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Reproductive biology, ecological life history/demography and genetic diversity of the megagenus Astragalus (Fabaceae, Papilionoideae)

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Abstract

Astragalus is the largest genus of seed plants; however, information on its reproductive biology and life history is widely scattered in the literature. About 96% of the species are perennials and 4% annuals; many are rare endemics. Astragalus species are obligate or facultative outcrossers, and inbreeding depression is higher in self-compatible (SC) than in self-incompatible (SI) species. The most frequent pollinators are Bombus, Osmia and Anthophora. On average, 48% of ovules produce seeds, and 40% of flowers produce fruits. Seed/ovule and fruit/flower ratios are lower in SC than in SI species. Predispersal insect seed predation ranges from 0 to 93%, and major predators are Acanthoscelides, Bruchophagus and Tychius. Seeds have physical dormancy and typically form a seed bank. C3 is the only photosynthetic pathway in the genus. Population growth may be cyclic or noncyclic, and genetic diversity of a taxon may or may not be related to size of geographic range.

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References

  • Acharya, S.N., J.P. Kastelic, K.A. Beauchemin & D.F. Messenger. 2006. A review of research progress on cicer milkvetch (Astragalus cicer L.). Canadian Journal of Plant Sciences 86: 49–62.

    Article  Google Scholar 

  • Alexander, J.A., A. Liston & S.J. Popovich. 2004. Genetic diversity of the narrow endemic Astragalus oniciformis (Fabaceae). American Journal of Botany 91: 2004-2012.

    Article  PubMed  Google Scholar 

  • Allphin, L., N. Brian & T. Matheson. 2005. Reproductive success and genetic divergence among varieties of the rare and endangered Astragalus cremnophylax (Fabaceae) from Arizona, USA. Conservation Genetics 6: 803-821.

    Article  Google Scholar 

  • Amiri, M.S., M.R. Joharchi, M. Nadaf & Y. Nasseh. 2020. Ethnobotanical knowledge of Astragalus spp.: the world’s largest genus of vascular plants. Avicenna Journal of Phytomedicine 10: 128-142.

    PubMed  PubMed Central  Google Scholar 

  • Anand, K.K., R.K. Srivastava, & L.B. Chaudhary. 2010. Analysis of genetic diversity in Astragalus rhizanthus Benth. ssp. rhizanthus var. rhizanthus (Fabaceae) using molecular markers from India. Journal of Botany 2010: 701975.

  • Arroyo, M.T.K. 1981. Breeding systems and pollination biology in Leguminosae. Pp. 723-768. In: Polhill, R.M. & Raven, P.H. (eds.) Advances in legume systematics, part 2. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Atasagun, B., A. Aksoy & K. Gürcan. 2018. Genetic diversity in Astragalus argaeus, a critically endangered species from Turkey. Biologia 73: 927-936.

    Article  CAS  Google Scholar 

  • Azani, N., A. Bruneau, M.F. Wojciechowski & S. Zarre. 2017. Molecular phylogenetics of annual Astragalus (Fabaceae) and its systematic implications. Botanical Journal of the Linnean Society 184: 347-365.

    Article  Google Scholar 

  • Azani, N., A. Bruneau, M.F. Wojciechowski & S. Zarre. 2019. Miocene climate change as a driving force for multiple origins of annual species in Astragalus (Fabaceae, Papilionoideae). Molecular Phylogenetics and Evolution 137: 210-221.

    Article  PubMed  Google Scholar 

  • Azimi, M., M. Mesdaghi, H. Riazi, M. Farahpour & M. Eravani. 2005. Ecological investigation on Astragalus adscendens in Feridounshahr region of Esfahan, Iran. Iranian Journal of Range and Desert Research 12: 499-524. (in Persian)

    Google Scholar 

  • Baer, K.C. & J.L. Maron. 2018. Pre-dispersal seed predation and pollen limitation constrain population growth across the geographic distribution of Astragalus utahensis. Journal of Ecology 106: 1646-1659.

