Introduction: the algae and their environments

Seaweeds

The term “seaweed” traditionally includes only macroscopic, multicellular marine red, green, and brown algae. However, each of these groups has microscopic, if not unicellular, representatives. All seaweeds at some stage in their life cycles are unicellular, as spores or gametes and zygotes, and may be temporarily planktonic (Amsler and Searles 1980; Maximova and Sazhin 2010). Some remain small, forming sparse but productive turfs on coral reefs (Hackney et al. 1989) while others, such as the “kelps” of temperate reefs, can form extensive underwater forests (Graham et al. 2007a). Siphonous algae such as Codium, Caulerpa and Bryopsis that form large thalli are, in fact, acellular. The prokaryotic Cyanobacteria have occasionally been acknowledged in “seaweed” floras (e.g. Setchell and Gardner 1919; Littler and Littler 2011a). They are widespread on temperate rocky and sandy shores (Whitton and Potts 1982) and are particularly important in the tropics, where large macroscopic tufts of Oscillatoriaceae and smaller but abundant nitrogen-fixing Nostocaceae are major components of the reef flora (Littler and Littler 2011a, b; Charpy et al. 2012). Benthic diatoms also form large and sometimes abundant tube-dwelling colonies that resemble seaweeds (Lobban 1989). An ancient lineage of (mostly) deep-water green algae, the Palmophyllales, that includes Verdigellas and Palmophyllum, have a palmelloid organization with complex thalli built from an amorphous matrix with a nearly uniform distribution of spherical cells (Womersley 1971; Zechman et al. 2010). On a smaller scale are the colonial filaments of some simple red algae, such as Stylonema (previously Goniotrichum). A “seaweed” is therefore problematic to precisely define: here “seaweed” refers to algae from the red, green, and brown lineages that, at some stage of their life cycle, form multicellular or siphonous macrothalli. In this book we shall consider macroscopic and microscopic marine benthic environments and how seaweeds respond to those environments.

The waters of the oceans are in constant motion. The causes of that motion are many, beginning with the great ocean currents, tidal currents, waves, and other forces, and ranging down to the small-scale circulation patterns caused by local density changes (Vogel 1994; Thurman and Trujillo 2004). Hydrodynamic force is a direct environmental factor, but water motion also affects other factors, including nutrient availability, light penetration, and temperature and salinity changes. The forces embodied in waves are difficult to comprehend, unless one has been dangerously close to them; because of the density of water, a wave or current exerts much more force than do the winds. “Imagine a human foraging for food and searching for a mate in a hurricane and you will have only an inkling of the physical constraints imposed on wave-swept life” (Patterson 1989b, p. 1374). The energy amassed from a great expanse of air–ocean interactions is expended on the shoreline as waves break (Leigh et al. 1987). Equally difficult to visualize are the microscopic layers of water next to seaweed surfaces where the seaweeds’ cells interact with water. Too much water motion imposes drag forces that can rip seaweeds from the rocks, but this also clears patches of “new” space for recruitment. Too little water motion and nutrient concentration gradients form at the seaweed surface which can restrict nutrient uptake, but the same gradients are used by seaweeds to sense how fast the surrounding seawater is moving and thereby cue gamete or spore release.

Studies of seaweed form and function in wave-exposed and wave-protected sites have provided insights into the trade-offs apparent in some species that allow them to maximize resource acquisition in slow flows and minimize drag forces in fast flows. The following texts and reviews provide the necessary background on fluid mechanics: Denny (1988, 1993, 2006); Vogel (1994); Denny and Wethey (2001). “Marine ecomechanics” is an emerging field that uses a “physical framework” to understand the responses of marine organisms on scales from cells to ecosystems (Denny and Helmuth 2009; Denny and Gaylord 2010). We begin this chapter by describing the hydrodynamic environments in which seaweeds grow, and then discuss the mechanisms by which seaweeds can enhance resource acquisition in slow flows and withstand hydrodynamic forces in wave-exposed sites. We finish with a discussion on the effects of wave action and sediments on seaweed communities.

The environment of an organism includes both biotic and abiotic (physiochemical) factors. Communities of marine organisms encompass not only the seaweed communities but also the animal communities, of which the benthic grazers and their predators are most important to seaweed ecology. Thus, the biotic interactions of seaweeds include not only competition with other seaweeds (both within and between species) and with sessile animals but also predator–prey relations at several trophic levels, and facilitation; the mix of such interactions will change as the individual changes with age and environmental history.

