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

Getting to the Root of the Matter

Both in the application of words and as a subject of study, much of terrestrial canopy biology has been based on our conception of sessile species as physical supports for other organisms. Because most substrates in a canopy are the parts of living organisms, a particular concern is the "social" (often interspecific) aspects of support, such as trees as supports for vines or vines as supports for trees (consider that by interlinking a canopy, vines could prop up weak trees or pull down neighboring trees when a tree does topple: Smith 1973, Putz & Mooney 1991). The word epiphyte can similarly imply a support function for a host or at least direct physical association with a host, as this term is widely defined by terrestrial scientists as a plant growing on another plant. "On" signifies intimate and superficial, that is nonendophytic, contact, without reference to gravity: thus, moss growing on the underside of a branch is "on" the tree.

[Footnote: An epiphyte mat (canopy plants and associated suspended soils in aggregate) unambiguously lies on a tree. Formally, however, an epiphyte growing in the suspended soil or in an ant carton nest is not necessarily "on" the tree, any more than the tree is "on" the earth's core, though these epiphytes are commonly included in the set of plants "on" a tree, apparently by loose application of the "canopy plants and soil in aggregate" perspective. Exclusion of animals that live and grow on plants from the epiphyte category may be attributed in part to the restriction of epiphyte to sessile residents, which is often how the word is used in marine biology. At least in terms of mobility on an appreciable scale relative to the host-plant size, epiphytes include most plants, fungi, and microbes. Nomadic vines (Moffett 2000) and insect scales, however, may render adherence to a strictly taxonomic interpretation problematic, if not archaic.]

The idea of "a plant growing on another plant" can be found as well in the rhizosphere literature, however. Roots of a plant can be said to grow on those of another in the sense that a tree's underground root mass may grow "on" bedrock. Still, in contrast to the aerial-plant literature, almost no data exists on the role of physical support between plant individuals in the rhizosphere. Studies to date on support functions of roots have treated each plant in isolation (e.g., Ennos 2000). But despite confounding effects from competition for space and nutrients (e.g., Atkinson et al. 1976, Mahall & Callaway 1992, Burgess et al. 1998), root systems in nature are seldom isolated: consider the drawings in Weaver & Clements (1929) of herb and grass communities (the distribution of tree roots is not known to this detail, but see Chilvers 1972, Lyford 1975, and the figures in Külla & Lõhmus 1999). Coutts (1986) writes that the "interlocking of thicker roots between adjacent trees can have a substantial effect" on anchorage. He notes that if one Sitka spruce is uprooted, neighbor trees with interlocking roots are likely to topple with it (Coutts 1983). Vogel (1996) ascribes a supportive function to the "diagonal guying" by tangled bamboo roots, while Keeley (1988) and Basnet et al. (1993) ascribe a likely supportive role to natural root grafting, which is common in trees. Only the roots within a few meters of the base of a large tree are significant to anchorage (Ennos 2000), meaning such interactive effects may have to occur inside that radius. Yet in spite of the obvious role of the soil itself in plant support, there’s no reason to assume the role of physical support between plant individuals is any less significant belowground than aboveground, at least for certain substrates and communities. Even for herbs, it is the commonplace observation of any gardener -- apparently not the subject of study as yet -- that pulling up one plant can cause full or partial dislodging of neighboring plants. This suggests structural support exists between forbs, insomuch as that the presence of neighbors may add to the force required (say, by a herbivore) to extract a given plant. (Incidentally, physical support between individuals within the substrate is likely to be absent for most if not all aquatic and microbial communities of affixed organisms, given that taxa such as algae and corals lack elaborate belowground organs.)

