Publications by authors named "James E Watkins"

26 Publications

  • Page 1 of 1

Ecophysiological differentiation between life stages in filmy ferns (Hymenophyllaceae).

J Plant Res 2021 Jun 12. Epub 2021 Jun 12.

Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA.

Desiccation tolerance was a key trait that allowed plants to colonize land. However, little is known about the transition from desiccation tolerant non-vascular plants to desiccation sensitive vascular ones. Filmy ferns (Hymenophyllaceae) represent a useful system to investigate how water-stress strategies differ between non-vascular and vascular stages within a single organism because they have vascularized sporophytes and nonvascular gametophytes that are each capable of varying degrees of desiccation tolerance. To explore this, we surveyed sporophytes and gametophytes of 19 species (22 taxa including varieties) of filmy ferns on Moorea (French Polynesia) and used chlorophyll fluorescence to measure desiccation tolerance and light responses. We conducted phylogenetically informed analyses to identify differences in physiology between life stages and growth habits. Gametophytes had similar or less desiccation tolerance (ability to recover from 2 days desiccation at - 86 MPa) and lower photosynthetic optima (maximum electron transport rate of photosystem II and light level at 95% of that rate) than sporophytes. Epiphytes were more tolerant of desiccation than terrestrial species in both life stages. Despite their lack of greater physiological tolerances, gametophytes of several species occurred over a wider elevational range than conspecific sporophytes. Our results demonstrate that filmy fern gametophytes and sporophytes differ in their physiology and niche requirements, and point to the importance of microhabitat in shaping the evolution of water-use strategies in vascular plants.
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http://dx.doi.org/10.1007/s10265-021-01318-zDOI Listing
June 2021

Leaf water relations in epiphytic ferns are driven by drought avoidance rather than tolerance mechanisms.

Plant Cell Environ 2021 Jun 18;44(6):1741-1755. Epub 2021 Mar 18.

Department of Biology, Colgate University, Hamilton, New York, USA.

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.
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http://dx.doi.org/10.1111/pce.14042DOI Listing
June 2021

Insights into the evolutionary history and widespread occurrence of antheridiogen systems in ferns.

New Phytol 2021 01 25;229(1):607-619. Epub 2020 Aug 25.

Department of Botany, Faculty of Science, University of South Bohemia, Branišovská 1760, České Budějovice, CZ, 37005, Czech Republic.

Sex expression of homosporous ferns is controlled by multiple factors, one being the antheridiogen system. Antheridiogens are pheromones released by sexually mature female fern gametophytes, turning nearby asexual gametophytes precociously male. Nevertheless, not all species respond. It is still unknown how many fern species use antheridiogens, how the antheridiogen system evolved, and whether it is affected by polyploidy and/or apomixis. We tested the response of 68 fern species to antheridiogens in cultivation. These results were combined with a comprehensive review of literature to form the largest dataset of antheridiogen interactions to date. Analyzed species also were coded as apomictic or sexual and diploid or polyploid. Our final dataset contains a total of 498 interactions involving 208 species (c. 2% of all ferns). About 65% of studied species respond to antheridiogen. Multiple antheridiogen types were delimited and their evolution is discussed. Antheridiogen responsiveness was not significantly affected by apomixis or polyploidy. Antheridiogens are widely used by ferns to direct sex expression. The antheridiogen system likely evolved multiple times and provides homosporous ferns with the benefits often associated with heterospory, such as increased rates of outcrossing. Despite expectations, antheridiogens may be beneficial to polyploids and apomicts.
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http://dx.doi.org/10.1111/nph.16836DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7754499PMC
January 2021

Life in the canopy: community trait assessments reveal substantial functional diversity among fern epiphytes.

New Phytol 2020 09 19;227(6):1885-1899. Epub 2020 May 19.

Department of Organismic and Evolutionary Biology and Harvard University Herbaria, Harvard University, 22 Divinity Avenue, Cambridge, MA, 02138, USA.

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.
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http://dx.doi.org/10.1111/nph.16607DOI Listing
September 2020

Hymenasplenium volubile: documentation of its gametophytes and the first record of a hemiepiphyte in the Aspleniaceae.

Ann Bot 2019 11;124(5):829-835

Colgate University, Department of Biology, Hamilton, NY, USA.

Background And Aims: Through careful field examination of the growth habit of the gametophytes and sporophytes of Hymenasplenium volubile across an ontogenetic series, we aim to understand better the evolution of epiphytism in this poorly understood group of ferns.

Methods: We made field observations of H. volubile sporophytes and gametophytes, and brought specimens back to the lab for microscopic analysis. In the field, sporophytes at each ontogenetic stage were photographed to document the species' growth habit. We used an existing phylogeny to optimize growth form of New World Hymenasplenium.

