The reproductive biology of the invasive ferns Lygodium microphyllum and L. japonicum (Schizaeaceae): implications for invasive potential
TL;DR: The mixed mating system observed in L. microphyllum appears to give this species the ability to invade distant habitats and then adapt to local conditions, which has likely facilitated their ability to colonize and spread through Florida.
Abstract: The effect of culture system and population source on sexual expression and sporophyte production was examined for two invasive fern species in Florida, USA, Lygodium microphyllumand L. japonicum (Schizaeaceae). Both species are currently spreading through Florida. Long-distance dispersal of ferns is thought to rely on successful intragametophytic selfing. Given the rate of spread observed in both Lygodium species, we hypothesized that both species are capable of intragametophytic selfing. To test this hypothesis, gametophytes of both species were grown in vitro as isolates, pairs, and groups. Both species were capable of intragametophytic selfing; 78% of L. microphyllum isolates produced sporophytes and over 90% of the L. japonicum isolates produced sporophytes. Lygodium microphyllum also displayed the ability to reproduce via intergametophytic crossing, facilitated by an antheridiogen pheromone. Sporophyte production was rapid across mating systems for both species, an advantage in Florida’s wet and dry seasonal cycles. The high intragametophytic selfing rate achieved by both species has likely facilitated their ability to colonize and spread through Florida. The mixed mating system observed in L. microphyllum appears to give this species the ability to invade distant habitats and then adapt to local conditions.
Citations
More filters
TL;DR: It appears likely that traits related to its reproduction, such as propagule pressure, and its ability to grow in a lowlight understorey environment, may be among the most important in explaining its able to invade both disturbed and undisturbed areas far from source populations.
Abstract: Lygodium microphyllum (Cav.) R. Br. ( Lygodiaceae) is a climbing fern that is becoming one of the worst non-indigenous invasive plant species in the greater Everglades ecosystem of southern Florida, USA. We examined the fern across a range of scales including the seasonality of its spore production, its height growth within infested sites and its community ecology. These attributes, combined with a series of aerial transects that identified L. microphyllum infestations across southern Florida, were used to develop a spatial model to predict its future spread in the Everglades landscape. The model shows that this non-indigenous invader could become widely established throughout the Everglades by 2014. Although several factors, such as release from natural enemies, may help explain the invasion success of L. microphyllum , it appears likely that traits related to its reproduction, such as propagule pressure, and its ability to grow in a lowlight understorey environment, may be among the most important in explaining its ability to invade both disturbed and undisturbed areas far from source populations.
89 citations
Cites background or result from "The reproductive biology of the inv..."
...Our previous work demonstrated that L. microphyllum possesses a highly plastic reproductive capability, being able to reproduce by a mixed-mating strategy, which is relatively uncommon among homosporous ferns (Klekowski, 1982; Lott et al., 2003)....
[...]
...L. microphyllum possesses all of these traits except vegetative reproduction (Lott et al., 2003)....
[...]
...Unlike kudzu, whose spread has been inhibited by a lack of viable seed (Mitich, 2000), L. microphyllum has high spore viability and a highly plastic reproductive strategy that allows it to become established far from source populations (Lott et al., 2003)....
[...]
...The high selfing rates and the ability to also mate by intergametophytic crossing enhance the ability of this species both to invade distant habitats and to adapt to local conditions (Lott et al., 2003)....
[...]
...The fern is able to reproduce by all three mating systems possible in homosporous ferns: intra- and intergametophytic selfing and outcrossing (Lott et al. , 2003)....
[...]
TL;DR: Baker's Law is extended by predicting other colonizing haplo‐diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage, as well as investigating shifts in reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla.