    Article  CAS  Google Scholar 

  • Bai, C., He, X., Tang, H., Shan, B. & Zhao, L. 2009. Spatial distribution of arbuscular mycorrhizal fungi, glomalin and soil enzymes under the canopy of Astragalus adsurgens Pall. in the Mu Su sandland, China. Soil Biology & Biochemistry 41: 941-947.

    Article  CAS  Google Scholar 

  • Barneby, R. 1964. Atlas of North American Astragalus. Memoirs of the New York Botanical Garden 13: 1–1188.

    Google Scholar 

  • Barroetavena, C., S.D. Gisler, D. L. Luoman & R.J. Meinke. 1998. Mycorrhizal status of the endangered species Astragauls applegatei Peck as determined from a soil bioassay. Mycorrhiza 8: 117-119.

    Article  Google Scholar 

  • Baskauf, C.J. & J.M. Burke. 2009. Population genetics of Astragalus bibullatus (Fabaceae) using AFLPs. Journal of Heredity 100: 424-431.

    Article  CAS  Google Scholar 

  • Baskauf, C.J. & S. Snapp. 1998. Population genetics of the cedar-glade endemic Astragalus bibullatus (Fabaceae) using isozymes. Annals of the Missouri Botanical Garden 85: 90–96.

    Article  Google Scholar 

  • Baskauf, C.J. 2001. Examining rarity through comparisons with widespread congeners: a genetic and ecophysiological example from limestone glade endemics. Castanea 66: 126-133.

    Google Scholar 

  • Baskin, C.C. & E. Quarterman. 1969. Germination requirements of seeds of Astragalus tennesseensis. Bulletin of the Torrey Botanical Club 96: 315-321.

    Article  Google Scholar 

  • Baskin, C.C. & J.M. Baskin. 1974. Responses of Astragalus tennesseensis to drought: changes in free amino acids and amides during water stress and possible ecological significance. Oecologia 17: 11-16.

    Article  PubMed  Google Scholar 

  • Baskin, C.C. & J.M. Baskin. 2014. Seeds: ecology, biogeography and evolution of dormancy and germination. Second edition. Elsevier/Academic Press, San Diego.

    Google Scholar 

  • Baskin, C.C., J.M. Baskin & E. Quarterman. 1972. Observations on the ecology of Astragalus tennesseensis. The American Midland Naturalist 88: 167-182.

    Article  Google Scholar 

  • Baskin, C.C., J.M. Baskin & E. Quarterman. 1981. Effect of drought stress on transpiration rates and leaf areas of Astragalus tennesseensis, a near endemic to cedar glades. Journal of the Tennessee Academy of Science 56: 27-31.

    Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 1981. A contribution to the ecological life cycle of Astragalus tennesseensis. Journal of the Tennessee Academy of Science 56: 4-6.

    Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 1989a. Photosynthesis pathway in 14 southeastern cedar glade endemics, as revealed by leaf anatomy. The American Midland Naturalist 114: 205-208.

    Article  Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 1989b. Cedar glade endemics in Tennessee, and a review of their autecology. Journal of the Tennessee Academy of Science 64: 63-74.

    Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 2005. Ecology of two geographically restricted Astragalus species (Fabaceae), A. bibullatus and A. tennesseensis, of the eastern United States. Brittonia 57: 345-353.

    Article  Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 2015. Inbreeding depression and the cost of inbreeding on seed germination. Seed Science Research 25: 355–385.

    Article  Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 2017. Seed germination in cleistogamous species: theoretical considerations and a literature survey of experimental results. Seed Science Research 27: 84–98.

    Article  Google Scholar 

  • Baskin, J.M. & C.C. Baskin. 2018. Pollen limitation and its effect on seed germination. Seed Science Research 28: 253-260.

    Article  Google Scholar 

  • Baskin, J.M., C.C. Baskin, & X. Li. 2000. Taxonomy, anatomy and evolution of physical dormancy in seeds. Plant Species Biology 15: 139-152.

