Effect of pH on growth, cell volume, and production of freshwater ciliates, and implications for their distribution

We investigated the effect of pH on growth, cell volume, and production of the freshwater ciliates Urotricha farcta, U. furcata, and U. castalia in laboratory cultures with Cryptomonas sp. as food. Overall, pH had a significant, species-specific effect on all parameters investigated. The food alga, Cryptomonas sp., showed a wide pH tolerance, with positive growth rates between pH 4.4 and pH 9.65. Among the ciliates, U. farcta was the most pH-tolerant and U. castalia was the most pH-sensitive species, with positive growth being confined to pH 6.5–8.2. The pH optimum was derived from cellular production rates. The pH optima of the three ciliate species were shifted; their production rates peaked at pH 4.4–5.3 (U. farcta), pH 5.9–7.3 (U. furcata), and pH 6.8–7.9 (U. castalia). The pH effect on growth and survival of the ciliates was minor at circumneutral and moderately alkaline pH values, relative to the effect of temperature and food measured in earlier experiments. The widths of the pH tolerances of the ciliates were positively related to the widths of their temperature niches and to their natural distributions. U. farcta and U. furcata were characterized as euryoecious species, with broad pH and temperature tolerances and ubiquitous distribution; U. castalia is a rare, stenoecious species, requiring specific pH and temperature conditions. pH is a major environmental factor of aquatic ecosystems at the interface of physicochemical and biological processes. It is regulated by carbonate equilibrium, both in the ocean and in most inland waters, and is impacted by biological processes such as photosynthesis and respiration. Although pH is relatively constant in the ocean, 8 6 0.5 (Lalli and Parsons 1993), it varies between ,2 and 12 in lakes and rivers (Wetzel 2001), in close relation to the geology (rock type) and hydrology of their drainage basins. Weathering of soils and rocks primarily controls the ion supply and, thus, the pH of inland waters. The effects of biological processes are less important when comparing the pH across different ecosystems, but may largely control seasonal pH fluctuations within a given water body. Biologically-driven seasonal variation in temperate, moderately-productive and moderately–hard-water lakes is typically #1 pH unit (e.g., BfW 2002). Larger pH fluctuations, up to .2 pH units, occur in lakes where the buffering capacity of the carbonate system is less efficient, in highly productive small water bodies, and in the littoral zones of shallow lakes with intense primary production (Talling 1976; Krambeck et al. 1994; Edmonson 2005). Effects of hydrogen ion activity on aquatic biota have received the most attention at the extremes of the pH range; in particular, the impact of lowered pH in poorly buffered waters as a consequence of acidic deposition was studied in great detail in Northern Europe and North America during the closing decades of the last century (Schindler 1988; Battarbee 1990; Charles 1991). Similarly, interdisciplinary studies investigated the impact of acid mine drainage on aquatic communities (Geller et al. 1998). As a result of those efforts, the general reduction of species diversity with decreasing pH and the tolerance limits for low pH are known for major aquatic taxa such as fish, zooplankton, and algae (Schindler 1988; Baker and Christensen 1991). Algal taxa with solid cell walls, such as diatoms and chrysophytes, are used by paleolimnologists to infer the natural and man-made changes of pH in lakes over the past 10,000 years (Smol et al. 1986; Psenner and Schmidt 1992). With the exception of the pioneering work by Beaver and Crisman in Florida lakes (Beaver and Crisman 1981; Bienert et al. 1991), protozoa, although they are important components of all aquatic food webs (Sherr and Sherr 1984; Laybourn-Parry 1992; Weisse 2003) and may dominate at low pH (Packroff 2000), were largely neglected in the previous investigations cited above. Beaver and Crisman (1981) reported a shift in the taxonomic composition of ciliates with decreasing pH, with oligotrichs becoming the dominant group at pH ,5. A recent review concluded that Prostomatida, Hypotricha, and Peritricha are the dominant ciliate orders in acidic lakes (Packroff 2000). Although there is some evidence for species-specific pH tolerance of planktonic freshwater ciliate species, primarily originating from cursory field measurements (compiled by Foissner et al. 1999), an experimental laboratory investigation of the pH reaction norm of common species is still lacking. Temperature, food, and predators are assumed to control the population dynamics of natural ciliate communities (Fenchel 1987; Laybourn-Parry 1992; Weisse 2003) and are responsible for niche partitioning among sympatric, closely related taxa (Weisse et al. 2001). The significance of pH for the occurrence and competitiveness of planktonic freshwater ciliates is virtually unknown. This may result from the assumption that daily and seasonal 1 Corresponding author ([email protected]). Acknowledgments We thank Ulrike Scheffel and Nicole Laufenstein for technical assistance. Jens Boenigk, Martin Hahn, and two anonymous reviewers provided helpful comments on an earlier version of this manuscript. Limnol. Oceanogr., 51(4), 2006, 1708–1715 E 2006, by the American Society of Limnology and Oceanography, Inc.