Herbivory

Plants of Erigeron clokeyi, Haplopappus apargioides, Chamaebatiaria millefolium, and Encelia californica were grown at elevations of 1,250 and 3,094 m for at least 4 weeks in the White Mountains of California. During this period the photosynthetic temperature response was different at the two elevations. However, there was no apparent photosynthetic acclimation to differences in the CO 2 tensions of the two growth environments.

@article{doi1023071932991,
    author = "Mooney, Harold A. and Strain, Boyd R. and West, Marda",
    title = "Photosynthetic Efficiency at Reduced Carbon Dioxide Tensions",
    year = "1966",
    journal = "Ecology",
    abstract = "Plants of Erigeron clokeyi, Haplopappus apargioides, Chamaebatiaria millefolium, and Encelia californica were grown at elevations of 1,250 and 3,094 m for at least 4 weeks in the White Mountains of California. During this period the photosynthetic temperature response was different at the two elevations. However, there was no apparent photosynthetic acclimation to differences in the CO 2 tensions of the two growth environments.",
    url = "https://doi.org/10.2307/1932991",
    doi = "10.2307/1932991",
    openalex = "W2109465976"
}

Zea mays and Gomphrena globosa form labeled aspartate and malate (C 4 -acids) via β-carboxylation of P-enolpyruvate during photosynthesis. Studies of the redistribution of 14 C in pulse- and chase-type feedings of 14 CO 2 indicate that most labeled phosphorylated compounds are formed from the C 4 -acids. A mechanism involving CO 2 as a transitory intermediate is advanced to explain the carboxyl transfer from the C 4 -acids to 3-phosphoglyceric acid (3-PGA). In this model, CO 2 is generated through the oxidative decarboxylation of malic acid by "malic" enzyme, and is refixed by RuDP carboxylase to form 3-PGA. The pattern of labeling of photosynthetic products, the extractable enzyme activities, and the gas exchange properties of these plants appear to be consistent with this proposed sequence of reactions. The location of 14 C-labeled compounds was determined by radioautography, and by nonaqueous density gradient separation. Differential grinding was used to study the location of some photosynthetic enzymes. These indicate that CO 2 fixation by β-carboxylation occurs in the leaf mesophyll. The carboxyl transfer and the reactions leading to the photosynthesis of starch appear to be confined predominantly to the bundle sheath cells. Rapid transport of C 4 -acids from the site of CO 2 fixation in the mesophyll to the bundle sheath may occur by plasmodesmata.

@article{doi101139b70106,
    author = "Berry, Joseph A. and Downton, W. J. S. and Tregunna, E. B.",
    title = "The photosynthetic carbon metabolism of Zea mays and Gomphrena globosa: the location of the CO 2 fixation and the carboxyl transfer reactions",
    year = "1970",
    journal = "Canadian Journal of Botany",
    abstract = {Zea mays and Gomphrena globosa form labeled aspartate and malate (C 4 -acids) via β-carboxylation of P-enolpyruvate during photosynthesis. Studies of the redistribution of 14 C in pulse- and chase-type feedings of 14 CO 2 indicate that most labeled phosphorylated compounds are formed from the C 4 -acids. A mechanism involving CO 2 as a transitory intermediate is advanced to explain the carboxyl transfer from the C 4 -acids to 3-phosphoglyceric acid (3-PGA). In this model, CO 2 is generated through the oxidative decarboxylation of malic acid by "malic" enzyme, and is refixed by RuDP carboxylase to form 3-PGA. The pattern of labeling of photosynthetic products, the extractable enzyme activities, and the gas exchange properties of these plants appear to be consistent with this proposed sequence of reactions. The location of 14 C-labeled compounds was determined by radioautography, and by nonaqueous density gradient separation. Differential grinding was used to study the location of some photosynthetic enzymes. These indicate that CO 2 fixation by β-carboxylation occurs in the leaf mesophyll. The carboxyl transfer and the reactions leading to the photosynthesis of starch appear to be confined predominantly to the bundle sheath cells. Rapid transport of C 4 -acids from the site of CO 2 fixation in the mesophyll to the bundle sheath may occur by plasmodesmata.},
    url = "https://doi.org/10.1139/b70-106",
    doi = "10.1139/b70-106",
    openalex = "W2123142109"
}

Species in the families Amaranthaceae, Aizoaceae, Chenopodiaceae, Convolvulaceae, Euphorbiaceae, Nyctaginaceae, Portulacaceae, and Zygophyllaceae were examined for leaf anatomy typical of plants having the C 4 type photosynthetic carbon fixation pathway. They are assembled by families into three groups: genera in which all species possess the specialization; genera in which some but not all species possess the specialization; and genera in which no species possess the specialization. The specialization in leaf anatomy was noted in species of 24 genera. Its presence is highly correlated with a habitat of limited water availability and (or) with a tropical origin. The carbon dioxide compensation points of nine species in the Chenopodiaceae family were measured. Low values were obtained only for those species that possess a form of specialized leaf anatomy (Atriplex confertifolia (Torr. & Frem.) Wats., A. falcata (M. E. Jones) Standl., Halogeton glomeratus (Bieb.) Meyer, Salsola kali L. var. tenuiflora Tausch.). The latter two species, having centric leaves, do not possess the more typical differential bundle sheath chlorenchyma but do possess two, individually distinct, single-cell layers of chlorenchyma, adjacent and external to the peripheral veins.

@article{doi101139b70309,
    author = "Welkie, George W. and Caldwell, M. M.",
    title = "Leaf anatomy of species in some dicotyledon families as related to the C 3 and C 4 pathways of carbon fixation",
    year = "1970",
    journal = "Canadian Journal of Botany",
    abstract = "Species in the families Amaranthaceae, Aizoaceae, Chenopodiaceae, Convolvulaceae, Euphorbiaceae, Nyctaginaceae, Portulacaceae, and Zygophyllaceae were examined for leaf anatomy typical of plants having the C 4 type photosynthetic carbon fixation pathway. They are assembled by families into three groups: genera in which all species possess the specialization; genera in which some but not all species possess the specialization; and genera in which no species possess the specialization. The specialization in leaf anatomy was noted in species of 24 genera. Its presence is highly correlated with a habitat of limited water availability and (or) with a tropical origin. The carbon dioxide compensation points of nine species in the Chenopodiaceae family were measured. Low values were obtained only for those species that possess a form of specialized leaf anatomy (Atriplex confertifolia (Torr. \& Frem.) Wats., A. falcata (M. E. Jones) Standl., Halogeton glomeratus (Bieb.) Meyer, Salsola kali L. var. tenuiflora Tausch.). The latter two species, having centric leaves, do not possess the more typical differential bundle sheath chlorenchyma but do possess two, individually distinct, single-cell layers of chlorenchyma, adjacent and external to the peripheral veins.",
    url = "https://doi.org/10.1139/b70-309",
    doi = "10.1139/b70-309",
    openalex = "W2107848808"
}

The view has long been held that the Calvin cycle operates ubiquitously in higher plants, algae, and probably photoautotrophic bacteria, but there is now evidence for alternative pathways in some plants and bacteria. In the present article, particular emphasis will be placed upon the alternative pro­ cess in higher plants, but some aspects of current interest concerning the op­ eration of the Calvin cycle will also be considered. Topics relating to photo­ synthetic CO2-fixation that are treated in detail in other chapters of this volume have been either excluded or dealt with only briefly. There have been several recent reviews, books, and symposia dealing with aspects of photosynthetic CO2-fixation (8, SO, 55, 63, 100, 125, 128).

@article{doi101146annurevpp21060170001041,
    author = "Hatch, M.D. and Slack, C. R.",
    title = "Photosynthetic CO2-Fixation Pathways",
    year = "1970",
    journal = "Annual Review of Plant Physiology",
    abstract = "The view has long been held that the Calvin cycle operates ubiquitously in higher plants, algae, and probably photoautotrophic bacteria, but there is now evidence for alternative pathways in some plants and bacteria. In the present article, particular emphasis will be placed upon the alternative pro­ cess in higher plants, but some aspects of current interest concerning the op­ eration of the Calvin cycle will also be considered. Topics relating to photo­ synthetic CO2-fixation that are treated in detail in other chapters of this volume have been either excluded or dealt with only briefly. There have been several recent reviews, books, and symposia dealing with aspects of photosynthetic CO2-fixation (8, SO, 55, 63, 100, 125, 128).",
    url = "https://doi.org/10.1146/annurev.pp.21.060170.001041",
    doi = "10.1146/annurev.pp.21.060170.001041",
    openalex = "W2135849317"
}

@article{doi101016s0031942200843241,
    author = "Bender, Margaret M.",
    title = "Variations in the 13C/12C ratios of plants in relation to the pathway of photosynthetic carbon dioxide fixation",
    year = "1971",
    journal = "Phytochemistry",
    url = "https://doi.org/10.1016/s0031-9422(00)84324-1",
    doi = "10.1016/s0031-9422(00)84324-1",
    openalex = "W2033332006"
}

@article{caswell1973photosynthetic,
    author = "Caswell, Hal and Reed, Frank and Stephenson, S. N. and Werner, Patricia A.",
    title = "Photosynthetic Pathways and Selective Herbivory: A Hypothesis",
    year = "1973",
    journal = "The American Naturalist",
    url = "https://doi.org/10.1086/282851",
    doi = "10.1086/282851",
    number = "956",
    pages = "465-480",
    volume = "107"
}

@phdthesis{caswell1973photosynthetic1,
    author = "Caswell, H. and Reed, F. and Stephenson, S. N. and Werner, P. A",
    title = "Photosynthetic pathways and selective herbivory",
    year = "1973",
    publisher = "a hypothesis: American Naturalist, v. 107, p. 465-480",
    note = "talkorigins\_source = {true}; raw\_reference = {Caswell, H., Reed, F., Stephenson, S. N., and Werner, P. A., 1973, Photosynthetic pathways and selective herbivory: a hypothesis: American Naturalist, v. 107, p. 465-480.}"
}

We propose that plants possessing the C4-dicarboxylic acid pathway of photosynthetic carbon fixation are generally inferior food sources for herbivores, and are often avoided by them, relative to plants possessing only the C3-Calvin cycle pathway. As initial support of this hypothesis, we present data from the literature, dealing primarily with insects, that suggest that C4 species are ingested in proportions lower than their availability in a number of natural situations, that they tend to be avoided in laboratory preference tests, and that they result in lower survival and fecundity in herbivores feeding on them. We suggest a number of physiological, anatomical, and nutritional differences between C3 and C4 species that may be involved in generating the observed pattern of herbivore preference. The ecological relevance of the differences between C3 and C4 species has been discussed to date only in relation to hypothetical effects on interspecific competition. If our hypothesis is true, selective herbivory may be another ecologically important consequence of the differences. There is enough evidence pointing toward the validity of our hypothesis that it should be further tested, and the distribution of plants as C3 and C4 species should be taken into account in community and ecosystem studies.

