The role of transparent exopolymer particles (TEP) - Journal of ...

Journal of Plankton Research Vol.22 no.3 pp.485–497, 2000

The role of transparent exopolymer particles (TEP) in the increase in apparent particle stickiness (a) during the decline of a diatom bloom Anja Engel Institut für Meereskunde, D-24105 Kiel, Germany Abstract. The termination of diatom spring blooms in temperate waters has been connected with the formation and subsequent rapid sedimentation of aggregates. According to coagulation theory, the rate of aggregate formation depends on the probability of particle collision and on the efficiency with which two particles adhere once they have collided (stickiness). During this study, the variation in particle stickiness was determined over the decline of a diatom bloom using the Couette Chamber assay with low shear (G = 0.86 s–1). A mixed diatom population, dominated by Skeletonema costatum, was sampled during the spring bloom in the Baltic Sea and incubated in the laboratory for 18 days. Measurements of diatom species composition, transparent exopolymer particles (TEP) and bulk particle abundance, as well as chemical and biological variables, were conducted in order to reveal the determinants of coagulation efficiency. The investigation showed that an increase in TEP concentration relative to conventional particles at the decline of the bloom significantly enhanced apparent coagulation efficiencies. High proportions of TEP led to apparent values of stickiness >1, which indicates that collision rates can be substantially underestimated when the stickiness parameter a is calculated on the basis of conventional particle counting only, e.g. with the Coulter Counter. A new stickiness parameter, a9, was therefore estimated based on the combined volume fractions of TEP and conventional particles. The problems of stickiness measurements are discussed and the role of TEP in coagulation processes is emphasized.

Introduction The role of large particle aggregates (marine snow) in the vertical flux of organic matter into the oceans’ interior is widely acknowledged (Shanks and Trent, 1980; Fowler and Knauer, 1986; Asper et al., 1992; Gardner, 1997; Jackson and Burd, 1998). Theoretical analyses of particle coagulation processes predict that aggregate formation depends on the probability of particle collision and on the efficiency with which two particles that collide stick together afterwards (stickiness) (Hunt, 1982; McCave, 1984; Jackson, 1990). The former is a function of particle concentration, size and the mechanism by which particles are brought into contact, e.g. Brownian motion, shear or the differential settlement of particles. The latter depends mainly on the physicochemical properties of the particle surface and may vary with the particle type. In the ocean, high particle concentrations occur during phytoplankton blooms and aggregates have readily been observed at these times (Smetacek, 1985; Alldredge and Gotschalk, 1989; Riebesell, 1991a, b; Tiselius and Kuylenstierna, 1996). However, the occurrence of aggregates does not always coincide with the peak of phytoplankton abundance. Rather, it is postponed towards the decline of the bloom (Smetacek, 1985; Riebesell, 1991a, b). This has been hypothesized to be due to an increase in particle stickiness (Smetacek, 1985), but has not so far been demonstrated empirically. Despite the importance of coagulation processes for biogeochemical cycles as well as for food web dynamics (Bochdansky and © Oxford University Press 2000 Downloaded from https://academic.oup.com/plankt/article-abstract/22/3/485/1451747 by guest on 06 November 2017

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Herndl, 1992; Green and Dagg, 1997), information on the magnitude and variability of particle stickiness is relatively scarce. There are only a few direct measurements of phytoplankton stickiness (Kiørboe et al., 1990; Kiørboe and Hansen, 1993; Drapeau et al., 1994; Waite et al., 1997) and even less describe its variability during the course of natural phytoplankton blooms (Kiørboe et al., 1994, 1998; Dam and Drapeau, 1995). Changes in particle coagulation efficiency have been attributed to the abundance of single species or as part of the life cycle strategy of cells (Smetacek, 1985; Kiørboe and Hansen, 1993; Crocker and Passow, 1995). Recently, a special class of particles was found to be readily abundant during phytoplankton blooms in water and aggregates as well. These transparent exopolymer particles (TEP) (Alldredge et al., 1993) are thought to play a central role in coagulation processes for two reasons. First, they are supposed to be very sticky and secondly their abundance may enhance the probability of particle collisions (Passow et al., 1994; Jackson, 1995). TEP are abundant in shelf seas (Passow and Alldredge, 1995; Schuster and Herndl, 1995; Mari and Burd, 1998) and in the open ocean (Engel et al., 1997; Hong et al., 1997). However, there is a lack of direct measurements that corroborate the role of TEP in the coagulation of particles. In this study, the variability of particle coagulation efficiency was examined during the decline of a natural diatom bloom. The stickiness parameter (a) was determined using the Couette Chamber assay and related to the abundance of TEP, diatom species and Coulter Counter-detectable particles. The methodological problems of stickiness measurement are discussed in connection with the role of TEP in coagulation processes. Method Sample collection and incubation Phytoplankton were sampled during a diatom spring bloom in the western Baltic Sea (Kiel Bight) on 24 March. A volume of 10 dm3 was sampled with Niskin bottles at 2 m depth. In the laboratory, the sample was filtered through a 200 µm mesh in order to remove the larger zooplankton and diluted with 14 dm3 of 0.2 µm (Nuclepore) pre-filtered sea water. Five aliquots of 4.5 dm3 were taken from the diluted sample and incubated in Plexiglas tubes. The tubes were well aerated by bubbling and received a photosynthetically active radiation flux of 210 µmol m–2 s–1, with a light:dark cycle of 12 h:12 h. The incubation was performed at a temperature of 15°C from 24 March to 11 April 1997. Biological and chemical analysis Analyses of biological and chemical variables were made daily from day 1 to day 6 and every second day thereafter. Aliquots of 100 cm3 were placed into polycarbonate bottles and frozen at –21°C for subsequent measurement of phosphate and nitrate with an autoanalyzer [after (Grasshof et al., 1983)]. Particulate organic carbon (POC) and nitrogen (PON) were determined with a Hereaus CHN analyzer (CHN-O-rapid) from duplicate 200 cm3 samples filtered onto 486 Downloaded from https://academic.oup.com/plankt/article-abstract/22/3/485/1451747 by guest on 06 November 2017

TEP and particle stickiness during bloom decline

pre-combusted glassfiber filters (Whatman GF/F). A total of 200 cm3 were filtered onto duplicate GF/F filters and chlorophyll (Chl) a was measured following the procedure of Jeffrey and Humphrey (Jeffrey and Humphrey, 1975). The concentration and size distribution of solid particles, 4 µm < equivalent spherical diameter (ESD) 8 µm ESD was about two orders of magnitude lower during the first part of the study (Figure 3a and b). Thereafter, TEP abundance increased clearly and reached a maximum of 5.25 3 102 cm–3 on day 18. Since the mean size of TEP (~16 µm ESD) was larger than that of CCP (~6 µm ESD), the volume concentration of CCP was approximately only three times the volume concentration of TEP at the beginning and roughly the same at the end of the study (Figure 3c and d). Highest ratios of TEP:CCP by volume were observed on day 14 and day 18, respectively. Variability of particle coagulation efficiency The apparent stickiness (a) of particles was