Key Results: Young sporophytes were at first fully epiphytic and produced one or two long feeding roots that extend to the soil where they branch profusely. The feeding roots remain in contact with the soil throughout the life of the plant. Thus, H. volubile is a hemiepiphyte. While immature, gametophytes are appressed to the tree trunk, but, as their gametangia mature, their lower margin lifts upward, imparting a shelf-like appearance to the thallus. The thallus attaches to the substrate by branched rhizoids produced along the margin of the thallus in contact with the substrate.

Conclusions: Hemiepiphytes are a key link in the evolution of epiphytic ferns and may act as a bridge between the forest floor and the canopy. Our finding is the first report of hemiepiphytism in Aspleniaceae, a large lineage with many epiphytic and terrestrial taxa. This work serves as an important model to understand the evolution of epiphytism in this group specifically and in ferns in general. The majority of our understanding of fern gametophyte biology is derived from laboratory studies. Our efforts represent a fundamental contribution to understanding fern gametophyte ecology in a field setting.
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http://dx.doi.org/10.1093/aob/mcz124DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6868390PMC
November 2019

A new protocol for psychrometric pressure-volume curves of fern gametophytes.

Appl Plant Sci 2019 May 10;7(5):e01248. Epub 2019 May 10.

Department of Botany University of Wisconsin Madison Wisconsin 35706 USA.

Premise: Pressurevolume curves are a widely used analytical framework to derive several key physiological traits related to plant-water relations, including a species' turgor loss point, osmotic potential at full turgor, and the elasticity of cell walls. We developed a novel protocol, including the preparation and treatment of fern gametophytes, to generate data for pressurevolume curve analyses using thermocouple psychrometry.

Methods And Results: Gametophytes of the fern species were grown from spore, harvested, and subjected to a series of drying intervals. We constructed pressure-volume curves using thermocouple psychrometers to calculate gametophyte water potential and a balance to measure relative water loss.

Conclusions: We present the first protocol for fern gametophyte pressure-volume curves that can accurately determine key physiological traits in fern gametophytes such as the turgor loss point and osmotic potential at full turgor.
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http://dx.doi.org/10.1002/aps3.1248DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6526695PMC
May 2019

Convergence of ecophysiological traits drives floristic composition of early lineage vascular plants in a tropical forest floor.

Ann Bot 2019 05;123(5):793-803

Department of Biology, Colgate University, Hamilton, NY, USA.

Background And Aims: Tropical understorey plant communities are highly diverse and characterized by variable resource availability, especially light. Plants in these competitive environments must carefully partition resources to ensure ecological and evolutionary success. One mechanism of effective resource partitioning is the optimization of functional traits to enhance competition in highly heterogeneous habitats. Here, we surveyed the ecophysiology of two early lineage vascular plant groups from a tropical forest understorey: Selaginella (a diverse lineage of lycophytes) and ferns.

Methods: In a lowland rain forest in Costa Rica, we measured a suite of functional traits from seven species of Selaginella and six fern species. We evaluated species microclimate and habitat; several photosynthetic parameters; carbon, nitrogen and phosphorus content; chlorophyll concentration; leaf mass per area (LMA); and stomatal size and density. We then compare these two plant lineages and search for relationships between key functional parameters that already exist on a global scale for angiosperms.

Key Results: Convergence of trait function filtered Selaginella species into different habitats, with species in heavily shaded environments having higher chlorophyll concentrations and lower light compensation points compared with open habitats. Alternatively, lower foliar nitrogen and higher stomatal densities were detected in species occupying these open habitats. Selaginella species had denser and smaller stomata, lower LMA and lower foliar nutrient content than ferns, revealing how these plant groups optimize ecophysiological function differently in tropical forest floors.

Conclusions: Our findings add key pieces of missing evidence to global explorations of trait patterns that define vascular plant form and function, which largely focus on seed plants. Broadly predictable functional trait relationships were detected across both Selaginella and ferns, similar to those of seed plants. However, evolutionary canalization of microphyll leaf development appears to have driven contrasting, yet successful, ecophysiological strategies for two coexisting lineages of extant homosporous vascular plants.
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http://dx.doi.org/10.1093/aob/mcy210DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6534666PMC
May 2019

Erratum: Sex-specific differences in functional traits and resource acquisition in five cycad species.

AoB Plants 2018 Oct 15;10(5):ply049. Epub 2018 Sep 15.

[This corrects the article DOI: 10.1093/aobpla/plx013.][This corrects the article DOI: 10.1093/aobpla/plx013.].
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http://dx.doi.org/10.1093/aobpla/ply049DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6146124PMC
October 2018

Germination fitness of two temperate epiphytic ferns shifts under increasing temperatures and forest fragmentation.

