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The Biology and Ecology of Giant Kelp Forests
By David R. Schiel, Michael S. Foster UNIVERSITY OF CALIFORNIA PRESS
Copyright © 2015 The Regents of the University of California
All rights reserved.
ISBN: 978-0-520-96109-8
CHAPTER 1
INTRODUCTION TO GIANT KELP FORESTS WORLDWIDE
After a very attentive examination of many hundreds of specimens, we have arrived at the conclusion that all the described species of this genus which have come under our notice may safely be referred to as Macrocystis pyrifera.
— Hooker (1847)
Numerous recent studies on Macrocystis interfertility, genetic relatedness, and morphological plasticity all suggest that the genus is monospecific. We propose that the genus be collapsed back into a single species, with nomenclatural priority given to M. pyrifera.
— Demes et al. (2009)
TAXONOMIC CLASSIFICATION
Macrocystis, commonly called giant kelp but also known as giant bladder kelp, string kelp (Australia), huiro (Chile), and sargasso gigante (Mexico), is a genus of brown algae, a group characterized by containing the accessory photosynthetic pigment fucoxanthin that gives them their characteristic color. Historically, brown algae were classified as plants in the Domain Eukaryota, Kingdom Plantae, and Phylum (Division) Phaeophyta. The Plantae contained most terrestrial plants and also included two other common algal phyla with multicellular species, the green (Chlorophyta) and red algae (Rhodophyta). Collectively, the large marine species in these three phyla are commonly called "seaweeds." It is now recognized through modern techniques, however, that brown and red seaweeds have characteristics so distinct that they are separate from true "plants." High-resolution microscopy has revealed striking differences in plastid and flagella morphology among many of the traditional plant phyla, or groups within them, as well as similarities in flagella morphology and other characteristics to some colorless flagellates. These more fundamental relationships have generally been supported by analyses of genetic similarities and a better understanding of the role of endosymbiosis in shaping the photosynthetic apparatus. This flood of new information and interpretation has led to fundamental taxonomic rearrangements and the creation of new kingdoms, but there is still debate about appropriate classification (e.g., Parfrey et al. 2006). Revisions will no doubt continue, but the basic classification scheme of Cavalier-Smith (2010) is currently accepted by most phycologists (e.g., Graham et al. 2009, Guiry and Guiry 2012). This scheme places the former Phaeophyta within the Kingdom Chromista, Phylum Ochrophyta, Class Phaeophyceae, with "kelp" being the term used to refer to members in the order Laminariales (figure 1.1). Diatoms are the other major group in the Ochrophyta. The kingdom name Heterokontophyta is preferred by some researchers, others use Stramenopila (discussion in Graham et al. 2009), while some prefer the supergroup designation Chromaveolata (e.g., Adl et al. 2005, Cock et al. 2010).
Within the order Laminariales, giant kelp is now usually placed in the family Laminariaceae (Lane et al. 2006, Guiry and Guiry 2012). Based on genetic similarities, Yoon et al. (2001) placed Macrocystis within the family Lessoniaceae but Lane et al. (2006) argued this lacked bootstrap support. Genetic analyses in both studies indicate that the kelp genera Pelagophycus, Nereocystis, and Postelsia are most closely related to Macrocystis, forming a clade or two closely related clades within the family (figure 1.1). There has been considerable taxonomic work on Macrocystis and the genus is now considered to be monospecific, the sole species worldwide being Macrocystis pyrifera (discussed below). Pelagophycus,Nereocystis, and Postelsia are also considered to be monospecific (Guiry and Guiry 2012) and are endemic to the Northeast Pacific. All but Postelsia form subtidal kelp forests (Abbott and Hollenberg 1976).
"Kelp" originally referred to the calcined ashes resulting from burning large brown algae. It is sometimes used as the common name for all large brown algae, but particularly species in the order Laminariales. In this book, we use "kelp" to mean only species in this order. Some argue that kelps should be called chromistans, ocrophytes, phaeophyceans, etc., and not plants, because they are no longer in the kingdom Plantae. Although taxonomically correct, these names are awkward in usage, so we will refer to kelps and other algae as seaweeds, algae, or plants.
