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What Is Canopy Biology? A Microbial Perspective*
CHAPTER 7
What Is Canopy Biology? A Microbial Perspective* Lynn Margulis
To be poor and be without trees is to be the most starved human being in the world. To be poor and to have trees is to be completely rich in ways that money can never buy. —Clarissa Pinkola Estes, T h e Faithful G a r d e n e r , 1995
The canopy at Tiputini, tributary of the JVapo River in Ecuador, is accessed by a magnificent three-tiered tower connected to three sets of hanging bridges constructed by Bart Bouricius some 40 m above the ground. I am especially proud because Bart, biologist and carpenter, is a neighbor and former student of mine in the graduate section of our Environmental Evolution course. I have more than once verified his reputation as the world's premiere designer-builder of canopy walkways, both temperate and tropical. In addition to the walkways at the Tiputini Biological Diversity Station, two towers of similar height permit views of the treetops. Emergent species are what first strike the eye. The viewer is drawn to a mental tracing of the curving river far below. Greenery of different shades topped by blue sky delight the walkway-climber as far as his or her view can fathom the recognizable. After a flight from Quito to Coca and a two-hour bus ride to the "canoa" (open-to-the-rain motor-powered riverboat), the visitor realizes that all evidence of people has receded. Roofed huts of fishing folk have given way to sunning birds, turtles, and palms on riverbanks profuse with a tangle of the unknown and unknowable liana, shrub, and tree. Experiencing the river, one wonders how any canopy could be, in principle, even more mysterious. For the next seven hours, down-river noise abounds—clacking, flapping, croaking, splashing, cawing, buzzing—but no human sounds other than the motor and murmurs of fellow boat people are heard. Speeding downstream, we marvel at the rapid currents and total absence of the 21st century—not even an airplane penetrates the wilderness. In this timeless land beside the river, the lush green appears nameless. Since 1977, in field studies and back in the campus laboratory, my students and I have studied a thriving ecological community of intertidal marine microbes, beholden to photosynthesizers of various types. At Laguna Figueroa in Baja California Norte, Mexico (see Figure 7-1), oxygenic Microcoleus, Lyngbya, and Gloeothece are underlain by the anoxygenic purple Thiocapsa and Chromatium. Certain hardy organisms, the resistant forms of Paratetramitus, in among the green and purple, are known to survive freezing and desiccation for more than five years. These Paratetramitus forms are difficult to distinguish from another hardy, similar-looking organism called Mychonastes desiccatus. These two kinds of life are the same size, the same spherical shape, and probably present in many populations in the same abundance. Distinguishing them in the community requires fluorescence for the chlorophyll wavelength. Both fluoresce when placed in A version of this paper appeared in Selbyana 22(2): 232-235; used with permission. 143
144
Lynn Margulis
*^^%.. ^ . •/*•« -u
Figure 7-1 Microbial mat communities. (A) An aerial view of Laguna Figueroa in Baja California Norte, Mexico. (B) Micmcoleus in microbial mats in situ (each unit of measure = 10 cm).
the ultraviolet spotlight but give off different colors. Mychonastes glows red, as chlorophylls enable it to photosynthesize, unlike Paratetramitus, whose fluorescent image reveals a green-glowing cyst wall. Beneath these two 8-micron spheres, greenish chlorobia of various types abound. Globules of sulfur give rise to hydrogen sulfide and other sulfurous gases, as we descend into the microbial community. Still further down in this vertically laminated ecological wilderness, at the low-tide level, Desulfovibrio and, presumably, Desulfobacter thrive. So, too, dwell Spirochaeta and the viviparous giant serpentine swimmer Spirosymplokos. A plethora of diatoms, Micmcoleus, Lyngbya, and Gloeothece, form the "canopy," in terms of Moffett (2000); Chromatium, Paratetramitus, Mychonastes,
7. What Is Canopy Biology? A Microbial Perspective
145
c Figure 7 - 1 — C o n t i n u e d (G) A hand sample (15 cm across) of a microbial mat community dominated by Microcoleus chthonoplastes (cyanobacterium).
