3. Resource allocation and growth
4. Responses to environmental conditions
5. Ecophysiology, distributions, and global climate change
Plant physiological ecology addresses the physiological interactions of plants with the abiotic and biotic environment and the consequences for plant growth, distributions, and responses to changing conditions. Plants have three unique features that influence their physiological ecology: they are autotrophs (obtaining energy from the sun), they are sessile and unable to move, and they are modular, exhibiting indeterminate growth. Plant growth depends on acquisition of four critical resources: light, CO2, mineral nutrients, and water. Light together with nitrogen-rich enzymes in the leaf drive photosynthetic assimilation of CO2 into carbohydrates. Uptake of nitrogen and phosphorus, the elements most often limiting growth, is facilitated by symbiotic associations on plant roots with bacteria and fungi, respectively. Most water acquired by plants is lost in transpiration in exchange for CO2 uptake through stomata. Water moves through a plant by cohesion-tension, drawn upward as a result of evaporation from leaves. Excessive tension can lead to embolism, in which air bubbles enter the water column and block water transport. Within the plant, allocation of resources to alternative functions creates important trade-offs that critically influence plant responses and performance in contrasting environments. Physiological ecology plays a critical role in understanding the distributions of individual species and of major biomes at a global scale and is vital to understand the potential impacts of global climate change on vegetation and biodiversity.
acquisition. The processes of acquiring resources from the environment, such as photosynthesis in leaves and nutrient uptake by roots.
allocation. The partitioning of resources among alternative structures or functions within a plant. The principle of allocation states that resources used for one purpose will be unavailable for other purposes, creating trade-offs that strongly influence plant growth and life cycles.
conditions. Factors of the environment that influence an organism but cannot be consumed or competed for (e.g., temperature, pH).
embolism (or cavitation). The blockage of water transport by air bubbles in the xylem (water-transporting cells), causing reduced water transport and, potentially, plant death.
leaf energy balance. The balance of energy inputs and outputs that influence leaf temperature. Solar radiation is the most important input, and transpirational cooling and convective heat loss are the most important outputs.
photosynthetic pathway. Plants exhibit three alternative photosynthetic pathways (C3, C4, and CAM) that differ in underlying biochemical and physiological mechanisms, resulting in contrasting performance depending on temperature and the availability of light, water, and nutrients.
resources. Aspects of the environment that are consumed during growth and that plants compete for. The most important are light, water, nutrients, and space.
water and nutrient use efficiency. The efficiency of photosynthesis relative to investment of water or nutrients, respectively.
Physiological ecology examines how plants acquire and utilize resources, tolerate and adapt to abiotic conditions, and respond to changes in their environment. The study of physiological ecology considers plant physiology in relation to the physics and chemistry of the abiotic world on one hand, and a broad ecological and evolutionary context on the other. Plant physiological ecology provides the basic sciences with essential information about plant evolution, biodiversity, ecosystem productivity, and carbon and nutrient cycling. It also plays an instrumental role in a wide range of applied sciences, including agriculture, forestry, management of invasive species, restoration ecology, and global change biology.
In its early years, plant ecophysiology addressed two broad themes. One was the effort beginning in the mid-nineteenth century to understand the global distribution of major biomes and vegetation types, led by pioneering plant geographers such as A. von Humboldt, A.F.W. Schimper, and their followers. These workers recognized that similar vegetation types arise under similar climates in different parts of the world, and they developed basic principles of plant form and function that could explain these global patterns. This led to a subsequent emphasis, in the early twentieth century, on the question of how plants survive in extreme environments. Principles of physiology and biophysics were applied in natural settings to understand how plants can tolerate and even thrive from the heat of the desert to the extreme cold of the high arctic and the upper limits of vegetation on high mountains. Both of these traditions combined the mechanistic view of the physiologist with the idea of evolutionary adaptation to understand why species with different physiological characteristics dominate under contrasting environmental conditions.
In the United States, plant physiological ecology played a key role in the development of ecology as a discipline. The Plant World, published until 1919, was the forerunner of Ecology, the flagship journal of the Ecological Society of America. Ecology in the early twentieth century emphasized physiological, functional, and ecosystem ecology. Population and community ecology as we now know them had not yet emerged.
