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What is stress to a wetland plant?
Environmental and Experimental Botany 46 (2001) 195– 202 www.elsevier.com/locate/envexpbot
What is stress to a wetland plant? Marinus L. Otte * Wetland Ecology Research Group, Department of Botany, Uni6ersity College Dublin, Belfield, Dublin 4, Ireland
Abstract The definitions of the term ‘stress’ and its applications are reviewed in relation to wetland plants. Three views on the use of the term stress prevail; (1) that it should not be used at all; (2) that it defines any situation which leads to a decrease from optimum performance; and (3) that it should only apply to extreme conditions, outside the normal range of the organism. It is argued here that View 3 should be accepted only; i.e. that stress should only be regarded to be arising from changes in environmental conditions outside the normal range encountered by plants. Conditions normally encountered by wetland plants, such as waterlogged, anaerobic soils and salinity, are not stressful to such plants, but only to non-adapted dryland plants. Stress occurs only when plants are exposed to environmental conditions outside the range they are normally exposed to due to natural or anthropogenic changes. Such conditions are found in agriculture—when plants are grown in places they would not naturally grow, in rapidly changing environments—for example when hydrology is changed due to subsidence or engineering works, and under conditions of environmental pollution. The actual stress imposed on wetland plants may be secondary to the factor thought to cause the stress. Very few studies exist showing direct stress on wetland plants. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Stress; Wetland; Salt marsh; Plants
1. Introduction The subject of this paper originates from an invitation to the author for participation in the symposium on ‘Plants and organisms in stressed wetland environments’ as part of the Quebec 2000 Millennium Wetland Event. The invitation immediately raised the question; what, indeed, is stress to a wetland plant? There is a discrepancy between the academic definition of stress and its perception by the gen* Corresponding author. Tel.: +353-1-716-2019; + 353-1-716-1153. E-mail address: [email protected] (M.L. Otte).
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eral public. For example, asked which would be a more stressful environment for plants, a salt marsh or a garden lawn, most people would probably answer; a salt marsh. This is because stress is often associated with environments that are extreme from a human point of view, e.g. deserts, polar regions, and wetlands, and are described as such even in scientific literature (for example Crawford, 1989). But the conditions prevailing in salt marshes are the normal conditions for naturally occurring plants, while grasses in lawns may be growing in an environment in which they would not normally grow and may be cut with a lawnmower once every 2 weeks during the grow-
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ing season, surely a stressful situation. It is against this background that the question ‘What is stress to a wetland plant’ is addressed in this paper.
often still lacking (for example Lerner, 1999). The views on how the term stress should be defined and used can be divided into three categories.
2.1. Stress is not a useful term (View 1) 2. Perceptions, misconceptions and definitions of stress How stress is defined by researchers depends on the research subject of interest and background of the researcher, and as a result many different definitions exist (for example Calow, 1989; Crawford, 1989; Grime, 1989; Jones and Jones, 1989; Da¨ mmgen et al., 1993; Lichtenthaler, 1996). But what is truly stressful to a plant is difficult to assess. The debate surrounding the definitions of stress, more specifically in relation to ecological processes, was particularly strong during the 1980s (Grime, 1989). How stress is defined and referred to is not only of academic importance, but can eventually affect public perception. Initially used in scientific publications, a term may be used in teaching and popular texts, and in the press. As a result, such terms in the public’s mind may become associated with certain environments. These associations can lead to misconceptions about such environments. The following statements regarding wetlands illustrate this: ‘‘Compared with the vegetation of well-drained soils, wetlands have a worldwide similarity which over-rides climate and is imposed by the common characteristics of a free water supply and the abnormally hostile chemical environment which plant roots must endure’’ (Etherington, 1983). ‘‘Wetland plants have developed mechanisms which allow them to survive in these stressful environments for extended periods of time’’ (Beall, 1997). Such statements convey the notion that wetlands are innately difficult environments in which to live or ‘survive’ (Crawford, 1989). Since the discussions on how stress should be defined reached a high point in the 1980s confusion has persisted, and to date no agreement has been reached among researchers. Even in the most recent literature proper definitions of the term are
The term ‘stress’ cannot be defined appropriately in biological terms and has different meanings in physics and psychology, and its use should thus be avoided. This view was voiced by Harper (1986).
2.2. Stress occurs continuously (View 2) Stress causes a deviation from the optimum conditions (usually a reduction) regarding variables such as biomass production and reproduction. It can be described as ‘‘external constraints limiting the rates of resource acquisition, growth or reproduction of organisms’’ (Grime, 1989). A similar definition was used by Crawford (1989): ‘‘Any environmental factor which restricts growth and reproduction of an organism or population’’, and was adopted for the textbook by Freedman (1995): ‘‘Stress is simplistically defined in this book as environmental influences that cause measurable ecological changes, or that limit ecological development’’.