and their associates comprise the understory. The emergent photosynthesizers (primarily diatoms), those gliding and swimming above the vertically laminated strata, tend to be brown and boat-shaped. Some 60 genera (perhaps 100 species) of these delicate-filigreed "emergents" have been identified at our field site by talented taxonomists. More than 200 distinguishable species documented in the literature are repeatedly present at our Mexican field site and at comparable cosmopolitan locales. Like the canopy seen fi:-om the swinging bridge built with plastic footholds by Bouricius, the vast majority of species in our field samples is unknown. We have an inkling of only those beings that survive mistreatment in the laboratory or greenhouse. The real number of the kinds of inhabitants in our samples is far more likely to be 1000 than the 210 or so that we and our colleagues have tabulated. A sample containing a thousand life forms cut from a marine microbial mat on the Pacific shore is but a 1 cubic millimeter in size. Similar samples from the delta of the Ebro River (Spain) or the shore at Matanzas (Cuba) are roughly 1 mm high by 1 mm deep by 1 mm millimeter long. How can the glorious canopy sample of Amazonia (say 100 X 100 X 50 km, so vastly larger than the microbial sample) possibly be analyzed by the amateurs who love her or even by the professionals who make her their life's work? Scientists admit to an extremely deficient view of our tiny microbial mat samples after more than two decades of study of this particular microcosm. We hardly know its major components and how the populations change in the most dramatic of temperature, salt concentration, and precipitation swings with the seasons. If so littie is known of a cubic millimeter, imagine my awe at the view from the tower of the Amazonian macrocosm (see Figure 7-2). "Life," sang John Lennon, "is what happens when you're making other plans." "Life" is what you see, smell, hear, and feel at the canopy tower. Words and numbers hardly make an organizational dent when attempting to describe the prodigiosity. Moffett (2000) makes a valiant attempt to regulate the unruly by delineating terms of canopy biology. At least he has ignored the pernicious financial jargon so detrimental to scientific analysis: benefit, cost, fitness, reciprocal altruism, and the like. Here I have an opportunity for a single suggestion, as I applaud his effort to stay as close as he can to the observations themselves. My suggestion regards terms for physical associations between organisms that are members of different taxa. First, abandon the use of common meaningless words. Purge the prose that uses
146
Lynn Margulis
Figure 7 - 2 At the Tiputini Biodiversity Station, this area under the canopy walkway may contain several hundred stable microbial communities that await study. Here we see the lower portion of a tree about 100 feet tall.
"host," "parasite," and other implied taxonomic categories such as "epiphyte" and "endophyte." Replace these with those pernicious terms that convey precisely what is meant. Why? Because the ambiguity intrinsic to these words is unavoidable and obfuscating. Topological, nutritional, and ecological concepts are not distinguished. Identificational, positional, metabolic, genetic, and temporal information becomes so conflated that these terms entirely lack meaning. All intertaxonomic physical associations that last for most of the life history of at least one of the partners are, by definition, symbioses. Such associations should never be classified by ecological outcome (e.g., beneficial, pathogenic, mutualistic, parasitic) because outcome always depends on particulars of environment and timing. Rather symbioses (whether strangler fig, vesicular-arbuscular zygomycotous fungi in the tissues of dicotyledonous plants, or bromeliads perched on palms) require analysis by level of association. By "levels" I mean whether the association is at the behavioral level (such as the topological relation of the bromeliad with the branch), metabolic level (such as the fungus that derives photosynthate from the dicot), or at the level of shared gene product (such as the nitrogen-fixing rhizobium of the Acacia or Mimosa root nodule), or even integration at the most intimate genie level (such as the Agrobacterium that sends its plasmid-borne genes to be incorporated into the plant cell's chromosomes in the crown gall). Often, in interspecific physical associations that are
7. JA^at Is Canopy Biology? A Microbial Perspective
147
