Abstract
The rise in the earth’s surface and water temperature is part of the effect of climatic change that has been observed for the last decade. The rates of climate change are unprecedented, and biological responses to these changes have also been prominent in all levels of species, communities and ecosystems. Aquatic-terrestrial ecotones are vulnerable to climate change, and degradation of the emergent aquatic macrophyte zone would have contributed severe ecological consequences for freshwater, wetland and terrestrial ecosystems. Most researches on climate change effects on biodiversity are contemplating on the terrestrial realm, and considerable changes in terrestrial biodiversity and species’ distributions have been detected in response to climate change. This is unfortunate, given the importance of aquatic systems for providing ecosystem goods and services. Thus, if researchers were able to identify early-warning indicators of anthropogenic environmental changes on aquatic species, communities and ecosystems, it would certainly help to manage and conserve these systems in a sustainable way. One of such early-warning indicators concerns the expansion of emergent macrophytes in aquatic-terrestrial ecotones. Hence, this review highlights the impact of climatic changes towards aquatic macrophytes and their possible environmental implications.
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1 Introduction
Global change has been revealed and forecast to have major effects on biodiversity at local, regional and global scales. The global change constitutes a number of different forms of anthropogenic impacts, including land use alterations, nitrogen deposition and invasions of exotic species, much recent interest has been directed at climate change (Sala et al., 2000; Parmesan, 2006; Hossain and Rama Rao, 2014). Although the earth has experienced considerable climate changes in the past, the rate and magnitude of the recent and projected future changes are unprecedented (IPCC, 2001; Hossain et al., 2016). Furthermore, the effect of future climate change on biodiversity has been predicted to be unparalleled, with 15–37 % of terrestrial species possibly facing extinction due to climate change alone in the next 50 years (Thomas et al., 2004), and a similarly dark future has been suggested for freshwater species in the next few decades (Xenopoulos et al., 2005). Biodiversity, integrity and functioning of different ecosystems are facing serious problems on the global scale and freshwaters are one of the most highly threatened ecosystems. Thus, research on the effects of climate change on freshwater organisms and ecosystems has increased hastily in the last decade.
Evaluation of anthropogenic impacts on freshwaters relies on the integrity of community structure of biological groups and on the presence of indicator species that provides information about ecological quality in a water body (Rickert and Hines 1978; Carpenter et al. 2006). Aquatic macrophytes belong to one traditionally studied biological group in ecological assessments. Macrophytes indicate well on long-term changes of the littoral zone, but reflect poorer on rapid changes in water quality (Palmer et al. 1992, Melzer 1999).
Vascular plants (emergent, floating or submerged), byrophytes and macro algae in the aquatic environment are all considered as aquatic macrophytes. They play a vital role in preserving the fresh water diversity as they provide living places for other aquatic organism (Thackeray et al. 2010; Akasaka et al. 2010; Akasaka and Takamura 2011).
Seagrasses are plant communities which represent diverse plant forms growing intermingled with algae, and phytoplankton. Aquatic macrophytes are also able to change the abundance of stream fauna and possess the potential to compete for resources such as nutrients, light and space. They also provide physical structure, an increase in habitat complexity and heterogeneity that affect different types of organisms such as invertebrates, fish and water birds.
In rivers and streams, aquatic macrophytes and benthic algae act as the major primary producers (Hari et al., 2006; Schneider et al., 2012). They provide food and habitat, influence sediment composition as well as physical stream characteristics (Maltchik et al., 2007; Istvánovics et al., 2008; Kleeberg et al., 2010). In the aquatic environment, plant tissues play different roles depending on their positions. Table 1 shows the roles of different plant tissues in the aquatic environment, categorized by their tissues’ position in the aquatic environment.
