Biosystems - An International Journal Dealing with all Aspects of Plant Biology Official Journal of the Societa Botanica Italiana

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Early spring warming as one of the factors responsible for expansion of aquatic natans (L.) All. in the Vistula delta (south Baltic Sea coast)

J. Szmeja, A. GałKa-Kozak, A. Styszyńska & A. Marsz

To cite this article: J. Szmeja, A. GałKa-Kozak, A. Styszyńska & A. Marsz (2016) Early spring warming as one of the factors responsible for expansion of aquatic fern Salvinia natans (L.) All. in the Vistula delta (south Baltic Sea coast), Plant Biosystems - An International Journal Dealing with all Aspects of Plant Biology, 150:3, 532-539, DOI: 10.1080/11263504.2014.987189 To link to this article: http://dx.doi.org/10.1080/11263504.2014.987189

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Download by: [University of Florida] Date: 16 February 2017, At: 15:13 Plant Biosystems, 2016 Vol. 150, No. 3, 532–539, http://dx.doi.org/10.1080/11263504.2014.987189

ORIGINAL ARTICLE

Early spring warming as one of the factors responsible for expansion of aquatic fern Salvinia natans (L.) All. in the Vistula delta (south Baltic Sea coast)

J. SZMEJA1, A. GAŁKA-KOZAK1, A. STYSZYN´ SKA2, & A. MARSZ2

1Department of Plant Ecology, University of Gdan´sk, ul. Wita Stwosza 59, PL 80-308 Gdan´sk, and 2Department of Meteorology and Nautical Oceanography, Gdynia Maritime University, ul. Sędzickiego 19, PL 81–374 Gdynia, Poland

Abstract From the mid-19th century to the end of the 20th century, Salvinia natans (L.) All. occurred very rarely in the Vistula Delta (northern Poland), but from the beginning of the 21st century it was present in almost every watercourse and had formed very abundant populations. We examined the influence of temperature on the abundance of this plant and the efficiency of macrospore germination. Field work was carried out in 10 permanent plots every 14 days for 5 years. Macrospores germinate at water temperature of 12.4 ^ 0.28C or higher; at 208C they develop more effectively than at 158C. Usually, ice cover on the rivers melts in the second half of March. At this time, macro- and microspores emerge on the water surface and germinate in April. They occur in the water surface film at 15.1 ^ 2.48C and massively die during spring frost. After 1989, March and April mean temperature in the Vistula Delta rose by 1.68C versus 1901–1988, and by 1.98C versus 1851–1988. In 1951– 1988, the mean temperature for March and April was þ4.68C and was characterized by considerable interannual variation

(SD ¼ 1.64), whereas in 1989–2009, it rose to þ5.78C and the variation range narrowed (SD ¼ 1.24). We found that macrospores are active earlier during the warm and mild summers, germination is more effective, survival of young stages is higher, the growing season is longer, and the number of vegetative offsprings in a year is larger.

Keywords: Germination, reproduction, vegetative propagation, clonal plant, North Atlantic Oscillation

Introduction 7th and 8th, sporadically from the 9th to the 15th, and probably absent from the 16th to the 18th Indigenous species undergo expansion as frequently centuries. In the mid-19th century, Salvinia occurred as alien ones do (Pieterse & Murphy 1990, Barrat- Segretain et al. 2002), but because the ecological or sparsely in seven watercourses (Klinggraeff 1858), socio-economic consequences are of less conse- the same ones and at a similar level of abundance as quence, their expansion is much less studied. One at the end of the 20th century (Markowski et al. indigenous species increasing the number of its sites 2004). and the size of populations is the aquatic fern Due to the dominance of very fertile soils in the Salvinia natans (L.) All. The spread of this plant has Vistula Delta, its watercourses have always been very been noted in Jammu and Kashmir (Zutshi & Vass fertile (Drwal 2002). They were of the same 1971), the Oder River (Spałek 2006), Rhineland- character when the plant formed very small and Palatinate, and Baden-Wu¨ rttemberg (Wolff & scattered populations; during that time, the system of Schwarzer 2005). Since the end of the 20th century, agricultural soil use and the frequency of floods in a similar phenomenon has been observed in the this area remained similar. In our opinion, the reason Vistula Delta. Palaeoecological studies presented by for the expansion may not be the floods. According to S´wie˛ta-Musznicka et al. (2011) indicate that Salvinia Makowski and Tomczak (2002), between 1328 and natans (hereinafter referred to as Salvinia)has 2000, more than 150 floods were recorded in the occurred in the delta for at least 1500 years: sparsely Vistula Delta. Moreover, in floristic notes published in the 5th and 6th centuries, on a massive scale in the from the mid-19th century to the end of the 20th

