Tropical red alga Compsopogon caeruleus: an indicator of thermally polluted waters of Europe in the context of temperature and oxygen requirements

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Abstract

INTRODUCTION

The red alga Compsopogon caeruleus (Balbis ex C. Agardh) Montagne 1846: 154 (as ‘coeruleus’) is a widespread species in freshwater as well as marine tropical and subtropical ecosystems (Guiry and Guiry 2022). This macroalga has often been described as a native species in the Americas, e.g., USA (Florida) and Brazil, Asia, e.g., India, Africa, e.g., Algeria, and the Pacific Islands, e.g., USA (Hawaiian Islands) (Starmach 1977, Guiry and Guiry 2022). In addition, C. caeruleus populations have been found in ecosystems outside their natural range, such as in rivers and channels in Central Europe, which contain thermally contaminated waters due to discharge from factories and powerhouses (Fig. 1, Supplementary Table S1) (Weiss and Murray 1909, Täuscher 2012, Žáková et al. 2013). However, this nonnative and, according to us, potentially invasive species is best ecologically suited to the southern part of the European continent. Based on a report published a decade ago, C. caeruleus is present in only a few independent stands in Europe (Eloranta and Kwandrans 2012). In our opinion, this perspective requires substantial extension and revision.

Fig. 1

Distribution of Compsopogon caeruleus in Europe. Red circles, stands in natural and seminatural habitats reported in the literature and herbaria materials; green circle, the new stand from Licheńskie Lake (Poland); blue circle, location in the Eire River (Germany) where the reference material was collected. The dotted lines (orange and green) indicate the range of climate zones (Köppen 1900, Beck et al. 2018).

Moreover, artificial systems in Europe, e.g., garden ponds, glass / palm houses, and public / private aquaria with tropical animals and vascular plants, can host C. caeruleus (Starmach 1978, Battiato et al. 1979, Szymańska and Krupińska 1983, Gärtner 1987, Stoyneva et al. 2006). Although these reports incidentally called these systems “new stands”, we disagree with this classification, as these locations seen as artificial “enclaves” are entirely irrelevant for biogeographical studies of C. caeruleus, including studies on the expansion, population dynamics and distribution patterns of this species. However, from such an artificial system, nonnative tropical species, including C. caeruleus, may “escape” into the local environment (Zhan et al. 2021). Importantly, such a scenario is only possible if this kind of species encounters favorable conditions in a given country, allowing gradual acclimatization and further spreading. To date, in Central Europe, stable populations of C. caeruleus, which have survived the winter, have been recorded only in constantly thermally contaminated water ecosystems (Weiss and Murray 1909, Täuscher 2012, Žáková et al. 2013, 2015).

The structure of the C. caeruleus thallus is very characteristic among red alga and usually shaped like a horse’s tail, but the color of the thallus varies from dark olive, greenish, and bluish to violet–green (Krishnamurthy 1962, Starmach 1977, Eloranta and Kwandrans 2007, 2012, Sheath and Vis 2015). C. caeruleus is most often a benthic alga (attaches to water plants, macroalgae or stones with rhizoids or basal discs), but sometimes, it can be found in free-floating forms (Starmach 1977, Zhan et al. 2021).