Plants share three important features that have profound consequences for their ecology and evolution, including physiological ecology. (1) Plants are autotrophs, converting sunlight to stored chemical energy that is the basis for terrestrial food webs and ecosystems. (Nonphotosynthetic and parasitic plants are an exception to this rule.) Photosynthesis is one of the outstanding products of evolution and is still more efficient than any photovoltaic mechanism for the capture and conversion of solar energy. (2) Plants are sessile—once a seed germinates and the seedling is established in the soil, plants cannot move. They cannot hide or escape from abiotic conditions or biotic enemies, and they cannot seek out mates, at least directly, for reproduction. Plants exhibit an enormous diversity of seed germination mechanisms that control the time and place of germination, thus shaping the environment the seedling and adult plant subsequently occupy. (3) Plants exhibit modular, indeterminate growth. They grow by cell division in regions known as meristems, located at the tips of growing branches, in axils at the base of leaves, beneath the bark of trees, and at the tips of roots. Meristematic cells are undifferentiated throughout the life of a plant, and most plants never reach a fixed, mature size. The combination of indeterminate growth and immobility means that growth and development are important mechanisms through which plants respond to the environment, and in this way growth in plants plays an analogous role to behavior in animals.
At the core of physiological ecology is the study of how organisms respond to and are affected by the abiotic environment. In the case of plants, it is useful to divide the environment into conditions and resources. Conditions are factors that cannot be consumed or depleted by organisms, such as temperature, pH, or salinity. Resources are substances (or sources of energy) that are captured or consumed, can be depleted, and can be the focus of competitive interactions among individuals. The following sections address the acquisition and allocation of resources and the mechanisms by which plants respond to and tolerate a wide range of environmental conditions.
All plants require the same basic resources for growth and reproduction: carbon, light, mineral nutrients, and water. The essential challenge for terrestrial plants is that these resources are located in different places (above versus below ground) and have very different modes and rates of supply in the environment.
Carbon, in the form of atmospheric carbon dioxide, is available at a relatively constant concentration. CO2 enters leaves through microscopic pores known as stomata. Stomata are formed by pairs of cells, known as guard cells, which are joined at either end, like two elongated balloons. When fluids move into the cells, they swell and bend, opening a small pore that allows gases to diffuse in and out of the leaf. The regulation of pressure within these cells is an intricate process influenced by chemical signals from the leaves and roots that depend on soil moisture availability and internal water status of the plant.
When stomata open, CO2 diffuses from the atmosphere into the pores, where it crosses an air–liquid interface and dissolves in the interior fluids of the leaf as carbonic acid. At the same time, however, water evaporates from inside the leaves and diffuses through the stomata into the surrounding atmosphere. This exchange of water for CO2 is one of the most fundamental trade-offs governing photosynthesis and plant growth. The concentration gradient driving the diffusion of water out is much steeper than the gradient for CO2 coming in. As a consequence, plants lose 100 to 500 molecules of water for each molecule of CO2 they absorb. Most of the water taken up by plants (see below) is used for this purpose. The ratio of water loss to CO2 uptake is known as water use efficiency and represents a critical physiological trait that influences plant growth and distribution in contrasting climates.
Photosynthesis is a biochemical reaction that uses energy from sunlight to combine CO2 and water to make carbohydrates (glucose, starch, and other sugars), releasing oxygen in the process. Photosynthesis involves two coupled processes, known as the light reactions and carbon reactions. The light reactions use solar energy to reduce NADP+ to NADPH and phosphorylate ATP. These provide energy for the carbon reactions of the Calvin cycle. The most important of these reactions is the fixation of a CO2 molecule to a five-carbon carbohydrate chain, followed by a rapid split into two three-carbon molecules, which gives this process the name C3 photosynthesis. The CO2 fixation step is regulated by the enzyme RUBISCO, which, because of its relatively low efficiency, is present in very high levels in the leaf. RUBISCO represents up to 50% of all proteins in a leaf and is thought to be the most abundant protein on the planet.
