Modeling fluid flow inMedullosa, an anatomically unusual Carboniferous seed plant

Abstract

Medullosa stands apart from most Paleozoic seed plants in its combination of large leaf area, complex vascular structure, and extremely large water-conducting cells. To investigate the hydraulic consequences of these anatomical features and to compare them with other seed plants, we have adapted a model of water transport in xylem cells that accounts for resistance to flow from the lumen, pits, and pit membranes, and that can be used to compare extinct and extant plants in a quantitative way. Application of this model to Medullosa, the Paleozoic coniferophyte Cordaites, and the extant conifer Pinus shows that medullosan tracheids had the capacity to transport water at volume flow rates more comparable to those of angiosperm vessels than to those characteristic of ancient and modern coniferophyte tracheids. Tracheid structure in Medullosa, including the large pit membrane area per tracheid and the high ratio of tracheid diameter to wall thickness, suggests that its xylem cells operated at significant risk of embolism and implosion, making this plant unlikely to survive significant water stress These features further suggest that tracheids could not have furnished significant structural support, requiring either that other tissues supported these plants or that at least some medullosans were vines. In combination with high tracheid conductivity, distinctive anatomical characters of Medullosa such as the anomalous growth of vascular cambium and the large number of leaf traces that enter each petiole base suggest vascular adaptations to meet the evapotranspiration demands of its large leaves. The evolution of highly efficient conducting cells dictates a need to supply structural support via other tissues, both in tracheid-based stem seed plants and in vessel-bearing angiosperms.

A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants

“…These pores are often modeled as straight channels, though in SEM observation they often appear tortuous and partially occluded by gel-like macromolecular compounds, such as pectin or hemicellulose (Choat et al 2008, Jansen et al 2007, Rabaey et al 2006, Sano and Jansen 2006. As in a previous study (Wilson et al 2008),…”

“…We have applied this model to fossil plants in earlier work, and the methods and results are described in detail therein (Wilson et al 2008). …”

Palaeoecology of Macroneuropteris scheuchzeri, and its implications for resolving the paradox of ‘xeromorphic’ plants in Pennsylvanian wetlands

“…In contrast with these findings about transpirative capacity, however, the medullosans also have been shown to have had capacities for rapid transport of water through their vascular systems to the point of dispersal to the atmosphere, as did vine-like lyginopterid seed ferns and the ground-cover sphenopsid scrambler, Sphenophyllum (Wilson et al, 2008;Wilson and Knoll, 2010). This presents us with somewhat of a dilemma -based on the work of Wilson et al (2008) and Wilson and Knoll (2010), some Pennsylvanian plants, including medullosans, had the capacity to get water to the evaporative surfaces nearly as rapidly and efficiently as some flowering plants, while, based on the work of Boyce et al (2009, these same plants seem to lack the ability to vent that water to the atmosphere at a rate comparable to its uptake and transport. The key to this may be the scaling of total evaporative surface area of the leaf array relative to the total water transport capacity of the stem and leaf -which ought to be in balance.…”

“…Additionally, medullosans had vascular systems that, while allowing for rapid rates of water transport (large diameter, thin-walled tracheids, with abundant areas for water transport between adjacent tracheidal cells, etc. ), likely would have made them extremely vulnerable to water stress (Wilson et al, 2008). These lines of evidence, all somewhat ambiguous, do not, in and of themselves, indicate that M. scheuchzeri grew under conditions of constantly high soil moisture, lacking drought (either ecological or physiological), but they are not inconsistent with such an inference.…”

“…This has been inferred mainly from constructional anatomy (e.g., Baxter, 1949). Throughout the clade, regardless of stem size or inferred growth habit, vascular cylinders, including secondary xylem, are divided into discrete bundles (e.g., Steidtmann, 1944;Stidd, 1981) with large diameter tracheary elements, permitting high fluid flow rates even though the total amount of stem and leaf vascular tissue is relatively small (Wilson et al, 2008). Both of these traits are found in modern lianas (Burnham, 2009;Isnard and Silk, 2009).…”