Biotic interactions are complex, and their study often requires large-scale and long-term observations and manipulations in the laboratory, as well as in the field. Interactions can be positive (e.g. facilitation, mutualism, and commensalism), negative (e.g. competitive exclusion, consumption) or neutral, where there is no effect of one species on another. Studies on biotic interactions in the marine environment have traditionally focused on competition but more recently facilitation has been recognized as an important way in which biota interact. The minireviews of Olson and Lubchenco (1990), Carpenter (1990), Paine (1990), and Maggs and Cheney (1990) remain useful frameworks, as are the more recent syntheses found within Marine Community Ecology (Bertness et al. 2001) and Marine Ecology (Connell and Gillanders 2007).

Introduction

As seaweed consumption has increased in the last several decades, seaweed mariculture has filled the gap between wild stock harvest and the present demand. Ancient records show that people collected seaweeds for food starting in about 2500 BP in China (Tseng 1981), and 1500 in Europe (Critchley and Ohno 1998). Presently, the wild harvest of seaweeds is about 1.8 m tonnes y-1, mainly brown seaweeds used for alginates (FAO 2009). In Japan, China, and other Asian countries, where seaweeds have long composed an important part of the human diet, seaweed farming is a major business and over 90% of the seaweed production is from farming for human consumption. Since 1970, the culture of seaweeds has increased at ~8% per year (FAO 2009). Seaweed production from farming nearly doubled from 8.8 to 15.9 million tonnes from 1999 to 2008, with a value of US$7.4 billion (FAO 2010). Most of the world seaweed supply comes from aquaculture and seaweeds were the first to pass the 50% farmed/wild harvest threshold in 1971, compared to fish aquaculture that will exceed the 50% threshold by 2012 (Chopin 2012). About 99% of the farmed production is in Asia and over 70% of the production (10.9 million tonnes) is in China, followed by Indonesia, the Philippines, South Korea, and Japan. Chile is the most important producer outside of Asia with a production of 90 000 tonnes y-1 of wild harvested seaweeds. Table 10.1 illustrates the production, value, price and the three main producing countries for the six most important seaweed genera that are grown in aquaculture systems. Brown seaweeds compose about 64% of the production (67% of the value), reds about 36% (33% of the value), and greens, with ~99% being produced by Asian countries, 0.2% of the production and value (Chopin and Sawhney 2009). There has been a rapid increase in production in the last decade, especially of reds and browns (Fig. 10.1). The largest production (4.6 million tonnes; Table 10.1) is from Saccharina japonica (previously Laminaria japonica; or kombu in Japan or haidai in China), mainly in China. Korea grows mainly Undaria pinnatifida (wakame) with 1.8 million tonnes annually and Pyropia (previously Porphyra, or nori), while Japan focuses mainly on Pyropia.

Seaweeds exist as individuals, but they also live together in communities with other seaweeds and animals – communities that affect and are affected by the environment. Ecologists and physiologists alike are drawn to coastal marine ecosystems because of the easy access to strong environmental gradients over short spatial scales. Marine organisms grow in often distinctive vertical or horizontal “zones” or “bands” along these gradients, thereby providing “natural laboratories” in which to study environmental (abiotic) and biological processes shaping the communities. Zones of vegetation are also found in terrestrial habitats, but here the spatial scales are typically much greater. On a mountain, for example, vegetation is zoned with altitude, but the vertical distance over which changes occur can be in the order of 1000 m rather than several meters in the intertidal zone (Raffaelli and Hawkins 1996). Vertical gradients in the intertidal are easily observed at low tide, but also extend underwater where the surface irradiance can be reduced to 1% at 15 m depth in many coastal waters (Lüning and Dring 1979; sec. 5.2.2). Horizontal gradients include the salinity gradients of estuaries and salt marshes, and wave exposure (Raffaelli and Hawkins 1996).

In Chapters 1 and 2, we reviewed the morphologies, life histories, and developmental processes of seaweeds as species. In this chapter we consider the patterns and processes in marine benthic communities as a starting point for later factor-by-factor dissection of the environment. We open with an overview of zonation patterns seen in the intertidal and subtidal environments.

There have been very significant advances in many areas of phycology since the last edition nearly 20 years ago. In particular, the advances in our understanding of the endosymbiotic origin of algal plastids, and molecular aspects and genetics, stand out. The wealth of new literature alone in all the areas has warranted adding two new co-authors, Catriona Hurd, who focuses on water motion and seaweed physiological ecology, especially in the southern hemisphere, and Kai Bischof, who is well known for his research on photobiology and stress physiology. Hence, the previous edition’s chapter on “Temperature and salinity” has been expanded to include other environmental stressors such as UV radiation, ocean acidification, oxidative stress responses and the interactions between stressors.

Seaweed Ecology and Physiology is a textbook for senior undergraduates and a reference book for researchers. The rapid growth of knowledge in this field is both exciting and daunting. Our goal was to select papers that help put together a coherent story on a wide variety of ecological and physiological aspects. This book provides an entry to the literature, not a systematic literature review. With two of our co-authors having experience in the tropics and the temperate southern hemisphere, we have tried to avoid the typical temperate northern hemisphere bias.

