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Behavioral Ecology | Acclimation 15

Finally, a practical rather than a conceptual problem with the method is that it relies on a painstaking and timeconsuming (and hence costly) analysis of samples in which all the species must be separated, counted, and weighed. Several groups of marine organisms are taxonomically difficult, for example (in the macrobenthos), several families of polychaetes and amphipods; as much time can be spent in separating a few of these difficult groups into species as the entire remainder of the sample, even in Northern Europe where taxonomic keys for identification are most readily available. Many taxa really require the skills of specialists to separate them into species, and this is especially true in parts of the world where fauna is poorly described. Identification to some higher taxonomic level, for example, family rather than species, is considerably easier and quicker, and the ABC method has proved to be encouragingly robust to analysis at the family level for both macrobenthos and fish; very little information appears to be lost. See also: k-Dominance Curves; r-Strategist/ K-Strategists.

Further Reading Agard JBR, Gobin J, and Warwick RM (1993) Analysis of marine macrobenthic community structure in relation to oil pollution, natural oil seepage, and seasonal disturbance in a tropical environment (Trinidad, West Indies). Marine Ecology Progress Series 92: 233–243. Beukema JJ (1988) An evaluation of the ABC-method (abundance/ biomass comparison) as applied to macrozoobenthic communities

living on tidal flats in the Dutch Wadden Sea. Marine Biology 99: 425–433. Blanchard F, LeLoc’h F, Hily C, and Boucher J (2004) Fishing effects on diversity, size, and community structure of the benthic invertebrate and fish megafauna on the Bay of Biscay coast of France. Marine Ecology Progress Series 280: 249–260. Clarke KR (1990) Comparisons of dominance curves. Journal of Experimental Marine Biology and Ecology 138: 143–157. Dauer DM, Luckenbach MW, and Rodi AJ (1993) Abundance biomass comparison (ABC method) – Effects of an estuarine gradient, anoxic hypoxic events and contaminated sediments. Marine Biology 116: 507–518. Ismael AA and Dorgham MM (2003) Ecological indices as a tool for assessing pollution in El-Dekhaila Harbour (Alexandria, Egypt). Oceanologia 45: 121–131. Jouffre D and Inejih CA (2005) Assessing the impact of fisheries on demersal fish assemblages of the Mauritanian continental; shelf, 1987–1999, using dominance curves. ICES Journal of Marine Science 62: 380–383. Lasiak T (1999) The putative impact of exploitation on rocky infratidal macrofaunal assemblages: A multiple area comparison. Journal of the Marine Biological Association of the United Kingdom 79: 23–34. Magurran AE (2004) Measuring Biological Diversity. Oxford: Blackwell. Penczak T and Kruk A (1999) Applicability of the abundance/biomass comparison method for detecting human impacts on fish populations in the Pilica River, Poland. Fisheries Research 39: 229–240. Warwick RM (1986) A new method for detecting pollution effects on marine macrobenthic communities. Marine Biology 92: 557–562. Warwick RM and Clarke KR (1994) Relearning the ABC: Taxonomic changes and abundance/biomass relationships in disturbed benthic communities. Marine Biology 118: 739–744. Warwick RM, Pearson TH, and Ruswahyuni (1987) Detection of pollution effects on marine macrobenthos: Further evaluation of the species abundance/biomass method. Marine Biology 95: 193–200. Yemane D, Field JG, and Leslie RW (2005) Exploring the effects of fishing on fish assemblages using abundance biomass comparison (ABC) curves. ICES Journal of Marine Science 62: 374–379.

Acclimation B Demmig-Adams, M R Dumlao, M K Herzenach, and W W Adams III, University of Colorado, Boulder, CO, USA ª 2008 Elsevier B.V. All rights reserved.

Acclimation versus Adaptation Do Plants Have a Particularly High Potential for Acclimation? Acclimation Patterns Depend on Species and the Severity of the Environment

Principal Types of Adjustments: Plant Form, Function, and Lifecycle Acclimation Responses to Specific Environmental Factors Oxidative Stress and Redox Signaling as Common Denominators in Stress Perception and Response Further Reading

Acclimation versus Adaptation

constrained by the genome of the individual. In turn, adaptation involves the acquisition or recombination of genetic traits that improve performance or survival over multiple generations. For example, all plants have the ability to adjust their form and function to acclimate to some extent to, for example, warmer versus cooler

Acclimation involves physiological, anatomical, or morphological adjustments within a single organism that improve performance or survival in response to environmental change. The extent of this acclimation is

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temperatures or higher versus lower light levels. However, only plants adapted to cool climates (i.e., species that have evolved in temperate or higher latitudes, or at higher elevations) possess a set of genetic traits permitting adjustments to the level necessary to survive extreme cold. Similarly, only plants adapted to shade are able to make the adjustments necessary to survive in the understory of a multilayered rainforest canopy. While acclimation will be the focus of this article, it will be discussed against the background of adaptation.

