Ecology. Michael Begon

of the overall process of carbon fixation does not change with temperature. Finally, the concentration of RuBisCO in the leaves is a third to a sixth of that in C₃ plants, and the leaf nitrogen content is correspondingly lower. As a consequence of this, C₄ plants are much less attractive to many herbivores and also achieve more photosynthesis per unit of nitrogen absorbed.

      It may seem surprising that C₄ plants, with such high water‐use efficiency, have failed to dominate the vegetation of the world, but there are clear costs to set against the gains. The C₄ system has a high light compensation point and is inefficient at low light intensities; C₄ species are therefore ineffective as shade plants. Moreover, C₄ plants have higher temperature optima for growth than C₃ species: most C₄ plants are found in arid regions or the tropics. The pathway is widely distributed amongst plant families but is most prominent in grasses, where many of the attempts to account for the distributions of C₃ and C₄ species have been focused.

The most common approach to understanding the proportion of C₃ and C₄ plants in any region goes back to Collatz et al. (1998). It involves the identification of a climatological crossover temperature, above and below which C₄ and C₃ plants, respectively, are favoured – that is, they have a carbon gain advantage – and also a level of precipitation sufficient for plants of both types to grow. Collatz et al. estimated these for grasses to be a mean daytime temperature of 22°C and precipitation of at least 25 mm per month. Then, for example, the number of months in the year typically favouring C₄ growth may be used to account, statistically, for the proportion of C₄ grasses in a local flora. Subsequent refinements of the approach have re‐estimated those growth criteria or acknowledged the importance of factors beyond temperature and precipitation. Thus, for instance, Griffith et al. (2015) explored a range of mean, minimum and maximum monthly temperatures for grasses in the USA and then found that the best fitting model was based on exceeding a monthly maximum temperature of 27°C, not a mean of 22°C (but still a mean monthly precipitation ≥25 mm; Figure 3.17). However, while this combination of temperature and precipitation thresholds was powerful in accounting for the distribution of C₄ grasses, in a number of regions, further factors were also important. In the Eastern Temperate Forest region, for example, there was a strong negative effect of tree cover on the proportion of C₄ grasses, since their shade promotes the cooler growing conditions more favourable to C₃ grasses; while in the Temperate US Sierras, there was a strong negative effect of mean annual precipitation, though whether this is favourable to C₃ grasses, unfavourable to C₄ grasses, or favourable to other plants that increase shading is uncertain.

Figure 3.17 Effects of temperature and precipitation on the proportional contributions of C₃and C₄grasses to the floras of various regions of the USA, as indicated. Data were collected from sampling plots within each region, with their location marked as dots on the map, and these data are shown as symmetrical ‘density curves’, associated with the number of months at each location where conditions exceeded the estimated temperature‐precipitation threshold (to the nearest month). The solid line is the predicted median proportion derived from a ‘quantile regression’ based on the temperature–precipitation threshold.

      Source: After Griffith et al. (2015).

      the CAM pathway

      Plants with a CAM pathway also use PEP carboxylase with its strong power of concentrating CO₂. (The system is now known in a wide variety of families, not just the Crassulaceae.) In contrast to C₃ and C₄ plants, though, CAM plants open their stomata and fix CO₂ at night (as malic acid). During the daytime the stomata are closed and the CO₂ is released within the leaf and fixed by RuBisCO. However, because the CO₂ is then at a high concentration within the leaf, photorespiration is prevented, just as it is in plants using the C₄ pathway. Plants using the CAM photosynthetic pathway have obvious advantages when water is in short supply, because their stomata are closed during the daytime when evaporative forces are strongest. This appears to be a highly effective means of water conservation – water use efficiency for CAM plants is estimated to be around three times greater than for C₄ plants and more than six times greater than for C₃ plants (Borland et al., 2009) – but CAM species have not come to inherit the earth. One cost to CAM plants is the problem of storing the malic acid that is formed at night: most CAM plants are succulents with extensive water‐storage tissues that cope with this problem. In general, CAM plants are found in arid environments where strict stomatal control of daytime water is vital for survival (desert succulents), and in habitats where CO₂ is in short supply during the daytime, for example in some submerged aquatic plants, and in photosynthetic organs that lack stomata (e.g. the aerial photosynthetic roots of orchids).

      APPLICATION 3.2 Turning to CAM crops

The high water use efficiency of CAM plants makes them excellent candidates for cultivation over areas where rainfall is too little or evapotranspiration too high for the cultivation of C₃ or C₄ crops. Such areas may well expand in future. Examples include the production of pineapple, Ananas comosus, for consumption, of Opuntia spp. for animal fodder, of sisal, Agave sisalana, for fibre, and of Agave tequilana for the alcoholic beverages tequila and mescal (Borland et al., 2009). In addition, species of Agave are grown for both liquid and gaseous biofuels and indeed other products such as enzymes and lactic and succinic acid (Perez‐Pimienta et al., 2017). Current quantities grown are small compared with the most common alternatives based around corn, sugar cane and wheat, and most of this is in Mexico. However, the much greater productivity of Agave (Figure 3.18), and the high water use efficiency it derives from its CAM metabolism, highlights its great potential for the future.

Figure 3.18 Agave species (CAM plants) exhibit high productivity due to their high water use efficiency. Comparison of the productivities of various species of Agave (double entries reflect separate studies) and four selected bioenergy feedstocks (raw products for the production of biofuels). Corn stover consists of the remains of plants left in the field after corn (Zea mays) has been harvested. Sugarcane bagasse is the fibrous matter than remains after sugarcane (Saccharum spp.) has been crushed to extract its juice.

      Source: After Perez‐Pimienta et al. (2017).

      APPLICATION 3.3 Genetic engineering of CCMs into crops

Another way to exploit the potential of CAM would be to engineer its molecular machinery into C₃ plants (Borland et al., 2014). Indeed there is great interest in general in engineering a wider range of CCMs, taken from C₄ plants and from microbes, into commercial crops. Complex metabolic alternatives, such as CAM, typically require a whole suite of co‐adapted changes, and implementing them will therefore be a massive challenge. However, promising results may be obtained from less ambitious approaches. Figure 3.19, for example, illustrates the results when the photosynthetic rate of a standard variety of