Effects of temperature, light and salinity on cyst production and morphology of Tuberculodinium vancampoae (the resting cyst of Pyrophacus steinii)
Introduction
The number and distribution of cysts in sediments is, among other factors, fundamentally 40 influenced by the production of cysts. In turn, cyst production can be strongly influenced by the environmental conditions within the habitat of the cyst forming dinoflagellates and as result, cyst associations in sediments can reflect these conditions in detail. Many studies have used these associations to reconstruct past environmental parameters such as temperature, salinity and nutrient input or industrial pollution (e.g. Thorsen and Dale, 1998, Marret et al., 2001, Mudie et al., 2002, Pross and Brinkhuis, 2005, de Vernal et al., 2005). Morphological variation within a cyst population of a single species has often been observed and it has been suggested that this might be related to environmental variability and as such might be an additional tool to reconstruct past environments (Wall and Dale, 1973, Nehring, 1994a, Dale, 1996, Brenner, 2001, Mudie et al., 2001, Marret et al., 2004). Indeed, recent studies have show that some environmental factors can have severe effects on cyst morphology (e.g. Kokinos and Anderson, 1995, Lewis and Hallett, 1997, Lewis et al., 1999, Hallett, 1999, Ellegaard, 2000, Ellegaard et al., 2002). Variations in salinity and a combination of salinity and temperature are especially known to affect the cyst morphology of some dinoflagellate cyst species. This can occur in such an extreme way, that the individual cyst morphotypes produced in a single unicellular culture were considered to be formed by different species when found in fossil sediments, e.g. Spiniferites (Ellegaard, 2000, Ellegaard et al., 2002).
Until now, no relationship between cyst morphology and light intensity has been documented despite the fact that this factor is known to influence the encystment of several dinoflagellate species. An inverse relationship between day length and encystment rates has been documented in cultures grown at temperatures between 20 °C and 25 °C. This inverse relationship was not the result of the total daily irradiance but was thought to be related to variations in the intensity and angle of radiation, the amount of sea surface reflection and the transparency of the water column (Dawson, 1966, Kirk and Tilney-Basset, 1978, Tett, 1990, Balzer and Hardeland, 1991, Godhe et al., 2001, Sgrosso et al., 2001). Sgrosso et al. (2001) found that cyst production was prevented by light breaks during the dark phase of the photocycle.
To use variation in cyst morphology to reconstruct past environments, detailed information about the relationship between this morphological variation and environmental conditions must be available (Servais et al., 2004, Brenner, 2005). However, although the discussion about the potential causal relationship between environmental conditions and cyst morphology has been a point of discussion for several decades (e.g. Evitt, 1961, May, 1977, Sarjeant et al., 1987) relatively little is known yet. Until now the relationship between cyst morphology and environment is available for a limited number of species (e.g. Lingulodinium machaerophorum (Deflandre and Cookson, 1955) Wall, 1967, Gonyaulax baltica Ellegaard et al., 2002, and some species within the Gonyaulax spinifera species complex (Lewis and Hallett, 1997, Hallett, 1999, Kouli et al., 2001, Ellegaard et al., 2002, Adl et al., 2005). In this study we investigate the effect of variations in temperature, salinity and light intensity on the morphology of Tuberculodinium vancampoa (Rossignol, 1962) Wall, 1967, the resting stage of the phototrophic dinoflagellate Pyrophacus steinii by growing it under different temperature, salinity and light conditions using a temperature and light gradient box.
Section snippets
Material and methods
Cysts were isolated from surface sediments collected from the Omura Bay (Nagasaki Prefecture, Kyushu, Japan) in September 2003. The sediment samples were stored at 4 °C and in the dark. Subsamples were rinsed with artificial sea water (salinity 34.5 psu; HW Meersalz Professional, Wiegandt GmbH, Krefeld, Germany) and sieved through a 20 μm nickel precision sieve (Stork Veco, mesh: 570). The sieved residue was than cleaned by ultrasound and rinsed again. Individual cysts were isolated with a
Temperature experiment
Cyst production took place at all tested temperatures (Fig. 1). The maximum number of cyst were produced at 27 °C (2905 cysts). At 30.2 °C cyst production was also relatively high (1322 cysts) whereas at 34.8 °C, 20 °C and 16.5 °C cyst production was much lower (4, 72 and 8 cysts respectively).