Do Plants Have a Particularly High Potential for Acclimation? It is often considered that plants, as sessile organisms, may require more powerful adjustments and defenses against environmental challenges than animals that are typically endowed with mobility and thus with the option of moving to a less hostile environment. Beyond these obvious differences, however, lies a striking similarity in the underlying principles and responses that govern the physiological acclimation of plants and animals to the environment. While this article focuses on plant acclimation, these parallels as well as some differences will be noted throughout.

Acclimation Patterns Depend on Species and the Severity of the Environment In plants as well as animals, one can distinguish three principal and different scenarios. (1) True internal tolerance to altered environmental conditions occurs when the internal conditions within tissues and cells of the organism are shifted as the external conditions change, and yet the organism’s metabolism is able to proceed under these somewhat altered conditions. For example, some plants exhibit osmotic adjustment, the accumulation of solutes that do not interfere with metabolism, when soil water availability decreases and thus track the external conditions by decreases in their tissue water content. (2) In contrast, other organisms avoid internal change by compensatory mechanisms (e.g., maintenance of a constant high tissue water content as a drought progresses). (3) Finally, in the most extreme example of evasion, life cycle adjustments allow an organism to persist through unfavorable conditions/seasons in a state with minimal or no metabolic activity. Remarkably, plant species employing these contrasting strategies often coexist in the very same habitat! For example, in a hot and dry desert environment, waterstoring cacti, maintaining a high internal tissue water

content, can be found growing side by side with species that allow their tissues to lose considerable amounts of water and yet remain metabolically active by virtue of osmotic adjustment. After a spring rainfall, the same desert may explode with soft-leafed ephemerals that are neither equipped to store water nor to tolerate low internal water content (except for their seeds). These ephemerals complete their life cycle in an extraordinarily short period and disappear before the drought returns, leaving only highly drought tolerant seeds behind. However, plants employing these different strategies do tend to differ in the range of environmental conditions they tolerate. For example, the proverbial cactus in the desert must periodically refill its water stores and is typically unable to survive in the most extreme deserts with extended periods of drought through which only species truly tolerant of low internal water content are able to persist. On the other hand, the seeds of the escape artist species may skip a year or more with no large rainfall events without germinating, only to repopulate the scene after an extended drought period through which no other plant life has survived. Another scenario is found along mountain slopes in temperate climates with cold winters, where lower altitudes are populated by a mix of annuals with soft tissues versus hardy evergreen ground covers and coniferous trees. At higher altitudes, the highly resistant conifers predominate by virtue of their tolerance to altered internal conditions, enabling them to survive long winters with subfreezing temperatures and frozen soils that deprive plants of access to liquid water. Above treeline, only ground-hugging evergreens, winter-deciduous species, and very few annuals are able to survive. Thus, acclimation to moderately stressful conditions frequently involves adjustments to maintain metabolic activity or to tolerate a modest departure from optimal internal conditions. In contrast, acclimation to the most extreme environments (like deserts, high altitudes), characterized by cycles of favorable and extremely harsh seasons, often involves the ability to shut down metabolism and survive harsh conditions in a metabolically inactive, yet highly resistant state. In summary, major principal response types include the following: short-lived species escape stressful seasons • Fast-growing, by completing their life cycle before the harshest conditions set in. While true in the extreme for the desert ephemerals, the same principle is used by many annual and biennial weeds and crops: when they encounter moderate stress, these species maintain a high level of metabolic activity, for example, keeping the capacity for photosynthesis up in the winter (in winter wheat and other crops), keeping leaf pores (stomata) open via

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•

•

•

osmotic adjustment under moderate drought (for more detail, see the final section, ‘Oxidative stress and redox signaling as common denominators in stress perception and response’), etc. Drought-deciduous or winter-deciduous species permit the most vulnerable portions of the plant to senesce as the plant enters a period of unfavorable conditions (e.g., low water availability, exceedingly high temperatures, subfreezing temperatures). This can involve the loss of leaves or needles, twigs, whole branches, the entire aboveground portion of the plant, or major portions of the root system. However, during the senescence process, essential mobile resources are recovered and stored for use during the next period of conditions favorable for activity and growth. Slow-growing evergreens naturally undergo multiple cycles of growth during favorable seasons and coordinated inactivation of whole metabolic pathways (like photosynthesis) during unfavorable seasons, for example, hot and dry summers in the desert or winters with subfreezing temperatures. At the extreme end of the stress tolerance range, many plant seeds, as well as a few specialists like resurrection plants, can dry out completely and remain in this state for years before becoming revived during a substantial precipitation event.

Plant species vary greatly in their ability to respond to an increased availability of resources, depending on their evolutionary history and adaptation to stress (for more detail, see below). Those adapted to persist through more stressful conditions are generally less responsive to factors such as increased nutrient, water, or CO2 availability. Part of the success of invasive species derives from their ability to respond positively to increased resource availability and outcompete the native species genetically constrained to respond less strongly.