The genus Compsopogon Montagne 1846 belongs to the family Compsopogonaceae (order: Compsopogonales, class: Compsopogonophyceae, subphylum: Proteorhodophytina, phylum: Rhodophyta) (Guiry and Guiry 2022). Historically, the Compsopogon genus was thought to include approximately 20 species (Guiry and Guiry 2022); however, as a result of the molecular revision, it was found that most of the organisms belong to the same species, namely, C. caeruleus (Balbis ex C. Agardh) Montagne 1846 (Necchi et al. 2013, Nan et al. 2016). Therefore, the following synonyms of C. caeruleus are used: C. hookeri Montagne 1846, C. chalybeus Kützing 1849, C. aeruginosus (J. Agardh) Kützing 1849, C. leptoclados Montagne 1850, C. lividus De Toni 1897, C. oishii Okamura 1915, C. minutus C. C. Jao 1941, C. iyengarii Krishnamurthy 1958, C. indicus Das 1963, C. lusitanicum M. P. Reis 1977, C. corticrassus Chihara & Nakamura 1980, C. aegyptiacus A. A. Aleem 1981, C. prolificus Yadava & Kumano 1985, C. tenellus Y. J. Ling & S. L. Xie 1998, C. aeruginosus var. catenatum Yadava & Pandey 1980, Compsopogonopsis leptoclados (Montagne) V. K. Krishnamurthy 1962 and Compsopogonopsis japonica Chihara 1976. Currently, within the genus Compsopogon, there are only six different species with taxonomically accepted names. Among these six species, C. argentinensis Pujals 1967, C. corinaldii (Meneghini) Kützing 1857, C. lividus De Toni 1897, C. occidentalis Tracanna 1980, and C. sparsus S. L. Xie & Y. J. Ling 1998 were recorded only in freshwater habitats, while C. helwanii El-Gamal & Salah El-Din 1999 was associated with sulphate springs (Guiry and Guiry 2022). C. caeruleus, the most common species in both hemispheres, has the widest range of tolerance to salinity and thus is found in freshwater, brackish and marine habitats (Guiry and Guiry 2022). In natural and seminatural ecosystems, populations of C. caeruleus develop mainly in flowing waters with temperatures above 20°C, high oxygenation and conductivity, and neutral pH (Tomás et al. 1980, Eloranta and Kwandrans 2007, Koletić et al. 2020b).

This work aims to update the understanding of the distribution of C. caeruleus in the water ecosystems of Europe, taking into account new findings and reviewed ecological data covering over 100 years. Moreover, in a novel assessment, we performed an ex situ characterization of how a temperature gradient (20–40°C) influences oxygen consumption by the thalli of C. caeruleus.

Our results fundamentally change the current view regarding the optimal temperature requirements and biogeography of this red alga, and this report describes a new and first stand of C. caeruleus in Poland (currently the northernmost and easternmost area of Europe where this species has been found). The potential application of C. caeruleus as an indicator of thermally polluted waters is highlighted.

MATERIALS AND METHODS

Lacustrine location of Compsopogon caeruleus

The samples of the studied red alga were collected from a stand in the artificially heated waters of Licheńskie Lake (52°18′56.9″ N, 18°21′05.0″ E; Licheń, Greater Poland) in June 2021 and September 2022. Licheńskie Lake is a seminatural ecosystem and belongs to the Konin-Pątnów powerhouse cooling system (Table 1, Fig. 2). This waterbody is eutrophic (according to Carlson indices), monomictic with a volume of 6,712.3 m³, has a water surface of approximately 147 ha, and has a mean depth of 4.5 m (Table 1) (Pyka et al. 2007, Ejsmont-Karabin and Hutorowicz 2011, Bogacka-Kapusta and Kapusta 2013, Ejsmont-Karabin et al. 2020, Zdanowski et al. 2020). In this thermally polluted lake (where the average water temperature of the epilimnion in summertime ranges from 25 to 28°C) (Table 2), Vallisneria spiralis L. (commonly known as tape grass) is the dominant macrophyte and forms dense phytocoenoses along the shoreline (Gąbka 2002, Hutorowicz 2006, Ejsmont-Karabin and Hutorowicz 2011, Bogacka-Kapusta and Kapusta 2013, Ejsmont-Karabin et al. 2020). The thermal pollution of Licheńskie Lake is defined as deviation from the natural temperature in a habitat resulting from elevated temperature associated with industrial cooling activities (Dodds and Whiles 2010).

Table 1

Morphometric and thermal data of the Konin Lakes included in the cooling water system of coal-fired Pątnów-Konin powerhouses

Fig. 2

(A) Licheńskie Lake in detail. (B) Schematic of the water cooling system for two powerhouses at Konin Lakes. Blue arrows, intake of cooling waters; red arrows, discharge of heated waters; PP, Pątnów powerhouse; KP, Konin powerhouse; 1, location of the new Compsopogon caeruleus population in Europe; 2, channels of the cooling system; 3, cold water flow direction; 4, heated water flow direction; 5, Vallisneria spiralis meadows; 6, stand of C. caeruleus in the lake.

