Causes of ecological gradients in leaf margin entirety: Evaluating the roles of biomechanics, hydraulics, vein geometry, and bud packing

Abstract

PREMISE OF THE STUDY:A recent commentary by Edwards et al. (Am. J. Bot. 103: 975–978) proposed that constraints imposed by the packing of young leaves in buds could explain the positive association between non‐entire leaf margins and latitude but did not thoroughly consider alternative explanations.METHODS:We review the logic and evidence underlying six major hypotheses for the functional significance of marginal teeth, involving putative effects on (1) leaf cooling, (2) optimal support and supply of the areas served by major veins, (3) enhanced leaf‐margin photosynthesis, (4) hydathodal function, (5) defense against herbivores, and (6) bud packing.KEY RESULTS:Theoretical and empirical problems undermine all hypotheses except the support–supply hypothesis, which implies that thinner leaves should have non‐entire margins. Phylogenetically structured analyses across angiosperms, the El Yunque flora, and the genus Viburnum all demonstrate that non‐entire margins are indeed more common in thinner leaves. Across angiosperms, the association of leaf thickness with non‐entire leaf margins is stronger than that of latitude.CONCLUSION:We outline a synthetic model showing how biomechanics, hydraulics, vein geometry, rates of leaf expansion, and length of development within resting buds, all tied to leaf thickness, drive patterns in the distribution of entire vs. non‐entire leaf margins. Our model accounts for dominance of entire margins in the tropics, Mediterranean scrub, and tundra, non‐entire margins in cold temperate deciduous forests and tropical vines and early‐successional trees, and entire leaf margins in monocots. Spinose‐toothed leaves should be favored in short‐statured evergreen trees and shrubs, primarily in Mediterranean scrub and related semiarid habitats.

Leaf margins in a deciduous lineage from the Greater Cape Floristic Region track climate in unexpected directions

“…Bailey and Sinnott's () hypothesis that herbaceous species are more likely to experience more moderate environments because they are beneath the canopy is unlikely to be the case for Pelargonium , as few species in the GCFR are protected by much of an overstory, although we note that several species grow in microsites partially shaded by rocks or other vegetation. We recognize that the paleobotanical community's goal of predicting climate from the percentage of species with teeth in the flora is quite different than understanding the functional significance of teeth, and we agree with both Givnish and Kriebel () and Edwards et al. (, ) that marginal teeth are likely to have a variety of functions and developmental explanations.…”

“…The support and supply (SS) hypothesis proposed by Givnish (), which posits that thicker leaves should have untoothed margins, was supported to various degrees in our analysis. If the SS hypothesis is indeed a universal driver in plant margins as suggested by Givnish and Kriebel (), then we would expect the pattern to appear within and across multiple lineages. Within subclades, a more nuanced patterns emerged.…”

“…Potential explanations for the increased presence of leaf teeth in colder climates were recently debated by Edwards et al. (, ) and Givnish and Kriebel (). These authors agree that several hypotheses are unlikely to be general explanations for why leaves in temperate zones are toothier, e.g., herbivore deterrence (Brown and Lawton, ; Rivero‐Lynch et al., ), the potential for seasonally emerging leaf teeth to provide early‐season photosynthesis across the leaf blade (Baker‐Brosh and Peet, ; Royer and Wilf, ), the role of leaf teeth in early‐season guttation (Feild et al., ), and the contribution of teeth to convectional cooling (Gates, ; Vogel, ).…”

“…These authors agree that several hypotheses are unlikely to be general explanations for why leaves in temperate zones are toothier, e.g., herbivore deterrence (Brown and Lawton, ; Rivero‐Lynch et al., ), the potential for seasonally emerging leaf teeth to provide early‐season photosynthesis across the leaf blade (Baker‐Brosh and Peet, ; Royer and Wilf, ), the role of leaf teeth in early‐season guttation (Feild et al., ), and the contribution of teeth to convectional cooling (Gates, ; Vogel, ). In the end, Givnish and Kriebel () argued that thinner lamina should have teeth because secondary and tertiary veins extend to the margins to support the typically thinner lamina of deciduous leaves. These veins taper toward their tips and, in conjunction with the lower hydraulic conductivity of thin tissue, supply less water.…”

Examining the support–supply and bud‐packing hypotheses for the increase in toothed leaf margins in northern deciduous floras

“…It is well documented that trees and shrubs from cold‐temperate climates often have toothed leaves, while trees and shrubs from warm‐tropical climates usually have entire‐margined leaves (Bailey and Sinnott, , ; Wolfe, , ; Peppe et al., ; Royer, ). What drives these correlations has remained enigmatic (Royer and Wilf, ; Royer, ; Edwards et al., , ; Givnish and Kriebel, ). One explanation for why low mean annual temperatures (MATs) favor species with toothed leaf margins is that cooler climates favor thinner leaves, which in turn require a strong vein system, with veins penetrating to the margin, resulting in craspedodromous venation (Fig.…”