Alien dandelion reduces the seed-set of a native congener through frequency-dependent and one-sided effects

In conservation biology, increasing numbers of studies have focused on reproductive interference (RI) between a native species and related aliens. However, few studies have examined the frequency dependence of RI, despite of its key importance to invasiveness. Here, we report for the first time frequency-dependent RI in a pair of native and alien dandelions: Taraxacum japonicum and T. officinale, respectively. Taraxacum japonicum has been displaced rapidly by the alien congener T. officinale in Japan and its causal mechanism are still poorly understood. Field observations revealed that the seed-set of natives decreased substantially as the proportion of alien neighbors increased. Subsequently, in a field experiment, the removal of alien flowers only greatly increased the seed-set of natives. We synthesized these results with existing theoretical models of RI and concluded that RI, which is mediated by strong frequency dependence, is presumably responsible for the displacement of T. japonicum by T. officinale.     

Comparisons among populations and individuals to evaluate pollen–pistil interaction as a mechanism of reproductive interference in Taraxacum

Reproductive interference (RI), an interspecific mating interaction that reduces the fitness of at least one of the species involved, can lead to exclusive distributions in closely related species. A hypothesis previously proposed is that RI in plants may occur by ovule usurpation, in which pistils lack interspecific incompatibility and mistakenly accept heterospecific pollen, thereby losing an opportunity for conspecific pollen fertilization. However, few comparative studies have evaluated the consistency of the inferred mechanism within and among individuals and populations. We conducted hand-pollination experiments in six populations of three native Taraxacum species that suffered from different levels of RI from an alien congener, T. officinale, and compared pollen–pistil interactions among populations. We also investigated the interactions for eight individual T. japonicum plants whose response to heterospecific pollen deposition had been previously measured. Our results revealed that pollen tubes often penetrated native ovaries following heterospecific pollination in populations suffering from strong RI, whereas they seldom did in populations suffering from marginal RI. However, the relative frequency of the pollen tube penetration was not significantly related to the strength of alien RI. Not all pistils on an individual plant showed the same pollen receptivity following heterospecific pollination; rather, some accepted and some refused the pollen tubes. The relationship between pollen tube penetration following heterospecific pollination and the strength of the alien RI was also not significant among individuals. Our present results generally support the ovule usurpation hypothesis, but suggest that other factors, such as competition for pollinator services, variation in the effects of heterospecific pollen donors, and condition of the native inflorescences, might also affect the observed RI strength.

     

Effective range of reproductive interference exerted by an alien dandelion, <Emphasis Type="Italic">Taraxacum officinale</Emphasis>, on a native congener

Reproductive interference (RI), defined as the fitness cost of interspecific sexual interactions, such as interspecific pollen transfer (IPT) in plants, is ecologically important. Theoretically, RI could result in competitive exclusion, as it operates in a frequency-dependent manner. Additionally, IPT may have a greater range than resource competition, although information about the range of IPT is lacking. In the present study, we measured the range of IPT exerted by Taraxacum officinale (an alien species) on a native dandelion, T. japonicum. We used two approaches. In one, we analyzed the RI effect on a native seed set at three spatial scales. In the second, we tracked IPT from alien to native flower heads using fluorescent pigments as markers. We estimated that pollination distances were in the order of several meters. These distances exceeded the mean distance from each native plant to the nearest alien. As hypothesized, the effect of RI reached farther than neighboring individuals. These data indicate the spatial range from which alien dandelions should be removed to allow the conservation of natives.     

An invasive dandelion unilaterally reduces the reproduction of a native congener through competition for pollination