ARBOREAL STROMATOLITES: A 210 MILLION YEAR RECORD m!M,mfmif»ii>i?i"-: t-^
Jessica Hope Whiteside Stromatolites (from Greek for "stony carpets") are lithified, microbially produced arches, spheres, or domes that can reach over one meter in height. Along with their nonlithified forerunners, microbial mats, stromatolites are widely assumed to have been the dominant form of microbial community life in the Precambrian. Stromatolites are dominated by cyanobacteria that shed their polysaccharide sheaths and move up in search of light in an incremental process (often less than 1 mm per year). The polysaccharide sheaths trap and bind sediment and calcium carbonate and the cyanobacteria provide photosynthate and additional compounds for other bacteria. (Another means of stromatolite growth is via the formation by cyanobacteria of their own carbonate network.) Originally known as "cryptozoans" ("hidden animals") because of their mysteriously biogenic shape, the first stromatolites to be correctly identified as containing and requiring bacteria for their precipitation were entirely marine. Freshwater stromatolites are also fairly common (Winsborough et al., 1994; DeWet et al. 2002; Whiteside et al., 2003). Fossil lacustrine examples include a '^210-million-year-old record of tree encrusting (arboreal) stromatolites (from 0.1 to +1 m in diameter) from the Newark Supergroup of Eastern North America (Whiteside et al. 2003), and in other age strata primarily in Wyoming (~50 Ma) and in California (-16 Ma). An analogy may be made between modern mats and stromatolites that inhabit hypersaline and otherwise extreme environments in space and lacustrine stromatolites arising during extreme climatic shifts (Olsen 1996) in time. For example, tufa calcite, stromatolitic coatings of carbonate on branches of trees from the Passaic Formation of the Newark basin have been interpreted to result from the transgression of the lake as low-lying vegetation is submerged. Fossilized arboreal stromatolites have been recovered from Triassic, Jurassic, Eocene, and Miocene lacustrine strata in North America. Gheirolepidiaceous conifers, encased by stromatolites and dated as old as ~210 and ~200 million years, have been uncovered from the Passaic and Towaco Formations of the Newark basin (Figure 1), and tree- and stem-encrusting stromatolites have also been retrieved from the East Berlin Formation in Connecticut and from the Scots Bay Formation in Nova Scotia, both about 200 Ma. Eocene fossils (~50 Ma) from the Laney Member of the Green River Formation in Wyoming (Figure 2) and Miocene forms (~16 Ma) from the Middle Miocene Barstow Formation in California provide more recent examples of "tree-hugging" stromatolites. In
Figure 1 Cross-section of Towaco (~200 Ma) Formation, Newark basin stromatolite from New Jersey. T h e remnants of the tree in cross section are represented by the dark oblong spearhead in the middle. T h e concentric stromatolitic rings suggest that this tree, a cheirolepidiaceous conifer, was upright and continued to grow after submergence. Continued
148
Lynn Margulis
ARBOREAL STROMATOLITES: A 210 MILLION YEAR RECORD-conf'd mmmmmmmrm'o.^ws'm^tiKr'^'f-^i
cyclical environments, as the climate shifts from arid to humid, the trunks and roots of flooded trees serve as temporary habitable zones for the anciently evolved stromatolites. Autoradiography of East Berlin, Towaco, Passaic (Figure 3), and Barstow stromatolites
Figure 2 Outcrop from Firehole Canyon in the Laney Member (~50 Ma) of the Green River Formation, Green River Basin in Wyoming. Left (panoramic perspective): Contiguous stromatolitic laminations embedded in cliff face. Upper right (close-up): lobate-shaped stromatolite with lithified remnant of tree trunk visible as dark end of cylinder protruding at right end of rock. Lower right (close-up): in situ photograph of wavy laminated stromatolite with two trees visible in cross-section at each end of photograph (light rings surrounded by concentric layers). Rock hammer for scale. Photograph courtesy of Malka Malchus.
Figure 3 Polished slab of stromatolitic tufa- (porous calcite-) coated branch from the Metlars Member (~210 Ma), Passaic Formation, Newark basin in Pennsylvania. Left: T h e central area with the light-colored calcite was a branch that provided the nucleus for stromatolite growth. Layers accrued from the center outward. Right:Autoradiograph of polished slab, showing a clear elevated uranium concentration with growth layers (dark areas). Photograph courtesy of Troy Rasbury.
