Opportunistic diversification has allowed ferns to radiate into epiphytic niches in angiosperm dominated landscapes. However, our understanding of how ecophysiological function allowed establishment in the canopy and the potential transitionary role of the hemi‐epiphytic life form remain unclear. Here, we surveyed 39 fern species in Costa Rican tropical forests to explore epiphytic trait divergence in a phylogenetic context. We examined leaf responses to water deficits in terrestrial, hemi‐epiphytic and epiphytic ferns and related these findings to functional traits that regulate leaf water status. Epiphytic ferns had reduced xylem area (−63%), shorter stipe lengths (−56%), thicker laminae (+41%) and reduced stomatal density (−46%) compared to terrestrial ferns. Epiphytic ferns exhibited similar turgor loss points, higher osmotic potential at saturation and lower tissue capacitance after turgor loss than terrestrial ferns. Overall, hemi‐epiphytic ferns exhibited traits that share characteristics of both terrestrial and epiphytic species. Our findings clearly demonstrate the prevalence of water conservatism in both epiphytic and hemi‐epiphytic ferns, via selection for anatomical and structural traits that avoid leaf water stress. Even with likely evolutionarily constrained physiological function, adaptations for drought avoidance have allowed epiphytic ferns to successfully endure the stresses of the canopy habitat.
The Cretaceous–Cenozoic expansion of tropical forests created canopy space that was subsequently occupied by diverse epiphytic communities including Eupolypod ferns. Eupolypods proliferated in this more stressful niche, where lower competition enabled the adaptive radiation of thousands of species. Here, we examine whether xylem traits helped shape the Cenozoic radiation of Eupolypod ferns. We characterized the petiole xylem anatomy of 39 species belonging to the Eupolypod I and Eupolypod II clades occupying the epiphytic, hemiepiphytic, and terrestrial niche, and we assessed vulnerability to embolism in a subset of species. The transition to the canopy was associated with reduced xylem content and smaller tracheid diameters, but no differences were found in species vulnerability to embolism and pit membrane thickness. Phylogenetic analyses support selection for traits associated with reduced water transport in Eupolypod 1 species. We posit that in Eupolypod epiphytes, selection favored water retention via thicker leaves and lower stomatal density over higher rates of water transport. Consequently, lower leaf water loss was coupled with smaller quantities of xylem and narrower tracheid diameters. Traits associated with water conservation were evident in terrestrial Eupolypod 1 ferns and may have predisposed this clade toward radiation in the canopy.
- Award ID(s):
- 1656876
- NSF-PAR ID:
- 10443030
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 237
- Issue:
- 5
- ISSN:
- 0028-646X
- Format(s):
- Medium: X Size: p. 1745-1758
- Size(s):
- ["p. 1745-1758"]
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Abstract -
more » « less
Summary The expansion of angiosperm‐dominated forests in the Cretaceous and early Cenozoic had a profound effect on terrestrial biota by creating novel ecological niches. The majority of modern fern lineages are hypothesized to have arisen in response to this expansion, particularly fern epiphytes that radiated into the canopy. Recent evidence, however, suggests that epiphytism does not correlate with increased diversification rates in ferns, calling into question the role of the canopy habitat in fern evolution.
To understand the role of the canopy in structuring fern community diversity, we investigated functional traits of fern sporophytes and gametophytes across a broad phylogenetic sampling on the island of Moorea, French Polynesia, including > 120 species and representatives of multiple epiphytic radiations.
While epiphytes showed convergence in small size and a higher frequency of noncordate gametophytes, they showed greater functional diversity at the community level relative to terrestrial ferns.
These results suggest previously overlooked functional diversity among fern epiphytes, and raise the hypothesis that while the angiosperm canopy acted as a complex filter that restricted plant size, it also facilitated diversification into finely partitioned niches. Characterizing these niche axes and adaptations of epiphytic ferns occupying them should be a priority for future pteridological research.
-
more » « less
Abstract Recent findings suggest that tree mortality and post‐drought recovery of gas exchange can be predicted from loss of function within the water transport system. Understanding the susceptibility of plants to hydraulic damage requires knowledge about the vulnerability of different plant organs to stress‐induced hydraulic dysfunction. This is particularly important in the context of vulnerability segmentation between plant tissues which is believed to protect more energetically ‘costly’ tissues, such as woody stems, by sacrificing ‘cheaper’ leaves early under drought conditions.