@article{doi101086282851,
    author = "Caswell, Hal and Reed, Frank C. and Stephenson, Stephen N. and Werner, Patricia A.",
    title = "Photosynthetic Pathways and Selective Herbivory: A Hypothesis",
    year = "1973",
    journal = "The American Naturalist",
    abstract = "We propose that plants possessing the C4-dicarboxylic acid pathway of photosynthetic carbon fixation are generally inferior food sources for herbivores, and are often avoided by them, relative to plants possessing only the C3-Calvin cycle pathway. As initial support of this hypothesis, we present data from the literature, dealing primarily with insects, that suggest that C4 species are ingested in proportions lower than their availability in a number of natural situations, that they tend to be avoided in laboratory preference tests, and that they result in lower survival and fecundity in herbivores feeding on them. We suggest a number of physiological, anatomical, and nutritional differences between C3 and C4 species that may be involved in generating the observed pattern of herbivore preference. The ecological relevance of the differences between C3 and C4 species has been discussed to date only in relation to hypothetical effects on interspecific competition. If our hypothesis is true, selective herbivory may be another ecologically important consequence of the differences. There is enough evidence pointing toward the validity of our hypothesis that it should be further tested, and the distribution of plants as C3 and C4 species should be taken into account in community and ecosystem studies.",
    url = "https://doi.org/10.1086/282851",
    doi = "10.1086/282851",
    openalex = "W1994800192",
    references = "doi101016s0065280608602301, doi101071bi9710159, doi101086282146, doi101086282415, doi101086282477, doi101086282478, doi1010970001069419620100000034, doi101126science17340021162, doi101146annureven12010167000423, doi1023071934239"
}

Large herbivores must select food from a wide variety of plant parts, species, and strains. These differ in nutritional value (protein, carbohydrate, etc.), toughness, spinosity, etc. Even greater differences are found in types and concentrations of secondary compounds. Every plant produces its own set of secondary chemical compounds, which to a great extent are unique to it or its species. Ingestion of natural concentrations of these compounds can lead to either death or severe physiological impairment. The ubiquitous nature of these compounds would make herbivory impossible unless animals had mechanisms for degrading and excreting them. An animal displaying no obvious symptoms of poisoning is not free of the problem of ridding itself of toxic compounds; if it is eating plants, it almost certainly has this problem. Herbivores are capable of detoxifying and eliminating secondary compounds. Limitations of these mechanisms force mammalian herbivores to consume a variety of plant foods at any one time, to treat new foods with caution, to ingest small amounts on the first encounter, and to sample food continuously. Selection of foods is based on learning in response to adverse internal physiological effects, and herbivores probably cannot predict these from the smell or taste of new foods. Herbivores prefer to eat familiar foods and can seek out and consume foods that rectify specific nutritional deficiencies induced by detoxification. They should prefer to feed on foods that contain small amounts of secondary compounds, and their body size and searching strategies should be adapted to optimize the number of types of foods available with respect to the total amount of food that can be eaten and will be present in the future. Natural selection can increase the efficiency of degrading particular secondary compounds. Specialist herbivores, like koala and mountain viscacha, are expected where a large amount of several related toxic foods is present in a year-round supply. However, few large herbivores are specialized on such a restricted range of foods.

@article{doi101086282907,
    author = "Freeland, W. J. and Janzen, Daniel H.",
    title = "Strategies in Herbivory by Mammals: The Role of Plant Secondary Compounds",
    year = "1974",
    journal = "The American Naturalist",
    abstract = "Large herbivores must select food from a wide variety of plant parts, species, and strains. These differ in nutritional value (protein, carbohydrate, etc.), toughness, spinosity, etc. Even greater differences are found in types and concentrations of secondary compounds. Every plant produces its own set of secondary chemical compounds, which to a great extent are unique to it or its species. Ingestion of natural concentrations of these compounds can lead to either death or severe physiological impairment. The ubiquitous nature of these compounds would make herbivory impossible unless animals had mechanisms for degrading and excreting them. An animal displaying no obvious symptoms of poisoning is not free of the problem of ridding itself of toxic compounds; if it is eating plants, it almost certainly has this problem. Herbivores are capable of detoxifying and eliminating secondary compounds. Limitations of these mechanisms force mammalian herbivores to consume a variety of plant foods at any one time, to treat new foods with caution, to ingest small amounts on the first encounter, and to sample food continuously. Selection of foods is based on learning in response to adverse internal physiological effects, and herbivores probably cannot predict these from the smell or taste of new foods. Herbivores prefer to eat familiar foods and can seek out and consume foods that rectify specific nutritional deficiencies induced by detoxification. They should prefer to feed on foods that contain small amounts of secondary compounds, and their body size and searching strategies should be adapted to optimize the number of types of foods available with respect to the total amount of food that can be eaten and will be present in the future. Natural selection can increase the efficiency of degrading particular secondary compounds. Specialist herbivores, like koala and mountain viscacha, are expected where a large amount of several related toxic foods is present in a year-round supply. However, few large herbivores are specialized on such a restricted range of foods.",
    url = "https://doi.org/10.1086/282907",
    doi = "10.1086/282907",
    openalex = "W2045653366",
    references = "doi101002path1700890112, doi101016s003169972506884x, doi101111j155856461964tb01674x, doi101111j155856461969tb03489x, doi101126science1723983579, doi101146annureves02110171002341, doi101146annureves03110172001025, doi1023071942161, doi105962bhltitle7320, openalexw2106632477"
}

@article{bennack1981the,
    author = "Bennack, Dan E.",
    title = "The effects of mandible morphology and photosynthetic pathway on selective herbivory in grasshoppers",
    year = "1981",
    journal = "Oecologia",
    url = "https://doi.org/10.1007/bf00540615",
    doi = "10.1007/bf00540615",
    number = "2",
    pages = "281-283",
    volume = "51"
}

@article{doi101007bf00540615,
    author = "Bennack, Dan E.",
    title = "The effects of mandible morphology and photosynthetic pathway on selective herbivory in grasshoppers",
    year = "1981",
    journal = "Oecologia",
    url = "https://doi.org/10.1007/bf00540615",
    doi = "10.1007/bf00540615",
    openalex = "W1974015487",
    references = "caswell1973photosynthetic, doi101007bf00344568, doi101007bf00582893, doi101016s0065280608602301, doi101093aesa283408, doi101093aesa37147, doi101111j146979981964tb05157x, doi1023071936580, doi1023073223017, openalexw3002178311"
}

Rates of herbivory and defensive characteristics of young and mature leaves were measured for saplings of 46 canopy tree species in a lowland tropical rain forest (Barro Colorado Island, Panama). Grazing rates were determined in the field for sample periods in the early wet, late wet, and dry seasons. Leaf properties such as pubescence, toughness, water, protein, fiber, and phenolic contents explained over 70% of the variation among plant species in the rates of herbivory on mature leaves. Leaf toughness was most highly correlated with levels of herbivory, followed by fiber content and nutritive value. Phenol content and phenol: protein ratios were not significantly correlated with damage. Mature leaves of gap—colonizing species were grazed six times more rapidly than leaves of shade—tolerant species. Gap—colonizers have less tough leaves, lower concentrations of fiber and phenolics, higher levels of nitrogen and water, shorter leaf lifetimes, and faster growth rates than do shade—tolerant species. Gap—colonizers did not escape discovery by herbivores to any greater extent than shade—tolerant species, as measured by the spatial distribution of plants or by the intraspecific distribution of herbivore damage under natural or experimentally manipulated conditions. In 70% of the species, young leaves suffered higher damage levels than mature leaves. Although young leaves are more nutritious and less tough and fibrous, they have two to three times the concentrations of phenols. The temporal appearance of young leaves was not correlated with the distribution of herbivory among individuals of a species. Interspecific patterns of defense mechanisms are discussed in terms of current theories of plant apparency, and an alternative model for the evolution of plant defenses is presented.