PLoS One 2018 11;13(5):e0197110. Epub 2018 May 11.

Department of Biology, Colgate University, Hamilton, New York, United States of America.

Ferns are an important component of ecosystems around the world. Studies of the impacts that global changes may have on ferns are scarce, yet emerging studies indicate that some species may be particularly sensitive to climate change. The lack of research in this subject is much more aggravated in the case of epiphytes, and especially those that live under temperate climates. A mathematical model was developed for two temperate epiphytic ferns in order to predict potential impacts on spore germination kinetics, in response to different scenarios of global change, coming from increasing temperature and forest fragmentation. Our results show that an increasing temperature will have a negative impact over the populations of these temperate epiphytic ferns. Under unfragmented forests the germination percentage was comparatively less influenced than in fragmented patches. This study highlight that, in the long term, populations of the studied epiphytic temperate ferns may decline due to climate change. Overall, epiphytic fern communities will suffer changes in diversity, richness and dominance. Our study draws attention to the role of ferns in epiphytic communities of temperate forests, emphasizing the importance of considering these plants in any conservation strategy, specifically forest conservation. From a methodological point of view, the model we propose could be easily used to dynamically monitor the status of ecosystems, allowing the quick prediction of possible future scenarios, which is a crucial issue in biodiversity conservation decision-making.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0197110PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5947888PMC
July 2018

Geometry, Allometry and Biomechanics of Fern Leaf Petioles: Their Significance for the Evolution of Functional and Ecological Diversity Within the Pteridaceae.

Front Plant Sci 2018 7;9:197. Epub 2018 Mar 7.

Biological Sciences, Wichita State University, Wichita, KS, United States.

Herbaceous plants rely on a combination of turgor, ground tissues and geometry for mechanical support of leaves and stems. Unlike most angiosperms however, ferns employ a sub-dermal layer of fibers, known as a hypodermal sterome, for support of their leaves. The sterome is nearly ubiquitous in ferns, but nothing is known about its role in leaf biomechanics. The goal of this research was to characterize sterome attributes in ferns that experience a broad range of mechanical stresses, as imposed by their aquatic, xeric, epiphytic, and terrestrial niches. Members of the Pteridaceae meet this criteria well. The anatomical and functional morphometrics along with published values of tissue moduli were used to model petiole flexural rigidity and susceptibility to buckling in 20 species of the Pteridaceae. Strong allometric relationships were observed between sterome thickness and leaf size, with the sterome contributing over 97% to petiole flexural rigidity. Surprisingly, the small-statured cheilanthoid ferns allocated the highest fraction of their petiole to the sterome, while large leaves exploited aspects of geometry (second moment of area) to achieve bending resistance. This pattern also revealed an economy of function in which increasing sterome thickness was associated with decreasing fiber cell reinforcement, and fiber wall fraction. Lastly, strong petioles were associated with durable leaves, as approximated by specific leaf area. This study reveals meaningful patterns in fern leaf biomechanics that align with species leaf size, sterome attributes and life-history strategy.
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http://dx.doi.org/10.3389/fpls.2018.00197DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5850050PMC
March 2018

Sex-specific differences in functional traits and resource acquisition in five cycad species.

AoB Plants 2017 03 5;9(2):013. Epub 2017 Apr 5.

Montgomery Botanical Centre, Miami, FL 33156, USA.

Selective pressures acting on plant life histories can drive extreme specialization. One example of such specialization is the evolution of dioecious breeding systems. Evolutionary and ecological theory posits that dioecy may subject male and female individuals to different selective pressures and result in unique sex-mediated adaptive traits related to resource allocation and ecophysiology. Cycads are the earliest diverging lineage of seed plants with strict dioecy, yet we know almost nothing about the ecology and physiology of this group. Especially limited is our understanding of potential sex-specific differences and how such differences may influence species ecology. Here we examine the ecophysiology of male and female cycads to understand better, the role that dioecy plays in this group. We evaluated sex-specific differences in ecophysiological traits and resource acquisition in five species. Specifically, we compared photosynthetic physiology, nitrogen and carbon content, isotope discrimination (δN and δC), and stomatal density. In some cycads, (i) males and females have similar investments in leaf nitrogen but females exhibit greater incorporation of nitrogen from nitrogen-fixing soil bacteria, (ii) males display higher photosynthetic capacity but females show decreased [corrected] water-use efficiency, and (iii) males have higher stomatal conductance but similar stomatal density to females. This study is the first to examine the ecophysiological differences that have evolved in the oldest dioecious lineage of seed-bearing plants. Our results show unexpected differences in photosynthetic physiology and highlight the co-evolution with nitrogen fixing soil bacteria as a potential new key player in an old lineage.
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http://dx.doi.org/10.1093/aobpla/plx013DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5420813PMC
March 2017

The economy of reproduction in dimorphic ferns.

