Colonization dynamics of ciliate morphotypes modified by shifting sandy sediments
Introduction
Aquatic ciliates in the benthic zone are an important component of the microbial loop since they link the carbon and energy transfer between bacteria, algae, other protozoans and metazoans (Augspurger et al., 2008, Norf et al., 2009) and contribute to the benthic–pelagic coupling (Kathol et al. 2011). Ciliates can enhance organic matter processing by modulating bacterial respiration and growth rates (Ribblett et al., 2005, Risse-Buhl et al., 2012) and, thus, play an important role in ecosystem function. Bed sediments of streams and rivers, which contribute significantly to ecosystem metabolism irrespective of sediment characteristics (e.g. Jones et al., 1995, Mulholland et al., 1997, Naegeli and Uehlinger, 1997), are an important habitat for ciliates. The highest ciliate abundances of 103–104 cells cm−3 have been recorded at a grain size range of 0.15–0.25 mm, corresponding to the fine and mid sand fraction (Baldock et al., 1988, Cleven, 2004, Gücker and Fischer, 2003, Packroff and Zwick, 1998).
The upper sediment layers in sandy streams and rivers are often transported in moving bed forms, such as ripples that migrate even at base flow (e.g., Baas 1999). Sediment particles in a migrating ripple are subject to frequent shifting where the particles erode at the stoss side, glide, role, or bounce over the crest, and avalanche down the lee side. Here, the particles are deposited and covered by following particles until the migrating ripple lee side approaches the particle's resting position, and are eroded into transport again (Baas 1999). The period of such transport-deposition cycles depends on the bulk flow velocity as well as the ripple length and height of the crest. Resulting ripple migration rates typically vary from less than a minute to several hours (Bridge, 2003, Harvey et al., 2012). Increasing shear stress and shear velocity at rising discharge initiate augmentation of turbulent eddies and transition of ripples to a mobile upper stage plane bed (Bennett et al., 1998, Bridge, 2003). Sediment particles of upper stage plane beds are transported as bed load and suspended load, where individual particles are shifted in turbulent motions and continuously glide, roll, bounce, and hence, collide with other particles (Bennett et al. 1998).
Shifting sediments can structure the ciliate assemblage either directly by habitat disturbance or indirectly by altering prey availability. At base flow, shifting sands inhabit a higher bacterial activity and production compared to stable or deeper sediments in the hyporheic zone or in near shore habitats (Fischer et al., 2005, Fischer et al., 2003). Thus, they seem to be a favorable habitat for bacterivorous ciliates. Suspension feeders, such as small scuticociliates or hymenostomes swimming freely in the pore space and associating with surfaces for feeding without distinct features for attachment (Foissner et al. 1994), are assumed to be most susceptible of being washed out into the overlying water layers at increasing bed shear stress (Shimeta et al., 1995, Shimeta and Sisson, 1999), whereas a flattened cell shape in combination with thigmotactic behavior, the tendency to persistently stay in contact with a surface, or a sessile life style enable ciliates to remain associated with surfaces even at high flow velocities (Risse-Buhl and Küsel, 2009, Schmitz, 1985).
We expect that colonization of shifting sediments by ciliate morphotypes will be defined by their morphology, ability to associate to surfaces and feeding strategy, and that the response of ciliates’ morphotypes differs with respect to the frequency of sediment shifting. Thus, we hypothesized that (1) free-swimming filter feeders reach higher numbers in stable sediments, and will be suspended into the overlying water when sediments start shifting, (2) vagile grasper feeders with a flattened cell shape in combination with a thigmotactic behavior can tolerate a range of sediment shifting frequencies, and (3) sessile filter feeders will tolerate sediment shifting by remaining attached to sediment particles.
Section snippets
Description and cultivation of ciliate morphotypes
We studied the dynamics of an assemblage of 3 bacterivorous ciliate species covering different morphological features, mechanisms to associate or attach to surfaces and feeding strategies typical for ciliate communities in sandy sediments. All 3 morphotypes typically colonize the uppermost bed sediments of sandy streams and rivers in which they co-occur and contribute significantly to the ciliate community (Cleven, 2004, Finlay et al., 1993, Königs and Cleven, 2007, Packroff and Zwick, 1996).
Colonization dynamics of ciliate morphotypes
Initial relative abundances of ciliate morphotypes in the pore water of sediments and in the overlying water were similar. D. campylum, C. uncinata and V. convallaria contributed respectively 14 ± 6%, 77 ± 6% and 9 ± 1% to the ciliate assemblage in pore water of sediments and 13 ± 2%, 75 ± 3% and 12 ± 5% in the overlying water. Within 24 h of sediment shifting, total ciliate abundance increased from 0.2 ± 0.1 × 103 cells mL−1 pore water to 3.4 ± 0.6 × 103 cells mL−1 in the pore water of stable sediments and 1.0 ± 0.1 × 103
Shifting of sandy sediments in microcosms and in streams
The horizontally rotating microcosm set-up (Fig. 1A) allowed us to simulate the sediment shifting of ripples, the typical bed forms of sandy sections in streams and rivers. In the rotating microcosms, the avalanching movement of the upper layer of sediment particles down the ripple's lee side and the periods of particles resting within the ripple were well achieved and realized periodic shifting of sediment particles. Typically, the length of stream ripples is greater than the length of the
Conclusion
Our data showed that specific ciliate morphotypes are advantageous in colonizing shifting sediments. Hence, sediment shifting that is spatio-temporally heterogeneous over a range of scales from reach to catchment in sandy streams (Bridge 2003) should be considered as a determinant of the fluctuating ciliate community structure in sandy sediments. Since ciliates are known to enhance microbial activity, the role of ciliates in the metabolism of streams and rivers will be maintained under
Acknowledgements
We thank T. Wolburg for technical support, K. Eisler for kindly providing a ciliate culture, and C. Mendoza-Lera for helpful discussions. The study was supported by grants from the German Research Foundation (DFG) to M. Mutz (Transregional Collaborative Research Centre SFB/TRR 38) and to U. Risse-Buhl (RI 2093/1-1).
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Both authors contributed equally to the manuscript.
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Present address: Leibniz Centre for Agricultural Landscape Research, Institute for Landscape Biogeochemistry, Eberswalder Straße 84, 15374 Müncheberg, Germany.