To sink or to be lysed? Contrasting fate of two large phytoplankton species in Lake Biwa

We estimated the contributions of sedimentation and cell lysis to the loss of two large phytoplankton species (Fragilaria crotonensis and Staurastrum dorsidentiferum) in Lake Biwa. Major loss process differed between species, and large phytoplankton did not necessarily function as a nutrient sink. The spring bloom of F. crotonensis was terminated by nutrient depletion and a subsequent increase in sedimentation rate. Although this species could be occasionally grazed by zooplankton, sedimentation eliminated nutrients from the surface. In contrast, the summer bloom of Staurastrum dorsidentiferum crashed mainly as a result of cell lysis caused by fungal infection within the surface mixing layer, which accounted for more than 75% of the mortality rate of this species. Cell lysis of S. dorsidentiferum may lead to nutrients within the surface mixing layer, supporting the production of bacteria and zooplankton. The different loss process of these two species implies that the function of phytoplankton in material flows cannot be assessed by cell size alone. Fungal parasitism can result in a different fate, which may play an important role in material cycling in lakes. Phytoplankton production is lost from the pelagic zone through various processes, such as sedimentation, zooplankton grazing, and cell lysis due to pathogenic infection and physiological death (Reynolds 1984). Because cell or colony size of phytoplankton is one of the important factors determining sedimentation rates and vulnerability to zooplankton grazing (Smayda 1970; Lampert 1974), loss processes have been thought to differ between large and small phytoplankton species (Malone 1980; Legendre and Le Fèvre 1991; Kiørboe 1993). Different loss processes of phytoplankton cause different material flows in aquatic ecosystems (Legendre and Le Fèvre 1991). Because small phytoplankton species (,20 mm) are in general highly vulnerable to zooplankton grazing, especially filter-feeding cladoceran zooplankton such as Daphnia (Lampert 1974; Sterner 1989; Kagami et al. 2002), their production is likely to enter the grazing chain and support the production of higher trophic levels. Large phytoplankton species (.20 mm) are, in contrast, less vulnerable to zooplankton grazing, although some large phytoplankton species are grazed by calanoid copepods (Sommer et al. 2001; Kagami et al. 2002). According to the Stokes law, large phytoplankton sink faster than small phytoplankton (Smayda 1970; Kiørboe 1993). It is therefore believed that large inedible phytoplankton species are lost from the pelagic zone mainly through sedimentation, resulting in exporting the material to the profundal zone and supporting the production of benthic organisms (Malone 1980; Legendre and Le Fèvre 1991; Fitzgerald and Gardner 1993). Thus, size structure of phytoplankton, which affects the fate of phytoplankton production, can be crucial in channeling and determining the material flows in aquatic ecosystems. Cell lysis of phytoplankton may also affect material flows within the microbial food web if cell contents are released as dissolved organic matter and nutrients (van Boekel et al. 1992; Brussaard et al. 1996). It is still unknown, however, whether cell lysis occurs to a similar extent between different phytoplankton species with similar size. In Lake Biwa, the largest lake in Japan with a surface area of 674 km2 and a maximum depth of 104 m, phytoplankton species forming large colonies or having a large cell size (.20 mm), such as Fragilaria crotonensis (diatom) and Staurastrum dorsidentiferum (green algae), occur abundantly and contribute more than 50% to the total primary production during the stagnant period from spring to fall (Nakanishi 1976; Tezuka 1984; Kagami et al. 2002). Because of its large cell size (40–60 mm), S. dorsidentiferum is hardly grazed by zooplankton (Okamoto 1984; Kawabata 1987; Kagami et al. 2002). Because F. crotonensis develops large belt-like colonies (40–170 mm), it is also less vulnerable to Daphnia grazing (Kawabata 1987). Thus, a large part of primary production in Lake Biwa may be transported to the profound zone without being consumed by zooplankton. Nonetheless, estimations of the material fluxes indicated that the grazing rate of the zooplankton community in the pelagic zone corresponded closely with the primary production rate, and that the sedimentation rate of organic matter is only 10% of primary production during the stagnant period (Hama et 1 To whom correspondence should be addressed. Present address: Netherlands Institute of Ecology (NIOO-KNAW), Center for Limnology, Rijksstraatweg 6, 3631AC, Nieuwersluis, The Netherlands ([email protected]). 2 Present address: Fisheries Research Division, Nepal Agricultural Research Council, Katmandu, Nepal. 3 Present address: Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York, 14853. 4 Present address: School of Life Sciences, Tohoku University, Aoba, Sendai, 980-8578, Japan.