Correspondence: Jo´zef Szmeja, Department of Plant Ecology, University of Gdan´sk, ul. Wita Stwosza 59, PL 80-308 Gdan´sk, Poland. Tel: þ48 58 523 61 06. Email: [email protected] q 2014 Societa` Botanica Italiana 2 Early spring warming and expansion of Salvinia 533 century, there is no evidence or suggestion that the century, Salvinia has appeared in almost every abundance of Salvinia in the delta is regulated by the watercourse in the Vistula Delta and has formed fertility of watercourses or by flooding. very abundant populations. The expansion of Salvinia in the Vistula Delta started at the end of the 1990s (Gałka & Szmeja Study plant 2012). In 2005, populations of this plant were abundant enough to clog the delta’s extensive hydro- The selected plant is an annual aquatic fern (Smith regulation system. As a result, by 2005 Salvinia et al. 2006) which occurs in areas under the sub- occurred in almost every river, canal, and ditch in the oceanic form of temperate, subtropical, and tropical delta area. In 2000–2004, it had moved into 14 climates in South, Southeast, and Southwest as watercourses where it had not grown for at least well as Eastern, Southern, Central, and South- 150 years. Based on these data, we explored the western Europe (Meusel et al. 1965). Most stands of distribution, abundance, and environmental con- this species are in lowland regions in tributaries of the ditions (Gałka & Szmeja 2012); the phenology (Gałka great Asian rivers, especially in East (the Amur, & Szmeja 2013); survival; and reproduction in Huang He and Yangtze), South (the Mekong, populations of Salvinia in the Vistula Delta (Szmeja Ganges, and Indus), and Southwest Asia (the Tigris, & Gałka 2013). In the present study, it has been Euphrates, Syr-Daria, and Amu-Daria). Outside hypothesized that the reason for the expansion of Europe, Asia, and Oceania, there are sparse stands in Salvinia in the Vistula Delta is the warming of early the north of and North America. In Europe, it springs, mostly in March and April. We supposed that is found mainly in the catchments of the Caspian, contemporary warming in the Baltic Sea Region, Black, Adriatic, Mediterranean, and Baltic Seas noted by, for example, Hurrell (1995, 1996) and (Casper & Krausch 1980). The geographical range of Marsz and Styszyn´ska (2010), favors the expansion of this plant generally covers areas warmer than the this plant. Baltic Sea region. The plant under study reproduces by sexual and asexual (vegetative) means. Sporocarps with micro- Material and methods and macrosporangia are the organs of sexual

