Periodic events of Potamogeton alpinus in NW Poland (Pomerania region)

Potamogeton alpinus (alpine pondweed, red pondweed) is a submerged aquatic plant with a boreal-mountain type of distribution in the Northern Hemisphere, which occurs in the northern parts of Europe (Meusel et al. 1965), North America and NW Asia (Hultén & Fries 1986), and even beyond the polar circle (Preston 1995; Bobrov & Chemeris 2009). The species occurs mostly in Scandinavia, whereas it is much less common in Central and Northwest Europe (Baattrup-Pedersen et al. 2008) (Fig. 1). The plant usually grows in watercourses which are small, not particularly fertile and exposed to full sunlight (Boedeltje et al. 2005) as well as in shallow, slightly acidic or alkaline rivers (Wiegleb & Todeskino 1983). In NE Poland, it usually grows on a thick layer of organic sediment in slowly flowing waters and in oligotrophic flow-through lakes (Zalewska-Gałosz 2008). In Central and Northwest Europe, the persistence of many of the P. alpinus sites is threatened by climate changes and human impact on water bodies (Sand-Jensen et al. 2000; Riis & Sand-Jensen 2001). According to Velichkevich and Zastawniak (2006), the presence of P. alpinus endocarps in wetland deposits is characteristic of the beginning or the end of interglacial periods. During paleoecological studies, the presence of P. alpinus was recorded in NE Poland (Gałka & Sznel 2013; Gałka 2014; Gałka et al. 2014), SE Poland (Kołaczek et al. 2014), the Czech Republic (Gálová et al. 2016) and Romania (Gałka et al. 2017) in sediments accumulated between 14 400 and 4500 cal yr BP, but usually during cooler climate stages. Alpine pondweed propagates mainly vegetatively (Wiegleb & Todeskino 1983; 1985), i.e. similarly to other perennial and clonal aquatic plants (Grace 1993; Szmeja & Gałka 2008; Szmeja 2010). Moreover, the species is also characterized by high phenotypic plasticity (Kaplan 2002; 2008; Kaplan & Zalewska-Gałosz 2004; Robionek et al. 2015), which together with its phenological reactions provides an opportunity to follow the adaptation of the species to changes in environmental conditions. It is worth emphasizing that changes and disruptions to habitat conditions have a major impact not just on the size of modular structures of plant individuals (Bociąg et al. 2013; Robionek et al. 2015), but also on the underwater community structure (Chmara et al. 2014; 2015).

Figure 1

Phenological studies could be used, for example, in research on the coexistence of species (Fargione & Tilman 2005), their invasion (Wolkovich & Cleland 2011), expansion (Szmeja et al. 2016) and reaction of populations and communities to climate change (Fitter & Fitter 2002; Menzel at al. 2006; Cleland et al. 2007; Święta-Musznicka et al. 2011), especially close to their geographic range limits (Chuine & Beaubien 2001; Schwartz 2003). The main focus of research has been on the timing of periodic events, such as leaf formation, flowering, fruiting or wintering, which in the case of aquatic plants is mainly dependent on temperature (Hutchinson 1975; Szmeja & Bazydło 2005; Gałka & Szmeja 2013; Szmeja 2010). Shifts in species phenology can occur due to a rise in temperature (Walther et al. 2002; Cleland 2007); therefore, phenological data could be useful for estimating the biological effects of the recent climate warming.

Although there are various conceptions regarding the cause of global warming, we suggest that in NW Poland it could be associated with an increase in the intensity and frequency of the positive phase of the North Atlantic Oscillation (NAO), during which warmer and moister air has been flowing from above the Atlantic to Northwest Europe, Scandinavia and the Baltic Sea region since 1989, especially in colder seasons (Hurrell 1995; 1996). One of the consequences of the recent climate warming in the studied area, i.e. near Gdańsk, is the expansion of Salvinia natans (Gałka & Szmeja 2013; Szmeja & Gałka 2013; Szmeja et al. 2016), which started in the late 1990s (Gałka & Szmeja 2012) with an intensity not observed since the early Middle Ages (Święta-Musznicka et al. 2011). The rapid population growth, like in the case of S. natans, applies only to species at most sites located in Southern Europe (Casper & Krausch 1980; Rothmaler et al. 1986), i.e. in areas warmer than the Baltic Sea region. It should be noted, however, that reactions to climate warming of boreal aquatic plants such as P. alpinus at the southern limit of their geographic range in the studied region are still unknown. As a result, there is an urgent need to update the scientific basis for the legal protection of boreal aquatic plants and their habitats in European countries close to the Baltic coast.