Principal Types of Adjustments: Plant Form, Function, and Lifecycle Acclimation While specific responses to individual environmental factors will be discussed further in the final section, a comprehensive overview of common adjustments is presented here. Two major aspects of how a plant can optimize performance and survival under changing environmental conditions are adjustments in (1) physical form or (2) metabolic function and, of course, combinations of the two. Similar principal responses can be seen in response to a variety of different environmental factors. At the end of this section, adjustments (such as arrest) of the life cycle are also briefly discussed.

Plant Form and Size In contrast to the relatively narrow genetic constraints on form and size within a given animal species, plants exhibit a great deal of phenotypic plasticity. Many plant species exhibit indeterminate growth, that is, continued growth throughout the entire lifespan of the organism. Such growth is continually adjusted in response to multiple environmental factors via internal signaling networks that optimize the expression of the plant’s genetic potential. Environmental factors contributing to the regulation of growth and development include light (quantity, quality, periodicity, and direction), temperature, water availability, nutrient availability, wind, pollution, soil compactness and available rooting volume, and gravity. The same factors also contribute to the modulation of plant function (see below). Each of these factors is perceived or measured by the plant, followed by transduction of that perception to a signal feeding into a network of regulatory pathways, and often involving one or more plant hormones as well as signals related to plant redox state (see below). Some of these factors will result in increased growth as a response to take advantage of available conditions or resources, whereas others will result in decreased growth as an acclimatory response to stress. Each plant makes continual adjustments to maintain a balance between investment of resources into a root system that is sufficiently elaborate to supply the shoot with water and nutrients versus a shoot system that is sufficiently developed to provide the plant and its symbionts with an adequate supply of reduced carbon. For instance, in the understory of a canopy, where light is typically limiting for plant growth, plants generally have a lower root-to-shoot ratio, thereby placing a greater emphasis on light collection and carbon reduction than on the acquisition of water and nutrients. On the other hand, plants that develop in an open field in full sunlight generally have a higher root-to-shoot ratio, thereby placing a greater emphasis on water and nutrient acquisition under conditions where abundant light is available for photosynthesis in the shoot. Exposure to greater levels of wind also results in shorter and stockier plants that invest a greater proportion of resources into structural components (e.g., lignin) that provide resistance to mechanical strain. Similarly, a root system that develops in a more compact soil will be less extensive than one that develops in a looser soil. This balance between investment into the root versus the shoot at the whole plant level is maintained through perception of the environmental conditions as well as the relative activities of the different portions of the plant. Plant hormones, and control over their synthesis, degradation, and inactivation through conjugation and transport, as well as control over the level and activity of hormone receptors, play a large role in this

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developmental flexibility. This is especially true of two hormones essential to plant viability (no mutants that lack either of these two hormones have been identified to date). The auxins are synthesized primarily in the shoot apical meristems and transported downward through the plant. On the other hand, the cytokinins are synthesized primarily in the root apical meristems and transported upward through the xylem of the plant. These two plant hormones act antagonistically with regard to differentiation of shoot versus root tissue, leading to appropriate adjustments in the development of each. When present at relatively higher levels, cytokinins stimulate shoot growth, whereas relatively higher levels of auxins stimulate root growth. Within the plant, the two transport systems primarily responsible for the upward movement of water and nutrients (the xylem) and the bi-directional movement of sugars and remobilized nutrients (the phloem) are also subject to some acclimation depending on the conditions under which they develop. Under conditions where water is readily available, as well as under conditions where nutrients are limiting, the conducting cells of the xylem (tracheids and vessels) develop with a greater diameter to facilitate higher rates of water and nutrient delivery. On the other hand, tracheids and vessels develop with a smaller diameter under conditions where water is limiting or nutrients are plentiful. This is especially important to prevent the introduction of air bubbles into the waterconducting xylem cells (a process known as cavitation), a phenomenon that prevents continued water flow and is more likely to occur in larger cells under increasing water stress as well as during freeze–thaw cycles during the winter. Acclimation of the vascular system can extend to the leaf level as well. In many species, leaves that grow and expand under high-light conditions develop a larger network of veins (have a higher vein density per leaf area) than those that acclimate to low-light conditions. In addition to supplying more water (important to support higher rates of transpirational water loss and cooling in the high-light environment) and nutrients to a leaf, a greater vein density can also provide for a more extensive pipeline for the export of sugars produced through the higher rates of photosynthesis in high-lightacclimated leaves. Other species (some of those that utilize an active, biochemical step to move sugars into the phloem; see below) do not exhibit any adjustments in the leaf vein density. Many other anatomical and morphological aspects of leaves are subject to acclimation. Leaves that develop in the shade tend to be larger, thinner, and displayed horizontally (features emphasizing light capture), whereas leaves in the sun tend to be smaller, to have more layers of, and/or longer, palisade mesophyll cells, and can be displayed more vertically (lesser emphasis on light