Table 2

Summer epilimnion water temperatures (mean values, with the range in parentheses) of Licheńskie Lake from 1965–2018 (Ejsmont-Karabin et al. 2020)

RESULTS

Stand, morphology, and ecology of Compsopogon from Poland

The presence of C. caeruleus has not been officially recorded in seminatural or natural habitats in Poland (outside closed artificial habitats such as aquaria). The new stand of C. caeruleus in Central Europe was located along the shoreline of Licheńskie Lake. The thalli of this red alga grew on the long leaves of the tropical vascular plant V. spiralis in summertime (Fig. 3A). The morphology of lacustrine C. caeruleus is consistent with the outline of previously described specimens from other freshwater habitats (see above). The thalli were greenish blue and strongly branched, especially in the middle part, with a length of 1 mm to 15 cm and a width of filaments 50–2,000 μm. The uniseriate central axis contained flat cells with a length of 50–140 μm and a width of 50–250 μm (Fig. 3G). The central axis of the thallus was constricted at the base and attached to the substratum with the help of the conical basal holdfast (Fig. 3B). The cortex consisted of polygonal or irregular cells (15–40 μm × 20–40 μm) (Fig. 3H) and formed colorless rhizoids in the middle and basal parts of filaments (Fig. 3C & D). The cortical cells contained several discoid-shaped, parietal, and olive-green chloroplasts (Fig. 3H). The young uniseriate filaments of lateral branches (without cortex layers) consisted of discoidal or cylindrical cells that were apically rounded (Fig. 3F). Monosporangia with an irregular shape were present mainly in the upper parts of the thalli and were 15–22 μm in diameter (Fig. 3H).

Fig. 3

Habitat and thalli of Compsopogon caeruleus from Licheńskie Lake. (A) Meadow of tape grass (white circle, thalli of C. caeruleus on Vallisneria spiralis leaves). (B) Thalli with conical basal holdfast (black arrow). (C) Basal part of thalli with visible colorless rhizoids (black arrows). (D) Cortex of thallus with (on the left side) and without (on the right side) rhizoids. (E) Irregular cells of the cortex. (F) Young uniseriate filament without cortex. (G) Central axis consisting of flattened cells. (H) Cortex layer with monosporangium (black arrow). (I) Details of the cortex layer. Scale bars represent: B & C, 200 μm; D & E, 100 μm; F, 50 μm; G–I, 20 μm.

The C. caeruleus thalli we studied were found in water with a mean temperature of 27.6°C, basic pH (8.6), and proper aerobic conditions (average oxygenation level: 79%, average oxygen concentration: 6.4 mg L⁻¹) (Table 3). The water was greenish (with a chlorophyll a concentration of 21.5 μg L⁻¹), but the sandy bottom was completely visible to a depth of 50 cm. The water color was 25 Pt-Co units on average, and the turbidity ranged from 18 to 23 nephelometric turbidity units (NTU). Notably, high concentrations of CaCO₃ (283.2 mg L⁻¹) and SO₄²⁻ (77.1 mg L⁻¹) were salient features of the C. caeruleus habitat, which had average concentrations of mineral compounds. Therefore, moderate levels of conductivity (617.3 μS cm⁻¹) and TDS (375.2 mg L⁻¹) were observed. The chemical analysis showed that the concentrations of nutrients were high (PO₄³⁻, 0.1 mg L⁻¹; NH₄⁺, 0.2 mg L⁻¹; and NO₃⁻, 0.9 mg L⁻¹) (Table 3).