7. What Is Canopy Biology? A Microbial Perspective
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suggests that the bacteria that form the coatings were also involved in uranium mineralization. As the climate becomes more humid, previous desiccated flats are vegetated. : As the expanding lake floods these flats, stromatolites encrust the trunks and exposed roots f of the drowned vegetation (De Wet et al. 2002) until they too are submerged below the photic zone, knocked down and transported, a n d / o r buried by accumulating muds. These arboreal stromatolites are very similar morphologically to living forms described by Winsborough et al. (1994) in spring-fed lakes and streams of the Cuatre Gienegas basin, Mexico. The 230-milllion-year record of tree-encrusting stromatolites shows that forms of life once thought to be solely marine and mostly ancient can, under extreme environmental conditions, form close associations, in freshwater and in Phanerozoic times, with submerged forest canopies.
References
__^____
DeWet, C. B., Mora, C. I., Gore, P . J . W., Gierlowshi-Kordesch, E., and Cucolo, S. J., 2002. Deposition and geochemistry of lacustrine and spring carbonates in Mesozoic rift basins, eastern North America. SEPM Special Publication 73: 309-325. Olsen, P.E., 1986, A 40-minion-year lake record of early Mesozoic orbital climatic forcing. Science 234: 842-848. Whiteside, J . H . , Olsen, P.E., and Rasbury, E.T. 2003. A 230 million year old record of arboreal stromatolites. Fourth International Symbiosis Society Congress Schedule and Abstracts. Etc. Press, Halifax, Nova Scotia, p. 173-174. Winsborough, B.M., Seeler, J-S., Golubic, S., Folk, R.L. & Maguire, Jr., B. 1994. Recent fresh-water lacustrine stromatolites, stromatolitic mats and oncoids from northeastern Mexico, pp. 71-100. In: Bertrand-Sarfati, J . & Monty, C. (Eds.) Phanerozoic Stromatolites II Kluwer Academic Publishers, Amsterdam. ^UXWemm.V^'^e^Airffj-'-]
symbioses by definition, the levels of partner association are simply not known, which needs to be explicitly stated. The topological and temporal bases of associations should be reflected in any permanent or casual physical association—at the canopy or below. Does the physical presence of one partner persist during the entire life history of both, as is the case for chloroplasts, mitochondria, and many fungi of plant roots? If impermanent for both, then, by definition, the association must be cyclical for at least one partner as, for example, the fungi that induce germination of orchid seeds. Terms like "endophyte" are particularly egregious since the "phyte" often refers to the fungal partner (and the fungi are, of course, in no way plants, even though "-phyte" is a Greek legacy). This type of rampant confusion and taxonomic ignorance by ecologists has a single major consequence. The field of ecology (which, in principle, extends far beyond the restrictions of academic biology, for example, into climatology, geology, paleontology, stratigraphy, atmospheric and soil sciences) is maligned, disdained, or ignored—except when desperately needed for practical (including financial-aesthetic) purposes like at Disneyland. If our descriptors employ unambiguous taxonomic information, such as that found in the list of aU taxa of afl organisms classified from phylum to class (Folch 2000), or for the higher taxa of kingdoms and phyla (Margulis and Schwartz 1998), one serious problem is resolved immediately. When ambiguous terms like "parasite," "endophyte," and "protozoa" are replaced by the actual taxonomic appeflations or the metabolic, temporal, and spatial relationships that are actually meant, the canopy and its biology will remain a mystery, but a somewhat less daunting one.
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References Estes, CD. (1995). "The Faithful Gardener: A Wise Tale about that which Can Never Die." HarperCollins, New York. Folch, R. (2000). The biosphere concept and index. In "Encyclopedia of the Biosphere." Volume 11, pp. 393-399. Gale Group, Detroit, Michigan. MarguHs, L. and Schwartz, K.V. (1998). "Five Kingdoms. An Illustrated Guide to the Phyla of Life on Earth." 3rd Edition. W.H. Freeman, New York. Moffett, M.W. (2000). What's "up"? A critical look at the basic terms of canopy biology. Biotropica 32(4a), 569-596.