capture but a greater emphasis on reducing water loss). Other leaf-level features that may be adjusted (depending on species) to contribute to decreased water loss under higher-light conditions include an increased deposition of cuticular waxes, increased development of epidermal hairs (to increase reflection and decrease heat load, as well as providing a barrier to water loss), and increased deposition of salts on the epidermis or in leaf hairs (increased reflectance). Many of these adjustments are effective as features that contribute to the acclimation of plants to higher temperatures as well. In contrast to the vast majority of animals, plants are, as noted above, able to self-amputate certain vulnerable portions of their structure as an acclimation strategy in response to stress or seasonal change. The most common is the annual shedding of leaves, but it is not unusual for entire branches and roots to be lost as well. Furthermore, plants can continue to thrive in the face of unanticipated loss or modification of their structure as a result of powerful winds or freeze-induced damage, or of the activity of organisms that rely on plants for shelter (birds, mammals, reptiles, insects) or resources (herbivores, parasites (e.g., mistletoes, dodder), and various pathogenic microorganisms (fungi, bacteria, and viruses)). Such losses often result in the compensatory growth of new foliage or roots. Plant Function: Metabolism/Biochemistry While the structural changes that plants undergo can be radical, the acclimatory adjustments at the molecular, biochemical, and physiological level are equally remarkable. For example, the primary pathways of energy metabolism, respiration and photosynthesis, are both subject to considerable regulation. When able to produce an abundance of carbohydrates, plants upregulate pathways for utilization (including respiration, and investment into additional growth and reproduction) and storage. If the demand for utilization and storage of carbon lags behind the production of sugars through photosynthesis, then the enzymes and electron-transport components of photosynthesis are downregulated. On the other hand, if the consumption of sugars exceeds their supply, then photosynthesis is upregulated in the source leaves to meet the demand of the plant for the carbohydrates. Also upregulated are enzymes responsible for converting photosynthetically produced sugars to the types of sugars transported throughout the plant, as well as transport proteins that move those sugars into the phloem (in those species that utilize such proteins). Many other enzymes and pathways are also subject to regulation depending on their role in the plant, the developmental state of the plant, and the environmental conditions. For example, synthesis and accumulation of secondary plant compounds such as the phenolic flavonoids (accumulating in the vacuoles of the epidermis, the

Behavioral Ecology | Acclimation 19

cuticle layer, in epidermal hairs, and in epidermal cell walls as a screen against the damaging effects of ultraviolet radiation) is strongly upregulated in response to the blue and ultraviolet portions of sunlight. A subset of flavonoids, the red/blue/purple anthocyanins, is upregulated and accumulates in the epidermis of leaves under a variety of conditions, depending on the plant species. Irrespective of their specific roles (suggestions include functions as a screen against intense sunlight, as powerful antioxidants, as a sink for excess carbon, as a visual cue to attract pollinators or seed distributors), anthocyanins are highly responsive to environmental conditions and are expressed most strongly under high light. In some plant species, anthocyanins accumulate in leaves during the early phase of expansion (prior to developing photosynthetic competence), in others during the flowering phase, and in many species they accumulate during the senescent phase of their lifespan prior to leaf fall. Anthocyanins also accumulate in the leaves of certain plant species during water stress, during high or low temperature stress, in response to insufficient or excessive nutrient levels (e.g., salinity), and in response to pollutants. Signaling pathways that stimulate the synthesis of defense compounds are activated by biotic stress, such as attack by herbivores, nematodes, or any of a multitude of pathogenic microorganisms. Some of the signaling molecules produced in response to biotic stress are rather volatile, and such signals generated by one plant that has been attacked can be transmitted to neighboring plants, resulting in a greater defensive response on the part of the second plant if it should be attacked. Plant Life-Cycle Adjustments and Arrested States Although the lifespan of annual plant species is relatively fixed and short, that of many other plant species is relatively flexible. Even many biennial species, which normally die at the end of the second growing season after flowering and leaving seeds, will live for years (without flowering) if they do not receive the environmental cues that signal the normal progression through the seasons. The timing of progression through the life cycle in many other species is highly flexible, depending on the conditions under which a plant grows and develops. Reproduction is typically delayed when resources are limiting, and occurs sooner in plants that grow in high-light, nutrient-rich sites. Overall development, at both the organ (e.g., leaf) and whole plant level, is generally accelerated under resource-rich conditions. The longest-lived plants are found in relatively resource-poor environments, for example, the creosote bush of the hot deserts of North and South America, and bristlecone pine found in the upper montane and subalpine regions of the western United States.