reproduction. Each macrosporangium produces 32 Study sites spores, only one of which survives (macrospore 70– The studies were conducted in the delta of the 75 mm in diameter), while the microsporangium Vistula river (northern Poland), which flows into the contains 64 microspores, each about 20 mmin Baltic Sea (Figure S1). The Vistula Delta formed diameter (Lawalre´e 1964). The macrospore develops towards the end of the Pleistocene, and in the into the female gametophyte, and the microspore Holocene its morphology and hydrology have into the male one. Fertilization takes place on the significantly changed. Today it is a wedge-shaped water surface, producing a zygote which becomes the area covering 1700 km2 and cut by a dense network sporophyte, clonal in structure. Vegetative reproduc- of polders, canals, and drainage ditches begun in the tion entails fragmentation of the mature clone. 13th century and gradually extended since then. Its In the Vistula Delta, Salvinia occurs in the form fertile soils have long been extensively exploited for of spores from November to the end of March, as agriculture. The delta’s hydrological system relies on gametophytes from April to the first days of May, and its proximity to the Baltic Sea and on the Vistula and as sporophytes from May to October. From its tributaries (Drwal 2002). November to the end of February, the majority of In the Vistula Delta, the watercourses with spores lie on the bottom of rivers. In the second half Salvinia are shallow (2.2 ^ 1.5 m), fairly narrow of March, after the ice cover has melted, macro- and (17.9 ^ 13.6 m), slow-flowing (0.11 ^ 0.12 m s21), microspores emerge on the water surface and usually and rich in total nitrogen (4.7 ^ 4.2 mg dm23), total germinate in April to female and male gametophytes. phosphorus (0.7 ^ 0.4 mg dm23), and calcium For about 45 days they occur in the water surface film (88.7 ^ 19.4 mg Ca2þ dm23). The water is neutral at 15.1 ^ 2.48C. The juvenile stage of the sporophyte or alkaline (pH 7.2–9.2) and slightly saline (53.8 ^ - (primordium of surface and underwater leaf) is just 21.3 mg Cl21 dm23). The salinity of the watercourses as inconspicuous as the gametophyte, forming at the is due to intrusion of water from the Vistula Lagoon beginning of May and persisting until the end of (Figure S1). The bottom of the watercourses ranges June. The mature stage (fully developed plant) from mineral to organic, and sediment is reduced appears at the beginning of July and is made up of (2195.3 ^ 2 179.3 mV); it is fairly well hydrated 2.1 ^ 1.1 modules, that is, repeated structural units. (59.3 ^ 24.5%), neutral, or alkaline (pH 6.9–7.8). The spore-producing stage in turn appears toward The watercourses did not freeze to the bottom during the end of August, can be found until the last week of the study years. From the beginning of the 21st September, and consists of 6.8 ^ 4.5 modules. 534 J. Szmeja et al. 3