Factors such as physico-chemical state of water in terms of pH and transparency of water, sedimentation types, water depth and surface area are believed to affect the distribution and the richness of macrophytes (Geurts et al. 2008). However, James et al. (2005) reported that water chemistry (nutrients and components present) is predominantly vital in determining the richness of macrophytes although Akasaka et al. (2010) indicated that the importance vary with the growth forms of macrophytes. Free-floating macrophytes often have a large impact on freshwater ecosystems. The limitations of carbon hydroxide and sunlight for photosynthesis rarely happened. When nutrient loading is high, free-floating macrophytes will form dense mats that cover the entire surface of the water body. Hence, submerged macrophytes are strongly affected by the decrease in the amount of light penetrated, as well as dissolved inorganic carbon (DIC).
According to the EU Water Frame-work Directive (WFD; European Parliament, 2000; Lekka et al., 2004)), aquatic macrophytes have been listed as bio-indicators as the survival of aquatic macrophytes is highly dependent on environmental factors (Akasaka et al., 2010). One of the early-warning indicators is the expansion of emergent macrophytes in the aquatic-terrestrial ecotones (Alahuhta et al., 2011). Hence, the dispersion and abundance of macrophytes diversity can act as indicators of many environmental conditions and in this review, the focus lies on the immediate effect of climate change towards the growth of macrophytes.
2 Climate change
Climate warming is undeniable. Changes that have been observed since the 1950s are unprecedented. Warming is occurring in the atmosphere, as well as the ocean. Snow and ice are diminishing and the level of sea water has risen. However, ocean warming is more evident on the surface. According to IPCC (2014), the upper 75 m of the ocean is warmed by 0.11 (0.09 to 0.13) °C per decade over the period 1971 to 2010. The shrinking of glaciers is happening worldwide. The loss of the mass of glaciers has contributed to the rise of the sea level throughout the twentieth century.
The concentration of greenhouse gases (GHGs) in the atmosphere is highest in at least 800,000 years (IPCC, 2014). Concentrations of GHGs such as methane, nitrous oxide and carbon dioxide are showing increment since 1750, and concentration of carbon dioxide is increasing at the fastest rate for the year 2002–2011 (2.0 ± 0.1 ppm/year). The concentration of methane has shown increment after being stable for many years since the late 1990s. Nitrous oxide has shown steady increment at the rate of 0.73 ± 0.03 ppb/year over the last three decades (IPCC, 2014).
The climate has shown profound alterations over the years. Increases in carbon dioxide (CO2) (an increase from 280 to 650 ppm) and other greenhouse gases have contributed to the increase in global temperatures (IPCC, 2007). Earth surface temperatures have increased by 0.6 °C and the mean global surface temperatures elevated for 1.4 to 5.8 °C in the next century is predicted (IPCC, 2007). An increment of 2–4 °C in temperature is expected by the end of the twenty-first century by; a 2–4 °C temperature increase is expected in the Mediterranean region in spring (Stocker et al., 2013). In the climatic region, freshwater ecosystems are often shallow water bodies or small lakes. Hence, they are predominantly prone to climate change (Álvarez-Cobelas et al., 2005; Morecroft and Keith, 2009; Parcerisas et al., 2012).
Climate change has imposed new selection pressure towards the distribution and abundance of the widespread macrophytes species (Rothausler et al., 2011; Lovejoy and Hannah, 2005). Higher tolerance level towards temperature change caused by climate change is expected specifically for species existing in an environment with numerous variables. Phenotypic features and phenotypic plasticity of the species may be changed to adapt in response to climate change (Walters, 2005).
Rise in temperature, CO2 concentration and alterations in precipitation affect growth, productivity and distribution of terrestrial and aquatic vegetation directly and indirectly (Lucht et al., 2006; Wrona et al., 2006; Heikkinen et al., 2009; Heino et al., 2009; Peeters et al., 2013). Alterations in water chemistry and hydrological regimes affect the structure and function of aquatic ecosystems (freshwater and marine) especially in the boreal regions (Rahel and Olden, 2008; Heino et al., 2009; Knutti and Sedlacek, 2013). Changes in climate alter the characteristics of the water. These include high nutrient loading from the catchment areas to the lakes (Jeppesen et al., 2009a, b; 2010, 2011, 2012, 2014) and high salinity causing a shift to oligosaline or mesosaline conditions (Wrona et al., 2006; Beklioglu and Tan, 2008; Jeppesen et al., 2009a, Jeppesen et al., 2009b; Beklioglu et al., 2011; Trenberth et al., 2014).