2.3. Stress occurs under extreme conditions only (View 3) Stress occurs when organisms are exposed to extreme conditions, i.e. conditions outside the normal range. This view is supported by, for example, Larcher (1991): ‘‘Stress is the exposure to extraordinarily unfavourable conditions’’, Da¨ mmgen et al. (1993): ‘‘Flux densities of energy, momentum and matter become stressors either by themselves or in combination, if they exceed or fall below normal ranges, i.e. if existing steady states of biotic systems (organ, organism, society,…) or abiotic systems (atmosphere) are changed’’, and Nilsen and Orcutt (1996) ‘‘conditions that cause an aberrant change in physiological processes resulting eventually in injury’’. The difference between views 2 and 3 is that, according to view 2, any deviations from the
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optimum situation (see Fig. 1, area A) would be considered as resulting from stress, in other words, organisms are continuously living under stress in one form or another. In contrast, view 3 does not consider variations within the optimum and sufficient ranges (Fig. 1, areas A+ B) to be stressful. What is an optimum situation according to view 2 is usually determined by measurement of growth or biomass production, with high values being considered ‘non-stressed’ and low values ‘stressed’. While the arguments against using the term stress (View 1) could be considered valid (as also Grime, 1989, concedes), the fact is that it has become embedded in ecological research and its use has helped us understand processes underlying changes at the population/community level. Also, inventing a new term would bring along with it the same problems of misinterpretation. View 1, therefore, is not a desirable approach to the problem. View 2 is not appropriate either, as variations in conditions outside the optimum, but within the normal range are not necessarily stressful. This is exemplified by the occurrence of two forms of Spartina alterniflora along the southeastern coasts of the US, the tall and short growth forms. The
Fig. 1. Diagram depicting a conceptual model of the effects of two factors on performance (e.g. growth) of plants (no interaction between factors). Lim, limiting (too low or too high), Suf, sufficient, O, optimal. Optimum conditions prevail for both factors in area A, while sufficient, but not optimal conditions prevail in area B. In area C conditions are limiting, but not lethal, while outside area C conditions are lethal and the plants could not survive. Under normal conditions, factors would vary within areas A and B.
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tall form tends to be associated with well-drained creekbanks, while the short form is associated with less drained areas between creeks. The differences in hydrology lead to differences in levels and fluctuations of, for example, nutrient inputs, porewater salinity and sulphide concentrations. The differences between the two forms can be explained by the differences in sediment chemistry of their habitats (Valiela et al., 1978; Howes et al., 1986; Ornes and Kaplan, 1989; Osgood and Zieman, 1998), but the forms also vary genetically (Stalter and Batson, 1969; Gallagher et al., 1988). Studies on the two growth forms tend to consider the short growth form as stressed compared with the tall form. This is illustrated by Osgood and Zieman (1998), who wrote ‘‘In a review of experimental studies, Chalmers (1982) concluded that increased porewater drainage has a positive effect on aboveground growth of Spartina alterniflora through alleviation of salinity stress, increased sediment oxygenation, or removal of phytotoxins such as hydrogen sulfide’’. Therefore, the suggestion is that the short form grows under various types of stress, whereas the tall form does not. But it seems more appropriate to view both forms as having adapted to their respective environments, performing optimally within the ranges of the prevailing environmental conditions, as both forms are stable over very long periods of time, even when grown under the same controlled conditions (Gallagher et al., 1988). The tall form of Spartina is not necessarily fitter compared with the short form, rather it has adapted to maximum fitness under its specific environmental conditions. As Whitlock (1997) argues, even small changes in environmental conditions can lead to substantial morphological evolution, with different, but equally optimal levels of fitness prevailing under the different conditions. Daehler et al. (1999) use this argument to explain the emergence of a new dwarf ecotype of Spartina alterniflora in the San Francisco Bay area. One could argue that at the scale of an entire salt marsh, considering both short and tall forms of Spartina alterniflora within that marsh to belong to one and the same population, the conditions prevailing in areas dominated by the short form are stressful. However, following Whitlock (1997), it is argued here that this
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Fig. 2. Diagram depicting the hypothetical situation for two populations of Spartina alterniflora, i.e of the short form, S, and tall form, T, using the conceptual model of Fig. 1 for each population (A, B and C as in Fig. 1), with salinity and oxygen concentration in porewater ([O2]porewater) as factors.
