More to Pond Scum Than Meets the Eye

The Nature and Limits of Canopy Biology:
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Published in Selbyana 2001.

Mark W. Moffett, Museum of Vertebrate Zoology, University of California, 3101 Valley Life Sciences, Berkeley, CA 94720, U.S.A., moffett@uclink4.berkeley.edu

More to Pond Scum Than Meets the Eye

The Essence of knowledge is generalization.

-- Hans Reichenbach (1951)

Incorporating into canopy science all studies of all aboveground (aerial) plant organs and their occupants within any community, natural and agricultural (Moffett 2000), is taken as a given in this article, and represents only a first step in the development of a truly comparative discipline. Indeed, widely unappreciated by terrestrial "macrobiologists," the word "canopy" is used extensively by aquatic and microbial scientists to describe ecosystems that share many properties with terrestrial plant canopies. Below is a preliminary synopsis of canopy studies on several of these systems, especially those pertaining to the community-level physical structure of the sessile hosts, which, in contrast to hosts in terrestrial systems, are typically algal species and zooxanthellae-bearing animals rather than vascular plants (for an exception, see the review of seagrass communities, including issues bearing on canopy structure, by Williams & Heck 2001).

To encompass these kinds of hosts, "canopy" can be redefined from Moffett (2000) as the parts of any community of sessile organisms that emerge from a substrate. Canopy biology (or canopy science) is by this criterion the study of that portion of the community, including the organs of the sessile individuals and any affixed products of those organisms, and anything in, on, or between those organs and products. The affixed "products" can be dead organisms (such as tree snags), the skeletons of living corals, and algal mucilage.

In this paper, "sessile" describes an organism that emerges from or adheres to a substrate at positions fixed over a large part of its life history. "Substrate" refers to any surface or structural matrix that provides points of attachment for a sessile species, fixing the location of individuals or colonies. The substrate thereby establishes the spatial relations between sessile individuals, including to some degree the organs that project into the fluid medium (the "canopy structure"); in turn, the sessile communities variously transform and stabilize the substrate (e.g., Stevenson 1996). (Many authors have applied "structure" and "architecture" to communities less literally than I have here, for example to nonphysical attributes of organization, such as to niche spaces and tropic hierarchies, e.g., Connell 1975) The substrate typically is a solid, but the air-water interface may give some level of stability to the relative position of organisms, such as in floating algal mats (metaphyton). I exclude from the canopy communities or portions of communities distributed entirely within the substrate matrix, as in the terrestrial soil community or its aquatic equivalent, the epipelic or bottom sediment community (consider for example the microphytobenthos: MacIntyre et al. 1996). I also exclude organisms located outside the canopy in the medium, namely most plankton or aerial plankton. As discussed in a later section, for many purposes these distinctions can be arbitrary. For example the same morphological adaptations of algae for attachment to substrates may be used for attachment to other algae to produce colonies in suspension (Stevenson 1996).

In some situations, the canopies of "different" ecosystems be studied as one. In the shade of a forest, stream-dwelling algae may show some of the same physiological adaptations as understory terrestrial plants (Robinson & Minshall 1986, Hill 1996).

Kelp canopies. Describing kelp communities off South America, Darwin (1839) wrote, "I can only compare those great aquatic forests of the southern hemisphere with the terrestrial ones in the inter-tropical regions." The term "kelp forest" has been common in the literature ever since. Application of the term "canopy" to kelp began with Jack Kitching, who, using a milk can with a window made from an old glass cookie box, was the first scientist to successfully dive into this ecosystem (Kitching et al. 1934; the human-biased perspective of experiencing a matrix of sessile organisms from within may be significant in the choice to apply the word canopy to systems such as forests or kelp: Moffett 2000). In these and other algal communities, there is a relationship between canopy height and algal growth form (Neushul 1972, Hay 1986, Steneck & Dethier 1994). All kelp forests convergently accommodate guilds of species that fall into five distinct "canopies," or strata (including coralline crust as a stratum: Dayton 1985) (Fig. 1). The largest and most complex canopies occur in shallow, productive sites (Vadas & Steneck 1988), however, as might be predicted given that water attenuates light sharply as compared to air in terrestrial communities. Indeed, illumination declines logarithmically as it passes through water, as it can passing through either aquatic or terrestrial vegetation as a result of shading, but of course in the former case attenuation occurs over a much larger scale.

