Amphicarpic Species Research Articles

Demographic study of a peripheral population of the rare amphicarpic species Scrophularia arguta

Scrophularia arguta (Scrophulariaceae) is a rare amphicarpic annual species with a fragmented distribution in North Africa, part of the Arabian Peninsula, and Macaronesia, with several peripheral populations on the Iberian Peninsula (south-western Europe) as well. The Iberian populations have a disjunct distribution: several endangered or critically endangered populations are present in the southeast versus a few non-listed ones representing a relict lineage with a unique plastid haplotype inhabiting the west-central region (Extremadura). In this study, we examined the largest and most important population of this relict lineage to assess potential threats to its survival. We evaluated pollination and reproductive systems, floral rewards, fruit and seed set from chasmogamous and cleistogamous flowers, and population dynamics (i.e., phenology, survival, reproductive success, and predation level). We found that the main threats to the population are predation by wild herbivores, such as red deer and, to a lesser extent, Cucullia scrophulariae caterpillars. These threats decrease reproductive success to such an extent that population survival may be in jeopardy if no action is taken to reduce the effects of herbivores. In addition, the existence of nearby beehives alters the presence and density of wild pollinators that contribute to gene flow via pollen transfer and increase genetic variability. Cleistogamous seeds may help maintain the population in specific microhabitats (mainly quartzite rock cracks), although at the cost of reducing genetic variability. Finally, we recommend that regional/national administrations responsible for biodiversity matters adopt measures to ensure the conservation and survival of west-central populations. Scrophularia arguta predation by vertebrates. Left, group of several individuals before and after vertebrate predation. Right, vertebrate predation level. • Wild vertebrates and caterpillars threaten a relict Scrophularia arguta population. • Managed honeybees displace natural pollinators. • The conflict between plant and animal conservation requires monitoring. • The action of regional/national administrations is needed to conserve this species.

Understanding how an amphicarpic species with a mixed mating system responds to fire: a population genetic approach.

Amphicarpic plants produce both above-ground and below-ground seeds. Because below-ground seeds are protected in the soil and may maintain viability when above-ground conditions are stressful, they were proposed as an adaptation to recolonize a site after disturbance. However, whether below-ground seeds are the main colonizers after a disturbance remains unknown. Our goal was to understand whether recolonization by an amphicarpic species after fire was accomplished primarily through germination of seeds produced above-ground or below-ground. We investigated Polygala lewtonii, an amphicarpic, perennial species endemic to fire-prone Florida sandhill and scrub, where fire kills plants but subsequently increases recruitment and population sizes. Polygala lewtonii produces three flower types: above-ground chasmogamous flowers and above-ground and below-ground cleistogamous flowers, with previous research demonstrating chasmogamous flowers produce a much greater proportion of seeds than cleistogamous flowers. We quantified outcrossing in seeds produced by chasmogamous flowers to determine whether it differed from the 100 % self-fertilized below-ground seeds. Approximately 25 % of seeds from chasmogamous flowers showed evidence of cross-pollination. Assuming that chasmogamous flowers produce the majority of the above-ground seeds, as was shown previously, this indicates it is possible to differentiate between germination by above-ground versus below-ground seeds in post-fire colonization. We next compared genetic diversity, admixture, inbreeding and population genetic structure pre- and post-fire. If fire promoted germination of chasmogamous seeds, heterozygosity and admixture would increase, and genetic structure and inbreeding would decrease. Instead, inbreeding and genetic structure increased and admixture decreased, suggesting that the below-ground selfed seeds (with limited dispersal ability) increased their contribution to the population after fire, possibly because fire reduced above-ground seed viability. Additionally, new alleles not found previously in range-wide analyses emerged from the seed bank post-fire. These results suggest that amphicarpy is a powerful adaptation to preserve genetic variation, maintain adaptive potential and promote rapid post-fire colonization.

Amphicarpic plants: definition, ecology, geographic distribution, systematics, life history, evolution and use in agriculture.