    Article  Google Scholar 

  • Batoli, H. 2008. The ecological study of Astragalus squarrosus Bunge in Kashan Rige-Boland sandy dunes. Pajouhesh and Sazandegi 80: 8-17. (in Persian)

    Google Scholar 

  • Beatley, J.C. 1970. Perennation in Astragalus lentiginosa and Tridens pulchellus in relation to rainfall. Madroño 20: 326-332.

    Google Scholar 

  • Becker, T. 2010. Explaining rarity of the dry grassland perennial Astragalus exscapus. Folia Geobotanica 45: 303-321.

    Article  Google Scholar 

  • Becker, T., N. Voss & W. Durka. 2011. Pollen limitation and inbreeding depression in an ‘old rare’ bumblebee-pollinated grassland herb. Plant Biology 13: 857-864.

    Article  CAS  PubMed  Google Scholar 

  • Bench, A. 2004. Soil seed bank of Astragalus ampullaroiodes, a rare endemic of southern Utah. Senior Thesis, Utah Valley State College, Orem, UT

  • Bencie, R. 1997. Genetic variation and inbreeding depression in the rare California endemic, Astragalus agnicidus (Leguminosae). M.A. thesis, Humboldt State Universtiy, Humboldt, CA.

  • Bergman, P., U. Molau & B. Holmgren. 1996. Micrometeorological impacts on insect activity and plant reproductive success in an alpine environment, Swedish Lapland. Arctic and Alpine Research 28: 196-202.

    Article  Google Scholar 

  • Bhattarai, K., D.A Johnson. T.A. Jones, K.J. Connors & D.R. Gardner. 2008. Physiological and morphological characterization of basalt milkvetch (Astragalus filipes): basis for plant improvement. Rangeland Ecology and Management 61: 444-455.

  • Blows, M.W. & A.A. Hoffmann. 2005. A reassessment of genetic limits to evolutionary change. Ecology 86: 1371-1384.

    Article  Google Scholar 

  • Boe, A. & K. Fluharty. 1993. Reproductive biology of a Canada milk-vetch population from eastern South Dakota. The Prairie Naturalist 25: 65-72.

    Google Scholar 

  • Boe, A. & P.J. Johnson. 2008. Seed predators of Canada milk-vetch and their parasitoids. Proceedings of the South Dakota Academy of Science 87: 229–236.

    Google Scholar 

  • Boe, A., B. McDaniel, & K. Robbins. 1989. Direct effect of parasitism by Dinarmus acutus Thomson on seed predation by Acanthoscelides perforatus (Horn) in Canada milkvetch. Rangeland Ecology & Management 42: 514-515.

    Article  Google Scholar 

  • Bojňanský, V. & A. Fargašová. 2007. Atlas of seeds and fruits of central and east-European flora. Springer, Netherlands.

    Google Scholar 

  • Boughalleb, F., R. Abdellaoui, N.B. Brahim & M. Neffati. 2016. Growth, photosynthesis, water use efficiency, and osmoregulation of the wild species Astragalus gombiformis Pomel. under water deficit. Brazilian Journal of Botany 39: 147-156.

    Article  Google Scholar 

  • Boutton, T.W., A.T. Harrison & B.N. Smith. 1980. Distribution of biomass of species differing in photosynthetic pathway along an altitudinal transect in southeastern Wyoming grassland. Oecologia 45: 287-298.

    Article  PubMed  Google Scholar 

  • Breinholt, J.W., R. Van Buren, O.R. Kopp & C.L. Stephens. 2009. Population genetic structure of an endangered Utah endemic, Astragalus ampullarioides (Fabaceae). American Journal of Botany 96: 661-667.

    Article  PubMed  Google Scholar 

  • Bunge A. 1868. Generis Astragali species Gerontogeae. Pars prior. Claves diagnosticae. Mémoirs de l’Academie Impériale des Sciences de Saint Pétersbourg 11: 1–140.

