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Mesocosm and Microcosm Experiments on the Feeding of Temperate Salt Marsh Foraminifera

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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/334147804 Mesocosm and Microcosm Experiments On the Feeding of Temperate Salt Marsh Foraminifera Article in The Journal of Foraminiferal Research · July 2019 DOI: 10.2113/gsjfr.49.3.259 CITATIONS READS 2 322 4 authors, including: Petra Mudie Alastair Simpson Dalhousie University Dalhousie University 194 PUBLICATIONS 7,274 CITATIONS 274 PUBLICATIONS 12,497 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Handbook of the Protists View project Atlas of Dinoflagellate Cysts of the Black Sea Corridor, including Caspian, Aral Seas. View project All content following this page was uploaded by Petra Mudie on 04 July 2019. The user has requested enhancement of the downloaded file. Journal of Foraminiferal Research, v. 49, no. 3, p. 259–274, July 2019 MESOCOSM AND MICROCOSM EXPERIMENTS ON THE FEEDING OF TEMPERATE SALT MARSH FORAMINIFERA Jennifer L. Frail-Gauthier1,*, Peta J. Mudie1, Alastair G. B. Simpson2 and David B. Scott1 ABSTRACT logic history since the Cambrian, because they are important biostratigraphic tools and key proxies for interpreting the Agglutinated foraminifera dominate in temperate salt paleoecology of ancient seas and fluctuations in relative sea marsh sediment, making them key indicators for monitoring level (RSL). The ecology of modern foraminifera has been sea level and environmental changes. Little is known about discussed in several major texts (Lee & Anderson, 1991; the biology of these benthic foraminifera because of difficul- Murray, 2006), but these reveal that many basic questions ties in distinguishing live from dead specimens in laboratory about feeding, growth, and reproduction remain unresolved cultures. We present data from 10 years of laboratory exper- and little explored since the early work of Bradshaw (1957, iments using comparisons of the agglutinant trochamminids 1968) and Arnold (1974). Limited information is also Trochammina inflata and Entzia macrescens and the mili- available in Murray & Alve (1999). This lack of knowledge olid Miliammina fusca with the calcareous rotalids Helenina is particularly acute for agglutinated marsh species and anderseni and Elphidium williamsoni. Specimens were taken other benthic foraminifera (Kitazato & Bernhard, 2014). from a laboratory mesocosm representing Chezzetcook Inlet, In effect, most environmental interpretations are based a cool-temperate salt marsh in eastern Canada. We deter- simply on relating generalised modern distributions to mined culture requirements for the agglutinated foraminifera abiotic conditions such as salinity, temperature, oxygen, and in Petri dishes over 10–12 week periods. Five inexpensive, marsh elevation. These must remain circumstantial until the non-terminal ways of identifying live organisms were devel- biological factors that constrain foraminiferal occurrences oped: spatial movement, detritus-gathering, attachment, clus- are understood, including their complex feeding habits tering, and test opacity. Comparison with rose Bengal staining (Goldstein, 1999; Mojtahid et al., 2011). For example, showed <10% diversion for calcareous species and T. inflata the notoriously high patchiness of foraminifera (e.g., Lee, but M. fusca was over-counted by >30%. Terminal chambers 1974) could be governed by food availability, feeding meth- of Trochammina inflata were examined by transmission elec- ods, competition with meiofauna, abiotic factors (salinity, tron microscopy to visualise food consumption and identify elevation), or a combination of some or all of these. food in digestive vacuoles, both in specimens from mesocosm A key objective of our study is to expand knowledge of and in culture. Bacteria and unidentified detritus in the vac- the trophic niches that control the spatial and temporal pop- uoles establish that this agglutinated species is a saprophagous ulation dynamics of temperate salt marsh foraminifera evi- and bacterivorous detritivore. The adhesive secretions by these dent in pioneering Quaternary paleo-sea level studies (e.g., species apparently help them gather and possibly farm food Scott et al., 2001 and references therein; Kemp et al., 2011, while being relatively immobile in the sediments. Our obser- 2013). Within the suite of salt marsh marker species, aggluti- vations of movement and feeding orientation in the aggluti- nated taxa, such as Entzia (Jadammina) macrescens (Brady, nants suggest links between form and function that underscore 1970), Miliammina fusca (Brady), and Trochammina inflata their value as ultra high resolution sea-level proxies. Meso- (Montagu), are the main tools for paleoenvironmental work cosm biomass and