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Seasonality in Lipid Content of the Demosponges Halichondria Panicea and H

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Seasonality in Lipid Content of the Demosponges Halichondria Panicea and H University of Southern Denmark Seasonality in lipid content of the demosponges Halichondria panicea and H. bowerbanki at two study sites in temperate Danish waters Lüskow, Florian; Kløve-Mogensen, Kirstine; Tophøj, Jakob; Pedersen, Lars Haastrup; Riisgård, Hans Ulrik; Eriksen, Niels Thomas Published in: Frontiers in Marine Science DOI: 10.3389/fmars.2019.00328 Publication date: 2019 Document version: Final published version Document license: CC BY Citation for pulished version (APA): Lüskow, F., Kløve-Mogensen, K., Tophøj, J., Pedersen, L. H., Riisgård, H. U., & Eriksen, N. T. (2019). Seasonality in lipid content of the demosponges Halichondria panicea and H. bowerbanki at two study sites in temperate Danish waters. Frontiers in Marine Science, 6, [328]. https://doi.org/10.3389/fmars.2019.00328 Go to publication entry in University of Southern Denmark's Research Portal Terms of use This work is brought to you by the University of Southern Denmark. Unless otherwise specified it has been shared according to the terms for self-archiving. If no other license is stated, these terms apply: • You may download this work for personal use only. • You may not further distribute the material or use it for any profit-making activity or commercial gain • You may freely distribute the URL identifying this open access version If you believe that this document breaches copyright please contact us providing details and we will investigate your claim. Please direct all enquiries to [email protected] Download date: 03. Oct. 2021 fmars-06-00328 June 11, 2019 Time: 18:1 # 1 BRIEF RESEARCH REPORT published: 12 June 2019 doi: 10.3389/fmars.2019.00328 Seasonality in Lipid Content of the Demosponges Halichondria panicea and H. bowerbanki at Two Study Sites in Temperate Danish Waters Florian Lüskow1†, Kirstine Kløve-Mogensen2, Jakob Tophøj2, Lars Haastrup Pedersen2, Hans Ulrik Riisgård1 and Niels Thomas Eriksen2* 1 Department of Biology, Marine Biological Research Centre, University of Southern Denmark, Kerteminde, Denmark, 2 Department of Chemistry and Bioscience, Aalborg University, Aalborg, Denmark Edited by: This study relates the lipid content of two marine filter-feeding demosponges, Oscar Monroig, Spanish National Research Council Halichondria panicea and H. bowerbanki to the seasonal availability of their suspended (CSIC), Spain food, mainly free-living bacteria and phytoplankton at two study sites in Danish waters. Reviewed by: The aim was to investigate if the lipid content of sponges is linked to food availability and Gilles Barnathan, L’Université Nantes Angers Le Mans season, and to what extend free-living bacteria are available in starvation periods where (L’UNAM), France the phytoplankton biomass is low. The highest concentrations of bacteria were observed Lorenzo Gallus, during summer when also chlorophyll a concentrations were high, and therefore bacteria University of Genoa, Italy and phytoplankton were available in similar ratio at all seasons. Bacterial cell carbon *Correspondence: Niels Thomas Eriksen was estimated to contribute 2.9 and 4.6% compared to phytoplankton cell carbon in [email protected] the food at the two sites, respectively, and free-living bacteria were available only as a †Present address: minor food source at all seasons. Highest lipid contents (29.5% of sponge dry weight) Florian Lüskow, Department of Earth, Ocean were seen in H. panicea at the site with lowest food availability, while the lipid content and Atmospheric Sciences, University of H. bowerbanki was 11.5% of dry weight. No seasonal variations in lipid content as of British Columbia, Vancouver, BC, fraction of sponge dry weight were observed, and the lipid content was not affected by Canada food availability or starvation. It remains unclear why the lipid-content levels at the two Specialty section: study sites were conspicuously different. This article was submitted to Aquatic Physiology, Keywords: free-living bacteria, phytoplankton, fatty acids, filter-feeding, seasonality, lipids, Porifera a section of the journal Frontiers in Marine Science Received: 26 March 2019 INTRODUCTION Accepted: 28 May 2019 Published: 12 June 2019 Halichondria is a common demosponge in for example coastal Dutch (Hummel et al., 1988), Citation: German (Barthel, 1986, 1989), Polish (Chojnacki, 2000), and Danish waters (Riisgård et al., 1993; Lüskow F, Kløve-Mogensen K, Olesen and Weeks, 1994). Sponges are sessile filter-feeders, evolutionary adapted to nourish on Tophøj J, Pedersen LH, Riisgård HU a dilute suspension of microscopic food particles, mainly phytoplankton and free-living bacteria and Eriksen NT (2019) Seasonality (Riisgård et al., 2016). Food uptake is low in autumn and winter (Koopmans et al., 2015) when in Lipid Content of the Demosponges low phytoplankton biomass may result in starvation and temporarily decreasing condition index, Halichondria