0017). In the next (optimal)

stage the clone was composed of 6.8 ± 4.5 modules and 17.2 ± 11.8

ramets. It appeared at the turn of August/September and was the

2

largest (21.1 ± 14.4 cm ). The clone extended very quickly in this

stage. The module growth coefficient (ratio of number of modules

on measurement day to number of modules at previous measure-

ment) was 0.6 modules/day. In this clonal development stage a

new module was formed every two days on average. In the fourth

(subterminal) stage at the beginning of October the clones disinte-

grated into pieces, the number of modules (3.5 ± 2.1) and ramets

(14.6 ± 11.0) in clones decreased, and consequently their surface

± 2

area fell to 17.9 13.5 cm . In the fifth (terminal) stage towards

the end of October, the clone usually had one module (1.1 ± 0.6)

2

consisting of 5.2 ± 2.0 ramets and a surface area of 6.3 ± 3.5 cm

and gradually disintegrated.

Fig. 3. Diagram of the Salvinia natans annual development cycle. Abbreviations:

SP: sporocarp; s: spore, Ma: macrospore, Mi: microspore, GM: male gametophyte. Discussion

Female gametophyte development stages: GFa: early, GFb: late. Sporophyte devel-

opment stages: J: juvenile; Ja: early; Jb: late, M: mature; s-p: spore-producing;

The expansion of Salvinia natans populations in the water-

SS: subsenile; S: senile. Roman numerals indicate consecutive months, and Arabic

numerals on the circumference of the circle indicate the week of the year. courses of the Vistula Delta is clearly associated to the positive

Please cite this article in press as: Gałka, A., Szmeja, J., Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the

context of climate warming. Limnologica (2012), http://dx.doi.org/10.1016/j.limno.2012.07.001

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Fig. 4. Clonal architecture in development (1–3) and disintegration (4, 5) stages. Explanations: 1 (early), 2 (suboptimal), 3 (optimal) development stages; 4 (subterminal), 5

(terminal) disintegration stages.

phase of the North Atlantic Oscillation (NAO) in the Baltic Sea subunits of the clone (Fig. 4). Each module consists of morpholog-

Region (Szmeja et al., 2012). Since 1989, warmer and moister air ically similar subunits (ramets). A young clone has one module,

has been moving from above the Atlantic to north-western Europe, and then it spreads radially to form a multi-module net-like struc-

especially in the colder seasons (Hurrell, 1995, 1996). As a result, ture. The clonal architecture of S. natans resembles what Harper

from 1989 to the first decade of the 21st century the air tempera- and Bell (1979) described in terrestrial plants. Its clonal geom-

ture rise in the Baltic Sea Region has been higher than in many other etry is no accident: new modules are arranged radially, which

◦

parts of the Northern Hemisphere. It is also 0.22 C/decade higher facilitates occupation of free space. New ramets grow apically in

than the global temperature increase (Marsz and Styszynska,´ 2010). turn, which increases the surface for active uptake of biogenic sub-

In this study we sought to analyze the development cycle of stances. This also favours the massive development of populations.

Salvinia natans in the context of contemporary climate change in (Room, 1983) occupies space in a similar way. Here

the Baltic Sea Region. From the 19th century to the end of the 20th we note that S. natans clones also undergo autofragmentation, as in

– for 150 years – this plant was very rare in the Vistula Delta. It Myriophyllum spicatum (Smith et al., 2002). In the optimal phase of

was always found in the same watercourses, forming sparse pop- clonal development (Fig. 4), autofragmentation entails separation

ulations. By around 2005 it was already very abundant in every of offspring modules from the clone’s marginal sections, boosting

watercourse of the delta (Szmeja et al., 2012). vegetative reproduction. In the subterminal and terminal stages

Climate warming favours the development of Salvinia natans. of the clone’s disintegration, autofragmentation is a symptom of

Early spring (April, May) is a crucial period, when populations form ageing and death of the clonal structure.

young gametophytes (April) and early sporophytes (May). They are

tiny, delicate (Figs. 2 and 3), and susceptible to freezing. In the study

◦ Acknowledgements

area, young gametophytes appeared at 12.4 ± 0.2 C water tem-

perature, as in Rhineland-Palatinate (Wolf and Schwarzer, 2005).

We thank our colleagues for discussions and valuable comments

The temperature of gametophyte activation is higher than for

on the manuscript. Michael Jacobs helped edit the English transla-

other aquatic plants. For example, seedlings emerge at tempera-

◦

tion. The paper is based on the results obtained in research under

ture slightly above 5.0 C in Zostera marina (Abe et al., 2008), at

◦ ◦

Project N N304 411638 funded by the Polish Ministry of Science

8.0 C in Trapa natans (Kurihara and Ikusima, 1991) and at 8–12 C

and Higher Education.

in Luronium natans (Szmeja and Bazydło, 2005). For S. natans the

sporing period took about 60 days, as long as in terrestrial

(Sawamura et al., 2009).

◦ References

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Please cite this article in press as: Gałka, A., Szmeja, J., Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the

context of climate warming. Limnologica (2012), http://dx.doi.org/10.1016/j.limno.2012.07.001

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