Primary production is important to all ecosystems as it supplies energy to other living organisms, thereby forming the foundation of food webs. Macroalgae are the dominant primary producers in coastal temperate marine ecosystems, representing some of the highest recorded per-area basis production values (Field et al., 1998; Gattuso et al., 2006). As macroalgae contribute significantly to total global system carbon production (Hill et al., 2015) it is important to understand better how macroalgal primary production links to growth in biomass and how different environmental factors affect these patterns.

Traditionally, the primary production of macroalgae has been quantified using detached pieces of algal thally or whole plants (Littler and Littler, 1980; Gómez et al., 1997) and more recently, the production of macroalgae has been measured directly in natural assemblages (Binzer and Middelboe, 2005; Tait and Schiel, 2010). While the first approach enables quantification of accurate response functions between different environmental variables and primary production (e.g., irradiance–net photosynthesis curves), the latter technique allows the scaling up of primary production in natural conditions. The estimates of primary production are highly dependent on the scale of observation with photosynthetic production being higher at individual than at community levels (Binzer et al., 2006; Pärnoja et al., 2014). Likewise, scale affects how macroalgae respond to changes in ambient conditions. The photosynthesis of individual plants often shows a typical light saturation curve (Lobban et al., 1985), whereas macroalgal photosynthesis in assemblages increases in a roughly linear fashion up to maximum levels of natural irradiance (Middleboe and Binzer, 2004). Changes in biomass integrate the net photosynthetic fixation of inorganic carbon into autotrophic biomass as well as the processes of natural loss of biomass and thereby permits estimation of large-scale variation in realized production over time. Expectedly, when compared to the patterns of photosynthesis, another set of combinations of environmental factors can influence change in macroalgal biomass or the same relationships can have very different functional shapes. In this respect, laboratory experiments have shown species-specific responses of macroalgae to environmental change in which macroalgal growth may increase, decrease or remain unchanged with increasing rates of plant photosynthesis (de los Santos et al., 2000; Israel and Hophy, 2002; Kim et al., 2016). Thus, understanding the nature of scale-dependence in macroalgal production can help to elucidate some of the possible controls by which primary production is incorporated into autotrophic biomass. Despite this importance, knowledge of such controls is limited as few studies have been undertaken to date that quantify the patterns of macroalgal production at different scales with most being performed under laboratory conditions (e.g., de los Santos et al., 2000; Israel and Hophy, 2002; Binzer and Middelboe, 2005; Pärnoja et al., 2014; Kim et al., 2016). Due to artificially induced conditions, as well as the use of separate phytoelements (thallus pieces, leaves), however, laboratory incubations often fail to characterize primary production to that which occurs in nature (Binzer and Middelboe, 2005; Binzer et al., 2006).

Primary production is controlled by both abiotic and biotic factors (Field et al., 1998; Hauxwell et al., 2003) but abiotic constraints are often dominant in natural environments (Hill et al., 2015). The availability of light and nutrients plays a crucial role in regulating primary production of macroalgae (Field et al., 1998; Hauxwell et al., 2003; Binzer et al., 2006). Light limitation may arise from the amount of irradiance arriving at the sea surface, the optical characteristics of water and self-shading within algal assemblages. The first two processes vary over multiple temporal and spatial scales and define the availability of light field above underwater canopies and the maximum photosynthetic rates of macroalgae (Kirk, 1994; Anthony et al., 2004). The third process, shelf-shading, is one of the most critical biological limitations because it sets an actual threshold for realized photosynthesis along vertical light gradient within macroalgal assemblages (Binzer et al., 2006; Tait and Schiel, 2010). The effect is stronger with increasing algal densities (Kotta et al., 2008; Paalme et al., 2013; Pärnoja et al., 2014) and in extreme cases, e.g., within giant kelp forests, only a fraction of light above algal canopy reaches the basal subcanopy species (Reed and Foster, 1984). This has large but mostly unknown affects on photosynthesis and growth of macroalgal assemblages. Even though algal photosynthesis is saturated in the upper layers of algal canopies with increasing irradiance, community photosynthesis will remain unsaturated because photosynthetic tissue in the lower layers of algal canopy has an unused photosynthetic potential (Binzer and Middelboe, 2005; Tait and Schiel, 2010).