ABSTRACTAlthough most plants produce all of their fruits (seeds) aboveground, amphicarpic species produce fruits (seeds) both above‐ and belowground. Our primary aims were to determine the number of reported amphicarpic species and their taxonomic, geographic, life form and phylogenetic distribution, to evaluate differences in the life history of plants derived from aerial and subterranean seeds, to discuss the ecological and evolutionary significance of amphicarpy, to explore the use of amphicarpic plants in agriculture, and to suggest future research directions for studies on amphicarpy. Amphicarpy occurs in at least 67 herbaceous species (31 in Fabaceae) in 39 genera and 13 families of angiosperms distributed in various geographical regions of the world and in various habitats. Seeds from aerial and subterranean fruits differ in size/mass, degree of dormancy, dispersal and ability to form a persistent seed bank, with aerial seeds generally being smaller, more dormant and more likely to be dispersed and to form a seed bank than subterranean seeds. In addition, plants produced by aerial and subterranean seeds may differ in survival and growth, competitive ability and biomass allocation to reproduction. Amphicarpic plants may exhibit a high degree of plasticity during reproduction. Subterranean fruits are usually formed earlier than aerial ones, and plants may produce only subterranean propagules under stressful environmental conditions. Differences in the life histories of plants from aerial and subterranean seeds may be an adaptive bet‐hedging strategy.

Genetic diversity assessed by microsatellite markers in the amphicarpic species Trifolium polymorphum Poir.

Trifolium polymorphum Poir. is an amphicarpic forage legume from southern Brazil, Uruguay, Argentina, Paraguay and Chile. Information on the genetic diversity of natural populations in natural grasslands in southern Brazil is limited. In order to increase the knowledge about this species, an analysis of the genetic diversity was carried out in 10 natural populations of T. polymorphum with the use of 20 microsatellite markers. The expected heterozygosity in T. polymorphum populations ranged from 0.40 to 0.43, with a mean of 0.42. A total of 193 alleles were detected with a mean of 9.3 alleles per locus and polymorphic information content (PIC) for these markers of 0.62 to 0.89 with a mean of 0.84.The grouping based on the Jaccard's coefficient of similarity classified populations, regardless of their regions of origin, into two groups with a mean similarity coefficient of 0.32, reflecting the high genetic variability of the populations, especially those located in the Campanha phytogeographic region. This information on diversity can be used to plan future germplasm collection strategies for conservation purposes and also for the breeding of the species.

Effect of seed morph and light level on growth and reproduction of the amphicarpic plant Amphicarpaea edgeworthii (Fabaceae)

Amphicarpic plants produce aerial and subterranean fruits on an individual plant, and these heteromorphic diaspores give rise to plants that differ in growth and ecology. Amphicarpaea edgeworthii is a summer annual amphicarpic species that grows over a range of light levels. We aimed to compare the response to shading intensity of plants of A. edgeworthii grown throughout their life cycle from aerial seeds (ASP) and from subterranean seeds (SSP). We hypothesized that vegetative and reproductive growth of plants from ASP and SSP respond differently to light. Plants were grown from ASP and SSP under 0, 46, 71 and 90% shading intensities. With plant height as a covariate, vegetative biomass of ASP and SSP did not differ. Leaf area and seed production of SSP were greater and internode length less than they were for ASP in all shading intensities. Aerial and subterranean seed yield, seed mass and number for both ASP and SSP were highest in full light. Aerial seed yield was affected more than subterranean seed yield by shading intensity. The growth and reproductive responses of ASP and SSP of A. edgeworthii may be adaptive to the range of low to high light environments in which this species grows.

Lack of divergence in seed ecology of two Amphicarpaea (Fabaceae) species disjunct between eastern Asia and eastern North America.

Many congeneric species are disjunct between eastern Asia and eastern North America. No previous study has compared the seed biology of closely related disjunct taxa of legumes or of a diaspore-heteromorphic species. Our objective was to compare seed dormancy in two such sister species in the genus Amphicarpaea (Fabaceae). We investigated the ecology and ecophysiology of aerial and subterranean seeds of the amphicarpic species Amphicarpaea edgeworthii from China and compared the results to those published for its sister species A. bracteata from eastern North America. The seed coat of aerial seeds of A. edgeworthii is well developed, whereas the seed coat of subterranean seeds is not. Aerial seeds have combinational dormancy (physical dormancy [PY] + physiological dormancy [PD]) broken by scarification followed by cold stratification or by after-ripening and scarification; whereas subterranean seeds have PD broken by cold stratification. Aerial seeds formed a persistent soil seed bank, and subterranean seeds a transient soil seed bank. Aerial seeds of A. bracteata also have PY+PD and subterranean seeds PD. Subterranean seeds of both species are desiccation intolerant. Dormancy in neither aerial nor subterranean seeds of both species has diverged over geological time. Compared to subterranean seeds, aerial seeds of both species dispersed over longer distances. Seed dispersal ability and degree of dormancy of neither species fits the high-risk/low-risk (H-H/L-L) strategy found in many diaspore-dimorphic species. Rather, both species have an H-L/L-H strategy for these two life history traits.

