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Harmful Algae
journal homepage: www.elsevier.com/locate/hal
Causal relationships of Raphidiopsis (formerly Cylindrospermopsis) dynamics
with water temperature and N:P-ratios: A meta-analysis across lakes with
diferent climates based on inferential modelling
Friedrich Recknagel
a,
⁎
, Tamar Zohary
b
, Jacqueline Rücker
c
, Philip T. Orr
d,1
,
Christina Castelo Branco
e
, Brigitte Nixdorf
c
a
University of Adelaide, School of Biological Sciences, Adelaide, Australia
b
Israel Oceanographic and Limnological Research, Kinneret Limnological Laboratory, Migdal, Israel
c
Brandenburg University of Technology, Department of Freshwater Conservation, Bad Saarow, Germany
d
Seqwater, Brisbane, Australia
e
Federal University of the State of Rio de Janeiro, Rio de Janeiro, Brazil
ARTICLEINFO
Keywords:
Raphidiopsis raciborskii
Meta-analysis
Four lakes
Climate
Eutrophication
Hybrid evolutionary algorithm HEA
Water temperature
N:P-ratios
Phenology
ABSTRACT
Raphidiopsis raciborskii is a tropical toxic cyanobacterium that is rapidly expanding to diverse lake habitats in
diferent climate zones by sophisticated adaptation mechanisms.
This meta-analysis investigated correlations of R. raciborskii with water temperature and N:P (nitrogen to
phosphorus)-ratios across four lakes with diferent climates and trophic states by means of long-term time series
and the hybrid evolutionary algorithm HEA. The results have shown that in the lakes with temperate and
Mediterranean climate, R. raciborskii is strongly correlated with water temperature since germination and
growth rely on rising water temperatures in spring. In contrast, there was a weaker correlation with water
temperature in subtropical and tropical lakes where pelagic populations of R.raciborskii are overwintering, and
are present all year round. However, the highest abundances of R. raciborskii coincided with highest water
temperature for the Mediterranean, subtropical and tropical lakes, whilst in the temperate Langer See the highest
abundances of R.raciborskii occurred at 24.1 °C, even though temperatures of up to 27 °C were recorded in 2013
and 2014. The correlation of R.raciborskii with N:P-ratios proved to be strongest for the meso- to eutrophic Lake
Kinneret (r
2
= 0.8) and lowest for the eutrophic Lake Paranoa (r
2
= 0.16). However, the assumption has been
confrmed that R.raciborskii is growing fastest when waters are N-limited regardless of trophic states. In terms of
phenology, the temperate and Mediterranean lakes displayed “fastest growth” in spring and early summer. In
contrast, the growing season in subtropical and tropical lakes lasted from spring to autumn most likely because
of overwintering populations, and growing importance of direct and indirect biotic regulating factors such as
competition, grazing, remineralisation of nutrients along warming climate. In order to carry out a meta-analysis
of time series across four diferent lakes, HEA served as powerful tool resulting in inferential models with
predictive capacity for population dynamics of R. raciborskii just driven by water temperature or N:P-ratios,
whilst coefcients of determination r
2
served as criteria for hypotheses testing.
1. Introduction
The expanding global distribution of Raphidiopsis raciborskii
(Wołoszyńska) Aguilera, Berrendero Gómez, Kastovsky, Echenique &
Salerno (Aguilera et al., 2018) is attributed to a suite of sophisticated
adaptation mechanisms characteristic of this bloom-forming nostoca-
lean cyanobacterium. Akinetes that germinate only when water
temperatures exceed 15 °C enable R. raciborskii to survive the cold
months in temperate waters (Padisak, 1997; Rücker et al., 2009). In
terms of nitrogen consumption, R. raciborskii shows a preference for
dissolved inorganic (ammonium, nitrate) and organic (urea) forms of
nitrogen (e.g. Saker and Neilan, 2001; Ammar et al., 2014; Burford
et al., 2018), whilst heterocyte cells allow R. raciborskii to grow in N-
limited waters by performing N
2
-fxation (e.g. Plominsky et al., 2013).
https://doi.org/10.1016/j.hal.2019.04.005
Received 30 October 2018; Received in revised form 10 April 2019; Accepted 10 April 2019
⁎
Corresponding author.
E-mail address: friedrich.recknagel@adelaide.edu.au (F. Recknagel).
1
Present address: Grifth University, Australian Rivers Institute, Nathan, Australia.
Harmful Algae 84 (2019) 222–232
1568-9883/ © 2019 Elsevier B.V. All rights reserved.
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