Future Directions and Research Priorities

3.1. THE QUEST FOR SPATIAL DATA IN SEAWEED BIOLOGY

In its simplest form, "spatially explicit" seaweed data would refer to the availability of georeferenced species occurrences. While we discussed the practice of georefer-encing and dissemination of spatially explicit seaweed data in depth in the second section of this chapter, we briefly show a couple of examples to demonstrate the dramatic state of the current availability of this information. For instance, looking at a random Nori species, Porphyra yezoensis Ueda, AlgaeBase (Guiry and Guiry, 2008) mentions 13 references to occurrence records throughout the northern hemisphere. However, the Ocean Biogeographic Information System (OBIS, an online integration of marine systematic and ecological information systems; Costello et al., 2007) contains no P. yezoensis records. Another random example, the sipho-nous (sub)tropical green alga Codium arabicum Kutzing illustrates this further: out of 55 direct or indirect occurrence references in Algaebase, 17 are georeferenced in OBIS. However, two of the specimens wrongly have zero longitudes, hence locating the records some 400 km inland from the coast of Ghana, instead of at the Indian coast. Five out of the 17 are recorded to no better than 0.1° in both longitude and latitude, making their position uncertain within up to 120 km2. Fifteen out of the 17 make no mention of the collector's name or publication, preventing to check the integrity of the identification. Eleven lack subcountry level locality name information, and none mention substate locality names, making it impossible to verify geographical coordinates through the use of gazetteers.

If the amount of coastal or marine publications using GIS, mapping, or remote sensing can be called minimal, averaging 8% of the total publications using these geographic techniques as previously shown, the proportion of these records mentioning seaweeds or macroalgae is statistically speaking barely existing, attaining 0.5-1% of the spatial marine studies. Studies investigating the other two best-known benthic marine communities, coral (reefs) and seagrasses, constitute up to 10%, while the remainder covers (in no particular order) mangroves and other supratidal coastal communities and structures, coastal or marine topography, and geomorphology or nautical issues. Some of the reasons accounting for this disproportion are obvious: for a start, relatively few investigate seaweeds. However, out of 12,074 studies mentioning seaweeds or macroalgae in ISI Web of Knowledge, a potential 7,279 in the fields of ecology, biogeography, phylogeography, or ecophysi-ology could benefit from some sort of spatial explicit information, while only 177 (2.5%) actually mention to do so in their title, abstract, or keywords. Other problems concern the nature of seaweed communities: while coral reefs and seagrass meadows usually form large and relatively homogeneous assemblages, seaweeds are spatially and spectrally very heterogeneous. This is particularly difficult to cope with in remote sensing studies, already challenged by the properties of the water column in comparison with terrestrial vegetation studies.

3.2. GEOREFERENCING SPECIMENS

Sections 1.4 and 2.1 demonstrate the need to prioritize the standardization of disseminating and linking geographical seaweed specimen information. Investigating the consequences of global change requires the availability of correct and complete global data sets. Therefore, we support the requirement of the dissemination of sample coordinates not only from geographically oriented studies, but from every study using in situ sampled seaweeds, to allow for informative and accurate meta-analyses. Coordinate pairs should be deposited in already existing global biodiversity databases such as OBIS, but minimal geographic accuracy and complete specimen information including collector's name should be required to allow vigorous quality control. The use of global biodiversity databases as a main depositing center for specimen coordinates rather than dedicated seaweed databases also opens perspectives to investigate potential correlations between seaweed and fau-nal distribution shifts in response to global change. However, it should also be investigated how general geographical biodiversity databases such as OBIS could be related to and synchronized with specific databases such as Algaebase and GenBank to optimize the dissemination of all kinds of specimen information.