view is not correct and that in fact two phenotypically (and according to Gallagher et al., 1988, also genotypically) distinct populations persist in such marshes, each with their own set of environmental conditions determining different but optimum levels of fitness. This is illustrated in Fig. 2, which shows a hypothetical situation for the short form (S) and tall form (T) of Spartina alterniflora using the conceptual model of Fig. 1 for the factors salinity and oxygen concentration, [O2], in porewater (Note: In this example the mode of action may be different for different levels of salinity/[O2]; the factors may be affecting performance of the plants directly—e.g. salt toxicity—or indirectly — e.g. increased competition for space due to low salinity). Due to differences in their respective environments what is optimum for the short form (AS) is different from that of the tall form (AT) and the same applies for the sufficient (BS, BT) and limiting (CS, CT) ranges. In this example, what is optimal for the short form (AS) falls within the limiting range of the tall form (CT), while optimal conditions for the tall form (AT) overlap with the limiting (CS) and sufficient (BS) ranges of the short form. The third view, therefore, seems more appropriate, in which a situation is only considered as
stress to an organism if it is outside its normal range. Using the example of the short and tall form Spartina alterniflora, what should be considered the normal range is different for each form individually. In Fig. 2 this means that the short form is not considered to be exposed to stress if the factors salinity and [O2] fall within both the AS and BS ranges, while for the tall form this includes both the AT and BT ranges. Thus, flooding and anaerobic substrate conditions are not in themselves stressful to wetland plants, neither is salinity in the specific case of salt marsh plants. But when the environmental conditions are changed due to natural or anthropogenic activities to create situations outside the normal range, not only in intensity, but also in duration, then this may create stress in plants. While present, such stressful conditions may lead to changes in organisms rendering them better adapted to the new situation. During that process, the condition may be considered stressful, but once the organism has adapted to the new situation, the conditions that led to the adaptation should no longer be regarded as stress. Adaptations are in themselves indications that stress occurred at some stage in the evolution of a population or species. For example, plants may be adapted to the nutrient status of their environment (Chapin, 1980). But once adapted, the conditions are no longer stressful to the plants. Low nutrient environments are only that in comparison to high nutrient environments, but plants adapted to low nutrient environments are equally unsuited to live in high nutrient environments as are plants adapted to high nutrient environments in low nutrient environments. In the latter case, plants would not survive due to the stress of nutrient deficiency, while in the former case plants would not survive due to stresses related to increased competition from other, better adapted species or populations (Chapin, 1980). The phrase ‘stresses related to competition’ is used here, as the actual stress imposed on the plants due to competition is probably secondary, for example due to lack of space for root development, or increased shadowing of leaves. Similar comparisons can be made for wetland plants, for example
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regarding tolerance to salt or flooding. Salt marsh plants vary in their adaptations to their saline environment. Plants not adapted to high salinity will not survive exposure to such conditions, but while many salt tolerant plants can be grown under controlled conditions in the absence of salt in their growth medium, they are exposed to stresses related to increased competition from less salt-tolerant plants when exposed to conditions of decreased salinity in the field (Adam, 1990). Likewise, when dryland plants are exposed to continuous flooding they may die from anoxia or exposure to high levels of ferrous iron or sulphide, while wetland plants exposed to continuous drought may die from lack of water. The interactions between adaptations of wetland plants to the characteristics of their specific environment and the effects of competition may explain vegetation zonation along ecotones, such as found in salt marshes (Adam, 1990). In European salt marshes, the lower marsh, which is home to the glasswort Salicornia dolichostachya is an equally stressful environment to the high marsh species Festuca rubra as is the high marsh environment to S. dolichostachya.
3. Under what circumstances are conditions stressful to wetland plants? Following the arguments above, only extreme changes in environmental conditions should be regarded as stress (View 3). Such changes include the conditions encountered by plants under the following circumstances.
3.1. When they are introduced for crop production (agriculture, forestry) into non-nati6e habitats With the notable exception of rice, wetland plants are not common crop plants. The increasing need for food on a global scale has made it desirable to improve resistance to conditions which are not normally encountered and are, therefore, stressful to common crop plants (e.g. Fukai et al., 1999; Grover et al., 1999). ‘Stress’ is a recurring theme in agricultural research (e.g.
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McKersie and Leshem, 1994; Smallwood et al., 1999).
3.2. When extreme changes in en6ironmental conditions occur due to natural or anthropogenic processes, e.g. changes in tidal regime due to sedimentation or subsidence Examples of such situations are the changes in hydrology due to the subsidence and engineering works of the Mississippi Delta, the (re)diversion of the Cooper River, South Carolina, USA, and the engineering works in The Netherlands (the so-called Delta Works), particularly in the former brackish tidal area of the Rhine/Meuse Delta. In all three examples, major changes in landscape and vegetation have been observed (Mississippi Delta; e.g. Ford et al., 1999, Cooper River; Bradley et al., 1990, Rhine/Meuse Delta, Smit et al., 1997), indicating serious stress was imposed on the plants due to the changing environments. But which factor (or combination of factors) contributed most to the changes is difficult to assess. Ewing et al. (1997) implicated altered salinity and nutrient availability among the stresses imposed on Spartina patens in the Mississippi Delta. But despite the fact that great changes in salinity have occurred in the Cooper River, due to diversion of freshwater from the Santee River into the Cooper River (Bradley et al., 1990), viable Spartina alterniflora stands have persisted in what has been freshwater for at least 50 years (Otte and Morris, 1994). Changes in salinity, along with flooding frequency and associated sediment oxygenation, may be the most obvious consequences of changes in hydrology, but may not immediately impose stress on plants. Perhaps the different fluctuations in salinity, and the occurrence and duration of extremes are more important (Howard and Mendelssohn, 1999). Changes in the physical, rather than chemical environment may be important too, as in the Rhine/Meuse Delta where changes in wave action have been implicated in altering the vegetation (Coops et al., 1991). Obviously, what is stress to a wetland plant in relation to a changing environment strongly depends on the species and its location.