The C3 pathway is dominant in plants of temperate and cool climates as well as in most trees. In deserts, grasslands, and other dry environments, two alternative photosynthetic pathways are found, each of which has evolved many times independently. C4 photosynthesis, common in grasses (including crops such as corn), utilizes the enzyme PEP-carboxylase instead of RUBISCO for the initial fixation of CO2. This is a more efficient alternative, which can operate at lower internal CO2 concentrations, so the plant can have fewer, smaller, or less open stomata and therefore lose less water. The first fixation step creates four-carbon compounds (hence the name), which are then shuttled to cells deeper inside the leaf where they are broken down, releasing the CO2 for incorporation into the Calvin cycle. The extra steps of the C4 pathway require additional energy, so C4 plants occur primarily in warm and high-light environments.
The third pathway is known as CAM photosynthesis (Crassulacean acid metabolism), named for the plant family Crassulaceae where it was first discovered. CAM photosynthesis is widespread in cactus, tropical euphorbias, yuccas, and other succulents. CAM also utilizes PEP-carboxylase for the initial fixation step, but the stomata are opened only at night, allowing CO2 to diffuse into the leaf with minimal water loss because of lower temperatures and higher relative humidity. The carbon is stored in carbon acids (hence the name) until daylight, when they are broken down and passed to the Calvin cycle. Almost all plants described as “succulents” have CAM photosynthesis, and the swollen and fleshy leaves or stems contain the expanded cells that are used to store the four-carbon compounds through the night. The nighttime uptake of carbon results in greatly enhanced water use efficiency because CAM plants lose only as few as 10 water molecules per CO2 molecule acquired. However, overall photosynthetic rates are very low, limiting growth rates.
Photosynthesis in sun versus shade also presents trade-offs that are important for plants growing in heterogeneous light environments such as the forest understory. Plants with C3 photosynthesis exhibit a characteristic light response of photosynthesis. In complete darkness, photosynthesis is shut down, and leaves have a net loss of CO2 as a result of background respiratory processes. With slight increases in light, photosynthetic rates increase until the light compensation point is reached, when photosynthesis balances respiration and there is no net loss or gain of CO2 by the leaf. Net photosynthetic rates become positive above this light level and increase rapidly until they reach a point where the concentration and activity levels of RUBISCO and other enzymes become more limiting than the availability of light energy. At this point, photosynthetic rates reach a plateau known as the light-saturated photosynthetic rate.
In shade, photosynthesis is primarily limited by light energy rather than enzyme levels. As a result, shade leaves have lower nitrogen concentrations per unit leaf area, a lower saturated photosynthetic rate, and lower background respiration. The result is that the light compensation point is lower, and shade plants can maintain zero or positive carbon balance at lower light levels. The differences between sun and shade leaves are generally observed both within and between species.
Competition for light is largely asymmetric or onesided: the highest leaves in the canopy capture the most light, and leaves lower down, on the same or other plants, receive much less. It has been argued that the evolution of plant height can be understood as an evolutionary game: if all the plants in a community “agreed” to reduce their height equally, they would all still receive the same amount of light. However, the community would be easily invaded by a taller “cheater” that received a disproportionate share of this critical resource. Taller strategies will continue to invade until the costs of additional height (in structural support, movement of water, etc.) outweigh the benefits, and an equilibrium is reached. This equilibrium will vary, depending on the availability of light, water, and nutrients and is thought to explain variation in the height of forests and other vegetation around the world.
Water is central to the life of a plant. In addition to the water lost in exchange for carbon uptake (see above), water is needed for tissue hydration, nutrient uptake, long-distance signaling, and as a source of pressure for structural support and cell expansion.
Water transport begins in the soil, where root hairs provide a large surface area for water uptake. Water moves through and around cells until it reaches the endodermis, a root layer in which the cell walls are impermeable to water because of a waxy inclusion in the cell membrane known as the Casparian strip. To move beyond the Casparian strip, water must pass through living cells. This allows the plant to regulate how much water enters the active root tissue and can be used to generate root pressure. The main water transport tissue inside roots, trunk, branches, and leaves is the xylem, composed of hollow cells that are dead at maturity. Water travels through the xylem to the leaves and evaporates from air/water interfaces within the stomata; evaporation from the leaves is known as transpiration. Movement along this path occurs as water moves from areas of high water concentration (high water potential) to areas of lower water concentration (lower water potential). Under all but the most humid conditions, the concentration of water (water potential) is much lower in the atmosphere than it is within the plant. The difference in concentration drives evaporation into the atmosphere.