@article{doi1023071942495,
    author = "Coley, Phyllis D.",
    title = "Herbivory and Defensive Characteristics of Tree Species in a Lowland Tropical Forest",
    year = "1983",
    journal = "Ecological Monographs",
    abstract = "Rates of herbivory and defensive characteristics of young and mature leaves were measured for saplings of 46 canopy tree species in a lowland tropical rain forest (Barro Colorado Island, Panama). Grazing rates were determined in the field for sample periods in the early wet, late wet, and dry seasons. Leaf properties such as pubescence, toughness, water, protein, fiber, and phenolic contents explained over 70\% of the variation among plant species in the rates of herbivory on mature leaves. Leaf toughness was most highly correlated with levels of herbivory, followed by fiber content and nutritive value. Phenol content and phenol: protein ratios were not significantly correlated with damage. Mature leaves of gap—colonizing species were grazed six times more rapidly than leaves of shade—tolerant species. Gap—colonizers have less tough leaves, lower concentrations of fiber and phenolics, higher levels of nitrogen and water, shorter leaf lifetimes, and faster growth rates than do shade—tolerant species. Gap—colonizers did not escape discovery by herbivores to any greater extent than shade—tolerant species, as measured by the spatial distribution of plants or by the intraspecific distribution of herbivore damage under natural or experimentally manipulated conditions. In 70\% of the species, young leaves suffered higher damage levels than mature leaves. Although young leaves are more nutritious and less tough and fibrous, they have two to three times the concentrations of phenols. The temporal appearance of young leaves was not correlated with the distribution of herbivory among individuals of a species. Interspecific patterns of defense mechanisms are discussed in terms of current theories of plant apparency, and an alternative model for the evolution of plant defenses is presented.",
    url = "https://doi.org/10.2307/1942495",
    doi = "10.2307/1942495",
    openalex = "W2076306922",
    references = "doi10100797814020561472260, doi101086281792, doi101086282907, doi1010970001069419511200000015, doi101111j155856461964tb01674x, doi101126science12933611466, doi101126science1713973757, doi1023071219834, doi1023072259845, doi1023073544308, openalexw1592882905, openalexw3118948871"
}

S. J. McNaughton, Compensatory Plant Growth as a Response to Herbivory, Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 329-336

@article{doi1023073544305,
    author = "McNaughton, S. J.",
    title = "Compensatory Plant Growth as a Response to Herbivory",
    year = "1983",
    journal = "Oikos",
    abstract = "S. J. McNaughton, Compensatory Plant Growth as a Response to Herbivory, Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 329-336",
    url = "https://doi.org/10.2307/3544305",
    doi = "10.2307/3544305",
    openalex = "W2018440025",
    references = "doi101086283426, doi101111j155856461980tb04849x, doi101126science1744011825"
}

John P. Bryant, F. Stuart Chapin, III, David R. Klein, Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory, Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 357-368

@article{doi1023073544308,
    author = "Bryant, John P. and Chapin, F. Stuart and Klein, David R.",
    title = "Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory",
    year = "1983",
    journal = "Oikos",
    abstract = "John P. Bryant, F. Stuart Chapin, III, David R. Klein, Carbon/Nutrient Balance of Boreal Plants in Relation to Vertebrate Herbivory, Oikos, Vol. 40, No. 3, Herbivore-Plant Interactions at Northern Latitudes. Proceedings of a Symposium Held 14-18 September, 1981, at Kevo, Finland (May, 1983), pp. 357-368",
    url = "https://doi.org/10.2307/3544308",
    doi = "10.2307/3544308",
    openalex = "W2063165095",
    references = "doi101086283426, doi1023072259845"
}

The potential benefits of herbivory to plants have been debated over the last decade. Several investigators claim that removal of or damage to the productive, absorptive, or reproductive tissue of plants by herbivores benefits some plant species by increasing their net primary productivity, seed production, or longevity, and that these changes increase plant fitness and result in the evolution of herbivore-plant mutualisms. Although more than 40 papers have been cited as presenting experimental evidence in support of these benefits and mutualisms, strong evidence is lacking. Increased plant biomass as a result of tissue removal has been found only under growth-chamber conditions and in cultivated crops. Although herbivores may benefit certain plants by reducing competition or removing senescent tissue, no convincing evidence supports the theory that herbivory benefits grazed plants.

@article{doi101086284531,
    author = "Belsky, A. Joy",
    title = "Does Herbivory Benefit Plants? A Review of the Evidence",
    year = "1986",
    journal = "The American Naturalist",
    abstract = "The potential benefits of herbivory to plants have been debated over the last decade. Several investigators claim that removal of or damage to the productive, absorptive, or reproductive tissue of plants by herbivores benefits some plant species by increasing their net primary productivity, seed production, or longevity, and that these changes increase plant fitness and result in the evolution of herbivore-plant mutualisms. Although more than 40 papers have been cited as presenting experimental evidence in support of these benefits and mutualisms, strong evidence is lacking. Increased plant biomass as a result of tissue removal has been found only under growth-chamber conditions and in cultivated crops. Although herbivores may benefit certain plants by reducing competition or removing senescent tissue, no convincing evidence supports the theory that herbivory benefits grazed plants.",
    url = "https://doi.org/10.1086/284531",
    doi = "10.1086/284531",
    openalex = "W2015296317",
    references = "doi1010079783642965456, doi101007bf00378790, doi101086283426, doi101086284321, doi101126science1904214515, doi101146annureves12110181002201, doi1023071942578, doi1023072260079, doi1023072408012, openalexw2045291252, openalexw2077454220"
}

Three old—field plant communities of varying composition near Aiken, South Carolina, were used to test the hypothesis that phytophagous insects avoid consuming plants possessing the C 4 photosynthetic pathway and consume plants that possess only the C 3 pathway. The relative abundances of stable carbon isotopes in insect tissues, which indicate consumption of C 3 or C 4 plants, were used to determine if insects were consuming C 3 and C 4 plants in proportion to their abundance in the plant community. In one community, the carbon isotope ratio for insects was significantly less than that expected for proportional consumption and indicated avoidance of C 4 species. Insect consumption of C 4 plants was °50% of that expected if insects were consuming C 3 and C 4 plants in proportion to their abundance. In the other two communities, the differences between observed and expected isotopic ratios were not significant. Levels of insect consumption of C 4 plants in these two communities were, respectively, °82% and °126% of those expected for proportional consumption. The results suggest that the degree of avoidance varies among plant communities.

@article{pinder1987insect,
    author = "Pinder, John E. and Kroh, Glenn C.",
    title = "Insect Herbivory and Photosynthetic Pathways in Old‐Field Ecosystems",
    year = "1987",
    journal = "Ecology",
    abstract = "Three old—field plant communities of varying composition near Aiken, South Carolina, were used to test the hypothesis that phytophagous insects avoid consuming plants possessing the C 4 photosynthetic pathway and consume plants that possess only the C 3 pathway. The relative abundances of stable carbon isotopes in insect tissues, which indicate consumption of C 3 or C 4 plants, were used to determine if insects were consuming C 3 and C 4 plants in proportion to their abundance in the plant community. In one community, the carbon isotope ratio for insects was significantly less than that expected for proportional consumption and indicated avoidance of C 4 species. Insect consumption of C 4 plants was °50\% of that expected if insects were consuming C 3 and C 4 plants in proportion to their abundance. In the other two communities, the differences between observed and expected isotopic ratios were not significant. Levels of insect consumption of C 4 plants in these two communities were, respectively, °82\% and °126\% of those expected for proportional consumption. The results suggest that the degree of avoidance varies among plant communities.",
    url = "https://doi.org/10.2307/1939255",
    doi = "10.2307/1939255",
    number = "2",
    pages = "254-259",
    volume = "68"
}

In a single population of Ipomopsis arizonica (Polemoniaceae), we show a continuum of compensatory responses to vertebrate herbivory. We demonstrate experimentally that the degree of herbivore impact depends on plant association, nutrient availability, and timing of grazing. From 1985 to 1987, the most common response to vertebrate herbivory was equal compensation, whereby grazed plants set numbers of fruits and seeds equal to controls within the same growing season. However, we also observed cases of significant overcompensation and undercompensation. In 1985 and 1987, overcompensation occurred in vertebrate-grazed plants that were supplemented with nutrients and growing free of competition. These plants produced 33% to 120% more fruit than control, ungrazed plants. Cases of undercompensation occurred in groups where I. arizonica grew in association with grasses or where nutrients were not supplemented. Grazed and clipped plants in these groups produced from 28% to 82% as many fruits as did ungrazed controls. Our studies indicate that the compensatory response of plants to grazing is probabilistic when three external factors are considered. The probability of compensation for herbivory decreases as competition with other plants increases, as nutrient levels decrease, and as the timing of herbivory comes later in the growing season.

@article{doi101086284962,
    author = "Maschinski, Joyce and Whitham, Thomas G.",
    title = "The Continuum of Plant Responses to Herbivory: The Influence of Plant Association, Nutrient Availability, and Timing",
    year = "1989",
    journal = "The American Naturalist",
    abstract = "In a single population of Ipomopsis arizonica (Polemoniaceae), we show a continuum of compensatory responses to vertebrate herbivory. We demonstrate experimentally that the degree of herbivore impact depends on plant association, nutrient availability, and timing of grazing. From 1985 to 1987, the most common response to vertebrate herbivory was equal compensation, whereby grazed plants set numbers of fruits and seeds equal to controls within the same growing season. However, we also observed cases of significant overcompensation and undercompensation. In 1985 and 1987, overcompensation occurred in vertebrate-grazed plants that were supplemented with nutrients and growing free of competition. These plants produced 33\% to 120\% more fruit than control, ungrazed plants. Cases of undercompensation occurred in groups where I. arizonica grew in association with grasses or where nutrients were not supplemented. Grazed and clipped plants in these groups produced from 28\% to 82\% as many fruits as did ungrazed controls. Our studies indicate that the compensatory response of plants to grazing is probabilistic when three external factors are considered. The probability of compensation for herbivory decreases as competition with other plants increases, as nutrient levels decrease, and as the timing of herbivory comes later in the growing season.",
    url = "https://doi.org/10.1086/284962",
    doi = "10.1086/284962",
    openalex = "W1967466803",
    references = "doi101086283426, openalexw2045291252"
}