In September, the individuals grow rapidly, repro- analyzed the time series of mean monthly air duce vegetatively, and form spores. Toward the end temperature from the stations in Kaliningrad of September, the individuals begin to disintegrate. (Ko¨nigsberg, until 1945; WMO Index 26 702) and This process stops toward the end of October, when in Elbla˛g (WMO Index 12 160). The datasets were water temperature falls to 7.8 ^ 3.58C (Gałka & obtained from the All-Russian Research Institute on Szmeja 2013). Hydrometeorological Information–World Data Center (for Kaliningrad) and from NOAA Monthly Climatic Data of the World (for Elbla˛g). The Germination conditions observation data from Kaliningrad cover the period From the Nogat River (Figure S1), 2.200 macrospores from 1851 to 2009, except for 1945. Those from were collected and placed in Petri dishes containing Elbla˛g begin with 1951. The period in common filter paper wetted with distilled water. The dishes between the datasets is 1951–2009. The Elbla˛g were placed in thermostatic chambers for 50 days, and station is located on the north-east edge of the every 48 h, the macrospores that had sprouted during Vistula Delta (see Figure S1), in the vicinity of the that time were counted. Germination conditions: (1) Vistula Lagoon. The Kaliningrad station is about constant temperature 21, þ 5, þ 10, þ 15 and 90 km north-east of the Vistula Delta but also lies in þ208C for 50 days, PAR radiation (49.7 ^ close proximity to the lagoon. The two stations are a 0.7 mmol m22 s21) and all under the same photo- similar distance from the open waters of the Gulf of period (13D/11N); 300 macrospores for each Gdan´ sk. For the analysis, we used standard temperature (six dishes of 50 macrospores each), climatological statistical methods: standard deviation total 1500 macrospores for this experiment; (2) (SD), standard error of estimation (SEE), analyses of temperature 208C, PAR and photoperiod as above, correlations, regressions (incl. trend analyses), 400 macrospores after prior drying for 14 days (eight according to Sokal and Rohlf (1995). dishes of 50 macrospores each); (3) temperature 208C in darkness, 300 macrospores (six dishes of 50 macrospores each). The experiment in darkness was Results done to check the germination of macrospores covered Temperature as a regulator of germination with sediment in rivers; the drying treatment was done to approximate the conditions of germination on In winter, Salvinia occurs in the form of macro- and the riverbank during floods. The significance of microspores lying on river bottoms, at first in differences in germination was determined with the sporocarps, from which they are released gradually Mann-Whitney U test (Sokal & Rohlf 1995). as the sporocarp walls disintegrate (in the River Tuga, 7.8 ^ 13.5 macrospores per 50 cm3 sediment sample). Winter diapause lasts from autumn to early Studies in the permanent plots spring of the next year, about 160 days. As soon as The residence time of Salvinia gametophytes and the ice cover has melted on the rivers (usually in the young sporophytes was investigated in the Tuga River second half of March or first decade of April), spores (Figure S1) at 10 permanent 0.25 m2 plots. emerge on the water surface and germinate. Anchored wooden 0.5 £ 0.5 m frames floating on Macrospores germinate at water temperature of the river surface marked the boundaries of the plots. 12.4 ^ 0.28C or higher and are viable for at least four They extended above the water surface, preventing years. Their long-term viability favors the formation penetration by immigrants. For five consecutive of spore banks in rivers. Spores did not germinate years (2006–2010), every 14 days (from April to after freezing at 21.08C for 5 days. The same spores November), individuals of Salvinia were counted in transferred to þ208C still did not germinate. the permanent plots and the temperature of surface In spring, after the ice cover withdraws, the water was measured. We counted genets (formed macrospores float on the water, drift with the from zygotes) and vegets (formed from sporophytes current, and receive light. Under illumination typical during their vegetative fragmentation). In addition, of April, 72.3 ^ 20.3% of the macrospores germi- from April to July in 2009 and 2010, we collected nated, while under the same thermal conditions samples (20 cm2) of water surface film every 7 days, but in darkness only 36.3 ^ 19.2% germinated and counted the gametophytes and youngest (U ¼ 87.0, Z ¼ 5.36, p ¼ 0.000001). Hence, light sporophyte stages under a binocular microscope. favors germination. Spore germination begins earlier at 208C than at 158C water temperature (6.1 ^ 0.6 day vs. Analysis of long-term temperature changes 19.3 ^ 1.2 day; U ¼ 0.0, Z ¼ 5.4, p ¼ 0.000001; In order to determine the character and scale of air Figure 1). March was warm in 2007, 2008 and 2009 temperature changes over the Vistula Delta area, we (4.3 ^ 0.18C) and cool in 2010 (0.7 ^ 0.18C). In the 4 Early spring warming and expansion of Salvinia 535

significantly correlated with the series from Elbla˛g (from r ¼ 0.872 in May to r ¼ 0.997 in November and r ¼ 0.975 for the year, p , 0.00001). Therefore, we can use the data from the Kaliningrad station to draw conclusions about climatic changes in the Vistula Delta during the period for which there are no meteorological observations recorded there. Regression analysis showed that temperatures at the Elbla˛g station were slightly warmer than at Kaliningrad throughout all the months of the year, and that for almost half of the year, the differences were not significant. The statistically significant Figure 1. Fraction of Salvinia natans macrospore germination temperature differences between the two stations in during 50 days. Conditions of experiments: Constant photoperiod 13D/11N (PAR 58.3 ^ 0.05 mmol m22 s21)at208C (solid line), at 1951–2009 were greatest in the spring months of 158C (thin line), in the dark and at 208C (broken line), and after March and April when Elbla˛g was warmer by 0.88C prior air-drying for 14 days (dotted line). Differences between the and 1.18C on average, respectively. Air temperature analyzed variants are statistically significant at p , 0.05. in Elbla˛g was also higher than in Kaliningrad in the Explanations: D – number of hours imitating daylight, N – winter months (0.5–0.78C), but the differences were night; n ¼ 300 macrospores (solid line), n ¼ 300 (thin line), n ¼ 400 (broken line), n ¼ 400 (dotted line). not statistically significant. The mean annual temperature in Elbla˛g was 0.38C higher than in Kaliningrad. first instance, the macrospores germinated in mid- Analysis of the series of monthly and annual April, and in the latter as late as in mid-May. temperatures at the Kaliningrad station indicated a Prolongation of its period of residence creates more positive trend over the last 158 years for which there generations of vegetative offsprings in the popu- are instrumental observations. Two periods of lations, causing huge, dense aggregations of this plant warming are visible against this weak positive trend form in rivers. (þ0.07 ^ 0.028C/decade). The first one reached its