3.3. REMOTE SENSING

No significant time gap exists between the development and deployment of airborne sensors; due to an optimal use of the most recent technologies, airborne sensors thus represent the best technical characteristics desirable for seaweed mapping to date. As time goes on, the most recent satellite sensors can benefit from the evolution in technologies to more closely resemble the properties of airborne sensors. Vahtmae et al. (2006) used a simulation study to demonstrate that submerged seaweeds in turbid coastal waters could well be mapped using hyperspectral satellite sensors like CHRIS and Hyperion, featuring 10 nm wide bands in the visual wavelengths. However, they also postulated a signal-to-noise ratio of 1,000:1, an image quality not met by these existing sensors. It is thus vital that similar new hyperspectral, very high resolution satellite sensors should be developed for seaweed mapping and monitoring in the framework of global change research. However, Fig. 2 shows that planned sensors for the next 3 years follow the historical trade-off toward multispectral very high resolution systems. Nowadays, this seems to be motivated by two elements: the huge thrust for coral reef research, in which macroalgae are often lumped into one or few functional classes and spatial resolution is considered more important than spectral resolution, and disaster event monitoring, focusing on a near-one day site revisiting time through the use of extensive off-nadir or off-track pointing capabilities (Table 2). The latter technique also generates huge amounts of data, adding a new dimension to the historical trade-off situation: current data storage capacities allow for two image characteristics out of three (spectral, spatial, and temporal resolution) to be optimized, but not all three. Unfortunately, no significant thrust seems to exist to develop sensors ideally suitable for large-scale algal mapping and monitoring to date, explaining the characteristics of the missions in development. As a means to deal with the lack of very high resolution hyperspectral imagery, efforts have been made to combine the information from several sensors with different characteristics into one data set. This is analogous to pan-sharpening techniques, which use the high spatial detail of a panchromatic band to spatially enhance the multispectral imagery from the same sensor (see also Fig. 2). Although useful in current conditions, we suspect these techniques to become less important as more advanced sensors would be developed, since processing information from one sensor evidently is less time- and resource-consuming and more accurate than using multisensor information.

Light-based active remote sensing involves the emission of laser pulses with a known frequency and subsequently detecting fluorescence in certain wavelengths. Kieleck et al. (2001) proved this technique to be successful in discerning submerged green, brown, and red seaweeds in lab conditions. Mazel et al. (2003) used a similar prototype in-water laser multispectral fluorescence imaging system to map different coral reef bottom structures, including macroalgae, on a 1-cm resolution. Airborne laser imaging has been used extensively to provide very high resolution imagery in terrestrial applications such as forestry. In the marine realm, its applications are mostly limited to in-water (boat-mounted) transect mapping strategies, although further research to develop aerial systems could prove useful to obtain very high resolution imagery of individual seaweed patches, e.g., to map the spreading of macroalgae on coral reefs.

3.4. DISTRIBUTION AND NICHE MODELING

Presence-only data are mostly inherent to seaweed niche distribution modeling due to sampling locality bias (caused by difficulty of coastal and submerged terrain access), small sizes, or seasonally microscopic life stages of seaweed species or cryptic species. Under the title of Species' Distribution Modeling, Pearson (2007) published a general manual including (presence-only) niche modeling, mostly based on Maxent. However, the manual is based on terrestrial experiences, as niche modeling algorithms have rarely been applied to seaweed distribution to date, and some issues characteristic of marine benthic niche modeling are not elaborated. For instance, there are more global environmental GIS data available for the terrestrial realm when compared with the marine environment. Table 3 lists marine environmental variables currently available from global satellite imagery, along with data that will become available in the near future. Especially, globally gridded salinity data are lacking to date. Other variable data sets (pH, nutrients, salinity, turbidity, etc.) may also be compiled from the interpolation of in situ data, e.g., from the Worldwide Ocean Optics Database (Freeman et al., 2006) or the World Ocean Database (NOAA, 2008). These data, consisting of vertical profiles, can be advantageous for 3D modeling, but the interpolation techniques necessary to obtain gridded maps may be challenging. Furthermore, global change climate extrapolations resulted in the production of global gridded maps of environmental variables for future scenarios in the terrestrial realm, but similar data for the marine realm are not yet available. The projection of calculated niches on future distributions can greatly enhance our understanding of global change consequences, and it is therefore crucial that future research is aimed at composing similar gridded maps of future scenarios for marine environmental variables. More research should also be aimed at setting model parameters to account for spatial autocorrelation and clustering of species occurrence data. Finally, model validation and output comparison statistics are under scrutiny in recent literature (e.g., Peterson et al., 2008), and more research is needed to agree on the best statistics suitable for marine data.

Modeling on a local scale allows for including high-resolution environmental variables that are not available for the entire globe. This is particularly the case where environmental variables not available from satellite data have been measured in situ and can be interpolated locally. In other cases, one or several (very) high resolution satellite scenes can be used to provide substrate data, not relevant on a global scale with 1-km gridded environmental variables. For instance, De Oliveira et al. (2006) included substrate, flooding frequency, and wave exposure to model the distribution of several intertidal and shallow subtidal brown seaweeds along a 20 km coastal stretch in Brittany, France. Thus, it can be expected that multiscale modeling approaches will gain importance in the near future.

