Seasonal dynamics of ciliated protozoa and their potential food in an eutrophic estuary (Bay of Biscay)

Abstract

Ciliate assemblages, together with phytoplankton and heterotrophic nanoflagellates (HNF) as their potential food, have been surveyed monthly along the salinity gradient of the Nervión River estuary from March 2000 to March 2002. A total of 135 taxa of ciliate have been identified corresponding to 20 orders. Scuticociliates, naked choreotrichs and oligotrichs were the most abundant groups, distributed throughout a broad range of salinity. In addition to these groups, which were the dominant taxa in the middle estuary, tintinnids were characteristic of the ciliate assemblages of the outer estuary whereas in the innermost part naked choreotrichs and oligotrichs decreased in number, being substituted by sessilids, hymenostomatids, peniculids and cyrtophorids. Total ciliate concentrations were among the highest reported in the literature for other estuaries and coastal waters, frequently reaching 10⁵ cells l⁻¹. Meanwhile, tintinnid concentrations were comparable with those of other estuarine and coastal waters. Based on a principal component analysis (PCA) three main groups were delineated, with ciliates and their potential food sources as variables. One was that constituted by freshwater ciliate such as sessilids, hymenostomatids, cyrtophorids and pleurostomatids, which appear in low numbers in the innermost part, mainly in winter. Another group contained diatoms, chlorophytes, flagellates, euplotids and scuticociliates, all of them broadly distributed along the estuary and reaching their maximum density in late spring–summer. The third group was made up of taxa mainly appearing at the seaward end such as dinoflagellates, cyanobacteria, haptorids, tintinnids, naked choreotrichs and oligotrichs, which reached the highest densities in summer and early autumn. Ciliates do not seem to be food limited in the Nervión River estuary or much controlled by metazoan grazing.

Introduction

Ciliates are a major component of the pelagic food webs in freshwater and marine systems where they play an important role in the transfer of carbon from the picoplankton and nanoplankton to the metazoans (Hadas et al., 1998; Pierce & Turner, 1992). The importance of ciliates was initially associated mainly with the microbial loop and corresponding microbial web, but now there is increasing evidence that these protists are also a crucial part of the herbivorous web, consuming a wide spectrum of particle sizes from bacteria to large diatoms and dinoflagellates as well as other ciliates. As a consequence, in the past decades, much research effort have been devoted to finding factors affecting ciliate abundance and distribution and their trophic behaviour in different environments. Among these factors, temperature and food availability as well as predator density seems to be of paramount importance as bottom-up and top-down control factors, respectively (Levinsen, Nielsen, & Hansen, 2000, Nielsen, & Kiorboe, 1994, Verity, 1985).

Selective feeding by both mechanosensory and chemosensory clues has been observed in ciliates. This permits them to select the size and the composition of food particles (Ayo et al., 2001, Bernard & Rassoulzadegan, 1990, Kamiyama & Arima, 2001), and exert a strong influence on the dynamics of the other components of the microplankton.

Estuaries are known to contain higher concentrations of nutrients and organics than most aquatic ecosystems. Although estuaries have generally lower specific diversity than their adjacent marine or freshwater relatives, planktonic euryhaline species both autotrophic and heterotrophic forms may grow in these rich systems to bloom proportions when unchecked by other controlling factors (Cloern, 2001).

The Nervión River is a nutrient rich estuary, that receives large amounts of dissolved and particulate organic matter from the catchment basin and from a wastewater treatment plant (WTP). Recently, the water quality has experienced a remarkable improvement leading to increased water transparency that has permitted the development and growth of the phytoplankton. Meanwhile, the estuary presents features of eutrophic waters with high levels of ammonia and low oxygen concentration together with high concentrations of bacteria and organics (Bilbao-Biscay Water Consortium, personal communication). On the other hand, recent studies on the sediment have revealed the existence of an impoverished invertebrate fauna, reduced to a few oligochaeta (González-Oreja, personal communication). Besides, rotifers, cladocera and copepods, which are major consumers on ciliate, are almost absent from the estuary (Uriarte, personal communication).

The aim of this paper was to know the relationships between ciliate distribution and abundance and their potential food sources along the salinity gradient of an eutrophic estuary. It is hypothesised that despite the strong longitudinal changes in salinity within the estuary, other factors such as availability of bacteria and heterotrophic nanoflagellates (HNF), and the size classes distribution of the phytoplankton must also play a major role in the structure of ciliate assemblages.