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Abstract
Abstract Insular woodiness refers to the evolutionary transition from herbaceousness towards derived woodiness on (sub)tropical islands and leads to island floras that have a higher proportion of woody species compared to floras of nearby continents. Several hypotheses have tried to explain insular woodiness since Darwin's original observations, but experimental evidence why plants became woody on islands is scarce at best. Here, we combine experimental measurements of hydraulic failure in stems (as a proxy for drought stress resistance) with stem anatomical observations in the daisy lineage (Asteraceae), including insular woody Argyranthemum species from the Canary Islands and their herbaceous continental relatives. Our results show that stems of insular woody daisies are more resistant to drought‐induced hydraulic failure than the stems of their herbaceous counterparts. The anatomical character that best predicts variation in embolism resistance is intervessel pit membrane thickness (TPM), which can be functionally linked with air bubble dynamics throughout the 3D vessel network. There is also a strong link between TPM vs. degree of woodiness and thickness of the xylem fibre wall vs. embolism resistance, resulting in an indirect link between lignification and resistance to embolism formation. Thicker intervessel pit membranes in Argyranthemum functionally explain why this insular woody genus is more embolism resistant to drought‐induced failure compared to the herbaceous relatives from which it has evolved, but additional data are needed to confirm that palaeoclimatic drought conditions have triggered wood formation in this daisy lineage. A plain language summary is available for this article.
Highlights
It has been known for a long time that island floras have a higher proportion of woody species compared to adjacent continents, and related species on islands are often woodier than their continental relatives (Carlquist, 1974; Darwin, 1859; Wallace, 1878)
The main objectives in our study are (1) to investigate whether the insular woody stems of Argyranthemum are more resistant to drought-induced hydraulic failure than those of their herbaceous relatives, (2) to findfunctional stem anatomical characters that best explain the observed variation in P50 between the daisy species observed and (3) to assess whether the woody species native to drier habitats are more resistant to embolism formation compared to Argyranthemum species growing in wetter habitats
We find that stems of the insular woody species of Argyranthemum are more resistant to drought-induced hydraulic failure than those of their herbaceous relatives native to the European mainland
Summary
It has been known for a long time that island floras have a higher proportion of woody species compared to adjacent continents, and related species on islands are often woodier than their continental relatives (Carlquist, 1974; Darwin, 1859; Wallace, 1878) This phenomenon refers to insular woodiness and describes the evolutionary transition from herbaceous towards (derived) woody flowering plant species on (sub)tropical oceanic islands Lens, unpublished data), suggesting a functional link between wood formation and increased drought stress resistance Experimental support for this link was found in Arabidopsis thaliana (Lens, Smets, & Melzer, 2012) using xylem physiological measurements in stems, but not a single study has compared drought-induced hydraulic failure with stem anatomy between derived woody plants and their herbaceous relatives growing in nature. The main objectives in our study are (1) to investigate whether the insular woody stems of Argyranthemum are more resistant to drought-induced hydraulic failure than those of their herbaceous relatives, (2) to find (non-)functional stem anatomical characters that best explain the observed variation in P50 between the daisy species observed and (3) to assess whether the woody species native to drier habitats are more resistant to embolism formation compared to Argyranthemum species growing in wetter habitats
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