CHAPTER 1
Solar radiation as an ecosystem modulator
Robert G. Wetzel
Table of contents
Abstract 5
1.1 Introduction 5 1.2 Size matters – radiation attenuation in relation to loadings of organic matter 6 1.3 Precipitation matters – importance of frequency and intensity of influents 7 1.4 Direct effects of UVR 9 1.5 Allochthonous vs. autochthonous organic matter – key UV-VIS mediated processes regulate heterotrophic utilization 9 1.5.1 Alterations of enzymatic accessibility by the macromolecules 10 1.5.2 Photolysis of humic macromolecules 10 1.5.3 Photolysis of dissolved organic nitrogen and phosphorus compounds 11 1.5.4 Complete photolysis of humic substances to CO and CO2 11 1.5.5 Less direct but important biogeochemical interactions of UVR 12 1.6 Recalcitrant organic matter, metabolic stability, and photolysis 13 References 15
Abstract
Solar radiation is the fundamental ecosystem modulator. Nearly all generation of organic matter is photosynthetic and as such the distribution of light in aquatic ecosystems is critical to regulation of major energetic inputs. However, simultaneously specific components of solar radiation, in particular the UV, function as both an accelerator of microbial degradation by enhancing bioavailability of complex organic substrates to microbes and by complete photolysis and oxidation of components of organic macromolecules to CO2 and other inorganic forms of nutrients. Alterations in UV intensities impinging upon and within inland aquatic and coastal marine ecosystems by natural or anthropogenic causes will modify the rates of metabolism and biogeochemical processes associated with these macromolecules. This cascade of effects can greatly modify the functioning of natural ecosystems.
1.1 Introduction
In the subsequent chapters of this volume, detailed evaluations provide a summary of contemporary understanding of the properties of ultraviolet radiation (UVR) in aquatic ecosystems and its effects on aquatic organisms. Here I attempt to provide an overview of the coupling of these properties to emphasize how individual effects of UVR are integrated and, at the ecosystem level, provide a master level of regulation of ecosystem biogeochemical cycling, energy fluxes, productivity, and system evolution.
In regard to these detailed treatments of specific components of solar radiation and their effects, it is useful to emphasize several related universal characteristics of aquatic ecosystems. Namely, ecosystems are biological systems, ecosystems are biogeochemical systems, and the cycling of materials and energy in ecosystems is regulated by a highly variable set of intercoupled physical, chemical, and biological parameters. It is extraordinarily important to evaluate the influences and changes of UVR in the ecological contexts of a highly dynamic, changing environment – dynamic spatial and especially temporal scales. The question then is whether UV effects within the ecosystems are so variable that analyses are chaotic or whether certain stoichiometric analyses allow quantitative predictions of generic system responses to changes in UVR.
The approach taken is to first analyze our present understanding of how UVR influences ecosystem processes and how these processes are intercoupled with other related influences of those processes, such as climatic or atmospheric processes related to UVR. Finally, can one reasonably predict how ecosystems of different characteristics will respond to changes in atmospheric or aquatic conditions that alter UVR.
1.2 Size matters – radiation attenuation in relation to loadings of organic matter
Nearly all UV-C (< 280 nm) is absorbed by the stratospheric gases and by the water of aquatic ecosystems. Although relatively little UV-B (280-320 nm) passes through the stratosphere (Chapter 2), UV-B is highly energetic and an important photactivating agent in waters. UV-A (320-400 nm) is less energetic than UV-B but is absorbed less readily and penetrates more deeply into water. The near UV light in the blue portion of the visible spectrum (400-500 nm) has recently been shown to be functionally similar to the adjacent UV-A radiation in many of the important photochemical reactions influenced by UVR and must be considered in any evaluation of composite effects.
Recent measurements in situ have demonstrated great variability in the penetration of UV-B and UV-A, but penetration has been found to be much greater than was believed previously (Chapters 3, 6, [1]). When referenced against pure water, the transmission of radiation is reduced drastically with increasing concentration of naturally occurring chromophoric dissolved organic compounds, particularly humic acids. UV-B attenuation depths (za = 1% of surface irradiance) range from a few centimeters to > 10 m among a number of waters [2-6]. Much (> 90%) of the among-habitat variation in diffuse attenuation coefficients (Kd) could be explained by differences in dissolved organic carbon (DOC) concentrations. Throughout the solar UV-B and UV-A range, Kd was well estimated with a univariate power model based on DOC concentration, particularly in waters of low to moderate phytoplanktonic productivity. The Za is strongly dependent on DOC concentrations when below 2 mg C 1-1. In eutrophic lakes, densities of phytoplankton can begin to influence UV attenuation [7].