No significant relationship between central body length, central body width and the ratio between central body length/width in relation to temperature differences was observed (Fig. 1A–C). In contrast,
Discussion and conclusions
Pyrophacus steinii is an armoured dinoflagellate that, until now has been considered to be one of the few species with a heterothallic sexual reproduction (Pholpunthin et al., 1999). Of our study with 22 unicellular cultures, only three produced cysts. These cultures were “non-crossed” but in the cultures crossed, no cysts were observed. This indicates that P. steinii can have a homotallic sexual reproduction as is known for most dinoflagellate species. Indeed only a few species are known to be
Acknowledgements
We thank Kazumi Matsuoka for providing the opportunity to sample fresh sediment material in the Omura Bay during the field trip of Seventh International Conference on Modern and Fossil Dinoflagellates (September 2003, Nagasaki, Japan). We thank Rex Harland and an anonymous reviewer for the useful suggestions that improved, especially, the readability of the manuscript. Monika Kirsh is thanked for the help in culturing Pyrophacus Steinii. This study was financed by the German Science foundation,
References (45)
Holocene environmental history of the Gotland Basin (Baltic Sea) — a micropalaeontological model
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2005)- et al.
Reconstruction of sea surface conditions at middle to high latitudes of the Northern Hemisphere during the Last Glacial Maximim (LGM) based on dinoflagellate cyst assemblages
Quat. Sci. Rev.
(2005) Morphological and abundance variations in Homotriblium-cyst assemblages related to epositional environments; uppermost Oligocene – Lower Miocene, Jylland, Denmark
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2004)Variations in dinoflagellate cyst morphology under conditions of changing salinity during the last 2000 years in the Limfjord, Denmark
Rev. Palaeobot. Palynol.
(2000)- et al.
Temperature effects on growth and cell size in the marine calcareous dinoflagellate Thoracosphaera heimii
Mar. Micropaleontol.
(2000) - et al.
Spiniferites cruciformis: a fresh water dinoflagellate cyst?
Rev. Palaeobot. Palynol.
(2001) - et al.
Atlas of modern organic-walled dinoflagellate cyst distribution
Rev. Palaeobot. Palynol.
(2003) - et al.
New organic-walled dinoflagellate cysts from recent sediments of Central Asian seas
Rev. Palaeobot. Palynol.
(2004) Distribution patterns of dinoflagellate cysts and other organic-walled microfossils in recent Norwegian–Greenland Sea sediments
Mar. Micropaleontol.
(1995)- et al.
Late Quaternary dinoflagellate cysts from the Black, Marmara and Aegean seas: variations in assemblages, morphology and paleosalinity
Mar. Micropaleontol.
(2001)
Dinoflagellate cysts, freshwater algae and fungal spores as salinity indicators in Late Quaternary cores from Marmara and Black Seas
Mar. Geol.
Dinocyst distribution in surface sediments from the northeastern Pacific margin (40–60° N) in relation to hydrographic conditions, productivity and upwelling
Rev. Palaeobot. Palynol.
Climatically influenced distribution of Gymnodinium catenatum during the past 2000 years in coastal sediments of southern Norway
Palaeogeogr. Palaeoclimatol. Palaeoecol.