The impact of invasive alien species on native species is of increasing global concern. Invasive plants have various negative effects on natives through competition; however, relatively little is known about competition for pollination. The relationship between Japanese native dandelions (Taraxacum spp.) and invasive congeners may be a typical case of such an interaction. For example, native dandelions are being replaced by invasive congeners, especially in urban and suburban areas of Japan. To explain this phenomenon, we hypothesized that when natives are mixed with attractive invasives, natives may suffer from reduced seed set because invasives deprive natives of pollinators or because pollinators frequently move between species, resulting in interspecific pollen transfer. To test this hypothesis, we studied the effect of the invasive dandelion T. officinale on the pollination and seed set of the native T. japonicum using artificial arrays of monospecific and mixed-species plots as well as natural populations. Taraxacum officinale attracted more pollinator visits, perhaps because it produced more nectar than T. japonicum. The number of pollinator visits to T. japonicum was reduced when the congeners were grown together, and pollinators moved frequently between the two species. The proportion of seed set for T. japonicum was reduced in the presence of T. officinale in both artificial arrays and natural populations. These results support our hypothesis that interspecific competition for pollination plays an important role in the recent replacement of native dandelions by invasive congeners in Japan. Because invasive dandelions are apomicts, negative effects are incurred only by sexual natives. Thus, this system can be recognized as a rare case of interspecific interaction through pollination.     

Alien pollen grains interfere with the reproductive success of native congener

The effects of invasive species on native species comprise important conservation issues. Determining the mechanisms by which invasives exclude natives is indispensable to efficiently control their impact, but most invasives remain poorly studied. The purpose of this study was to elucidate potentially important but neglected mechanisms, reproductive interference, in wild Taraxacum systems, in which invasive Taraxacum officinale has displaced its native congener T. japonicum in Japan. Hand-pollination of mixed pollen grains significantly reduced the native seed-set compared to conspecific-only pollination. Moreover, natives with a high ratio of invasive pollen on their stigmas suffered severe seed-set reduction, and the proportion of invasive pollen on native stigmas increased as frequencies of the alien neighbor increased. These results, combined with those of previous studies, revealed that depositing invasive pollen on native stigmas contributes to the observed alien-frequency-dependent reduction of native seed-set, and strongly suggest that reproductive interference was the primary cause of displacement in the Taraxacum systems.     

Prezygotic barriers to gene flow between <Emphasis Type="Italic">Taraxacum ceratophorum</Emphasis> and the invasive <Emphasis Type="Italic">Taraxacum officinale</Emphasis> (Asteraceae)

Prezygotic reproductive barriers limit interspecific gene flow between congeners. Here, I examine the strength of floral isolation and interspecific pollen-pistil barriers between an invasive apomictic, Taraxacum officinale, and the indigenous sexual alpine dandelion, Taraxacum ceratophorum. Experimental arrays of either native inflorescences or a mixture of native and exotic inflorescences were used to examine insect preference and to track movement of a pollen analog. Using hand-pollinations, conspecific and heterospecific pollen germination success on native stigmas was compared. To additionally test for interspecific pollen competition, T. ceratophorum plants received one of three possible hand-pollinations: control conspecific pollination, concomitant conspecific and heterospecific pollination (mixed), or conspecific pollen followed by heterospecific pollen 15 min later (staggered). Floral isolation was negligible as no insect preference was detected. On a presence/absence basis, florets on native inflorescences received slightly less pollen analog from heterospecific donors than from conspecific donors; however, the amount of dye particles transferred from either Taraxacum species to stigmas on recipient T. ceratophorum inflorescences was equivalent. In contrast to weak floral isolation, strong pollen germination and pollen competition barriers should reduce the potential for hybridization. Heterospecific T. officinale pollen exhibited reduced germination success on T. ceratophorum stigmas in comparison to conspecific pollen. Furthermore, a significant pollen-competition effect on the percentage of hybrid offspring was detected only when T. officinale preceded T. ceratophorum pollen by 15 min. This result indicates that conspecific pollen out-competes heterospecific pollen but further suggests that biotic and abiotic factors reducing pollen accrual rates may partially remove barriers to natural hybridization.     

Formation of a hybrid triploid agamosperm on a sexual diploid plant: evidence from progeny tests in Taraxacum platycarpum Dahlst.