C4 and CAM photosynthesis are evolutionarily derived from C3 photosynthesis. The morphological and biochemical modifications necessary to achieve either C4 or CAM photosynthesis are thought to have independently arisen numerous times within different higher plant taxa. It is thought that C4 photosynthesis evolved in response to the low atmospheric CO2 concentrations that arose sometime after the end of the Cretaceous. Low CO2 concentrations result in significant increases in photorespiration of C3 plants, reducing productivity; both C3-C4 intermediate and C4 plants exhibit reduced photorespiration rates. In contrast, it may be argued that CAM arose either in response to selection of increased water-use efficiency or for increased carbon gain. Globally, all three pathways are widely distributed today, with a tendency toward ecological adaptation of C4 plants into warm, monsoonal climates and CAM plants into water-limited habitats. In an anthropogenically altered CQ2 environment, C4 plants may lose their competitive advantage over C3 plants. 411

@article{doi101146annureves24110193002211,
    author = "Ehleringer, James R. and Monson, Russell K.",
    title = "Evolutionary and Ecological Aspects of Photosynthetic Pathway Variation",
    year = "1993",
    journal = "Annual Review of Ecology and Systematics",
    abstract = "C4 and CAM photosynthesis are evolutionarily derived from C3 photosynthesis. The morphological and biochemical modifications necessary to achieve either C4 or CAM photosynthesis are thought to have independently arisen numerous times within different higher plant taxa. It is thought that C4 photosynthesis evolved in response to the low atmospheric CO2 concentrations that arose sometime after the end of the Cretaceous. Low CO2 concentrations result in significant increases in photorespiration of C3 plants, reducing productivity; both C3-C4 intermediate and C4 plants exhibit reduced photorespiration rates. In contrast, it may be argued that CAM arose either in response to selection of increased water-use efficiency or for increased carbon gain. Globally, all three pathways are widely distributed today, with a tendency toward ecological adaptation of C4 plants into warm, monsoonal climates and CAM plants into water-limited habitats. In an anthropogenically altered CQ2 environment, C4 plants may lose their competitive advantage over C3 plants. 411",
    url = "https://doi.org/10.1146/annurev.es.24.110193.002211",
    doi = "10.1146/annurev.es.24.110193.002211",
    openalex = "W2137725470",
    references = "caswell1973photosynthetic, doi101007bf00344568, doi101007bf00351210, doi101007bf00377192, doi101007bf00379558, doi101007bf00582893, doi101007bf02861058, doi101029jd089id01p01267, doi101038329408a0, doi101038342163a0, doi101086282851, doi101146annurevpp11060160000501, doi101146annurevpp40060189002443, doi102475ajs2894333, doi102475ajs2914339, pinder1987insect"
}

▪ Abstract In this review, we discuss the ecological and evolutionary consequences of plant-herbivore interactions in tropical forests. We note first that herbivory rates are higher in tropical forests than in temperate ones and that, in contrast to leaves in temperate forests, most of the damage to tropical leaves occurs when they are young and expanding. Leaves in dry tropical forests also suffer higher rates of damage than in wet forests, and damage is greater in the understory than in the canopy. Insect herbivores, which typically have a narrow host range in the tropics, cause most of the damage to leaves and have selected for a wide variety of chemical, developmental, and phenological defenses in plants. Pathogens are less studied but cause considerable damage and, along with insect herbivores, may contribute to the maintenance of tree diversity. Folivorous mammals do less damage than insects or pathogens but have evolved to cope with the high levels of plant defenses. Leaves in tropical forests are defended by having low nutritional quality, greater toughness, and a wide variety of secondary metabolites, many of which are more common in tropical than temperate forests. Tannins, toughness, and low nutritional quality lengthen insect developmental times, making them more vulnerable to predators and parasitoids. The widespread occurrence of these defenses suggests that natural enemies are key participants in plant defenses and may have influenced the evolution of these traits. To escape damage, leaves may expand rapidly, be flushed synchronously, or be produced during the dry season when herbivores are rare. One strategy virtually limited to tropical forests is for plants to flush leaves but delay “greening” them until the leaves are mature. Many of these defensive traits are correlated within species, due to physiological constraints and tradeoffs. In general, shade-tolerant species invest more in defenses than do gap-requiring ones, and species with long-lived leaves are better defended than those with short-lived leaves.

@article{doi101146annurevecolsys271305,
    author = "Coley, Phyllis D. and Barone, John A.",
    title = "HERBIVORY AND PLANT DEFENSES IN TROPICAL FORESTS",
    year = "1996",
    journal = "Annual Review of Ecology and Systematics",
    abstract = "▪ Abstract In this review, we discuss the ecological and evolutionary consequences of plant-herbivore interactions in tropical forests. We note first that herbivory rates are higher in tropical forests than in temperate ones and that, in contrast to leaves in temperate forests, most of the damage to tropical leaves occurs when they are young and expanding. Leaves in dry tropical forests also suffer higher rates of damage than in wet forests, and damage is greater in the understory than in the canopy. Insect herbivores, which typically have a narrow host range in the tropics, cause most of the damage to leaves and have selected for a wide variety of chemical, developmental, and phenological defenses in plants. Pathogens are less studied but cause considerable damage and, along with insect herbivores, may contribute to the maintenance of tree diversity. Folivorous mammals do less damage than insects or pathogens but have evolved to cope with the high levels of plant defenses. Leaves in tropical forests are defended by having low nutritional quality, greater toughness, and a wide variety of secondary metabolites, many of which are more common in tropical than temperate forests. Tannins, toughness, and low nutritional quality lengthen insect developmental times, making them more vulnerable to predators and parasitoids. The widespread occurrence of these defenses suggests that natural enemies are key participants in plant defenses and may have influenced the evolution of these traits. To escape damage, leaves may expand rapidly, be flushed synchronously, or be produced during the dry season when herbivores are rare. One strategy virtually limited to tropical forests is for plants to flush leaves but delay “greening” them until the leaves are mature. Many of these defensive traits are correlated within species, due to physiological constraints and tradeoffs. In general, shade-tolerant species invest more in defenses than do gap-requiring ones, and species with long-lived leaves are better defended than those with short-lived leaves.",
    url = "https://doi.org/10.1146/annurev.ecolsys.27.1.305",
    doi = "10.1146/annurev.ecolsys.27.1.305",
    openalex = "W2150998549",
    references = "doi101001jama196203050110085031, doi101086284369, doi101111j155856461964tb01674x, doi101126science2304728895, doi1023071942495, doi1023072406212, ehrlich1964butterflies, openalexw2097385721"
}

Abstract Herbivorous insects exploit many different plants and plant parts and often adopt different feeding strategies throughout their life cycle. The conceptual framework for investigating insect–plant interactions relies heavily on explanations invoking plant chemistry, neglecting a suite of competing and interacting pressures that may also limit herbivory. In the present paper, the methods by which ontogeny, feeding strategies and morphological characters inhibit herbivory by mandibulate holometabolous insects are examined. The emphasis on mechanical disruption of plant cells in the insect digestive strategy changes the relative importance of plant ‘defences’, increasing the importance of leaf structure in inhibiting herbivory. Coupled with the implications of substantial morphological and behavioural changes in ontogeny, herbivores adopt a range of approaches to herbivory that are independent of plant chemistry alone. Many insect herbivores exhibit substantial ontogenetic character displacement in mandibular morphology. This is tightly correlated with changes in feeding strategy, with changes to the cutting edges of mandibles increasing the efficiency of feeding. The changes in feeding strategy are also characterized by changes in feeding behaviour, with many larvae feeding gregariously in early instars. Non‐nutritive hypotheses considering the importance of natural enemies, shelter‐building and thermoregulation may also be invoked to explain the ontogenetic consequences of changes to feeding behaviour. There is a need to integrate these factors into a framework considering the gamut of potential explanations of insect herbivory, recognizing that ontogenetic constraints are not only viable explanations but a logical starting point. The interrelations between ontogeny, size, morphology and behaviour highlight the complexity of insect–plant relationships. Given the many methods used by insect herbivores to overcome the challenges of consuming foliage, the need for species‐specific and stage‐ specific research investigating ontogeny and host use by insect herbivores is critical for developing general theories of insect–plant interactions.

@article{doi101046j14429993200101135x,
    author = "Hochuli, Dieter F.",
    title = "Insect herbivory and ontogeny: How do growth and development influence feeding behaviour, morphology and host use?",
    year = "2001",
    journal = "Austral Ecology",
    abstract = "Abstract Herbivorous insects exploit many different plants and plant parts and often adopt different feeding strategies throughout their life cycle. The conceptual framework for investigating insect–plant interactions relies heavily on explanations invoking plant chemistry, neglecting a suite of competing and interacting pressures that may also limit herbivory. In the present paper, the methods by which ontogeny, feeding strategies and morphological characters inhibit herbivory by mandibulate holometabolous insects are examined. The emphasis on mechanical disruption of plant cells in the insect digestive strategy changes the relative importance of plant ‘defences’, increasing the importance of leaf structure in inhibiting herbivory. Coupled with the implications of substantial morphological and behavioural changes in ontogeny, herbivores adopt a range of approaches to herbivory that are independent of plant chemistry alone. Many insect herbivores exhibit substantial ontogenetic character displacement in mandibular morphology. This is tightly correlated with changes in feeding strategy, with changes to the cutting edges of mandibles increasing the efficiency of feeding. The changes in feeding strategy are also characterized by changes in feeding behaviour, with many larvae feeding gregariously in early instars. Non‐nutritive hypotheses considering the importance of natural enemies, shelter‐building and thermoregulation may also be invoked to explain the ontogenetic consequences of changes to feeding behaviour. There is a need to integrate these factors into a framework considering the gamut of potential explanations of insect herbivory, recognizing that ontogenetic constraints are not only viable explanations but a logical starting point. The interrelations between ontogeny, size, morphology and behaviour highlight the complexity of insect–plant relationships. Given the many methods used by insect herbivores to overcome the challenges of consuming foliage, the need for species‐specific and stage‐ specific research investigating ontogeny and host use by insect herbivores is critical for developing general theories of insect–plant interactions.",
    url = "https://doi.org/10.1046/j.1442-9993.2001.01135.x",
    doi = "10.1046/j.1442-9993.2001.01135.x",
    openalex = "W1819702572",
    references = "doi101007bf00317222"
}