Within the xylem, water is connected by cohesion to form a single column between leaf and root. As a result, evaporation at the leaves’ surface effectively pulls water out of the soil. Cohesion, which is the result of hydrogen bonding between water molecules, gives the water column the ability to withstand stretching, also known as tension or negative pressure. This scenario, first proposed in 1893, is known as the tension–cohesion theory. The underlying mechanisms have been questioned from time to time, but in general, it is considered to be well supported by empirical evidence.
Like a supersaturated or supercooled solution, water under tension is in a metastable state. As a result, it is vulnerable to disruption and can vacuum boil, spontaneously forming an air bubble or embolism. This process is known as cavitation. Because embolisms break the water column, they block the transport of water from root to leaf. MRI studies show that cavitation is constantly occurring, and being repaired, during transpiration. Stresses, such as drought and freezing, can cause more damaging levels of embolism. Xylem architecture is highly redundant, and plants can survive, and sometimes repair, many of these losses. However, if a sufficient proportion of the xylem is blocked, embolism can cause the death of distal branches and leaves. When a plant dies in a drought, embolism is likely the proximal cause of death.
Mineral nutrients, like water, are primarily acquired below ground. Roots are the essential foraging organs for below-ground resources. Many roots also sustain colonies of mycorrhizal fungi, which are important for the uptake of nutrients. The two soil nutrients that are most often limiting to plant growth are nitrogen, in the form of nitrate or ammonium, and phosphorus, usually taken up as phosphate. Other macronutrients required in relatively large quantities are potassium, calcium, magnesium, and sulfur; micronutrients, required in much smaller quantities, include chlorine, iron, manganese, boron, zinc, copper, nickel, and molybdenum and (in some plants) sodium, cobalt, and silicon.
Nitrogen is one of the most abundant elements in the biosphere but one that is often available in limited supplies. The primary source of nitrogen is dinitrogen gas from the atmosphere; however, plants are unable to assimilate this nitrogen directly. Instead, atmospheric nitrogen is assimilated by nitrogen-fixing bacteria; many of these bacteria enter into symbiotic relationships with plants and occupy nodules on plant roots. N-fixing symbioses are widespread among thousands of species in the legume family (Fabaceae) as well as at least nine other related groups. Once nitrogen has entered an ecosystem, decomposition of litter and mineralization of organic nitrogen by soil microbes makes nitrogen available for uptake by plants. Photosynthetic nitrogen use efficiency (PNUE) is the ratio of photo-synthetic productivity to the concentration of nitrogen within the leaves (or the whole plant). On a short-term basis, PNUE is higher in faster-growing plants with short leaf lifespan, high tissue nitrogen concentrations, and high photosynthetic rates. However, over the lifespan of the leaf, PNUE tends to be higher in slower-growing plants with lower instantaneous rates of photosynthesis but long-lived leaves.
Phosphorus is primarily derived from weathering and soil formation and then is cycled within an ecosystem in parallel with nitrogen. Phosphorus is relatively immobile and diffuses very slowly in soil water. Symbiotic relationships between plants and mycorrhizal fungi play a critical role in phosphorus uptake, as the hyphae of the mycorrhizas greatly extend the foraging area of the root system. As in the N-fixing symbioses, plants provide carbohydrate as an energy source for the fungi. Plants may also leach organic acids into soil, and the reduction in soil pH increases the availability of phosphorus as cations are exchanged on clay particles and other surfaces. Recent studies have shown that 10% to 30% of net carbon gained by a plant may be lost into the soil either as leachates or carbohydrate supplied to symbiotic fungi or microorganisms.
Resource acquisition is only a part of the story. To understand how plants grow, respond to the environment, and differ from each other, we must examine the allocation of resources. Allocation refers to the partitioning of acquired resources among different structures and functions within the plant. The principle of allocation underlies many of the fundamental trade-offs involved in plant growth: energy or materials can be allocated to only one structure or function at a time, so investment in one process will invariably entail trade-offs in others. Carbohydrates synthesized in the leaf by photosynthesis are loaded into the phloem and can be transferred to other parts of the canopy, to the branches and trunk, to flowers and fruits, and down into the roots. Nutrients, taken up in the roots, move upward in the xylem sap and are also divided among different parts of the canopy and utilized in the production of new leaves, stems, and roots; the provisioning of seeds; and the synthesis of enzymes and proteins throughout the plant.
