Unprecedented slow growth and mortality of the rare colonial cyanobacterium, Nostoc zetterstedtii, in oligotrophic lakes

Abstract

Centimeter-large colonies of Nostoc zetterstedtii from a Swedish oligotrophic lake had the lowest growth and mortality rates of any studied temperate macrophyte. Annual growth rates at two shallow sites averaged 0.57-0.73 3 10 23 d 21 , corresponding to doubling times of colony dry weight in 2.6-3.3 yr. With such low growth rates, the largest colonies measuring 7 cm in diameter are 24-31 yr old. We found no mortality of incubated colonies and calculated the mortality rate to , 7.3 3 10 25 d 21 and the life span to . 24 yr in accordance with age of the largest colonies. The firm gelatinous tissue of high mass density, low nutrient content, and antibacterial property can account for the low growth and mortality rates. The measured daily surplus of photosynthesis minus respiration can support only small increments of the large mass per colony surface in accordance with the low growth rates. Growth and mortality rates of N. zetterstedtii correspond best with general allometric relationships for macroalgae using surface area to carbon biomass as the scaling parameter, but measurements are lower than predictions probably because of extra costs to sustain the substantial colony matrix. N. zetterstedtii is adapted to pristine Lobelia lakes with clear water and chronically low nutrient levels, but it is threatened by strong attenuation of light by brownification or eutrophication.

Comparative growth and metabolism of gelatinous colonies of three cyanobacteria, Nostoc commune, Nostoc pruniforme and Nostoc zetterstedtii, at different temperatures

“…Oxygen values were converted to carbon values assuming a 1 : 1 molar ratio between exchange of O 2 and DIC as previously found for N. pruniforme and N. zetterstedtii (Raun et al ., ; Sand‐Jensen et al ., ). Colony dry weight was converted to organic carbon content (Col C ) using the measured average percentage of C to DW of 40.8% (Sand‐Jensen & Møller, ). Thus:…”

“…Because N. zetterstedtii has a much harder and denser colony matrix than N. commune and N. pruniforme , it is expected to grow much more slowly than the other two species because of greater costs to produce and maintain the massive colony matrix. Investment in a dense and chemically well‐protected colony matrix should, on the other hand, ensure low mortality and extended survival, as previously shown for N. zetterstedtii (Sand‐Jensen et al ., ; Sand‐Jensen & Møller, ), illustrating the common trade‐off between growth and persistence (Sand‐Jensen & Borum, ; Cebrian & Duarte, ; Poorter et al ., ). We examined experimentally if observed growth rates and estimated growth rates from the photosynthetic–respiratory balance are indeed low for all three species and particularly low for N. zetterstedtii and whether growth rates decline as anticipated with increasing colony size of N. pruniforme and N. zetterstedtii .…”

“…It is recognised for its unprecedented ability to survive extended periods of frost, drought and extreme temperatures (−269–70 °C) as inactive dry crusts, while the colony rapidly swells and reactivates ion exchange, photosynthesis and respiration at moderate temperatures (0–35 °C) when water becomes available (Scherer et al ., ; Sand‐Jensen & Jespersen, ). The high annual temperature ranges in the terrestrial habitats of N. commune under arctic (about −60–25 °C; Davey, ) and temperate (about −30–50 °C) conditions (Sand‐Jensen & Jespersen, ) suggest that the species may possess a broader temperature tolerance also in the active rehydrated stage than N. pruniforme and N. zetterstedtii living under more dampened annual temperature ranges typically between 0 and 25 °C in north‐temperate lakes (Sand‐Jensen & Møller, ). We compared growth and metabolism of these three colonial Nostoc species of different form and habitat in experiments at different temperatures (6–43 °C) and evaluated their adaptation and growth strategy.…”

“…Extensive self‐shading, low photosynthetic rates, high proportions of dark respiration to photosynthesis and high ratio of dry mass to surface area of the thick colonies of all three Nostoc species suggest that they should grow slowly (Raun et al ., ; Sand‐Jensen et al ., ; Sand‐Jensen & Jespersen, ). Field measurements have confirmed unprecedented low in situ growth rates of N. zetterstedtii in an oligotrophic, softwater lake corresponding to doubling of the colony dry matter in 2.6–3.3 years (Sand‐Jensen & Møller, ). A close negative relationship of growth rate to colony size, volume to surface area (V:SA) and dry mass to surface area (DW:SA) of plants and macroalgae can be deduced from first principles (Nielsen & Sand‐Jensen, ; Lambers & Poorter, ; Markager & Sand‐Jensen, , ).…”

Inverse relationship of epilithic algae and pelagic phosphorus in unproductive lakes: Roles of N2 fixers and light

“…In a previous study, the dominance of gelatinous taxa has indeed been shown to correlate with increased epilithon C:P and N:P ratios (Liess & Kahlert, ). In addition, Sand‐Jensen and Møller () observed molar ratios of C:P > 5,700 and of N:P > 680 in Nostoc zetterstedtii in a Swedish lake, but this appears to be an extreme value and more data are needed to describe the elemental stoichiometry of N 2 ‐fixing benthic cyanobacteria.…”