Amphicarpy in Trifolium argentinense: morphological characterisation, seed production, reproductive behaviour and life strategy

Trifolium argentinense Speg. is an amphicarpic species that occurs naturally in native pastures of Rio Grande do Sul, southern Brazil. Amphicarpy is a rare mode of reproduction in which aerial and subterranean seeds are produced by the same individual. In the present paper, we compare morphology, anther number, pollen viability, seed production and mode of reproduction of T. argentinense flowers, and comment on the life strategy of the species. Plants grown from aerial seeds and from the regrowth of storage roots of aerial plants had longer stolons and a larger plant diameter than did those grown from subterranean plants. Plants grown from seeds were also taller than plants grown from storage roots. More resources were allocated to subterranean reproduction in plants of subterranean origin than in those of aerial origin. Aerial flowers produced more seeds, presented more anthers and produced more pollen grains than did the subterranean ones. T. argentinense is a versatile species, self- and cross-pollinated, consistent with the values of high polymorphism information content. T. argentinense adopts the ‘pessimistic strategy’ (early allocation of energy to large subterranean propagules), common in amphicarpic species when growing in disturbed habitats, such as the native pastures of Rio Grande do Sul, where intense grazing and trampling, as well as long seasonal dry spells, may periodically destroy the aerial plants, thus assuring survival by germination of subterranean seeds and regrowth of storage roots.

Comparative studies on reproductive structures in four amphicarpic tropical Phaseoleae legumes

Amphicarpy, an adaptive trait whereby both aerial and underground fruits are formed on the one plant, occurs in several plant taxa, notably the Phaseoleae legumes. Amphicarpic species offer the dual potential benefits of enhanced persistence through their underground seed, combined with ease of harvest of their aerial seed. While amphicarpy has been reported in several endemic Australian tropical legumes, information on the trait is sparse. The objective of the current research was to compare aerial and underground reproductive structures in amphicarpic tropical legumes from four different sub-tribes within the Phaseoleae: three Australian endemic species, Vigna lanceolata (sub-tribe Phaseolinae), Flemingia pauciflora (sub-tribe Cajaninae), and Glycine falcata (sub-tribe Glycininae); and the exotic pasture legume Centrosema rotundifolium (sub-tribe Clitoriinae). As far as we know, this report of amphicarpy in F. pauciflora is the first record of the trait in a member of the Cajaninae. Descriptions, drawings, and photographs of the morphology and anatomy of the aerial and underground fruiting structures were documented. In general, the aerial flowers in all genotypes studied were chasmogamous, allowing at least some opportunity for outcrossing. In contrast, the underground flowers were invariably much reduced, with a small, non-pigmented corolla enclosed in much-reduced, scale-like sepals. Nonetheless, anthers and viable pollen were observed in the underground flowers in all four species. With the exception of C. rotundifolium, the underground fruiting structures formed on rhizomes which initially arose either from the underground cotyledonary nodes or, in the case of G. falcata, which is epigeal, from the junction of the stem and taproot. The rhizomes gave rise to ramets when they emerged at the surface or from holes in pot bases. The V. lanceolata accessions also produced fleshy tubers which gave rise to rhizomes, especially in subsequent years. In C. rotundifolium, the geocarpic structures arose on specialised, fleshy, geotropic stems that grew down from the stoloniferous stems. In all species, the number of seeds per underground pod was fewer than in the aerial pods, and the underground seeds were invariably larger, although the extent differed between legume genotypes. There was no evidence of effects on growth or development depending on whether plants were grown from aerial or underground seeds. Some of the adaptive and agronomic implications of the key findings are discussed. In particular, it is argued that amphicarpy in the Australian species is an adaptation to seed predation, and to spatially heterogeneous inland soils.

Seed dimorphism, chromosome number and karyotype of the amphicarpic species Trifolium argentinense Speg.

Amphicarpy, a specialized form of dimorphism where fruits and seeds are formed in underground and aerial flowers, has been reported in only ca. 50 flowering plants. Trifolium argentinense Speg. is an amphicarpic legume species that occurs in native pastures of Southern Brazil. Data on seed dimorphism, chromosome number and karyotype of the species are presented for the first time. T. argentinense is diploid, with 2n = 2x = 16. Chromosome size range from ca. 2.8 to 1.6 μm, the karyotypic formula is 3 metacentric + 1 satellite-bearing metacentric + 3 acrocentric + 1 subacrocentric and a TCL (total complement length) of 18.10 μm. All the subterranean, but around 70% of the aerial legumes formed seeds. Subterranean seeds were larger and heavier (2.1 mm and 0.0029 g, respectively) than the aerial ones (1.8 mm and 0.0016 g, respectively). As a follow up to this work, we plan to characterize aerial and subterranean-seed-derived plants regarding aspects such as growing rate, height, leaf size and forage production, as well as to determine the exact mode of reproduction of T. argentinense by pollination experiments and the use of molecular markers.