While human-induced effects on habitats are thought to drive short-term species dynamics, it is often stated that global climate change will influence the capacity of alien species to invade new areas on a medium to long term. Range shifts of individual species in an assemblage under climate change are based on largely the same processes driving the spread of alien species. Hence, the two can be addressed using the same approach (Thuiller et al., 2007). Although very complex processes are involved, the geographic component of species' invasions can be very well predicted using niche modeling techniques (Peterson, 2003). Once a comprehensive marine environmental data set is compiled, invaded areas and areas at risk of invasion can be successfully predicted based on the native niche of alien species (Peterson, 2005; Pauly et al., 2009), although Bronnimann et al. (2007) warn that a niche shift may occur after invasion. Nevertheless, niche modeling approaches are promising in future research of seaweeds' range shifts and invasions. Verbruggen et al. (2009) also applied niche modeling techniques to unravel the evolutionary niche dynamics in the green algal genus Halimeda, concluding that globally changing environments may allow certain macroalgae to invade neighboring niches and subsequently to form a divergent lineage. They also used Maxent to identify key areas to be targeted for future field work in search for new sister species - an application in biodiversity considered important in the light of global change.

To date, seaweed assemblages have often been characterized using quantitative vegetation analyses and multivariate statistics to delineate different community types and to establish the link between environmental variables and communities. With quickly developing niche modeling algorithms now regarded as the most advanced way to accomplish the latter, community niche modeling will be of particular value in global change-related seaweed research in the coming years. Ferrier and Guisan (2006) defined three ways to predict the niche of communities as a whole, rather than the niches of individual species. The assemble-first, predict-later strategy seems to be the most promising for seaweed data, since the existing floristic data have often been statistically assembled into communities. We suggest that prioritizing the development of community niche modeling algorithms can greatly speed up our insight into seaweed community response to future climate change.

4. References

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Biodata of Dinghui Zou and Kunshan Gao, authors of "Physiological Responses of Seaweeds to Elevated Atmospheric CO2 Concentrations"

Dr. Dinghui Zou is currently the Professor of College of Environmental Science and Engineering, South China University of Technology, China. He obtained his Ph.D. from the Institute of Hydrobiology, the Chinese Academy of Sciences, in 2001. Professor Zou's scientific interests are in the areas of: the relationship of seaweeds and global change, the mechanisms of inorganic carbon utilization in seaweeds, and the environmental regulation of growth and development of seaweeds.

E-mail: [email protected]

Professor Kunshan Gao is currently the distinguished Chair Professor of State Key Laboratory of Marine Environmental Science, Xiamen University, China. He obtained his Ph.D. from Kyoto University of Japan in 1989 and continued his research since then at Kansai Technical Research Institute of Kansai Electrical Co. and at University of Hawaii in USA as a postdoctoral fellow. He was appointed as Associate Professor of Shantou University in 1995, and became recognized as the outstanding young scientist in 1996 by NSFC, then as Professor for 100 talented programmes in the Institute of Hydrobiology by the Chinese Academy of Sciences in 1997. Professor Gao's scientific interests are in the areas of: ecophysiology of algae and algal photobiology, focusing on the environmental impacts of increasing atmospheric CO2 under solar radiation.

E-mail: [email protected]

Dinghui Zou Kunshan Gao

A. Israel et al. (eds.), Seaweeds and their Role in Globally Changing Environments,

Cellular Origin, Life in Extreme Habitats and Astrobiology 15, 115-126

DOI 10.1007/978-90-481-8569-6_7, © Springer Science+Business Media B.V. 2010

PHYSIOLOGICAL RESPONSES OF SEAWEEDS TO ELEVATED ATMOSPHERIC CO2 CONCENTRATIONS

DINGHUI ZOU1 AND KUNSHAN GAO2

'College of Environmental Science and Engineering, South China University of Technology, Guangzhou, 510640, China 2State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, 361005, China

1. Introduction

The atmospheric CO2 concentration has been rising since the industrial revolution, and will continue to rise from the present 375 to about 1,000 ppmv by 2100 (Pearson and Palmer, 2000), increasing dissolution of CO2 from the air and altering the carbonate system of Surface Ocean (Stumm and Morgan, 1996; Takahashi et al., 1997; Riebesell et al., 2007). For example, an increase in atmospheric CO2 from 330 to 1,000 ppmv will lead to an increase in CO2 concentration from 12.69 to 38.46 mM in seawater (at 15°C and total alkalinity of 2.47 eq m-3) and an increase in the concentration of dissolved inorganic carbon (DIC, i.e., CO2(aq), HCO3-, and CO32-) from 2.237 to 2.412 mM, with a concurrent decrease in the pH of the surface seawater from 8.168 to 7.735 (Raven, 1991; Stumm and Morgan, 1996). Increasing atmospheric CO2 and its associated changes in the carbonate system can influence the physiology and ecology of seaweeds.

