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.W. Touchette, J.M. Burkholder J. Exp. Mar. Biol. Ecol. 250 2000 169 –205
dissolved oxygen concentrations are low, indicating increased carbon metabolism in response to anoxic hypoxic conditions Sachs et al., 1996; Germain et al., 1997;
Touchette, 1999. In contrast, a positive relationship has been shown between below- ground tissue SS activity and temperature in Z
. marina Touchette, 1999. This temperature-associated increase in SS activity and, thus, higher sucrolysis, may be
associated with increased respiratory demand Touchette, 1999. 5.3. Starch metabolism
Starch synthesis occurs in plastids and, like sucrose production, is activated by an accumulation of triose-P and yields fructose 1,6-bisP as an initial product Godwin and
Mercer, 1983; Fig. 3. It differs from sucrose synthesis in that an ADP-glucose rather than UDP-glucose is involved, from which starch is formed by the enzyme starch
synthase.
The data on starch storage in seagrasses are highly variable. Low starch content has been reported in Thalassia testudinium Jagels, 1983 and Zostera marina ,5 of the
total carbohydrates, US Pacific Coast, Alcoverro et al., 1999; Touchette, 1999. In contrast, Burke et al. 1996 reported that starch could form more than 65 up to 140
21
mg g dry weight of the total nonstructural carbohydrate content in Z
. marina from Chesapeake Bay. In Z
. noltii, starch levels can approach one-third of the total nonstructural carbohydrates in belowground tissues Pirc, 1989; Vermatt and Verhagen,
1996. Halophila ovalis has also been found to accumulate up to 90 of its total nonstructural carbohydrates as starch in leaf and root tissue Longstaff et al., 1999.
Moreover, in plants with low shoot and root-rhizome starch, there may be substantial starch accumulation in fruit tissues e.g., in Halodule spp., Halophila ovalis, Phyllos-
padix iwatensis, P. japonicus, Thalassia hemprichii — Bragg and McMillan, 1986; Kuo et al., 1990; Kuo et al., 1991; Kuo and Kirkman, 1992.
6. Respiration
Respiration is considered here as the controlled mobilization and oxidation of stored carbohydrates. During this process free energy is released and incorporated into NADH
and ATP, which can then be utilized to support other metabolic processes Taiz and Zeiger, 1991. Respiration in plants may be considered in three stages as glycolysis and
fermentation; the tricarboxylic acid cycle TCA cycle or Krebs cycle, in mitochondria; and the electron transport chain, yielding ATP in mitochondria. These processes are
conserved among many organisms, including seagrasses. In glycolysis, carbohydrates are converted in the cytosol to produce NADH and a 3-carbon product, pyruvate. Under
1
aerobic conditions in glycolysis, two electrons are required to reduce the NAD to
NADH, which can then be used as a means to store free energy. The NADH eventually drives the synthesis of ATP via the electron transport chain. However, during anaerobic
conditions both the TCA cycle and electron transport do not function Taiz and Zeiger, 1991.
In the absence of oxygen, a surplus of NADH may develop, and a concomitant deficit
B .W. Touchette, J.M. Burkholder J. Exp. Mar. Biol. Ecol. 250 2000 169 –205
195
1 1
1
in NAD . Because NAD is a required cofactor for many enzymes, a deficit in NAD
can significantly impair important metabolic processes Taiz and Zeiger, 1991. To
1
alleviate NAD depletion, pyruvate may be further metabolized through fermentation. In
plants, both lactic acid and alcohol fermentation have been described Davies, 1980; Roberts et al., 1984; Smith et al., 1988. Alternatively, some plants including
seagrasses may accumulate other compounds during fermentation such as organic acids malate, shikimate or amino acids alanine, g-amino butyric acid; Smith and Ap Rees,
1979; Davies, 1980; Mendelssohn et al., 1981; Joly and Crawford, 1982; Pregnall et al., 1984.