Many findings from kelp forests parallel those for terrestrial communities, such as light attenuation through strata in relation to frond coverage (Gerard 1984), which at the benthos beneath kelp communities often declines to ca. 1% of surface light, as is common in tropical rainforests (Richards 1996); the importance to succession of disturbance and gaps (Neushul 1971, Foster 1975, Dayton 1975a, Hurby 1976, Pearse & Hines 1979, Reed & Foster 1984, Dayton et al. 1999); the importance of sun flecks to understory growth and survivorship (Wing et al. 1993); differential survivorship resulting from the shading of benthic plants (Kastendiek 1982, Santelices & Ojeda 1984, Dean et al. 1989) and phytoplankton (Borchers & Field 1981), and other diverse competitive effects leading to specialized shade-tolerant (understory) communities (Dayton 1975b, Dayton et al. 1999). Unless predation is severe, sessile animals may outcompete kelp in low-light conditions in deeper parts of the benthos (Foster 1975), a pattern that holds to some extent in understory shade in shallower waters, though low-light adapted algae also occur there. Dayton (1971) distinguishes competition for space on the substrate ("primary space") from competition within the volume above that surface, that is, within the canopy ("secondary space"), a concept worthy of widespread application. Because of their flexible tissues, kelp and other (Carpenter 1986) algal communities could in some ways be more ecologically comparable to grassland than to terrestrial forest (but see Holbrook et al. 1991), even though kelp can rise 50 m or more in height. Because of their reliance on the opportunities for flotation offered by water, the capacity for upward growth in kelp is of course greatly enhanced over nonwoody terrestrial plants.

There have been general studies on the relation between canopy residents and kelp forest structure. Many fish stratify in a kelp forests, although this generally becomes less pronounced as the fish mature (Anderson 1994). Manipulations of physical structure are common in the study of kelp communities, showing for example that simplifying canopy structure can increase fish mortality by removing refuges (Anderson 2001). Predators can be so efficient at feasting on prey passing through kelp canopies that recruitment to ecosystems closer to shore is strikingly reduced (Gaines & Roughgarden 1987). Shading by the kelp overstory can reduce algal growth rates in lower strata, thereby altering the abundance of some fish relative to canopy gaps (Carr 1989, Schmitt & Holbrook 1990, Jones 1992). In algal mats on boulders and within tide pools, canopy-resident diversity relates to algal architectural complexity (Dean & Connell 1987, Hacker & Steneck 1990; for a successional study of this kind of ecosystem, see Sousa 1979). Williams & Seed (1992) review the positive and negative effects of epiphytic animals on large algae.

Periphyton and algal turf canopies. Periphyton (aufwuchs) constitute a "complex community of microbiota (algae, bacteria, fungi, animals, inorganic and organic detritus) that is attached to substrata" (Wetzel 1983; for further terms, see Wetzel 1979) -- the microbial equivalent of an epiphyte mat. Indeed, periphyton can be epiphytic (Ruinen 1961, 1975, Morris et al. 1997, Claflin 1968; for the rhizosphere equivalent, see Pearce et al. 1995), albeit "periphyton" also applies to growth on nonliving or deceased substrates, such as submerged leaf litter and carcasses that teem with predictable successions of microorganisms. Periphyton "have extensive vertical development on a small scale, and cells within the community matrix are tightly packed" (Boston & Hill 1991). They show a repeatable pattern of succession (Lowe et al. 1996). This pattern can be disrupted by a high disturbance regime as occurs with communities on the surface of sand grains (Miller et al. 1987) except when algal mucilage binds the grains together, allowing further community development (Hoagland et al. 1982). Succession proceeds from a monolayer community to a stratification of species and chemistry within a matrix of cells and their secretions (Jørgensen & Revsbech et al. 1979, 1983, Kuenen et al. 1986, Lassen et al. 1994, Johnson et al. 1997) (Fig 2). Stalked microalgae can contribute to the greater depth of late-successional communities, resulting in "an upperstory of growth perhaps functionally analogous to the canopies characteristic of terrestrial forests" (Hoagland et al. 1982). The upper stratum provides attachment points for diatoms that are specialized as epiphytes (Roos 1979, Roemer et al. 1983), described as "dependent organisms" or pseudo-periphyton, and treated as part of the same community as their hosts (Sládecková 1962). While some sessile algae cannot adhere to other algae and so require a direct connection with the substrate, other species may preferentially attach to algae in the layer below and thereby epiphytically form a canopy stratum of their own (Fig. 2a). This strategy is unknown for terrestrial canopies. Vines positioning their foliage uniformly above that of their hosts (Putz 1995) may approach it, although being rooted to the ground these canopy plants are of course not epiphytes.