abundance counts show that foraminifera in coastal environments because of their better preserva- represent >50% of the meiofaunal biomass, emphasising their tion potential in acidic salt marsh sediments compared to importance in the food web and energy-flow dynamics of tem- calcareous taxa (reviewed in Berkeley et al., 2007). Most perate salt marsh systems. trophic niche studies, however, have focused on calcareous taxa common on mudflats or in deeper coastal water, in- INTRODUCTION cluding Ammonia beccari/tepida (Cushman), Haynesina ger- manica (Ehrenberg), and Elphidium spp. Montfort (Dupuy Although foraminiferal biology has been extensively et al., 2010; Seuront & Bouchet, 2015; Jauffrais et al., 2016). studied for over 150 years (e.g., Myers, 1943; Arnold, 1974; Thus, previous conclusions about the behavioural, feeding, Loeblich & Tappan, 1988; Sen Gupta, 1999; Murray, 2006; and biotic interactions of salt marsh benthic foraminifera Kitazato & Bernhard, 2014), details of their feeding remain are based on a restricted part of the total assemblage and enigmatic. Most studies of foraminifera focus on taxonomy, do not consider the agglutinated species that are widespread faunal assemblages, or distributions in marine and brackish throughout the entire salt marsh and often present in ex- environments, both around the world and throughout geo- tremely high abundances. Direct observation of feeding and behavioural habits in dominant salt marsh foraminifera is crucial for inferring 1 Department of Earth Sciences, Life Science Centre, Dalhousie Uni- their role in the ecosystem, but few studies have exam- versity, 1355 Oxford Street, Rm 3006, Halifax, Nova Scotia, Canada ined these species in incubator (microcosm) cultures (Gold- B3H 4R2 stein & Alve, 2011; Weinmann & Goldstein, 2016; van Dijk 2 Department of Biology, Life Science Centre, Dalhousie University, 1355 Oxford Street, P.O. Box 15000, Halifax, Nova Scotia, Canada B3H et al., 2017). Past observations and/or feeding experiments 4R2 have shown that benthic foraminifera can be photosyn- * Correspondence author. E-mail: [email protected] thetic (hosting diatoms), chemosynthetic (hosting bacteria), 259 Downloaded from https://pubs.geoscienceworld.org/cushmanfoundation/jfr/article-pdf/49/3/259/4788203/i0096-1191-49-3-259.pdf by Dalhousie Univ Libraries Serials/Killam Library user on 03 July 2019 260 FRAIL-GAUTHIER AND OTHERS fluorescent dye (CellTrackerTM Green, CTG) is very expen- sive and also requires specialised fluorescence microscopes for time-consuming stain-reaction studies that are difficult to quantify (Figueira et al., 2012). We sought to determine suitable non-harmful and inexpensive methods for exam- ining living populations of agglutinated foraminifera with thick, opaque tests by compiling a check-list of criteria to distinguish living benthic salt marsh foraminifera from dead specimens in laboratory experiments. The salt marsh mesocosm in the Dalhousie Aquatron (Scott et al., 2014) allowed implementation of feeding tri- als with foraminifera and meiofauna from a cool temper- ate environment on a year-round basis over a period of five years. Additionally, new observations could be made on the key agglutinated and calcareous salt marsh paleo-sea level proxies that have been overlooked in past biological stud- ies of foraminifera and marshes in warmer regions (e.g., Texas and California: Bradshaw, 1957, 1968; Georgia and Florida, USA: Weinmann & Goldstein, 2016). Our work as- Figure 1. Five species used for culturing and feeding experiments. sesses the feeding habits of the mesocosm temperate climate Top row: agglutinants (A) Miliammina fusca, with small horse-shoe- salt marsh foraminifera by direct observation of specimens shaped terminal aperture; (B) Entzia macrescens, with arenaceous test in vitro and by investigation of detritus accumulation around and small, round terminal aperture; (C) Trochammina inflata, organics tests. The accumulation of detritus at the terminal cham- at aperture (arrow). Bottom row: calcareous (D) Elphidium williamsoni and (E) Helenina anderseni. Scale bar = 100 µm. ber aperture (Goldstein, 1999) or around the whole speci- men (Arnold, 1974) has been previously called formation of “feeding cysts” (Heinz et al., 2005). Transmission electron herbivorous (grazing on diatom mats), detritivorous, carniv- microscopy (TEM) of the food vacuoles in the agglutinant orous, or parasitic (e.g., Lee & Anderson, 1991; Bernhard & Trochammina inflata was used to provide novel information Bowser, 1992; Sen Gupta, 1999; Suhr et al., 2003; Mojtahid on feeding mechanisms in selected individuals fed with un- et al., 2011; Jauffrais et al., 2016). Their crucial importance altered marsh mud or with marsh bacteria isolates. Biomass in some ecosystems is evident from the
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