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3.3. When exposed to pollutants Wetlands tend to accumulate substances, including pollutants, from water passing through them, and as a result the structure of the wetland may alter over time. Effects of plant macronutrients, for example, have been well investigated (Mitch and Gosselink, 1986; Richardson et al. 1999). But what exactly should be considered stress in such cases remains to be seen. For example, Richardson et al. (1999) explain the shift from a sawgrass (Cladium jamaicense) dominated patchy vegetation to cattail dominated (Typha domingensis) stands in the Everglades by the increase in phosphate inputs into the system. Does this mean that phosphate is actually toxic to C. jamaicense (‘phosphate stress’), or does it mean that the stress of nutrient limitation to T. domingensis was lifted, or is the real stress a secondary effect of eutrophication due to increased competitive ability of T. domingensis? Proof of direct stress from pollutants on wetland plants is rare. Oil is perhaps the most researched organic pollutant in wetlands, particularly regarding its effects on salt marsh plants (e.g. Zengel and Michel, 1996; Smith and Proffitt, 1999). Oil spillage onto wetland plants can seriously damage the plants, but again it is not clear whether the stress imposed is the direct toxicity of the oil itself, or indirectly due to shading of leaves and covering of stomata. Probably the most researched inorganic pollutants apart from the macronutrients nitrogen and phosphorus, both in relation to wetland and dryland plants, are heavy metals. It is striking that very few reports exist of direct negative effects of metals on wetland plants in the field. Mhatre et al. (1980) reported that elevated sediment metal concentrations were associated with strongly reduced vegetation (both in cover and species numbers) downstream from urbanised and industrial areas along a river, but whether this was a causal relationship was not assessed. While the development of metal-tolerant plant populations has been well established for dryland plants (Ernst 1974), to the knowledge of the author no such observations have been reported to date for wetland plants. In fact, the use of wetlands for removal of
metals from contaminated water and for rehabilitation of mine wastes (Dunbabin and Bowmer, 1992; Beining and Otte 1996, 1997; McCabe and Otte, 1997, 2000) seems to indicate that high metal concentrations do not impose stress on wetland plants. Recent research comparing populations from metal-exposed and non metal-exposed populations of Typha latifolia (Ye et al., 1997) and Glyceria fluitans (McCabe and Otte, 2000) did not indicate differences in tolerance to elevated substrate metal concentrations, suggesting that exposure of wetland plants to high concentrations of metals does not impose stress. The lack of observations on metal tolerance in wetland plants, while many species can easily be established on metal-rich substrates and take up metals to concentrations several magnitudes higher compared with control plants (McCabe and Otte, 1997, 2000), suggests that wetland plants may be innately tolerant to metals. However, proper comparisons between wetland and dryland plants have not been made. The above examples illustrate that wetland plants appear to be highly plastic in their response to ‘stress’, and reports of effects of truly stressful conditions to wetland plants are rare. It further appears that what is referred to as a primary response to stress, e.g. ‘salinity stress’ or ‘oil stress’, may well be due to secondary effects.
4. Conclusion As argued above, how we as scientists and teachers address stress may affect public perception of the environments associated with it. While public perception regarding wetlands in the USA is now generally positive and wetlands are legally protected, the situation is quite different in many other countries. In Ireland, for example, wetlands are still considered wastelands by many and no legal protection specific to wetlands exists. As recently as September 1999, a Dublin Corporation councillor, N. Cosgrave, was quoted as referring to the North Bull Island (Dublin Bay, Ireland) salt marshes and mudflats as an ‘‘unsightly mud and algae covered flat’’ which ‘‘causes a serious blight on a possible watersports area’’ in a local
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newspaper (North Side News, 29 September 1999, p. 10). The view might develop that, if these environments are considered ‘stressful’ to the organisms living in them as well, then why not get rid of them as quickly as possible? What is considered stress to wetland plants is, therefore, not just about semantics. Scientists need clear, unequivocal definitions of terms, and while scientists should perhaps not be concerned with how their work is interpreted by the general public, it would help if the use of emotive terms would be avoided. The term stress has a negative connotation in most languages. Applying it to any deviation from optimum conditions is confusing, to say the least. Neither is it helpful to use derived terms, such as ‘eustress’, to indicate ‘mild stress’ that leads to positive changes, i.e. adaptations, or ‘disstress’, to indicate levels of stress that are damaging to the organism, as proposed by Lichtenthaler (1996). Small changes in environmental conditions, within the normal range, should perhaps be referred to as ‘pressure’, rather than ‘stress’. Environmental conditions characteristic of wetlands are not stressful to wetland plants. It is only in comparison with non-adapted plants, i.e. when dryland plants are exposed to wetland conditions outside their normal range (such as waterlogging, low availability of oxygen to roots, high concentrations of ferrous iron, sulphide or salt) that wetland conditions are seen to be stressful; to the dryland plants, not to the wetland plants.