@incollection{crossref2008engineering,
    title = "Engineering Photosynthetic Pathways",
    year = "2008",
    booktitle = "Advances in Plant Biochemistry and Molecular Biology",
    url = "https://doi.org/10.1016/s1755-0408(07)01004-1",
    doi = "10.1016/s1755-0408(07)01004-1",
    pages = "81-105"
}

Summary Despite their potential to provide a mechanistic understanding of ecosystem processes, the functional traits that govern interaction networks remain poorly understood. We investigated the extent to which biomechanical traits are related to consumption in a plant–grasshopper herbivory network. Using a choice experiment, we assessed the feeding patterns of 26 grasshopper species for 24 common plant species from subalpine grasslands. We quantified shear and punch toughness for each plant species, while grasshopper incisive and molar strengths were estimated by a lever mechanics model, following the measurement of mandibular traits. Models incorporating co‐phylogenetic effects showed that the ratio between the grasshopper incisive strength and plant toughness, that reflects the cutting effort, is correlated with the mass of plant eaten. Moreover, a strong relationship between the incisive strength of the grasshoppers and the weighed mean toughness of the plants they eat was found. Our results suggest that biomechanical constraints imposed by plants influence the evolution of grasshoppers' mandibular traits. Such scaling relationships offer promising avenues towards the understanding of trait – function links in interaction networks.

@article{doi1011111365243512058,
    author = "Ibanez, Sébastien and Lavorel, Sandra and Puijalon, Sara and Moretti, Marco",
    title = "Herbivory mediated by coupling between biomechanical traits of plants and grasshoppers",
    year = "2013",
    journal = "Functional Ecology",
    abstract = "Summary Despite their potential to provide a mechanistic understanding of ecosystem processes, the functional traits that govern interaction networks remain poorly understood. We investigated the extent to which biomechanical traits are related to consumption in a plant–grasshopper herbivory network. Using a choice experiment, we assessed the feeding patterns of 26 grasshopper species for 24 common plant species from subalpine grasslands. We quantified shear and punch toughness for each plant species, while grasshopper incisive and molar strengths were estimated by a lever mechanics model, following the measurement of mandibular traits. Models incorporating co‐phylogenetic effects showed that the ratio between the grasshopper incisive strength and plant toughness, that reflects the cutting effort, is correlated with the mass of plant eaten. Moreover, a strong relationship between the incisive strength of the grasshoppers and the weighed mean toughness of the plants they eat was found. Our results suggest that biomechanical constraints imposed by plants influence the evolution of grasshoppers' mandibular traits. Such scaling relationships offer promising avenues towards the understanding of trait – function links in interaction networks.",
    url = "https://doi.org/10.1111/1365-2435.12058",
    doi = "10.1111/1365-2435.12058",
    openalex = "W2079095306",
    references = "doi1023072425324"
}

C4 photosynthesis is characterized by a CO2-concentrating mechanism between mesophyll (M) and bundle sheath (BS) cells of leaves. This generates high metabolic fluxes between these cells, through interconnecting plasmodesmata (PD). Quantification of these symplastic fluxes for modeling studies requires accurate quantification of PD, which has proven difficult using transmission electron microscopy. Our new quantitative technique combines scanning electron microscopy and 3D immunolocalization in intact leaf tissues to compare PD density on cell interfaces in leaves of C3 (rice [Oryza sativa] and wheat [Triticum aestivum]) and C4 (maize [Zea mays] and Setaria viridis) monocot species. Scanning electron microscopy quantification of PD density revealed that C4 species had approximately twice the number of PD per pitfield area compared with their C3 counterparts. 3D immunolocalization of callose at pitfields using confocal microscopy showed that pitfield area per M-BS interface area was 5 times greater in C4 species. Thus, the two C4 species had up to nine times more PD per M-BS interface area (S. viridis, 9.3 PD µm(-2); maize, 7.5 PD µm(-2); rice 1.0 PD µm(-2); wheat, 2.6 PD µm(-2)). Using these anatomical data and measured photosynthetic rates in these C4 species, we have now calculated symplastic C4 acid flux per PD across the M-BS interface. These quantitative data are essential for modeling studies and gene discovery strategies needed to introduce aspects of C4 photosynthesis to C3 crops.

@article{doi101105tpc1600155,
    author = "Danila, Florence R. and Quick, W. Paul and White, Rosemary G. and Furbank, Robert T. and von Caemmerer, Susanne",
    title = "The Metabolite Pathway between Bundle Sheath and Mesophyll: Quantification of Plasmodesmata in Leaves of C 3 and C 4 Monocots",
    year = "2016",
    journal = "The Plant Cell",
    abstract = "C4 photosynthesis is characterized by a CO2-concentrating mechanism between mesophyll (M) and bundle sheath (BS) cells of leaves. This generates high metabolic fluxes between these cells, through interconnecting plasmodesmata (PD). Quantification of these symplastic fluxes for modeling studies requires accurate quantification of PD, which has proven difficult using transmission electron microscopy. Our new quantitative technique combines scanning electron microscopy and 3D immunolocalization in intact leaf tissues to compare PD density on cell interfaces in leaves of C3 (rice [Oryza sativa] and wheat [Triticum aestivum]) and C4 (maize [Zea mays] and Setaria viridis) monocot species. Scanning electron microscopy quantification of PD density revealed that C4 species had approximately twice the number of PD per pitfield area compared with their C3 counterparts. 3D immunolocalization of callose at pitfields using confocal microscopy showed that pitfield area per M-BS interface area was 5 times greater in C4 species. Thus, the two C4 species had up to nine times more PD per M-BS interface area (S. viridis, 9.3 PD µm(-2); maize, 7.5 PD µm(-2); rice 1.0 PD µm(-2); wheat, 2.6 PD µm(-2)). Using these anatomical data and measured photosynthetic rates in these C4 species, we have now calculated symplastic C4 acid flux per PD across the M-BS interface. These quantitative data are essential for modeling studies and gene discovery strategies needed to introduce aspects of C4 photosynthesis to C3 crops.",
    url = "https://doi.org/10.1105/tpc.16.00155",
    doi = "10.1105/tpc.16.00155",
    openalex = "W2409484068",
    references = "doi101071bi9710159"
}

