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Laminariales) DYNAMICS OF CARBON ALLOCATION IN A DEEP WATER POPULATION OF THE DECIDUOUS KELP, Pleurophycus gardneri (LAMINARIALES) A thesis Presented to the F acuity of California State University at Monterey Bay through Moss Landing Marine Laboratories In Partial Fulfillment of the Requirements for the Degree Master of Science in Marine Science by Clare Margaret Dominik March 25, 2004 ABSTRACT Pleurophycus gardneri (Laminariales) is common in the low intertidal in the Pacific Northwest, but dominates many deep (30 to 40 m) reefs in central California. Seasonal dynamics of productivity and resource allocation of a deep-water population of this deciduous, stipitate kelp were studied to understand how blade abscission affects the annual carbon budget. Patterns of growth, metabolism, carbon storage and mobilization were measured monthly for one year relative to in situ light and temperature, and used to model the annual carbon budget. The carbon budget model was used to determine if blade abscission effectively reduced respiratory demand during winter when light availability was lowest. Blade growth occurred between February and July, followed by senescence and sloughing from August to December. Concentrations of laminaran and mannitol increased in the blades from the onset of sloughing until just prior to blade abscission (mid-December) suggesting translocation may have occurred from the blade to the stipe and holdfast. The initial model overestimated net production most probably because it failed to account for movement of the blade relative to the incident light. Sensitivity analysis resulted in the best fit when blades were assumed to utilize only 25 to 50% of ambient irradiance at 30m. The model indicated that blades could be retained over the winter assuming they received 25 to 50% of in situ irradiance. Thus, abscission was not necessary for metabolic survival and abscission may be related to other factors such as reduction in winter­ storm/surge induced damage/loss or enhanced spore dispersal through drift of abscised blades with sori. Keywords: Carbon budget, photosynthesis and abscission. 2 INTRODUCTION Autumnal leaf abscission has commonly been associated with conservation of energy in deciduous trees by synchronously senescing and dropping leaves. Large respiratory requirements of the leaves cannot be met during shortened winter photoperiods (Addicott 1982). Translocation of cellular material occurs from the leaves to the phloem during senescence (Pennell and Lamb 1997) prior to abscission for storage and possible utilization over the winter (Addicott 1982). Among most deciduous trees, cold temperatures and/or light (day-length) are the most influential cues for abscission. Light is also a common limiting factor for many plants in marine kelp dominated systems (Schiel and Foster 1986, Dean 1985). Canopy cover of Macrocystis pyrifera can limit light availability and growth of understory algae (Reed and Foster 1984, Wantanabe et al. 1992, Edwards 1998). Disturbance by large storms can increase light availability to under-story plants in shallow water by removing over-story layers (Graham 1997). These seasonal or episodic events can allow algae that would otherwise be excluded due to insufficient light, to establish and grow. In northern latitudes, kelps have a variety of physiological mechanisms that allow them to survive seasonally through alternating periods of nutrient limitation during the summer and light­ limitation in winter (Gagne et al. 1982). Laminaria solidungula utilized stored carbohydrates accumulated during summer to complete 90% of its annual linear blade growth during the virtual darkness of the Arctic winter (Dunton and Schell 1986, Chapman and Craigie 1977, 1978, Mann 1973 ). Summer accumulation of carbohydrates for use during winter requires periods of high summer irradiance combined with nutrient limitation that prevents growth. 3 Cellular photoacclimation increases photosynthetic efficiency and thus can contribute to survival when light availability is low. Algae from deep water may contain more accessory pigments, which harvest light more efficiently at low light intensities (Ramus 1983). Another characteristic includes thinner thalli compared to algae in shallow water, resulting in lower respiration rates that promotes survival in low light (Markager and Sand-Jensen 1992). Another potential way algae can survive the low light conditions of winter is to reduce total biomass and thus, respiratory demand. Abscission of reproductive tissues is common among brown algae, including Nereocystis sp., Fucus spp.. and Ascophyllum sp., and also possibly among A/aria sp., Lessoniopsis sp.. Pterogophora sp. (Addicott 1982). It is unclear whether Laminaria sinclarii truly abscises or whether the blade