What Is Canopy Biology? A Microbial Perspective* Lynn Margulis
To be poor and be without trees is to be the most starved human being in the world. To be poor and to have trees is to be completely rich in ways that money can never buy. —Clarissa Pinkola Estes, T h e Faithful G a r d e n e r , 1995
The canopy at Tiputini, tributary of the JVapo River in Ecuador, is accessed by a magnificent three-tiered tower connected to three sets of hanging bridges constructed by Bart Bouricius some 40 m above the ground. I am especially proud because Bart, biologist and carpenter, is a neighbor and former student of mine in the graduate section of our Environmental Evolution course. I have more than once verified his reputation as the world's premiere designer-builder of canopy walkways, both temperate and tropical. In addition to the walkways at the Tiputini Biological Diversity Station, two towers of similar height permit views of the treetops. Emergent species are what first strike the eye. The viewer is drawn to a mental tracing of the curving river far below. Greenery of different shades topped by blue sky delight the walkway-climber as far as his or her view can fathom the recognizable. After a flight from Quito to Coca and a two-hour bus ride to the "canoa" (open-to-the-rain motor-powered riverboat), the visitor realizes that all evidence of people has receded. Roofed huts of fishing folk have given way to sunning birds, turtles, and palms on riverbanks profuse with a tangle of the unknown and unknowable liana, shrub, and tree. Experiencing the river, one wonders how any canopy could be, in principle, even more mysterious. For the next seven hours, down-river noise abounds—clacking, flapping, croaking, splashing, cawing, buzzing—but no human sounds other than the motor and murmurs of fellow boat people are heard. Speeding downstream, we marvel at the rapid currents and total absence of the 21st century—not even an airplane penetrates the wilderness. In this timeless land beside the river, the lush green appears nameless. Since 1977, in field studies and back in the campus laboratory, my students and I have studied a thriving ecological community of intertidal marine microbes, beholden to photosynthesizers of various types. At Laguna Figueroa in Baja California Norte, Mexico (see Figure 7-1), oxygenic Microcoleus, Lyngbya, and Gloeothece are underlain by the anoxygenic purple Thiocapsa and Chromatium. Certain hardy organisms, the resistant forms of Paratetramitus, in among the green and purple, are known to survive freezing and desiccation for more than five years. These Paratetramitus forms are difficult to distinguish from another hardy, similar-looking organism called Mychonastes desiccatus. These two kinds of life are the same size, the same spherical shape, and probably present in many populations in the same abundance. Distinguishing them in the community requires fluorescence for the chlorophyll wavelength. Both fluoresce when placed in A version of this paper appeared in Selbyana 22(2): 232-235; used with permission. 143
144
Lynn Margulis
*^^%.. ^ . •/*•« -u
Figure 7-1 Microbial mat communities. (A) An aerial view of Laguna Figueroa in Baja California Norte, Mexico. (B) Micmcoleus in microbial mats in situ (each unit of measure = 10 cm).
the ultraviolet spotlight but give off different colors. Mychonastes glows red, as chlorophylls enable it to photosynthesize, unlike Paratetramitus, whose fluorescent image reveals a green-glowing cyst wall. Beneath these two 8-micron spheres, greenish chlorobia of various types abound. Globules of sulfur give rise to hydrogen sulfide and other sulfurous gases, as we descend into the microbial community. Still further down in this vertically laminated ecological wilderness, at the low-tide level, Desulfovibrio and, presumably, Desulfobacter thrive. So, too, dwell Spirochaeta and the viviparous giant serpentine swimmer Spirosymplokos. A plethora of diatoms, Micmcoleus, Lyngbya, and Gloeothece, form the "canopy," in terms of Moffett (2000); Chromatium, Paratetramitus, Mychonastes,
7. What Is Canopy Biology? A Microbial Perspective
145
c Figure 7 - 1 — C o n t i n u e d (G) A hand sample (15 cm across) of a microbial mat community dominated by Microcoleus chthonoplastes (cyanobacterium).