Perhaps the most extreme mechanism for dealing with stress is to enter a state of dormancy until the stress is relieved. The multitude of different adaptations exhibited within the plant kingdom include seeds/spores that can desiccate fully (a state equally effective for persisting through a prolonged drought or subfreezing winter temperatures), whole plants that can desiccate fully, plants that allow their more sensitive portions to senesce (leaves, twigs, branches, shoots, or roots), or evergreen plants that downregulate photosynthesis and remain inactive until conditions and resources permit a resumption of metabolic activity. In fact, the persistence of desiccationtolerant seeds, sometimes for decades, is the single adaptation that permits plant life to exist in the most arid habitats on Earth.

Responses to Specific Environmental Factors Low to High Solar Energy Availability: Shaded versus Sunny Environments Most plants are capable of pronounced sun or shade acclimation. In the shade, plants place an emphasis on efficient light collection via large, thin, deep green leaves with a high chlorophyll content that are thrifty with respect to everything else: low respiration rates and low maximal capacities for photosynthetic electron transport and CO2 fixation as well as other processes. At the other end of the spectrum, under full sunlight, plants increase their maximal photosynthesis and respiration rates and may lower light-harvesting efficiency. While different species differ in their shade tolerance, most plant species are able to survive and thrive in full sunlight. Even shade-tolerant plants frequently reproduce only in full sun, where the greater light energy availability results in a greater production of photosynthate (sugars and other energy-rich compounds). However, different plant species differ widely in the extent to which they are able to take advantage of the greater availability of solar energy. Evergreen species are typically slow growing and have lower maximal capacities for photosynthesis than fast-growing, short-lived (annual or biennial) species with high maximal photosynthesis rates. As discussed above, it has been well documented that photosynthetic capacity is regulated by whole plant demand for photosynthate or sink activity (utilization of photosynthate in growth and storage). The low maximal photosynthetic capacity of slow-growing evergreens is thus likely a result of a genetically fixed low sink activity, an adaptation to lessresource-rich conditions during those species’ evolutionary history. When plants grow in sunny habitats, they typically absorb much more sunlight at midday than they can

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utilize for photochemistry. Such excess absorbed sunlight, in turn, has the potential to lead to the production of reactive oxygen species (ROS) that oxidize various macromolecules. All plants therefore dissipate excess absorbed sunlight via an alternative route, photoprotective dissipation of excitation energy as harmless thermal energy (heat). In addition, plants upregulate their antioxidant pools (e.g., ascorbate, or vitamin C, and tocopherols, or vitamin E) when growing in the sun. Those plant species with a more limited maximal photosynthesis rate exhibit the strongest upregulation of the capacity for the harmless alternative dissipation of excess absorbed sunlight and other antioxidant defenses, all directed at preventing ROS accumulation. It turns out that many other environmental stresses enhance the need for photoprotection as does high light stress: irrespective of the specific nature of the stress, plant growth rate and maximal photosynthetic rate can decrease under more pronounced stress, thus resulting in more of the absorbed sunlight becoming excessive and thereby increasing the potential for increased ROS production. Under pronounced environmental stress, even moderate light intensity can represent highly excessive light. A wide variety of different environmental stresses thus have in common that they increase the potential for oxidative stress and shift the cellular redox homeostasis. Low to Favorable to Excessive Water Availability For living organisms, liquid water is essential to metabolic activity (albeit not necessary for survival of some species or developmental stages, as noted above). Thus, both acquisition and retention of water have been major driving forces in the evolution of plants in the terrestrial environment. When faced with a period of reduced water availability, plants place a greater emphasis on root growth toward the regions of higher water content (hydrotropism), increase the hydraulic conductivity of the roots, upregulate the transport of ions into the roots, and increase the synthesis of organic compounds (compatible solutes) to maintain a gradient in water concentration between the surrounding soil and the plant so that water will continue to flow down a concentration gradient from the soil into the plant. During the period when leaf pores (stomata) are closed, some species will further transport water from the moister regions of the soil through the root system and out of the root tips that extend into drier regions of the soil (along existing gradients in water content). This redistributed water can then be utilized by those roots in the drier soil regions upon stomatal opening, which leads to reversal of the water gradient so that water from all regions of the soil–root interface flow into the plant. As mentioned above, there are a number of anatomical features that exhibit some degree of acclimation in

