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Plant and Animal Physiological Ecology, Comparative Physiology/Biochemistry, and Evolutionary Physiology: Opportunities for Synergy: An Introduction to the Symposium1
1 Department of Organismal Biology & Anatomy, The Committee on Evolutionary Biology, and The College, The University of Chicago, 1027 East 57th Street, Chicago, Illinois 60637
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Both plant biologists and animal biologists seek to understand how their focal organisms have evolved to interact with the environment. Despite this similarity in goals, the differing biology of plants and animals as well as other factors have led these scientific communities to diverge. Scientific discoveries that have occurred in each community in relative isolation may advance progress in the other community and set the stage for broad scientific syntheses. The accompanying papers, summarized herein, exemplify such discoveries, and collectively argue that the plant and animal ecophysiological communities have much to gain from improved cooperation and communication.
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Adaptation to the environment is a major theme in modern biology, and both plant and animal biologists have formed scientific communities around this theme. Both communities have interests in the mechanisms that enable their focal organisms to persist in natural environments, how these mechanisms enable persistence (i.e., affect fitness) in the wild, and how evolution originated and maintains these mechanisms. Both communities study multiple levels of biological organization, from the molecule to the ecosystem, and both examine genotype and phenotype. Both communities might identify themselves as physiological ecologists, ecological physiologists, evolutionary physiologists, or environmental physiologists. Despite this similarity in outlook, scope, and objective, however, these plant biologist and animal biologist communities are often separate. At the level of scientific societies in the USA, the relevant animal biologists might join the Section of Comparative Physiology and Biochemistry of the Society for Integrative and Comparative Biology or the American Physiological Society, whereas the corresponding plant biologists might join the Physiological Ecology Section of the Ecological Society of America or the American Society for Plant Physiology. The two communities might also publish in different journals, attend different conferences, and otherwise distance themselves intellectually from one another. If this separation signals only the differing orientation of the two communities, it is an unfortunate but necessary consequence of the prevailing pressures towards specialization in the modern life sciences. By contrast, if this separation deprives each community of ideas, approaches, techniques, and relevant findings generated by the other, it then impedes scientific progress. The major purpose of the papers assembled here is to argue that this separation deprives each community of important benefits that could derive from better communication if not integration.
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Clearly, the commitment of individuals or entire fields exclusively to botanical and zoological models is not obligatory. Darwin himself worked on both plant and animal material, and the rediscovery of Mendel's work on plants rapidly pervaded both plant and animal communities. Both plant and animal biologists contributed to the founding and development of ecology, and both (e.g., Ledyard Stebbins, Theodosius Dobzhansky, George Simpson, Ernst Mayr) helped consolidate the New Evolutionary Synthesis. A few exceptional individuals (e.g., Per Scholander [Scholander, 1978
]) made seminal contributions to both plant and animal ecophysiology, and others (e.g., Nevo [1995]) have similar goals in terms of evolutionary biology. One mechanistic/evolutionary discipline, comparative biomechanics, seems to investigate plant and animal materials with equal enthusiasm, and another, plant-animal interactions (Schultz, 2002), depends on it.
But the mainstreams of the fields did diverge, and often for sound reasons. First, the modal plant differs from the modal animal. (As is immediately obvious, few attributes are unique to plants or animals: movement and behavior, sessile habits, photosynthesis, and tree-like morphology, for example, characterize some plants and some animals. Both kingdoms exhibit effective mechanisms for long-range dispersal in space and time [see below].) One especially consequential difference is in capacity for behavior; the modal animal can better escape from harmful or lethal environments than the modal plant (Huey, 2002). In terms of mechanism, this difference leads to research emphasizing motility, control of motility, and metabolic support of activity in animals; and on resistance to stress or phenotypic plasticity in plants. In terms of population biology and evolution, Bradshaw (1970) suggests some typical differences: (a) plants are subject to stronger selection pressures than animals; (b) selection is more constant in direction in plants than in animals; (c) plant species comprise populations of smaller geographic size than those of animal species, and thus intraspecific variation in environmental regime will be greater in plant species than in animal species; (d) consequently, plant populations vary more in the direction of selection than animal species; (e) less gene flow among plant populations than among animal populations; (f) greater resemblance between the habitats of parents and offspring in plants; (g) less replacement of parents by offspring because of perenniation in plants; and (h) in response to environmental change, the entire breeding system may change more rapidly in plants than in animals. Huey (2002) explores these predictions in detail. Thus, as the focal or model organisms typically differ in substantial ways, the communities that study them may lack common foci.
