Linking functional traits to multiscale statistics of leaf venation networks

Benjamin Blonder; Sabine Both; Miguel Jodra; Hao Xu; Mark Fricker; Ilaíne S Matos; Noreen Majalap; David F R P Burslem; YitArn Teh; Yadvinder Malhi

doi:10.1111/nph.16830

Linking functional traits to multiscale statistics of leaf venation networks

Benjamin Blonder, Sabine Both, Miguel Jodra, Hao Xu, Mark Fricker, Ilaíne S Matos, Noreen Majalap, David F R P Burslem, YitArn Teh, Yadvinder Malhi

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Abstract

Leaf venation networks evolved along several functional axes, including resource transport, damage resistance, mechanical strength, and construction cost. Because functions may depend on architectural features at different scales, network architecture may vary across spatial scales to satisfy functional tradeoffs. We develop a framework for quantifying network architecture with multiscale statistics describing elongation ratios, circularity ratios, vein density, and minimum spanning tree ratios. We quantify vein networks for leaves of 260 southeast Asian tree species in samples of up to 2 cm2 , pairing multiscale statistics with traits representing axes of resource transport, damage resistance, mechanical strength, and cost. We show that these multiscale statistics clearly differentiate species' architecture and delineate a phenotype space that shifts at larger scales; functional linkages vary with scale and are weak, with vein density, minimum spanning tree ratio, and circularity ratio linked to mechanical strength (measured by force to punch) and elongation ratio and circularity ratio linked to damage resistance (measured by tannins); and phylogenetic conservatism of network architecture is low but scale-dependent. This work provides tools to quantify the function and evolution of venation networks. Future studies including primary and secondary veins may uncover additional insights.

Original language	English
Pages (from-to)	1796-1810
Number of pages	15
Journal	New Phytologist
Volume	228
Issue number	6
Early online date	31 Aug 2020
DOIs	https://doi.org/10.1111/nph.16830
Publication status	Published - Dec 2020

Bibliographical note

Funding Information
UK Natural Environment Research Council. Grant Number: NE/M019160/1
US National Science Foundation. Grant Number: DEB‐2025282
NERC Human‐modified Tropical Forest Programme. Grant Number: NE/M017508/1
Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI). Grant Numbers: NE/K016253/1, NE/K016253/1
Sime Darby Foundation
Stability of Altered Forest Ecosystems (SAFE) Project
Sabah Biodiversity Council
Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS)
Sabah Forest Research Centre (FRC) at Sepilok
Sabah Forestry Department
SEARRP, Yayasan Sabah (Maliau Basin Conservation Area)
Maliau Basin and Danum Valley Management Committees

Acknowledgements
Fieldwork was supported by Unding Jami, Matheus Henrique Nuñes, Rudi Saul Cruz Chino, Milenka Ximena Montoya, and South East Asia Rainforest Research Program (SEARRP) staff. Research was facilitated by Rob Ewers, Laura Kruitbos, Reuben Nilus, Glen Reynolds, and Charles Vairappan. Species identifications were made by Bernadus Bala Ola, Bill McDonald, Alexander Karolus, and MinSheng Khoo. This work also was supported by the UK Natural Environment Research Council (NERC; no. NE/M019160/1, to BB) and the US National Science Foundation (no. DEB‐2025282, to BB). This publication is a contribution from the NERC Human‐modified Tropical Forest Programme (no. NE/M017508/1, to YAT) and Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI) consortium (no. NE/K016253/1, to YM and no. NE/K016253/1, to YAT). The SAFE Project was funded by the Sime Darby Foundation and the UK NERC. The study areas are part of the Global Ecosystems Monitoring Network (GEM) via an ERC Advanced Investigator Award to YM (no. 321131). The project also was supported by the Stability of Altered Forest Ecosystems (SAFE) Project, the Sabah Biodiversity Council (SaBC, permits JKM/MBS.1000‐2/2 JLD.3‐126 and ‐154), the Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS), the Sabah Forest Research Centre (FRC) at Sepilok, the Sabah Forestry Department, the SEARRP, Yayasan Sabah (Maliau Basin Conservation Area), and the Maliau Basin and Danum Valley Management Committees. Sean Gleason and several anonymous reviewers provided constructive feedback on the manuscript.