Aquatic macrophytes are keystone species in the aquatic ecosystems. Hence, it becomes mandatory to study and discuss the effects of climate change on aquatic vegetation.
3 Growth and distribution of macrophytes influenced by abiotic factors for climate change
Temperatures of river and lake water are expected to be affected imminently by climate change (Hammond and Pryce, 2007). As river water temperatures are in close equilibrium with the air temperature, when the air temperature increases, the river temperature will be affected as well. The European Environment Agency (EEA) (EEA 2007) reported, in the past 100 years, a temperature rise of 1–3 °C has been observed in major European rivers. In addition, Hari et al. (2006) reported significant increment in temperature for water courses in Switzerland at all altitudes.
Temperature influences plant growth extensively. However, the effects of increased temperature somehow depend on individual species and their thermal tolerances. Temperature may alter plant phenology, for instance, busting of leaf bud, flowering period, nutrient uptake, competition between species and lastly the metabolic events including photosynthesis, respiration and enzyme-mediated processes (Meis et al., 2009; Thackeray et al., 2010; Mooij et al., 2005).
Emergent aquatic macrophytes will become more abundant (increase by 25 %) as the reproductive capacity including spore production, germination and sporophyte growth will be enhanced (Heikkinen et al., 2009; Anja et al., 2009).
Enhancement in growth measured as an increase in shoot length, plant height, leaf surface area and biomass production has been reported in Phalaris arundinacea, Potamogeton natans, Lemna major, Equisetum fluviatile, and Typha on exposure to high temperature (3–7 °C above ambient). The enhanced growth could be attributed to the increase in elemental contents especially N and P and increased physiological activities such as photosynthesis and respiration. Enhancement in productivity of seaweeds due to the increase in temperature is due to the increase in photosynthesis. Increased seed germination in response to the increase in temperature has been reported in Ruppia sp., Zostera marina and Zostera noltii. Biochemical and physiological adaptations such as heat shock proteins have been noted in aquatic species to encounter high temperatures (Sorte and Hofmann, 2005; Kim et al., 2011; Eggert, 2012).
In contrast, very high temperatures will have an overall negative impact on the net primary productivity (NPP) of plants as an increase in the rate of respiration is more rapid compared to photosynthesis. At higher temperatures, the rate of respiration increases at a faster speed, and primary productivity compromised. The changes are evident in microalgae and seagrasses (Rosset et al., 2010; Tait and Schiel, 2013). In eelgrass, Z . marina L., the rate of leaf respiration increases more rapidly with rising temperature than photosynthesis, leading to a steady decrease in the photosynthesis-to respiration ratio (P/R) (Short and Neckles, 1999; Demars and Trémolières 2009).
Higher temperature plays a vital role in accelerating most of the chemical reactions and bacteriological processes. Therefore, the increase in temperature due to climate change will affect the growth of macrophytes. Elevation in temperature had a small effect on macrophytes relative to nutrient effect (Feuchtmayr et al., 2007). In a nutshell, warming will favour the growth of a few species; hence, the diversity and species richness of macrophytes will decrease (Feuchtmayr et al., 2010).
4 Nutrient
According to Brown et al. (2007), climate change is expected to have effects on river regimes, river flow velocity, hydraulic characteristics, water levels, inundation patterns, residence times, changes in the wetted areas as well as habitat availability and connectivity across habitats. Most probably, under the influence of climate change, rivers will be under low flow conditions during summer. Biochemical oxygen demand (BOD) and phosphorus level would increase. However, ammonia levels would reduce as higher nitrification rates that may occur. Hence, nitrate concentration will increase as ammonia decays (Kleeberg et al., 2010; Whitehead et al., 2009). Suspended solids and nutrients from land are transported by runoff to water bodies; thus, they stimulate the growth of emergent aquatic macrophytes. Alteration in the nutrient composition will particularly affect the free-floating and rooted macrophytes (Feuchtmayr et al. 2007; Human et al. 2015).