A second reason for separate communities of plant and animal biologists is that the differing characteristics of typical subjects give rise to differing experimental technologies, laboratory husbandry procedures, and other logistical issues. As Huey (2002) observes, while the two communities might each focus on phenotypic plasticity, plant investigators routinely do so in terms of soil, light, and CO2 while animal investigators routinely work on temperature and oxygen. Comparing the outcomes of this work becomes difficult. Thus, at a scientific meeting, a plant biologist may find sharing "the tools of the trade" with an animal biologist to be counterproductive (and vice versa).
A third reason for the separation may be that the animal community has undergone strong societal pressures to discover the basis and cure of human disease, and the plant community has not. Often these pressures have taken the form of massive funding from the U.S. National Institutes of Health and non-governmental biomedical organizations, which has led both individual scientists and academic administrators to eschew more broadly biological research in favor of biomedical relevance. One negative consequence in the USA was a decline in botany departments and marginalization of plant sciences (which must have encouraged resentment of animal scientists). One positive consequence may have been that the plant biologist community, less needing to relate its science to human disease, was freer to focus on diverse study systems and biological problems than the animal biologist community. Only recently has the plant biologist community converged upon a model organism (Arabidopsis) similar to those upon which the animal biologist/biomedical communities have converged (Drosophila, mice and rats, yeast, E. coli, and recently C. elegans and zebrafish, among others). Another difference is that the exploitation of model organisms in the animal biologist/biomedical communities created a schism within this community (for an autobiographical account, see Wilson [1994]). On one side were biomedically-oriented scientists, often using model systems, often working at the molecular and cellular levels with experimental genetics as a principal tool, and often eschewing biological diversity in hopes of discovering the principles underlying the common features of living things. On the other side were "comparative" or non-biomedical scientists, often working at the organ, organismal or population level, and often eschewing model systems to discover the principles underlying biological diversity. The plant biology community escaped much of the suffering due to this schism. Although the schism has healed or is currently healing in the animal biologist community in the post-genomic era, it may be opening in the plant biologist community with the ever-increasing emphasis of Arabidopsis and the proliferation of agricultural plant genomes.
Whatever the causes of separation, the communities, once separate, developed along independent pathways and diverged. Each community fostered distinctive (but largely distinct) scientific accomplishments. Some recent book titles in plant physiological ecology (see http://www.botany.duke.edu/jackson/ecophys/books/index.html) exemplify major themes in that community, including global climate change, atmospheric levels of carbon dioxide and trace gases, scaling from the individual plant to entire communities and ecosystems if not to the entire biosphere, abiotic stress in general and that of particular environments, and variation in metabolic pathways (C3 and C4): Plants in Changing Environments: Linking Physiological, Population, and Community Ecology (Bazzaz, 1996); Plant Resource Allocation (Bazzaz and Grace, 1997); Arctic Ecosystems in a Changing Climate: An Ecophysiological Perspective (Chapin, 1992); Scaling Physiological Processes: Leaf to Globe (Ehleringer and Field, 1993); Stable Isotopes and Plant Carbon-Water Relations (Ehleringer et al., 1993); Carbon Dioxide and Terrestrial Ecosystems (Koch and Mooney, 1996); Carbon Dioxide, Populations, and Communities (Körner and Bazzaz, 1996); Water Relations of Plants and Soils (Kramer and Boyer, 1995); Carbon Dioxide and Environmental Stress (Luo and Mooney, 1999); Terrestrial Global Productivity (Mooney and Saugier, 2000); Response of Plants to Multiple Stresses (Mooney, 1991); Physiology of Plants Under Stress: Abiotic Factors (Nilsen and Orcutt, 1996); Physicochemical and Environmental Plant Physiology (Nobel, 1999); Physiology of Plants Under Stress: Soil and Biotic Factors (Orcutt and Nilsen, 2000); Landscape Function and Disturbance in Arctic Tundra (Reynolds and Tenhunen, 1996); C4 Plant Biology (Sage