Seaweeds (Chlorophyta, Rhodophyta, and Phaeophyta) are usually distributed in intertidal and subtidal zones of coastal waters. They play an important role in the coastal carbon cycle (Reiskind et al., 1989) and contribute remarkably to sea-farming activities. The rate of primary production of some species is comparable with those of the most productive land plants; therefore, seaweeds have a great potential for CO2 bioremediation (Gao and Mckinley, 1994). On the other hand, increasing pCO2 in seawater would affect physiology of seaweeds. Therefore, a number of studies have been performed to envisage the impacts of CO2 enrichment on photosynthesis, growth, nutrients metabolism, and cell components of seaweeds. Results showed that increased CO2 concentration may enhance, inhibit, or not affect the growth of the species investigated. This work is intended to examine how the macroalgal species respond and acclimate to elevated CO2 levels.

2. Inorganic Carbon Limitation

The effects of elevated CO2 concentrations on seaweeds largely depend on the degree of carbon limitation present in natural systems. Photosynthesis of seaweeds would be severely limited under current atmospheric conditions if it were dependent only on diffusional entry of CO2 from the medium to the site of fixation via the carbon-assimilating enzyme Rubisco. There are several aspects of CO2 limitation of carbon assimilation in seaweeds (Beardall et al., 1998): (1) rather low dissolved CO2 concentration; (2) low diffusion rate of CO2 in seawater, being four orders of magnitude slower than in air; (3) the slow spontaneous formation of CO2 from HCO3- dehydration; and (4) the high Km values (40-70 mM) of Rubisco of algae. Nevertheless, photosynthesis in the investigated species can be fully or nearly saturated with the current ambient dissolved inorganic carbon (Ci) composition because of the presence of CO2-concentrating mechanisms (CCMs) that enable the algae to efficiently utilize the bulk HCO3- pool in seawater (Beer, 1994; Beer and Koch, 1996; Raven, 1997; Larsson and Axelsson, 1999; Zou et al., 2004; Giordano et al., 2005), which is about 150 times more abundant than free CO2. Some species, however, exhibit Ci-limited photosynthesis in natural seawater (e.g., Johnston et al., 1992; Andria et al., 1999a; Zou et al., 2003).

HCO3- is usually dehydrated extracellularly as mediated by periplasmic carbonic anhydrase (CA) to release CO2, which is then taken up into the cell. Another important approach for Ci acquisition of algae is the active uptake of HCO3- through the plasma membrane facilitated by an anion exchange protein (Drechsler et al., 1993, 1994; Axelsson et al., 1995). Additionally, H+-ATPase-driven HCO3- uptake has also been recognized in several marine seaweeds (Choo et al., 2002; Snoeijs et al., 2002). Seaweeds show different capacities to take advantage of the HCO3- pool in seawater (Axelsson and Uusitalo, 1988; Maberly, 1990; Mercado et al., 1998). Therefore, they can exhibit heterogeneous, often species-specific responses to elevated CO2. Their physiological responses to elevated CO2 levels can also depend on their acclimation strategies and the environmental constraints under which CO2 enrichment is imposed.

3. Growth

When juveniles of Porphyra yezoensis germinated from the chonchospores were grown at enriched CO2 levels of 1,000 or 1,600 ppmv for 20 days, their growth was significantly enhanced (Gao et al., 1991; Fig. 1). Similar findings were reported in Gracilaria sp., Gracilaria chilensis, and Hizikia fusiforme (Gao et al., 1993a; Zou, 2005). Although these species are capable of using bicarbonate, they still showed carbon-limited photosynthetic rates in natural seawater. Growth of a nonbicarbon-ate-user, the red alga Lomentaria articulata, was stimulated by enriched CO2 (Kubler et al., 1999). The enhancement could be attributed to the accelerated photosynthetic carbon fixation by increasing Ci availability or the depression of photorespiration by elevating the ratio of CO2 to O2 in the culture medium. It was interesting that growth of a green alga, Ulva rigida, which showed efficient ability of HCO3- utilization and

Figure 1. Enhanced growth of Porphyra yezoensis when 50 juveniles each (germinated from the same bunch of chonchospores released from the same chonchocelis, about 5 mm long at the beginning of the culture) were grown at different CO2 concentrations in aeration. The photo images were taken after 20 days culture (Gao et al., 1991).

