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The Narrow-Leaf Syndrome: a Functional and Evolutionary Approach to the Form of Fog-Harvesting Rosette Plants

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The Narrow-Leaf Syndrome: a Functional and Evolutionary Approach to the Form of Fog-Harvesting Rosette Plants Copyright Notice This electronic reprint is provided by the author(s) to be consulted by fellow scientists. It is not to be used for any purpose other than private study, scholarship, or research. Further reproduction or distribution of this reprint is restricted by copyright laws. If in doubt about fair use of reprints for research purposes, the user should review the copyright notice contained in the original journal from which this electronic reprint was made. Oecologia DOI 10.1007/s00442-006-0614-x ECOPHYSIOLOGY The narrow-leaf syndrome: a functional and evolutionary approach to the form of fog-harvesting rosette plants Carlos Martorell Æ Exequiel Ezcurra Received: 15 October 2006 / Accepted: 16 November 2006 Ó Springer-Verlag 2006 Abstract Plants that use fog as an important water- net fog interception was independent of leaf form, but source frequently have a rosette growth habit. The interception efficiency was maximized by large num- performance of this morphology in relation to fog bers of narrow leaves. Atmospheric Tillandsia species interception has not been studied. Some first-principles show the narrow-leaf syndrome. Their fog interception from physics predict that narrow leaves, together with efficiencies were correlated to the ones predicted from other ancillary traits (large number and high flexibility aluminum-model data. In the larger xerophytic rosette of leaves, caudices, and/or epiphytism) which consti- species, the interception efficiency was greatest in tute the ‘‘narrow-leaf syndrome’’ should increase fog- plants showing the narrow-leaf syndrome. The adap- interception efficiency. This was tested using aluminum tation to fog-harvesting in several narrow-leaved ro- models of rosettes that differed in leaf length, width settes was tested for evolutionary convergence in 30 and number and were exposed to artificial fog. The xerophytic rosette species using a comparative method. results were validated using seven species of Tillandsia There was a significant evolutionary tendency towards and four species of xerophytic rosettes. The total the development of the narrow-leaf syndrome the amount of fog intercepted in rosette plants increased closer the species grew to areas where fog is frequently with total leaf area, while narrow leaves maximized available. This study establishes convergence in a very interception efficiency (measured as interception per wide group of plants encompassing genera as con- unit area). The number of leaves in the rosettes is trasting as Tillandsia and Agave as a result of their physically constrained because wide-leafed plants can dependence on fog. only have a few blades. At the limits of this constraint, Keywords Comparative method Á Epiphyte Á Functional morphology Á Montane rosette scrub Á Communicated by Todd Dawson. Xerophyte Electronic Supplementary Material The online version of this article (http://dx.doi.org/10.1007/s00442-006-0614-x) contains supplementary material, which is available to authorized users. Introduction C. Martorell (&) Departamento de Ecologı´a y Recursos Naturales, While rain provides water for most plants, several Facultad de Ciencias, Universidad Nacional Auto´ noma species have evolved the capacity to use fog in envi- de Me´xico, Circuito exterior s/n, Ciudad Universitaria, ronments where rainwater is limited (Cavelier and 04510 Mexico D.F., Mexico e-mail: [email protected] Golstein 1989; Rundel et al. 1991; Martin 1994; Dawson 1998; Martorell and Ezcurra 2002). We have suggested E. Ezcurra the term nebulophyte for species that use fog as an Biodiversity Research Center of the Californias, important water source (Martorell 2002), such as epi- San Diego Natural History Museum, 1788 E1 Prado, San Diego CA 92101, USA phytic bromeliads (Mez 1904; Smith and Downs 1974; e-mail: [email protected] Martin 1994). Nebulophytes may also be large ground- 123 Oecologia living plants, such as the trees, shrubs and columnar the wind speed. This relationship means that large cacti from the hyperarid Atacama Desert (Rundel and leaves have thicker boundary layers (Nobel 1991). Fog Mahu 1976; Rundel et al. 1991). Large rosette plants, is composed of water droplets having an average size of such as some Agavaceae and Nolinaceae, constitute as 20 lm; as such, they have a large surface:volume ratio much as 88% of the individuals and 54% of the vege- compared to larger drops (Jones 1992). When they tation cover in the montane rosette scrub of arid North- cross the boundary layer, their large surfaces are sub- American mountains where fog provides as much water ject to strong friction forces, while their reduced mass as rainfall. It is likely that these rosettes are also neb- retains little kinetic energy. As a result, the fog drop- ulophytes (Martorell and Ezcurra 2002). lets are easily slowed down by the boundary layer, Many nebulophytes, both epiphytes and