Ann Bot 2016 11 1;118(6):1139-1149. Epub 2016 Sep 1.

Department of Biology, Colgate University, Hamilton, NY 13346, USA

Background And Aims: Organisms often balance among reproduction, growth and survival. When these processes are in competition, selection may act to drive functional dimorphism. Unlike seed plants, ferns use their foliar surfaces for reproduction and carbon fixation. Across species, ferns exhibit a gradient of fertile-sterile dimorphy: from the production of highly reduced fertile fronds (holodimorphic) to no reduction (monomorphic) in laminar area between fronds. Here the physiological impacts of fertile-sterile dimorphy were investigated through a series of observational and experimental field manipulations.

Methods: Temporal shifts in photosynthesis, respiration and percent nitrogen (%N) were examined to evaluate changes in physiological behaviour over the growing season of two species of fern of similar ecological niche, yet of different degrees of fertile-sterile frond dimorphism: Osmundastrum cinnamomeum (holodimorphic) and Osmunda regalis (hemidimorphic). These data are combined with experimental fertile and sterile frond removal to evaluate relative costs of reproduction in both species. Finally, labelled δC gas was used to follow carbon allocation across the growing season.

Key Results: The data demonstrate that reproductive structures in the holodimorphic O. cinnamomeum come at more significant carbon and nitrogen costs relative to those in the hemidimorphic O. regalis Excision experiments demonstrate that investment in fertile fronds strongly impacted future allocation to reproduction in the holodimorphic species but had a lesser effect on the hemidimorphic species. The labelling experiments showed that fixed carbon is translocated to the rhizomes only, but at different times in the two species. Investment in underground resources probably allows these plants to manage the costs of reproduction associated with increased dimorphy.

Conclusions: Fertile-sterile dimorphy has evolved multiple times in ferns in spite of the apparent physiological costs associated with a reduction in photosynthetically active tissues. These apparent costs may be offset by an increase in potential spore dispersal distance and/or increased spore production. The phenomenon may further influence species ecology as dimorphic taxa often occupy resource-rich environments.
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http://dx.doi.org/10.1093/aob/mcw177DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5091731PMC
November 2016

A site for sori: Ecophysiology of fertile-sterile leaf dimorphy in ferns.

Am J Bot 2016 05 10;103(5):845-55. Epub 2016 May 10.

Arnold Arboretum, Harvard University, 3105 Biological Laboratories, 16 Divinity Avenue.

Premise Of The Study: Reproduction often requires significant investment and can move resources away from growth and maintenance; maintaining a balance between reproduction and growth can involve trade-offs. Extreme functional specialization has separated reproduction and photosynthesis in most seed plants, yet ferns use the laminar surface of their fronds for both reproduction and photosynthesis. This dual function selects for a variety of frond morphologies that range from no specialization (monomorphy) to extreme dimorphy between fertile and sterile fronds (holodimorphy). Here we examined the ecological and physiological consequences of variation in frond dimorphy in ferns, evaluated reproductive trade-offs across a dimorphy gradient, and speculate on factors controlling the occurrence of holodimorphy.

Methods: Ecophysiological measurements of photosynthetic rate, water potential, hydraulic conductivity, and gross morphological comparisons of frond area and angle were used to evaluate differences between fertile and sterile fronds. We examined three temperate and three tropical fern species that vary in degree of fertile-sterile dimorphy.

Key Results: Holodimorphic species produced fewer fertile fronds, which had significantly higher respiratory rates than in sterile fronds on the same plant or in any frond produced on monomorphic species; hemidimorphic species were frequently intermediate. We found no differences in vulnerability to cavitation between fertile and sterile fronds. In dimorphic species, fertile fronds had higher (less negative) water potential and lower stipe hydraulic conductivity relative than in sterile fronds.

Conclusions: Fertile-sterile dimorphy in ferns appears to come at considerable carbon cost in holodimorohic species. It is possible that the relative costs of this reproductive system are offset by increased spore dispersal, yet such trade-offs require further exploration.
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http://dx.doi.org/10.3732/ajb.1500505DOI Listing
May 2016

On the widespread capacity for, and functional significance of, extreme inbreeding in ferns.

New Phytol 2016 08 20;211(3):1108-19. Epub 2016 Apr 20.

Biology Department, Colgate University, 129 Ho Science Center, 13 Oak Drive, Hamilton, NY, 13346, USA.