and Monson, 1999); Trace Gas Emissions by Plants (Sharkey et al., 1991); and Invasive Species in a Changing World (Mooney and Hobbs, 2000). Interestingly, "evolution," "adaptation," and "molecular" are entirely absent from these titles, but are common in the counterpart animal literature (Feder et al., 2000). Although both communities have interests in stress (e.g., from authors working primarily with animals, see Extreme Environmental Change and Evolution [Hoffmann and Parsons, 1997] and Environmental Stress, Adaptation, and Evolution [Bijlsma and Loeschcke, 1997]), the remainder of the plant themes (including "ecology" itself) are typically rare in the counterpart animal literature. As the accompanying papers and many individual research programs demonstrate, these differences neither are obligatory nor reflect disinterest of each community in the other's themes. Rather, just as diverging populations may by chance accumulate very different characteristics once they have speciated, the two communities happen to have developed in different directions.
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The themes not developed in each community represent obvious opportunities for growth, but have done so for some time. The confluence of several events now makes the potential for cross-fertilization more evident. One is that general molecular biological techniques and genomics are increasingly permeating every discipline and scientific community. At the laboratory bench, plant and animal biologists are increasingly doing the same thing; in the scientific literature as well, questions and paradigms are increasingly converging as a result. Another event is the realization that cross-taxon communities and programs may have real advantages, economies of scale, and greater scientific strength through diversity. This realization has led to corresponding reorganizations and redefinition of missions. For example, when the National Science Foundation reorganized its programs in the 1990s, first as "Functional and Physiological Ecology" and then as "Ecological and Evolutionary Physiology," it combined both plant and animal biology in this program, departing from its previous practice of separating the two. Also in the 1990s, the American Society of Zoologists became the Society for Integrative and Comparative Biology. A final event making this symposium timely is that the increasing dominance of Arabidopsis as a model system in the plant physiology community is leading non-Arabidopsis plant physiologists to realize that they may have much in common intellectually with non-model organism animal physiologists.
This confluence (and acquaintances formed when plant and animal biologists began to serve on a common National Science Foundation panel) led representatives of both the plant and animal communities to ponder whether closer ties at the level of scientific societies would be beneficial. This process culminated in two events. First, officers and representatives of the largely-zoological Society for Integrative and Comparative Biology and the largely-botanical Physiological Ecology Section of the Ecological Society of America organizing a workshop, entitled "Towards Potential Synergies of Plant and Animal Ecophysiology," at the Ecological Society's annual meeting in August 2000. Second, these same two groups co-sponsored the symposium whose record is published here, entitled "Plant and animal physiological ecology, comparative physiology/biochemistry, and evolutionary physiology: opportunities for synergy" at the annual meeting of the Society for Integrative and Comparative Biology in January 2001. A grant from the Ecological and Evolutionary Physiology Program of the National Science Foundation supported both events.
The intent of the present symposium was two-fold. First, it was an experiment in social engineering. Just as the formation of a joint plant-animal Program at NSF led to interactions among plant and animal panelists that would not otherwise have occurred, this symposium was intended as a substrate for unprecedented interactions among plant and animal biologist symposiasts, members of the audience, and attendees of the SICB meeting. The outcome of this experiment is presently unknown. A second intent was, through the symposium presentations and the corresponding manuscripts published here, to exemplify common interests, paradigms, approaches, findings, principles, and opportunities for future scientific synergy between plant and animal scientists investigating organism-environment interactions. Of the many possible topics on which plant and animal investigators can provide complementary insights, the following papers touch on four.