  • Bushman, A.B., K. Bhattarai & D.A. Johnson. 2010. Population structures of Astragalus filipes collections from western North America. Botany 88: 565-574.

    Article  Google Scholar 

  • Cane, J.H., C. Johnson, J.R. Napoles, D.A. Johnson & R. Hammon. 2013. Seed-feeding beetles (Bruchinae, Curculionidae, Brentidae) from legumes (Dalea ornate, Astragalus filipes) and other forbs needed for restoring rangelands of the Intermountain West. Western North American Naturalist 73: 477-484.

    Article  Google Scholar 

  • Catling, P.M., & A. Sinclair. 2002. Initial beneficial effects of fire and bulldozing on neglected milkvetch, Astragalus neglectus, in an eastern Ontario alvar woodland. Canadian Field-Naturalist 116: 640-642.

    Google Scholar 

  • Center, T.D. & C.D. Johnson. 1974. Coevolution of some seed beetles (Coleoptera: Bruchidae) and their hosts. Ecology 55: 1096-1103.

    Article  Google Scholar 

  • Center, T.D. & C.D. Johnson. 1976. Host plants and parasites of some Arizona seed-feeding insects. Annals of the Entomological Society of America 69: 195-201.

    Article  Google Scholar 

  • Charis (Charis Coporation) 2003. Lane mountain milk-vetch pollination. A report prepared for the U.S. Army National Training Center, Fort Irwin, CA.

  • Chaudhary, L.B., T.S. Rana & K.K. Anand. 2008. Current status of the systematics of Astragalus L. (Fabaceae) with special reference to the Himalayan species in India. Taiwania 53: 338-355.

    Google Scholar 

  • Chaudhary, L.B., T.S. Rana, D. Narzary & S. Verma. 2007. A new species of Astragalus L. (Leguminosae) from India based on morphological and molecular markers. Botanical Journal of the Linnean Society 154: 27-34.

    Article  Google Scholar 

  • Choi, I.S. & B.H. Choi. 2016. Isolation and characterization of ten microsatellite loci from Korean Astragalus mongholicus (Fabaceae). Journal of Genetics 93: 73-76.

    Article  CAS  Google Scholar 

  • Clement, S.L. & D.H. Miller. 1982. Insect seed predation on Astragalus bisulcatus (Hook.) Gray (Leguminosae). Pan-Pacific Entomologist 58: 38-41.

    Google Scholar 

  • Clement, S.L., T.L. Griswold, R.W. Rust, B.C. Hellier & D.M. Stout. 2006. Bee associates of flowering Astragalus and Onobrychis genebank accessions at a Snake River site in Eastern Washington. Journal of the Kansas Entomological Society 79: 254-261.

    Article  Google Scholar 

  • Combs, J.K., A.M. Lambert & S.H. Reichard. 2013. Predispersal seed predation is higher in a rare species than in its widespread sympatric congeners (Astragalus, Fabaceae). American Journal of Botany 100: 2149-2157.

    Article  PubMed  Google Scholar 

  • Combs, J.K., S.H. Reichard, M.J. Groom, D.L. Wilderman & P.A. Camp. 2011. Invasive competitor and native seed predators contribute to rarity of the narrow endemic Astragalus sinuatus Piper. Ecological Applications 21: 2498-2509.

    Article  PubMed  Google Scholar 

  • Cornelius, J.M., P.R. Kemp, J.A. Ludwig & G.L. Cunningham. 1991. The distribution of vascular plant species and guilds in space and time along a desert gradient. Journal of Vegetation Science 2: 59-72.

    Article  Google Scholar 

  • Crone, E.E. & P. Lesica. 2006. Pollen and water limitation in Astragalus scaphoides, a plant that flowers in alternate years. Oecologia 150: 40–49.