Intrafloral phenology of Trifolium polymorphum Poir. (Leguminosae) aerial flowers and reproductive implications

Trifolium polymorphum is an amphicarpic species that grows in Uruguay, Argentina, Brazil, Paraguay and Chile. Underground flowers are cleistogamous, obligately autogamous and morphologically highly modified in structure and function. Aerial flowers are chasmogamous, and as mentioned in earlier literature, either allogamous or autogamous. The aim of this study is to identify flower characteristics that facilitate or prevent autogamous or allogamous processes. Floral phenology stages are thus studied in correlation with estimated models of aerial flower development, pollen viability and stigmatic receptivity in three Uruguayan T. polymorphum populations. Flower longevity and development (length, width, and anther-stigma distance), anthesis and anther dehiscence initiation, pollen viability and stigmatic receptivity are the variables correlated with floral phenology. Morphological characteristics of aerial flowers favor autogamy processes - even in pre-anthesis - but phenological characteristics tend to prevent it. The most important reproductive events occurring during flower development, that facilitate autogamous or allogamous processes, are discussed here.

Development of microsatellite markers in an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae)

AbstractEight polymorphic simple sequence repeats (SSRs) markers were developed for Amphicarpaea edgeworthii Benth., an amphicarpic species in East Asia. The low level of heterozygosity in populations and the high level of population differentiation found in this study suggest that A. edgeworthii has a mixed mating system that is predominantly selfing. The findings also indicate that the new markers can be used in genetic analyses of the mating system and the estimation of the construction of progeny populations contributed by chasmogamously and cleistogamously produced seeds.

Comparative Study on the Aerial and Subterranean Flower Development in Amphicarpaea edgeworthii Benth. (Leguminosae: Papilionoideae), an Amphicarpic Species

Amphicarpy is a rare phenomenon in angiosperms. There are few studies on the floral development of aerial and especially subterranean flowers of the amphicarpic species. In this study, we examine the floral ontogeny of Amphicarpaea edgeworthii, an amphicarpic legume, using SEM. Three types of flowers can be produced in the same individual of the species: the subterranean flowers, solitary without subtending leaves; the aerial cleistogamous flowers, generally solitary in leaf axils; and the aerial chasmogamous flowers, one or two subtended by a bract. There is little difference in terms of the organ initiation among the three flower morphs. The order of initiation among whorls is sepals, petals, carpel, outer‐whorl stamens, and inner‐whorl stamens. Within each whorl, no obvious unidirectional order is found among the floral organ components. The development of petals, two‐whorl stamens, and a carpel in the aerial and subterranean flowers diverges at the mid‐ to late‐development stage. The mature aerial cha...

Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers

Amphicarpaea edgeworthii Benth. is an amphicarpic legume widespread in China. Amphicarpy describes the phenomenon that a plant produces aerial as well as subterranean fruits. A. edgeworthii can reproduce via three kinds of flowers: aerial chasmogamous flowers, aerial cleistogamous flowers, and subterranean cleistogamous flowers. Although there are some studies on the population genetic structure of species with both chasmogamous and cleistogamous flowers, none has been done for that of an amphicarpic species so far. The present study uses random amplified polymorphic DNA (RAPD) to assess level and pattern of genetic variation in 15 natural populations of A. edgeworthii. A total of 131 stable and clearly scored RAPD bands were achieved from 13 primers. The average genetic diversity within populations estimated by Shannon's information index was 0.218 at the population level, but ranged from 0.119 to 0.302, which was significantly different ( P < 0.01). Different statistical analyses revealed a high level of genetic differentiation among populations ( G ST = 0.473–0.527). Thus, the pattern of genetic structure of A. edgeworthii is consistent with that of an inbreeding species.