Table 3

Physicochemical and biological properties of the water (mean values, with the range in parentheses) from the stand of Compsopogon caeruleus in Licheńskie Lake (n = 10)

Temperature affects oxygen consumption by Compsopogon caeruleus thalli

Among the five different temperatures tested, i.e., 20, 25, 30, 35, and 40°C, the maximal respiratory rate of C. caeruleus thalli at a steady state (V_Omax) was achieved at two temperatures, namely, 35 and 40°C, with rates of 228.24 ± 20.44 and 231.34 ± 22 nmol O min⁻¹ g⁻¹ of thallus, respectively (Fig. 4). The lowest V_O was observed at 20°C (48.12 ± 6.58), but the rate was just over double the value at 25°C (108.1 ± 9.7). Interestingly, the dark respiration rate can also be approximately doubled for this species after a shift from 20 to 25°C (Necchi and Zucchi 2001). At 30°C, another increase in the V_O was observed (128.4 ± 10.66), and this increase almost doubled after the transition to higher temperatures (35 and 40°C). This trend was also observed for the reference C. caeruleus from SAG with very similar values of V_O and V_Omax. Our results fit the general observation for plants where the respiratory rate can be doubled per 10°C rise in temperature (Q₁₀ = 2) (Atkin and Tjoelker 2003). However, we also observed that a 5°C rise in temperature can lead to this type of change in V_O. This means that the acceleration of oxygen metabolism may depend on starting temperature, i.e., for C. caeruleus, the shift from 20 to 25 or 30 to 35°C resulted in an approximate doubling in V_O, but the other doubling in V_O occurred for the change from 25 to 35°C. Again, it fits the Q₁₀ interpretation in the context of V_O changes, as the value of this factor is not constant and influenced by the temperature range (Atkin and Tjoelker 2003). Targeting nucleotide metabolism combined with oxygen metabolism, we used exogenous nucleotides such as ATP, ADP, GTP, and GDP (up to 2 mM). However, the addition of these nucleotides did not influence the V_O regardless of the temperature.

Fig. 4

(A) Schematic representation of the oxygraph chamber with a water jacket and Clark-type electrode. (B) Representative oxygraphic traces (series of technical repetition) of Compsopogon caeruleus thalli (from Licheńskie Lake) exposed to different temperatures (oxygen content on the x-axis is exponential, where 100 indicates full air saturation and 0 indicates anoxia). (C) The effect of temperature change on respiratory rate at steady state (V_O) expressed in nmol O min⁻¹ g⁻¹ of C. caeruleus thallus. ns, non-statistically significant; ***, statistically significant (p < 0.001).

DISCUSSION

Currently, the presence of C. caeruleus, a nonindigenous European algal flora species (with presumable origins in South America), has been reported mainly in the southern and southwestern parts of the continent (Fig. 1, Supplementary Table S1) (Koletić et al. 2020b, Guiry and Guiry 2022). In particular, the natural and seminatural freshwater and brackish riverine ecosystems of continental Spain are inhabited by C. caeruleus (Donze 1968, Tomás et al. 1980, 2013, Tomás 1981, 1988, Álvarez Cobelas 1984, Busquets et al. 1985, Aboal 1986, Aboal Sanjurjo 1989, Sabater et al. 1989, Aboal et al. 1994, Cantoral Uiza and Aboal Sanjurjo 2001, Edigos and Aboal 2003, Sánchez Castillo et al. 2011, Chapuis et al. 2014, García-Fernández et al. 2015). Stands of this alga in the Spanish Canary Islands have still not been reported, although the presence of this species in that area is mistakenly indexed in AlgaeBase (Guiry and Guiry 2022). In the area of the Mediterranean Sea, island populations of C. caeruleus were found in Mallorca (Balearic Islands, Spain) (Sánchez Castillo et al. 2011) and Malta (Maltese Archipelago, Europe) (Battiato et al. 1979). The Mediterranean basin’s subtropical climate favors this species in a few locations in France (originally identified as C. hookeri or C. aeruginosus [J. Agardh] Kützing) (Boillot 1958, Eloranta et al. 2011, Breton 2014) and Croatia (Koletić et al. 2019, 2020a, 2020b).

