Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters

Literature review and synthesis of growth rates of aquatic protists focused on the role of temperature in the formation of massive annual algal blooms in high-latitude ecosystems. Maximal growth rates of herbivorous protists equaled or exceeded maximal growth rates of phototrophic protists at temperatures above 15uC. Maximal growth rates of herbivorous protists declined more rapidly with decreasing temperature than did those of phototrophic protists, and at the very low temperatures common to high-latitude ecosystems, the maximal growth rates of herbivorous protists were less than half the maximal growth rates of phototrophic protists. Growth rates of herbivorous protists were consistently lower than those of bacterivorous protists and were unrelated to differences in cell volume between the two groups. Linear equations describing the relationship of the natural log of maximal growth rates of bacterivorous and herbivorous protists to temperature were generated and compared to published information for maximal growth rates of phototrophic protists and copepods. The three heterotrophic groups had similar slopes (0.12 for bacterivorous protists, 0.10 for herbivorous protists, and 0.13 for copepods) that were approximately double that of phototrophic protists (0.06). The massive annual algal blooms observed in high latitudes are due in part to a fundamental difference in the relationship between growth and temperature for phototrophic protists and their grazers. Phytoplankton blooms are common occurrences in many aquatic ecosystems. These phenomena can positively or negatively affect food web structure and carbon flow in marine ecosystems. For example, spring blooms in temperate environments are often characterized by phytoplankton species that are subsequently grazed by larger zooplankton, resulting in the efficient transfer of energy to higher trophic levels and away from energetic losses within the microbial loop. Conversely, blooms of toxic or noxious species of phytoplankton can disrupt energy transfer in planktonic food webs and/or result in illness or death of mammals, birds, and commercially important fish and shellfish. Formation of a phytoplankton bloom indicates a fundamental imbalance between growth and removal of phytoplankton. Assuming that grazing dominates other loss factors, this imbalance may be accomplished through the stimulation of phytoplankton growth relative to extant grazing pressure, the inhibition of herbivory in the presence of phytoplankton growth, or some combination of the two. Most research has emphasized the importance of the stimulation of the intrinsic growth rate of phytoplankton as the primary underlying cause for massive accumulations of phytoplankton and has deemphasized the importance of removal processes (Verity and Smetacek 1996). This predilection is rooted in the preponderance of studies that have examined responses of phytoplankton growth to availability of nutrients and light (Riley 1942; Sverdrup 1953; Platt et al. 1991). Increases in phytoplankton standing stock can only occur if the algal population is growing. Nonetheless, reduced grazing pressure due to constraints on herbivory (e.g., as a result of low zooplankton abundance, low individual feeding rates, or the production of toxic or inhibitory compounds by phytoplankton) will yield a higher net population growth rate for a given intrinsic growth rate of the phytoplankton assemblage and thus can serve as an explanation for some phytoplankton blooms (Smayda 1997; Liu and Buskey 2000; Tagliabue and Arrigo 2003). One classical explanation for the initiation of nontoxic (i.e., ‘edible’) phytoplankton blooms (e.g., the spring bloom of many temperate and polar ecosystems) is the temporal offset that occurs between onset of rapid phytoplankton growth in early spring and subsequent development of a zooplankton assemblage sufficient to affect phytoplankAcknowledgments We are grateful to Rebecca Gast for helpful discussions on the topic. We would also like to acknowledge Suzanne Strom, Peter Jumars, and one anonymous reviewer for valuable suggestions for improving the manuscript. Funding was provided by National Science Foundation grant OPP-0125437. 1 To whom correspondence should be addressed (jmrose@udel. edu). Present address: College of Marine Studies, University of Delaware, 700 Pilottown Road, Lewes, Delaware 19958.