response to low water availability. One is the development of smaller-diameter conducting elements in the xylem to reduce the likelihood of cavitation as the water in the xylem stream is placed under greater tension. Leaves may grow or move to minimize light interception at midday, so that they heat up less during the period when evaporative demand is greatest. Depending on species, a thicker layer of water-impermeable cuticular waxes may be deposited on the epidermis of leaves to further reduce water loss. In those species with the genetic disposition, a denser mat of leaf hairs may develop on the leaves to both reflect more light (decreasing the heat load and the driving force for evaporative water loss) as well as providing a windbreak against water loss. A small number of (only several dozen) vascular species as well as many lichens, mosses, liverworts, club mosses, and ferns can tolerate complete tissue desiccation and rehydration. Such extreme adjustment requires the downregulation of primary metabolic pathways as well as the upregulation of the synthesis of compatible solutes during the desiccation process. Compatible solutes serve to protect many of the vital components of the cellular matrix in the absence of hydration, particularly proteins, enzymes, and membranes (which often collapse as water leaves the cells), and can be found in all groups of living organisms. One extreme, but very effective acclimatory adjustment to water stress, involves the upregulation of a suite of genes that result in crassulacean acid metabolism (CAM). The vast majority of plant species open stomata during the day in order to carry out photosynthesis, but this results in maximal loss of water when the air is driest and the leaves are heated the most. CAM is a photosynthetic pathway found primarily in succulent plants (e.g., cacti, agaves, orchids) growing in arid habitats (e.g., deserts) or microhabitats (e.g., rock outcrops, branches of subtropical and tropical trees). In contrast to the majority of plants, CAM plants fix CO2 at night (causing the stomata to open as CO2 is consumed), storing it as an acid in the vacuole, and then release the CO2 from the stored acid during the day (causing the stomates to close) for fixation into sugars in the chloroplast. This is a very effective means to minimize water loss, since the stomata are only open during the night when the driving force for the loss of water from the plant is minimal. A very few species actually acclimate to water stress by switching from the more common daytime fixation of atmospheric CO2 to CAM. At the other end of the water availability spectrum, the majority of plant species are unable to persist under conditions where their root system is continually flooded. The primary problem faced by plants growing in an aquatic habitat is access to oxygen to support aerobic respiration in the roots’ mitochondria. Aquatic plants normally develop a specialized tissue known as aerenchyma that runs

Behavioral Ecology | Acclimation 21

throughout the interior of the plant. This tissue develops large cells that undergo programmed cell death, after which it serves as ductwork for the plant. Currents of air have actually been measured flowing through such plants, bringing oxygen to all of the living cells and carrying carbon dioxide away. In nonaquatic plants subjected to waterlogged conditions, a precursor in the synthesis of the plant hormone ethylene accumulates in the flooded portion of the plant and moves upward through the xylem until it reaches the water/air interface, at which point it is immediately converted to ethylene (oxygen is required for this final enzyme-catalyzed step). As ethylene builds up at the water/air interface, it induces cell death and a region of dead cells begins to develop leaving a passageway for air. This passageway migrates downward as oxygen reaches down further into the plant, permitting a kind of pseudoaerenchyma tissue to develop even in plants not adapted to flooding. Low to Moderate to High Temperature High temperature stress

Two primary problems arise at higher temperatures. First, membranes have the potential to become too fluid, (1) making it more difficult for the plant to maintain cellular and intracellular compartmentation between the various membrane-bound organelles and (2) increasing the likelihood that membrane-associated processes (e.g., electron transport in photosynthesis and respiration, transport of substances across membranes) will be disrupted. Plants have the ability to decrease the fluidity of their membranes by increasing the ratio of saturated to unsaturated membrane lipids (whereas animals also modulate membrane fluidity via changing cholesterol levels). Second, as temperatures increase, proteins/enzymes may become denatured and nonfunctional. While various microbes are able to synthesize different forms of an enzyme with the same function that denature at higher temperatures in response to heat stress, only few plant and animal species show this ability. Plants, like all organisms, also upregulate the synthesis of heat shock proteins that aid in the stabilization of essential cellular components and the maintenance of redox homeostasis. Moderation of high leaf temperatures can, to some extent, be achieved through increased evapotranspirational water loss through the stomata; however, this is only effective as long as the water supply from the roots through the xylem is sufficient to resupply water lost from the plant’s canopy. Constraints in water movement at any step along the pathway for water transport can lead to an imbalance resulting in stomatal closure as a compensatory measure to conserve water. Plants can exhibit some level of acclimation that alters these constraints, including regulation of the numbers and activity of aquaporins (water-transport proteins), the extent of hydrogels lining

the pores between xylem cells, alteration of the level of ions present in the xylem (which causes the hydrogels to swell or shrink), and the structural adjustments in the diameter of the tracheids and vessels mentioned above. Finally, plants (as well as some animals) exhibit flexibility in a number of morphological and structural features that provide increased reflection of solar radiation (and thus lower the heat load arising from absorption; see above). In addition, some plant species produce smaller leaves and/or more highly lobed or dissected leaves at higher temperatures, which permit more efficient convective cooling even in the absence of evapotranspirational cooling. Low temperature stress