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COMPLEMENTARY INSIGHTS FROM STUDIES OF ANIMALS AND PLANTS |
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Global climate change
Past or ongoing global climate change, whether natural or anthropogenic, can elucidate the physiology-environment interactions critical for persistence, extinction, or expansion of existing populations and species, and evolutionary changes in their traits. Predicting (if not mitigating) the biological impact of future climate change motivates this same understanding. Accordingly, global climate change has become a hot topic among both plant and animal ecophysiologists.
The accompanying paper by Ehleringer et al. (2002) is a striking example of the "Law of Unintended Consequences" in the context of global climate change. It suggests that past decreases in atmospheric CO2 led to multiple independent evolutions of plants with C3 photosynthesis into plants with C4 photosynthesis, which subsequently proliferated in warm climates and expanded their ranges into higher latitudes during interglacial periods. The morphological changes in leaf structure to support C4 photosynthesis and the metabolic products/by-products of C4 photosynthesis in turn dramatically affected the nutritional quality of plants. This decreased nutritional quality in turn may have affected the diversity of mammalian herbivores; indeed, the expansion of C4-dominated ecosystems 6–8 Ma b.p. coincided with massive faunal change. Because the predominance of C3 and C4 species appears to be a joint function of atmospheric CO2 levels and temperature among other variables, future generations could witness major changes in C4 abundance, with corresponding effects on herbivores.
As Porter et al. (2002) demonstrate, plants can influence the distribution and abundance of animals not only because animals eat them, but also because they determine the microclimates that animals experience. This demonstration exploits biophysical models of energy flux coupled with molar balance models of mass flux and GIS-based information on climate, topography, and vegetation. The models predict that for large mammals such as elk, radiative heat exchange with a forested canopy (instead of a clear night sky) is tantamount to a significant savings in energy that would otherwise be expended in thermoregulation. In other words, the loss of conifer needles due to forest fires may increase the daily energy requirement of elk by 20–25%. In a second example, Porter et al. (2002) calculate that exclusion of sunlight by vegetation may significantly reduce the temporal overlap of a basking ectothermic predator (rattlesnake) with its endothermic prey (ground squirrels). Thus, these models can reveal unsuspected but significant interactions among climate, terrain, vegetation, and animals.
Sensing and signaling
At one time, biomedical significance, the dramatic nature of animal responses to environmental stimuli, and the conspicuousness of nervous and endocrine systems in animals led studies of extracellular and intracellular signaling to advance more rapidly in animals than in plants. Since then, however, plant biologists have been making equally rapid advances, revealing signaling mechanisms that are comparable to animals' in many ways. For example, the chemical structures of jasmonic acid and its derivatives, major signaling molecules of plants, and eicosanoids such as prostaglandins in animals, are remarkably similar, suggesting either evolutionary homology or convergence in their use (Schultz, 2002). So similar are these and other signaling mechanisms, in fact, that either kingdom may be able to exploit the other, as Schultz (2002) suggests. In one case that Schultz (2002) reviews, caterpillar regurgitant contains a signaling compound so similar to the plant's own that the corresponding plant signaling pathway is activated, leading to release of volatiles that attract caterpillar parasitoids. Alternatively, many insects synthesize plant cytokinins, which they administer to cause plants to form structures that protect the insect or its offspring (i.e., galls). Thus, Schultz (2002) proposes that evolution has produced biochemical counterparts of much of modern warfare in plant and animal combatants: stealth, signal jamming, outright biowarfare, espionage, germ warfare, and signaling third parties to attack one's enemies.
Their ongoing warfare notwithstanding, plants and animals have common enemies, which include physical limitations and environmental conditions that may disrupt the normal supply or excretion of the respiratory gases, CO2 and O2. As several of the accompanying papers (Ehleringer et al., 2002; Lutz and Prentice, 2002; Sage, 2002) discuss, atmospheric concentrations of both gases have fluctuated dramatically during Earth's history, and many organisms (or parts thereof) that are typically normoxic and normocapnic temporarily experience excesses or shortages of these gases. Through mechanisms that are becoming increasingly well-understood (Lutz and Prentice, 2002; Sage, 2002), inappropriate gas exchange damages plant and animal cells. Accordingly, both plants (Sage, 2002) and animals (Lutz and Prentice, 2002) have evolved mechanisms for coping with acute change. These include acute adjustments to alter the transport of gas between organism and environment, "switches" that maintain productive metabolism despite changing gas levels, and activation of protective mechanisms and organized shutdown of cellular processes when all else fails. Many mechanistic issues remain unresolved, such as the identity and mechanism of the molecules that sense inappropriate gas levels and signal responses, and which genes undergo altered expression in response. An evolutionary issue is whether the acute response mechanisms that evidently can cope with current short-term variation in CO2 and O2 will also be able to cope with long-term anthropogenic changes in mean atmospheric gas levels (Sage, 2002), or whether wholesale floral/faunal replacement will occur if these mechanisms cannot (Ehleringer et al., 2002).
