Abstract

BackgroundRecent theoretical and empirical work has identified redundancy as one of the benefits of the reticulate form in the evolution of leaf vein networks. However, we know little about the costs of redundancy or how those costs depend on vein network geometry or topology. Here, we examined both costs and benefits to redundancy in 339 individual reticulate leaf networks comprising over 3.5 million vein segments. We compared levels of costs and benefits within reticulate networks to those within analogous networks without loops known as Maximum Spanning Trees (MSTs).ResultsWe show that network robustness to varying degrees of simulated damage is positively correlated with structural indices of redundancy. We further show that leaf vein networks are topologically, geometrically and functionally more redundant than are MSTs. However, increased redundancy comes with minor costs in terms of increases in material allocation or decreases in conductance. We also show that full networks do not markedly decrease the distance to non-vein tissue in comparison to MSTs.ConclusionsThese results suggest the evolutionary transition to the reticulate type of networks found in modern Angiosperm flora involved a relatively minor increase in material and conductance costs with significant benefits in terms of network redundancy.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-014-0234-2) contains supplementary material, which is available to authorized users.

Highlights

  • Recent theoretical and empirical work has identified redundancy as one of the benefits of the reticulate form in the evolution of leaf vein networks

  • We evaluated four metrics related to the reticulate structure and redundancy of leaves: vein length per area (VLA), loopiness, meshedness and robustness

  • Whereas VLA provides a measure of vein investment per unit area, loopiness is a better indicator of features like distance from nonphotosynthetic tissue; meshedness provides a strong indicator of the shape of the network and its tendency to be redundant, and robustness provides a measure of a network’s ability to remain connected under perturbations that damage the network

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Summary

Introduction

Recent theoretical and empirical work has identified redundancy as one of the benefits of the reticulate form in the evolution of leaf vein networks. Not all biological networks are strictly hierarchical, and many networks exhibit both a hierarchical structure and loops that ostensibly allow for redundancy in the face of disturbance or perturbations, where redundancy is defined as the existence of multiple flow paths. This is perhaps most evident in the reticulate networks of the leaves of higher plants, notably most angiosperm lineages (Figure 1) [4,5,6,7,8], but reticulate structures are found in animal lineages such as mammalian capillary beds or some Gorgonian corals. The continued dominance of some communities and ecosystems by taxa such as ferns or gymnosperms, with little or no reticulation, suggests that these network strategies remain viable

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