Ecophysiologists have long been fascinated by the photosynthetic behaviour of alpine plants, which often have to withstand extreme environmental pressures (Gale, 1972; Friend & Woodward, 1990; Körner, 2003, 2007; Shi et al., 2006). About 8% of the world's land surface is above 1500 m altitude (Körner, 2007). High altitudes can be climatically unusual, often with (for example) low temperatures, strong winds, and now high rates of warming (Körner, 2003; Pepin & Lundquist, 2008; Rangwala & Miller, 2012). Moreover, the low atmospheric pressure provides a set of environmental conditions unique on Earth (Table 1). There has been extensive speculation about altitudinal effects on photosynthesis and, in particular, how to account for the puzzling – but consistently observed – tendencies towards higher carbon dioxide (CO2) drawdown (low ratio of leaf-internal to ambient CO2 partial pressures (ci: ca; hereafter, χ), resulting in low carbon isotope discrimination) and higher carboxylation capacity (Vcmax) with increasing altitude (Gale, 1972; Körner & Diemer, 1987; Friend et al., 1989; Terashima et al., 1995; Bresson et al., 2009; Zhu et al., 2010). At first glance, it might be expected that CO2 assimilation rates would be reduced at high altitudes due to the low partial pressure of CO2 (Friend & Woodward, 1990). However, actual measured photosynthetic rates are usually as high as, or even higher than, those at low altitudes (Mächler & Nösberger, 1977; Körner & Diemer, 1987; Cordell et al., 1999; Shi et al., 2006). One group of hypotheses that attempt to explain the effects of altitude on photosynthetic physiology focuses on the effects of low temperature. It has been argued that alpine plants possess thick leaves as an adaptation to low temperatures, and thus higher leaf nitrogen (N) on an area basis (Narea). Higher Narea is taken to imply higher Vcmax, in turn leading to higher CO2 drawdown due to higher photosynthetic rates (Woodward, 1979; Körner & Diemer, 1987; Friend et al., 1989; Sparks & Ehleringer, 1997). This reasoning assumes that higher Narea in thicker leaves would be associated with higher Vcmax, but this is not necessarily so, as a substantial fraction of leaf N in thick leaves (with low specific leaf area) is located in cell walls rather than in chloroplasts (Onoda et al., 2004). An alternative argument, from the perspective of carbon isotope discrimination, suggests that increased leaf thickness could lengthen the diffusional pathway for CO2 from the atmosphere to the site of carboxylation, and therefore potentially decrease χ (Vitousek et al., 1990). However, low air pressure would be expected to counteract this effect, by allowing CO2 to diffuse more readily through the stomata (Table 1). In any case, no hypothesis based on temperature effects can account for the difference in plant responses to altitudinal and latitudinal gradients, i.e. why the same adaptations in photosynthetic capacity observed on high mountains are not observed in polar regions where growing-season temperatures are also low (Billings et al., 1961; Mooney & Billings, 1961; Billings & Mooney, 1968; Chabot et al., 1972; Zhu et al., 2010). It is moreover worth noting that although low temperatures can depress photosynthesis, measured growing-season leaf temperatures and optimal temperatures for photosynthesis in both alpine and arctic plants are typically only reduced by a few degrees, in contrast with a much larger decline in air temperature with altitude or latitude (Körner & Diemer, 1987; Körner, 2007). The dense canopy structure and crowded leaf arrangement on stems of cushion and prostrate alpine plants create a low boundary-layer conductance and thus allow the maintenance of large differences between the temperatures of leaves and air (Gauslaa, 1984; Körner, 2003; Michaletz et al., 2015). The effect of such morphological adaptations is superimposed on the universal tendency, rooted in the fundamentals of leaf energy balance, for leaf temperatures to be maintained in a narrower range than air temperatures (Campbell & Norman, 1998; Michaletz et al., 2015). A further group of hypotheses suggests that low atmospheric pressure might influence photosynthesis through more direct physiological influences, independently of temperature (Decker, 1959; Billings et al., 1961; Mooney & Billings, 1961). However, despite much previous speculation, and the fact that many biophysical quantities relevant to gas exchange are known to change with air pressure and leaf temperature in a predictable manner (Table 1), effects of those biophysical quantities on plant physiology have not been fully explored. Misconceptions abound in the literature. For example, alpine plants were predicted to be more sensitive to the decreased CO2 concentration (molar mixing ratio) in the Quaternary glacial periods simply because the CO2 partial pressure at high altitudes is low (Street-Perrott et al., 1997). This is incorrect, however, because the partial pressure of O2 is also reduced at high altitudes – implying a reduced photorespiratory burden which counteracts the effect of CO2 concentration on photosynthesis, as previously noted, for example, by Körner et al. (1991) and Terashima et al. (1995). Natural selection implies that plants optimize ecophysiological traits by regulating the allocation of resources to different functions. This principle leads to the least-cost hypothesis and the coordination hypothesis for the optimal photosynthetic behaviour of C3 plants. These hypotheses can be incorporated into the standard (Farquhar et al., 1980) model, thereby potentially generating a unifying explanation and prediction of photosynthetic trait responses to environmental factors (Wang et al., 2016). The composite parameter ξ represents the sensitivity of χ to D and is influenced by both the cost terms. The mathematical form of Eqn 1 is the same as that proposed by Medlyn et al. (2011), which is based on a widely-cited stomatal optimality hypothesis stating that plants minimize E − λA (Cowan & Farquhar, 1977). However, the marginal cost of transpiration (λ) in that expression is not clearly defined. In the least-cost hypothesis, by contrast, the parameter ξ can be expressed explicitly as a function of the cost factors and the effective Michaelis–Menten coefficient of Rubisco (K), which is related to the partial pressure of O2 (O) and the Michaelis–Menten coefficients of Rubisco for CO2 and O2 (KC and KO). The temperature dependencies of KC and KO follow an Arrhenius relationship as described by Bernacchi et al. (2001) and this also gives rise to a temperature dependency of ξ (Prentice et al., 2014). The leaf-to-air VPD (D) is the difference between the vapour pressure in the intercellular spaces and the vapour pressure in the free air beyond the leaf boundary layer. The intercellular vapour pressure is usually assumed to be saturated and is determined by the leaf temperature. The free-air vapour pressure is the actual vapour pressure, which depends on the molar mixing ratio of water vapour in the air and on the atmospheric pressure. The conductance for gas exchange between leaves and air that corresponds to this vapour pressure gradient is composed of stomatal conductance and boundary-layer conductance in series. The boundary-layer conductance is generally many times larger than the stomatal conductance, so differences among leaves in boundary-layer conductance can be compensated by changes in stomatal conductance, allowing the maintenance of optimal χ. By introducing the known altitudinal responses of various key biophysical quantities, we show here how the partial responses of χ, Vcmax and A to atmospheric pressure and leaf temperature along the altitude gradient can be predicted from the equations mentioned earlier. Moreover, these predictions appear to be consistent with the field observed altitudinal trends in χ, Vcmax and A (Table 2; Fig. 1). To separate the effects of pressure and temperature, and also to cover a realistic leaf temperature variation along altitude gradients, we start by listing 10 potential influences of atmospheric pressure on plant physiological processes under constant leaf temperature, which may be a reasonable approximation for herbaceous plants as discussed earlier. Then we impose the additional effects of temperature, assuming that leaf temperature declines with altitude but follows a lapse rate shallower than air temperature due to the general homoeostatic tendency of leaf temperatures (Campbell & Norman, 1998; Michaletz et al., 2015). This approach may be realistic for tree species, whose leaves are situated well above the ground and subject to a potentially high wind speed, and therefore cannot be expected to maintain leaf temperatures near-constant with altitude (Table 1). Among the listed biophysical quantities, VPD and K are key variables predicting an altitudinal response of χ (Eqns 1, 2), whereas Γ*, ca, and PPFD impose further effects on Vcmax and A (Eqns 4, 5). With a constant leaf temperature, the pressure-induced decrease in K and enhancement of D both lead to a lower χ for alpine plants (Eqns 1, 2). As indicated in Table 1, K declines with altitude, due to the reduced partial pressure of O2, thereby increasing the affinity of Rubisco for CO2 and reducing the carboxylation capacity required per mole of carbon fixed (Bresson et al., 2009). However, for a given molar mixing ratio of water vapour to air, lowered atmospheric pressure leads to reduced actual vapour pressure. As the saturated leaf-internal vapour pressure is invariant with atmospheric pressure, this reduction tends to increase leaf-to-air VPD, thereby increasing the water transport required per mole of carbon fixed. According to the least-cost hypothesis, both effects support a shift in the investment of resources towards increased Rubisco capacity and against water transport capacity (Wang et al., 2016). The predicted outcome of a lowered χ with atmospheric pressure can be shown mathematically by differentiation of the expression for optimal χ, which shows that the partial response of χ to decreasing atmospheric pressure is always negative (Supporting Information Notes S1). Our predicted response of χ to pressure is consistent with observations by Körner & Diemer (1987) where leaf temperature was shown to vary only a few degrees (Table 2). After superimposing temperature effects, declining leaf temperature reduces the saturated vapour pressure, and thus decreases the leaf-to-air VPD – leading to a lower cost of water transport, opposite to the effect of air pressure. However, the declining leaf temperature still reduces K and this has the stronger influence, favouring a decline in χ (Table 1). By separating altitudinal and latitudinal trends, Körner et al. (1991) showed that aside from the effect of pressure, lower temperature reduces χ, potentially reinforcing the decline of χ with altitude. The leaf-internal partial pressure of CO2, ci, is the product of χ and ca. Although ci declines with altitude due to declines in both ca and χ, this does not automatically imply an increased limitation of CO2 on photosynthesis. This is because CO2 limitation is also determined by the CO2 compensation point (Γ*), as shown by Eqn 4. If a constant leaf temperature is assumed, Γ* is proportional to the O2 partial pressure and thus changes in proportion to ca (Farquhar et al., 1980) (Table 1). Consequently, a stronger CO2 limitation due to the reduction in χ (not due to ca or Γ*) is expected for alpine plants. After imposing a temperature effect, the decline in Γ*, following an Arrhenius relationship (Bernacchi et al., 2001), is much faster than that of χ (Table 1) and this leads to a weaker CO2 limitation on photosynthesis. It has been suggested that photosynthesis might be influenced by the more rapid diffusion of gases in air at lower pressure (Table 1) (Gale, 1972; Smith & Donahue, 1991; Terashima et al., 1995). We might therefore predict that the consequence of more rapid gaseous diffusion at high altitudes would be a reduction in stomatal density and/or diameter. In reality, both positive (Wagner, 1892; Bonnier, 1895; Paridari et al., 2013) and negative (Körner et al., 1983) responses of stomatal density to altitude increase have been reported, suggesting that some other environmental factors or morphological adaptations might also be involved in determining stomatal density (Körner et al., 1986; Friend & Woodward, 1990). According to the least-cost hypothesis, a relatively lower cost of maintaining carboxylation due to increased affinity to CO2 (lower K) in turn implies an increased Vcmax, as required (by the coordination hypothesis) to achieve an optimal assimilation rate that is set by PPFD. Mathematically, the sensitivity of Vcmax to air pressure based on Eqn 2 (Notes S1) shows that the response is always positive provided K ≫ Γ*. In this response, either enhanced PPFD on clear days or reduced ci is a secondary contributor to the positive response of Vcmax to altitude, whereas the decline in K is the main contributor – being about three times larger than the other contributions. Reduced leaf temperature superimposes a negative effect on Vcmax, which is opposite to the positive effect of pressure decline. This can also be theoretically predicted by the ‘kinetic’ response of biochemical rate parameters (Kc, Ko and Γ*) to temperature and is supported by field observations (Dong et al., 2016). Our predictions are supported by previous observations (Table 2; Fig. 1). Quantitative comparison with Körner & Diemer (1987) is possible because this study reported all of the relevant environmental variables (in addition to altitude) that would be expected theoretically to influence χ and Vcmax (Table 2). Our literature search revealed a number of other studies of altitude effects (Fig. 1) but it was not generally possible to exclude other effects, for example, of changes in leaf temperature or cloudiness (it is worth noting that Körner & Diemer (1987) reported negligible changes in leaf temperature). Therefore, the observed changes in Vcmax are variable (Shi et al., 2006; Fan et al., 2011), but nonetheless consistent with our predicted range (Fig. 1). The coordination hypothesis also allows prediction of the sensitivity of the assimilation rate A to air pressure through Eqn 4 (Notes S1). Table 1 shows how much each pressure-dependent quantity contributes to changes in A under defined reference conditions. The increased diffusion coefficients for water vapour and CO2 may physically affect how stomatal regulation achieves the optimal χ, but should not influence its value, nor the value of A. As discussed earlier, the opposite effects of the declining O2 and CO2 partial pressures approximately cancel each other. Therefore, the sensitivity of A to altitude depends on the competition between the negative effect of reduced χ and the positive effects of enhanced PPFD, due to a shorter path length (enhanced clear-sky transmittivity), and reduced Γ* if leaf temperature declines. Therefore, either a negative or a positive response of A can be expected, depending on the conditions. Referring again to the study by Körner & Diemer (1987), as altitude increases from 600 m to 2600 m, PPFD is predicted to increase by 5.4%, as observed (Table 2). Our predicted change in A is only 0.4%, and Körner & Diemer (1987) reported no significant change (Table 2). Bresson et al. (2009) also found no significant change in A with altitude, while measurements made at constant (low-elevation) CO2 partial pressure showed a consistent increase; this is in line with our prediction of increasing Vcmax with altitude. Bresson et al. (2009) also found increasing Narea with altitude, which is to be expected, given increasing Vcmax. In principle, photosynthesis could be enhanced at high altitudes, if the benefit from increased radiation and reduced photorespiration were to overcome the effect of the reduction of ci. However, reduced photorespiration relies on a reduction in leaf temperature, whereas radiation is also influenced by cloud cover, which in reality can decrease or increase with altitude, depending on latitude and continentality (Barry, 1992). Thus a diversity of trends might be found in a wider sampling of altitudinal gradients in different plant types and climatic regions. Nevertheless, the theoretical analysis presented here provides a first-order explanation for some commonly observed trends in photosynthetic traits along altitudinal gradients. The explanation is derived from a proposed general model to predict photosynthetic rates via eco-evolutionary optimization of photosynthetic traits (Wang et al., 2016). By disentangling the effects of pressure and temperature on a number of variables influencing leaf-level gas exchange, we show that both declining χ and increasing Vcmax can be predicted by air pressure change alone, while superimposed temperature effects typically modify the magnitude of the responses – accounting for why these trends in χ and Vcmax have been so widely observed. The authors thank Vincent Maire for discussions. This research was supported by the National Natural Science Foundation of China (Grant no. 31600388) to H.W. and by an Australian Research Council Discovery grant (DP120103600) to I.C.P. and I.J.W. It represents a contribution to the AXA Chair Programme in Biosphere and Climate Impacts and the Imperial College initiative on Grand Challenges in Ecosystems and the Environment. T.F.K. was supported in part by the Laboratory Directed Research and Development Programme of Lawrence Berkeley National Laboratory under US Department of Energy (Contract no. DE-AC02-05CH11231), and by a Macquarie University research fellowship. H.W. and I.C.P. derived the predictions. H.W. carried out all the analyses, constructed the figures and tables, and wrote the first draft. H.W., I.C.P., T.F.K., I.J.W., T.W.D. and C.P contributed to subsequent drafts. H.W., T.W.D. and I.C.P. summarized altitudinal dependences of gas exchange and various relevant biophysical quantities. I.C.P. and T.F.K contributed to the data analysis. I.J.W. first proposed the least-cost theory, and I.C.P further developed the theory. Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