Macrocystis and its putative species have undergone considerable taxonomic revision since originally being described in 1771 by Linnaeus, who included it with other brown algae under the name Fucus pyriferus (reviews in Womersley 1954, Neushul 1971a, Coyer et al. 2001, Demes et al. 2009). Agardh (1820) placed F. pyriferus into a separate genus, Macrocystis, and described three species based on differences in blade and float (pneumatocyst) morphology. The number of species based on these characters increased to 10 by the mid-1800s. Hooker's (1847) extensive field observations indicated these characters were highly variable and he argued there was only one species, M. pyrifera. Recognition of variability in these characteristics led to species revisions based primarily on holdfast morphology. This character was not considered by early investigators because they relied on specimens collected by others, specimens that generally did not include holdfasts (Womersley 1954). More recent investigators examined plants as they grew in the field, and used holdfast morphology as the primary character to distinguish species. This resulted in three commonly recognized species in both hemispheres: M. pyrifera, M. integrifolia, and M. angustifolia (Womersley 1954, Neushul 1971a). Hay (1986) described a fourth species, M. laevis, from the subantarctic Marion Islands based on its unusually smooth blades (compared to rugose / corrugated blades in other recognized giant kelp species). Morphometric measurements and transplant experiments by Brostoff (1988) showed that the holdfast morphology of M. angustifolia populations described by Neushul (1971a) in California intergraded with that of M. pyrifera. M. angustifolia was subsequently considered to occur only in the southern hemisphere (e.g., Macaya and Zuccarello 2010a).
Holdfast morphology did not stand up to scrutiny as a species indicator, however, as more research was done. Field observations and transplant experiments have shown that holdfast morphology varies with environment and that blade smoothness also does not distinguish species well (review in Demes et al. 2009; figure 1.2). Genetic and molecular studies confirm that external morphological characters are not good discriminators of species. Lewis and Neushul (1994) showed that the three "species" (M. 'pyrifera' and M. 'integrifolia' from the Northeast Pacific, and M. 'angustifolia' from Australia) distinguished by differences in holdfast morphology could hybridize and produce normal sporophytes, and Westermeier et al. (2007) produced hybrids with normal sporophytes in crosses of M. 'pyrifera' and M. 'integrifolia' from Chile. Molecular taxonomic work comparing the similarity of noncoding rDNA internal transcribed spacer regions (ITSi and ITS2) by Coyer et al. (2001), and DNA barcoding (Macaya and Zuccarello 2010a) of all four "species" in the southern hemisphere and M. pyrifera and M. integrifolia in the northern hemisphere indicate that Macrocystis is a monospecific genus, and this was confirmed by Astorga et al. (2012). All these findings indicate there is only one species of giant kelp, M. pyrifera (Linnaeus) C. Agardh, and this is currently accepted (Guiry and Guiry 2012). Unless otherwise noted, therefore, we refer to this species in the text as giant kelp or Macrocystis. However, when referring to the literature on Macrocystis it can be advantageous for clarity to refer to the former species names. Where necessary we designate these, including M. 'pyrifera,' as ecomorphs by enclosing the ecomorph name in quotes.
EVOLUTION
The timing of origins of kelp and their relatives is problematic and not completely resolved, but significant progress has been made in the past 20 years. A variety of morphological, biochemical, and, most recently, genetic evidence indicates that species in the kingdom Chromista, as well as other photosynthetic eukaryotes, obtained their plastids via endosymbiosis with other organisms that took up residence inside cells (reviews in Yoon et al. 2004, Graham et al. 2009) early in the evolution of eukaryotic organisms. Primary endosymbiosis between prokaryotic cyanobacteria (blue-green algae) and eukaryotic protists resulted in the red and green algae (with green algae being the progenitor of "higher plants"). A secondary endosymbiosis between a uni cellular red alga and another eukaryotic protist resulted in the golden-brown algae, a lineage of which was the progenitor of kelps. Given the number of green chloroplast genes in the genome of the filamentous brown alga Ectocarpus siliculosus, the protist in the partnership that produced the brown algae may have been previously inhabited by a green chloroplast (Cock et al. 2010). Molecular clock methods indicate that red and green algae arose around 1500 Ma (Ma = SI unit for mega-annum or million years ago), and the secondary symbiosis that eventually led to the chromists occurred around 1300 Ma (Yoon et al. 2004) during the late Mesoproterzoic era, after the earth's transition to a more highly oxygenated atmosphere with an ozone screen (Cloud 1976). Fossil evidence (Cloud 1976) is consistent with these gene-based estimates. Medlin et al. (1997) suggested the chromists originated between 275 and 175 Ma (in the Permian-Jurassic period), but Yoon et al. (2004) suggested a much earlier origin at about 1000 Ma at the Mesoproterozoic-Neoproterozoic boundary, with the Ochrophyta arising soon afterward. An earlier study by Saunders and Druehl (1992) analyzed 5S rRNA similarities and concluded that the Phaeophyceae originated "within 200 Ma." Medlin et al. (1997) estimated this origin at 150-90 Ma (in the Jurassic-Cretaceous period) from a molecular clock analysis based on 18S rRNAs (figure 1.3).