Our objective was to examine the timing of periodic events in the population of P. alpinus close to the southern limit of the geographic range of the species on the Central European Plain. Such data would be the basis for assessing the impact of global warming on the phenology of alpine pondweed and could be used to protect boreal aquatic plant species and their habitats in this part of Europe as well as for comparative analyses of the Scandinavian population. The results presented in this paper have also a potential for palaeoecological reconstructions.

This study was performed in 15 watercourses with P. alpinus, between 1 and 120 km south of the Baltic coast (54°26’–53°48’N, 17°01’–18°32’E) in NW Poland (Pomerania region; Fig. 1). This terrain was formed during the last glaciation event and is characterized by the presence of numerous lakes, rivers and watercourses; the latter are usually small, shallow and slow flowing. This area is close to the south-eastern limit of the geographic range of P. alpinus and is separated from its central part by the Baltic Sea.

Three 0.5 dm³ samples of water and sediment per site were collected from aggregations of P. alpinus in 15 watercourses, on one occasion in the middle of the growing season (July or August, 2014–2015). The measured environmental variables of water are as follows: 1 – pH; 2 – conductivity (μS cm^-1); 3 – concentration of calcium (mg Ca²⁺ dm^-3); 4 – total nitrogen (mg TN dm^-3, for λ = 340 nm); 5 – total phosphorus (mg TP dm^-3), spectrophotometrically, for λ = 880 nm; 6 – water color (mg Pt dm^-3); 7 – water flow (m s^-1), measured with a Valeport M-801 Electromagnetic Flow Meter; 8 – PAR light intensity (photosynthetic active radiation, as %, measured with a LiCOR Li-250 light meter). The following parameters were measured in the sediment: 8 – organic matter content (%), 9 – mineral matter content (%), 10 – sediment water content (%), 11 – granulometry (fractions: f1 < 0.1, f2 0.1–0.25, f3 0.25–0.5, f4 0.5–1.0, f5 1.0–2.0, f6 > 2.0 mm), and 12 – concentration of calcium (mg Ca g^-1 d.w. – dry weight). The measurements were performed according to the methods suggested by Eaton et al. (2005). The environmental conditions of watercourses with P. alpinus were described in more detail by Robionek et al. (2015).

Characteristics of the age stages (morphological development stages) were determined on the basis of 728 modules of P. alpinus, i.e. a repeating structural unit consisting of an aboveground shoot (leaves, stem, inflorescence) and the stretch of a rhizome to the nearest aboveground shoot. Plants were collected randomly by hand from 15 watercourses and transported to the laboratory for measurements. We measured the following traits: 1 – height of shoot (cm) and 2 – the number of leaves on the fresh material as well as on the dry material (drying at 80°C for 48 h); 3 – biomass (mg d.w.); 4 – allocation of biomass to shoot (%); 5 – allocation of biomass to rhizome with roots (%); 6 – allocation of biomass to leaves (%); and 7 – allocation of biomass to generative structures (inflorescence with peduncle, as %). The data were used to characterize the following age stages: juvenile (young, not fully developed), mature (fully developed), generative (flowering and/or fruiting), senile (dieback of the aboveground shoot and fragmentation of the rhizome) and winter buds.

Phenological data were collected from permanent plots (0.5 × 0.5 m) every 14 days during the whole growing season (from March to November) in 2014 and 2015. In winter, samples were collected every 30 days. On each sampling occasion, the temperature of water was measured and the number of modules as well as their age stages (juvenile, mature, generative, senile, winter bud) were counted (without plant removal). On the basis of the quantitative dominance of the age stages, the phenological phases were established in the development of the studied population.

