Catchment properties and the photosynthetic trait composition of freshwater plant communities

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Science  15 Nov 2019:
Vol. 366, Issue 6467, pp. 878-881
DOI: 10.1126/science.aay5945

Change in plants as bicarbonate rises

Freshwater plants can be broadly divided into two major categories according to their photosynthetic traits: Some use carbon dioxide as their carbon source, whereas others use bicarbonate. Iversen et al. found that the relative concentrations of these two inorganic carbon forms in water determine the functional composition of plant communities across freshwater ecosystems (see the Perspective by Marcé and Obrador). They created global maps revealing that community composition is structured by catchment geology and not climate (in contrast to the terrestrial realm, where the trait composition is structured by temperature and rainfall). Anthropogenic influences from land-use change are causing large-scale increases in bicarbonate concentrations in freshwater catchments and are thus leading to wholesale changes in the composition of their aquatic plant communities.

Science, this issue p. 878; see also p. 805


Unlike in land plants, photosynthesis in many aquatic plants relies on bicarbonate in addition to carbon dioxide (CO2) to compensate for the low diffusivity and potential depletion of CO2 in water. Concentrations of bicarbonate and CO2 vary greatly with catchment geology. In this study, we investigate whether there is a link between these concentrations and the frequency of freshwater plants possessing the bicarbonate use trait. We show, globally, that the frequency of plant species with this trait increases with bicarbonate concentration. Regionally, however, the frequency of bicarbonate use is reduced at sites where the CO2 concentration is substantially above the air equilibrium, consistent with this trait being an adaptation to carbon limitation. Future anthropogenic changes of bicarbonate and CO2 concentrations may alter the species compositions of freshwater plant communities.

The biogeography of terrestrial plants is influenced by climatic factors—primarily air temperature and precipitation (1). Furthermore, the distribution of biochemical traits, such as the two terrestrial CO2-concentrating mechanisms, C4 photosynthesis and crassulacean acid metabolism, are linked to temperature and water availability (2). Although freshwater angiosperms evolved from terrestrial ancestors (3), their growth is controlled by light, nutrients, and inorganic carbon (4) rather than water, and therefore the factors influencing their biogeography are likely to be different. Inorganic carbon potentially limits photosynthesis in aquatic systems, because the diffusion of CO2 is 104-fold lower in water than in air. Consequently, the CO2 concentration needed to saturate photosynthesis is up to 12 times the air equilibrium concentration (5). Moreover, rapid photosynthesis can reduce CO2 in water substantially below air saturation (4).

In response to carbon limitation, a few aquatic angiosperms evolved the same CO2-concentrating mechanisms found in their terrestrial ancestors, but the most frequent mechanism, found in about half of studied submerged freshwater plants, is the exploitation of bicarbonate (HCO3) (4, 6), which is derived from mineral weathering of soils and rocks in the catchment. Bicarbonate is the dominant form of inorganic carbon in fresh waters when the pH is between ~6.3 and ~10.2, and its concentration often exceeds that of CO2 by a factor of 10 to 100 (6). The ability to use bicarbonate is present in most taxonomic groups and appears to have evolved independently in cyanobacteria, eukaryotic algae, and vascular aquatic plants (7). This shows the fundamental importance of bicarbonate use to plant fitness (6); increase of photosynthesis, growth, and primary productivity at higher bicarbonate concentrations has been documented (810). However, bicarbonate use is not ubiquitous, because it involves costs as well as benefits. Costs include energy, as it is an active process (11) and rates of photosynthesis at limiting concentrations of inorganic carbon are greater in CO2 users than in bicarbonate users (5, 12). Thus, where CO2 concentrations are substantially above air saturation, as is often the case in streams, the benefit of bicarbonate use will be reduced (13). Furthermore, obligate CO2 users can exploit alternative CO2 sources in the air, lake sediment, or the water overlying the sediment (14), allowing continued photosynthesis without the need to invest in mechanisms required for bicarbonate use.

We hypothesized that because limitation of photosynthesis by inorganic carbon supply is widespread in freshwater plants, the relative concentrations of bicarbonate and CO2 at a particular site should determine the proportion of plants that are obligate CO2 users versus bicarbonate users. Because geochemical catchment characteristics determine bicarbonate concentration, there should be broad biogeographical patterns in the proportion of freshwater plants able to use bicarbonate, whereas at a smaller scale both the CO2 and bicarbonate concentrations in lakes and streams might structure the functional group composition.