Differences in vulnerability segmentation between co‐occurring plant species could explain divergent behaviours during drought, yet there are few studies considering how this characteristic may vary within a plant community. Here we investigated community‐wide vulnerability segmentation by comparing leaf/shoot and stem vulnerability in all coexistent dominant canopy and understory woody species in a diverse dry sclerophyll woodland community, including multiple angiosperms and one gymnosperm.
Previously published terminal leaf/shoot vulnerability to loss of water transport capacity was compared with stem xylem vulnerability to embolism measured on the same species at the same site. We calculated hydraulic safety margins for stems to determine variation in the risk of hydraulic failure during drought among species.
The xylem of all species was found to be highly resistant to hydraulic dysfunction, with only two of the eight species exhibiting significantly different vulnerability to the overall mean. No evidence of vulnerability segmentation between shoots/leaves and stems was found in seven of the eight species.
Phylogenetically diverse canopy and understory species in this evergreen sclerophyll woodland appear to have evolved similar strategies of drought resistance, including low xylem vulnerability to embolism and general lack of vulnerability segmentation. This convergence in hydraulic safety indicates a lack of hydraulic niche partitioning in this woodland community.
A free
plain language summary can be found within the Supporting Information of this article. -
more » « less
Summary Deep‐water access is arguably the most effective, but under‐studied, mechanism that plants employ to survive during drought. Vulnerability to embolism and hydraulic safety margins can predict mortality risk at given levels of dehydration, but deep‐water access may delay plant dehydration. Here, we tested the role of deep‐water access in enabling survival within a diverse tropical forest community in Panama using a novel data‐model approach.
We inversely estimated the effective rooting depth (ERD, as the average depth of water extraction), for 29 canopy species by linking diameter growth dynamics (1990–2015) to vapor pressure deficit, water potentials in the whole‐soil column, and leaf hydraulic vulnerability curves. We validated ERD estimates against existing isotopic data of potential water‐access depths.
Across species, deeper ERD was associated with higher maximum stem hydraulic conductivity, greater vulnerability to xylem embolism, narrower safety margins, and lower mortality rates during extreme droughts over 35 years (1981–2015) among evergreen species. Species exposure to water stress declined with deeper ERD indicating that trees compensate for water stress‐related mortality risk through deep‐water access.
The role of deep‐water access in mitigating mortality of hydraulically‐vulnerable trees has important implications for our predictive understanding of forest dynamics under current and future climates.
-
more » « less
Abstract Severe droughts have led to lower plant growth and high mortality in many ecosystems worldwide, including tropical forests. Drought vulnerability differs among species, but there is limited consensus on the nature and degree of this variation in tropical forest communities. Understanding species‐level vulnerability to drought requires examination of hydraulic traits since these reflect the different strategies species employ for surviving drought.
Here, we examined hydraulic traits and growth reductions during a severe drought for 12 common woody species in a wet tropical forest community in Puerto Rico to ask: Q1. To what extent can hydraulic traits predict growth declines during drought? We expected that species with more hydraulically vulnerable xylem and narrower safety margins (SMP50) would grow less during drought. Q2. How does species successional association relate to the levels of vulnerability to drought and hydraulic strategies? We predicted that early‐ and mid‐successional species would exhibit more acquisitive strategies, making them more susceptible to drought than shade‐tolerant species. Q3. What are the different hydraulic strategies employed by species and are there trade‐offs between drought avoidance and drought tolerance? We anticipated that species with greater water storage capacity would have leaves that lose turgor at higher xylem water potential and be less resistant to embolism forming in their xylem (P50).
We found a large range of variation in hydraulic traits across species; however, they did not closely capture the magnitude of growth declines during drought. Among larger trees (≥10 cm diameter at breast height—DBH), some tree species with high xylem embolism vulnerability (P50) and risk of hydraulic failure (SMP50) experienced substantial growth declines during drought, but this pattern was not consistent across species. We found a trade‐off among species between drought avoidance (capacitance) and drought tolerating (P50) in this tropical forest community. Hydraulic strategies did not align with successional associations. Instead, some of the more drought‐vulnerable species were shade‐tolerant dominants in the community, suggesting that a drying climate could lead to shifts in long‐term forest composition and function in Puerto Rico and the Caribbean.
Read the free
Plain Language Summary for this article on the Journal blog.