Warm climate support eutrophication (typically oligotropic-mesotrophic boreal lakes) and hence increases the availability of phosphorus to plants. High phosphorus concentrations negatively influence the growth of submerged macrophytes. Increase in phosphorous concentration increase competition between macrophytes and phytoplankton (Lacoul and Freedman, 2006). This results in phytoplankton dominance and the disappearance of macrophytes (Declerck et al., 2005). Warming lead to a shift from a clear, macrophyte dominated state to a turbid, phytoplankton-dominated state (Mooij et al., 2007).
Thus, a long-term effect of global change may cause more rapid eutrophication and accelerate the loss of seagrass habitats. Eutrophication promotes algal (benthic and planktonic) growth, ultimately decreasing the light reaching the other plants, hence decreasing growth, productivity and distribution of macrophytes. In a nutshell, increased nutrient loading increases the abundance of algae but decreases the diversity of other macrophytes (Partanen and Luoto, 2006).
Studies also indicate that high nitrate concentrations support the growth of free-floating species and hence instigate low species richness. Macrophyte populations might decrease from nutrient enrichment (Harley, 2011). Nutrient enrichment stimulates the production of planktonic microalgae and opportunistic macroalgae at the cost of seagrasses and perennial macroalgae (Human et al. 2015).
Nevertheless, severe eutrophication (nitrogen or phosphorus overloading) has caused a decrease in species diversity and disappearance of submerged macrophytes (Ansari et al., 2011; Xing et al., 2013). However, in eutrophic condition, high macrophytes diversities can still be observed (Le Bagousse-Pinguet et al., 2012). Sand-Jensen et al. (2008) indicated that the declining of diversities is only at the very end of the eutrophication gradient.
5 CO2 concentration
Aquatic plant species survive on either CO2 or both HCO3 and CO2. The CO2 (inorganic carbon source) in the air is mainly being utilized by free-floating plants whereas submerged species survived on both CO2 from sediments, air and water and HCO3. The rise of CO2 level in the atmosphere will directly promote the photosynthesis process leading to intensification of productivity which favours the growth of aquatic plants specifically those mainly utilizing CO2. Nevertheless, the survival of other species may be negatively affected (BhupinderDhir, 2015).
Limiting factors for the growth and the productivity of submerged macrophytes are the limited availability of free CO2 in natural water bodies and limited uptake of inorganic carbon due to high diffusion resistance. Emergent and floating macrophytes use CO2 as a carbon source; hence, their growth will be promoted as a direct result of the CO2 increase. Enhancement of growth (2–8 times) has been observed in plants such as Vallisneria americana, Ceratophyllum demersum and Hydrilla verticillata exposed to elevated CO2 (approx. 700 μmol−1) concentrations (Alahuhta et al., 2011). The increased photosynthetic rate supported height development and production of more root, rhizome and leaf biomass. However, the response of seagrasses to long-term increases in CO2 depends on the physiological and morphological acclimation. Seaweeds will benefit from the increase in inorganic carbon concentration as more CO2 is more accessible while the growth of macroalgae will be reduced (Kroeker et al., 2010).
The growth rate of algae and macrophytes utilizing CO2 and HCO3 may be doubled due to atmosphere CO2 elevation under the eutrophic condition. On the other hand, threefolds of growth of macrophytes that are restricted to CO2 assimilation may be observed (Schippers et al., 2004).
