CAM PHOTOSYNTHESIS IN SUBMERGED AQUATIC PLANTS

Crassulacean acid metabolism (CAM) is a CO2-concentrating mechanism se lected in response to aridity in terrestrial habitats, and, in aquatic environments, to ambient limitations of carbon. Evidence is reviewed for its presence in five genera of aquatic vascular plants, including Isoetes, Sagittaria, Vallisneria, Crassula, and Littorella. Initially, aquatic CAM was considered by some to be an oxymoron, but some aquati c species have been studied in sufficient detail to say definitively t hat they possess CAM photosynthesis. CO2-concentrating mechanisms in p hotosynthetic organs require a barrier to leakage; e.g., terrestrial C -4 plants have suberized bundle sheath cells and terrestrial CAM plant s high stomatal resistance. In aquatic CAM plants the primary barrier to CO2 leakage is the extremely high diffusional resistance of water. This, coupled with the sink provided by extensive intercellular gas sp ace, generates daytime CO2(p(i)) comparable to terrestrial CAM plants. CAM contributes to the carbon budget by both net carbon gain and carb on recycling, and the magnitude of each is environmentally influenced. Aquatic CAM plants inhabit sites where photosynthesis is potentially limited by carbon. Many occupy moderately fertile shallow temporary po ols that experience extreme diel fluctuations in carbon availability. CAM plants are able to take advantage of elevated nighttime CO2 levels in these habitats. This gives them a competitive advantage over non-C AM species that are carbon starved during the day and an advantage ove r species that expend energy in membrane transport of bicarbonate. Som e aquatic CAM plants are distributed in highly infertile lakes, where extreme carbon limitation and light are important selective factors. C ompilation of reports on diel changes in titratable acidity and malate show 69 out of 180 species have significant overnight accumulation, a lthough evidence is presented discounting CAM in some. It is concluded that similar proportions of the aquatic and terrestrial floras have e volved CAM photosynthesis. Aquatic Isoetes (Lycophyta) represent the o ldest lineage of CAM plants and cladistic analysis supports an origin for CAM in seasonal wetlands, from which it has radiated into oligotro phic lakes and into terrestrial habitats. Temperate Zone terrestrial s pecies share many characteristics with amphibious ancestors, which in their temporary terrestrial stage, produce functional stomata and swit ch from CAM to C-3 Many lacustrine Isoetes have retained the phenotypi c plasticity of amphibious species and can adapt to an aerial environm ent by development of stomata and switching to C3 However, in some neo tropical alpine species, adaptations to the lacustrine environment are genetically fixed and these constitutive species fail to produce stom ata or loose CAM when artificially maintained in an aerial environment . It is hypothesized that neotropical lacustrine species may be more a ncient in origin and have given rise to terrestrial species, which hav e retained most of the characteristics of their aquatic ancestry, incl uding astomatous leaves, CAM and sediment-based carbon nutrition. In b oth terrestrial and aquatic CAM plants, dark CO2 fixation may result i n net carbon uptake plus the conservation of carbon by refixation of r espiratory CO2. In aquatic plants, CAM's contribution to the total car bon budget is variable. Exemplary studies of the contribution of CAM t o the carbon budget, such as those by Boston and Adams, Madsen, and Ro be and Griffiths for lacustrine species, are needed in a greater range of habitats. Quantitative estimates of the CAM contribution to the ca rbon budget are likely to provide more insights than attempts to typol ogically categorize variation with terms such as ''idling,'' ''cycling ,'' AAM, SCAM, TAAM, and so forth. Although we have a reasonably good understanding of the selective factors favoring CAM in seasonal pools and oligotrophic lakes, there are other habitats (Section VII.C) where the role of CAM is not apparent. These species need to be examined in greater detail. Future research should focus on species with predicta ble diel acid fluctuations, but with characteristics that do not fit r ecognized criteria for CAM. Of particular interest is the seasonal poo l species Downingia bella (Campanulaceae), which may reflect an innova tive CAM mechanism. Other roles for dark CO2 fixation should be examin ed. Dark CO2 fixation may be important as a source of carbon skeletons for both carbon and nitrogen assimilation, particularly in nutrient-p oor habitats. Of practical concern is the manner in which lake acidifi cation and eutrophication alter carbon budgets (e.g., Robe & Griffiths , 1994). Also, in many parts of the globe aquatic CAM spe-` cies are t hreatened: I. andicola of Peru, for instance, is clearly threatened by habitat loss (Leon & Young, 1996), and two of the three primitive Iso etes, morphologically similar to the extinct Isoetites, are apparently extinct (Hickey, 1986). At the other extreme, the aquatic CAM Crassul a helmsii is an aggressive alien (Dawson & Warman, 1987), in need of f urther studies such as those of Newman and Raven (1995) in a greater r ange of habitats. Isoetes, being the oldest lineage of CAM plants, pot entially holds further interesting discoveries with respect to photosy nthetic patterns. The most primitive species in the group are distinct in their lack of the typical terete ''isoetid'' leaf. These species a re restricted to isolated sites in South America and have seldom been collected. They are apparently basal to the group, sharing the laminat e leaf characteristic with the extinct and possibly ancestral Isoetite s (Hickey, 1986). The hypothesized amphibious origin for CAM suggests the possibility that these primitive species may lack CAM. Further stu dy of the photosynthetic metabolism and habitat characteristics of the se would be a stimulating contribution to the story of aquatic CAM pho tosynthesis. Here, and in other aspects of aquatic CAM photosynthesis, a multitude of possibilities are presented with new molecular genetic techniques, now being applied to terrestrial CAM plants (Cushman & Bo hnert, 1997).