and their associates comprise the understory. The emergent photosynthesizers (primarily diatoms), those gliding and swimming above the vertically laminated strata, tend to be brown and boat-shaped. Some 60 genera (perhaps 100 species) of these delicate-filigreed "emergents" have been identified at our field site by talented taxonomists. More than 200 distinguishable species documented in the literature are repeatedly present at our Mexican field site and at comparable cosmopolitan locales. Like the canopy seen fi:-om the swinging bridge built with plastic footholds by Bouricius, the vast majority of species in our field samples is unknown. We have an inkling of only those beings that survive mistreatment in the laboratory or greenhouse. The real number of the kinds of inhabitants in our samples is far more likely to be 1000 than the 210 or so that we and our colleagues have tabulated. A sample containing a thousand life forms cut from a marine microbial mat on the Pacific shore is but a 1 cubic millimeter in size. Similar samples from the delta of the Ebro River (Spain) or the shore at Matanzas (Cuba) are roughly 1 mm high by 1 mm deep by 1 mm millimeter long. How can the glorious canopy sample of Amazonia (say 100 X 100 X 50 km, so vastly larger than the microbial sample) possibly be analyzed by the amateurs who love her or even by the professionals who make her their life's work? Scientists admit to an extremely deficient view of our tiny microbial mat samples after more than two decades of study of this particular microcosm. We hardly know its major components and how the populations change in the most dramatic of temperature, salt concentration, and precipitation swings with the seasons. If so littie is known of a cubic millimeter, imagine my awe at the view from the tower of the Amazonian macrocosm (see Figure 7-2). "Life," sang John Lennon, "is what happens when you're making other plans." "Life" is what you see, smell, hear, and feel at the canopy tower. Words and numbers hardly make an organizational dent when attempting to describe the prodigiosity. Moffett (2000) makes a valiant attempt to regulate the unruly by delineating terms of canopy biology. At least he has ignored the pernicious financial jargon so detrimental to scientific analysis: benefit, cost, fitness, reciprocal altruism, and the like. Here I have an opportunity for a single suggestion, as I applaud his effort to stay as close as he can to the observations themselves. My suggestion regards terms for physical associations between organisms that are members of different taxa. First, abandon the use of common meaningless words. Purge the prose that uses
146
Lynn Margulis
Figure 7 - 2 At the Tiputini Biodiversity Station, this area under the canopy walkway may contain several hundred stable microbial communities that await study. Here we see the lower portion of a tree about 100 feet tall.
"host," "parasite," and other implied taxonomic categories such as "epiphyte" and "endophyte." Replace these with those pernicious terms that convey precisely what is meant. Why? Because the ambiguity intrinsic to these words is unavoidable and obfuscating. Topological, nutritional, and ecological concepts are not distinguished. Identificational, positional, metabolic, genetic, and temporal information becomes so conflated that these terms entirely lack meaning. All intertaxonomic physical associations that last for most of the life history of at least one of the partners are, by definition, symbioses. Such associations should never be classified by ecological outcome (e.g., beneficial, pathogenic, mutualistic, parasitic) because outcome always depends on particulars of environment and timing. Rather symbioses (whether strangler fig, vesicular-arbuscular zygomycotous fungi in the tissues of dicotyledonous plants, or bromeliads perched on palms) require analysis by level of association. By "levels" I mean whether the association is at the behavioral level (such as the topological relation of the bromeliad with the branch), metabolic level (such as the fungus that derives photosynthate from the dicot), or at the level of shared gene product (such as the nitrogen-fixing rhizobium of the Acacia or Mimosa root nodule), or even integration at the most intimate genie level (such as the Agrobacterium that sends its plasmid-borne genes to be incorporated into the plant cell's chromosomes in the crown gall). Often, in interspecific physical associations that are
7. JA^at Is Canopy Biology? A Microbial Perspective
147