Agamospermous dandelions of hybrid origin between a native sexual diploid species (Taraxacum platycarpum Dahlst. or T. japonicum Koidz.) and an alien agamospermous triploid [T. officinale Weber and T. laevigatum (Willd.) DC.] are now widely distributed throughout mainland Japan. These hybrid dandelions are known to be genetically variable. We hypothesized that this variability is maintained by repeated ongoing hybridization, based on the fact that triploid dandelions not only produce seeds agamospermously, but also produce some functional pollen grains that are able to sire seeds of sexual dandelions. To test this hypothesis, we examined whether heads of Japanese diploid dandelions produce new hybrid seeds after fertilization by pollen from triploid agamosperms under field conditions. One of the 430 tested plants grown from sexual dandelion seeds had morphological and molecular characteristics, which are consistent with a hybrid origin. The plant formed a hybrid surrounded by many individuals having recurved involucral bracts, in which frequency of T. officinale was very low (3.5 %). Cytological data and bagging experiments demonstrate triploidy and asexual seed production of the hybrid. Taken together, these results supported that the new hybrid is probably derived from a backcross of a hybrid to the native sexual species. Our findings provide evidence for the evolution of a new agamosperm through interspecific hybridization as a contemporary population process.     

Relative abundance of an invasive alien plant affects native pollination processes

One major characteristic of invasive alien species is their occurrence at high abundances in their new habitat. Flowering invasive plant species that are visited by native insects and overlap with native plant species in their pollinators may facilitate or disrupt native flower visitation and fertilisation by forming large, dense populations with high numbers of flowers and copious rewards. We investigated the direction of such a proposed effect for the alien invasive Rhododendron ponticum in Irish habitats. Flower visitation, conspecific and alien pollen deposition, fruit and seed set were measured in a self-compatible native focal plant, Digitalis purpurea, and compared between field sites that contained different relative abundances of R. ponticum. Flower visitation was significantly lower at higher alien relative plant abundances than at lower abundances or in the absence of the alien. Native flowers experienced a significant decrease in conspecific pollen deposition with increasing alien abundance. Heterospecific pollen transfer was very low in all field sites but increased significantly with increasing relative R. ponticum abundance. However, lower flower visitation and lower conspecific pollen transfer did not alter reproductive success of D. purpurea. Our study shows that indirect interactions between alien and native plants for pollination can be modified by population characteristics (such as relative abundance) in a similar way as interactions among native plant species. In D. purpurea, only certain aspects of pollination and reproduction were affected by high alien abundances which is probably a result of high resilience due to a self-compatible breeding system. Native species that are more susceptible to pollen limitation are more likely to experience fitness disadvantages in habitats with high relative alien plant abundances.     

The potential for genetic assimilation of a native dandelion species, Taraxacum ceratophorum (Asteraceae), by the exotic congener T. officinale

Exotic plant species can threaten closely related native congeners through asymmetric hybridization and subsequent backcrossing, the process known as genetic assimilation. I explore the initial stages of this process in Taraxacum ceratophorum (Asteraceae), the native alpine dandelion, and the invasive apomict T. officinale. In central Colorado, seven T. ceratophorum populations all occur in sympatry with T. officinale. In one large population on Pennsylvania Mountain, surveys further revealed that flowering phenologies and visiting insect taxa overlap almost completely for both Taraxacum species. Together these results indicated that heterospecific pollen transfer is likely. Crossing experiments showed that T. ceratophorum is an obligate outcrosser, and interspecific hand pollinations resulted in 37.3% seed set. However, molecular analysis of the F1 offspring indicated that only 33.2% of germinating seeds were hybrids; the remainder were selfed offspring produced from a breakdown in self-incompatibility (the mentor effect). Although the mentor effect helps reduce the production of hybrids, the asymmetrical direction of hybridization creates the potential for genetic assimilation of T. ceratophorum by T. officinale.     

Invasive Eupatorium adenophorum suffers lower enemy impact on carbon assimilation than native congeners

Enemy release hypothesis predicts that alien plants that escape from their natural enemies suffer lower enemy regulation in their introduced ranges than in native ranges. An extension of this theory suggests that if enemy release plays a crucial role in invasive success, then in the introduced range, invasive plants should also suffer lower local enemy impact than native residents (local enemy release hypothesis, LERH). In order to test LERH, we compared invasive Eupatorium adenophorum with two native congeners (E. heterophyllum and E. japonicum) in terms of damage by leaf enemies at two natural field sites and two manipulated sites. We also determined enemy impact on carbon assimilation at two manipulated sites. In each site, E. adenophorum was only damaged by herbivores, while in native congeners, leaf scabs or (and) leaf rolls was found in addition to herbivory damage. In both manipulated sites, the total enemy impact on carbon assimilation was lower for E. adenophorum than for native congeners; this observation was consistent with LERH. The results of this study indicate that a short co-existence time with generalist enemies (behavior constraint) might be the main contributor to the lower enemy impact on E. adenophorum.     