    Article  PubMed  Google Scholar 

  • Crone, E.E. 2013. Desynchronization and re-synchronization of reproduction by Astragalus scaphoides, a plant that flowers in alternate years. Ecological Research 28: 133-142.

    Article  Google Scholar 

  • Dalling, J.W., M.D. Swaine & N.C. Garwood. 1997. Soil seed bank community dynamics in seasonally moist lowland tropical forest, Panama. Journal of Tropical Ecology 13: 659-680.

    Article  Google Scholar 

  • Decker, K. 2005. Astragalus wetherillii Jones (Wetherill’s milkvetch): a technical conservation assessment. USDA Forest Service, Rocky Mountain Region. Available: http://fs.fed.us/r2/projects/scp/assessments/astragaluswetherilii.pdf

  • Decker, K. 2006. Astragalus missouriensis Nutt. var. humistratus Isely (Missouri milkvetch): a technical conservation assessment. USDA Forest Service, Rocky Mountain Region. Available: http://fs.fed.us/r2/projects/scp/assessments/astragalusmissouriensisvarhumistratusi.pdf

  • DePrenger-Levin, M.E., J.M.R. Neale, T.A. Grant, C. Dawson & Y.E. Baytok. 2013. Life history and demography of Astragalus microcymbus Barneby (Fabaceae). Natural Areas Journal 33: 264-276.

    Article  Google Scholar 

  • Díaz, M.L. & E. Domínguez. 1981. Cleistogamy and pollen dimorphism in Astragalus cymbaecarpos Brot. Botanica Macaronesica 8-9: 79-87. (in Spanish with English summary)

  • Dizkirici, A., M. Ekici & Z. Kaya. 2014. Comparative molecular phylogenetics of Astragalus L. sections from Turkey with New World Astragalus species using nrDNA ITS sequences. Plant Systematics and Evolution 300: 163-175.

    Article  Google Scholar 

  • Duan, Q.M., Z.S. Liang, X.Q. Mu & W.L. Wang. 2005. Germination characteristics of Astragalus membranaceus seeds. Acta Botanica Boreali-Occidentalia Sinica 25: 1246. (in Chinese)

  • Eckert, C.G., K.E. Samis & S.C. Lougheed. 2008. Genetic variation across species’ geographical ranges: the central–marginal hypothesis and beyond. Molecular Ecology 17: 1170-1188.

    Article  CAS  PubMed  Google Scholar 

  • Edwards, A.L., B. Wiltshire & D.L. Nickrent. 2004. Genetic diversity in Astragalus tennesseensis and the federal endangered Dalea foliosa (Fabaceae). Journal of the Torrey Botanical Society 131: 279-291.

    Article  Google Scholar 

  • Ehrlén, J. & K. Lehtilä. 2002. How perennial are perennial plants? Oikos 98: 308-322.

    Article  Google Scholar 

  • Ehrman, T. & P.S. Cocks. 1990. Ecogeography of annual legumes in Syria: distribution patterns. Journal of Applied Ecology 27: 578-591.

    Article  Google Scholar 

  • Eisvand, H.R., H.M. Arefi, & R. Tavakol-Afshari. 2006. Effects of various treatments on breaking seed dormancy of Astragalus siliquosus. Seed Science and Technology 34: 747-752.

    Article  Google Scholar 

  • Ellstrand, N.C. & D.R. Elam. 1993. Population genetic consequences of small population size: implications for plant conservation. Annual Review of Ecology and Systematics 24: 217-242.

    Article  Google Scholar 

  • Erickson, A.N. & A.H. Markhart. 2002. Flower developmental stage and organ sensitivity of bell pepper (Capsicum annuum L.) to elevated temperature. Plant Cell and Environment 25: 123-130.

    Article  Google Scholar 

  • Evans, R.D. & J.R. Ehleringer. 1994. Plant δ15N values along a fog gradient in the Atacama Desert, Chile. Journal of Arid Environments 28: 189-193.