Keywords

venation network
network architecture
functional trait
resource transport
damage resistance
mechanical strength
construction cost
leaf
DESIGN
EVOLUTION
ARCHITECTURE
ECOLOGY
ECONOMICS
SPECTRUM
VEIN
HYDRAULICS

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Blonder_et_al_Linking_functional_New_phytologist_vor
©2020 The Authors New Phytologist ©2020 New Phytologist Trust This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. https://creativecommons.org/licenses/by/4.0/
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Cite this

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title = "Linking functional traits to multiscale statistics of leaf venation networks",

abstract = "Leaf venation networks evolved along several functional axes, including resource transport, damage resistance, mechanical strength, and construction cost. Because functions may depend on architectural features at different scales, network architecture may vary across spatial scales to satisfy functional tradeoffs. We develop a framework for quantifying network architecture with multiscale statistics describing elongation ratios, circularity ratios, vein density, and minimum spanning tree ratios. We quantify vein networks for leaves of 260 southeast Asian tree species in samples of up to 2 cm2 , pairing multiscale statistics with traits representing axes of resource transport, damage resistance, mechanical strength, and cost. We show that these multiscale statistics clearly differentiate species' architecture and delineate a phenotype space that shifts at larger scales; functional linkages vary with scale and are weak, with vein density, minimum spanning tree ratio, and circularity ratio linked to mechanical strength (measured by force to punch) and elongation ratio and circularity ratio linked to damage resistance (measured by tannins); and phylogenetic conservatism of network architecture is low but scale-dependent. This work provides tools to quantify the function and evolution of venation networks. Future studies including primary and secondary veins may uncover additional insights.",

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author = "Benjamin Blonder and Sabine Both and Miguel Jodra and Hao Xu and Mark Fricker and Matos, {Ila{\'i}ne S} and Noreen Majalap and Burslem, {David F R P} and YitArn Teh and Yadvinder Malhi",

note = "Funding Information UK Natural Environment Research Council. Grant Number: NE/M019160/1 US National Science Foundation. Grant Number: DEB‐2025282 NERC Human‐modified Tropical Forest Programme. Grant Number: NE/M017508/1 Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI). Grant Numbers: NE/K016253/1, NE/K016253/1 Sime Darby Foundation Stability of Altered Forest Ecosystems (SAFE) Project Sabah Biodiversity Council Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS) Sabah Forest Research Centre (FRC) at Sepilok Sabah Forestry Department SEARRP, Yayasan Sabah (Maliau Basin Conservation Area) Maliau Basin and Danum Valley Management Committees Acknowledgements Fieldwork was supported by Unding Jami, Matheus Henrique Nu{\~n}es, Rudi Saul Cruz Chino, Milenka Ximena Montoya, and South East Asia Rainforest Research Program (SEARRP) staff. Research was facilitated by Rob Ewers, Laura Kruitbos, Reuben Nilus, Glen Reynolds, and Charles Vairappan. Species identifications were made by Bernadus Bala Ola, Bill McDonald, Alexander Karolus, and MinSheng Khoo. This work also was supported by the UK Natural Environment Research Council (NERC; no. NE/M019160/1, to BB) and the US National Science Foundation (no. DEB‐2025282, to BB). This publication is a contribution from the NERC Human‐modified Tropical Forest Programme (no. NE/M017508/1, to YAT) and Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI) consortium (no. NE/K016253/1, to YM and no. NE/K016253/1, to YAT). The SAFE Project was funded by the Sime Darby Foundation and the UK NERC. The study areas are part of the Global Ecosystems Monitoring Network (GEM) via an ERC Advanced Investigator Award to YM (no. 321131). The project also was supported by the Stability of Altered Forest Ecosystems (SAFE) Project, the Sabah Biodiversity Council (SaBC, permits JKM/MBS.1000‐2/2 JLD.3‐126 and ‐154), the Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS), the Sabah Forest Research Centre (FRC) at Sepilok, the Sabah Forestry Department, the SEARRP, Yayasan Sabah (Maliau Basin Conservation Area), and the Maliau Basin and Danum Valley Management Committees. Sean Gleason and several anonymous reviewers provided constructive feedback on the manuscript. ",

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T1 - Linking functional traits to multiscale statistics of leaf venation networks