Acknowledgements Thanks to Mark McCorry and Donna Jacob for their helpful comments on the manuscript.
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What is stress to a wetland plant? Marinus L. Otte * Wetland Ecology Research Group, Department of Botany, Uni6ersity College Dublin, Belfield, Dublin 4, Ireland
Abstract The definitions of the term ‘stress’ and its applications are reviewed in relation to wetland plants. Three views on the use of the term stress prevail; (1) that it should not be used at all; (2) that it defines any situation which leads to a decrease from optimum performance; and (3) that it should only apply to extreme conditions, outside the normal range of the organism. It is argued here that View 3 should be accepted only; i.e. that stress should only be regarded to be arising from changes in environmental conditions outside the normal range encountered by plants. Conditions normally encountered by wetland plants, such as waterlogged, anaerobic soils and salinity, are not stressful to such plants, but only to non-adapted dryland plants. Stress occurs only when plants are exposed to environmental conditions outside the range they are normally exposed to due to natural or anthropogenic changes. Such conditions are found in agriculture—when plants are grown in places they would not naturally grow, in rapidly changing environments—for example when hydrology is changed due to subsidence or engineering works, and under conditions of environmental pollution. The actual stress imposed on wetland plants may be secondary to the factor thought to cause the stress. Very few studies exist showing direct stress on wetland plants. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Stress; Wetland; Salt marsh; Plants
1. Introduction The subject of this paper originates from an invitation to the author for participation in the symposium on ‘Plants and organisms in stressed wetland environments’ as part of the Quebec 2000 Millennium Wetland Event. The invitation immediately raised the question; what, indeed, is stress to a wetland plant? There is a discrepancy between the academic definition of stress and its perception by the gen* Corresponding author. Tel.: +353-1-716-2019; + 353-1-716-1153. E-mail address: [email protected] (M.L. Otte).
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eral public. For example, asked which would be a more stressful environment for plants, a salt marsh or a garden lawn, most people would probably answer; a salt marsh. This is because stress is often associated with environments that are extreme from a human point of view, e.g. deserts, polar regions, and wetlands, and are described as such even in scientific literature (for example Crawford, 1989). But the conditions prevailing in salt marshes are the normal conditions for naturally occurring plants, while grasses in lawns may be growing in an environment in which they would not normally grow and may be cut with a lawnmower once every 2 weeks during the grow-
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ing season, surely a stressful situation. It is against this background that the question ‘What is stress to a wetland plant’ is addressed in this paper.
often still lacking (for example Lerner, 1999). The views on how the term stress should be defined and used can be divided into three categories.
2.1. Stress is not a useful term (View 1) 2. Perceptions, misconceptions and definitions of stress How stress is defined by researchers depends on the research subject of interest and background of the researcher, and as a result many different definitions exist (for example Calow, 1989; Crawford, 1989; Grime, 1989; Jones and Jones, 1989; Da¨ mmgen et al., 1993; Lichtenthaler, 1996). But what is truly stressful to a plant is difficult to assess. The debate surrounding the definitions of stress, more specifically in relation to ecological processes, was particularly strong during the 1980s (Grime, 1989). How stress is defined and referred to is not only of academic importance, but can eventually affect public perception. Initially used in scientific publications, a term may be used in teaching and popular texts, and in the press. As a result, such terms in the public’s mind may become associated with certain environments. These associations can lead to misconceptions about such environments. The following statements regarding wetlands illustrate this: ‘‘Compared with the vegetation of well-drained soils, wetlands have a worldwide similarity which over-rides climate and is imposed by the common characteristics of a free water supply and the abnormally hostile chemical environment which plant roots must endure’’ (Etherington, 1983). ‘‘Wetland plants have developed mechanisms which allow them to survive in these stressful environments for extended periods of time’’ (Beall, 1997). Such statements convey the notion that wetlands are innately difficult environments in which to live or ‘survive’ (Crawford, 1989). Since the discussions on how stress should be defined reached a high point in the 1980s confusion has persisted, and to date no agreement has been reached among researchers. Even in the most recent literature proper definitions of the term are
The term ‘stress’ cannot be defined appropriately in biological terms and has different meanings in physics and psychology, and its use should thus be avoided. This view was voiced by Harper (1986).
2.2. Stress occurs continuously (View 2) Stress causes a deviation from the optimum conditions (usually a reduction) regarding variables such as biomass production and reproduction. It can be described as ‘‘external constraints limiting the rates of resource acquisition, growth or reproduction of organisms’’ (Grime, 1989). A similar definition was used by Crawford (1989): ‘‘Any environmental factor which restricts growth and reproduction of an organism or population’’, and was adopted for the textbook by Freedman (1995): ‘‘Stress is simplistically defined in this book as environmental influences that cause measurable ecological changes, or that limit ecological development’’.