Abstract: Baker's Law predicts uniparental reproduction will facilitate colonization success in novel habitats. While evidence supports this prediction among colonizing plants and animals, few studies have investigated shifts in reproductive mode in haplo-diplontic species in which both prolonged haploid and diploid stages separate meiosis and fertilization in time and space. Due to this separation, asexual reproduction can yield the dominance of one of the ploidy stages in colonizing populations. We tested for shifts in ploidy and reproductive mode across native and introduced populations of the red seaweed Gracilaria vermiculophylla. Native populations in the northwest Pacific Ocean were nearly always attached by holdfasts to hard substrata and, as is characteristic of the genus, haploid–diploid ratios were slightly diploid-biased. In contrast, along North American and European coastlines, introduced populations nearly always floated atop soft-sediment mudflats and were overwhelmingly dominated by diploid thalli without holdfasts. Introduced populations exhibited population genetic signals consistent with extensive vegetative fragmentation, while native populations did not. Thus, the ecological shift from attached to unattached thalli, ostensibly necessitated by the invasion of soft-sediment habitats, correlated with shifts from sexual to asexual reproduction and slight to strong diploid bias. We extend Baker's Law by predicting other colonizing haplo-diplontic species will show similar increases in asexuality that correlate with the dominance of one ploidy stage. Labile mating systems likely facilitate colonization success and subsequent range expansion, but for haplo-diplontic species, the long-term eco-evolutionary impacts will depend on which ploidy stage is lost and the degree to which asexual reproduction is canalized.
75 citations
Cites background from "The reproductive biology of the inv..."
...…after Baker’s (1955) seminal paper was published, it is now clear that his ideas apply to haplodiplontic life cycles, such as those found in ferns (Lott et al. 2003; Flinn 2006; de Groot et al. 2012), mosses (Pati~no et al. 2013; Laenen et al. 2016) and, now, explicitly in seaweeds (but see…...
[...]
...For ferns (Klekowski 2003; Lott et al. 2003; Flinn 2006; Wubs et al. 2010; de Groot et al. 2012), mosses (Pati~no et al. 2013; Laenen et al. 2016), fungi (Gladieux et al. 2015) and seaweeds (West et al. 2001; Gabrielson et al. 2002; Hwang et al. 2005; Fierst et al. 2010; KruegerHadfield et al.…...
[...]
...Decades after Baker’s (1955) seminal paper was published, it is now clear that his ideas apply to haplodiplontic life cycles, such as those found in ferns (Lott et al. 2003; Flinn 2006; de Groot et al. 2012), mosses (Pati~ no et al....
[...]
...For ferns (Klekowski 2003; Lott et al. 2003; Flinn 2006; Wubs et al. 2010; de Groot et al. 2012), mosses (Pati~ no et al....
[...]
TL;DR: Evidence is presented from the largest study of mating behavior in ferns to date that the capacity for extreme inbreeding is prevalent in this lineage, and its implications and relevance are discussed and recommendations are made for future studies of fern mating systems.
Abstract: Summary
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.
60 citations
Cites background from "The reproductive biology of the inv..."
...…should be more tolerant of selfing than their diploid relatives (see, e.g., Stebbins, 1950; Grant, 1956; Soltis & Soltis, 1987; Haufler, 1989; Masuyama & Watano, 1990; Barringer, 2007; Ozimec & Husband, 2011), we did see higher average isolate potentials in polyploid compared with diploid…...
[...]
...It has therefore long been suggested that polyploids should be more tolerant of GS than diploids (Klekowski & Baker, 1966; Klekowski, 1973; Chapman et al., 1979; Holsinger, 1987; Haufler, 1989; Soltis & Soltis, 1989; Masuyama & Watano, 1990)....
[...]
TL;DR: The hypothesis that selfing may facilitate colonization in better-colonizing species and post-agricultural forest populations have greater selfing ability is supported and the general pattern that polyploid fern species have higher rates of self-fertilization than related diploids is exemplified.