Canopy complexity of periphyton may be greater at sites with higher light intensities (Hudon & Bourget 1983). Furthermore, the internal physiognomy depends on local flow regime, in part because, for example, greater turbulence increases the penetration of nutrients and light (Peterson 1996). (Wetzel [1993] argues in contrast that such penetration is rare, and that the high productivity of periphyton is a result of efficient recycling of nutrients within their canopies.) Growth of the outer layer can shade the strata below (Johnson et al. 1997, Dodds et al. 1999) and block nutrient inputs to the understory (McCormick & Stevenson 1991, Peterson & Grimm 1992). Shading can lead to understory deterioration (Stock & Ward 1991) in time causing a community to slough from its substratum (Meulemans & Roos 1985). Substrates are colonized both by these detached communities (detrital microcosms: Korte & Blinn 1983) and by isolated cells in suspension (Stevenson 1983). Sloughing can be reduced where understory algae species can produce more photopigments or become increasingly heterotropic in dim conditions (Tuchman 1996, Peterson 1996), in which case the periphyton can last longer and achieve higher biomasses. Because of the cycle of growth, death, and sloughing, the community that establishes after a site is scoured by herbivores may depend on the prior successional status at the site (Peterson 1996), among other factors (Tuchman & Stevenson 1991).

Turfs are filamentous periphyton communities, typically a few millimeters high (Fig. 3) that occur widely on coral reef surfaces and produce the bulk of reef primary productivity (Adley & Steneck 1975). Disturbances (say, by herbivores) reduce turf height and increase light penetration and turbulence through their canopy (Carpenter 1986, Williams & Carpenter 1990 Carpenter & Williams 1993, Cheroske et al. 2000). Stratification can occur within turfs, but is limited (Hackney et al. 1989, R.C. Carpenter, pers. comm.).

Bacterial films. Until the 1980s, bacteria were studied only by traditional sampling and culture methods. Extrapolations from monospecies laboratory cultures led to serious misunderstandings about bacterial ecosystems (Costerton et al. 1995). In fact, almost all bacteria live packed within surfacebound multispecies communities (Molin et al. 2000, Watnick & Kolter 2000) called biofilms. When the bacteria and their accumulated remains form thick accretions, biofilms are called microbial mats or "stromatolites," which can include eukaryotes (Stal 2000). Indeed, biofilms often intergrade with eukaryote-dominated periphyton, and increasingly the term has been used broadly to include periphyton and even fungi (Reynolds & Fink 2001). In the algal dominated systems discussed in the previous section, for example, bacteria colonize early in succession (Hoagland et al. 1982), and, in combination with certain diatoms and fungi, "precondition" the substrate for adherence of algae (Korte & Blinn 1983, Burkholder & Wetzel 1989). In a developed periphyton community, the bacteria can be nutritionally dependent on excreted algal products (Haack & McFeters 1982, Sobczak 1996). The remainder of this section will focus on communities dominated by bacteria.

For macroscopic canopies, interest typically falls into two arenas: studies of the substrate-bound species themselves (the hosts), and studies on species that live within the canopy generated by the hosts (canopy residents). This distinction is apparently of limited utility for bacterial biofilms and mats, which are formed of cells en masse (Fig. 4). The internal organization of films and mats (including stratification, with anaerobic or anoxic species often occupying the depths of a film: Jørgensen et al. 1986, Sagan & Margulis 1988: 53-54, Ramsing et al. 1993) is revealed by microscopic techniques (Molin et al. 2000) and other methods (Wimpenny 1992, Lewandowski et al. 1993, Kühl et al. 1994). Light penetration and chemical gradients are critical to the structuring of these communities (Jørgensen & Revsbech 1983, Revsbech et al. 1983, Wimpenny & Kinniment 1995, Stal 2000). While most biofilm residents are sessile or at least relatively immobile within the cell matrix (Costerton et al. 1995) the integrity of biofilms may be as much a product of a secreted matrix of polymers as of the fixed location of organisms. Thus motile species can shift position within the film – for example, moving to different "microzones" (strata) – in response to light or chemical cycles (Doemel & Brock 1977, Garcia-Pichel et al. 1994, Stal 2000; this is also true of some periphyton-dwelling diatoms: Johnson et al. 1997). Biofilm residents are phenotypically distinct from conspecific planktonic forms, which are often physiologically dormant and function as a dispersal stage. The sloughing of bacteria from films, adhesion of the colonists to a surface or within the matrix, and other aspects of establishment and development of films have been documented or modeled in three dimensions (Bryers 2000), as has the succession of residents through time (Paerl 1985, Lawrence et al. 1995, Korber et al. 1995, Jackson et al. 2001).