The earliest, i.e., from December 1908, record of C. caeruleus (originally identified as C. leptocladus) in a European location with a humid oceanic climate, namely, the United Kingdom (Manchester), concerns the Reddish Canal water (approximately 23°C), which was contaminated with artificially heated water from cotton factories (Weiss and Murray 1909); the species was observed again decades later (Fig. 1, Supplementary Table S1) (Blackler and Krishnamurthy 1961, Krishnamurthy 1962). The occurrence of all known populations of C. caeruleus found in Germany (some identified as C. hookeri Montagne) was also correlated with the postindustrial discharge of heated water (Friedrich 1966, 1973, Mauch et al. 2003, Hussner and Lösch 2005, Täuscher 2012). The same is true for Central European areas with a humid continental climate; in Austria and the Czech Republic, populations of C. caeruleus (first identified as C. aeruginosus [J. Agardh] Kützing) were observed in flowing-water habitats that were affected by thermal pollution from a chemical factory and nuclear powerhouse (Eloranta et al. 2011, Žáková et al. 2013). As the Reddish Canal in Manchester was closed many years ago, the currently described stand of C. caeruleus in Poland constitutes a novel record and the northernmost habitat of this species in Europe; the southernmost population of this red alga was found on Malta Island (Battiato et al. 1979).

Over the last 60 years, the biodiversity of Polish freshwater ecosystems has been profoundly influenced by the introduction of nonindigenous species (Najberek and Solarz 2011). A major biogeographical change occurred with the opening of coal-fired powerhouses, which typically use natural water (from nearby ponds, lakes, and rivers) for cooling installations. The discharge of heated water directly into the environment creates places that are called “invasion gates” for alien plant and animal species (Wilk-Woźniak and Najberek 2013). The Konin Lakes have been affected by this practice since 1958; thus, these lakes have been the object of eco-bioinvasive research and modeling for global warming changes (Zdanowski et al. 2020, Dziuba et al. 2021). This semiartificial lake system with heated waters (sometimes called “heated islands”) imitates the thermal conditions of tropical ecosystems; therefore, it can be easily colonized by alien organisms preferring warmer waters (Wilk-Woźniak and Najberek 2013). The Konin Lakes are inhabited by approximately 100 alien species, including vascular plants such as V. spiralis and Hygrophila polysperma (Indian swampweed) and animals such as Dreissena polymorpha (zebra mussel), Sinanodonta woodiana (Chinese pond mussel), and Pseudorasbora parva (topmouth gudgeon) (Gąbka and Owsianny 2009, Najberek and Solarz 2011, Zdanowski et al. 2020). The toxic bloom-forming cyanobacteria Raphidiopsis raciborskii (syn. Cylindrospermopsis raciborskii) and green microalgae Hariotina polychorda (syn. Coelastrum polychordum) have been reported among the microorganisms found in these lakes (Berger et al. 2006, Wilk-Woźniak and Najberek 2013). Alien species that achieve substantial biomass, e.g., tape grass and clams, and therefore modulate the structure and function of the Konin Lakes should be considered invasive. Unfortunately, people may treat Konin Lakes as a place where they can throw away unwanted tropical animals and plants. As a curiosity, some aquarium animals but alien species for Europe, such as herbivorous piranha (unpublished data without species details) and turtle, i.e., Trachemys scripta elegans known as the red-eared slider (personal observation), were noted in Konin Lakes. We can only presume how C. caeruleus was introduced into Licheńskie Lake, intentionally or accidentally. It is a very high probability that this red alga presence in Poland is a consequence of human activity.

No reports concerning the invasive potential of C. caeruleus, which inhabits artificially heated aquatic ecosystems of Europe, have been published to date. Currently, this red alga does not achieve substantial biomass in Licheńskie Lake. However, C. caeruleus, an epiphytic or epilithic species, is a competitor for native phytobenthos species such as micro- and macroalgae or animals, e.g., Rotifers, because it occupies habitat niches and exploits environmental resources such as nutrients, light, and oxygen. In this context, C. caeruleus has already modified or disrupted the ecosystem in which it began colonizing. Therefore, at this moment, we propose to use the term “potentially invasive species” for this red alga. The aspects and details of C. caeruleus synecology in semiartificial habitats of Europe require further research.

