G Model LIMNO-25289; No. of Pages 5 ARTICLE IN PRESS Limnologica xxx (2012) xxx–xxx Contents lists available at SciVerse ScienceDirect Limnologica jou rnal homepage: www.elsevier.de/limno Phenology of the aquatic fern Salvinia natans (L.) All. in the Vistula Delta in the context of climate warming ∗ Agnieszka Gałka, Józef Szmeja University of Gdansk,´ Department of Plant Ecology, 80-308 Gdansk,´ Wita Stwosza 59, Poland 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 Salvinia natans 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 microspores 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 species 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 spore-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 spores. © 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 G Model 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 family 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 Marsilea 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 microspore 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.