Pollen quality limitation in the Iberian critically endangered genus <Emphasis Type="Italic">Pseudomisopates</Emphasis> (Antirrhinaceae)

Pollen limitation occurs when sexual reproduction is decreased due to inadequate pollen receipt. Limitation is usually associated with the quality and the quantity of pollen; still, most studies do not discriminate between the two. We used hand-pollination experiments and observations of floral visitors to determine the mating system and limitations to seed production of the Spanish endangered species Pseudomisopates rivas-martinezii. We tested for agamospermy, autogamy, obligated autogamy, cross-pollination and supplementation. The response variables considered were fruit set, seed set and viable seed set. Previous studies indicated that (i) the species exhibits extensive clonal growth, (ii) plants flower profusely in summer, (iii) seeds showed to be highly unviable, and (iv) no seedlings were observed in the field. We found that P. rivas-martinezii is predominantly self-incompatible, has an unexpected generalized pollination system considering its occluded corolla, and is limited by qualitative rather than quantitative pollen limitation. These results indicate that, in addition to other presumed environmental factors, the low seed viability of this self-incompatible species is due to pollen quality limitation as a result of reduced mate availability.     

Phenotypic plasticity of invasive Alternanthera philoxeroides in relation to different water availability, compared to its native congener

Phenotypic plasticity and genetic differentiation are two possible mechanisms that plants use to cope with varying environments. Although alligator weed (Alternanthera philoxeroides) possesses very low genetic diversity, this alien weed has successfully invaded diverse habitats with considerably varying water availability (from swamps to dry lands) in China. In contrast, its native congener (Alternanthera sessilis) has a much narrower ecological breadth, and is usually found in moist habitats. To understand the mechanisms underlying the contrasting pattern, we performed a greenhouse experiment to compare the reaction norms of alligator weed with those of its native congener, in which water availability was manipulated. Our results revealed that the two congeners had similar direction of phenotypic plasticity. However, A. philoxeroides showed greater plasticity in amount than did A. sessilis in many traits examined during the switch from wet to drought treatment. Nearly all of the phenotypic variance in A. philoxeroides could be ascribed to plasticity, while A. sessilis had a much higher fraction of phenotypic variance that could be explained by genotypic variation. These interspecific differences in plastic responses to variable water availability partially explained the difference in spatial distribution of the two congeners.     

Variation of pollen limitation in the early flowering Mediterranean geophyte Narcissus assoanus (Amaryllidaceae)

A recent literature review indicates that pollen limitation of female fertility is a common feature of flowering plants. Despite the ecological and evolutionary significance of pollen limitation, most studies have only examined fertility in a single population at one time. Here we investigate pollen limitation of fruit and seed set in five populations of Narcissus assoanus, a self- sterile, insect-pollinated geophyte, over 2–3 years in southern France. In common with many early spring flowering plants, pollinator visitation to N. assoanus is often infrequent. Supplemental hand-pollination of flowers with outcross pollen significantly increased overall fruit and seed set by 11% and 19%, respectively. Four of the five populations experienced some pollen limitation during the study. For a given year, there was significant variation in pollen limitation among populations. Two of the populations were pollen limited in one year but not in other years in which they were studied. Seed:ovule ratios for open- and hand-pollinated flowers averaged 0.29 and 0.33, respectively. While hand pollination significantly increased the seed:ovule ratio, the low value obtained indicates that the majority of ovules in flowers do not mature seeds despite hand pollination. The role of genetic and environmental factors governing low seed:ovule ratios in N. assoanus is discussed. Received: 28 December 1999 / Accepted: 6 April 2000     

Reproductive interference and salinity tolerance differentiate habitat use between two alien cockleburs: <Emphasis Type="Italic">Xanthium occidentale</Emphasis> and <Emphasis Type="Italic">X. italicum</Emphasis> (Compositae)