    Article  Google Scholar 

  • Farhangisabet, M., A. Majd, T. Nejadsattari, A.A. Maassomi & A. Mazouji. 2011. Megagametophyte and embryo development in five species of Astragalus (Fabaceae). The Iranian Journal of Botany 17: 167-174.

    Google Scholar 

  • Faria, S.M., Lewis, G.P., Sprent, J.I. & Sutherland, J.M. 1989. Occurrence of nodulation in the Leguminosae. New Phytologist 111: 607-619.

    Article  Google Scholar 

  • Fotheringham, C.J. & J.E. Keeley. 1998. Ecology and distribution of Braunton's milkvetch (Astragalus brauntonii) and Lyon's pentachaeta (Pentachaeta lyonii). California Department of Fish and Game. Long Beach, CA.

  • Fox W.E., III, K.W. Alfred & E.H. Roalson. 2010. A guide to the common locoweeds and milkvetches of New Mexico. New Mexico State University. Cooperative Extension Service Cicular 557.

  • Freeman, J.L., L.H. Zhang, M.A. Marcus, S. Fakra, S.P. McGrath & E.A. Pilon-Smits. 2006. Spatial imaging, speciation, and quantification of selenium in the hyperaccumulator plants Astragalus bisulcatus and Stanleya pinnata. Plant Physiology 142: 124-134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Friedlander, J.D. 1980. The status of rare and endangered plant species in Mesa Verde National Park, Colorado. Masters Thesis. Colorado State University, Fort Collins.

  • Frodin, D.G. 2004. History and concepts of big plant genera. Taxon 53: 753-776.

    Article  Google Scholar 

  • Funes, G., S. Basconcelo, S. Díaz & M. Cabido. 1999. Seed size and shape are good predictors of seed persistence in soil in temperate mountain grasslands of Argentina. Seed Science Research 9: 341-345.

    Article  Google Scholar 

  • Gallardo, R., E. Dominguez & J.M. Muñoz. 1993. The heterochronic origin of the cleistogamous flower in Astragalus cymbicarpos (Fabaceae). American Journal of Botany 80: 814-823.

    Article  Google Scholar 

  • Gallardo, R., E. Dominguez & J.M. Muñoz. 1994. Pollen-ovule ratio, pollen size, and breeding system in Astragalus (Fabaceae) subgenus Epiglottis: a pollen and seed allocation approach. American Journal of Botany 81: 1611-1619.

    Article  Google Scholar 

  • Galloni, M., L. Podda, D. Vivarelli & G. Cristofolini. 2007. Pollen presentation, pollen-ovule ratios, and other reproductive traits in Mediterranean legumes (fam. Fabaceae-subfam. Faboideae). Plant Systematics and Evolution 266: 147-164.

    Article  Google Scholar 

  • Gama-Arachchige, N.S., J.M. Baskin, R.L. Geneve & C.C. Baskin. 2011. Acquisition of physical dormancy and ontogeny of the micropyle–water-gap complex in developing seeds of Geranium carolinianum (Geraniaceae). Annals of Botany 108: 51-64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, J., Z. Terefework, W. Chen & K. Lindström. 2001. Genetic diversity of rhizobia isolated from Astragalus adsurgens growing in different geographical regions of China. Journal of Biotechnology 91: 155-168.

    Article  CAS  PubMed  Google Scholar 

  • Gazer M. 1993. Revision of Astragalus L. sect. Sesamei DC. (Leguminosae). Sendtnera 1: 69–155.

    Google Scholar 

  • Geer, S.M. & V.J. Tepedino. 1992. Breeding systems of the rare heliotrope milkvetch (Astragalus montii Welsh: Fabaceae) and two common congeners. Southwestern rare and endangered plants. Proceedings of the Southwestern Rare and Endangered Plant Conference. New Mexico Forestry and Resources, Conservation Division. Miscellaneous Publication 2: 334-344.