Notably, the bioindication potential of C. caeruleus is proposed here. Generally, species or communities that help to evaluate the quality of the environment affected by natural and / or anthropogenic changes over time are named bioindicators (Holt and Miller 2010, Parmar et al. 2016). For example, the presence of a given species in a stressed ecosystem is often correlated with the transmission of physicochemical factors such as temperature. According to the classification of bioindicators accepted by the World Conservation Union or International Union for Conservation of Nature in the context of our analyses, C. caeruleus may fit the subtype termed the “pollution bioindicator”. Our point of view is based on the fact that outdoor populations of C. caeruleus occur yearly and only in constantly thermally contaminated ecosystems of humid oceanic and humid continental climate zones of Europe (Fig. 1), i.e., C. caeruleus thalli are able to regenerate after possibly cold winters (December–March) but without a drop in water temperature below 0°C (Supplementary Table S1). More than 100 years ago, it was suggested that this red alga is prone to be winter-killed in an outdoor garden without heating based on observations in Great Britain (Colley 1916). The exact low and lethal water temperature for C. caeruleus has not been reported to date. In the Konin Lakes system, Ślesińskie Lake is the coldest (the average annual temperature of the water surface varies from 13.4 to 13.9°C), while Licheńskie Lake, in which C. caeruleus was found, is the warmest (the average annual temperature of the water surface varies from 15.6 to 16.6°C) (Tables 1 & 2, Fig. 1) (Ejsmont-Karabin et al. 2020). It must be noted that in Licheńskie Lake, even during the winter, the water temperature is never lower than 6.6°C (when powerhouses are working), and during the summertime, the surface water reaches temperature approximately 30°C (Table 2) (Zdanowski and Prusik 1994, Socha and Hutorowicz 2009, Najberek and Solarz 2011, Ejsmont-Karabin et al. 2020). Similarly, C. caeruleus was identified in the thermally polluted Dyje River in the Czech Republic during the vegetation period, which may reach only 0.8°C in winter (Žáková et al. 2013, 2015). Therefore, we can only surmise that the abovementioned low-temperature values make it possible for this species to survive in a given ecosystem in a resting form / stage. Accordingly, this red alga provides the bioindication potential for constant thermal pollution derived from human activity.

Moreover, our interpretation of C. caeruleus presence in some regions of Europe is fundamental for assessing the expansion of tropical algae outside the natural range. Importantly, the occurrence of C. caeruleus and its use as the bioindicator constitutes a considerable advantage compared to the manual / automatic measurement of water temperature from time to time. For example, during winter, the water temperature in Licheńskie Lake, which hosts C. caeruleus, may be as low as 6.6°C (Table 1). Such a temperature value measured directly by thermometer during warm winters in lakes / rivers of Poland, and other countries with a moderate climate, does not necessarily indicate permanent thermal pollution of the water ecosystem. In such cases, whether the measurement of water temperature is the result of weather conditions or temporary / constant thermal contamination may be ambiguous.

For many organisms, including algae, oxygen respiration is essential for maintaining metabolic homeostasis, and adequate nucleotide metabolism ensures survival (Woyda-Ploszczyca and Rybak 2021). Nucleoside diphosphate kinase (NDPK) is an important enzyme that regulates the pools of various nucleotides in cells. This transphosphorylase affects cell division by providing building blocks for the synthesis of DNA and RNA; for instance, this enzyme produces GTP via the following reaction: ATP + GDP → ADP + GTP. During the oxygraph measurement experiments, regardless of the temperature, C. caeruleus thalli did not respond to exogenously administered purine nucleotides (ATP, ADP, GTP, and GDP) as substrates or products related to NDPK. This could mean that the endogenous nucleotides were at saturating concentrations, and the cultivation medium fulfilled the requirements for proper growth. NDPK is a thermostable and well-conserved enzyme among different species (prokaryotic and eukaryotic), and the temperature of half denaturation for this kinase may reach 76°C; thus, 37°C can be the optimal temperature for the function of this kinase, while 60°C can completely inhibit its function (Miranda et al. 2008, Georgescauld et al. 2013). Therefore, our temperature gradient probably did not inhibit NDPK or other enzymes that are involved in nucleotide metabolism. It must be highlighted that unsuitable low or high temperatures (nonoptimal) may limit plants, including algae, development, e.g., growth rate, by decreasing enzyme activities / capacities and ultimately depleting ATP level below requirements (Raven and Geider 1988, Atkin and Tjoelker 2003, Nejrup et al. 2013, Ahmad et al. 2020).