For terrestrial systems, I explicitly identify "epiphyte" with residents of aboveground plant organs, that is, the canopy (Moffett 2000), conforming with the word's use in practice. Giving the literature on roots due consideration, commonplace definitions such as Barkman (1958) phrased in terms of "plants on other plants" are not at all clear on that score. This ambiguity may be unintentional. Still, based purely on the word's derivation (epi = on, phyte = plant) and the scarcity of clear definitions to the contrary, we may conclude that if one organism grows in physical intimacy with (on the surface of) a larger one (its host), and that larger one is a plant, the smaller individual could be called an epiphyte even if it occurs within the rhizosphere; after all, the term in general currency today is epiphyte, not air plant. Because such usage would break with convention among terrestrial ecologists, however, a more satisfactory choice to denote "a plant growing on another plant" would be "epibiont," a term common in marine biology (Wahl 1997). For example, definitions of epiphytes as "plants on plants" apply equally to any canopy plant, be it vine, mature hemiepiphyte or nomad, as confirmed by wordings used throughout the literature to indicate the position of these plants with respect to the host (for example, see Putz & Mooney 1992, Ray 1992, Lawton & Williams-Linera 1996).

Admittedly, beyond microbes such as mycorrhizae, root parasites, hemiparasites such as certain Scrophulariaceae, and plantlets growing from root buds, it remains problematic which subterranean associates might be considered epibiontic (or "epiphytic") on this basis. Whether or not the idea of epiphytism could (or should) ever be applied to the subterranean realm, my point is that the traditional split between rhizosphere and canopy can be arbitrary, which has fragmented of our understanding of life on or in plant bodies.

Does this apply as well to our understanding the plants themselves? Roots evolved from shoots prior to the evolution of leaves (Barlow 1994), and have remained developmentally distinct from leaves, without intermediates except in extraordinary cases (e.g., Von Teichman und Logischen & Robbertse 1977). In allorhizic species (dicots and most monocots), the difference begins to be expressed within the embryo, whereas in homorhizic plants (some monocots and all pteridophytes) it’s not, and furthermore homorhizic species lack a root "system" in that all roots originate adventitously from within the shoot system (Groff & Kaplan 1988; in both groups roots can also arise from shoots and shoots from roots). In separating canopy from rhizosphere, however, it is especially significant that roots and shoots are not necessarily distinguishable in either function or location relative to the ground surface: shoots can absorb nutrients and water (Parker 1983, Schaefer & Reiners 1989) and can occur belowground, where they are referred to as rhizomes; whereas roots can occur aboveground, where they are often photosynthetic (Benzing 1991) or have ventilation and aeration functions, as in mangroves. As is the case for canopy biologists, then, the distinction made by botanists between belowground and aboveground (and often between root and shoot) have been largely methodological, for example a matter of choice between using a climbing rope or a shovel. The resulting academic fragmentation can be transcended, as in the architectural research by Kohyama & Grubb (1994), Van der Putten et al. (2001).

It is true that ecology took a long time to enter the treetops (Moffett & Lowman 1995). Yet given its inaccessibility, barring in most cases wholesale destructive intrusion (Smit et al. 2000), and its complexity (compare Beare et al. 1995 with Freiberg 1997), in many ways it's not the aerial world but the subterranean one that remains most alien to us today. The rhizosphere along with the soil associated with the roots therefore could merit equal consideration to the rainforest canopy as the last – though assuredly not the highest – biotic frontier (André et al. 1994); for example, compared to their crown architecture, the architecture of tree root systems is relatively poorly known (but see Jenik 1978 Atger & Edelin 1993). Detailed 3D studies of roots that extend beyond simple depth measurements of the kind reviewed by Jackson et al. (1996) are scarce (Mullins & Diggle 1995, Tsegaye et al. 1995, Lynch et al. 1997, Ge et al. 2000, Pages 2000, Pages et al. 2000) and most examples have been done at the level of a single plant rather than for a community (but see Caldwell & Richards 1986).

How would parasitology stand as a coherent discipline if its practitioners chose to look at the head of their subject while ignoring what its feet were doing? By amalgamating the findings from canopy biology with those from soil sciences, terrestrial biologists could fashion a comprehensive science of plant associates, roughly congruent with marine epibiosis. It could be helpful to use a different term, such as "structural ecology," to designate the discipline that takes the principles of canopy biology and applies them at the level of whole sessile organisms within any affixed community.



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

© Mark W. Moffett, please e-mail naturalist@erols.com to obtain a complete reprint.