    Google Scholar 

  • Geer, S.M., V.J. Tepedino, T.L. Griswold & W.R. Bowlin. 1995. Pollinator sharing by three sympatric milkvetches, including the endangered species Astragalus montii. The Great Basin Naturalist 55: 19-28.

    Google Scholar 

  • Geneve, R.L., C.C. Baskin, J.M. Baskin, K.G. Jayasuriya & N.S. Gama-Arachchige. 2018. Functional morpho-anatomy of water-gap complexes in physically dormant seed. Seed Science Research 28: 186-191.

    Article  Google Scholar 

  • Gentry, H.S. 1957. Gum tragacanth in Iran. Economic Botany 11: 40-63.

    Article  Google Scholar 

  • Gibson, A.C., M.R. Sharifi & P.W. Rundel. 1998. Ecophysiological observations on Lane Mountain milkvetch, Astragalus jaegerianus (Fabaceae), a proposed endangered species of the Mojave Desert. Aliso 17: 77-82.

    Article  Google Scholar 

  • Gillett, J.B. 1963. Astragalus L. (Leguminosae) in the highlands of tropical Africa. Kew Bulletin 17: 413-423.

    Article  Google Scholar 

  • Gitzendanner, M.A. & P.S. Soltis. 2000. Patterns of genetic variation in rare and widespread plant congeners. American Journal of Botany 87: 783-792.

    Article  CAS  PubMed  Google Scholar 

  • Glacolva, T. A. & O.V. Zalensky. 1978. Oxygen effects on photosynthesis and 14C metabolism in desert plants. Plant Physiology 62: 204-209.

    Article  Google Scholar 

  • Glémin, S. 2003. How are deleterious mutations purged? Drift versus nonrandom mating. Evolution 57: 2578-2687.

    Google Scholar 

  • Glenn, M. 2009. Astragalus lentiginosus var. piscinensis (Fish Slough milk-vetch) 5-year review: summary and evaluation. U.S. Fish and Wildlife Service, Ventura Fish and Wildlife Office, Ventura, CA.

  • Gomez-Sosa, E. 1979. Las especies sudamericanas del género Astragalus (Leguminosae) I. Las especies Patagónicas Argentinas. Darwiniana 22: 313-376.

  • Goncharov N.F., A.G. Borisova, S.G. Gorshkova, M.G. Popov & I.T. Vassilczenko. 1946. Astragalus. In: Komarov VL, Shishkin BK, eds. Flora of the U.S.S.R. Vol. 12. Moscow: Editio Academiae Scientiarum URSS, 1–918.

  • Govindaraj, M., Vetriventhan, M. & Srinivasan, M. 2015. Importance of genetic diversity assessment in crop plants and its recent advances: an overview of its analytical perspectives. Genetics Research International 2015: ID 431487.

  • Grant, K.A. & V. Grant. 1967. Effects of hummingbird migration on plant speciation in the California flora. Evolution 21: 457-465.

    Article  PubMed  Google Scholar 

  • Green, T.W. & G.E. Bohart. 1975. The pollination ecology of Astragalus cibarius and Astragalus utahensis (Leguminosae). American Journal of Botany 62: 379-386.

    Article  Google Scholar 

  • Green, T.W. & I.G. Palmbald. 1975. Effects of insect seed predators on Astragalus cibarius and Astragalus utahensis (Leguminosae). Ecology 56: 1435-1440.

    Article  Google Scholar 

  • Gremer, J.R. & A. Sala 2013. It is risky out there: the costs of emergence and the benefits of prolonged dormancy. Oecologia 172: 937-947.

    Article  PubMed  Google Scholar 

  • Gremer, J.R., A. Sala, & E.E. Crone. 2010. Disappearing plants: why they hide and how they return. Ecology 91: 3407-3413.

    Article  PubMed  Google Scholar 

  • Gremer, J.R., E.E. Crone & P. Lesica. 2012. Are dormant plants hedging their bets? Demographic consequences of prolonged dormancy in variable environments. The American Naturalist 179: 315-327.