Figure 1. Enhanced growth of Porphyra yezoensis when 50 juveniles each (germinated from the same bunch of chonchospores released from the same chonchocelis, about 5 mm long at the beginning of the culture) were grown at different CO2 concentrations in aeration. The photo images were taken after 20 days culture (Gao et al., 1991).

saturated photosynthesis at the current Ci concentration of seawater (Bjork et al., 1993; Mercado et al., 1998), was also enhanced at high CO2 concentrations (Bjork et al., 1993; Gordillo et al., 2001). Such an enhancement of growth was suggested to be caused by the enhanced N-assimilation (Gordillo et al., 2001), but could also be attributed to downregulation of HCO3- uptake and consequent energy saving for its operation. On the other hand, a decrease in growth rate caused by elevated CO2 has been reported in G. tenuistipitata (García-Sánchez et al., 1994), P. leucostica (Mercado et al., 1999), and P. linearis (Israel et al., 1999). Such an inhibition of growth was associated with lowered photosynthetic activity even measured at high CO2 concentrations (García-Sánchez et al., 1994). However, such a negative effect could also be caused by acidification of the medium (Israel et al., 1999). A more recent study by Israel and Hophy (2002) reported that the growth rates of 13 species (representing Chlorophyta, Rhodophyta, and Phaeophyta) cultivated in normal seawater were comparable with their growth in CO2-enriched seawater. The authors ascribed such nonresponsive behavior to the presence of CCMs that rely on the utilization of HCO3-. Obviously, researches show that enrichment of CO2 in seawater may affect, positively, neutrally, or negatively, the growth of seaweeds in direct or indirect ways.

4. Photosynthesis

4.1. PHOTOSYNTHETIC Ci UTILIZATION

The response of macroalgal photosynthesis to elevated pCO2 in seawater is species-specific. When cultured in high CO2, the light-saturated photosynthetic rate was reduced in Fucus serratus (Johnston and Raven, 1990), G. tenuistipitata

(García-Sánchez et al., 1994), and P. yezoensis (Gao, unpublished data) when measured at normal Ci of seawater. When the photosynthetic rate was measured at elevated DIC levels, it was significantly higher in the thalli grown at enriched CO2 levels in P. yezoensis (Gao et al., 1991) and Gracilaria sp. (Andría et al., 1999b). In P. leucostica, Mercado et al. (1999) found no significant difference between the maximal gross photosynthetic rates of the thalli grown at enriched and current inorganic carbon concentrations.

The photosynthetic affinity for Ci and the capacity of HCO3- utilization are usually lowered in seaweeds following exposures to high CO2 (Johnston and Raven, 1990; Bjork et al., 1993; Mercado et al., 1997; Andría et al., 1999a, b; Zou et al., 2003). Growing the cells at high CO2 levels decreased activity of the external (periplasmic) or total CA activity in Ulva sp. (Bjork et al., 1993), G. tenuistipitata (García-Sánchez et al., 1994), P. leucosticta (Mercado et al., 1997), and H. fusi-morme (Zou et al., 2003). Such a decrease reflects a decline in the capacity of HCO3- utilization. Israel and Hophy (2002) showed that the enzymatic features of Rubisco did not differ in the seaweeds when compared between the CO2-enriched and control cultures, though enrichment of CO2 was reported to decrease the content of Rubisco in G. tenuistipitata (García-Sánchez et al., 1994), Gracilaria sp. (Andría et al., 1999a), and P. leucosticta (Mercado et al., 1997).

4.2. PHOTOCHEMICAL EFFICIENCY

Photosynthetic acclimation in seaweeds to high levels of Ci generally resembles their responses to high irradiances, resulting in a decrease in pigment contents. For example, the phycobiliprotein (phycoerythrin and phycocyanin) and Chl a contents were reduced in Gracilaria sp. (Andría et al., 1999b, 2001), G. tenuistipitata (García-Sánchez et al., 1994), and P. leucosticta (Mercado et al., 1999) grown at high levels of Ci than those at normal Ci level. On the other hand, both maximum quantum yield and effective quantum yield were downregulated in P. leucostica when grown under high Ci conditions (Mercado et al., 1999), suggesting that enriched CO2 lowered the demand of energy for the HCO3- utilization mechanism.

4.3. EMERSED PHOTOSYNTHESIS OF INTERTIDAL SEAWEEDS

Intertidal seaweeds experience continual alternation of living in air and in water as the tidal level changes. Their photosynthesis undergoes dramatic environmental changes between the aquatic and terrestrial exposures. When the tide is high, they are submerged in seawater, where HCO3- pool is available for their photosynthesis (Beer and Koch, 1996; Beardall et al., 1998). When the tide is low, intertidal seaweeds are exposed to air, large buffering reservoir of HCO3- in seawater is no longer present, and atmospheric CO2 becomes the only exogenous carbon resource for their photosynthesis. The acquisition of CO2 is less constrained in air than in seawater, through which CO2 diffuses about 10,000 times slower (Raven, 1999). However, this constraint can be offset by the abundance of HCO3-, as many intertidal algae can use HCO3- as the exogenous inorganic carbon source for photosynthesis (Maberly, 1990; Gao and McKinley, 1994). Thus, carbon limitation during photosynthesis in intertidal species may be potentially more important in air than in water.