Coping with stress in general
Individuals or populations may respond to environmental stress in at least 5 ways: behaviorally selecting favorable environments (Huey, 2002), regulating the internal environment (i.e., homeostasis), adjusting the impact of the environment on function (i.e., phenotypic plasticity or acclimation), having a phenotype that is resistant to the impact of environmental stress, and/or evolutionary change in some or all of the preceding 4 alternatives. Many plants, animals, and other organisms combine these tactics in a stress-resistant stage of the life cycle (seed, spore, egg/embryo, pupa), often capable of prolonged stasis or diapause, which can disperse in space and/or time until benign conditions occur. This capacity may result in substantially different population and evolutionary dynamics than in organisms incapable of withdrawing from ongoing stress. For example, seed banks or egg banks may contain not only the offspring of the just-completed generation but those of up to thousands of generations past, allowing for remarkable mixtures of genotypes in the germinating generation. At the symposium in Chicago, Lawrence Venable discussed plant biologists' current view of these implications and ecological-evolutionary correlates of long-lived seeds, as well as his own work (Venable and Brown, 1988, 1993; Pake and Venable, 1995, 1996; Venable and Pake, 1999; Clauss and Venable, 2000; Moriuchi et al., 2000). Seed counterparts can be common in the animal kingdom; for example, 62% of crustacean species living in inland water habitats have prolonged egg diapause (Hairston and Kearns, 2002). The parallel evolution of propagule dormancy/diapause in plants and animals provides several opportunities for researchers. First, independent tests of ecological and evolutionary predictions are readily possible (Hairston and Kearns [2002]; unlike for other aspects of phenotypic plasticity, in which plant and animal investigators typically study entirely different variables in different ways [Huey, 2002]). Second, unlike with fossils, investigators can compare living organisms conceived many generations before present with their descendants and so directly study the historical evolution of non-morphological traits (Feder et al., 2000; Hairston and Kearns, 2002). A problem with so doing is that geological, limnological, or biological processes may mix the strata in which diapausing organisms are deposited, and obscure ancestor-descendant relationships. At least for zooplankton egg banks in lakes, this mixing may be insufficient to disrupt sediments completely, although the situation in terrestrial seed banks may be far more problematic (Hairston and Kearns, 2002).
With respect to homeostasis, plants face several challenges that animals do not (Holbrook et al., 2002). First, they have few or no moving parts. They lack a heart and ventilatory, gastrointestinal, and thermoregulatory musculature, and thus must exploit other regulatory effectors. Second, much of a plant is dead, including the walls of cells and the entire xylem. Third, in terms of fluid balance, they take in and lose prodigious amounts of water by animal standards (each day a typical plant will lose 
800 times as much as an animal of similar size (Raven et al., 1999), which must be replaced through dead tissue and without moving parts). As Holbrook et al. (2002) describe, plants replace this lost water by literally sucking it from the soil through their xylem, generating as much as –15 atmospheres of pressure in the process. Moreover, plants can modulate the conductance of these xylem vessels via active transport of solutes into them, which swells or deswells internal hydrogels. If the coherent water column ruptures (i.e., is interrupted by a gas embolism), however, the result would be disastrous for plant water balance if not repaired. Holbrook et al. (2002) propose a remarkable 3-step mechanism for repair of embolisms. In the first step, living cells adjacent to the embolism actively pump ions into it, creating an osmotic gradient for water entry. Second, the geometry of pores ("pits") connecting embolized xylem vessels to adjacent filled vessels creates a positive pressure forcing the gas in the embolus into solution. Third, reconnection to adjacent filled vessels must occur, but its mechanism currently awaits explanation.