Introduction

There are several categories of marine pollution. In this chapter, six categories of pollution encountered by macroalgae are discussed: metals, such as mercury, lead, cadmium, zinc, and copper; oil; synthetic organic chemicals, such as pesticides, industrial chemicals, and antifouling compounds; eutrophication (excessive nutrients, such as nitrogen or phosphorus); radioactivity, and thermal pollution. In the 1970s and ’80s, marine pollution was a hot topic and therefore some of these important early references have been retained. Over the last two decades, research on metals and eutrophication has been particularly active, followed by oil, antifouling paints, and organic wastes. There has been very little research on thermal pollution, even though it could be a good surrogate at local sites for assessing the potential long-term effects of global warming/climate change. Emerging anthropogenic issues are ocean acidification (see sec. 7.7 and Essay 4) and nanoparticles such as titanium dioxide (TiO2) (Miller et al. 2010, 2012).

General aspects of pollution

Several general considerations apply to studies on pollutants. Among these are the choice of test organisms, whether to study chronic or acute effects, the level of the effect such as lethal or sub-lethal, the complexities at various levels of organization from physiology to communities, and the issue of what is the biologically available quantity and form or species of the pollutant. Overall effects of a compound are assessed by acute or chronic exposure. Acute effects are the result of short-term exposure (e.g. 48–96 h) and are determined from the percent survival of an organism over a range of toxin concentrations. Chronic effects are the result of exposure for a relatively long time (e.g. 10% of the organism’s life span or longer (Walker et al. 2006)).

What is stress?

Any given environmental factor can become a “stress” to a given seaweed species, if it exceeds the upper or lower threshold values of tolerance. Seaweed communities are shaped by the complex interplay of a multitude of external biotic and abiotic factors and the intrinsic responses of the individual seaweed species. These factors are not stable over space or time, requiring frequent metabolic adjustments, termed acclimation (sec. 1.1.3). The genetic frame setting the limitations of acclimation is termed adaptation. Species-specific adaptation and the effectiveness of acclimation to change determine the competitive success of each species in the interaction with other species and thus shape the complex composition of a seaweed community in the field. For example, it is now well established that many biotic interactions of macroalgae (e.g. competition, predation, etc.) are mediated by the environmental stress, and the ways in which they manage it (Menge et al. 2003; Essay 2, Chapter 3). Major changes in abiotic factors occur along spatial and temporal gradients: spatially, on a global scale along latitudinal gradients, large changes in temperature, light availability, and seasonality are observed; along the coastline steep gradients in abiotic factors exist stretching from the intertidal to the subtidal zone; but even on very small scales the abiotic environment of seaweeds may change dramatically, e.g. within algal mats (Bischof et al. 2006b). Temporally, there are natural fluctuations of abiotic factors due to seasonal events, daily or tidal cycles, and climate variability such as El Niño Southern Oscillation (ENSO) events. The extent of natural change in the physico-chemical environment to which a seaweed species is exposed can be summarized by the term “habitat stability” and is often tightly linked to vertical zonation patterns along the phytal zone, with intertidal species populating the most demanding, least stable habitat (Davison and Pearson 1996; sec. 3.1). Apparently, the magnitude of the environmental stress along different spatial scales is important to explain the distribution patterns of macroalgae as was reported for rocky intertidal assemblages from Helgoland Island (Valdivia et al. 2011). Valdivia et al. (2011) indicated that vertical variation in community structure was significantly higher than patch- and site-scale horizontal variation but lower than shore-scale horizontal variation. Most concern and research effort is now directed towards the additional anthropogenic sources of variation in the abiotic environment, from the local to the global scale.

Introduction

The basic patterns of alternation of sporophyte and gametophyte must be regarded as a theme on which many variations are played (Fig. 2.1). Each generation may reproduce itself asexually, and sexual reproduction should be taken to include meiosporogenesis as well as gametogenesis and mating (Clayton 1988). Asexual reproduction allows an economical population increase but no genetic mixing, whereas sexual reproduction allows genetic mixing but is more costly because of the waste of gametes that fail to mate (Clayton 1981; Russell 1986; Santelices 1990). Most seaweeds use both means of reproduction, and, as Russell (1986) has noted, where there are isogametes, these can function equally as asexual swarmers. Vegetative reproduction by “multicellular propagules”, defined by Cecere et al. (2011) as “a vegetative, multicellular structure which detaches from the parent thallus and gives rise to a new individual”, is also common, for example Halimeda (Walters et al. 2002). However, their roles in species’ dispersal, and forming overwintering and resting “organs” that allow the survival of unfavorable environmental conditions, is unknown (Russell 1986; Cecere et al. 2011). Clonal seaweeds may spread by stolons and/or rhizomes, giving a significant competitive edge in the space race (sec. 1.2.3, 4.2.3). Some floating algal populations depend entirely on vegetative reproduction by fragmentation (sec. 3.3.7).

