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The Effect of the Salinity, Light Regime and Food Source on Carbon and Nitrogen Uptake in a Benthic Foraminifer

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The Effect of the Salinity, Light Regime and Food Source on Carbon and Nitrogen Uptake in a Benthic Foraminifer Biogeosciences, 18, 1395–1406, 2021 https://doi.org/10.5194/bg-18-1395-2021 © Author(s) 2021. This work is distributed under the Creative Commons Attribution 4.0 License. The effect of the salinity, light regime and food source on carbon and nitrogen uptake in a benthic foraminifer Michael Lintner1, Bianca Lintner1, Wolfgang Wanek2, Nina Keul3, and Petra Heinz1 1Department of Palaeontology, University of Vienna, Vienna, Austria 2Division of Terrestrial Ecosystem Research, Department of Microbiology and Ecosystem Science, University of Vienna, Vienna, Austria 3Institute of Geosciences, Christian-Albrechts-Universität zu Kiel, Kiel, Germany Correspondence: Michael Lintner ([email protected]) Received: 6 August 2020 – Discussion started: 25 August 2020 Revised: 4 January 2021 – Accepted: 19 January 2021 – Published: 23 February 2021 Abstract. Foraminifera are unicellular organisms that play showed a stimulation of food uptake after 7 d. In summary, it an important role in marine organic matter cycles. Some can be concluded that E. excavatum copes well with changes species are able to isolate chloroplasts from their algal food of salinity to a lower level. For changes in light regime, we source and incorporate them as kleptoplasts into their own showed that light reduction caused a decrease of C and N metabolic pathways, a phenomenon known as kleptoplastidy. uptake by E. excavatum. One species showing this ability is Elphidium excavatum, a common foraminifer in the Kiel Fjord, Germany. The Kiel Fjord is fed by several rivers and thus forms a habitat with strongly fluctuating salinity. Here, we tested the effects of 1 Introduction the food source, salinity and light regime on the food uptake (via 15N and 13C algal uptake) in this kleptoplast-bearing 1.1 General information foraminifer. In our study E. excavatum was cultured in the lab at three salinity levels (15, 20 and 25) and uptake of C and N Foraminifera are unicellular, highly diverse marine organ- from the food source Dunaliella tertiolecta (Chlorophyceae) isms known since the early Cambrian (e.g., Scott et al., 2003; and Leyanella arenaria (Bacillariophyceae) were measured Pawlowski et al., 2003). As major consumers of phytode- over time (after 3, 5 and 7 d). The species was very well tritus they play an important role in organic matter recy- adapted to the current salinity of the sampling region, as both cling in marine environments, particularly in marine sedi- algal N and C uptake was highest at a salinity of 20. It seems ments (benthos), from coasts to the deep sea and in brack- that E. excavatum coped better with lower than with higher ish water (Boltovskoy and Wright, 1976). Most foraminifera salinities. The amount of absorbed C from the green algae D. are heterotrophic, but some can isolate functional chloro- tertiolecta showed a tendency effect of salinity, peaking at a plasts from their algal food sources, keep them viable in salinity of 20. Nitrogen uptake was also highest at a salinity their cells and incorporate them into their own cellular of 20 and steadily increased with time. In contrast, C uptake metabolism, a process termed kleptoplastidy (Bernhard and from the diatom L. arenaria was highest at a salinity of 15 Bowser, 1999). Elphidium, a benthic foraminifer, is one and decreased at higher salinities. We found no overall sig- of nine currently known genera of foraminifera (Bulimina, nificant differences in C and N uptake from green algae vs. Elphidium, Haynesina, Nonion, Nonionella, Nonionellina, diatoms. Furthermore, the food uptake at a light–dark rhythm Reophax, Stainforthia and Virgulinella) which perform klep- of 16 V 8 h was compared to continuous darkness. Darkness toplastidy (Lopez, 1979; Lee et al., 1988; Cedhagen, 1991; had a negative influence on algal C and N uptake, and this Bernhard and Bowser, 1999; Correia and Lee, 2000; Grzym- effect increased with incubation time. Starving experiments ski et al., 2002; Goldstein et al., 2004; Pillet et al., 2011; Lechliter, 2014; Tsuchiya et al., 2015). Elphidium has a Published by Copernicus Publications on behalf of the European Geosciences Union. 1396 M. Lintner et al.: The effect of the salinity, light regime and food source on C and N uptake worldwide distribution and occurs from tropical to Arctic leads to an increased intracellular pH environment which al- waters (Murray, 1991). This genus makes up a particularly lows foraminifera to produce a high magnesian calcite test high proportion of the total foraminiferal population in the (Tsuchiya et al., 2020). shallow water of the Mediterranean, the English Channel, Currently little is known about the feeding behavior and the North Sea and the Baltic Sea (Murray, 1991). More than the C and N metabolism of foraminifer species exhibiting 60 morphospecies of Elphidium are known (Murray, 1991), kleptoplastidy, such as Elphidium or Haynesina. Moreover, many of which are present in the North Sea and