Homosporous vascular plants utilize three different mating systems, one of which, gametophytic selfing, is an extreme form of inbreeding only possible in homosporous groups. This mating system results in complete homozygosity in all progeny and has important evolutionary and ecological implications. Ferns are the largest group of homosporous land plants, and the significance of extreme inbreeding for fern evolution has been a subject of debate for decades. We cultured gametophytes in the laboratory and quantified the relative frequencies of sporophyte production from isolated and paired gametophytes, and examined associations between breeding systems and several ecological and evolutionary traits. The majority of fern species studied show a capacity for gametophytic selfing, producing sporophytes from both isolated and paired gametophytes. While we did not follow sporophytes to maturity to investigate potential detrimental effects of homozygosity at later developmental stages, our results suggest that gametophytic selfing may have greater significance for fern evolution and diversification than has previously been realized. We present evidence from the largest study of mating behavior in ferns to date that the capacity for extreme inbreeding is prevalent in this lineage, and we discuss its implications and relevance and make recommendations for future studies of fern mating systems.
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http://dx.doi.org/10.1111/nph.13985DOI Listing
August 2016

Ecophysiology of four co-occurring lycophyte species: an investigation of functional convergence.

AoB Plants 2015 Nov 24;7. Epub 2015 Nov 24.

Department of Biology, Colgate University, Hamilton, NY 13346, USA

Lycophytes are the most early divergent extant lineage of vascular land plants. The group has a broad global distribution ranging from tundra to tropical forests and can make up an important component of temperate northeast US forests. We know very little about the in situ ecophysiology of this group and apparently no study has evaluated if lycophytes conform to functional patterns expected by the leaf economics spectrum hypothesis. To determine factors influencing photosynthetic capacity (Amax), we analysed several physiological traits related to photosynthesis to include stomatal, nutrient, vascular traits, and patterns of biomass distribution in four coexisting temperate lycophyte species: Lycopodium clavatum, Spinulum annotinum, Diphasiastrum digitatum and Dendrolycopodium dendroideum. We found no difference in maximum photosynthetic rates across species, yet wide variation in other traits. We also found that Amax was not related to leaf nitrogen concentration and is more tied to stomatal conductance, suggestive of a fundamentally different sets of constraints on photosynthesis in these lycophyte taxa compared with ferns and seed plants. These findings complement the hydropassive model of stomatal control in lycophytes and may reflect canalization of function in this group. Our data also demonstrate functional ecological similarities: De. dendroideum and D. digitatum are species that have substantial belowground biomass investment and are consistently more similar to each other across multiple traits than either is to the more surficial S. annotinum and L. clavatum. Such differences may partition environments in ways that allow for the close coexistence of these species.
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http://dx.doi.org/10.1093/aobpla/plv137DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4689120PMC
November 2015

Dynamics of asymmetrical hybridization in North American wood ferns: reconciling patterns of inheritance with gametophyte reproductive biology.

New Phytol 2015 Apr 1;206(2):785-95. Epub 2014 Dec 1.

Department of Plant Biology, University of Vermont, 111 Jeffords Hall, 63 Carrigan Drive, Burlington, VT, 05405, USA.

Hybridization is an important evolutionary force in plants, but the mechanisms underlying it have not been well studied for many groups. In particular, the drivers of non-random patterns of interspecific gene flow (asymmetrical hybridization) remain poorly understood, especially in the seed-free vascular plants. Here, we examine patterns of asymmetrical hybridization in two widespread fern hybrids from eastern North America and study the role of gametophyte ecology in the determination of hybridization bias. We characterized the maternal parentage of > 140 hybrid sporophytes by sequencing a c. 350-bp region of chloroplast DNA (cpDNA). To identify factors contributing to patterns of asymmetrical hybridization, we cultured gametophytes of the parental species and evaluated critical aspects of their reproductive biology. We found that asymmetrical hybridization was prevalent across the populations of both hybrids. Reproductive traits varied across species and suggest that selfing potential, antheridiogen responsiveness, sperm dispersal capacity and gamete size all contribute to the mediation of the direction of hybridization in this group. Our findings suggest that asymmetrical hybridization in ferns is driven by an array of reproductive traits. This study helps to sharpen and define a mechanistic understanding of patterns of hybridization in this group and demonstrates the importance of considering gametophyte biology when studying evolutionary processes in ferns.
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http://dx.doi.org/10.1111/nph.13213DOI Listing
April 2015

Understanding mechanisms of rarity in pteridophytes: competition and climate change threaten the rare fern Asplenium scolopendrium var. americanum (Aspleniaceae).

Am J Bot 2013 Nov 3;100(11):2261-70. Epub 2013 Nov 3.

Department of Plant Biology, University of Vermont, 111 Jeffords Hall, 63 Carrigan Drive, Burlington, Vermont USA 05405.

