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Seasonal Variations of Fucus Vesiculosus Fertility Under Ocean Acidification and Warming in the Western Baltic Sea

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Seasonal Variations of Fucus Vesiculosus Fertility Under Ocean Acidification and Warming in the Western Baltic Sea Botanica Marina 2017; aop Angelika Graiff*, Marie Dankworth, Martin Wahl, Ulf Karsten and Inka Bartsch Seasonal variations of Fucus vesiculosus fertility under ocean acidification and warming in the western Baltic Sea DOI 10.1515/bot-2016-0081 of F. vesiculosus in spring and summer, which may alter Received 28 July, 2016; accepted 21 April, 2017 and/or hamper its ecological functions in shallow coastal ecosystems of the Baltic Sea. Abstract: Ocean warming and acidification may substan- tially affect the reproduction of keystone species such as Keywords: bladder wrack; mesocosm; multi-factorial Fucus vesiculosus (Phaeophyceae). In four consecutive change; reproduction; seasonal pattern. benthic mesocosm experiments, we compared the repro- ductive biology and quantified the temporal development of Baltic Sea Fucus fertility under the single and com- Introduction bined impact of elevated seawater temperature and pCO2 (1100 ppm). In an additional experiment, we investigated In the Baltic Sea, Fucus vesiculosus L. is the most common the impact of temperature (0–25°C) on the maturation of canopy-forming and hence structurally important seaweed North Sea F. vesiculosus receptacles. A marked seasonal dominating the biomass along rocky and stony coasts reproductive cycle of F. vesiculosus became apparent in (Kautsky et al. 1992, Torn et al. 2006, Rönnbäck et al. 2007). the course of 1 year. The first appearance of receptacles on Fucus communities provide food for numerous organisms, vegetative apices and the further development of immature thereby supporting complex trophic interactions (Kautsky receptacles of F. vesiculosus in autumn were unaffected by et al. 1992, Middelboe et al. 2006, Korpinen et al. 2007) and warming or elevated pCO . During winter, elevated pCO 2 2 providing various ecosystem goods and services (Rönn- in both ambient and warmed temperatures increased the bäck et al. 2007). Vulnerability of F. vesiculosus to environ- proportion of mature receptacles significantly. In spring, mental change is suggested by the sharp decline of Baltic warming and, to a lesser extent, elevated pCO acceler- 2 populations over the last five decades (Torn et al. 2006). ated the maturation of receptacles and advanced the The severe changes in Fucus distribution and biomass release of gametes by up to 2 weeks. Likewise, in the labo- have recently been attributed to multifactorial stressors ratory, maturation and gamete release were accelerated (Wahl et al. 2011), where indirect effects may outweigh at 15–25°C relative to colder temperatures. In summary, direct effects (Wahl et al. 2015a). Crucial points for the per- elevated pCO and/or warming do not influence receptacle 2 sistence of Fucus populations have also been identified in appearance in autumn, but do accelerate the maturation its reproductive cycle (Andersson et al. 1994, Serrão et al. process during spring, resulting in earlier gamete release. 1996a,b, 1999). Hence, it is important to study factors gov- Temperature and, to a much lesser extent, pCO affect 2 erning the reproduction of this seaweed. the temporal development of Fucus fertility. Thus, rising Fucus species generally show a marked seasonality in temperatures will mainly shift or disturb the phenology fertility (Knight and Parke 1950, Carlson 1991, Serrão et al. 1996a, Berger et al. 2001). Reproductive seasonality may be a result of various abiotic factors that are used as envi- *Corresponding author: Angelika Graiff, Institute of Biological ronmental cues to induce and synchronize reproduction Sciences, Applied Ecology and Phycology, University of Rostock, and/or to meet the physiological requirements for repro- Rostock, Albert-Einstein-Straße 3, 18059 Rostock, Germany, e-mail: [email protected] duction (Lüning and tom Dieck 1989, reviewed by Brawley Marie Dankworth and Inka Bartsch: Alfred Wegener Institute, and Johnson 1992). In fucoid species, environmental Helmholtz-Centre for Polar and Marine Research, Am Handelshafen 12, factors not only induce reproduction but also determine 27570 Bremerhaven, Germany the period and duration of reproduction (Mathieson et al. Martin Wahl: GEOMAR Helmholtz Centre for Ocean Research Kiel, 1976, Terry and Moss 1980, Bäck et al. 1991, Andersson Kiel, Germany Ulf Karsten: Institute of Biological Sciences, Applied Ecology and et al. 1994). Photoperiod is the most common factor induc- Phycology, University of Rostock, Rostock, Albert-Einstein-Straße 3, ing reproduction in seaweeds (Santelices 1990, Brawley 18059 Rostock, Germany and Johnson 1992). For example, Fucus distichus L. and Bereitgestellt von | Universitätsbibliothek