To test these hypotheses, we generated a database of freshwater angiosperms and their ability to use bicarbonate as an inorganic carbon source, based on data found in the literature. These were complemented with new data we gathered on 35 species from mainly tropical regions where few prior data existed (table S1) (15). The resulting 131 species represent ~10% of known species with a submerged life stage (16), and of these, 58 (44%) can use bicarbonate. To quantify the distribution of bicarbonate users versus CO2 users, we used: (i) ~1 million geo-referenced plant records, (ii) global plant ecoregion species lists, and (iii) 963 site-specific plant compositions from Northern Hemisphere lakes and streams (fig. S1). In each of the investigated 963 sites, plant composition was related to measured concentrations of CO2 and bicarbonate. The geo-referenced plant records and ecoregion species lists were linked to local bicarbonate concentrations derived from a constructed global map of bicarbonate concentrations (fig. S2) (15).

In the analyzed lake and stream sites, concentrations of both bicarbonate and CO2 affected the occurrence of obligate CO2 users versus bicarbonate users, albeit differently within and between lakes and streams (Fig. 1 and fig. S3). The chance of observing a bicarbonate user in lakes and streams correlated directly with concentrations of bicarbonate and CO2 [∆Habitat = 0.82 (−1.64, 0.01); mean (95% confidence interval); ∆ represents the difference between streams and lakes in parameter estimates on a log(odds) scale (fig. S3)] (Fig. 1A). However, with increasing bicarbonate concentrations, the likelihood of observing a bicarbonate user increased in lakes but not in streams [∆βBicarbonate = −0.82 (−1.10, −0.54)] (Fig. 1B) [see (15) for an explanation of β]. Moreover, with an increase in CO2, the chance of observing a bicarbonate user decreased in both habitat types [∆βCO2= −0.04 (−0.22, 0.13)] (Fig. 1C). The present study shows that the concentration of bicarbonate has a different effect on the proportion of bicarbonate users in lakes versus streams. Unlike in lakes, no relationship between bicarbonate availability and bicarbonate users was found in streams. This upholds our hypothesis that where concentrations of CO2 are high, the competitive advantage of using bicarbonate as a carbon source for photosynthesis will be reduced even if bicarbonate is available.

Fig. 1 Bicarbonate use in submerged freshwater plant communities.

(A) Likelihood of observing a bicarbonate user versus a CO2 user in streams (n = 172 samples; red) and lakes (n = 791 samples; blue). (B and C) Modeled odds of observing a bicarbonate user versus a CO2 user as a function of bicarbonate (B) or CO2 (C) concentration. Values >1 indicate a higher likelihood (A) or increase in likelihood (B and C) of observing a bicarbonate user versus a CO2 user with a one-unit increase in bicarbonate (B) or CO2 (C) concentration. The dotted vertical lines show mean estimates, and shaded areas show the 95% confidence limits around the mean.

Across global plant regions (17), the shifting proportions of bicarbonate users versus obligate CO2 users showed distinct spatial patterns (Fig. 2A). Compared to the overall mean, a higher proportion of bicarbonate users was observed in Africa, temperate Asia, and the northern part of North America (Fig. 2A). Globally, species using bicarbonate were found in areas with higher bicarbonate concentrations [bicarbonate users − CO2 users = 0.16 mM (0.02, 0.30)] (Fig. 2C; see Fig. 3 for a local example). The proportion of bicarbonate-using species increased with bicarbonate concentration within ecoregions [β = 0.14 (0.05, 0.24)] (Fig. 2B). Because catchment geology and geological history shape the distributions of lakes and rivers, as well as the bicarbonate concentrations in freshwater ecosystems (18, 19), they are the chief determinants of plant distributions in fresh waters. CO2 concentrations are largely regulated by local CO2 supersaturated inflow (20) and ecosystem metabolism, making modeling difficult at large spatial scales (19, 21). Thus, future models of freshwater CO2 concentrations may improve the prediction of plant distributions even further. Although global lake and river data exist to some extent as annual means (22), given the temporal variability in CO2 concentration, the appropriate concentration would be that during the growing season at the specific site (20).

Fig. 2 Global relationship between bicarbonate concentration and the proportion of bicarbonate users in freshwater plants.

(A) Proportion of bicarbonate-using species across 52 plant ecoregions. Gray areas indicate regions where information on bicarbonate use in local plants is not available. (B) Relationship between mean bicarbonate concentration in plant regions and frequency of bicarbonate users. The line represents the mean proportion of bicarbonate users. (C) Density plots of bicarbonate preferences for bicarbonate users (n = 57) and obligate CO2 users (n = 72). The central horizontal black lines represent the means, and the boxes indicate the 95% confidence intervals around the means.