Nutrient availability strongly affects the production of macroalgae but the responses are mostly taxon-specific and highly influenced by the local light climate (Raven and Hurd, 2012). Importantly, macroalgae can store nutrients in their tissue in order to overcome temporal disparity between nutrient availability and optimal growth season. For example, the marine Laminariales grow fastest during summer when irradiance is the highest, but when nutrients are depleted above the thermocline. During the peak growth the algae use their nitrogen and phosphorus reserves that were stored during winter when the nutrient availability is greater but light levels are lower (Chapman and Craigie, 1977; Lüning, 1990). In addition, the Charales can effectively transport nutrients from rhizoids (in sediment with high N and P but no light) to shoots (in water with low N and P but high light irradiance) (Vermeer et al., 2003). However, when nutrients are plentiful in the water column and light levels are sufficient to support photosynthesis, direct nutrient uptake from the water through the outer cells of the branchlets and stems is expected (Raven, 2003).

Temperature controls primary productivity of macroalgae to a lesser extent than light and nutrients unless the temperature is above or below the tolerances of the species. Within tolerance limits, macroalgae exhibit relative uniform responses to temperature change (Raven and Smith, 1978; Wiencke and tom Dieck, 1990). The species-specific temperature demands for survival and production relate to different types of temperature stress the macroalgal species have locally adapted (Breeman and Pakker, 1994). Controlled experimental trials further demonstrate the high plasticity of response of macroalgae to specific limiting temperature conditions in which a long-term acclimation of macroalgae at extreme temperatures significantly relaxes this temperature limitation (Nejrup et al., 2013). Thus, estimations of primary production in natural assemblages are increasingly relevant given the growing need for obtaining realistic response patterns to a complex of environmental factors.

Charophytes are found in diverse aquatic habitats, so this group consists of both early colonizers of newly-formed water bodies as well as species preferring more stable environmental conditions and habitats (Blindow and van de Weyer, 2016). The lush charophyte meadows play a underpinning role by providing food and/or refuge to zooplankton (Puche et al., 2020), benthic invertebrates (Kotta et al., 2004), fish and fish larvae (Hargeby et al., 2005), microbes (Kataržytė et al., 2017), and waterfowl (Schmieder et al., 2006). They also reduce water turbidity by stabilizing the sediment with rhizoids (Nõges et al., 2003), immobilizing nutrients (Kufel and Kufel, 2002), and inhibiting phytoplankton biomass (Hilt, 2015). Charophytes are most common in freshwater habitats but are also found in brackish water. The Baltic Sea is one of the best-studied brackish regions with respect to charophytes. In this marginal environment, the shallow low salinity embayments are often dominated by charophytes (Schubert and Blindow, 2003). The most common and widespread species in such habitats is Chara aspera Willd., a species characterized by a broad environmental niche space (Herkül et al., 2018).

To address the importance of scale on the factors regulating macroalgal production, we quantified experimentally the seasonal variability in individual photosynthesis, community production and biomass growth of the charophyte C. aspera in the brackish Baltic Sea. We then analyzed how seasonal change in the assemblage of environmental variables manifested in the production of macroalgae at these different scales. We hypothesized that C. aspera with its well-known broad environmental tolerances can maintain high photosynthetic and growth potential across wide gradients in light, temperature, and water nutrients. We also expected that the relationships between the environment and photosynthesis when assessed on individual plants are strong and simple. At the community level, however, charophytes have an ability to adjust photosynthesis and growth to a different set of environmental conditions. Moreover, below-ground processes may occasionally contribute to the oxygen fluxes. Therefore relationships between light, nutrient concentration, temperature, community photosynthesis and growth are weaker and more complex compared to individual plants.

In this study we experimentally quantified seasonal variability in individual photosynthesis, community production and growth in biomass of the charophyte C. aspera in the Baltic Sea along with the key environmental variables that are known to determine the production of macroalgae. We found that temperature and light availability were the best overall predictors of the production of C. aspera, followed by macroalgal coverage, flow velocity and water level. Importantly, the observed scale notably regulated the importance of different predictors, as well as the relationships between the environment and plant responses in the models. This implies that although the physiological responses of C. aspera should always be interpreted in the context of scale, temperature and light availability predict a significant proportion in the variability of charophyte production.