Rostock Angemeldet | [email protected] Autorenexemplar Heruntergeladen am | 17.05.17 09:18 2 A. Graiff et al.: Fucus fertility under ocean acidification and warming Ascophyllum nodosum (L.) Le Jolis formed receptacles As the onset and duration of reproduction in Fucus is at their apices under short-day conditions (SD, e.g. 8 h triggered and regulated by various environmental factors light:16 h darkness), whereas the apices remained veg- (Bäck et al. 1991, 1993, Andersson et al. 1994, Berger et al. etative under long-day conditions (LD, e.g. 16 h light:8 h 2001, Kraufvelin et al. 2012), development of reproduc- darkness) in the laboratory (Bird and McLachlan 1976, tive tissue and the corresponding physiological processes Terry and Moss 1980). Increase in temperature and/or may be particularly sensitive to environmental change. exceeding temperature thresholds, either alone or in com- Global warming and acidification of the oceans as a con- bination with irradiance, stimulate receptacle and gamete sequence of rising atmospheric CO2 concentrations are the maturation in fucoids (Mathieson et al. 1976, Pearson most widespread effects of global change. Mean sea-sur- and Brawley 1996, Kraufvelin et al. 2012). Finally, gamete face temperatures in the Baltic Sea have increased in all release seems to be governed by endogenous free-running seasons since 1985 (HELCOM 2013). A doubling of atmos- circadian or circalunar cycles (Pearson and Serrão 2006), pheric CO2 by the year 2100 (Caldeira and Wickett 2005, which may be synchronized by environmental factors Orr et al. 2005, Bindoff et al. 2007) is predicted to cause a such as tidal height, wave action, salinity (Serrão et al. rise of 3–6°C in surface temperatures of the Baltic Sea by 1999, Ladah et al. 2008), time of day and lunar phase the end of the century (Gräwe et al. 2013, Elken et al. 2015). (Andersson et al. 1994). The endogenous cycles, however, The increase of the CO2 partial pressure (pCO2) in sea-sur- have not been unequivocally identified in fucoids. face waters will cause a pH decrease of 0.1–0.5 units at the In the western Baltic Sea, F. vesiculosus populations ocean surface in the 21st century (Feely et al. 2004, Sabine release gametes in early summer (May–July), in autumn et al. 2004, Caldeira and Wickett 2005, Orr et al. 2005). (September–October) or in both seasons (Carlson 1991, Increasing seawater temperature and ocean acidifica- Berger et al. 2001, Maczassek 2014). Receptacles are tion are expected to shift synchronously and may singly or induced in summer-reproducing individuals during the interactively affect reproduction of Fucus. This impact may preceding autumn under SD conditions, but only mature vary seasonally according to natural growth and repro- in the following spring. Possibly low winter temperatures duction periods, and because these two factors, together delay the development. Autumn-reproducing individuals with potentially interacting factors such as photoperiod initiate receptacles in spring, mature over the summer and or nutrient concentration, follow natural fluctuations. release gametes in September and October. Both reproduc- Thus, we hypothesized that the influence of warming and tion types abscise their decaying receptacles after gamete increased pCO2 (singly and combined) on the reproductive release, and start to develop new vegetative tips before the biology of F. vesiculosus (e.g. receptacle formation, matura- next reproductive cycle (6–9 months long) starts (Berger tion and gamete release) would differ among seasons. We et al. 2001). Some populations of F. vesiculosus reproduce exposed F. vesiculosus to the same orthogonally crossed in both seasons and probably comprise a mixture of both factors of warming and elevated pCO2 in all four seasons, reproduction types (Carlson 1991, Berger et al. 2001). at levels expected for the shallow western Baltic Sea region Induction of receptacle initiation by SD has been experi- within the next 100 years (Gräwe et al. 2013, Elken et al. mentally proven for summer-reproducing Fucus individu- 2015, Schneider et al. 2015). These near-natural climate- als (Berger et al. 2001). change scenarios, including all natural fluctuations, were In dioecious F. vesiculosus, the reproductive tissue simulated using benthic mesocosms (Kiel Outdoor Bentho- (receptacles) develops at the frond tips and contains the cosms, Wahl et al. 2015b). In an additional experiment we conceptacles with egg-containing oogonia or the anther- quantified the direct and isolated effect of temperature on idia with sperm cells. During maturation, the receptacles the maturation of F. vesiculosus receptacles. grow in volume, the number of conceptacles per recepta- cle increases, and the egg and sperm cells mature (Bäck et al. 1991, Andersson et al. 1994). Mature conceptacles contain eight eggs per oogonium and 64 spermatozoids Materials and methods
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