In recent years, reproductive interference (RI), the fitness cost of reproductive activities among species, has received much attention as a factor in competitive exclusion by alien species. In this study, we aimed to explain the distribution of two annual alien Xanthium species (X. occidentale and X. italicum) found in the northern Kinki Distinct of Japan from the viewpoint of RI. First, specimen records demonstrated that Xanthium occidentale was more dominant in all habitats except seaside habitats. Subsequently, using artificial patches of potted plants, we demonstrated that X. italicum suffered intense RI from X. occidentale. Finally, X. italicum was superior to X. occidentale in tolerating salinity stress. Combining these results, we concluded that the asymmetrical RI caused by X. occidentale displaced X. italicum except in seaside habitats, where X. occidentale could not establish colonies. Furthermore, we discuss the possibility that a similar RI effect caused the extinction of native species.     

Germination characteristics of native Japanese dandelion autopolyploids and their putative diploid parent species

Germination characteristics of native Japanese Taraxacum lineages of Taraxacum platycarpum (diploid), T. venustum (triploid and tetraploid), and T. albidum (pentaploid) have been studied at different temperatures. Taraxacum platycarpum ssp. hondoense is the putative diploid parent of T. venustum. Diploid T. platycarpum ssp. hondoense and the polyploids T. venustum and T. albidum are found in different areas of Japan, and distribution differences may reflect divergent ecological and physiological traits among ploidy levels. In this study, to prevent mixing of seeds of different polyploidy we used flow cytometry to examine the ploidy level of the plants from which seeds were collected. Results from seed-germination experiments showed that dependence on temperature of final percentage germination was qualitatively similar for both autopolyploids T. venustum and diploids T. platycarpum—germination was suppressed at high and low temperatures. It was also shown that seed germination of autopolyploids was suppressed more than that of the ancestral diploid at low temperatures and that seed germination for polyploids was higher than for the diploid. Threshold variations at low temperatures might affect the distribution of native dandelions. Taraxacum venustum, which occurs in cool climates, might have developed a distinctly lower germination threshold at low temperatures whereas T. albidum, which is native to warm climates, might have developed an adaptive threshold at high temperatures.     

Isolation affects reproductive success in low-density but not high-density populations of two wind-pollinated <Emphasis Type="Italic">Thalictrum</Emphasis> species

Since pollen usually travels limited distances in wind-pollinated plant species, plants growing at low density may become pollen limited. We examined how local pollen availability and population density affect reproductive success in two wind-pollinated, dioecious species, Thalictrum fendleri and Thalictrum dioicum. Distance to the nearest flowering male, the number of flowering males within 2 m, and flower number on those males served as measures of local pollen availability. Increased distance from pollen donors reduced seed set in the lowest-density population of each species, but seed set in high-density populations was not correlated with local pollen availability. For plants in high- and low-density populations at similar distances from pollen donors, this distance only affected seed set in low-density populations. To ensure that differences in resource availability were not causing spurious correlations between seed set and plant density, we constructed low-density artificial arrays in populations of T. dioicum. In these, seed set decreased rapidly with increases in distance from pollen donors. Despite these effects, the density of males in a population was not correlated with average seed set in T. dioicum, and hand pollination in the T. dioicum populations also failed to increase seed set over natural levels. These results suggest that pollen receipt only limits seed set on isolated plants within low- density populations of T. dioicum and T. fendleri.     

A defective pollen-pistil interaction contributes to hamper seed set in the<Emphasis Type="Italic"> parthenocarpic fruit</Emphasis> tomato mutant