It is known that intertidal seaweeds can tolerate the emersed conditions, and the photosynthesis during emersion contributes significantly to their total carbon fixation budget (e.g., Gao and Aruga, 1987; Maberly and Madsen, 1990). Our previous works (Gao et al., 1999; Zou and Gao, 2002; Zou and Gao, 2004a, b, 2005; Zou et al., 2007) showed that elevated atmospheric CO2 might have a fertilizing effect increasing photosynthesis while exposed to air at low tide in most of the tested species, i.e. the red seaweeds P. haitanensis, Gloiopeltisfurcata, and Gigartina intermedia, the brown seaweeds Ishige okamura, H. fusiformis, and Sargassum hemiphyllum, and the green seaweeds Enteromopha linza and Ulva lactuca. The relative photosynthetic enhancement by the elevated CO2 levels increased with desiccation, although the absolute photosynthetic rate decreased with desiccation. The enhancement of daily photosynthetic production by elevated CO2 concentration during emersion differs among species owing to their zonational depths and exposure durations and the daily timing of emersion (Gao et al., 1999; Zou and Gao, 2005; Zou et al., 2007). Additionally, the CO2 compensation points increased with enhanced desiccation, with higher CO2 concentrations required to maintain positive photosynthesis (Gao et al., 1999; Zou and Gao, 2002, 2005).

5. Calcification

It is estimated from more than two million surveys that the oceans have absorbed more than one third of the anthropogenic CO2 released to the atmosphere (Sabine et al., 2004). With increasing atmospheric CO2 concentration, CO2 dissolves in sea-water to reach new equilibrium in the carbonate system. This leads to an increase in the concentrations of HCO3- and H+ and a decrease in the concentration of CO32-and of saturation state of calcium carbonate (Gattuso et al., 1999; Gattuso and Buddemeier, 2000; Caldeira and Wickett, 2003; Orr et al., 2005). The surface water of the ocean is known to have been acidified by 0.1 pH unit (corresponding to a 30% increase of H+) since 1800 (Orr et al., 2005), and will be further acidified by another 0.3-0.4 unit (about 100-150% increase of H+) by 2100 (Brewer, 1997; Caldeira and Wickett, 2003). Such an ocean-acidifying process has been suggested to harm marine-calcifying organisms by reducing the rate of calcification of their skeletons or shells (e.g., Gao et al., 1993b; Gattuso et al., 1999; Riebesell et al., 2000; Orr et al., 2005).

In the coastal waters where seaweeds are distributed, pH of seawater fluctuates within a larger range than pelagic waters because of inputs from terrestrial systems and fisheries. Nevertheless, additional CO2 input can still affect the biological activities in coastal waters, because ocean acidification will lower the pH regimes, shifting the pH range to a lower one. Therefore, increased pCO2 and decreased pH and CO32- will affect calcifying seaweeds. Gao et al. (1993b) showed that enrichment of CO2 to 1,000 and 1,600 ppmv in aeration inhibited the calcification in the articulated coralline alga Corallina pilulifera. It has also been shown that the increase in CO2 concentrations significantly slowed down calcification of temperate and tropical corals and coralline macroalgae (Gattuso et al., 1998; Langdon et al., 2000). For the marine-calcifying phytoplankton Emiliania huxleyi, calcification was reported to be reduced by the enriched CO2 (Riebesell et al., 2000), while a recent study showed that its calcification increased with elevated CO2 (Iglesias-Rodriguez et al., 2008). On the other hand, when pH was controlled at a constant level, elevated concentrations of DIC enhanced the calcification of Bossiela orbigniana (Smith and Roth, 1979) and C. pilulifera (Gao et al., 1993b).

6. Nitrogen Metabolism

Zou (2005) reported that both the nitrate uptake rate and the activity of nitrate reductase (NR) in the brown algae H. fusiforme were increased following cultures at high CO2 levels. It was also shown that elevated CO2 concentrations in culture stimulated the uptake of NO3- in Gracilaria sp. and G. chilensis (Gao et al., 1993a), Ulva lactuca (Zou et al., 2001), and U. rigida (Gordillo et al., 2001), and enhanced the activity of NR in P. leucosticta (Mercado et al., 1999) and U. rigida (Gordillo et al., 2001, 2003). This indicates that elevated CO2 concentrations can enhance nitrogen assimilation, as more nitrogen is required to support higher growth rate. The regulation of NR activity in seaweed by CO2 might be through a direct action on de novo synthesis of the enzyme, rather than through physiological consequences in carbon metabolism as occurring in terrestrial higher plants (Gordillo et al., 2001, 2003). Contrarily, decreased uptake rate of NO3- by high CO2 in G. tenuistipitata (García-Sánchez et al., 1994) and G. gaditana (Andría et al., 1999b) was also reported. Mercado et al. (1999) stated that NO3- uptake and reduction might be uncoupled when algae are grown at high CO2. Responses of macroalgal nitrogen assimilation to elevated CO2 could be species-specific; however, the results from different studies might be also generated from different culture systems or methods.