climax in the second half of the 1930s, and the second, after a temperature drop in the 1960s and Residence time in the population 1970s, began towards the end of the 1980s and has In the permanent plots, gametophytes occur from the continued to the present day. Here, we term this beginning of April to mid-May, that is, during the latter period “contemporary warming”. period of occasional frost. An early developmental Contemporary warming began with a strong and stage of the gametophyte resides in the population sudden temperature rise at the turn of 1988/1989. from the beginning of April (water temperature In 1989, the temperature increased stepwise and 12.4 ^ 0.28C) till the end of April (14.2 ^ 0.4 8C), persisted, with fluctuations, at the highest level noted and a late stage in the first half of May (18.3 ^ 1.58C). in the period of instrumental observations. After The density of early gametophytes (25,220 ^ 33,275 1989, its range of interannual variation narrowed, individuals/0.25 m2) is nearly an order of magnitude especially in winter (DJF) and spring (MAM), higher than the density of late ones (4375 ^ 3264 manifested as reduction of the number of deep indiv./0.25 m2; U ¼ 105.5, Z ¼ 2.03, p ¼ 0.04). temperature minima. Reproduction is highly dependent on the water The mean annual temperature in Kaliningrad temperature in streams. In May, the number of was þ 7.08C (standard error of estimation, genets is positively correlated with temperature in SEE ¼ 0.088C) during the entire period of 1851– April (r ¼ 0.93; p ¼ 0.026), whereas the number of 1988 (137 years), but between 1989 and 2009 vegets in September is related to temperature in July (20 years), it increased to þ8.28C (SEE ¼ 0.168C). (r ¼ 0.91; p ¼ 0.039). There are two modes of The difference (þ1.28C) is statistically significant at vegetative propagation: fragmentation of clones and 99% confidence level. The increase of annual gemmation along the peripheral part of the clone. temperature during contemporary warming (after The start of each of them is statistically highly 1989) is largely the outcome of a sharp temperature correlated with water temperature (r ¼ 0.91 for rise in winter and spring, mostly in March and April fragmentation and r ¼ 0.87 for gemmation). (Figure 2). Here we should note that over the Vistula Delta the winter temperature median has increased to Long-term temperature changes above 08C during this latest warming period: through The 1951–2009 series of mean monthly and annual more than half of the winters, the mean air temperatures from Kaliningrad is very strongly and temperature was not lower than 08C, and only 25% 536 J. Szmeja et al.

Figure 2. Variation of mean annual temperature (Tyear), winter temperature (December, January and February – TDJF), and mean temperature in first half of spring (March and April – TMA) at Kaliningrad. A – mean temperature prior to contemporary warming (1851– 1988); B – mean temperature during contemporary warming (1989 – 2009). of the winters had mean temperatures lower than range narrowed (SD ¼ 1.24). In the latter period, the 218C. Mean winter temperatures higher than 08C mean temperature of March and April fell below indicate that temperature drops below zero were þ3.88C only once, in 2006. Before 1988, there were short-term and/or generally not deep. Snow cover in temperature drops below þ3.88C every 2–4 years the Vistula Delta was not persistent during such (Figure 3). winters and was limited to snow episodes lasting a Our analysis of daily March and April tempera- few days. Under such conditions the ice cover does tures in 1951–2009 in Elbla˛g shows that the mean not remain very long. April temperature depends on the variation of March During contemporary warming, a significant temperature. If the monthly temperature in March is temperature rise was recorded in March and April higher than 08C, the snow cover, if present in the last (Figure S2 and S3). In the earlier period (1851– winter phase, begins to disappear toward the end of 1988), the mean temperature of those months in March, as does the ice cover on lakes and rivers. Kaliningrad was þ3.28C (SD ¼ 1.69), but in 1989– Devoid of snow and ice, the land surface and water 2009, it increased to þ5.18C (SD ¼ 1.32). In Elbla˛g, surface warm more quickly and the ground thaws. the mean daily temperature of March and April In consequence, the rise of air and water surface before contemporary warming (1951–1988) was temperature in April becomes higher than average. þ4.38C and was characterized by considerable If the mean for both these months is þ3.58C or less, interannual variation (SD ¼ 1.64), whereas in the likelihood of below-zero episodes lasting a few 1989–2009 it rose to þ5.78C and the variation days or weeks in March reaches 95%. Due to the mild