Acclimation to lower temperatures involves increasing membrane fluidity (so that membranes do not become too solid, preventing the normal membrane-associated processes), and, for those species that experience subfreezing temperatures, the ability to permit water to leave the cells (to facilitate extracellular freezing and prevent destructive intracellular ice formation) and to then reenter the cells upon thawing. Thus, acclimation to subfreezing temperatures is not unlike acclimation to low water availability, in that the cellular contents must be able to tolerate low water content. This typically involves the accumulation of cryoprotectants (e.g., compatible solutes mentioned in the section above), organic compounds that maintain enzymes in a functional state, as well as to maintain the functional integrity of membranes that often collapse as the water leaves the cell. Overwintering plants that permit continued transport of water out of the cells are those that can tolerate the lowest temperatures; death occurs once water freezes inside the cell. For some plants that maintain photosynthetic tissues during the winter, photosynthesis is downregulated and photoprotective thermal energy dissipation is permanently engaged at very high levels, thereby minimizing ROS production, shifts in redox balance, and damage. As mentioned above, seeds and plants that are completely desiccation tolerant can also withstand subfreezing temperatures. Low to high nutrient availability

The most limiting nutrients for plants are typically nitrogen, phosphorus, potassium, and magnesium. Acclimatory changes that improve nutrient acquisition include enhanced mining for nutrients by (1) altered and increased growth of root and root hairs, (2) enhancement of colonization by symbiotic fungi (mycorrhizae) and bacteria (nitrogen-fixing bacteria or cyanobacteria), (3) upregulation of membranebound transporters and channels for enhanced nutrient uptake, and (4) increased deposition of protons into the cell wall spaces as well as into the soil to release cations bound to soil particles and to provide the driving force (electrochemical gradient) for the uptake of essential

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elements into the root (via protein channels or protoncoupled transport proteins). To optimize nutrient utilization within the plant, mobile nutrients like nitrogen and phosphorus can be reallocated from old to young leaves, while the aging/senescence of old leaves is accelerated. Furthermore, plant size is reduced and overall protein content downregulated under nutrient-limiting conditions. In the presence of excess nutrients, plants may secrete certain organic compounds into the soil to complex with the undesired element, they may reduce uptake through a decrease in specific transporters or channels, or they may sequester certain elements away from the sites of primary metabolism, for example, into vacuoles, into the cell walls, etc. Some species that grow in saline environments have secretory glands that can excrete the excess salts near the soil surface, into epidermal glands or hairs, or from the epidermis of the leaves where they may be washed away during rainfall events.

Oxidative Stress and Redox Signaling as Common Denominators in Stress Perception and Response While signaling pathways involving plant hormones have been studied for a long time, it has only recently been recognized that a common factor interacts or cross-talks with a multitude of other signaling pathways. This common and central factor is the cellular redox homeostasis (or balance between oxidants and antioxidants) that is affected by both internal and environmental events. A common response to a host of different types of adverse environmental conditions is an increased internal production of potentially destructive oxidants (ROS), resulting in oxidative stress. These ROS arise through interaction of oxygen with the electron-transport chains of both respiration in the mitochondria and photosynthesis in the chloroplast, as well as during plant defense against invaders. The downregulation of photosynthesis in response to stress mentioned above has a role in minimizing the generation of these ROS. In addition, ROS are formed by the light-absorbing, photosynthetic pigments whenever more light is absorbed than can be used through photosynthesis. On the one hand, generation of such potentially harmful products serves as a signal to upregulate certain metabolic pathways that increase the chances of survival. On the other hand, if allowed to accumulate unchecked, these ROS have the potential to (1) cause direct damage to vital biomolecules, such as components of membranes, proteins, and DNA/RNA; and (2) trigger signaling pathways that can ultimately lead to the demise of the organism via, for example, programmed cell death. Therefore, acclimation to all forms of environmental stress involves enhancement of defenses against ROS.

These defenses detoxify ROS and/or restore oxidized biomolecules. Due to the common enhancement of ROS production as a result of many kinds of environmental disturbances, all organisms possess vitally important redox-sensitive signaling pathways that inform the organism of environmental change and orchestrate adjustments, defenses, life-and-death decisions (involving the control of cell division and cell death), and other crucial decisions affecting resource allocation, reproduction, and senescence. This central role of cellular redox homeostasis in gene regulation is common to all organisms, including microbes, plants, and animals. This area is a new and fascinating field of biology, and much remains to be explored. What is clear is that there is a continuum from the ability to sensitively detect environmental change via redox sensing and signaling all the way to destruction by excess ROS. Furthermore, highly complex interactions exist between multiple signaling networks, and different cell compartments as well as different tissues and organs are in communication and redox balance. Current research is revealing interactions, or cross talk, between redox signals and previously characterized major signaling and regulatory pathways involving hormones, photoreceptors, and a range of other messengers. Finally, and as stated above, the most central aspects of life, including growth, development, reproduction, defense, and death, are controlled by these redox-modulated signaling networks as the organism’s eyes to the world in their nature as global environmental sensors. While under moderate conditions ROS production is balanced via detoxification by antioxidants and other defenses, survival under the harshest conditions depends on the ability to go to more extreme measures and actually shut down the metabolic processes that generate ROS. Some of these metabolic processes, such as respiration and photosynthesis, are vital for the support of an organism’s normal activity. Paradoxically, these essential metabolic processes are also the primary internal sources of ROS production. Both plants and animals that have the capacity to survive severe environmental conditions are capable of entering a metabolically inactive, but highly stress resistant state.