Growth under enrichment of CO2 would alter the cellular components of seaweeds. Contents of soluble proteins and phycobiliprotein were decreased in Graciaria tenuisitipitata (García-Sánchez et al., 1994), Gracilaria sp. (Andría et al., 1999b), and P. leucosticta (Mercado et al., 1999) when they were grown at high DIC levels. In contrast, the content of soluble carbohydrate was increased in Gracilaria sp. (Andría et al., 1999b). As a result of these changes, C/N ratios were increased in the seaweeds grown at elevated CO2 levels (García-Sánchez et al., 1994; Kübler et al., 1999; Mercado et al., 1999). Although phycobiliprotein, soluble proteins, and Rubisco contents were found to decrease under DIC-enriched conditions, internal N content was not significantly affected by the DIC levels. Andría et al. (1999b)

thereby suggested that the exposure and acclimation to high CO2 would involve the reallocation of resources, such as N, away from Rubisco and other limiting components (electron transport) towards carbohydrate synthesis and nonphoto-synthetic processes.

8. Summary

Atmospheric CO2 rise leads to a proportional increase in pCO2 of seawater and alters the carbonate chemistry, reducing the carbonate ions and pH while increasing that of bicarbonate. Physiological responses of seaweeds to elevated CO2 concentrations are highly variable, depending on the species, growing conditions, and duration of CO2 enrichment. In the species investigated, growth was enhanced, inhibited, or not affected by enrichment of CO2, while photosynthetic performance varied according to Ci acquisition mechanisms or the acclimation strategies. Usually, net photosynthesis was enhanced in elevated DIC levels for the species with less efficiency in bicarbonate utilization or CCMs. Growing the seaweeds in high CO2 downregulated their CCMs and possibly the electron transport demanded for its operation. On the other hand, calcification of calcifying seaweeds is negatively affected; nitrogen metabolism and the cellular C/N ratio would be increased in high-CO2-grown cells. For the intertidal species, large buffering reservoir of HCO3- in seawater is no longer present and atmospheric CO2 becomes the only exogenous carbon resource for their photosynthesis at low tide, elevation of atmospheric CO2 might have a fertilizing effect, increasing their photosynthesis during emersion. More research efforts on biochemical and molecular aspects for a wider range of species grown at high CO2/low pH conditions are needed to further evaluate the impacts of increasing atmospheric CO2 concentrations on seaweeds. At the same time, physiological approaches are required to distinguish the effects of high CO2 from that of lowered pH.

9. Acknowledgments

This work was supported by the Chinese 973 Project (No. 2009CB421207), the Key Project of Chinese Ministry of Education (No. 207080), and the National Natural Science Foundation (No. 40930846).

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Biodata of Professor Rafael Riosmena-Rodriguez and Professor Marco Antonio Medina-Lopez, authors of "The Role of Rhodolith Beds in the Recruitment of Invertebrate Species from the Southwestern Gulf of California, Mexico"

Professor Rafael Riosmena-Rodriguez is currently the leader of the Marine Botany research group of Universidad Autónoma de Baja California Sur in La Paz Baja California Sur, México. He obtained his Ph.D. from the La Trobe University in 2002. Professor Riosmena-Rodriguez is deeply interested in understanding the role of marine plants (where algae are included) in coastal habitats and their evolutionary significance. His research areas include systematic, biogeography, and ecology of marine plants from subtropical habitats. He is an expert on rhodolith beds.

E-mail: [email protected]

Professor Marco Antonio Medina-López is currently the Chairman of the Marine Biology Department of Universidad Autónoma de Baja California Sur in La Paz Baja California Sur, México. He obtained his B.Sc. from the Universidad Autónoma de Baja California Sur in La Paz Baja California Sur, México, in 1999. His scientific interests are in the areas of taxonomy and ecology of invertebrates.