Figure 3. Mean air temperature series for first half of spring (March and April) at Elbla˛g station in 1951–2009. Lower broken line – March and April mean temperature in 1951–1988, (before contemporary warming). Upper broken line – mean during 1989–2009. Vertical line divides the time periods. Early spring warming and expansion of Salvinia 537 winters and less frequent frost in March during the Atlantic-European sector at the time and the positive contemporary warming period, the development phase of the North Atlantic Oscillation (Hurrell cycle of Salvinia begins earlier in a given year and 1995, 1996) – when in cold seasons a warm and lasts longer. humid polar-maritime air mass from the Atlantic flows to the north-west of Europe, including Scandinavia and around the Baltic Sea – became Discussion more intense and frequent. Winters became milder, Successful expansion of an indigenous species or the spring seasons warmer, the growing season invasion by a geographically alien one entails quick started earlier (Marsz & Styszyn´ska 2001). and effective occupation of new territories. One The winter air temperature rise brought on by cause of this phenomenon is natural or anthropo- increased atmospheric circulation, which transports genic transformation of environmental conditions warm Atlantic air from the west and south-west (Pieterse & Murphy 1990; Keane & Crawley 2002; (NAO), limits the uptake of heat from Baltic waters. Aguiar & Ferreira 2013; Brundu et al. 2013), which At the same time, during positive NAO phases, the disturbs the relation between an expansive or invasive development of ice cover on the Baltic Sea is inhibited species and its competitors, pathogens, or herbivores (Omstedt & Chen 2001) and the sea surface is (Davis et al. 2000; Blumenthal 2005; Seastedt 2009). warmer toward the end of the cooling process (Marsz The occurrence of Salvinia in the Vistula Delta is & Styszyn´ska 2010). Maximum ice extent (MIE) on likely due to environmental factors, but neither the the Baltic Sea (see Seina¨ & Palosuo 1993) is highly trophic level of watercourses nor frequent flooding in negatively correlated with air temperature in March this area are responsible for it. and April at stations around the Baltic Sea. Salvinia was very rare in the Vistula Delta from Consequently, the phases and amplitude of the 1850 to 2000, but after this period, it occurred North Atlantic Oscillation that occur in winter exert a frequently and in masse. Today it occupies small considerable effect, through thermal inertia, on the watercourses which are slow-flowing and rich in air temperature series in spring at stations around nitrogen and phosphorus (see chapter Study sites). the Baltic. For the 59 years between 1950 and 2009, The concentrations of nutrients in watercourses with the variation of Hurrell’s (1995) winter (DJFM)