Abstract: Because selfing enables a single individual to reproduce in a new location, the ability to self-fertilize should enhance plants' capacity for colonization. This study examined whether selfing ability correlated with successful migration in three fern species, Dryopteris carthusiana, Dryopteris intermedia, and Polystichum acrostichoides, which vary in their ability to colonize forests on abandoned agricultural lands in central New York, USA. Polystichum acrostichoides is much more frequent in forests that were never cleared for agriculture, D. carthusiana is more frequent in forests that developed on former fields, and D. intermedia is equally frequent in the two forest types. To test the hypothesis that better-colonizing species and post-agricultural forest populations have greater selfing ability, I assessed the sporophyte production of gametophytes grown in isolation and in pairs of varying relatedness. Dryopteris carthusiana had the highest reproductive success and selfing ability and P. acrostichoides the lowest. These results support the hypothesis that selfing may facilitate colonization in these species. They also exemplify the general pattern that polyploid fern species have higher rates of self-fertilization than related diploids, as the allotetraploid D. carthusiana had greater selfing ability than both diploid species.
57 citations
Cites background from "The reproductive biology of the inv..."
...A high capacity for self-fertilization may also have facilitated the spread of two invasive fern species in Florida (Lott et al., 2003)....
[...]
TL;DR: Soil pH 8.0 was not strong enough for a pronounced growth decline, thus further increasing soil pH could provide a desired outcome and merit further investigation, although its potential negative impact on native flora (both plants and microorganisms) would need to be assessed.
Abstract: Lygodium microphyllum is an invasive exotic plant species taking over many sites in freshwater and moist habitats in Florida. Managing it has been a significant challenge for land resource managers and researchers due to its extensive rapid invasion. To assess the effects of soil pH on growth, nutrient uptake, and mycorrhizal colonization in the roots of L. microphyllum, we conducted a 60-day greenhouse experiment by growing it in pots filled with pH-adjusted soils to a range from 4.5 to 8.0. L. microphyllum was able to survive and grow at all soil pH levels; however, final biomass, relative growth rate, photosynthesis, and specific leaf area were all greater in soil pH 5.5–6.5 compared to the other treatments. Correspondingly, nitrogen concentration was also related to these four plant parameters. Root colonization by mycorrhizal fungi was higher in soil pH 5.5–7.5 and lowest for plants growing in 4.5 or 8.0 and was correlated with plant growth parameters as well as elemental concentration in the leaves. Soil pH 8.0 was not strong enough for a pronounced growth decline, thus further increasing soil pH could provide a desired outcome and merit further investigation, although its potential negative impact on native flora (both plants and microorganisms) would need to be assessed.
52 citations
Cites methods or result from "The reproductive biology of the inv..."
...Plant material Experimental plants were grown from spores following the method used by Lott et al. (2003)....
[...]
...Previous studies have shown that L. microphyllum is extremely plastic in its ability to respond to myriad environmental conditions, including plasticity in reproduction, physiology, biomass allocation, and morphology (see: Lott et al. 2003; Gandiaga et al. 2009; Volin et al. 2004, 2010)....
[...]
References
More filters
University of California, Irvine1, University of Montana2, University of California, Riverside3, University of Notre Dame4, University of Vermont5, Kansas State University6, State University of New York at Plattsburgh7, Rockefeller University8, Vanderbilt University9, University of New Orleans10, University of California, Santa Cruz11
TL;DR: In this article, the introduction of invasive species and identifying life history stages where management will be most effective are discussed. And evolutionary processes may be key features in determining whether invasive species establish and spread.
Abstract: ■ Abstract Contributions from the field of population biology hold promise for understanding and managing invasiveness; invasive species also offer excellent opportunities to study basic processes in population biology. Life history studies and demographic models may be valuable for examining the introduction of invasive species and identifying life history stages where management will be most effective. Evolutionary processes may be key features in determining whether invasive species establish and spread. Studies of genetic diversity and evolutionary changes should be useful for
3,280 citations
1,570 citations
"The reproductive biology of the inv..." refers background in this paper
...…reproductive age or size, high and continuous seed (spore) production, adaptations for short- and long-distance seed (spore) or vegetative dis- persal, and vegetative as well as sexual reproduction (Baker, 1974; Newsome and Noble, 1986; Roy, 1990; Reichard and Hamilton, 1997; Sakai et al., 2001)....
[...]
TL;DR: In this paper, a retrospective analysis of several structural, life history, and biogeographical attributes of woody plants introduced in North America to determine which traits characterize species that have and have not invaded.