Outright stress resistance, whether plastic or constitutive and in plants or animals, can be problematic because the features that make many biological molecules susceptible to stress (i.e., weak bonds and conformational flexibility) are otherwise essential for function (Hochachka and Somero, 1984; Somero, 1995). Desiccation has a particularly pernicious effect on cells via the cell membrane; even if the cell survives water loss, rehydration destroys the integrity of the membrane (Crowe and Oliver, 2002). Despite this fact, some eukaryotes (e.g., seeds and pollen of many plants, the resurrection plant [Myrothamnus], brine shrimp, yeast, some nematodes) can survive complete loss of their cellular water, as Crowe and Oliver (2002) describe. Remarkably, this ability appears to stem from a small number of common mechanisms involving accumulation of two disaccharides, trehalose and sucrose. In the first, when membranes pass through the gel-liquid crystalline phase transition, the contents of the cell may leak through them; trehalose and sucrose depress the temperature of the gel-liquid crystalline phase transition so that it does not occur at typical environmental temperatures. In another, even in dehydrated cells phospholipases may act on membranes to produce free fatty acids, which in turn destabilize the membrane; arbutin, a substance that some resurrection plants produce, inhibits phospholipases. To come full circle to biomedical relevance, described above as a potential contributor to the schism between plant and animal biologists: These lessons in stress tolerance learned from plants and fungi are now enabling the freeze-drying of blood platelets, which otherwise must be maintained in blood banks at room temperature and even then must be discarded after 5 days.
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CONCLUSION: PARAPHRASING KROGH AND DOBZHANSKY |
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Although plants and animals clearly are different, each can elucidate principles of organism-environment interaction, biological mechanism, and evolutionary process and product that apply to both. For either the plant or the animal ecophysiological communities, to forgo the insights and advances produced by the other would be to squander a significant opportunity for scientific advancement. The Krogh Principle (Krogh, 1929
), often cited by animal physiologists (Krebs, 1975), states: "For many problems there is an animal on which it can be most conveniently studied." Perhaps the Krogh Principle needs revision; as written, plants (and, for the matter, members of all kingdoms) are "animals" too. But the interdependence of plant and animal studies is even more fundamental. As the most elementary of biology teaches, most plants and animals rely on one another for energy and mass fixation, and/or reproduction. As the accompanying papers and recent/forthcoming symposia on symbiosis in this journal exemplify particularly well, direct interactions of plants and animals have had a substantial impact on one another's evolution. Surely the investigation of plant and animal biology needs to mirror this evolution. Thus, to adapt the famous phrase of Dobzhansky (1973), little in animal biology makes sense except in the light of plant biology, and vice versa.
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ACKNOWLEDGMENTS |
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This symposium, its publication in Integrative and Comparative Biology, and its predecessor workshop at the annual meeting of the Ecological Society of America have been supported by a grant from the National Science Foundation (IBN0097876), which also, through its formation of a joint plant-animal program in ecological and evolutionary physiology, set the stage for this symposium and supported much of the research described. Preparation of this manuscript was also supported by NSF Grant IBN9986158. Equally important was support from the Program Innovation Fund of the Society for Integrative and Comparative Biology (SICB). As described, this entire project was a collaborative effort of SICB, particularly the Division of Comparative Physiology and Biochemistry (DCPB), and the Physiological Ecology Section of the Ecological Society of America (PES-ESA). James Coleman (PES-ESA), Vincent Gutschick (PES-ESA), Arnold Bloom (a member of the American Society for Plant Physiology), Steven Hand (SICB-DCPB), and Dennis Bramble (SICB) all contributed to the organization and execution of the symposium and the ESA workshop. May Berenbaum (University of Illinois) contributed concluding remarks at the symposium.
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1 From the symposium Plant/Animal Physiology presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: m-feder{at}uchicago.edu
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