Low light can limit the production potential of temperate macroalgae, particularly during low-light seasons or in turbid waters (Wallentinus, 1978; Littler, 1980); many studies have suggested a direct dependence of charophytes on light availability (Libbert and Walter, 1985; Blindow, 2000; Schneider et al., 2006; Schubert et al., 2018). However, due to high tolerances of C. aspera to low light environments (Blindow, 1992; Sand-Jensen et al., 2000), we hypothesized that the species could maintain positive photosynthesis and growth potential in a wide range of light conditions. In general, this held true for individual photosynthesis, community production and growth in biomass. However, individual photosynthesis was typically higher than community production under the same light conditions. This difference in photosynthesis can be partly attributed to lower light availability (light limitation) in a three-dimensional algal canopy than to individual algae exposed to ambient light levels. For the same reason, the photosynthesis-irradiance curve at community level was smoother than that of individual plants. Specifically, different parts of the algal canopy are expected to receive different amounts of light and therefore are expected to respond differentially. For example, the upper parts may often be oversaturated with light, whereas lower parts are undersaturated. This results in different light adaptation (different light saturation points) along the spatial light gradient and a smooth response of the algal community to light. This also applies for C. aspera, which is known to increase the light saturation point of photosynthesis with increasing irradiance from 100 to 400 μmol quanta m^–2 s^–1 (Blindow et al., 2003). Similar responses of net photosynthesis along light gradients have been observed for C. aspera in other areas (Kovtun-Kante et al., 2014) and for other charophyte species, such as C. baltica and C. canescens (Küster et al., 2004). Beside shelf-shading, sediment respiration is an additional explanation for the differences between individual and community photosynthesis. At high load of organic debris and/or elevated temperatures algal respiration and sediment decomposition may dominate over benthic production (Carvalho et al., 2005).

Differential responses of photosynthesis and growth to light irradiance is also related to the different approaches used to calculate production at different scales. Specifically, the photosynthesis of individual plants and communities is expressed as relative change per plant biomass, whereas biomass growth is reported on an absolute scale. In spring and early summer with abundant light, photosynthesis of individual plants and communities is enhanced. However, the absolute change in biomass is actually low because the plants themselves are small. Later, when the plants are taller, biomass increases are greater despite moderate light conditions and low photosynthesis of individual plants and communities. This is happening because some inorganic carbon is fixed into autotrophic biomass even at low photosynthesis levels between 100 and 500 μmol quanta m^–2 s^–1.

In addition to light irradiance reaching the algal canopy, water turbidity affects light availability and the production of charophytes in many habitats (Hellström, 1991; Schneider et al., 2006). Likewise, the sediments in Rame Bay are composed of fine fractions (very fine sand, silt, and clay) and even slow underwater currents (1 cm s^–1) can bring silt and mud particles into the water column and thereby modulate the light environment as well as deposit sediment particles on plant thalli. Consequently, less light reaches plant photopigments and the rate of community photosynthesis and biomass growth decreases. This process is supported by experimental evidence in which long exposure to high levels of suspended sediment leads to cessation of growth and ultimately death of charophytes (Henricson et al., 2006). On the other hand, an experimental reduction of light availability to 25% of the natural irradiance does not induce a chronic compensatory reduction of the photosynthesis of charophyte communities (Kovtun-Kante et al., 2014). This suggests that charophytes recover easier from longer-term light reduction than sedimentation and may explain why water velocity (i.e., the intensity of resuspension) was the key predictor in the models of biomass growth. In addition to underwater currents, water level explained a significant part of charophyte growth in biomass. The current charophyte meadows are located in very shallow water (1 m) and a decline in water level of only a few tens of centimeters is expected to improve light conditions in the algal canopy.

It has been suggested that an increased production of photosynthetic pigments and chloroplasts supports more efficient production of charophytes and helps plants to recover when light becomes limiting (Andrews et al., 1984; Küster et al., 2000; Marquardt and Schubert, 2009). Our study did not support this, as variability in photosynthesis and growth along light gradient was independent of the chloroplast content of charophyte tissue. The chloroplast content was measured during fieldwork but due to lack of significance, the variable was not retained in the models and therefore not reported. It has been also suggested that charophytes elongate quickly when light levels are low. This adaptation enables charophytes to reach the water surface where light is more plentiful (Andrews et al., 1984; Henricson et al., 2006). However, the shoot elongation in C. aspera is salinity-dependent and brackish water plants fail to elongate under impoverished light conditions (Blindow et al., 2003). Our study corroborated this as underwater light conditions were not inversely related to plant production throughout the light gradient.