The record presented in this paper substantially extends our knowledge about the eastward and northward distribution of C. caeruleus in Europe. The maximal water temperature of the seminatural habitats in which C. caeruleus has been found thus far is 32.2°C (Supplementary Table S1) (Žáková et al. 2013, 2015). However, the optimal temperature that supports the highest frequency of C. caeruleus, e.g., from natural ecosystems in Croatia (Neretva River valley), is approximately 25°C (Eloranta and Kwandrans 2007, Koletić et al. 2020b). A temperature of 25°C seems to be the most favorable for populations of C. caeruleus in non-European (Brazilian) regions, considering photosynthetic performance (Necchi 2006). Surprisingly, according to our ex situ polarographic measurements with the Clark-type oxygen electrode, the previously modeled thermal optimum for this red alga could be an underestimate. In our study, the shift from 35 to 40°C (independent measurements) did not result in further increases in the V_O of C. caeruleus thalli, which can mean that 35°C is a borderline temperature for optimal development (Fig. 4). Therefore, the optimal temperature for growth of C. caeruleus may be increased by at least 10°C. Our results are strongly supported by laboratory findings that place the maximum photosynthesis rate of Compsopogon at 30–35°C (Kremer 1983, Necchi and Zucchi 2001, Sheath and Vis 2015). We are aware that regional ecotypes may differ in their environmental requirements, which explains variations in data concerning the optimum temperature for C. caeruleus. However, if 35°C is more optimal for the metabolic pathways of C. caeruleus, including respiration and photosynthesis, tested under laboratory conditions in different countries over nearly 40 years, namely, for populations of Poland (this paper) and Germany (Kremer 1983, Necchi and Zucchi 2001, Sheath and Vis 2015), this feature is relatively independent of geography. In this context, it could mean that even potential genetic variation between different populations did not affect the general metabolic strategy of this species. Such an interpretation is supported by our results concerning measurements of respiratory rates because regardless of C. caeruleus thalli origination, we observed very similar values of V_O for a given temperature. Moreover, C. caeruleus from Licheńskie Lake revealed 100% identity with C. caeruleus from SAG, taking into account COI (OP747576) and V9 (OP737799) sequences.

Finally, we propose that C. caeruleus can populate warmer habitats, e.g., those affected by thermal pollution. Therefore, the presence of C. caeruleus in moderate climate zones can be a simple and easy-to-recognize (even without taking the thallus samples) indicator of artificially and permanently heated systems by a regular discharge of postindustrial water. Such conditions, combined with other environmental factors (e.g., nutrient levels), favor the expansion of alien species in a given region of Europe. The Konin Lakes can be a model for tracking the mechanisms of tropical / subtropical species adaptation into generally colder climatic zones. The growing demand for electricity and the resulting higher discharge of heated water may favor the development of this nonnative algae species in Europe. Interestingly, C. caeruleus can transiently survive even at 40°C (Fig. 4). Notably, only time will reveal how the distribution of this red alga will expand in response to an additional factor, i.e., an increase in the average annual temperature due to global warming. Importantly, changes in plant respiration influenced by temperature are currently seen as a crucial feature of the ecosystem response to global climate change (Atkin and Tjoelker 2003). Institutions responsible for environmental monitoring using phytobenthos as a bioindicator of the ecological state should include in their training programs and protocols information on the possibility of observing mesophilic macroalgae, such as C. caeruleus, in aquatic ecosystems.

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