Baltic Sea. given that plastids may either supplement the nutrition of A detailed description of the different species and morpho- foraminifera by providing photosynthates or by being di- types is given in Darling et al. (2016). The most common gested, kleptoplastid species may show a slower detrimen- species are E. albiumbilicatum, E. excavatum clavatum, E. tal response to starvation or a slower uptake of (pulses of) excavatum excavatum, E. gerthi, E. guntheri, E. incertum and algal food (Lintner et al., 2020). Foraminiferal food uptake E. williamsoni (Weiss, 1954; Terquem, 1876; Williamson, depends on several factors such as the size of food (Mur- 1858; Lutze, 1965; Frenzel et al., 2005; Nikulina et al., ray, 1963), type of food (e.g., Lee and Müller, 1973; No- 2008; Polovodova and Schönfeld, 2008). Elphidium exca- maki et al., 2014), age of the foraminifera and food quality vatum shows a large morphological intraspecific variability (Lee et al., 1966), water temperature (Wukovits et al., 2017; (Miller et al., 1982). Two subspecies of this foraminifer (E. Heinz et al., 2012), or salinity (Lintner et al., 2020; Dissard e. excavatum and E. e. clavatum) have been found to coex- et al., 2009). Salinity and light conditions are highly vari- ist in the Baltic Sea (Lutze, 1965). Schweizer et al. (2011) able in intertidal and brackish milieus where foraminifera showed that these species exhibit large genetic differences thrive in highly diverse and active communities. Very lit- with respect to each other and therefore can be regarded as tle is known about such light–dark and salinity effects subspecies rather than as ecophenotypes. on the feeding behavior of foraminifera. For example, the During longer periods of starvation, kleptoplasts may pos- kleptoplastid species Haynesina germanica showed no re- sibly serve as a nutritional source that can be digested sponse to changes in salinity, while food uptake by the non- (Falkowski and Raven, 2007). But they can also supplement kleptoplastid species Ammonia tepida increased with salinity the nutrition through photosynthesis under light conditions. (Lintner et al., 2020). In the same study, both species showed Diatoms are the major chloroplast sources for Elphidium, large differences in the retention of C relative to N, with sub- with an average of 3:7 × 104 chloroplasts possessed by one sequent adverse effects on the recycling of these elements foraminiferal individual (Correia and Lee, 2000). The re- by mineralization and respiration and excretion to the envi- tention time of functional chloroplasts in foraminifera may ronment. Such differences, given that these species are (co- vary from several days to several months (Lopez, 1979; Lee )dominant in their foraminiferal community, can have impor- et al., 1988; Correia and Lee, 2002). Another genus, Hay- tant implications for local marine biogeochemical cycles of nesina (Pillet at al., 2011), can sustain their kleptoplasts effi- C and N. ciently for more than a week (Jauffrais et al., 2016). The up- Based on the abovementioned aspects, this study investi- take of kleptoplasts by Haynesina germanica and Elphidium gated the food uptake and food preference (green algae vs. di- williamsoni through the consumption of diatoms can be seen atoms) of Elphidium excavatum spp. at different salinity lev- in the comparison of spectral signatures and pigment com- els and a changing light–dark rhythm. Elphidium excavatum position (Jauffrais et al., 2016; 2019a). Further experiments is optimally suited for this purpose, as it is representative of showed that not all algae are excellent chloroplast donors foraminifera in coastal regions and can account for over 90 % (Lee and Lee, 1989; Correia and Lee, 2001). It was observed of the total foraminiferal population in some areas (Schön- that Elphidium absorbs up to 5 times more chloroplasts from feld and Numberger, 2007). After Darling et al. (2016) our diatoms than from green algae (Correia and Lee, 2000). It used foraminifera (E. excavatum) are called E. selseyense. was also pointed out that different light–dark regimes had no Actually E. selseyense is officially called Cribroelphidium influence on the uptake of chloroplasts by Elphidium (Cor- selseyense. But due to the high importance of the “older” reia and Lee, 2000). Foraminifera below the photic zone can name we used for this paper the most common and more of- also perform kleptoplastidy (Bernhard and Bowser, 1999). ten cited name, E. excavatum. These aspects suggest that foraminifera can not only incor- porate chloroplasts for photosynthetic activity but may also 1.2 Sampling location Kiel Fjord benefit from other catabolic mechanisms (LeKieffre et al., 2018). This means these are not only C or N pathways; one Foraminifera studied here were collected in the Kiel Fjord in of these mechanisms could also be the sulfur cycle (Jauf- northern Germany. The Kiel Fjord covers 9.5 km in length. It frais et al., 2019b). Recent studies showed that foraminifera is about 250 m wide in the south (inner fjord) and widens to host sulfur cycle bacteria which have the potential to act the northern part to a width of 7.5 km (outer fjord) (Nikula as endobionts (Salonen et al., 2019).
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