panicea and H. bowerbanki at Two Study i.e., the ratio of organic to inorganic matter (Barthel, 1986; Lüskow et al., 2019). The seasonal role Sites in Temperate Danish Waters. of possible energy-storage compounds in sponges is largely unknown. Analysis of the biomass Front. Mar. Sci. 6:328. composition of H. panicea from Kiel Bight revealed glycogen and lipid contents of 10–30 mg doi: 10.3389/fmars.2019.00328 per g ash-free dry weight and 80–140 mg per g ash-free dry weight, respectively (Barthel, 1986). Frontiers in Marine Science| www.frontiersin.org 1 June 2019| Volume 6| Article 328 fmars-06-00328 June 11, 2019 Time: 18:1 # 2 Lüskow et al. Seasonality of Lipids in Halichondria Sponges Neither the lipid, nor the glycogen content seemed, however, by relatively high phytoplankton biomass and the presence of to be affected by season (Barthel, 1986). Glycogen is present a closely related species, H. bowerbanki. The aim was to link only in low quantities (<1–3.7% of the dry weight), while lipids the lipid content of sponges to seasonal food availability with may constitute up to 17.3% of the dry weight in demosponges particular emphasis on the importance of free-living bacteria (Stone, 1970; Elvin, 1979). Potentially, lipids may therefore pose in order to achieve a better understanding of their nutritional the largest energy-storage potential in demosponges, but this has role for sponges. hardly been studied since sponges have no organs or real tissue that may store fat (Rod’kina, 2005). Sponges contain the greatest diversity of fatty acids among MATERIALS AND METHODS aquatic animals (Rod’kina, 2005), including a variety of long chain (>C22) fatty acids, which are synthesized by elongation Collection and Storage of Sponges of fatty acids from the diet (Carballeira et al., 1986; Rezanka Halichondria panicea (Fleming, 1828) was regularly collected and Sigler, 2009) and used as structural components in cellular in the inlet to Kerteminde Fjord, Denmark (55◦26'59.1"N membranes (Rod’kina, 2005). Short chained C16 and C18 fatty 10◦39'41.0"E), while H. bowerbanki (Burton, 1930) was collected acids may also be abundant in H. panicea and other sponges in Frederik den VII’s Kanal, an excavated harbor channel (Lawson et al., 1984; Rod’kina et al., 2003, Rod’kina, 2005). connected to Limfjorden, Denmark (56◦57'51.1"N 9◦14'27.0"E) Palmitic acid (C16:0) and stearic acid (C18:0) account for 1.5– between October 2016 and September 2017. Five specimens were 33.0% of the fatty acids in most sponges (Rod’kina, 2005). These cleaned of epifauna, weighed and stored separately in plastic fatty acids can be acquired directly from the diet, but their bags at −20◦C until analysis. Specimens were identified based metabolic roles in sponges have not attracted much attention. on spicule morphology as H. panicea in Kerteminde Fjord and Sponges also contain filter-feeding trapped phytoplankton and as H. bowerbanki in Frederik den VII’s Kanal. free-living bacteria (Thomassen and Riisgård, 1995) as well as various symbiotic microorganisms (Lee et al., 2001; Hentschel Dry Weight and Lipid Content et al., 2006), which also contribute to the lipids that can be The wet weight of sponge specimens was measured after extracted from sponges (Rod’kina, 2005). water at their surface had been removed by a napkin. Dry Sponges efficiently retain free-living bacteria and other weight was measured after drying for 24 h at 100◦C. Ash free particles down to about 0.1 mm in diameter (Fjerdingstad, 1961; dry weight was measured after incubation for 6 h at 500◦C. Reiswig, 1971, 1975; Langenbruch, 1983; Leys et al., 2011) and Concentrations of carbon present in sponges were estimated are thus more efficient in retaining such small particles than using a conversion factor of 0.142 mg C per mg sponge dry weight other co-occurring marine filter-feeding animals, such as, e.g., (Thomassen and Riisgård, 1995). Lipid contents were quantified blue mussels (Lüskow and Riisgård, 2018). The importance of in lyophilized subsamples of sponge tissue (approximately 1 g) bacteria versus phytoplankton has therefore been debated (see, after 24 h of extraction in chloroform/methanol and subsequent e.g., Koopmans et al., 2015; Riisgård et al., 2016) and bacteria evaporation of the solvent as described by Pleissner and Eriksen contribute approximately 20% of the diet of sponges in Danish (2012). Fatty acids were subsequently transmethylated in 3 ml waters (Lüskow et al., 2019). Since odd numbered long chain fatty CH OH:HCl:CHCl (10:1:1 v/v/v) at 90◦C for 1 h, and the fatty acids, stemming from elongation of shorter chain odd numbered 3 3 acid methyl esters were extracted in hexane and analyzed using fatty acids of bacterial origin can be found in sponges, including GC-FID, as also described by Pleissner and Eriksen(2012). H. panicea from coastal Dutch waters, bacteria certainly play a nutritional role (Carballeira et al., 1986; Koopmans et al., 2015). Coastal seawater contains 106 to 5 × 106 free-living bacteria Chlorophyll a and Bacterial ml−1 (Azam et al., 1983; Fenchel, 2008).
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