The matrix of bacteria in a biofilm is typically described as developing channels or pores through which nutrients enter and wastes leave the community (Costerton et al. 1994, Massol-Deyá et al. 1995, Stoodley et al. 1999a). The structure of many biofilms is so fragmented by these "waterways" that on close inspection they do not resemble a "film" at all but rather a landscape of coneshaped and mushroomshaped bodies called "microcolonies" distributed intriguingly like trees in a forest (Fig. 4). When mature the microcolonies may grow into contact, but they do not fuse so that they wave past each other when shear forces operate (J.W. Costerton pers. com.). Although not universal (Wimpenny & Colasanti 1997), microcolony formation is widespread in natural and artificial systems, both for monocultures and for mixed-species communities, and is presumed to result from nutrient limitation and niche exploitation (Costerton et al. 1995). The distribution of microcolonies (including both the cells and the exopolymeric materials they secrete) and the channels and other spaces between them is referred to as biofilm "architecture" (Lawrence et al. 1991). Both the species composition and the nature of the substrate effect this architecture (Costerton et al. 1995, Wimpenny & Colasanti 1997). So does water flow around biofilms, which may cause entire microcolonies to drift across a surface (Stoodley et al. 1999b), straining the definitions of "sessile" and "canopy."

The advantages of living in biofilms include the proximity to nutrients associated with surfaces, buffering from external chemistry, and modulation of physical conditions within a film, as well as resistance to drying, to predation by protozoa, to infection by bacteriophages, and to antibiotic therapy and other chemical treatments (Allison et al. 2000). Microbiologists describe biofilms as coordinated communities with "primitive homeostasis, a primitive circulatory system and metabolic cooperativity" that can "resemble the tissues formed by eukaryotic cells" (Costerton et al. 1995, Costerton & Lappin-Scott 1995) perhaps as a result of rapid evolution through gene transfer within the films (Hausner & Wuertz 1999). There appears to be a stronger interdependency between different species in a biofilm than there is between most plants in a forest, such that certain bacteria depend on the metabolic products of other microbes (Kühl et al. 1996, Molin et al. 2000, Paerl et al. 2000) and show other forms of cooperation (Crespi 2001). In addition to these mutualistic "consortia," biofilms and microbial mats are home to diverse competitive and predator-prey interactions (Lawrence et al. 1995, Allison et al. 2000). A question wide open for investigation is how selective forces operating in the establishment and development of biofilms lead in time to cohesive systems that appear stable, functionally integrated, and structurally convergent.

Stolzenbach (1989) applied the word "canopy" to biofilms. Indeed, microbial communities could be easily manipulated for studies of canopy structure: various combinations of microbial species or strains could be mixed, centrifuged, and allowed to form biofilms to investigate assembly rules for canopies under specified nutrient or substrate regimes.

Coral reefs as canopies. Dahl (1973) writes of coral reefs that "organisms often occur in many layers and the substratum itself is organism generated." Because of the abundance of sessile animals throughout these layers, marine scientists are less concerned than plant-focused terrestrial canopy researchers with the phyla of the substrate organisms. It’s not surprising, then, that overarching corals have been described as producing a "canopy" overtopping an "understory" community (Baird & Hughes 2000). While a coral’s supportive structure is not living, it is an immediate by-product of living things and therefore can be treated as a part of a canopy in much the same way as snags are treated as part of a terrestrial canopy. Actually, there is a veneer of living tissue on live coral, much as there is a small zone of living phloem surrounding the mostly "dead" xylem of trees, so that in fact in both ecosystems a large part of the structural foundation of the canopy is dead.

Somewhat like trees (Horn 1971), the architectures of photosynthetic corals change with light regime (Porter 1976). Death or suppression of the growth of corals from shading by other corals results in an understory that can include shade-tolerant phototropic species (Stimson 1985) and that incorporates abundant sessile heterotrophs (Karlson 1999, Baird & Hughes 2000). Other shade-tolerant (or, in the case of sessile animals, shade-indifferent) species can densely occupy the undersurfaces of the corals themselves (Jackson et al. 1971, Maida et al. 1994). Colonization of these habitats can depend on active larval choice for "cryptic" (shaded) microsites (Maida et al. 1994, Mundy & Babcock 1998). The change of species composition with shading can parallel community changes resulting from light falloff with depth in the water column, such that understory shade permits certain deep-water species to extend their distribution into shallow water. In general, however, these understory corals are distinct from reef-building corals, as the latter, when adapted to dim conditions, tend to specialize on deeper or more turbid water. Other species prosper in the gaps formed by the death of overstory coral colonies, yielding a habitat mosaic (Stimson 1985). The coral reef community includes algae (among them the turfs discussed previously) that show a complex pattern of competition depending on their heights and interfrond densities (Steneck 1997). The structural complexity of coral reefs provides for a high abundance and diversity of canopy-dwelling organisms, such as fish (Dahl 1973) and zooplankton (Porter 1974).