The fossil record has not shed much light on the origins and radiation of kelp and other brown algae because, with the exception of a few lightly calcified species, they lack hard parts and do not fossilize well. There are no calcified Laminariales and the only fossil found so far that is generally accepted as a kelp is the extinct species Julescraneia grandicornis from the Miocene Monterey formation in southern California (Parker and Dawson 1965). This fossil consists of impressions on two rock fragments, one with a portion of a blade and another with "antler-like branches from a large pneumatocyst" (figure 1.4). Parker and Dawson (1965) interpreted J. grandicornis as having characteristics of modern Pelagophycus and Nereocystis, which are close relatives of Macrocystis (cf. figure 1.1). The deposit was dated at 13.5-7.5 Ma (upper Miocene). The molecular clock analyses of Saunders and Druehl (1992) and their review of similar analyses by others indicate kelps diverged from other brown algae 30-16 Ma (Oligocene-Miocene), and that morphologically similar kelp taxa radiated 3 - 6 Ma. These periods roughly correspond to those suggested by Lüning and Dieck (1990) based on temperature tolerances and paleo-oceanographic conditions (figure 1.3). Saunders and Druehl (1992) pointed out that "The extensive morphological variation observed among the kelp comes from genotypically similar plants." They reference other studies supporting these dates, including the fossil record of kelp-associated limpets, the number of monospecific kelp taxa, biogeographic distributions, and hybridization among kelps.
Various selective processes may have stimulated the radiation of kelp genera and species within the times discussed above. Evolutionary attention has been focused on processes in the North Pacific region because it contains the greatest diversity of kelps (review in Lane et al. 2006) and is therefore considered to be the likely area of origin and high diversification. Various processes have been hypothesized as being primary drivers of kelp evolution. Modern kelps occur in generally cool temperate waters and so the primary evolutionary processes are likely to be related to paleo-environmental changes that caused North Pacific waters to cool. A series of ice ages between 23.7 and 5.3 Ma (Miocene) cooled the North Pacific, as did the growth of the Isthmus of Panama, both of which generally coincided with the appearance of kelps (review in Stanley 2009). Some argue that trophic dynamics were a factor. For example, Estes and Steinberg (1988) wrote that kelp evolution in the region from Canada to northern Japan was facilitated by predatory marine mammals like sea otters that primarily foraged at depths shallower than 30 m, a depth range that coincided with the high-light zone that most kelps occupy. Their proposed mechanism was that by eating sea urchins, which can be extensive grazers of kelp, these mammals removed a potential impediment to kelp evolution. Domning (1989), a noted marine mammal biologist, countered their argument by pointing out that Stellar's sea cows (Hydrodamalis gigas, large, surface-dwelling, herbivorous marine mammals related to dugongs and manatees, which were hunted to extinction around 1770) and their relatives were also present, and grazing by these mammals may have affected kelp evolution. He questioned the assumption that the strength of the modern sea otter / sea urchin / kelp interaction applies to the past, given that the dynamics of kelp stands may have been quite different then. He further postulated that kelp diversification may have occurred in habitats, including those in deep water, that were inaccessible to predatory and grazing mammals.
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Excerpted from The Biology and Ecology of Giant Kelp Forests by David R. Schiel, Michael S. Foster. Copyright © 2015 The Regents of the University of California. Excerpted by permission of UNIVERSITY OF CALIFORNIA PRESS.
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