Only certain portions of the heterogeneous dissolved organic matter (DOM) absorb solar radiation. In inland waters, phenolic and other aromatic-based humic compounds (fulvic and humic acids), largely of terrestrial and higher aquatic plant origin, form a major component of dissolved organic acids and can constitute some 80% of the total DOM, 30-40% of which is composed of aromatic carbon compounds [8]. Humic substances are the largest component of chromophoric dissolved organic matter (CDOM). Of the soluble part of humic substances, heterogeneous fulvic acids have molecular weights from 500 to 1200 Da and contain many acidic functional groups, primarily carboxylic acids [9-11]. Humic acids are less hydrophilic than fulvic acids and are of greater molecular weight (mean ca. 4000-5000 Da) [12]. Humic substances dominate CDOM and are the most important component in the absorption of solar UV and blue radiation [4,13].
Concentrations of 4-8 mg organic acids liter-1 are common in surface waters and often exceed 50 mg l-1 in organic-rich waters, such as those of wetlands, flood plains of river ecosystems, and interstitial waters of hydrosoils [1]. Concentrations of both CDOM and humic substances commonly decrease along the gradient of fresh-to-coastal-to-oceanic waters.
Because the effects of UVR on aquatic ecosystems are so strongly influenced by concentrations of CDOM, factors that influence the loading rates of CDOM to aquatic ecosystems will influence strongly the selective distribution of UV and its effects on habitats and biota. Two aspects are particularly important in this regard. Firstly, the proportion of the DOM that is derived from higher plant tissues (terrestrial and wetland/littoral sources) that are dominated by chromophoric humic compounds vs. that derived form algae, which contain few fulvic and no humic constituents [10,14,15]. The DOM of streams and rivers is almost totally dominated by partial decomposition products of terrestrial and wetland higher plants. Similarly, small lakes receive a high proportion of DOM from terrestrial and wetland sources dominated by higher plant productivity and a high proportion of humic substance residues from partial degradation of structural tissue constituents, particularly lignocelluloses.
Secondly, the morphology of the receiving aquatic ecosystem is imperative because of the direct relationships between lake basin volume to water retention times, dilution of influent DOM, and mixing frequencies into photic zones. Most of the millions of lakes are small (< 10 km2) and relatively shallow, usually < 10 m in depth [1,16]. As a result, the frequency of interaction of DOM-entrained water with solar radiation is often high both within stratified lakes and in shallow non-stratified lakes and ponds. Similarly, the frequency with which DOM in water of streams and rivers interacts with solar radiation is also high, particularly among larger stream orders (> 3rd order) where the influence of shading from riparian tree canopy is small.
1.3 Precipitation matters – importance of frequency and intensity of influents
Because the penetration of UVR and its effects on ecosystem metabolism and functioning is so strongly influenced by DOM, the rates and timing of loading of DOM to receiving waters is important. Many studies have demonstrated the dominance of allochthonous inputs of terrestrial organic matter, in the form of detrital DOM and particulate organic matter (POM) for material and energy cycling in stream and river ecosystems. Much of that DOM is released from soils into groundwater and from anaerobic processes in adjoining wetlands [e.g., 1,17-19].
The DOM inputs from terrestrial organic matter to streams and lakes results from direct leaching from living vegetation and from soluble compounds carried in runoff from dead plant materials in various stages of decomposition. Very high concentrations of organic matter emanate from wetlands. Inputs of DOM are often directly correlated with precipitation, with high loading rates to receiving waters in the initial flushing stages of precipitation events. DOM loading then declines markedly in the later stages as dilution increases and eventually the discharge volume declines. Similarly, the DOM loading during the initial stages of snowmelt is much higher than subsequently. Although the total loading of DOM is high during these flushing events, dilution is also high. Some of the highest DOM concentrations and resulting UV attenuation occur during periods of low flow in rivers. In stratified lakes, the longer residence time allows for higher rates of photolysis of DOM in the photic zone. As in shallow, non-stratified lakes that mix frequently to the surface layers of high UV insolation, the concentrating effects of water residence time are countered by time available for UV alteration and microbial mineralization (Chapter 4).
The seasonal timing of the DOM loading also affects the effectiveness of UV photolysis and microbial utilization. Obviously, runoff loading events in cold, low light periods of the year will lead to less effective degradation and utilization of the organic compounds by biota of the ecosystem. These altered rates of UV- mediated metabolism will in turn affect rates of nutrient regeneration and subsequent productivity at many biotic levels.