Culture studies are critical in establishing the range of possible life histories that can occur. Sufficient variations have been discovered in the basic pattern – between and within species – that today’s generalizations must be viewed only as working hypotheses. New variations in what are considered to be well-known life cycles are regularly uncovered. For example, male gametophytes of Laminaria digitata can reproduce themselves via fragmentation (Destombe et al. 2011). Although a basic alternation of a sporophyte (typically diploid) and a gametophyte (typically haploid) is common among seaweeds various extras and shortcuts are known (Fig. 2.1). Indeed, a better generalization may be that almost any alternation is possible, and even no alternation at all. Moreover, the term “alternation” is a misnomer, in that it implies only two phases and a regular progression from one to the other; clearly that is not always the case (e.g. Scytosiphon, Fig. 2.2). Maggs (1988, p. 488) concluded that “life-history patterns seem to be more labile than morphological features, and the role of life-history variability in speciation, and in ecological success, should not be underestimated”.

In their natural environment, seaweeds grow in exceptionally diverse and dynamic light climates. Water transparency and the continual ebb and flood of tides have profound effects on the quantity and quality of the light that reaches seaweeds at their growth sites, adding greatly to the variation already present in the irradiance at the Earth’s surface. The primary importance of light to seaweeds is in providing the energy for photosynthesis, energy that ultimately is passed on to other organisms. In addition, light perceived as a signal also has many photoperiodic and photomorphogenetic effects (see secs. 2.3.1, 2.3.3, 2.6.2). Thus, light is the most important abiotic factor affecting seaweeds, and also one of the most complex.

The principles of photosynthesis are similar in algae and higher plants, and indeed some principles (e.g. the Calvin cycle) were worked out using (mostly unicellular) algae. However, there are several important features of seaweeds and their habitats that stand in sharp contrast to those in higher, and mostly terrestrial plants, and it is on these that we shall focus. Such features include the diversity of pigmentation among marine algae and the diversity of the light climate in the oceans, the nature of carbon supply in the sea, and the diversity of photosynthetic products in different algal classes. This chapter focuses on the processes in eukaryotic algae. Reference is also made to the prokaryotic cyanobacteria, only to highlight evolutionary or functionally important differences or commonalities. It is assumed that the common details of photosynthetic mechanisms and pathways have been covered in introductory courses; they will be reviewed only briefly in the following section. Textbooks on plant physiology and biochemistry offer extensive treatments of all aspects of angiosperm photosynthesis (e.g. Buchanan et al. 2000; Raven et al. 2005). The accounts of radiation climate, light harvesting, and carbon metabolism presented here with respect to aquatic ecosystems owe much to the detailed books by Falkowski and Raven (2007) and Kirk (2010), which readers should consult for more information and references.

In their natural environment, seaweeds grow in exceptionally diverse and dynamic light climates. Water transparency and the continual ebb and flood of tides have profound effects on the quantity and quality of the light that reaches seaweeds at their growth sites, adding greatly to the variation already present in the irradiance at the Earth’s surface. The primary importance of light to seaweeds is in providing the energy for photosynthesis, energy that ultimately is passed on to other organisms. In addition, light perceived as a signal also has many photoperiodic and photomorphogenetic effects (see secs. 2.3.1, 2.3.3, 2.6.2). Thus, light is the most important abiotic factor affecting seaweeds, and also one of the most complex.

The principles of photosynthesis are similar in algae and higher plants, and indeed some principles (e.g. the Calvin cycle) were worked out using (mostly unicellular) algae. However, there are several important features of seaweeds and their habitats that stand in sharp contrast to those in higher, and mostly terrestrial plants, and it is on these that we shall focus. Such features include the diversity of pigmentation among marine algae and the diversity of the light climate in the oceans, the nature of carbon supply in the sea, and the diversity of photosynthetic products in different algal classes. This chapter focuses on the processes in eukaryotic algae. Reference is also made to the prokaryotic cyanobacteria, only to highlight evolutionary or functionally important differences or commonalities. It is assumed that the common details of photosynthetic mechanisms and pathways have been covered in introductory courses; they will be reviewed only briefly in the following section. Textbooks on plant physiology and biochemistry offer extensive treatments of all aspects of angiosperm photosynthesis (e.g. Buchanan et al. 2000; Raven et al. 2005). The accounts of radiation climate, light harvesting, and carbon metabolism presented here with respect to aquatic ecosystems owe much to the detailed books by Falkowski and Raven (2007) and Kirk (2010), which readers should consult for more information and references.