2.3. Stress occurs under extreme conditions only (View 3) Stress occurs when organisms are exposed to extreme conditions, i.e. conditions outside the normal range. This view is supported by, for example, Larcher (1991): ‘‘Stress is the exposure to extraordinarily unfavourable conditions’’, Da¨ mmgen et al. (1993): ‘‘Flux densities of energy, momentum and matter become stressors either by themselves or in combination, if they exceed or fall below normal ranges, i.e. if existing steady states of biotic systems (organ, organism, society,…) or abiotic systems (atmosphere) are changed’’, and Nilsen and Orcutt (1996) ‘‘conditions that cause an aberrant change in physiological processes resulting eventually in injury’’. The difference between views 2 and 3 is that, according to view 2, any deviations from the
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optimum situation (see Fig. 1, area A) would be considered as resulting from stress, in other words, organisms are continuously living under stress in one form or another. In contrast, view 3 does not consider variations within the optimum and sufficient ranges (Fig. 1, areas A+ B) to be stressful. What is an optimum situation according to view 2 is usually determined by measurement of growth or biomass production, with high values being considered ‘non-stressed’ and low values ‘stressed’. While the arguments against using the term stress (View 1) could be considered valid (as also Grime, 1989, concedes), the fact is that it has become embedded in ecological research and its use has helped us understand processes underlying changes at the population/community level. Also, inventing a new term would bring along with it the same problems of misinterpretation. View 1, therefore, is not a desirable approach to the problem. View 2 is not appropriate either, as variations in conditions outside the optimum, but within the normal range are not necessarily stressful. This is exemplified by the occurrence of two forms of Spartina alterniflora along the southeastern coasts of the US, the tall and short growth forms. The
Fig. 1. Diagram depicting a conceptual model of the effects of two factors on performance (e.g. growth) of plants (no interaction between factors). Lim, limiting (too low or too high), Suf, sufficient, O, optimal. Optimum conditions prevail for both factors in area A, while sufficient, but not optimal conditions prevail in area B. In area C conditions are limiting, but not lethal, while outside area C conditions are lethal and the plants could not survive. Under normal conditions, factors would vary within areas A and B.
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tall form tends to be associated with well-drained creekbanks, while the short form is associated with less drained areas between creeks. The differences in hydrology lead to differences in levels and fluctuations of, for example, nutrient inputs, porewater salinity and sulphide concentrations. The differences between the two forms can be explained by the differences in sediment chemistry of their habitats (Valiela et al., 1978; Howes et al., 1986; Ornes and Kaplan, 1989; Osgood and Zieman, 1998), but the forms also vary genetically (Stalter and Batson, 1969; Gallagher et al., 1988). Studies on the two growth forms tend to consider the short growth form as stressed compared with the tall form. This is illustrated by Osgood and Zieman (1998), who wrote ‘‘In a review of experimental studies, Chalmers (1982) concluded that increased porewater drainage has a positive effect on aboveground growth of Spartina alterniflora through alleviation of salinity stress, increased sediment oxygenation, or removal of phytotoxins such as hydrogen sulfide’’. Therefore, the suggestion is that the short form grows under various types of stress, whereas the tall form does not. But it seems more appropriate to view both forms as having adapted to their respective environments, performing optimally within the ranges of the prevailing environmental conditions, as both forms are stable over very long periods of time, even when grown under the same controlled conditions (Gallagher et al., 1988). The tall form of Spartina is not necessarily fitter compared with the short form, rather it has adapted to maximum fitness under its specific environmental conditions. As Whitlock (1997) argues, even small changes in environmental conditions can lead to substantial morphological evolution, with different, but equally optimal levels of fitness prevailing under the different conditions. Daehler et al. (1999) use this argument to explain the emergence of a new dwarf ecotype of Spartina alterniflora in the San Francisco Bay area. One could argue that at the scale of an entire salt marsh, considering both short and tall forms of Spartina alterniflora within that marsh to belong to one and the same population, the conditions prevailing in areas dominated by the short form are stressful. However, following Whitlock (1997), it is argued here that this
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Fig. 2. Diagram depicting the hypothetical situation for two populations of Spartina alterniflora, i.e of the short form, S, and tall form, T, using the conceptual model of Fig. 1 for each population (A, B and C as in Fig. 1), with salinity and oxygen concentration in porewater ([O2]porewater) as factors.