Areas located in temperate climates are characterized by seasonal phenomena in plant populations, which very often makes them the object of phenological studies. An example of such research might be the course of periodic events in the development of P. alpinus, as described by Brux et al. (1987, 1989) and Germ et al. (2002). Nevertheless, to the best of our knowledge, the complete phenological spectrum of this species in undisturbed conditions has never been determined. Recording the timing of periodic events in plant populations, especially close to the limit of their geographic range, becomes vitally important because of the increasing human impact and, most of all, the recent climate warming (Walther et al. 2002). Phenological analysis of aquatic populations has shown that the timing of life history events responds to changes in global environmental conditions (Gałka & Szmeja 2013).

An increase in global air temperature does not raise serious concerns (Hurrell 1995; 1996; Stocker 2014). The globally averaged, combined land and ocean surface temperature data show a warming of 0.85°C during the 1880–2012 period (Stocker 2014). In N Poland, as in most of the Baltic basin, the warming has been particularly strong since 1980. In the period from 1980 to 2010, the annual air temperature at the weather stations located along the south Baltic coast rose by 0.104°C per decade (Marsz & Styszyńska 2010). The mean annual air temperature near Gdańsk rose from +7.0°C (during the period of 1851–1988) to +8.2°C (between 1989 and 2009). The increase in annual temperature during the present warming (after 1989) is largely due to a sharp temperature rise in winter and spring, mostly in March and April (Szmeja et al. 2016). Air temperature influences environmental conditions in water bodies, for example by regulating the length and timing of the period of ice, temperature of the surface layer of water (Wetzel 2001), and duration of the growing season of plants, as well as the rate of growth and development (Szmeja et al. 2016). There is a close relationship between air temperature and water temperature. The correlation coefficient between the average monthly temperature of the air near Gdańsk and that of the Baltic waters in the area is high and usually 0.85–0.90 (Marsz & Styszyńska 2010). The correlation between the temperatures of air and water in watercourses with P. alpinus is equally high.

Terrestrial plant species growing in similar regions have developed a similar phenology (Thuiller et al. 2004). Additionally, previous studies on aquatic plants, as presented by e.g. Santamaria et al. (2003), show that patterns in the phenology of plant species usually correlated with certain environmental variables, such as temperature, precipitation, latitude or altitude. The results of these studies show that most P. pectinatus genets can grow and reproduce asexually at distant latitudes. Subarctic and temperate genets have been found to grow and produce tubers at sites, for instance, in Norway, the Netherlands, and Spain. For all genets, regardless of the region and population of origin, the biomass yield and tuber production increased when grown at a decreasing latitude. This might suggest that in Europe, optimal conditions for the growth of P. pectinatus are found in the Mediterranean. For populations of P. alpinus, i.e. a species with a boreal geographic coverage, the trend of changes along the north-south gradient is probably the opposite. In N Poland, the species flowers and fruits, but probably does not reproduce sexually, because seedlings have never been found (personal observation). Similar observations of the reaction of this plant were recorded in other localities on the Central European Plain and Western Europe (Wiegleb & Todeskino 1985; Brux et al. 1987). There is nothing unusual in this reaction, because some species of remnant populations in the periphery of their geographic range, such as Decodon verticillatus, lose their capacity for sexual reproduction, and permanent inability of a population to reproduce sexually is defined as sexual extinction (Eckert et al. 1999; Eckert 2002; Honnay & Bossuyt 2005; Eckert et al. 2008). Also Stratiotes aloides is known to reproduce mainly in the vegetative way in Europe (Cook & Urmi-König 1983), which might be attributed to the climatic conditions; a relationship between its fructification and thermal conditions can be observed while analyzing fossil distribution (Gałka 2010). Clonal reproduction as well as a shift in the duration of the development of age stages offer a safe escape route for many species under suboptimal environmental conditions. In our view, climate warming might disturb the timing of P. alpinus development, reducing the probability of sexual reproduction of the species and the phenological distance between the Central European Plain and the Scandinavian populations.