Salvinia are as high as in other regions, for example in NAO indicator explains 45.9% of the variation of Jammu and Kashmir (Zutshi & Vass 1971), Rhine- mean March and April temperature in Kaliningrad; land-Palatinate, and Baden-Wu¨rttemberg (Wolff & variation of SST (Sea Surface Temperature) from the Schwarzer 2005). In the Vistula Delta, the trophic year before in the eastern North Atlantic (39–418N, level of surface water was constantly high and varied 19–218W) explains 8%, and the variation of MIE, little through time, mainly due to the domination of indirectly associated with NAO, explains 5% very fertile hydrogenic soils on this area (Drwal 2002; (R ¼ 0.767, F (3.56) ¼ 26.7, p , 0.00001). The Gałka & Szmeja 2012). This was the case both when same variables show similar explanatory power for Salvinia was forming only a few scattered popu- early spring mean temperature in Elbla˛g. lations (1850–2000), as well as during its expansion One of the consequences of NAO in the Vistula during the study years (2006–2010). Delta is higher survival of the youngest development It is difficult to agree with Puchalski et al. (2002) stages of Salvinia and higher germinability of the that floods, especially those of 1994 and 1996, are spores of this plant. This weather phenomenon responsible for the massive growth of Salvinia in the prolongs the vegetative season, during which, instead Vistula Delta. It is true that during the flood many of two or three generations of vegetative offsprings spores are transmitted from the upper and middle (vegets), five or six emerge (Gałka & Szmeja 2013). courses of the Vistula River to the delta. Floods were Such a large number of vegetative offsprings in a year frequent from the mid-19th to late 20th centuries; was observed in, for instance, a population of the they occurred in 1865, 1892, 1910, 1925, 1941, invasive tropical plant Salvinia molesta (Room 1983). 1948, 1961, 1963, 1980, 1981, 1994, and 1996. Both species have rapid growth strategies which During that period, this plant was a very rare enable them to successfully occupy the available component of the local flora (Markowski et al. 2004). space (Seastedt 2009). In summer, the number of Supply of spores during floods enabled the species to modules in a clone of Salvinia natans doubles after persist in the delta, but flooding was not a significant 7 days thanks to the rapid growth of 0.3 modules/day. cause of its occurrence. Other aquatic grow more slowly: for example, In our opinion it is the increase in the mean Spirodela polyrhiza with a speed of 0.08 segments annual and seasonal air (and water) temperature in (corresponding to S. natans modules) per day the Vistula Delta that caused the expansion of (Lemon et al. 2001), Ranunculus circinatus at Salvinia from 1989 on (Figures S2, S3 and Figure 3). 0.05 cm/day, Elodea canadensis at 0.04 cm/day, and There was a change in atmospheric circulation in the Nymphoides peltata at 0.02 cm/day (Larson 2007). 538 J. Szmeja et al.

In 1951–1988, the mean daily March and April and the vegetative season lasts longer. More temperature in the Vistula Delta was þ4.68C and generations of vegetative offsprings are formed in was characterized by substantial interannual vari- the populations. The clonal (modular) structure of ation (SD ¼ 1.64). It increased to þ5.78C in 1989– an individual, ease of spore germination, and high 2009 and its variation range narrowed (SD ¼ 1.24). effectiveness of vegetative reproduction are attributes This change boosted S. natans spore germination of Salvinia allowing the plant to occupy free space and the survival rate of the youngest development quickly and successfully. Salvinia population size in a stages. The spores germinate mainly in spring, given year is determined by mortality in the cohort of generally in early April, at 12.4 ^ 0.28C or higher spring gametophytes and by the number of vegetative water temperature. The gametophytes develop at offsprings in summer. water temperature exceeding 148C in the Vistula Delta and also in Rhineland-Palatinate (Wolff & Schwarzer 2005). The minimum temperature initi- Acknowledgements ating the growth cycle is higher than for other aquatic We thank our colleagues for discussions and valuable 8 plants: Zostera marina seedlings appear at 5.0 C (Abe comments on the manuscript. Michael Jacobs helped 8 et al. 2008), Trapa natans at 8.0 C (Kurihara & edit the English translation. Ikusima 1991), Bidens tripartita at 9.08C (Bra¨ndel 2004), and Luronium natans starts development at 8– 128C (Szmeja & Bazydło 2005). Funding The gametophytes occur in delta watercourses from early April to the end of the first week of May. The paper is based on the results obtained in work They locate directly under the surface film (Gałka & under Project N N304 411638 funded by the Polish Szmeja 2013); that is, they form the hyponeuston. National Science Centre. They are tiny and delicate, and do not survive ground frost. Before the expansion of Salvinia, frost periods Supplemental data and ground frost were much more frequent (see Figure 3). The gametophytes emerge before other Supplemental data for this article can be accessed

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