Other canopies. Various other sessile animals form dense aggregations that could be studied as canopies including both clonal (e.g., anenomes, bryozoans, ascidians) and nonclonal species such as mussels and barnacles (Paine & Suchanek 1983). Further, if we allow that communities of these organisms have canopies we can apply the idea of an extended phenotype (that is, extending the definition of phenotype to include nonliving products of an organism such as nests or retreats: Dawkins 1982, Turner 2000) to enlarge the concept of canopy almost indefinitely, depending on our interests. Least controversial would be static structures like coral skeletons whose architectures and spatial relations are produced directly by living things. Tubes of polychaetes (Bell & Coen 1982) and stream fly larvae (Pringle 1985) attract assemblages of plants and animals. These structures recolonize rapidly after defaunation, forming communities organized around tube architecture (Bell & Coen 1982). On land, patches of earthworm castings (Maraun et al. 1999) or of fungal fruiting bodies (O'Connell & Bolger 1997) are possible analogs of plant canopies.

Systems that are not canopies by any definition could be useful models for examining canopy life. Suspended bacteria can stratify under conditions of low turbulence (Guerrero & Mas 1989). Studies of the planktonic cells show that "increased productivity produces a physical scaffold to support biological heterogeneity (as, for example, in the spatial complexity of forest canopies) on which other species can build" (Morin 2000).

Mineral Acquisition. In terrestrial communities, the capture of atmospheric nutrients by canopies may be significant to mineral budgets (Lindberg et al. 1986). Regardless, the possibility that productivity in these communities can be limited by atmospheric minerals remains to be proved, and clearly most habitats depend almost entirely on the substrate for mineral nutrition (for an exception, see Art et al. 1974) . The situation is reversed in most aquatic and microbial communities, which absorb nutrients from water, a medium with a higher capacity to deliver nutrients than air (Lobban & Harrison 1997). These communities show complex patterns of cycling of the nutrients within their canopies (Burkholder 1996; indeed, internal cycling may become increasingly important with increasing canopy complexity during succession, reducing loss of resources from the system: Sand-Jensen 1983, Paul & Duthie 1989, Peterson & Grimm 1992). Algal holdfasts are believed to be just that: organs specialized at holding on to substrates. Although the complete absence of nutrient absorption from these organs is a commonplace assumption, holdfasts are localized structures without any rootlike proliferation of surface area presumably necessary to efficiently exploit substrates for nutrients. Further, most algal communities grow on rock, sand, and other relatively nutrient-poor substrates. In these situations, nutrient inputs are likely to be greatest in the upper (outer) canopy rather than at the substrate level, and therefore traits adaptive for light and nutrient procurement ideally will function in synchrony (McCormick 1996).

Seagrass ecosystems are an exception, in that these marine angiosperms receive most of their nutrition from the rich sediments into which they root (Williams & Heck 2001) and a few algae in the same communities produce rootlike rhizoids that absorb substrate nutrients as well (Williams 1984). Biofilms and some periphyton (Pringle 1990) are a second exception: those on organic matter clearly receive the preponderance of their nutrition from the substrate. Actually, this can also be true on inert surfaces like plastic or metal, at least in the initial growth phase of a bacterial community. Through surface charges and other effects, these substrates tend to concentrate mineral ions and organic matter from solution, encouraging biofilm establishment (Bryers 2000). Otherwise, the dependence of aquatic systems on minerals in solution and the direct relation between the rate at which nutrients are encountered in a medium and the flow of the medium means that the growth of affixed aquatic systems can be limited by the availability of waterborne nutrients (Atkinson 1988, Stevenson & Glover 1993, Carpenter & Williams 1993, Lobban & Harrison 1997, Sebens 1997, Hurd 2000). With sufficient water flow, even seagrass beds absorb a significant portion of their nutrient requirements through their canopies (S.L. Williams, pers. com.).

Continue reading this paper:

Abstract

Seeing the Forest for the Herbs

More to Pond Scum Than Meets the Eye

The Geometry of Canopy Biology

Getting to the Root of the Matter

Conclusions