James E. Watkins

Gametophyte ecology and demography of epiphytic and terrestrial tropical ferns

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.

Ferns in an Angiosperm World: Cretaceous Radiation into the Epiphytic Niche and Diversification on the Forest Floor

The Cretaceous period saw dramatic shifts in the functional plant biology of the Earth’s flora. This was an episode of explosive plant radiations that produced our modern angiosperm-dominated world. This period was also a time of great Pteridophytic diversification and experimentation and saw the rise of most extant fern lineages. Prominent among these was the widespread appearance of epiphytic species. In modern tropical forest canopies, epiphytic ferns often represent some of the most abundant taxa and can dominate epiphyte biomass. Yet from most perspectives, the epiphytic habitat is vastly different from the forest floor. What happened during the Cretaceous that led to such widespread epiphyte fern diversification? What are the traits that allow extant ferns to flourish in this dry, nutrient-poor, bright habitat? How did terrestrial ferns cope with this new habitat? We review a number of functional aspects of fern biology to include both gametophytic and sporophytic physiology. It is possible that angiosperms engineered conditions that lead to aseasonal tropical forests. Data suggest that ferns may have reduced water use efficiency. If so, then wetter forests may have facilitated fern diversification. Successful epiphytic species would have required major modification in the gametophyte generation to include indeterminate growth, extreme stress tolerance, and an outcrossing breeding system. Terrestrial species also radiated at this time and may have relied on unique aspects of photobiology to take advantage of low-light terrestrial habitats. The study of fern ecology has reached a fevered pitch. Continued investigation will no doubt reveal some of the most exciting changes in our understanding of this remarkable lineage.

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

UNLABELLED 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.

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

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.

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

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 δ15N and δ13C 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.

Prevalence of coagulation abnormalities associated with intrauterine fetal death

PurposeThe purpose of this study was to determine factors associated with abnormal coagulation in the setting of intrauterine fetal death (IUFD).MethodsWe reviewed the charts of 238 patients diagnosed with IUFD over ten years. Data included demographics, coexisting obstetric disease and coagulation studies. A coagulation score was assigned based on the platelet count, prothrombin time, activated partial thromboplastin time and plasma fibrinogen concentration. Approximately 90% of the study population had coagulation scores <4. A score of > 4 was considered abnormal.ResultsComplete coagulation analysis was available in 183/238 patients (77%) within 24 hr of delivery. One hundred and sixty-four of these (89.6%) had a coagulation score <4 and 19 had a score > 4 (10.4%). No relationship between the coagulation score and age, parity, gestational age at delivery, and number of days the dead fetus remained in utero was found. A coagulation score > 4 was associated with the presence of a pregnancy-related disease (P < 0.05), notably abruption (P < 0.001) and uterine perforation (P < 0.05). Four patients without co-existing disease (3.2%), had a coagulation score ≥4.ConclusionIn most pregnancies complicated by fetal demise, the fetus and placenta are delivered within one week of fetal demise. The previously reported severe coagulation disturbances are largely eliminated by early delivery. Our study shows that coagulation abnormalities occur in some patients with uncomplicated IUFDs (3.2%) and that this number rises in the presence of abruption or uterine perforation.RésuméObjectifCette étude visait à déterminer les facteurs associés à une coagulation anormale dans un contexte de mortalité foetale in utero (MFIU).MéthodesLes auteurs ont relevé les dossiers de 238 patientes porteuses d’un diagnostic de MFIU sur une période de dix ans. Les données incluaient la démographie, les affections obstétricales associées et le bilan hémostatique. Un score de coagulabilité a été assigné d’après le décompte plaquettaire, le temps de prothrombine, le temps de thromboplastine partielle activé et la concentration plasmatique du fibrinogène. Environ 90% de la population étudiée avait un score de coagulabilité <4. Un score ≥4 était considéré comme anormal.RésultatsUn bilan hémostatique était disponible chez 183/238 patientes (77%) à 24 h de l’accouchement. De ces patientes, 164 (89,6%) avaient un score de coagulabilité <4, et 19 avaient un score ≥4 (10,4%). On n’a pas trouvé de rapport entre le score de coagulabilité et l’âge, la parité, l’âge gestationel à l’accouchement et la durée de présence du foetus mort in utero. Un score de coagulabilité ≥ 4 était associé à une maladie de la grossesse (P < 0,05), notamment à un décollement placentaire (P < 0,001) ou à perforation utérine (P < 0,05). Quatre patientes sans maladies obstétricales associées (3,2%) avaient un score de coagulabilité ≥4.ConclusionLa plupart des grossesses compliquées par une mort foetale expulsent le foetus et le placenta dans le semaine qui suit ta mort du foetus. Les dérangements graves de la coagulation rapportés antérieurement sont en grande partie éliminés par un accouchement précoce. Notre étude montre que les anomalies de la coagulation surviennent chez certaines patientes avec une MFIU (3,2%) et que ce nombre augmente en présence d’un décollement placentaire ou d’une perforation utérine.

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

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 gametophytes 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.

Fern Laminar Scales Protect Against Photoinhibition from Excess Light

ABSTRACT The laminar scales of the fern Elaphoglossum paleaceum were studied to determine if they act as a morphological mechanism to protect leaves from excess light. We hypothesized that if scales serve this purpose, then individual plants growing in high light would have greater laminar scale density than those in low light. For our first experiment, plants from high light roadsides were collected and subjected to artificial scale removal and then exposed to super-saturating pulse of light for 30 min. We found that leaves with their scales removed exhibited significantly greater photoinhibition than leaves with scales intact. Leaves with intact scales recovered fully after twelve hours whereas those with scales removed remained photoinhibited. Scale density on the adaxial side of leaves was positively correlated with light intensity. The data from this study indicate that fern laminar scales help reduce photoinhibition and potentially function as a morphological defense against photodamage.

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

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.

Habitat differentiation of ferns in a lowland tropical rain forest.

Abstract Fern species and growth form diversity peak in tropical rainforests. In such forests, ferns often play important ecological roles. However the distribution and diversity patterns of different growth forms (i.e., epiphytic vs. terrestrial ferns) have not been broadly quantified. We compared the distribution and diversity patterns of epiphytic pteridophytes on the trunks of six individuals of the emergent canopy tree species Hyeronima alchorneoides (Euphorbiaceae) to those of terrestrial species at La Selva Biological Station in Heredia province, Costa Rica. A total of 21 species of epiphytic and 20 terrestrial ferns was recorded, with only one species found as an epiphyte and as a terrestrial species. Epiphytic species also exhibited increasing species diversity with increasing trunk height. Epiphytic species exhibited predictable patterns of distribution along the trunk and were easily grouped into high-trunk, low trunk, or bimodal categories. In terms of percent cover and number of species, simple-leaved ferns dominated the epiphytic growth form, 13 of 21 species, whereas ferns with compound or dissected leaves dominated the hemi-epiphytic and terrestrial floras with 20 of 20 species. These results indicate that there are significant functional differences in the ecology of epiphytic and terrestrial ferns and that reciprocal establishment is difficult and extremely rare.