**1.2.2 In the aquatic environment**

116 Artificial Photosynthesis

These sunflecks are combined with diurnal fluctuations in irradiance, ranging from sunflecks lasting only a few seconds or less in heavily shaded sites to cloud-induced fluctuations ("shadeflecks") lasting up to an hour or longer in open sites (Knapp & Smith, 1987). The nature of sunflecks, their size, shape, duration, and peak photon flux density depends on the height and precise arrangement of vegetation within the forest canopy as well as the position of the sun in the sky. The occurrence of a sunfleck at a particular location and time in the forest understory depends on different, often interacting, factors: the coincidence of the solar path with a canopy opening; the movement of clouds that obscure or reveal the sun; and the wind-induced movement of foliage and branches (in the canopy or in the understory plants themselves). These factors interact to yield a highly dynamic light environment in which the photon flux reaching leaves can increase or decrease over orders of magnitude in a matter of seconds. The effects of sunflecks on understory photosynthesis were studied in several works and revealed conflicting results (Leakey et al., 2002, 2005). In some cases, photosynthesis as CO2 assimilation by understory

seedlings was enhanced, whereas at elevated temperatures (38ºC), it decreased.

Seconds to minutes

Caused by leaf movement in forest understory

Underwater highfrequency light fluctuation resulting from lens effect on the water surface

Sunlight focusing by short seasurface waves; appears in peculiar form of irradiance pulses, termed 'flashes'

Sunflecks

Flickering light

Fluctuating light

light

Flashing light

underwater

Intermittent Short flashes

**Subject Condition Frequency Organism Reference** 

High frequency Less than one second

At depth of 1 m, up to 200 min-1

In values of a few milliseconds. The critical flash time is a function of the incident intensity. The dark time must be 10 times as long as the flash time

photobioreactors, known as 'flashing

light effect'

Table 1. Some historical observations of fluctuating light on the water surface and

Leakey et al. (2002,

Yamasaki and Nakamura (2008); Veal et al. (2010)

2005)

Reef-building Stramski (1986)

*Chlorella* Kok (1953)

Dipterocarp seedlings

endosymbiont photosynthesis of reef-building corals

coral *Acropora digitifera* 

*pyrenoidosa* cultures

In Myers (1953)

In natural aquatic systems, there are several factors that cause variations in irradiance. Irregular variations are caused by surface wave movement (Walsh & Legendre, 1983), cloud cover (Marra & Heinemann, 1982), and the vertical movement of phytoplankton (Falkowski & Wirick, 1981).

The high-frequency (less than 1 Hz) light fluctuations, known as 'flicker light', are produced by a lens effect of moving water surface, or waves, that simultaneously focuses and diffuses sunlight in the few upper meters (Hieronymi & Macke, 2010) (Fig. 1a). Because flicker light potentially produces excessively strong light as well as dimmer light, such fluctuations may have profound effects on the photosynthesis of benthic algae, seagrasses, and zooxanthellate corals. We will limit our discussion to shallow-water sessile organisms that are particularly prone to be influenced by a recurrent light provision anomaly such as these flickers. The effect diminishes with depth due to the shape- and hence the focal length of waves and scattering by particles (Fig. 1).

Waves act as lenses because of the differences in refractive indices between air and water, focusing light below the wave for a brief period. In shallow water, this effect can be seen clearly by eye (Fig. 1), appearing against a dark background as flickering bands of focused light. The location of the focusing events depends upon the shape of the waves. Large, rounded waves focus into deeper regions than small, sharply curved ripple waves (Kirk, 1994; Schubert et al., 2001) (Fig. 1).

Fig. 1. Underwater light patterns on a shallow sandy bottom due to surface waves

The Enhancement of Photosynthesis by Fluctuating Light 119

Fig. 3. Downward irradiance patterns below three waves with respect to 100% at the surface (note the logarithmic color scale and the different scales of the x axes) Wave I, flat surface, no lensing; Wave II, strong lensing; wave III, large radius, weak lensing (after Hieronymi

Due to its dependence on wave geometry and on their horizontal movement, there is a tight coupling between wind velocity, wave height, surface smoothness and the underwater light field (Fig. 4). The effect of small-scale roughness on preventing wave lensing was applied in the study by Veal et al. (2010), who used water sprinklers to obtain

and Macke (2010)).

non-lensing controls.