We also hypothesized that C. aspera could maintain positive production and growth potential in a wide range of temperature conditions. This hypothesis held true for individual and community photosynthesis but not for growth in biomass. Interestingly, photosynthesis in individual plants increased with increasing temperature throughout the gradient, whereas this temperature dependence translated into relatively stable positive community photosynthesis with somewhat higher photosynthesis at temperatures >14°C. Nevertheless, at temperatures >22°C benthic production declined substantially due to the dominance of below-ground processes (e.g., sediment decomposition) and algal respiration over algal production (Carvalho et al., 2005; Torn et al., 2006). Thus, C. aspera should sustain positive growth in its Baltic Sea habitats even under relatively extreme temperature conditions, which substantiates earlier studies showing that temperature does not significantly control photosynthesis and growth of charophytes (Raven et al., 1979; Libbert and Walter, 1985; Torn et al., 2006). Due to such broad temperature tolerance, charophytes are expected to benefit from contemporary climate change and broaden their distribution range in the Baltic Sea region (Torn et al., 2020).

Finally, we expected that C. aspera could maintain high photosynthesis and growth potential across wide gradients in water nutrients. This hypothesis was fully supported as nutrient concentrations in water were not significant in all models. Although charophytes are able to acquire nutrients from the water column (Raven, 2003), nutrient concentration in water has been shown to play a marginal effect on the physiological state of charophytes (Blindow, 1988; Munsterhjelm, 2005). Charophytes in our study area seem to rely on nutrients stored in their tissues as shown by the inverse relationship between macroalgal nutrient content and the photosynthesis of charophyte individuals (R² = 0.15). Such strategy is widely used among long-living macroalgae in order to overcome temporal and/or spatial mismatch between nutrient availability and optimal growth season (Chapman and Craigie, 1977; Lüning, 1990; Raven, 2003).

Prior to the study, we anticipated that models of photosynthesis in individual plants would involve fewer important environmental predictors than the models of photosynthesis and growth of charophyte communities. This prediction also held true. Although water temperature and light irradiance account for most of variability in the photosynthesis of individual plants, this share is less than in models of community photosynthesis and growth. The existence of a weak negative relationship between algal cover and community photosynthesis at the community level suggests that density dependence does play some role in photosynthesis regulation (Binzer and Middelboe, 2005; Tait and Schiel, 2010). Moreover, water properties (water level and flow velocity) were important in regulating charophyte growth. However, as judged by the importance of different predictors in the models, the effects of macroalgal density and water properties were much weaker than light dependence of production and growth of C. aspera.

The availability of different forms of inorganic carbon may limit the photosynthesis of submerged vegetation including C. aspera (van den Berg et al., 2002). Shallow water habitats of our study area are also characterized by a large amplitude of natural variability in pH and pCO2 with a daily range of pH recorded between 8 and 9 (Pajusalu et al., 2013). Among different charophyte communities inhabiting our study area C. aspera is way less sensitive to inorganic carbon limitation compared to C. horrida and C. tomentosa (Pajusalu et al., 2015). Thus, as compared to light and temperature, the limitation of inorganic carbon is likely not a prominent stress to the studied community.

Our study did not focus on interspecific interactions that potentially shape the photosynthesis and growth of C. aspera. A wealth of experimental studies has demonstrated that marine herbivores play key roles in regulating macroalgal communities (Hayward, 1988; Sala and Graham, 2002; Kotta and Witman, 2009). However, previous experiments suggest that herbivory or plant fragmentation induced by herbivores is not crucial in the studied charophyte communities (Kotta et al., 2004). Moreover, C. aspera largely dominates the studied charophyte community and interspecific competition among algae and submerged vegetation is slight. It is plausible that spatial heterogeneity or differential utilization of abiotic resources are behind the pattern in distribution of species (Chambers and Prepas, 1990).

A large set of experimental data is a prerequisite to understand and accurately model the patterns of production of any macroalgal assemblages. In this study we experimentally quantified seasonal variability in individual photosynthesis, community production and growth in biomass of the charophyte C. aspera in the Baltic Sea along with the key environmental variables known to determine the production of macroalgae. The experiments suggested that the production and growth of C. aspera was defined largely by light and partly by temperature at all studied scales. However, algal production was systematically lower at the community than at an individual level under the same light conditions, suggesting the importance of shelf-shading and below-ground processes in natural plant assemblages (e.g., Carvalho et al., 2005; Binzer et al., 2006). Moreover, the observation scale also defined response types between the environment, plant production and growth. This implies that the patterns of variability of the production and growth of macrophytes should always be interpreted in the context of scale and any multiscale model development should involve experimental validation at all important scales.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

KT, MR, and JK built the databases. MR and JK analyzed the data. JK, KT, and TP wrote the manuscript. All authors conceived the study, discussed the results, edited the manuscript, and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.