Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates)

To examine the grazing effects of copepod-dominated mesozooplankton on heterotrophic microbial communities, four mesocosm experiments using gradients of zooplankton abundance were carried out at a coastal marine site. The responses of different protist groups (nanoflagellates, ciliates) and bacterioplankton in terms of abundance and additionally, for bacteria, diversity, production, and exoenzymatic activity, were monitored during 1 week of incubation. Independent of the initial experimental abiotic conditions and the dominating copepod species, zooplankton caused order-of-magnitude changes in microbial functional groups in a clear community-wide four-link trophic cascade. The strongest predatory effects were observed for protist concentrations, thus generating inverse relationships between mesozooplankton and ciliates and between ciliates and nanoplankton. Copepod grazing effects propagated even further, not only reducing the abundance, production, and hydrolytic activity of bacterioplankton but also increasing bacterial diversity. The overall strength of this trophic cascade was dampened with respect to bacterial numbers, but more pronounced with respect to bacterial diversity and activity. High predation pressure by heterotrophic nanoflagellates, realized at the highest copepod abundance, was probably the underlying mechanism for these structural changes in the bacterial assemblages. Our results thus suggest a mechanism by which changes in higher trophic levels of marine plankton indirectly affect prokaryotic assemblages and microbially mediated ecosystem functions. Microorganisms mediate most biogeochemical processes in the oceans and their activities are influential in element cycling on a global scale. In contrast to the accruing knowledge of prokaryotic diversity and functions in the ocean, much less is known about how microbial communities interact with the pelagic food web. Similar to other trophic levels, bacterioplankton communities are regulated by bottom-up factors, e.g., nutrient limitation, and by topdown factors, e.g., protist predation and viral infection (Thingstad 2000). Several trophic levels are organized within the pelagic microbial food web. The main predators of planktonic prokaryotes (picoplankton, 0.2–2 mm) are small heterotrophic and mixotrophic nanoflagellates, mainly in the size range of 3–5 mm (Fenchel 1986; Sherr and Sherr 2002). There is plentiful evidence that ciliates are important omnivorous grazers of nanoplankton (2–20 mm) and their micro-sized forms (.20 mm) especially are often the dominating herbivores in marine systems (Sherr and Sherr 2002). Mesozooplankton (0.2–2 mm in size), which prey on phytoplankton as well as on different heterotrophic protistan groups, connect the microbial food web with the classical algae–zooplankton–fish food chain (Sanders and Wickham 1993; Kiørboe 1997). For example, copepods, which constitute the majority of the mesozooplankton in the oceans (Verity and Smetacek 1996), are known to be efficient predators on planktonic ciliates (Calbet and Saiz 2005). The effect of zooplankton on microbial food webs has been studied extensively in freshwater systems (Wickham 1998; Zöllner et al. 2003), where copepods and cladocerans may dominate the mesozooplankton. Marine studies have focused mainly on the copepod–ciliate link (Levinsen et al. 2000; Broglio et al. 2004; Calbet and Saiz 2005); only a few field investigations have examined whether predation effects on microzooplankton are transferred to heterotrophic nanoand picoplankton (Sipura et 1 Corresponding author ([email protected]).