Premise Of The Study: Understanding the ecology of rare species can inform aspects of conservation strategies; however, the mechanisms of rarity remain elusive for most pteridophytes, which possess independent and ecologically distinct gametophyte and sporophyte generations. To elucidate factors contributing to recent declines of the rare fern Asplenium scolopendrium var. americanum, we studied the ecology and ecophysiology of its gametophyte generation, focusing on responses to competition, temperature, and water stress.

Methods: Gametophytes of A. scolopendrium var. americanum, its widespread European relative A. scolopendrium var. scolopendrium, and five co-occurring fern species were grown from spores. Gametophytes were grown at 20°C and 25°C, and germination rates, intra- and interspecific competition, desiccation tolerance, and sporophyte production were determined for all species.

Key Results: Gametophytes of A. scolopendrium var. americanum had the lowest rates of germination and sporophyte production among all species studied and exhibited the greatest sensitivity to interspecific competition, temperature increases, and desiccation. Mature gametophytes of A. scolopendrium var. americanum grown at 25°C were 84.6% smaller than those grown at 20°C, and only 1.5% produced sporophytes after 200 d in culture. Similar responses were not observed in other species studied.

Conclusions: The recent declines and current status of populations of A. scolopendrium var. americanum are linked to its gametophyte's limited capacity to tolerate competition and physiological stress linked to climate change. This is the first study to develop a mechanistic understanding of rarity and decline in a fern and demonstrates the importance of considering the ecology of the gametophyte in plants with independent sporophyte and gametophyte generations.
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http://dx.doi.org/10.3732/ajb.1300150DOI Listing
November 2013

The physiological resilience of fern sporophytes and gametophytes: advances in water relations offer new insights into an old lineage.

Front Plant Sci 2013 5;4:285. Epub 2013 Aug 5.

Department of Ecology and Evolutionary Biology, University of California Santa Cruz, CA, USA.

Ferns are some of the oldest vascular plants in existence and they are the second most diverse lineage of tracheophytes next to angiosperms. Recent efforts to understand fern success have focused on the physiological capacity and stress tolerance of both the sporophyte and the gametophyte generations. In this review, we examine these insights through the lens of plant water relations, focusing primarily on the form and function of xylem tissue in the sporophyte, as well as the tolerance to and recovery from drought and desiccation stress in both stages of the fern life cycle. The absence of secondary xylem in ferns is compensated by selection for efficient primary xylem composed of large, closely arranged tracheids with permeable pit membranes. Protection from drought-induced hydraulic failure appears to arise from a combination of pit membrane traits and the arrangement of vascular bundles. Features such as tracheid-based xylem and variously sized megaphylls are shared between ferns and more derived lineages, and offer an opportunity to compare convergent and divergent hydraulic strategies critical to the success of xylem-bearing plants. Fern gametophytes show a high degree of desiccation tolerance but new evidence shows that morphological attributes in the gametophytes may facilitate water retention, though little work has addressed the ecological significance of this variation. We conclude with an emergent hypothesis that selection acted on the physiology of both the sporophyte and gametophyte generations in a synchronous manner that is consistent with selection for drought tolerance in the epiphytic niche, and the increasingly diverse habitats of the mid to late Cenozoic.
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http://dx.doi.org/10.3389/fpls.2013.00285DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3733004PMC
August 2013

Influence of plant size on the ecophysiology of the epiphytic fern Asplenium auritum (Aspleniaceae) from Costa Rica.

Am J Bot 2012 Nov 6;99(11):1840-6. Epub 2012 Nov 6.

Department of Biology, 13 Oak Drive, Colgate University, Hamilton, New York 13346, USA.

Premise Of The Study: A central goal of plant ecophysiological studies is to generate patterns of physiological behavior that are applicable to a species, which can be complicated when plant size is considered. Studies indicate that plant size can influence numerous ecophysiological parameters, especially in vascular epiphytes. The few studies that have included ferns in their analyses suggest that plant size is less important in ferns than angiosperms. This study investigates this apparent disparity by examining the relationship between plant size and an array of ecophysiological parameters in the epiphytic fern Asplenium auritum, especially the role of plant size in determining responses to water stress.

Methods: Plants were classified according to size and measured for a variety of functional traits, including maximum photosynthetic rate, stomatal conductance, water-use efficiency, stomatal density, chlorophyll content, chlorophyll a/b ratio, specific leaf area, whole plant drying rates, and desiccation tolerance. Results for all traits were compared across size classes to determine size-related differences.

Key Results: Plant size significantly influenced most traits examined, most notably photosynthetic rate, stomatal density, stomatal conductance, whole plant drying rates, and recovery from desiccation. We report the first evidence of size-mediated shifts in desiccation tolerance in plants: small individuals tolerated water loss, whereas larger individuals avoided desiccation.