The increase in CO2 concentration in the atmosphere is very likely to affect plant traits including photosynthesis and plant growth. Acclimation towards the climate changes will be essential for the plant to compete and expand. Phenotypic plasticity has been known as a vital feature of submerged aquatic plants for capturing resources (Hyldgaard and Brix, 2012; Malheiro et al., 2013). Malheiro et al. (2013) found a strong phenotypic response with submerged species Myriophyllum aquaticum (Vell.) Verdc. The leaf surface was reported to be maximized in order to increase CO2 uptake.
Increased concentrations of free CO2 may bring disadvantages for some species that survive under low light intensity. Hence, the high concentrations of free CO2 may not have significant impact towards submerged species as their invasiveness is partly due to their capability to use bicarbonate. The study also suggested that the invasive bicarbonate users responded little to changes in free CO2 availability. Hence, in the future, the increase of free CO2 concentration in water bodies may be more likely to favour species that are currently limited by the ambient free CO2 concentration (Caldeira and Wickett 2005; Eller et al., 2015).
Carbon and light availability are the two major factors that are interrelated with each other on the effects on growth and photosynthetic traits of macrophytes especially the submerged species. The rate of supply of dissolved inorganic carbon (DIC) is one of the major constraints associated with underwater photosynthesis. However, aquatic macrophytes often have adaptive features which will assuage this constraint. Sediment and atmospheric CO2 pools will be utilized in conjunction with a physiological and biochemical mechanism to enhance the efficiency of carbon uptake.
6 Light conditions
Light intensity is a crucial limiting factor when it comes to the growth of aquatic plants. Eutrophication indirectly resulted from climate change has affected water turbidity of major shallow lakes with transparencies ranging from 0.25 to 0.5 m. This has resulted in growth suppression of macrophytes as only very limited light is available. On the other hand, the rising of sea level has further increased the water depth which thereby reduced the availability of light. Under high water turbidity, only floating plant communities will strive (BhupinderDhir, 2015). According to Hussner et al. (2010, 2011), the growth of Elodea canadensis, Egeria densa, and Lagarosiphon major decreased by threefold in branching, as well as the below-ground mass under reduced light conditions (25–50 %). Variations in light and temperature have led to acclimation within the submerged aquatic plants.
In a study conducted by Eller et al. (2015) with four invasive aquatic plants, the results indicated that under high free CO2 concentration, Hydrilla verticillata showed 12 times higher root/shoot ratio in low light intensity condition compared to those in high light intensity condition. As for E. Canadensis, higher main and total shoot lengths were reported in high light intensity. However, the number of internodes was greater in low light intensity condition. Few species such as Thalassia testudinum and Cymodocea nodosa have shown an increase in leaf biomass, width and canopy height because of the increased photosynthetic rate (Harley et al., 2012).
Morphological adaptation due to light intensity was observed in Charahispida and Cattleya intermedia. Branches were reported to be pointing steeply upward towards the high light intensity condition (Schneider et al., 2015). The stems of Chara that were branching out towards the light under high light intensity can be interpreted as a protective mechanism in order to protect the plant from excessive light (Schneider et al., 2015). Enhanced elongation under low light intensities is construed as a method to increase light harvest by growing into an area with higher available light (Blindow and Schütte, 2007).
7 Salinity
Coastal flooding and changes in sea level caused by climate change will affect the salinity of estuaries. A slight increase in salinity to 0.5–5.0 parts per thousand will lead to the replacement of species such as oligohaline and mesohaline submerged macrophyte populations by seagrasses (BhupinderDhir, 2015). Low salinities (1 ± 10 ppt) stimulate germination of Zostera nana, Z. marina, Z. noltii and Zostera capricorni seeds, and while in high salinities, the seedlings survival is affected. Germination of many upper estuarine submerged macrophyte species has been shown to decrease with the increase in salinity. The salinity of ~5–18 parts per thousand (mesohaline) supports the growth of salt-tolerant submerged and emergent species such as Vallisneria americana, Ruppia maritima and Potamogeton pectinatus (Luoto et al., 2007; Luoto and Heikkinen, 2008; Heino and Toivonen, 2008; Lampinen and Lahti, 2009; Tingley and Herman, 2009).