@article{doi101111nph14332,
    author = "Wang, Han and Prentice, I. Colin and Davis, T. W. and Keenan, Trevor F. and Wright, Ian J. and Peng, Changhui",
    title = "Photosynthetic responses to altitude: an explanation based on optimality principles",
    year = "2016",
    journal = "New Phytologist",
    abstract = "Ecophysiologists have long been fascinated by the photosynthetic behaviour of alpine plants, which often have to withstand extreme environmental pressures (Gale, 1972; Friend \& Woodward, 1990; Körner, 2003, 2007; Shi et al., 2006). About 8\% of the world's land surface is above 1500 m altitude (Körner, 2007). High altitudes can be climatically unusual, often with (for example) low temperatures, strong winds, and now high rates of warming (Körner, 2003; Pepin \& Lundquist, 2008; Rangwala \& Miller, 2012). Moreover, the low atmospheric pressure provides a set of environmental conditions unique on Earth (Table 1). There has been extensive speculation about altitudinal effects on photosynthesis and, in particular, how to account for the puzzling – but consistently observed – tendencies towards higher carbon dioxide (CO2) drawdown (low ratio of leaf-internal to ambient CO2 partial pressures (ci: ca; hereafter, χ), resulting in low carbon isotope discrimination) and higher carboxylation capacity (Vcmax) with increasing altitude (Gale, 1972; Körner \& Diemer, 1987; Friend et al., 1989; Terashima et al., 1995; Bresson et al., 2009; Zhu et al., 2010). At first glance, it might be expected that CO2 assimilation rates would be reduced at high altitudes due to the low partial pressure of CO2 (Friend \& Woodward, 1990). However, actual measured photosynthetic rates are usually as high as, or even higher than, those at low altitudes (Mächler \& Nösberger, 1977; Körner \& Diemer, 1987; Cordell et al., 1999; Shi et al., 2006). One group of hypotheses that attempt to explain the effects of altitude on photosynthetic physiology focuses on the effects of low temperature. It has been argued that alpine plants possess thick leaves as an adaptation to low temperatures, and thus higher leaf nitrogen (N) on an area basis (Narea). Higher Narea is taken to imply higher Vcmax, in turn leading to higher CO2 drawdown due to higher photosynthetic rates (Woodward, 1979; Körner \& Diemer, 1987; Friend et al., 1989; Sparks \& Ehleringer, 1997). This reasoning assumes that higher Narea in thicker leaves would be associated with higher Vcmax, but this is not necessarily so, as a substantial fraction of leaf N in thick leaves (with low specific leaf area) is located in cell walls rather than in chloroplasts (Onoda et al., 2004). An alternative argument, from the perspective of carbon isotope discrimination, suggests that increased leaf thickness could lengthen the diffusional pathway for CO2 from the atmosphere to the site of carboxylation, and therefore potentially decrease χ (Vitousek et al., 1990). However, low air pressure would be expected to counteract this effect, by allowing CO2 to diffuse more readily through the stomata (Table 1). In any case, no hypothesis based on temperature effects can account for the difference in plant responses to altitudinal and latitudinal gradients, i.e. why the same adaptations in photosynthetic capacity observed on high mountains are not observed in polar regions where growing-season temperatures are also low (Billings et al., 1961; Mooney \& Billings, 1961; Billings \& Mooney, 1968; Chabot et al., 1972; Zhu et al., 2010). It is moreover worth noting that although low temperatures can depress photosynthesis, measured growing-season leaf temperatures and optimal temperatures for photosynthesis in both alpine and arctic plants are typically only reduced by a few degrees, in contrast with a much larger decline in air temperature with altitude or latitude (Körner \& Diemer, 1987; Körner, 2007). The dense canopy structure and crowded leaf arrangement on stems of cushion and prostrate alpine plants create a low boundary-layer conductance and thus allow the maintenance of large differences between the temperatures of leaves and air (Gauslaa, 1984; Körner, 2003; Michaletz et al., 2015). The effect of such morphological adaptations is superimposed on the universal tendency, rooted in the fundamentals of leaf energy balance, for leaf temperatures to be maintained in a narrower range than air temperatures (Campbell \& Norman, 1998; Michaletz et al., 2015). A further group of hypotheses suggests that low atmospheric pressure might influence photosynthesis through more direct physiological influences, independently of temperature (Decker, 1959; Billings et al., 1961; Mooney \& Billings, 1961). However, despite much previous speculation, and the fact that many biophysical quantities relevant to gas exchange are known to change with air pressure and leaf temperature in a predictable manner (Table 1), effects of those biophysical quantities on plant physiology have not been fully explored. Misconceptions abound in the literature. For example, alpine plants were predicted to be more sensitive to the decreased CO2 concentration (molar mixing ratio) in the Quaternary glacial periods simply because the CO2 partial pressure at high altitudes is low (Street-Perrott et al., 1997). This is incorrect, however, because the partial pressure of O2 is also reduced at high altitudes – implying a reduced photorespiratory burden which counteracts the effect of CO2 concentration on photosynthesis, as previously noted, for example, by Körner et al. (1991) and Terashima et al. (1995). Natural selection implies that plants optimize ecophysiological traits by regulating the allocation of resources to different functions. This principle leads to the least-cost hypothesis and the coordination hypothesis for the optimal photosynthetic behaviour of C3 plants. These hypotheses can be incorporated into the standard (Farquhar et al., 1980) model, thereby potentially generating a unifying explanation and prediction of photosynthetic trait responses to environmental factors (Wang et al., 2016). The composite parameter ξ represents the sensitivity of χ to D and is influenced by both the cost terms. The mathematical form of Eqn 1 is the same as that proposed by Medlyn et al. (2011), which is based on a widely-cited stomatal optimality hypothesis stating that plants minimize E − λA (Cowan \& Farquhar, 1977). However, the marginal cost of transpiration (λ) in that expression is not clearly defined. In the least-cost hypothesis, by contrast, the parameter ξ can be expressed explicitly as a function of the cost factors and the effective Michaelis–Menten coefficient of Rubisco (K), which is related to the partial pressure of O2 (O) and the Michaelis–Menten coefficients of Rubisco for CO2 and O2 (KC and KO). The temperature dependencies of KC and KO follow an Arrhenius relationship as described by Bernacchi et al. (2001) and this also gives rise to a temperature dependency of ξ (Prentice et al., 2014). The leaf-to-air VPD (D) is the difference between the vapour pressure in the intercellular spaces and the vapour pressure in the free air beyond the leaf boundary layer. The intercellular vapour pressure is usually assumed to be saturated and is determined by the leaf temperature. The free-air vapour pressure is the actual vapour pressure, which depends on the molar mixing ratio of water vapour in the air and on the atmospheric pressure. The conductance for gas exchange between leaves and air that corresponds to this vapour pressure gradient is composed of stomatal conductance and boundary-layer conductance in series. The boundary-layer conductance is generally many times larger than the stomatal conductance, so differences among leaves in boundary-layer conductance can be compensated by changes in stomatal conductance, allowing the maintenance of optimal χ. By introducing the known altitudinal responses of various key biophysical quantities, we show here how the partial responses of χ, Vcmax and A to atmospheric pressure and leaf temperature along the altitude gradient can be predicted from the equations mentioned earlier. Moreover, these predictions appear to be consistent with the field observed altitudinal trends in χ, Vcmax and A (Table 2; Fig. 1). To separate the effects of pressure and temperature, and also to cover a realistic leaf temperature variation along altitude gradients, we start by listing 10 potential influences of atmospheric pressure on plant physiological processes under constant leaf temperature, which may be a reasonable approximation for herbaceous plants as discussed earlier. Then we impose the additional effects of temperature, assuming that leaf temperature declines with altitude but follows a lapse rate shallower than air temperature due to the general homoeostatic tendency of leaf temperatures (Campbell \& Norman, 1998; Michaletz et al., 2015). This approach may be realistic for tree species, whose leaves are situated well above the ground and subject to a potentially high wind speed, and therefore cannot be expected to maintain leaf temperatures near-constant with altitude (Table 1). Among the listed biophysical quantities, VPD and K are key variables predicting an altitudinal response of χ (Eqns 1, 2), whereas Γ*, ca, and PPFD impose further effects on Vcmax and A (Eqns 4, 5). With a constant leaf temperature, the pressure-induced decrease in K and enhancement of D both lead to a lower χ for alpine plants (Eqns 1, 2). As indicated in Table 1, K declines with altitude, due to the reduced partial pressure of O2, thereby increasing