Conclusions: Our findings indicate that size-mediated ecophysiological shifts are more important than previously thought in ferns, particularly in regard to water relations. Desiccation tolerance may allow young fern sporophytes to establish in stressful environments and is subsequently lost in older individuals.
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http://dx.doi.org/10.3732/ajb.1200329DOI Listing
November 2012

Hydraulic properties of fern sporophytes: Consequences for ecological and evolutionary diversification.

Am J Bot 2010 Dec 24;97(12):2007-19. Epub 2010 Nov 24.

Department of Biology, Colgate University, 13 Oak Drive, Hamilton, New York 13346 USA.

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Premise Of The Study: Ferns are an important component of both tropical and temperate forests; yet, our understanding of the water relations of their sporophyte generation is limited. Indeed, to date there has been no large scale survey that attempts to clarify how ferns fit into current ideas of plant water relations. This study examines several tropical ferns with the goal of understanding how these characters vary between species from various habitats and across life forms •

Methods: We measured stipe hydraulic conductivity, water potential, and vulnerability to cavitation along with photosynthetic variables and leaf allometry of 21 species from 14 genera to identify physiological trait assemblages across taxa. •

Key Results: Epiphytic ferns have significantly lower hydraulic conductivity and a vascular system more resistant to cavitation (i.e., higher P(50) values). They reached lower mid-day water potentials and produced leaves with reduced stipe lengths and reduced laminar area relative to terrestrial species. Xylem specific hydraulic conductivity (K(S)) was correlated with the mean hydraulic diameter of tracheids in terrestrial species, but not in epiphytes. There was no evidence of safety-efficiency trade-offs in any group. •

Conclusions: When compared across life forms, our data shed light on physiological mechanisms that may have allowed for terrestrial ferns to move into the epiphytic habit. When compared across a diverse assemblage of terrestrial plants, we find that resistance to water flow in fern stipes is significantly higher than that recorded from the stems of seed plants.
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http://dx.doi.org/10.3732/ajb.1000124DOI Listing
December 2010

Ants mediate nitrogen relations of an epiphytic fern.

New Phytol 2008 ;180(1):5-8

University of Florida, Department of Botany, Gainesville, FL 32611, USA.

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http://dx.doi.org/10.1111/j.1469-8137.2008.02606.xDOI Listing
November 2008

Ecological and evolutionary consequences of desiccation tolerance in tropical fern gametophytes.

New Phytol 2007 23;176(3):708-717. Epub 2007 Aug 23.

University of Florida, Department of Botany, 211 Bartram Hall, Gainesville, FL 32611-0500, USA.

Ferns have radiated into the same diverse environments as spermatophytes, and have done so with an independent gametophyte that is not protected by the parent plant. The degree and extent of desiccation tolerance (DT) in the gametophytes of tropical fern species was assessed to understand mechanisms that have allowed ferns to radiate into a diversity of habitats. Species from several functional groups were subjected to a series of desiccation events, including varying degrees of intensity and multiple desiccation cycles. Measurements of chlorophyll fluorescence were used to assess recovery ability and compared with species ecology and gametophyte morphology. It is shown that vegetative DT (rare in vascular plants) is widely exhibited in fern gametophytes and the degree of tolerance is linked to species habitat preference. It is proposed that gametophyte morphology influences water-holding capacity, a novel mechanism that may help to explain how ferns have radiated into drought-prone habitats. Fern gametophytes have often been portrayed as extreme mesophytes with little tolerance for desiccation. The discovery of DT in gametophytes holds potential for improving our understanding of both the controls on fern species distribution and their evolution. It also advances a new system with which to study the evolution of DT in vascular plants.
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http://dx.doi.org/10.1111/j.1469-8137.2007.02194.xDOI Listing
February 2008

The influence of life form on carbon and nitrogen relationships in tropical rainforest ferns.

Oecologia 2007 Aug 6;153(2):225-32. Epub 2007 Apr 6.

Arnold Arboretum, Harvard University, 3105 Biological Laboratories, 16 Divinity Ave, Cambridge, MA 02138, USA.

Tropical ferns are characterized by a high diversity of plant life forms, yet there have been few large-scale studies on the functional ecology of these different forms. We examined epiphytic, hemiepiphytic, and terrestrial ferns, and asked whether there are differences in the mineral nutrition and water relations across different growth forms of a diverse assemblage of species. We measured specific leaf area, leaf nitrogen concentrations, and natural abundance of the stable isotopes delta(15)N and delta(13)C of 48 fern species from 36 genera across a wide range of habitats at La Selva Biological Station in Costa Rica. We found that epiphytes were significantly different in all measured variables from hemiepiphytic and terrestrial species, and that terrestrial and soil-rooted hemiepiphytes were indistinguishable in all variables excluding SLW. A multivariate analysis revealed that aspects of N nutrition were the most reliable at separating epiphytic species from other life forms. Our study demonstrates that the natural abundance of both C and N as well as N relations and leaf morphology are useful when segregating different plant life forms, and that the N cycle of epiphytic and terrestrial habitats function independently from each other.
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http://dx.doi.org/10.1007/s00442-007-0723-1DOI Listing
August 2007

Gametophyte ecology and demography of epiphytic and terrestrial tropical ferns.