view is not correct and that in fact two phenotypically (and according to Gallagher et al., 1988, also genotypically) distinct populations persist in such marshes, each with their own set of environmental conditions determining different but optimum levels of fitness. This is illustrated in Fig. 2, which shows a hypothetical situation for the short form (S) and tall form (T) of Spartina alterniflora using the conceptual model of Fig. 1 for the factors salinity and oxygen concentration, [O2], in porewater (Note: In this example the mode of action may be different for different levels of salinity/[O2]; the factors may be affecting performance of the plants directly—e.g. salt toxicity—or indirectly — e.g. increased competition for space due to low salinity). Due to differences in their respective environments what is optimum for the short form (AS) is different from that of the tall form (AT) and the same applies for the sufficient (BS, BT) and limiting (CS, CT) ranges. In this example, what is optimal for the short form (AS) falls within the limiting range of the tall form (CT), while optimal conditions for the tall form (AT) overlap with the limiting (CS) and sufficient (BS) ranges of the short form. The third view, therefore, seems more appropriate, in which a situation is only considered as
stress to an organism if it is outside its normal range. Using the example of the short and tall form Spartina alterniflora, what should be considered the normal range is different for each form individually. In Fig. 2 this means that the short form is not considered to be exposed to stress if the factors salinity and [O2] fall within both the AS and BS ranges, while for the tall form this includes both the AT and BT ranges. Thus, flooding and anaerobic substrate conditions are not in themselves stressful to wetland plants, neither is salinity in the specific case of salt marsh plants. But when the environmental conditions are changed due to natural or anthropogenic activities to create situations outside the normal range, not only in intensity, but also in duration, then this may create stress in plants. While present, such stressful conditions may lead to changes in organisms rendering them better adapted to the new situation. During that process, the condition may be considered stressful, but once the organism has adapted to the new situation, the conditions that led to the adaptation should no longer be regarded as stress. Adaptations are in themselves indications that stress occurred at some stage in the evolution of a population or species. For example, plants may be adapted to the nutrient status of their environment (Chapin, 1980). But once adapted, the conditions are no longer stressful to the plants. Low nutrient environments are only that in comparison to high nutrient environments, but plants adapted to low nutrient environments are equally unsuited to live in high nutrient environments as are plants adapted to high nutrient environments in low nutrient environments. In the latter case, plants would not survive due to the stress of nutrient deficiency, while in the former case plants would not survive due to stresses related to increased competition from other, better adapted species or populations (Chapin, 1980). The phrase ‘stresses related to competition’ is used here, as the actual stress imposed on the plants due to competition is probably secondary, for example due to lack of space for root development, or increased shadowing of leaves. Similar comparisons can be made for wetland plants, for example
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regarding tolerance to salt or flooding. Salt marsh plants vary in their adaptations to their saline environment. Plants not adapted to high salinity will not survive exposure to such conditions, but while many salt tolerant plants can be grown under controlled conditions in the absence of salt in their growth medium, they are exposed to stresses related to increased competition from less salt-tolerant plants when exposed to conditions of decreased salinity in the field (Adam, 1990). Likewise, when dryland plants are exposed to continuous flooding they may die from anoxia or exposure to high levels of ferrous iron or sulphide, while wetland plants exposed to continuous drought may die from lack of water. The interactions between adaptations of wetland plants to the characteristics of their specific environment and the effects of competition may explain vegetation zonation along ecotones, such as found in salt marshes (Adam, 1990). In European salt marshes, the lower marsh, which is home to the glasswort Salicornia dolichostachya is an equally stressful environment to the high marsh species Festuca rubra as is the high marsh environment to S. dolichostachya.
3. Under what circumstances are conditions stressful to wetland plants? Following the arguments above, only extreme changes in environmental conditions should be regarded as stress (View 3). Such changes include the conditions encountered by plants under the following circumstances.
3.1. When they are introduced for crop production (agriculture, forestry) into non-nati6e habitats With the notable exception of rice, wetland plants are not common crop plants. The increasing need for food on a global scale has made it desirable to improve resistance to conditions which are not normally encountered and are, therefore, stressful to common crop plants (e.g. Fukai et al., 1999; Grover et al., 1999). ‘Stress’ is a recurring theme in agricultural research (e.g.
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McKersie and Leshem, 1994; Smallwood et al., 1999).
3.2. When extreme changes in en6ironmental conditions occur due to natural or anthropogenic processes, e.g. changes in tidal regime due to sedimentation or subsidence Examples of such situations are the changes in hydrology due to the subsidence and engineering works of the Mississippi Delta, the (re)diversion of the Cooper River, South Carolina, USA, and the engineering works in The Netherlands (the so-called Delta Works), particularly in the former brackish tidal area of the Rhine/Meuse Delta. In all three examples, major changes in landscape and vegetation have been observed (Mississippi Delta; e.g. Ford et al., 1999, Cooper River; Bradley et al., 1990, Rhine/Meuse Delta, Smit et al., 1997), indicating serious stress was imposed on the plants due to the changing environments. But which factor (or combination of factors) contributed most to the changes is difficult to assess. Ewing et al. (1997) implicated altered salinity and nutrient availability among the stresses imposed on Spartina patens in the Mississippi Delta. But despite the fact that great changes in salinity have occurred in the Cooper River, due to diversion of freshwater from the Santee River into the Cooper River (Bradley et al., 1990), viable Spartina alterniflora stands have persisted in what has been freshwater for at least 50 years (Otte and Morris, 1994). Changes in salinity, along with flooding frequency and associated sediment oxygenation, may be the most obvious consequences of changes in hydrology, but may not immediately impose stress on plants. Perhaps the different fluctuations in salinity, and the occurrence and duration of extremes are more important (Howard and Mendelssohn, 1999). Changes in the physical, rather than chemical environment may be important too, as in the Rhine/Meuse Delta where changes in wave action have been implicated in altering the vegetation (Coops et al., 1991). Obviously, what is stress to a wetland plant in relation to a changing environment strongly depends on the species and its location.