Abstract: Plant species continue to be introduced in North America for various purposes. If the trend continues, it is probable that some will escape cultivation and become invasive in native ecosystems. We present a retrospective analysis of several structural, life history, and biogeographical attributes of woody plants introduced in North America to determine which traits characterize species that have and have not invaded. Predictive models derived from discriminant analysis correctly classified 86.2% of the species in cross-validation, whereas those derived from classification and regression trees classified 76% correctly. From these models we created a hierarchical predictive tree that allows the user to divide species into three categories: admit (low risk of invasiveness), deny admission (high risk of invasiveness), or delay admission for further analyses and/or monitor intensively (risk cannot adequately be assessed based on only the included attributes). We recommend that species that are highly invasive elsewhere not be allowed into the U.S. and that a more conservative introduction policy using a hierarchical predictive method be employed.
Especies de plantas continuan siendo introducidas a Norteamerica para diversos motivos. De continuar la tendencia, es probable que alguna escape y se vuelva invasiva en ecosistemas nativos. Presentamos un analisis retrospectivo de varios atributos estructurales, biologicos y biogeograficos de plantas lenosas introducidas a Norteamerica para determinar los rasgos caracteristicos de las especies que han invadido y de las que no han invadido. Los modelos predictivos derivados de analisis discriminatorio clasificaron correctamente al 86.2% e las especies en validacion cruzada, mientras que los modelos derivados de dendrogramas de clasificacion y de regresion clasificaron correctamente al 76%. A partir de estos modelos creamos un dendrograma predictivo jerarquico que permite al usuario dividir a las especies en tres categorias: admitir (bajo riesgo de invasividad), negar admision (alto riesgo de invasividad) o retrasar admision para analisis posterior y/o monitoreo intensivo (el riesgo no puede evaluarse adecuadamente solo con base en los atributos incluidos. Recomendamos que no se permita la entrada a E.U.A. de especies que son altamente invasivas en otras partes y que se aplique una politica de introduccion conservadora basada en un modelo predictivo jerarquico.
750 citations
"The reproductive biology of the inv..." refers background in this paper
...…reproductive age or size, high and continuous seed (spore) production, adaptations for short- and long-distance seed (spore) or vegetative dis- persal, and vegetative as well as sexual reproduction (Baker, 1974; Newsome and Noble, 1986; Roy, 1990; Reichard and Hamilton, 1997; Sakai et al., 2001)....
[...]
TL;DR: It is suggested that ecosystem alteration may be relatively common among invasive non-indigenous species and where ecosystem processes have been altered, site restoration likely will require both control of the invader(s) and recovery of processes.
Abstract: Individual plant species that modify ecosystem properties have traditionally been thought to be uncommon in natural systems. I hypothesize that many invasive non- indigenous species do alter these properties at several scales. The non-indigenous plant species in Florida considered the most invasive by the Florida Exotic Pest Plant Council are examined for this capability through review of the available literature. Out of 31 species total, 12-20 (39-64%) potentially alter the ecosystem properties of geomorphology, hy- drology, biogeochemistry, and disturbance. When population-level properties that indicate superior competitive ability of the invading species are examined, 13-24 (42-77%) of the species are included, with the majority of species showing traits capable of modifying natural systems at both ecosystem and community/population scales. This review suggests that ecosystem alteration may be relatively common among invasive non-indigenous spe- cies. However, much of the current information is anecdotal. Empirical studies directly examining the effects of species on ecosystem and smaller-scale processes are necessary, and highly invasive species may be particularly appropriate for such research. Further, as non-indigenous species homogenize the global flora, they may also homogenize the local flora by increasing the representation of ruderal species. Where ecosystem processes have been altered, site restoration likely will require both control of the invader(s) and recovery of processes.
623 citations
"The reproductive biology of the inv..." refers background in this paper
...The Everglades in southern Florida are considered among the top locations in the United States in the severity of nonindigenous plant invasion (Loope, 1992; Gordon, 1998)....
[...]