Seed yield and hardseededness of two amphicarpic pasture legumes (Vicia sativa ssp. amphicarpa and Lathyrus ciliolatus) and two annual medics (Medicago rigidula and M. noeana)

SUMMARYYields and hardseed breakdown of underground and aerial seeds in subterranean vetch (Vicia sativa ssp. amphicarpa) and lathyrus (Lathyrus ciliolatus) and aerial seeds of Medicago rigidula and M. noeana were compared at Tel Hadya, near Aleppo, in north Syria between 1990 and 1992. Underground and aerial seed and straw (mature herbage) yields were measured at maturity in the first spring, and hardseed breakdown over the following summer, autumn and winter. Regenerating herbage production was measured in the second spring.In the establishment year (292 mm rainfall) the medics produced twice as much straw as the amphicarpic species. In contrast, seed yields were less than half: M. rigidula and M. noeana produced 412 and 110 kg/ha respectively, while subterranean vetch and lathyrus produced 1174 and 736 kg/ha. More than 95 % of the total seed yield of the amphicarpic legumes was underground. Underground seeds of the amphicarpic legumes were larger than aerial seeds, and almost 10 times as large as the medic seeds.Seeds of all species were &gt; 90% hard when newly set in summer. At the first seasonal rains &gt; 95% of underground seed had softened, compared with 5 and 40% of the aerial seeds of vetch and lathyrus respectively. The medics remained &gt; 90% hardseeded. In laboratory tests, embryo dormancy was observed in all species prior to the onset of first seasonal rains. For the amphicarpic legumes, but not for the medics, embryo dormancy persisted into winter. In the field, and after all germination events, 900–1430 seeds/m2 of subterranean vetch seed remained in the soil. This was considerably more than expected, based on the low levels of hardseededness and embryo dormancy observed in the laboratory. The results suggest that dormant seeds of the amphicarpic legumes need light to germinate.In the second year (353 mm rainfall), regenerating M. rigidula produced 5·3 t/ha compared with 3·4 t/ha by the best subterranean vetch from approximately equal numbers of seedlings. The amphicarpic legumes germinated later and over a more extended period than the medics, indicating that they could become weeds in a cereal/pasture rotation. However, the results suggest that in drier areas or in drier years the vetches will compare favourably with the medics in most respects. Clearly, subterranean vetch and lathyrus have great potential for pasture improvement in dry areas.

Amphicarpy in the Cyperaceae, With Novel Variation in the Wetland Sedge Eleocharis caespitosissima Baker

Amphicarpy, the heterocarpic production of serial and basal fruits, occurs in the Cyperaceae in species of the primarily mesophytic genera Bulbostylis and Trianoptiles and in species of the helophytic genera Eleocharis and Schoenoplectus. There is a variety of breeding systems and growth forms across these amphicarpic species. Eleocharis caespitosissima is amphicarpic, with basal fruits buried by positively geotropic culms. The seeds of basal fruits in this species may arise asexually. The selective pressures likely to be important in the development of amphicarpy in the Cyperaceae are discussed.

REPRODUCTIVE BEHAVIOR OF AMPHICARPAEA BRACTEATA (LEGUMINOSAE), AN AMPHICARPIC ANNUAL

Amphicarpaea bracteata, an annual legume common in woodland communities in the eastern United States, produces three distinct types of flower: subterranean cleistogamous (SCL), aerial cleistogamous (ACL), and aerial chasmogamous (ACH). We sought to quantitatively describe the growth and reproduction of four diverse A. bracteata populations in an effort to explain the adaptive significance of this species’ variable reproductive modes. Virtually all plants develop 1 to 3 SCL seeds on subterranean cotyledonary shoots, starting in late July. Larger plants produce additional SCL seeds later from the tips of axillary shoots which bury. Seeds produced by SCL flowers are large (39 to 134 mg), have restricted dispersal, lack dormancy, have high germination , and produce relatively vigorous seedlings. ACL flowers develop from early August through plant senescence in early October, while ACH flowers appear in a pulse in late August. The number of each aerial flower type was positively correlated with plant size. The ACL flowers take significantly less time to develop mature fruits than do ACH flowers. Both aerial seeds are smaller than the subterranean (mean weights: ACL 12.1, ACH 8.7 mg), have lower germination (ACL 20.2%, ACH 15.3%), appear relatively resistant to environmental extremes, and have the potential for more widespread dispersal. Plants derived from subterranean seeds are much larger than plants derived from aerial seeds, which makes them more likely to produce axillary SCL and aerial seeds. Only larger plants derived from subterranean seeds and growing in favored sites produce ACH flowers. This imposes an alternation of selfing with outcrossing generations. This pattern of reproductive behavior in A. bracteata is similar to that found in several other amphicarpic species.