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3.3. When exposed to pollutants Wetlands tend to accumulate substances, including pollutants, from water passing through them, and as a result the structure of the wetland may alter over time. Effects of plant macronutrients, for example, have been well investigated (Mitch and Gosselink, 1986; Richardson et al. 1999). But what exactly should be considered stress in such cases remains to be seen. For example, Richardson et al. (1999) explain the shift from a sawgrass (Cladium jamaicense) dominated patchy vegetation to cattail dominated (Typha domingensis) stands in the Everglades by the increase in phosphate inputs into the system. Does this mean that phosphate is actually toxic to C. jamaicense (‘phosphate stress’), or does it mean that the stress of nutrient limitation to T. domingensis was lifted, or is the real stress a secondary effect of eutrophication due to increased competitive ability of T. domingensis? Proof of direct stress from pollutants on wetland plants is rare. Oil is perhaps the most researched organic pollutant in wetlands, particularly regarding its effects on salt marsh plants (e.g. Zengel and Michel, 1996; Smith and Proffitt, 1999). Oil spillage onto wetland plants can seriously damage the plants, but again it is not clear whether the stress imposed is the direct toxicity of the oil itself, or indirectly due to shading of leaves and covering of stomata. Probably the most researched inorganic pollutants apart from the macronutrients nitrogen and phosphorus, both in relation to wetland and dryland plants, are heavy metals. It is striking that very few reports exist of direct negative effects of metals on wetland plants in the field. Mhatre et al. (1980) reported that elevated sediment metal concentrations were associated with strongly reduced vegetation (both in cover and species numbers) downstream from urbanised and industrial areas along a river, but whether this was a causal relationship was not assessed. While the development of metal-tolerant plant populations has been well established for dryland plants (Ernst 1974), to the knowledge of the author no such observations have been reported to date for wetland plants. In fact, the use of wetlands for removal of
metals from contaminated water and for rehabilitation of mine wastes (Dunbabin and Bowmer, 1992; Beining and Otte 1996, 1997; McCabe and Otte, 1997, 2000) seems to indicate that high metal concentrations do not impose stress on wetland plants. Recent research comparing populations from metal-exposed and non metal-exposed populations of Typha latifolia (Ye et al., 1997) and Glyceria fluitans (McCabe and Otte, 2000) did not indicate differences in tolerance to elevated substrate metal concentrations, suggesting that exposure of wetland plants to high concentrations of metals does not impose stress. The lack of observations on metal tolerance in wetland plants, while many species can easily be established on metal-rich substrates and take up metals to concentrations several magnitudes higher compared with control plants (McCabe and Otte, 1997, 2000), suggests that wetland plants may be innately tolerant to metals. However, proper comparisons between wetland and dryland plants have not been made. The above examples illustrate that wetland plants appear to be highly plastic in their response to ‘stress’, and reports of effects of truly stressful conditions to wetland plants are rare. It further appears that what is referred to as a primary response to stress, e.g. ‘salinity stress’ or ‘oil stress’, may well be due to secondary effects.
4. Conclusion As argued above, how we as scientists and teachers address stress may affect public perception of the environments associated with it. While public perception regarding wetlands in the USA is now generally positive and wetlands are legally protected, the situation is quite different in many other countries. In Ireland, for example, wetlands are still considered wastelands by many and no legal protection specific to wetlands exists. As recently as September 1999, a Dublin Corporation councillor, N. Cosgrave, was quoted as referring to the North Bull Island (Dublin Bay, Ireland) salt marshes and mudflats as an ‘‘unsightly mud and algae covered flat’’ which ‘‘causes a serious blight on a possible watersports area’’ in a local
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newspaper (North Side News, 29 September 1999, p. 10). The view might develop that, if these environments are considered ‘stressful’ to the organisms living in them as well, then why not get rid of them as quickly as possible? What is considered stress to wetland plants is, therefore, not just about semantics. Scientists need clear, unequivocal definitions of terms, and while scientists should perhaps not be concerned with how their work is interpreted by the general public, it would help if the use of emotive terms would be avoided. The term stress has a negative connotation in most languages. Applying it to any deviation from optimum conditions is confusing, to say the least. Neither is it helpful to use derived terms, such as ‘eustress’, to indicate ‘mild stress’ that leads to positive changes, i.e. adaptations, or ‘disstress’, to indicate levels of stress that are damaging to the organism, as proposed by Lichtenthaler (1996). Small changes in environmental conditions, within the normal range, should perhaps be referred to as ‘pressure’, rather than ‘stress’. Environmental conditions characteristic of wetlands are not stressful to wetland plants. It is only in comparison with non-adapted plants, i.e. when dryland plants are exposed to wetland conditions outside their normal range (such as waterlogging, low availability of oxygen to roots, high concentrations of ferrous iron, sulphide or salt) that wetland conditions are seen to be stressful; to the dryland plants, not to the wetland plants.
Acknowledgements Thanks to Mark McCorry and Donna Jacob for their helpful comments on the manuscript.
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