ARBOREAL STROMATOLITES: A 210 MILLION YEAR RECORD m!M,mfmif»ii>i?i"-: t-^
Jessica Hope Whiteside Stromatolites (from Greek for "stony carpets") are lithified, microbially produced arches, spheres, or domes that can reach over one meter in height. Along with their nonlithified forerunners, microbial mats, stromatolites are widely assumed to have been the dominant form of microbial community life in the Precambrian. Stromatolites are dominated by cyanobacteria that shed their polysaccharide sheaths and move up in search of light in an incremental process (often less than 1 mm per year). The polysaccharide sheaths trap and bind sediment and calcium carbonate and the cyanobacteria provide photosynthate and additional compounds for other bacteria. (Another means of stromatolite growth is via the formation by cyanobacteria of their own carbonate network.) Originally known as "cryptozoans" ("hidden animals") because of their mysteriously biogenic shape, the first stromatolites to be correctly identified as containing and requiring bacteria for their precipitation were entirely marine. Freshwater stromatolites are also fairly common (Winsborough et al., 1994; DeWet et al. 2002; Whiteside et al., 2003). Fossil lacustrine examples include a '^210-million-year-old record of tree encrusting (arboreal) stromatolites (from 0.1 to +1 m in diameter) from the Newark Supergroup of Eastern North America (Whiteside et al. 2003), and in other age strata primarily in Wyoming (~50 Ma) and in California (-16 Ma). An analogy may be made between modern mats and stromatolites that inhabit hypersaline and otherwise extreme environments in space and lacustrine stromatolites arising during extreme climatic shifts (Olsen 1996) in time. For example, tufa calcite, stromatolitic coatings of carbonate on branches of trees from the Passaic Formation of the Newark basin have been interpreted to result from the transgression of the lake as low-lying vegetation is submerged. Fossilized arboreal stromatolites have been recovered from Triassic, Jurassic, Eocene, and Miocene lacustrine strata in North America. Gheirolepidiaceous conifers, encased by stromatolites and dated as old as ~210 and ~200 million years, have been uncovered from the Passaic and Towaco Formations of the Newark basin (Figure 1), and tree- and stem-encrusting stromatolites have also been retrieved from the East Berlin Formation in Connecticut and from the Scots Bay Formation in Nova Scotia, both about 200 Ma. Eocene fossils (~50 Ma) from the Laney Member of the Green River Formation in Wyoming (Figure 2) and Miocene forms (~16 Ma) from the Middle Miocene Barstow Formation in California provide more recent examples of "tree-hugging" stromatolites. In
Figure 1 Cross-section of Towaco (~200 Ma) Formation, Newark basin stromatolite from New Jersey. T h e remnants of the tree in cross section are represented by the dark oblong spearhead in the middle. T h e concentric stromatolitic rings suggest that this tree, a cheirolepidiaceous conifer, was upright and continued to grow after submergence. Continued
148
Lynn Margulis
ARBOREAL STROMATOLITES: A 210 MILLION YEAR RECORD-conf'd mmmmmmmrm'o.^ws'm^tiKr'^'f-^i
cyclical environments, as the climate shifts from arid to humid, the trunks and roots of flooded trees serve as temporary habitable zones for the anciently evolved stromatolites. Autoradiography of East Berlin, Towaco, Passaic (Figure 3), and Barstow stromatolites
Figure 2 Outcrop from Firehole Canyon in the Laney Member (~50 Ma) of the Green River Formation, Green River Basin in Wyoming. Left (panoramic perspective): Contiguous stromatolitic laminations embedded in cliff face. Upper right (close-up): lobate-shaped stromatolite with lithified remnant of tree trunk visible as dark end of cylinder protruding at right end of rock. Lower right (close-up): in situ photograph of wavy laminated stromatolite with two trees visible in cross-section at each end of photograph (light rings surrounded by concentric layers). Rock hammer for scale. Photograph courtesy of Malka Malchus.
Figure 3 Polished slab of stromatolitic tufa- (porous calcite-) coated branch from the Metlars Member (~210 Ma), Passaic Formation, Newark basin in Pennsylvania. Left: T h e central area with the light-colored calcite was a branch that provided the nucleus for stromatolite growth. Layers accrued from the center outward. Right:Autoradiograph of polished slab, showing a clear elevated uranium concentration with growth layers (dark areas). Photograph courtesy of Troy Rasbury.