Fig. 3 Steep gradients in bicarbonate concentrations and spatial separation in species distribution in the British Isles.

Distribution of two pondweed species with contrasting bicarbonate use in the British Isles. Potamogeton polygonifolius (obligate CO2 user; black triangles) is found in areas with lower bicarbonate concentrations than are present where Potamogeton crispus (bicarbonate user; white circles) is found. The top left inset shows the density distribution of the two species across bicarbonate concentrations. Bicarbonate concentrations are from the global bicarbonate map (fig. S2), and species data were extracted from the geo-referenced plant occurrences (15).

Anthropogenic changes as a consequence of deforestation, cultivation of land, application of nitrate fertilizers, and reduced atmospheric acid deposition (23) are causing large-scale increases in bicarbonate concentrations (24, 25). The observed increasing bicarbonate concentrations are expected to cause a severe impact on bicarbonate-poor lakes, because higher bicarbonate concentrations will markedly change species composition (26) by allowing tall, fast-growing bicarbonate users to colonize and suppress smaller species adapted to the use of CO2 alone in or near the sediment (27). There is evidence for reestablishment of species that are able to use bicarbonate, after the bicarbonate has increased because of liming (28) or as a result of reduction in acid deposition (29). Moreover, systematic changes in species composition caused by changes in CO2 concentration have also been demonstrated in a river system where the proportion of CO2 users declined as CO2 decreased downstream (13). In contrast, increasing atmospheric CO2 concentrations, even if they influence dissolved CO2, will have little effect on the abundance of bicarbonate users, because increases in CO2 will be small relative to bicarbonate concentrations and will have little effect on plant photosynthesis rate (30).

Our study shows that bicarbonate use by aquatic angiosperms is widespread in fresh waters around the globe and that the proportion of obligate CO2 users to bicarbonate users is significantly related to the bicarbonate concentration. Among terrestrial plants, the evolution of leaf traits and different photosynthetic pathways that enable rapid carbon assimilation and improved water economy (31) has resulted in global biogeographical patterns that are linked to variations in climate (32, 33). In contrast, for freshwater plants, we show that biogeographical patterns of bicarbonate use exist and that these are caused by catchment properties that determine the concentrations of bicarbonate and CO2. This insight will help evaluate the repercussions of future changes in concentrations of bicarbonate and CO2 on the biodiversity and ecosystem functions for fresh waters.

Supplementary Materials

Materials and Methods

Figs. S1 to S7

Table S1

References (3591)

References and Notes

  1. See supplementary materials.
Acknowledgments: We thank L. Adamec for providing data on Oenanthe aquatica, Tropica Aquarium Plants for the generous supply of tropical aquatic plants, and K. Murphy for sharing the species list of plants with a submerged life form. We acknowledge constructive suggestions by C. M. Duarte, H. Lambers, and H. H. Bruun. Funding: L.L.I. was funded by the Carlsberg Foundation (CF17-0155 and CF18-0062). L.B.-S. was funded by the Aage V. Jensen Foundation. D.G. was funded by the Polish National Agency for Academic Exchange (PPN/BEK/2018/1/00401), J.A. was funded by The Academy of Finland (332652), and K.S.-J. was funded by the Carlsberg Foundation (grant CF14-0136). Author contributions: L.L.I., A.W., L.B.-S., S.C.M., K.S.-J., and O.P. designed the study, framed the research questions, and wrote the manuscript, with input from the working group (A.B.H., J.A., A.B.-P., P.B., P.A.C., F.E., T.F., J.H., T.S.J, S.J.M., T.R., L.S., and O.V.). L.L.I. analyzed the data and prepared the figures. A.B.H. and O.P. performed the pH drift experiments and together with A.W. searched the literature on bicarbonate uptake in aquatic plants. A.W., L.L.I., and L.B.-S. assembled the data for the global analysis. F.E., L.B.-S., L.S., S.C.M., S.J.M., J.A., and T.F. assembled the site-specific lake data; A.B.-P., P.B., P.A.C., D.G., K.S.-J., T.R., and T.S.J. assembled the site-specific stream data; O.V., A.W., L.L.I., and L.B.-S. prepared the site-specific data for further analysis. Competing interests: O.V. is a staff member of the United Nations Environment Programme. The authors alone are responsible for the views expressed in the publication, and they do not necessarily represent opinions, decisions, or policies of the United Nations Environment Programme. The authors declare no other competing interests. Data and materials availability: All R scripts and cleaned datasets used for this analysis are available at the Dryad Digital Repository (34).
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