Construction and maintenance of plant tissues require a significant amount of energy as well. For each gram of biomass used to construct new leaf tissue, approximately 0.5 g of carbohydrate will be required to provide the energy for biosynthesis. Biochemical reactions and maintenance of enzyme pools also require a continual input of energy. Leaves in particular, where the photosynthetic machinery are at work, will burn off 5–10% of their photosynthetic uptake as maintenance respiration.
Patterns of allocation are critically important for plant growth. In particular, allocation to leaves creates a positive feedback, as leaves can then capture more carbon, which can be used for additional growth, etc. Investment in leaves is like investment in a savings account, with the benefits of compound interest over time. For example, wild radish plants invest approximately twice as much of their carbon gain in new leaves, compared to the domestic radish, which has been selected for high allocation to the tuber. Although the leaves of the two types have identical photosynthetic rates, the wild type grows to three times larger than its domestic relative over the course of a season. On the other hand, there must be limits to the benefits of investing in leaves. A plant with too few roots would have lower growth rates as a result of insufficient water or nutrients or might simply fall over if it were not well rooted in the soil. A plant with too little above-ground structures (stems and petioles) would have a canopy packed with leaves, all shading each other, with very inefficient light capture. The principle of optimal allocation captures these trade-offs, as it is clear that there is an intermediate optimum in the allocation of resources to leaves at which the growth rate of the plant is maximized. In practice, it can be difficult to determine whether a plant is actually at its optimum, but the idea plays a central role as a guiding principle of ecology.
Over the entire life cycle, natural selection favors those genotypes that maximize their fitness, usually thought of in terms of lifetime reproductive output (see chapter I.14). In short-lived plants such as annuals, allocation must shift rapidly from vegetative growth to the production of flowers and the maturation of seeds and fruits. At the end of the life cycle, 50% or more of the biomass in many annual plants is allocated to reproductive structures. In longer-lived plants, a key component of lifetime fitness is survival through periods of adversity, including cold and drought, or recovery from disturbance or herbivory. Regrowth after disturbance relies on the mobilization of reserve energy in the form of nonstructural carbohydrates that can be stored in stems and roots. For example, shrubs of Mediterranean-type climate regions that are adapted to regrowth after fire have increased allocation to these energy reserves, with ensuing trade-offs in growth rate and annual reproduction.
Because they are sessile and exothermic, plants must tolerate a wide range of conditions. They cannot seek shelter or migrate to a more hospitable habitat except through reproduction. As a result, almost anything that moves a plant away from its optimal conditions may be considered “stressful,” including extremes of light levels (too much or too little), temperature (both hot and cold), water supply (drought or flooding), and soil composition. However, it is important to remember that what is “stressful” depends on what conditions the genotype has adapted to. For instance, salty conditions that would kill most crop or house plants may be those under which a salt-marsh or mangrove plant grows best and reproduces most efficiently. Nonetheless, it appears that plants that tolerate generally stressful habitats (the very cold, hot, dry, wet, salty, toxic, or nutrient-poor) do so through conservative, slow-growth strategies.
The study of leaf energy balance demonstrates the insights gained by combining ecophysiology with first principles of biophysics. The temperature of a leaf, like that of any other object, will reach an equilibrium when energy inputs and outputs are balanced. The primary input for plants is solar radiation, although the amount of radiation absorbed by a leaf may be reduced by reflective coverings such as hairs or a steeply angled leaf surface. The most important energy output is the heat loss that accompanies the evaporation of water lost in transpiration. As the temperature of a leaf increases, heat loss also goes up as a result of the steeper temperature gradient between the leaf and its surroundings, and this will eventually bring a leaf to equilibrium. Depending on radiation, wind, humidity, and other conditions, leaf temperatures may range from 5°C below to 15°C, or more, above ambient air temperatures. The size of a leaf has an important effect on leaf energy balance, as smaller leaves interrupt air circulation less, and are thus more closely coupled to air temperatures and less prone to overheat.