the affinity of Rubisco for CO2 and reducing the carboxylation capacity required per mole of carbon fixed (Bresson et al., 2009). However, for a given molar mixing ratio of water vapour to air, lowered atmospheric pressure leads to reduced actual vapour pressure. As the saturated leaf-internal vapour pressure is invariant with atmospheric pressure, this reduction tends to increase leaf-to-air VPD, thereby increasing the water transport required per mole of carbon fixed. According to the least-cost hypothesis, both effects support a shift in the investment of resources towards increased Rubisco capacity and against water transport capacity (Wang et al., 2016). The predicted outcome of a lowered χ with atmospheric pressure can be shown mathematically by differentiation of the expression for optimal χ, which shows that the partial response of χ to decreasing atmospheric pressure is always negative (Supporting Information Notes S1). Our predicted response of χ to pressure is consistent with observations by Körner \& Diemer (1987) where leaf temperature was shown to vary only a few degrees (Table 2). After superimposing temperature effects, declining leaf temperature reduces the saturated vapour pressure, and thus decreases the leaf-to-air VPD – leading to a lower cost of water transport, opposite to the effect of air pressure. However, the declining leaf temperature still reduces K and this has the stronger influence, favouring a decline in χ (Table 1). By separating altitudinal and latitudinal trends, Körner et al. (1991) showed that aside from the effect of pressure, lower temperature reduces χ, potentially reinforcing the decline of χ with altitude. The leaf-internal partial pressure of CO2, ci, is the product of χ and ca. Although ci declines with altitude due to declines in both ca and χ, this does not automatically imply an increased limitation of CO2 on photosynthesis. This is because CO2 limitation is also determined by the CO2 compensation point (Γ*), as shown by Eqn 4. If a constant leaf temperature is assumed, Γ* is proportional to the O2 partial pressure and thus changes in proportion to ca (Farquhar et al., 1980) (Table 1). Consequently, a stronger CO2 limitation due to the reduction in χ (not due to ca or Γ*) is expected for alpine plants. After imposing a temperature effect, the decline in Γ*, following an Arrhenius relationship (Bernacchi et al., 2001), is much faster than that of χ (Table 1) and this leads to a weaker CO2 limitation on photosynthesis. It has been suggested that photosynthesis might be influenced by the more rapid diffusion of gases in air at lower pressure (Table 1) (Gale, 1972; Smith \& Donahue, 1991; Terashima et al., 1995). We might therefore predict that the consequence of more rapid gaseous diffusion at high altitudes would be a reduction in stomatal density and/or diameter. In reality, both positive (Wagner, 1892; Bonnier, 1895; Paridari et al., 2013) and negative (Körner et al., 1983) responses of stomatal density to altitude increase have been reported, suggesting that some other environmental factors or morphological adaptations might also be involved in determining stomatal density (Körner et al., 1986; Friend \& Woodward, 1990). According to the least-cost hypothesis, a relatively lower cost of maintaining carboxylation due to increased affinity to CO2 (lower K) in turn implies an increased Vcmax, as required (by the coordination hypothesis) to achieve an optimal assimilation rate that is set by PPFD. Mathematically, the sensitivity of Vcmax to air pressure based on Eqn 2 (Notes S1) shows that the response is always positive provided K ≫ Γ*. In this response, either enhanced PPFD on clear days or reduced ci is a secondary contributor to the positive response of Vcmax to altitude, whereas the decline in K is the main contributor – being about three times larger than the other contributions. Reduced leaf temperature superimposes a negative effect on Vcmax, which is opposite to the positive effect of pressure decline. This can also be theoretically predicted by the ‘kinetic’ response of biochemical rate parameters (Kc, Ko and Γ*) to temperature and is supported by field observations (Dong et al., 2016). Our predictions are supported by previous observations (Table 2; Fig. 1). Quantitative comparison with Körner \& Diemer (1987) is possible because this study reported all of the relevant environmental variables (in addition to altitude) that would be expected theoretically to influence χ and Vcmax (Table 2). Our literature search revealed a number of other studies of altitude effects (Fig. 1) but it was not generally possible to exclude other effects, for example, of changes in leaf temperature or cloudiness (it is worth noting that Körner \& Diemer (1987) reported negligible changes in leaf temperature). Therefore, the observed changes in Vcmax are variable (Shi et al., 2006; Fan et al., 2011), but nonetheless consistent with our predicted range (Fig. 1). The coordination hypothesis also allows prediction of the sensitivity of the assimilation rate A to air pressure through Eqn 4 (Notes S1). Table 1 shows how much each pressure-dependent quantity contributes to changes in A under defined reference conditions. The increased diffusion coefficients for water vapour and CO2 may physically affect how stomatal regulation achieves the optimal χ, but should not influence its value, nor the value of A. As discussed earlier, the opposite effects of the declining O2 and CO2 partial pressures approximately cancel each other. Therefore, the sensitivity of A to altitude depends on the competition between the negative effect of reduced χ and the positive effects of enhanced PPFD, due to a shorter path length (enhanced clear-sky transmittivity), and reduced Γ* if leaf temperature declines. Therefore, either a negative or a positive response of A can be expected, depending on the conditions. Referring again to the study by Körner \& Diemer (1987), as altitude increases from 600 m to 2600 m, PPFD is predicted to increase by 5.4\%, as observed (Table 2). Our predicted change in A is only 0.4\%, and Körner \& Diemer (1987) reported no significant change (Table 2). Bresson et al. (2009) also found no significant change in A with altitude, while measurements made at constant (low-elevation) CO2 partial pressure showed a consistent increase; this is in line with our prediction of increasing Vcmax with altitude. Bresson et al. (2009) also found increasing Narea with altitude, which is to be expected, given increasing Vcmax. In principle, photosynthesis could be enhanced at high altitudes, if the benefit from increased radiation and reduced photorespiration were to overcome the effect of the reduction of ci. However, reduced photorespiration relies on a reduction in leaf temperature, whereas radiation is also influenced by cloud cover, which in reality can decrease or increase with altitude, depending on latitude and continentality (Barry, 1992). Thus a diversity of trends might be found in a wider sampling of altitudinal gradients in different plant types and climatic regions. Nevertheless, the theoretical analysis presented here provides a first-order explanation for some commonly observed trends in photosynthetic traits along altitudinal gradients. The explanation is derived from a proposed general model to predict photosynthetic rates via eco-evolutionary optimization of photosynthetic traits (Wang et al., 2016). By disentangling the effects of pressure and temperature on a number of variables influencing leaf-level gas exchange, we show that both declining χ and increasing Vcmax can be predicted by air pressure change alone, while superimposed temperature effects typically modify the magnitude of the responses – accounting for why these trends in χ and Vcmax have been so widely observed. The authors thank Vincent Maire for discussions. This research was supported by the National Natural Science Foundation of China (Grant no. 31600388) to H.W. and by an Australian Research Council Discovery grant (DP120103600) to I.C.P. and I.J.W. It represents a contribution to the AXA Chair Programme in Biosphere and Climate Impacts and the Imperial College initiative on Grand Challenges in Ecosystems and the Environment. T.F.K. was supported in part by the Laboratory Directed Research and Development Programme of Lawrence Berkeley National Laboratory under US Department of Energy (Contract no. DE-AC02-05CH11231), and by a Macquarie University research fellowship. H.W. and I.C.P. derived the predictions. H.W. carried out all the analyses, constructed the figures and tables, and wrote the first draft. H.W., I.C.P., T.F.K., I.J.W., T.W.D. and C.P contributed to subsequent drafts. H.W., T.W.D. and I.C.P. summarized altitudinal dependences of gas exchange and various relevant biophysical quantities. I.C.P. and T.F.K contributed to the data analysis. I.J.W. first proposed the least-cost theory, and I.C.P further developed the theory. Please note: Wiley Blackwell are not responsible for the content or functionality of any Supporting Information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.",
    url = "https://doi.org/10.1111/nph.14332",
    doi = "10.1111/nph.14332",
    openalex = "W2549259980",
    references = "doi1023071934239"
}

@incollection{crossref2021photosynthetic,
    title = "Photosynthetic Pathways",
    year = "2021",
    booktitle = "Encyclopedic Dictionary of Archaeology",
    url = "https://doi.org/10.1007/978-3-030-58292-0\_160489",
    doi = "10.1007/978-3-030-58292-0\_160489",
    pages = "1047-1047"
}