To avoid anaerobic respiration in belowground tissues, seagrasses and many other aquatic angiosperms translocate and release O
in the rhizosphere during periods of
2
active photosynthesis Sand-Jensen et al., 1982; Smith et al., 1984; Crawford, 1987; Caffrey and Kemp, 1991. However, during darkness or extended low light for
example, from sustained cloud cover or water turbidity, belowground tissues may undergo periods of anerobiosis Crawford, 1987. High rates of ethanol synthesis have
been shown in excised roots of Zostera marina during anaerobic conditions from use of
14
C-sucrose; Smith et al., 1988. However, typically ethanol does not accumulate. For example, in the above laboratory study, more than 95 of the ethanol produced was
released into the rhizosphere, indicating effective removal from belowground tissues. Field populations similarly yielded little or no accumulation of ethanol in root tissues,
even during extended periods of sediment anoxia associated with long periods of low light Penhale and Wetzel, 1983; Pregnall et al., 1984.
It is likely that the low ethanol content in belowground tissues reflects its release into the rhizosphere. Nonetheless, alternative fermentation pathways have been described
with significant increases in alanine and g-amino butyric acid, and decreases in glutamate and glutamine within 2–4 h of anaerobiosis Pregnall et al., 1984; Smith et al.,
1988. It was hypothesized that in Z . marina, pyruvate undergoes transamination via
glutamate and or glutamine to form alanine Pregnall et al., 1984; Smith et al., 1988. Thus, pyruvate from glycolysis would be converted to alanine, thereby lowering
production of the more toxic end product, ethanol. This preference for alanine accumulation would further benefit the plant by conserving carbon skeletons and
assimilated nitrogen Pregnall et al., 1984.
The primary environmental factor believed to influence respiration rates in seagrasses is temperature Marsh et al., 1986; Zimmerman et al., 1989; Terrados and Ros, 1995;
Masini and Manning, 1997. Unlike photosynthesis which increases with temperature up to |5–108C above ambient, respiration rates continue to increase with increasing
temperatures in excess of 408C Drew, 1978; Bulthius, 1983; Marsh et al., 1986. Light and other environmental factors can also significantly influence respiration. For example,
seagrasses in deeper water tend to have lower respiration rates Dennison and Alberte, 1982. Z
. marina grown at 5.5 m had respiration rates that were |40 lower than rates observed in plants at 1.3 m Dennison and Alberte, 1982. Respiration rates in Z
. marina have been shown to increase, as well, with increasing water-column nitrate enrichment
and tissue NR activity Touchette, 1999, as has been observed for terrestrial angio- sperms Bloom et al., 1992. Dark respiration rates in Z
. marina leaf tissue increased by as much as 36 following an 8 mM pulse of water-column nitrate. The increased
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respiration under nitrate enrichment may help to supply the energy and carbon needed to assimilate and reduce nitrate Bloom et al., 1992; Touchette, 1999.
In seagrasses, aboveground tissues typically have higher respiration rates Table 9. On a weight basis, respiration rates in root-rhizome tissues have been reported as only
12–36 of the rates measured for leaves. Respiration rates in root tissues |4.5 mg O
2 21
21
g dw min
, for example, in Thalassia testudinum, are substantially higher than
21 21
rhizome respiration |1 mg O g dw min
; Fourqurean and Zieman, 1991. A
2
cautionary note is warranted, however, because in many studies of seagrass respiration, belowground tissues were maintained under aerobic conditions despite the fact that the
natural sediment environment is often anaerobic or microaerobic. Respiration rates in non-photosynthetic tissues can be strongly influenced by sediment anoxia Smith et al.,
1988. For example, sucrose metabolism in belowground tissues of Zostera marina during anoxia was reported as only |65 of rates observed during aerobic periods
Smith et al., 1988. Thus, respiration studies of seagrass belowground tissues under aerobic conditions may overestimate respiration rates in anoxic sediments Smith et al.,
1988; Herzka and Dunton, 1998. Nevertheless, the general differences in respiration that have been reported for above- and belowground tissues likely reflect differences in
metabolic function. That is, rhizomes tend to be primarily storage tissues, whereas leaf and root tissues are involved in more energy-costly metabolism such as carbon
assimilation, nutrient absorption, and reduction.
7. Future research directions