Underwater irradiance fluctuations result from temporal, non-linear variations of seasurface topography. When solar radiation is broken, the intensity and light penetration depth depend on the wavelength of light and general and local water features. Phytoplankton, which live at different depths, must adjust and be acclimated to the features of the underwater field to which they are exposed for doing photosynthesis (Kirk, 1994).

Ripples on the water surface cause considerable heterogeneity of subsurface light (Figs. 2, 3) through the lens effect, which simultaneously focuses and diffuses sunlight in the upper few meters, producing a constantly moving pattern of interspersed light and shadows on the substrate. Due to that effect, light intensity in shallow water environments sometimes reaches more than 9,000 μmol quanta m-2s-1, corresponding to 300-500% of the surface light intensity (Fig. 1) (Schubert et al., 2001). The lens effect produced by waves generates narrow belts of supersaturating light that pass over the bottom surface for less than a second (Figs. 2, 3). In addition to the focusing effect of light, the same curvature of the water surface also produces lower light intensity intervals interspersed between the intense peaks, namely, producing a light-diffusing effect (Schubert et al., 2001). This light-diffusing effect may serve as a relaxation period for algal photosynthesis.

Fig. 2. Focusing beams beneath wave crests and scattering under troughs. The arrows indicate the dependence of maximal-effect depth on wave radius (after Grosser et al., 2008).

Underwater irradiance fluctuations result from temporal, non-linear variations of seasurface topography. When solar radiation is broken, the intensity and light penetration depth depend on the wavelength of light and general and local water features. Phytoplankton, which live at different depths, must adjust and be acclimated to the features of the underwater field to which they are exposed for doing photosynthesis (Kirk,

Ripples on the water surface cause considerable heterogeneity of subsurface light (Figs. 2, 3) through the lens effect, which simultaneously focuses and diffuses sunlight in the upper few meters, producing a constantly moving pattern of interspersed light and shadows on the substrate. Due to that effect, light intensity in shallow water environments sometimes reaches more than 9,000 μmol quanta m-2s-1, corresponding to 300-500% of the surface light intensity (Fig. 1) (Schubert et al., 2001). The lens effect produced by waves generates narrow belts of supersaturating light that pass over the bottom surface for less than a second (Figs. 2, 3). In addition to the focusing effect of light, the same curvature of the water surface also produces lower light intensity intervals interspersed between the intense peaks, namely, producing a light-diffusing effect (Schubert et al., 2001). This light-diffusing effect may serve as a relaxation period for algal

Fig. 2. Focusing beams beneath wave crests and scattering under troughs. The arrows indicate the dependence of maximal-effect depth on wave radius (after Grosser et al., 2008).

1994).

photosynthesis.

Fig. 3. Downward irradiance patterns below three waves with respect to 100% at the surface (note the logarithmic color scale and the different scales of the x axes) Wave I, flat surface, no lensing; Wave II, strong lensing; wave III, large radius, weak lensing (after Hieronymi and Macke (2010)).

Due to its dependence on wave geometry and on their horizontal movement, there is a tight coupling between wind velocity, wave height, surface smoothness and the underwater light field (Fig. 4). The effect of small-scale roughness on preventing wave lensing was applied in the study by Veal et al. (2010), who used water sprinklers to obtain non-lensing controls.

The Enhancement of Photosynthesis by Fluctuating Light 121

between the surface of the pond, the transparent wall of the reactor, or the dark depth of the culture, the cells are exposed to a fluctuating light regime whose properties depend on the light source and its intensity, spectral distribution and beam geometry, culture density and depth, reactor architecture, and the hydrodynamics of mixing. These parameters define the

There are two major types of photobioreactors that are considered the most common production systems: outdoor open ponds (Fig. 5) and enclosed photobioreactors (Fig. 6). Open ponds have been the most widely used system for large-scale outdoor microalgae cultivation for food and medicine supplements during the last few decades (Borowitzka, 1993). They were built as a single unit or multiple joint units, with agitation by means of

range of light intensities to which the cells are exposed, as well as their frequency.

paddlewheels, propellers, or airlift pumps.

Fig. 5. Open ponds

Fig. 4. PAR fluctuations as measured by PRR800 at 0.8 m depth: A) on a very calm day (0.4 m/sec wind); and B) on a windy day (7 m/sec wind). The depth values are not calibrated but do represent the amplitude of surface waves as sensed by the pressure sensor of the PRR800 unit. Data were recorded at 15 Hz without any shading effect, downwind of the IUI pier, in the gulf of Eilat. Coefficient of variance=40% (Dishon, personal communication)