Localized elimination of non-halophytic macrophytes species was caused by a drastic rise in salinity. Though these may not change the community’s composition, evidence suggested that such salinity elevation could modify the habitat ranges of non-halophytic macrophyte species in wetlands by reducing their inundation stress tolerance (Salter et al., 2008). The rise in salinity will probably restrict the ability of macrophytes to alleviate the effect of rising water levels. Keddy (2010) reported macrophytes species strongly displayed zonation as a result of their inundation tolerance limit as inundation reduces the availability of light and atmospheric gases to plants and species. As a result, the reduction in tolerance towards inundation due to the increase in salinity will control the potential of elevation ranges of susceptible species within salt-affected wetlands (Johns et al. 2014).
Plants develop morphological and biochemical adaptations such as salt exclusion mechanisms, thickened cell walls and increased numbers of chloroplasts and mitochondria in leaf epidermal cells. Various organic acids, nitrogen compounds such as proline, alanine, glutamate and carbohydrates also function internally in seagrasses to counter increased osmotic potential. Increases in salinity caused changes in seagrass leaf ultrastructural morphology and increased the complexity of the plasmalemma mitochondrial system (Bornette and Puijalon, 2011). Such adaptations to saline environments allow successful physiological functioning of many seagrass species within the upper ranges of the salinity in oceanic and estuarine environments. Nevertheless, very limited studies were carried out on macrophytes’ growth in response to various conditions in the last decade (Table 2).
8 Conclusions and future prospective
Climate represents an important part of vegetation distribution globally. Each species has its own distribution patterns and the limitations of which are mostly defined by climate at a worldwide scale. Vegetation distribution patterns show the influence of climatic change towards plant survival, physiology and growth, as well as the climatic effects on ecological interactions (competitions, pollination and herbivory). Different types of plants are adapted to the different climatic conditions. Hence, it is reasonable to expect that climatic change would gradually lead to a change in species distributions and community composition (Morecroft and Keith, 2009).
Studies demonstrated that alterations in different components of climate will affect aquatic vegetation to a broader extent. The responses of assemblages will vary among different plant groups in response to changing temperature, light and the availability of nutrients. Impact of climate changes is evident in terms of effects on their physiology, growth, reproduction and survival in macrophytes. Bioclimatic envelope models suggested an increase in emergent aquatic plant species followed by an expansion in their distribution.
Impact on macrophytes growth and distribution brought by climatic change is inevitable. Anthropogenic activities have caused endless possibilities of pollution towards the natural environment and macrophytes habitat. Diversity and distribution of macrophytes may be altered due to climate change just as indicated in studies. Increase in nutrient concentrations, temperature and sediment accumulation (siltation) will support the growth of emergent macrophytes such as Phragmites australis, E. fluviatile, Typhalatifolia and Schoenoplectus lacustris leading to their increased vegetation cover, hence altering the community structure (Partanen and Luoto, 2006; Park and Blossey, 2008). Significant alteration in the production of macroalgae, phytoplanktons and macrophytes will have a great impact on the other ecosystems. Hence, macrophytes can be taken as a reliable bio-indicator to study the relationships between environmental disturbance and vegetation growth. Responses to vegetation growth in relation to temperature have been the most imminent. However, there is no doubt that in a long run, a local change in precipitation or other climatic change may become more significant due to the global rise of temperature.
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The authors acknowledge The World Academic of Science (TWAS), Italy, and Universiti Sains Malaysia, Malaysia, for providing world class infrastructure to continue the research work.
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Hossain, K., Yadav, S., Quaik, S. et al. Vulnerabilities of macrophytes distribution due to climate change. Theor Appl Climatol 129, 1123–1132 (2017). https://doi.org/10.1007/s00704-016-1837-3
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DOI: https://doi.org/10.1007/s00704-016-1837-3