In the parthenocarpic fruit (pat) tomato mutant, parthenocarpy is associated with partial aberrations of stamens (shortness and carpelloidy) and ovules (defective integument growth) that contribute to impair seed set. However, these do not seem to be the only reasons for seed infertility because hand-pollination fails to restore seed set in ovaries where a fraction of the ovules are still morphologically normal. Therefore, it is conceivable that other unreported defects occur during the reproductive process in the mutant. In this research, we show that the mutation does not affect pollen or embryo sac development and viability, but generates sporophytic effects that reduce seed production and seed size. While pollen germination and stylar growth were normal in mutant pistils, fertilization does not take place because of abnormalities in the pollen tube-ovary interaction in this genotype. Inside the ovary of pat plants, pollen tubes appeared to be disorientated; they wandered about in the ovarian cavity and often lost their adherence to the placental surface. Interestingly, in pat ovaries fertilization was strongly impaired even in those ovules that appeared normal. It may be that apparently 'normal' ovules cannot guide pollen tubes to their micropyle in the altered pat ovary because adhesion molecules are not properly arrayed on a placenta that is already preparing for cell division or, alternatively, chemotropic signals in the pat ovary may be altered by the presence of aberrant ovules, which are not simply devoid of attractivity, but disrupt pollen tube guidance overall.     

Allocation to reproduction following experimental defoliation in Platanthera bifolia (Orchidaceae)

The roles of herbivory and pollination success in plant reproduction have frequently been examined, but interactions between these two factors have gained much less attention. In three field experiments, we examined whether artificial defoliation affects allocation to attractiveness to pollinators, pollen production, female reproductive success and subsequent growth in Platanthera bifolia L. (Rich.). We also recorded the effects of inflorescence size on these variables. We studied the effects of defoliation on reproductive success of individual flowers in three sections of inflorescence. Defoliation and inflorescence size did not have any negative effects on the proportion of opened flowers, spur length, nectar production or the weight of pollinia. However, we found that hand-pollination increased relative seed production and defoliation decreased seed set in most cases. Interactions between hand-pollination and defoliation were non-significant indicating that defoliation did not affect female reproductive success indirectly via decreased pollinator attraction. Plants with a large inflorescence produced relatively more seeds than plants with a small inflorescence only after hand-pollination. The negative effect of defoliation on relative capsule production was most clearly seen in the upper sections of the inflorescence. In addition to within season effects of leaf removal, defoliated P. bifolia plants may also have decreased lifetime fitness as a result of lower seed set within a season and because of a lower number of reproductive events due to decreased plant size (leaf area) following defoliation. Our study thus shows that defoliation by herbivores may crucially affect reproductive success of P. bifolia.     

Innate and evolutionarily increased advantages of invasive <Emphasis Type="Italic">Eupatorium adenophorum</Emphasis> over native <Emphasis Type="Italic">E. japonicum</Emphasis> under ambient and doubled atmospheric CO<Subscript>2</Subscript> concentrations

Both innate and evolutionarily increased ecophysiological advantages can contribute to vigorous growth, and eventually to invasiveness of alien plants. Little effort has been made to explore the roles of innate factors of alien plants in invasiveness and the effects of CO₂ enrichment on alien plant invasions. To address these problems, we compared invasive Eupatorium adenophorum, its native conspecific, and a native congener (E. japonicum) under ambient and doubled atmospheric CO₂ concentrations. Native E. adenophorum from Mexico grew slower than invasive E. adenophorum but faster than native E. japonicum under both CO₂ concentrations. The faster growth rate of invasive E. adenophorum was associated with higher photosynthetic capacity and leaf area ratio. For invasive E. adenophorum, the higher photosynthetic capacity was associated with higher nitrogen (N) allocation to photosynthesis, which was related to lower leaf mass per area; the higher leaf area ratio was due to lower leaf mass per area and higher leaf mass fraction. Tradeoff between N allocations to photosynthesis versus defenses was found. CO₂ enrichment significantly increased relative growth rate and biomass accumulation by increasing actual photosynthetic rate for all studied materials. However, the relative increase in growth was not significantly different among them. CO₂ enrichment did not influence N allocation to photosynthesis, but increased N allocation to cell walls. The reduced leaf N content decreased N content in photosynthesis, explaining the down-regulation of photosynthetic capacity under prolonged elevated CO₂ concentration. Our results indicate that both innate and evolutionary advantages in growth and related ecophysiological traits contribute to invasiveness of invasive E. adenophorum, and CO₂ enrichment may not aggravate E. adenophroum’s invasion in the future.     

Variation in the strength of reproductive interference from an alien congener to a native species in Taraxacum

Journal of Plant Research - Reproductive interference (RI) may be a contributing factor to the displacement of native species by an alien congener, and RI strength has been shown theoretically to...