Both low- and high-temperature stresses are important determinants of photosynthesis, growth and distribution, and, by extension, of vegetation type and community composition. There is no one optimal temperature range for all plants; instead, optimal temperature ranges vary. In addition, the lowest or highest temperatures that a plant can tolerate can frequently be expanded by prior exposure to sublethal cold or hot temperatures, a process known as acclimation. Adaptations to heat stress include decreases in leaf size, increases in leaf reflectance, the production of molecular chaperones that stabilize proteins and membranes, and a shift toward saturated lipids in cell membranes. Adaptations to cold stress include narrow vessel diameters, the production of molecular chaperones that stabilize proteins and membranes, and a shift toward unsaturated lipids in cell membranes.
Drought stress occurs when the water potential of the soil drops below that of the plant and the atmosphere, and the plant cannot isolate itself from the soil or draw enough water to facilitate carbon gain. Flooding stress occurs when roots are deprived of oxygen and can no longer perform necessary functions such as water and nutrient uptake. The range of drought or flooding that can be tolerated varies widely across both clades and habitats. The composition of soil can also have important effects on the uptake of water and nutrients. Soil pH, salt concentration, and heavy metal concentration can all limit the uptake of water and nutrients and inhibit root growth. Some plants are adapted specifically to these stresses and thrive in alkaline, salty, or contaminated soils. Phytoremediation, the effort to remove soil contaminants through specially adapted vegetation, relies on such plants.
The science of ecology is often defined as the study of distribution and abundance of organisms. Ecophysiology clearly plays a central role in these broad questions, particularly in explaining distributional limits of species along environmental gradients. Species distributions often reflect intrinsic tolerance limits related to physiological traits. One particularly well-studied case is the distribution of the saguaro cactus in the southwestern United States, where the northern limits of the geographic range closely parallel the −7°C winter isotherm. More generally, the traits of species tend to change as one moves across environmental gradients because distribution patterns reflect the adaptations of plants to contrasting environments. A well-studied example is the relationship between the resistance to xylem embolism and water deficit and distributions, where less-resistant species either live closer to water sources or have deeper roots to maintain access to water through dry periods. However, species may employ very different mechanisms to survive in any particular environment, so there is no simple one-to-one relationship between any particular physiological trait and the environmental conditions where species live.
Understanding the physiological basis of species distributions is more important than ever in relation to global climate change. Paleoecological data demonstrate that plant distributions can track changing climate over centuries and millennia. Since the last glacial maximum, 10–20 thousand years ago, tree species in eastern North America and Europe have expanded their northern range limits by 1000 km or more. Rising CO2 levels from burning of fossil fuels, deforestation, and other factors are expected to cause sharp increases in temperature in the next century, coupled with spatially and temporally variable shifts in precipitation. These changes are occurring much more rapidly than postglacial climate changes, raising significant concerns about whether plants and animals will be able to track favorable climates. Mechanistic models that incorporate physiological tolerances, as well as biotic interactions and dispersal capacity, are critical to improve these forecasts, especially for invasive species that may not occupy the full extent of their potential range in many parts of the world.
Physiological information has also been used to model the distribution of the world’s major biomes. Vegetation modeling uses the idea of plant functional types, an idealized representation of a small number of physiological strategies. Carbon gain and growth of these life forms are simulated under mean climate characteristics of large grid cells that span the globe; the mix of types that prevail is then used to infer typical vegetation types, such as temperate deciduous forest, evergreen tropical forest, etc. These models have been calibrated with great success and are able to predict the broad patterns of global vegetation.
Within a region, vegetation type can be a critical determinant of energy, water, and nutrient cycles. Recent work suggests that understanding these cycles at an organismal level may be critical to understanding fluxes and cycles at the scale of landscapes, regions, or ecosystems. For instance, grasslands process, consume, and convert resources in different ways, and at different rates, than forests. This occurs, in part, because of the many physiological differences between grasses and trees. Combining information about the physiology and behavior of plants with an understanding of ecosystem-scale patterns and processes provides essential data for models of global climate, biogeochemistry, and atmospheric circulation. Interaction with these disciplines is essential to scaling up to landscape, biome, and global levels.
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