E-mail: [email protected]

Rafael Riosmena-Rodriguez

Marco Antonio Medina-López

A. Israel et al. (eds.), Seaweeds and their Role in Globally Changing Environments,

Cellular Origin, Life in Extreme Habitats and Astrobiology 15, 127-138

DOI 10.1007/978-90-481-8569-6_8, © Springer Science+Business Media B.V. 2010

THE ROLE OF RHODOLITH BEDS IN THE RECRUITMENT OF INVERTEBRATE SPECIES FROM THE SOUTHWESTERN GULF OF CALIFORNIA, MÉXICO

RAFAEL RIOSMENA-RODRIGUEZ AND MARCO A. MEDINA-LÓPEZ

Programa de Investigación en Botánica Marina, Dept. Biol. Mar, Universidad Autónoma de Baja California Sur, Apartado postal 19-B, La Paz, B. C.S. 23080, México

1. Introduction

Rhodoliths are free-living forms of nongeniculate coralline red algae (Corallinaceae, Rhodophyta) that form extensive beds worldwide over broad latitudinal and depth ranges (Foster, 2001). Synonymous with the maerl beds common in the northeastern Atlantic, rhodolith beds are hard benthic substrates, albeit mobile, made up of branching crustose coralline thalli. Collectively, they create a fragile biogenic matrix over carbonate sediment deposits thought to be the result of long-term accumulation of dead thalli (Bosence, 1983a). A wide morphological variation of individuals exists and appears to be a response to variation in physical factors (Bosence, 1983b; Steller and Foster, 1995). This variation in morphology and incorporation of whole rhodolith and carbonates into the fossil record has led to their use as paleoindicators of environmental conditions (Foster et al., 1997). Unconsolidated rhodolith deposits have long been harvested for human use as soil amendment in European waters (Blunden et al., 1977, 1981). However, recent studies have shown that such beds are highly susceptible to anthropogenic disturbance such as trawling harvesting and reduced water quality (review in Birkett et al., 1998). Slow rhodolith growth (Rivera et al., 2003; Steller, 2003) combined with the negative impacts of burial make recovery after disturbance predictably slow. Foster et al. (1997) found rhodolith beds to be very common in the Gulf of California and suggested that there are two main types of beds: wave beds in shallow water (0-12 m) that are influenced by wave action (Steller and Foster, 1995), and current beds in deeper water (10->30 m) that are influenced by currents. Both types, especially current beds, are also influenced by bioturbation (Marrack, 1999). To persist, these algal beds require light, nutrients and movement from water motion (waves and currents), or bioturbation, which maintains them in an unattached and unburied state (Bosence, 1983a, b; Marrack, 1999).

The structure of individual rhodoliths influences the abundance patterns in the cryptofaunal assemblage. Intact, complex thalli, along with high rhodolith densities, are important factors driving this pattern. Complex thalli may provide more space, refuge, and resources through increased interstitial or interbranch space. As a result, rhodolith complexity appears to be a good predictor of abundance and potentially for richness. This matrix provides habitat for diverse assemblages of invertebrates and algae (Cabioch, 1968; Keegan, 1974; Bosence, 1983a, b; Steller et al., 2003). This also supports the hypothesis that the availability and shape of interstitial cavities are important for the associated crustaceans' assemblage (De Grave, 1999). Variation in physical factors, thought to influence rhodolith morphology (Bosence, 1983a; Steller and Foster, 1995), may therefore directly influence community structure. Thus, we predict that conditions that enhance structural complexity increase the available refuge among the rhodolith branches, and enhance overall species richness and abundance. Rhodolith beds support a rich community of flora and fauna found to be higher in species diversity than soft-sediment benthos alone (Steller et al., 2003). Organisms within a bed can associate with the surface of algal thalli (epi-fauna/flora), within the branches (crypto-fauna/flora) or in the underlying sediments (in-fauna/flora) (Steller et al., 2003). Factors influencing diversity patterns include increased architectural complexity and grain size, reduced sedimentation (Grall and Glemarec, 1997), and seasonal variation (Ballesteros, 1988) and reduced predation.

Bivalves have been shown to be abundant and associated with rhodolith beds and in the NE Atlantic (Hall-Spencer, 1998, 1999). Possibly, this is due to larval settlement preferences for coralline, structured, or large grain substrates, or refuge from predation. Depth stratification of bivalve species may also be related to variability in substrate type (Steller, 2003; Kamenos et al., 2004). The high density of bivalves at intermediate bed depths may reflect larval attraction to the structured settlement substrate provided by the rhodoliths or physical conditions found there. In addition, Steller and Foster (1995) found that rhodolith turnover and protection from burial was greater at shallow versus intermediate depths, suggesting that the latter affords reduced sedimentation and water flow favored by surface dwelling bivalves. Increases in summer densities may correspond to winter/spring recruitment periods of many species. It appears that rhodolith beds may positively enhance bivalve populations. However, there is a clear conservation problem between these positive attributes and the degradation resulting from commercial fishing (Hall-Spencer, 1998, 1999; Hall-Spencer and Moore, 2000).

Studies have shown that rhodolith beds support a diverse and dynamic ben-thic community. Community descriptions of diversity include common associ

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