See also: Adaptation; Alpine Forest; Autotrophs; Deserts; Ecophysiology; Environmental Tolerance; Global Warming Potential and the Net Carbon Balance; Life Forms, Plants; Limiting Factors and Liebig’s Principle; Organismal Ecophysiology; Physiological Ecology; Plant Growth Models; Plant Physiology; Respiration; Salinity; Temperate Forest; Temperature Regulation; Tolerance Range; Transport over Membranes; Tree Growth; Water Availability.

Ecological Processes | Acidification

Further Reading Demmig-Adams B and Adams WW, III (2006) Photoprotection in an ecological context: The remarkable complexity of thermal energy dissipation. New Phytologist 172: 11–21. Demmig-Adams B, Adams WW, III, and Mattoo AK (eds.) (2006) Advances in Photosynthesis and Respiration, Vol. 21: Photoprotection, Photoinhibition, Gene Regulation, and Environment. Dordrecht: Springer. Feder ME (2002) Plant and animal physiological ecology, comparative physiology/biochemistry, and evolutionary physiology: Opportunities for synergy: An introduction to the symposium. Integrative and Comparative Biology 42: 409–414. Hikosaka K (2004) Interspecific difference in the photosynthesis– nitrogen relationship: Patterns, physiological causes, and ecological importance. Journal of Plant Research 117: 481–494. Huey RB, Carlson M, Crozier L, et al. (2002) Plants versus animals: Do they deal with stress in different ways? Integrative and Comparative Biology 42: 415–423. Johnson DW (2006) Progressive N limitation in forests: Review and implications for long-term responses to elevated CO2. Ecology 87: 64–75. Korner C (2006) Plant CO2 responses: An issue of definition, time and resource supply. New Phytologist 172: 393–411.

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Ledford HK and Niyogi KK (2005) Singlet oxygen and photo-oxidative stress management in plants and algae. Plant, Cell and Environment 28: 1037–1045. Mahajan S and Tuteja N (2005) Cold, salinity and drought stresses: An overview. Archives of Biochemistry and Biophysics 444: 139–158. Stitt M and Krapp A (1999) The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background. Plant, Cell and Environment 22: 583–621. Suzuki N and Mittler R (2006) Reactive oxygen species and temperature stresses: A delicate balance between signaling and destruction. Physiologia Plantarum 126: 45–51. Taulavuori K, Prasad MNV, Taulavuori E, and Laine K (2005) Metal stress consequences on frost hardiness of plants at northern high latitudes: A review and hypothesis. Environmental Pollution 135: 209–220. Van Buskirk HA and Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiologia Plantarum 126: 72–80. Walters RG (2005) Towards an understanding of photosynthetic acclimation. Journal of Experimental Botany 56: 435–447. Wilson KE, Ivanov AG, Oquist G, et al. (2006) Energy balance, organellar redox status, and acclimation to environmental stress. Canadian Journal of Botany 84: 1355–1370.

Acidification A Lu¨kewille, Norwegian Institute for Air Research (NILU), Kjeller, Norway C Alewell, University of Basel, Basel, Switzerland ª 2008 Elsevier B.V. All rights reserved.

Introduction Acidification Processes in Soil and Bedrock Acidification of Groundwater, Freshwaters, and Oceans

Consequences of Acidification Further Reading

Introduction

NH3 emissions mainly from agricultural activity (volatilization from fertilizers and animal liquid manure) trigger acidification processes in soils. After deposition to ecosystems the conversion of NHþ 4 to either amino acids or to in soils is connected to the production of acidifying NO 3 þ H ions. Since the end of the nineteenth century, industrialized regions of the world have been confronted with the consequences of acidic atmospheric deposition, ‘acid rain’. There was, and still is, substantial concern about the environmental impacts of air pollution at the local, regional, and global scale. ‘Acid rain’ has threatened vegetation, wildlife, soil biology, and human health, caused damage to materials, and changed the chemistry of soils and waters. Anthropogenic land-use changes and use of fossil fuels have further led to dramatically increasing atmospheric CO2 concentrations worldwide. CO2 is absorbed by oceans

Acidification processes in soils, freshwaters, and oceans are natural processes in geological time frames. However, anthropogenic activities on planet Earth have considerably accelerated acidification by enhancing natural processes as well as by changing dynamics, balances, and pathways. Acidifying substances can have ecosystem external natural sources such as volcanism, dimethyl sulfide (C2H6S) emissions from oceans, or, to a minor extent, sulfide emissions from freshwater wetlands. However, most important are anthropogenic emission sources, mainly fossil fuel combustion processes (e.g., public power plants, industry, and traffic) and agriculture. Emissions of SO2 and NOx to the atmosphere increase the natural acidity of rainwater due to the formation of H2SO4 and HNO3, both being strong acids. Furthermore,