Am J Bot 2007 Apr;94(4):701-8

Department of Botany, University of Florida, Gainesville, Florida 32601 USA.

Factors that influence the distribution of ferns are poorly understood and likely reflect the ecology of both the sporophyte and the gametophyte generation. Little study has been done on the ecology of the gametophyte generation, especially in regard to tropical species. The goal of this study was to examine demography and the influence of light and disturbance on the distribution of the gametophytes of several tropical epiphytic, hemiepiphytic, and terrestrial fern species. Through a series of observational and experimental studies, we found that increased terrestrial gametophyte density and richness were related to both increased light and disturbance. By contrast, increased light had no influence, and increased disturbance negatively affected epiphytic density. Over a 25-mo demographic study, epiphytic and hemiepiphytic species had significantly greater longevities and lower recruitment rates than terrestrial species. Such unique strategies may have evolved in response to different disturbance regimens between the two habitats. Terrestrial species encounter and are adapted to more frequent disturbance and have invested in rapid gametophyte growth and recruitment. Epiphytic species may be more influenced by bryophyte competition, and in habitats of relatively low disturbance, they have invested in greater size and longevities. In such systems, gametophytes are able to survive for years waiting for favorable recruitment conditions.
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http://dx.doi.org/10.3732/ajb.94.4.701DOI Listing
April 2007

Mechanical stress activates xanthine oxidoreductase through MAP kinase-dependent pathways.

Am J Physiol Lung Cell Mol Physiol 2006 Sep 21;291(3):L345-53. Epub 2006 Apr 21.

Division of Pulmonary and Critical Care Medicine, Bloomberg School of Public Health, Baltimore, Maryland, USA.

Xanthine oxidoreductase (XOR) plays a prominent role in acute lung injury because of its ability to generate reactive oxygen species. We investigated the role of XOR in ventilator-induced lung injury (VILI). Male C57BL/6J mice were assigned to spontaneous ventilation (sham) or mechanical ventilation (MV) with low (7 ml/kg) and high tidal volume (20 ml/kg) for 2 h after which lung XOR activity and expression were measured and the effect of the specific XOR inhibitor allopurinol on pulmonary vascular leakage was examined. In separate experiments, rat pulmonary microvascular endothelial cells (RPMECs) were exposed to cyclic stretch (5% and 18% elongation, 20 cycles/min) for 2 h before intracellular XOR activity measurement. Lung XOR activity was significantly increased at 2 h of MV without changes in XOR expression. There was evidence of p38 MAP kinase, ERK1/2, and ERK5 phosphorylation, but no change in JNK phosphorylation. Evans blue dye extravasation and bronchoalveolar lavage protein concentration were significantly increased in response to MV, changes that were significantly attenuated by pretreatment with allopurinol. Cyclic stretch of RPMECs also caused MAP kinase phosphorylation and a 1.7-fold increase in XOR activity, which was completely abrogated by pretreatment of the cells with specific MAP kinase inhibitors. We conclude that XOR enzymatic activity is significantly increased by mechanical stress via activation of p38 MAP kinase and ERK and plays a critical role in the pathogenesis of pulmonary edema associated with VILI.
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http://dx.doi.org/10.1152/ajplung.00453.2005DOI Listing
September 2006

Genetic variation in populations of the morphologically and ecologically variable fern Stegnogramma pozoi subsp. mollissima (Thelypteridaceae) in Japan.

J Plant Res 2002 Feb;115(1117):29-38

Department of Botany, Graduate School of Science, Kyoto University, Kyoto 606-8502, Japan.

In Japanese Stegnogramma pozoi subsp. mollissima (Fisher ex Kunze) K. Iwats. there is the intrasubspecific variation among rbcL sequences. Northern and southern plants are genetically differentiated for maternally inherited cpDNA. In the present study we examined allozyme polymorphisms to test the hypothesis that northern and southern plants may be separate species. Based on allozyme data, the degree of gene flow among populations was estimated to be large. The artificial crossing experiments between cpDNA haplotypes also suggested that isolation has not developed among these cpDNA haplotypes. However, interpopulation genetic differentiation in cpDNA was observed even in the small area at the foot of Mt. Hakone, and the cpDNA haplotypes appear to have different habitat preferences.
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http://dx.doi.org/10.1007/s102650200005DOI Listing
February 2002