As the DOM is delivered to marine coastal regions by rivers, reduction of transport rates occurs in the estuarine regions with complex hydrodynamic dispersion of water currents. The less dense saline water overlies that of the coastal waters and is exposed to solar photolysis with greater intensity and frequency than the underlying waters. The result is increased rates of partial and complete photolysis, largely by UV radiation, with higher mineralization rates of CDOM to CO2 by enhanced microbial metabolism and by direct degradation to CO2. As a result, a significant portion of the residual DOM is non-chromophoric (NCDOM). This relatively recalcitrant NCDOM, constituting perhaps 10-20% of the total DOM, tends to persist in marine environments with appreciable chemical stability and longevity (decades to centuries).
How the loading rates of allochthonous dissolved organic matter to freshwater ecosystems and to continental marine regions are and will be affected by climatic changes is unclear. There are indications among long-term data sets that DOC concentrations are declining gradually in lakes over several decades [e.g., 1(p. 779),20,21]. Particularly in oligotrophic lakes where DOC concentrations are often low, UVR penetrates to depths of several meters and can negatively influence organisms by genetic damage, diverting production to increased synthesis of protective pigments, or in high elevations or latitudes where higher plant source materials and DOM loading is low. Organisms in such lakes can be exposed to high intensities of UVR [22]. Even in lakes with higher concentrations of DOM, the long-term trends are often toward slowly decreasing concentrations of DOM [1].
There is little question that both temperature and carbon dioxide concentrations of the atmosphere are increasing. Rising temperature has also influenced precipitation patterns and has led to large regions in which rainfall and snow accumulations have been reduced [1]. Droughts are a cumulative result of numerous meteorological factors affecting precipitation, evapotranspiration, and other water losses. Droughts usually do not become severe until after long periods of deficient rainfall and unrestrained water use.
DOC in some lakes has declined appreciably over the last quarter century coincident with substantial warming [e.g., 1(p. 780),23]. Reduced precipitation and increased evapotranspiration in the drainage basin result in reduced stream flows and lower DOC loading to the streams and lakes. Transparency of lake water to UV photolysis increases under these conditions. Similar reductions in DOC have been observed in streams [19]. The decrease in annual DOC yields of streams occurs in spite of higher concentrations in storm flows following periods of prolonged drought [23,24].
1.4 Direct effects of UVR
Photosynthesis of algae is clearly inhibited by exposure to natural levels of UV-B and especially UV-A radiation. Physiological and genetic recovery occurs, and as a result a quasi-steady physiological state is found commonly between damage and recover processes [25,26, Chapters 9, 11, and 13]. Many species repair damage to photosystems and DNA during daily periods of darkness. Many species produce UV-absorbing compounds – mycosporine-like amino acids are an important and ubiquitous class of such compounds [27,28, Chapter 10]. Many species have biochemical defenses against toxic end products of UVR, such as radical scavenging by carotenoid pigments and superoxide dismutase (Chapter 15). Some species have limited abilities to avoid intense surface UV by migration to deeper areas.
UV radiation can impact zooplankton and fish directly in shallow water habitats by damage to DNA and generation of harmful photochemicals (free radicals, reactive oxygen species) [29,30, Chapter 8]. Although many animals can avoid UV-intense habitats, as well as develop photoprotective pigments (carotenoids, cuticular melanin), both of these strategies can alter their susceptibility to predation by other organisms, particularly fish.
1.5 Allochthonous vs. autochthonous organic matter – key UV-VIS mediated processes regulate heterotrophic utilization
Some 90 per cent or more of the total metabolism in aquatic ecosystems is microbial, accomplished by heterotrophic metabolism of bacteria, fungi, and many protists, all of a size less than 100 µm [1,31]. Therefore, the material and energy fluxes of aquatic ecosystems is totally dominated by metabolism of particulate detritus (non-living) and especially DOM from autochthonous and allochthonous sources. The pelagic open water is but a portion of the whole lake or river ecosystem. Inrelation to loading and fluxes of DOM, allochthonous and littoral sources are critical because of their chemical differences from that produced by algal photosynthesis.
The modes of senescence, death, and degradation rates of biota are also of considerable importance to rates and pathways of degradation and energetic utilization. For example, the continual slow senescence and release of DOM from a higher aquatic plant is very different from the relatively instantaneous biochemical death and release of DOM from a bacterium or alga. Non-predatory death and metabolism of non-living detrital POM and DOM by prokaryotic and protistan heterotrophs dominate in all aquatic ecosystems.
In providing a synthesis of the ramifications of UV on aquatic ecosystems, a key component is the simultaneous importance of DOM in regulating the distribution and attenuation of UVR as well as the effects that UV has both directly and indirectly on the metabolism, growth, reproductive, and production efficacy of biota. Because these effects of UV are so interactive and coupled, it is difficult to separate them without some redundancy. Several points can be characterized, however, in summary of some of the more detailed discussions in subsequent chapters.