xerophytes, where they are swept away by a slow laminar air show the same rosette growth habit. The reason for this stream flowing parallel to the object’s surface (Welty may be that rosettes resemble funnels that conduct 1984). Only a small fraction of the droplets – known as water to the plant’s roots or to the central tank in impaction efficiency – has enough energy to follow its ‘‘pitcher plant’’ bromeliads. The stem flow of some original (perpendicular or oblique to the surface) tra- Agavaceae is highly efficient, even during very small jectory, ultimately colliding with the plant. The (1 mm) rain events (Gentry 1982; Ramı´rez de Arellano impaction efficiency is inversely proportional to the 1996). We have observed that fog may also initiate thickness of the boundary layer, and it is increased in stem flow in dryland rosettes, and the tanks of some the presence of turbulence. Turbulent eddies may drive bromeliads are known to be replenished entirely by fog droplets that are far from the plant into its surface. water (Rundel and Dillon 1998). Strong turbulence also drags the water into the leeward Several epiphytic Bromeliaceae absorb humidity side of the leaf, where no droplets would normally directly at the leaf surface; these plants have no water collide (Jones 1992). tanks, and their roots serve merely as holdfasts (Smith Therefore, three factors may facilitate fog-water and Downs 1974; Martin 1994). In these ‘‘atmospheric’’ transfer to the plants. (1) Small or narrow leaves result species, conducting water to the plant’s base would be in thin boundary layers. Leaf form is variable in ro- futile or even disadvantageous, so water interception – settes, and the length:width ratio of the nearly trian- rather than its subsequent conduction – should be gular leaves of xerophytes ranges from 2 (Agave optimized. There are some remarkable morphological potatorum) to 265 (Dasylirion longissimum), possibly convergences in nebulophytes that may serve this reaching above 450 in some Tillandsia. (2) Fast winds purpose. Atmospheric bromeliads have very narrow reduce boundary layers and provide sufficient kinetic leaves (Benzing 1990), as it also happens in the energy to droplets. Since wind-speed increases with Agavaceae and Nolinaceae that grow in foggy moun- distance from the ground, rosettes should be placed tains. Nebulophytic lichens and mosses have narrow high above the soil. This may be achieved either by thalli, a trait that increases water uptake rates at the having a stem or caudex, as in some Yucca and Nolina, organism’s surface (Larson 1981). This may also apply or by being an epiphyte. (3) Turbulence is induced by to bromeliads, but Agavaceae or Nolinaceae do not complex surfaces (Jones 1992), such as many-leafed absorb water at the leaf surface. Thus, an alternative rosettes, or by flexible leaves that whisk in the wind. hypothesis is needed to explain the reiterated conver- Therefore, narrow leaves, together with some ancillary gence of narrow leaves or thalli in nebulophytes. In this traits (leaf distance from the ground and flexible leaves paper we suggest that narrow surfaces, in addition to in large numbers), should characterize efficient fog enlarging water-absorption rates, are an adaptation harvesters. These co-occurring traits would then con- that increases fog interception. stitute what we have named the narrow-leaf syndrome. Fog is conveyed to the plant through wind, and wind Two complementary approaches may be used to test speed decreases as it gets closer to surfaces, forming an the adaptive value of the syndrome (Harvey and Pagel envelope of slow-moving air around objects known as 1991; Coddington 1994; Pagel 1994; Wenzel and Car- the boundary layer. For a flat surface such as a leaf, the penter 1994). According to the homology approach, a following relationship holds: trait can be proved to be adaptive if it increases the rffiffiffi performance of the organisms that possess it. Detailed l studies on the evolution of the trait are often needed dbl / ; ð1Þ v that lack generality because the evolution of a trait on any species is a ‘‘historical unique’’ (Coddington 1994). bl where d is the thickness of the boundary layer, l is the The convergence approach states that adaptation may length of the surface in the downwind direction and v is be shown through the repeated evolution of the same 123 Oecologia trait in different taxa as a result of the same evolu- the amount of water intercepted to be measured pre- tionary pressures. This approach has the advantage of cisely by weighing. Because of the non-linear effect generality and provides strong evidence to discard that size was expected to have on water interception alternative explanatory factors (Coddington 1994; (Eq. 1), it was important to use models of at least three Wenzel and Carpenter 1994). A highly widespread different sizes. The leaves of the models were trian- convergence rules out exaptation and, therefore, gular, with lengths of 12, 18 and 24 cm, and there were evinces adaptation rather than mere adaptive value three leaf-form variants. Leaf form was defined as the (Harvey and Pagel 1991; Pagel 1994).
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