AU - Blonder, Benjamin

AU - Both, Sabine

AU - Jodra, Miguel

AU - Xu, Hao

AU - Fricker, Mark

AU - Matos, Ilaíne S

AU - Majalap, Noreen

AU - Burslem, David F R P

AU - Teh, YitArn

AU - Malhi, Yadvinder

N1 - Funding Information UK Natural Environment Research Council. Grant Number: NE/M019160/1 US National Science Foundation. Grant Number: DEB‐2025282 NERC Human‐modified Tropical Forest Programme. Grant Number: NE/M017508/1 Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI). Grant Numbers: NE/K016253/1, NE/K016253/1 Sime Darby Foundation Stability of Altered Forest Ecosystems (SAFE) Project Sabah Biodiversity Council Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS) Sabah Forest Research Centre (FRC) at Sepilok Sabah Forestry Department SEARRP, Yayasan Sabah (Maliau Basin Conservation Area) Maliau Basin and Danum Valley Management Committees Acknowledgements Fieldwork was supported by Unding Jami, Matheus Henrique Nuñes, Rudi Saul Cruz Chino, Milenka Ximena Montoya, and South East Asia Rainforest Research Program (SEARRP) staff. Research was facilitated by Rob Ewers, Laura Kruitbos, Reuben Nilus, Glen Reynolds, and Charles Vairappan. Species identifications were made by Bernadus Bala Ola, Bill McDonald, Alexander Karolus, and MinSheng Khoo. This work also was supported by the UK Natural Environment Research Council (NERC; no. NE/M019160/1, to BB) and the US National Science Foundation (no. DEB‐2025282, to BB). This publication is a contribution from the NERC Human‐modified Tropical Forest Programme (no. NE/M017508/1, to YAT) and Biodiversity And Land‐use Impacts on Tropical Ecosystem Function (BALI) consortium (no. NE/K016253/1, to YM and no. NE/K016253/1, to YAT). The SAFE Project was funded by the Sime Darby Foundation and the UK NERC. The study areas are part of the Global Ecosystems Monitoring Network (GEM) via an ERC Advanced Investigator Award to YM (no. 321131). The project also was supported by the Stability of Altered Forest Ecosystems (SAFE) Project, the Sabah Biodiversity Council (SaBC, permits JKM/MBS.1000‐2/2 JLD.3‐126 and ‐154), the Institute for Tropical Biology and Conservation (ITBC) at the University of Malaysia, Sabah (UMS), the Sabah Forest Research Centre (FRC) at Sepilok, the Sabah Forestry Department, the SEARRP, Yayasan Sabah (Maliau Basin Conservation Area), and the Maliau Basin and Danum Valley Management Committees. Sean Gleason and several anonymous reviewers provided constructive feedback on the manuscript.

PY - 2020/12

Y1 - 2020/12

N2 - Leaf venation networks evolved along several functional axes, including resource transport, damage resistance, mechanical strength, and construction cost. Because functions may depend on architectural features at different scales, network architecture may vary across spatial scales to satisfy functional tradeoffs. We develop a framework for quantifying network architecture with multiscale statistics describing elongation ratios, circularity ratios, vein density, and minimum spanning tree ratios. We quantify vein networks for leaves of 260 southeast Asian tree species in samples of up to 2 cm2 , pairing multiscale statistics with traits representing axes of resource transport, damage resistance, mechanical strength, and cost. We show that these multiscale statistics clearly differentiate species' architecture and delineate a phenotype space that shifts at larger scales; functional linkages vary with scale and are weak, with vein density, minimum spanning tree ratio, and circularity ratio linked to mechanical strength (measured by force to punch) and elongation ratio and circularity ratio linked to damage resistance (measured by tannins); and phylogenetic conservatism of network architecture is low but scale-dependent. This work provides tools to quantify the function and evolution of venation networks. Future studies including primary and secondary veins may uncover additional insights.

AB - Leaf venation networks evolved along several functional axes, including resource transport, damage resistance, mechanical strength, and construction cost. Because functions may depend on architectural features at different scales, network architecture may vary across spatial scales to satisfy functional tradeoffs. We develop a framework for quantifying network architecture with multiscale statistics describing elongation ratios, circularity ratios, vein density, and minimum spanning tree ratios. We quantify vein networks for leaves of 260 southeast Asian tree species in samples of up to 2 cm2 , pairing multiscale statistics with traits representing axes of resource transport, damage resistance, mechanical strength, and cost. We show that these multiscale statistics clearly differentiate species' architecture and delineate a phenotype space that shifts at larger scales; functional linkages vary with scale and are weak, with vein density, minimum spanning tree ratio, and circularity ratio linked to mechanical strength (measured by force to punch) and elongation ratio and circularity ratio linked to damage resistance (measured by tannins); and phylogenetic conservatism of network architecture is low but scale-dependent. This work provides tools to quantify the function and evolution of venation networks. Future studies including primary and secondary veins may uncover additional insights.

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KW - damage resistance

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KW - construction cost

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KW - EVOLUTION

KW - ARCHITECTURE

KW - ECOLOGY

KW - ECONOMICS

KW - SPECTRUM

KW - VEIN

KW - HYDRAULICS

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EP - 1810

JO - New Phytologist

JF - New Phytologist

IS - 6

ER -

Linking functional traits to multiscale statistics of leaf venation networks

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Keywords

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