is removed by physical abrasion (Markham 1972). Pleurophycus gardneri (Laminariales) is a deciduous perennial (Germann 1986) or pseudoperennial (Sears and Wilce 1975) and is the only kelp known now to undergo synchronous defoliation of the vegetative (photosynthetic) blade each winter. Germann (1989) suggested abscission of the senescent blade may be more advantageous than its retention because the high photosynthetic efficiency and low respiration of the stipe and the holdfast may compensate for loss of greater photosynthetic surface area of the blade, which has large respiratory requirements. The perennial stipe and holdfast may also function as a reservoir for carbohydrates translocated from the blade before abscission. The distribution of Pleurophycus gardneri was originally reported to be from Montague Island, Alaska to Fort Bragg, California, in the low intertidal to upper subtidal (Abbott and Hollenberg 1976). Individuals are common in the northern part of the range but comparatively rare in the south. VanBlaricom et al. (1986) found low densities of P. gardneri (<1 individual -2) m at depths above 15m, and much higher densities (up to 10 plants m-2) in deep water off the 4 coast of Big Sur, California. Stands of plants with densities of 5 plants m-2 have recently been observed at depths between 27 and 34m in Carmel Bay, California (Spalding eta!. 2003). These observations prompted this investigation into the ability of a kelp previously thought restricted to intertidal regions, to flourish at 30m depth almost 500 km south of its originally reported southern limit. Many species ofLaminariales have been rigorously studied to examine the relationships between light availability (Luning 1979, Dunton 1985, Dunton and Jodwalis 1988, Dunton and Schell 1986), translocation and production of carbohydrates (Luning et a!. 1973, Chapman and Craigie 1978), nitrate concentrations and growth (Chapman et al. 1978, Germann et al. 1987). The objective of this study was to explore the dynamics of carbon assimilation and its utilization for growth by Pleurophycus gardneri in this deep water habitat. Physiological rate measurements, in situ growth studies and chemical analysis were used to construct a numerical carbon budget model. This model was used to explore 1) whether abscission is an effective mechanism for reducing whole plant respiratory demand and, 2) the length of time that perennial tissues can survive on storage carbohydrates alone during the winter. METHODS To create this model all inputs and outputs of the plants were quantified to establish net production with respect to carbon. Light was the major driver of the model, and Zimmerman et al. 0994) have shown that production estimates based on instantaneous irradiance measurements are more accurate than hours of daily irradiance saturated photosynthesis (HsAT) to model daily carbon gain by a plant. Instantaneous light measurements and photosynthetic production estimates yielded a d · · . gross pro uctmn estimate from winch losses (respiratiOn and sloughmg) were 5 subtracted. Chemical composition (carbohydrate and pigment concentrations) was determined to evaluate source/sink relationships among the four different tissue types of the plant. Plant size, 1 defined as total carbon (gC planf ) summed from each tissue type, and plant growth and/or sloughing were quantified and used to evaluate the models ability to predict changes in plant size as a function oflight availability. Carbon budget models of hypothetical plants retaining blades suggests what would happen to plant size if abscission did not occur. Study Site The study area was located in 30m of water at the East Pinnacles (36°33'35" N, 121°57'53" W), approximately 1.5 km offshore from Stillwater Cove, Carmel Bay, California. High relief granite pinnacles interspersed with large boulders and small sand channels characterized the area. Pinnacle tops above 20 m depth support a canopy ofMacrocystis pyrifera, which is thinned annually by winter storms. The stipitate kelps Pterygophora califomica, Eisenia arborea, and Pleurophycus gardneri were interspersed with giant kelp at 20 m but higher densities of P. gardneri were found in deeper water outside the giant kelp canopy. Fleshy red and geniculate coralline algae comprised a variably abundant algal turf underneath the stipitate kelps. Stipitate kelps outside the kelp canopy periodically lay flat and overlap one another when there is no surge or current (typically during summer months) providing shading and structure much like a sub-surface "canopy." Nongeniculate coralline algae, along with red and occasionally green encrusting algae, generally occupied the primary substrate interspersed with encrusting invertebrates (see also Spalding et al. 2003). Light Availability
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