7. What Is Canopy Biology? A Microbial Perspective
149
suggests that the bacteria that form the coatings were also involved in uranium mineralization. As the climate becomes more humid, previous desiccated flats are vegetated. : As the expanding lake floods these flats, stromatolites encrust the trunks and exposed roots f of the drowned vegetation (De Wet et al. 2002) until they too are submerged below the photic zone, knocked down and transported, a n d / o r buried by accumulating muds. These arboreal stromatolites are very similar morphologically to living forms described by Winsborough et al. (1994) in spring-fed lakes and streams of the Cuatre Gienegas basin, Mexico. The 230-milllion-year record of tree-encrusting stromatolites shows that forms of life once thought to be solely marine and mostly ancient can, under extreme environmental conditions, form close associations, in freshwater and in Phanerozoic times, with submerged forest canopies.
References
__^____
DeWet, C. B., Mora, C. I., Gore, P . J . W., Gierlowshi-Kordesch, E., and Cucolo, S. J., 2002. Deposition and geochemistry of lacustrine and spring carbonates in Mesozoic rift basins, eastern North America. SEPM Special Publication 73: 309-325. Olsen, P.E., 1986, A 40-minion-year lake record of early Mesozoic orbital climatic forcing. Science 234: 842-848. Whiteside, J . H . , Olsen, P.E., and Rasbury, E.T. 2003. A 230 million year old record of arboreal stromatolites. Fourth International Symbiosis Society Congress Schedule and Abstracts. Etc. Press, Halifax, Nova Scotia, p. 173-174. Winsborough, B.M., Seeler, J-S., Golubic, S., Folk, R.L. & Maguire, Jr., B. 1994. Recent fresh-water lacustrine stromatolites, stromatolitic mats and oncoids from northeastern Mexico, pp. 71-100. In: Bertrand-Sarfati, J . & Monty, C. (Eds.) Phanerozoic Stromatolites II Kluwer Academic Publishers, Amsterdam. ^UXWemm.V^'^e^Airffj-'-]
symbioses by definition, the levels of partner association are simply not known, which needs to be explicitly stated. The topological and temporal bases of associations should be reflected in any permanent or casual physical association—at the canopy or below. Does the physical presence of one partner persist during the entire life history of both, as is the case for chloroplasts, mitochondria, and many fungi of plant roots? If impermanent for both, then, by definition, the association must be cyclical for at least one partner as, for example, the fungi that induce germination of orchid seeds. Terms like "endophyte" are particularly egregious since the "phyte" often refers to the fungal partner (and the fungi are, of course, in no way plants, even though "-phyte" is a Greek legacy). This type of rampant confusion and taxonomic ignorance by ecologists has a single major consequence. The field of ecology (which, in principle, extends far beyond the restrictions of academic biology, for example, into climatology, geology, paleontology, stratigraphy, atmospheric and soil sciences) is maligned, disdained, or ignored—except when desperately needed for practical (including financial-aesthetic) purposes like at Disneyland. If our descriptors employ unambiguous taxonomic information, such as that found in the list of aU taxa of afl organisms classified from phylum to class (Folch 2000), or for the higher taxa of kingdoms and phyla (Margulis and Schwartz 1998), one serious problem is resolved immediately. When ambiguous terms like "parasite," "endophyte," and "protozoa" are replaced by the actual taxonomic appeflations or the metabolic, temporal, and spatial relationships that are actually meant, the canopy and its biology will remain a mystery, but a somewhat less daunting one.
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Lynn Margulis
References Estes, CD. (1995). "The Faithful Gardener: A Wise Tale about that which Can Never Die." HarperCollins, New York. Folch, R. (2000). The biosphere concept and index. In "Encyclopedia of the Biosphere." Volume 11, pp. 393-399. Gale Group, Detroit, Michigan. MarguHs, L. and Schwartz, K.V. (1998). "Five Kingdoms. An Illustrated Guide to the Phyla of Life on Earth." 3rd Edition. W.H. Freeman, New York. Moffett, M.W. (2000). What's "up"? A critical look at the basic terms of canopy biology. Biotropica 32(4a), 569-596.