The new higher level classification of Eukaryotes with emphasis on the taxonomy of protists
J. Eukaryot. Microbiol.
Photoperiodism and effect of indoleamines in a unicellular alga Gonyaulax polyedra
Science
Organic walled microfossils from the central Baltic Sea, indicators of environmental change and base for ecostratigraphic correlation
Baltica
Öko- und chronostratigraphische Korrelierung der Zentralen Ostsee mit der Kieler Bucht anhand organisch-wandiger Mikrofossilien
Meyniana
Dinoflagellate cyst ecology: modeling and geological applications
Marine Botany — An Introduction
Cyst-theca relationship, life cycle, and effects of temperature and salinity on the cyst morphology of Gonyaulax baltica sp. nov. (Dinophyceae) from the Baltic Sea area
J. Phycol.
Morphological and LSU rDNA sequence variation within the Gonyaulax spinifera – Spiniferites group (Dinophyceae) and proposal of G. elongata comb. nov. and G. membranacea comb. nov
Phycologia
Observations on the morphology of fossil dinoflagellates
Micropaleontology
Cited by (21)
Dinoflagellate planktonic-motile-stage and benthic-cyst assemblages from a monsoon-influenced tropical harbour: Elucidating the role of environmental conditions
2019, Estuarine, Coastal and Shelf ScienceMolecular methods for cost-efficient monitoring of HAB (harmful algal bloom) dinoflagellate resting cysts
2019, Marine Pollution BulletinCitation Excerpt :High cyst abundance in bottom sediments have been reported in areas characterized by a high frequency of dense toxic algal blooms, which mainly occur in the temperate seas (McGillicuddy et al., 2003; Bravo et al., 2006; Anglés et al., 2010). Resting cyst production, which seems to be triggered by stress or unfavourable conditions, is a part of the sexual reproduction stage of the dinoflagellate life cycle (Figueroa and Bravo, 2005; Kremp et al., 2009; Zonneveld and Susek, 2007; Wagmann et al., 2012). Phytoplankton resting stages are a common strategy conferring several ecological advantages, such as genetic recombination, dispersal, and seeding or regulation of the seasonal succession of dinoflagellates (Anderson et al., 2005; Figueroa et al., 2007; Smayda and Trainer, 2010).
Marine productivity, water column processes and seafloor anoxia in relation to Nile discharge during sapropels S1 and S3
2018, Quaternary Science ReviewsAtlas of modern dinoflagellate cyst distributions in the Black Sea Corridor: from Aegean to Aral Seas, including Marmara, Black, Azov and Caspian Seas
2017, Marine MicropaleontologyCitation Excerpt :Wall (1967) describes the archeopyle as large and polyhedral; however, Matsuoka et al. (1998) consider that the archeopyle is a compound epicystal type although its outline cannot clearly be ascribed to apical or precingular plates arranged in longitudinal rows. T. vancampoae is the cyst of Pyrophacus steinii (Schiller) Wall and Dale, 1971 and has been cultured to show that it grows in a range of salinity from 20 to 45 without significant change in morphology (Zonneveld and Susek, 2007) but tubercle length is strongly influenced by temperature above and below 27 °C within the range from c. 16.5–34.8. In the BSC, Pyrophacus steinii is part of the Black Sea plankton (Gómez and Boicenco, 2004) but the cysts have not been found in surface sediment although T. vancampoae occurs sporadically in late Pleistocene – earliest Holocene sediments of cores from Marmara Sea (Londeix et al., 2009; Roberts, 2012).
Eemian sea-level highstand in the eastern baltic sea linked to long-duration white sea connection
2014, Quaternary Science ReviewsCitation Excerpt :Today's global distribution of Tuberculodinium vancampoae shows few records where summer SSTs are below 15 °C, and abundances exceeding 2% only above 17 °C (Zonneveld et al., 2013), and the modern distribution of the motile stage is warm temperate to tropical (Faust, 1998). Culturing experiments have shown that while cysts hatched at 16 °C, the optimal temperature was 27 °C (Zonneveld and Susek, 2007). Judging from the Lusitanian/Mediterranean affinities of T. vancampoae and T. pellitum and overall modern distribution patterns for these species, summer SSTs must have exceeded 17 °C for the sample at 29.6 m.