Effects of temperature, light and salinity on cyst production and morphology of Tuberculodinium vancampoae (the resting cyst of Pyrophacus steinii)

https://doi.org/10.1016/j.revpalbo.2006.09.001Get rights and content

Abstract

Cyst forming dinoflagellates are useful in reconstructing past environments. For accuracy it is essential to know how environmental parameters such as salinity, temperature and light influence dinoflagellate cyst production and morphology. Here the effect of variation in these parameters on production and morphology of Tuberculodinium vancampoae (the resting stage of Pyrophacus steinii) is detailed. Encystment of T. vancampoae has been observed in all studied culture-experiments although only a few cysts are being formed at the limits of the temperature and salinity ranges (16.5°C, 34.8 °C and 20, 45 psu) with highest cyst production at 27 °C and 35 psu. Temperature clearly affects cyst morphology; cysts formed in cultures grown at 16.5 °C and 34.8 °C possess small, flattened processes. These cysts are not completely absent in cultures grown at intermediate temperatures but form only a minor part of the association.

In previous studies, salinity has been found to influence the cyst morphology of several dinoflagellate species but this seems not to be the case for T. vancampoae. In this study there was no morphological variation related to salinity.

High cyst production was observed in cultures grown under moderate to strong illumination but variation in illumination did not lead to morphological change.

Our findings correspond to field observations where T. vancampoae has been observed in surface sediments of the sub-tropical to tropical regions characterised by mean sea surface temperatures between 12.7 °C and 29.5 °C, and sea surface salinities between 16.9 and 36.6 psu.

In contrast to previous suggestions, T. vancampoae appears to be heterothallic rather than homothallic.

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)

  • P.J. Mudie et al.

    Dinoflagellate cysts, freshwater algae and fungal spores as salinity indicators in Late Quaternary cores from Marmara and Black Seas

    Mar. Geol.

    (2002)
  • T. Radi et al.

    Dinocyst distribution in surface sediments from the northeastern Pacific margin (40–60° N) in relation to hydrographic conditions, productivity and upwelling

    Rev. Palaeobot. Palynol.

    (2004)
  • T.A. Thorsen et al.

    Climatically influenced distribution of Gymnodinium catenatum during the past 2000 years in coastal sediments of southern Norway

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (1998)
  • S.M. Adl et al.

    The new higher level classification of Eukaryotes with emphasis on the taxonomy of protists

    J. Eukaryot. Microbiol.

    (2005)
  • I. Balzer et al.

    Photoperiodism and effect of indoleamines in a unicellular alga Gonyaulax polyedra

    Science

    (1991)
  • W. Brenner

    Organic walled microfossils from the central Baltic Sea, indicators of environmental change and base for ecostratigraphic correlation

    Baltica

    (2001)
  • W. Brenner et al.

    Öko- und chronostratigraphische Korrelierung der Zentralen Ostsee mit der Kieler Bucht anhand organisch-wandiger Mikrofossilien

    Meyniana

    (2002)
  • B. Dale

    Dinoflagellate cyst ecology: modeling and geological applications

  • E.Y. Dawson

    Marine Botany — An Introduction

    (1966)
  • M. Ellegaard et al.

    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.

    (2002)
  • M. Ellegaard et al.

    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

    (2003)
  • W.R. Evitt

    Observations on the morphology of fossil dinoflagellates

    Micropaleontology

    (1961)
  • Cited by (21)

    • Molecular methods for cost-efficient monitoring of HAB (harmful algal bloom) dinoflagellate resting cysts

      2019, Marine Pollution Bulletin
      Citation 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).

    • Atlas of modern dinoflagellate cyst distributions in the Black Sea Corridor: from Aegean to Aral Seas, including Marmara, Black, Azov and Caspian Seas

      2017, Marine Micropaleontology
      Citation 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 Reviews
      Citation 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.

    View all citing articles on Scopus
    View full text