    Article  PubMed  Google Scholar 

  • Gvaladze, G. & M. Akhalkatsi. 1996. Comparative embryology of some Astragalus species. Bulletin of the Georgian Academy of Science 153: 432–434.

    Google Scholar 

  • Hafenrichter, A.L., R.B. Foster & J.L. Schwendiman. 1965. Effect of storage at four locations in the west on longevity of forage seeds. Agronomy Journal 57: 143-147.

    Article  Google Scholar 

  • Hamilton, J. 1892. Note on Bruchus alboscutellatus, Miarus hispidulus, Coeliodes acephalus, and a new Thiobius. Entomology News 3: 253-255.

    Google Scholar 

  • Hamilton, M.B. & Mitchell-Olds, T. 1994. The mating system and relative performance of selfed and outcrossed progeny in Arabis fecunda (Brassicaceae). American Journal of Botany 81: 1252-1256.

    Article  Google Scholar 

  • Han, Y.J., J.M. Baskin, D.Y. Tan, C.C. Baskin & M.Y. Wu. 2018. Effects of predispersal insect seed predation on the early life history stages of a rare cold sand-desert legume. Scientific Reports 8: 3240.

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrison, J.G., M.L. Forister, S.R. Mcknight, E. Nordin & T.L. Parchman. 2019. Rarity does not limit genetic variation or preclude subpopulation structure in the geographically restricted desert forb Astragalus lentiginosus var. piscinensis. American Journal of Botany 106: 260-269.

    Article  PubMed  Google Scholar 

  • Hedhly, A., J.I. Hormaza & M. Herrero. 2005. Influence of genotype-temperature interaction on pollen performance. Journal of Evolutionary Biology 18: 1494-1502.

    Article  CAS  PubMed  Google Scholar 

  • Hedhly, A., J.I. Hormaza & M. Herrero. 2009. Global warming and sexual plant reproduction. Trends in Plant Science 14: 30-36.

    Article  CAS  PubMed  Google Scholar 

  • Hegazy, A.K., O. Hammouda, J. Lovett-Doust & N.H. Gomaa. 2009. Variations of the germinable soil seed bank along the altitudinal gradient in the northwestern Red Sea region. Acta Ecologica Sinica 29: 20-29.

    Article  Google Scholar 

  • Hoffmann, A. A., & P.A. Parsons. 1997. Extreme environmental change and evolution. Cambridge University Press, Cambridge.

    Google Scholar 

  • Hoffmann, A.A. & M.W. Blows. 1994. Species borders: ecological and evolutionary perspectives. Trends in Ecology & Evolution 9: 223-227.

    Article  CAS  Google Scholar 

  • Houghton, S., M.T. Stevens, & S.E. Meyer. 2020. Pods as sails but not as boats: dispersal ecology of a habitat-restricted desert milkvetch. American Journal of Botany 107: 864-875.

    Article  PubMed  Google Scholar 

  • Huggins, T.R., B.A. Prigge, M.R. Sharifi & P.W. Rundel. 2010. The effects of long-term drought on host plant canopy condition and survival of the endangered Astragalus jaegerianus (Fabaceae). Madroño 57: 120-128.

    Article  Google Scholar 

  • Hull, A.C. 1973. Germination of range plant seeds after long periods of uncontrolled storage. Rangeland Ecology & Managemen 26: 198-200.

    Article  Google Scholar 

  • Hurd, P.D. 1978. An annotated catalog of the carpenter bees (genus Xylocopa Latreille) of the western hemisphere (Hymenoptera: Anthophoridae). Smithsonian Institution Press, Washington, DC.

    Google Scholar 

  • Husband, B.C. & D.W. Schemske. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70.

    Article  PubMed  Google Scholar 

  • ILDIS [International Legume Database & Information Service]. 2002. World database of legumes. Southampton, ILDIS.

    Google Scholar 

  • Jaganathan, G.K., J. Li, M. Biddick, K. Han, D. Song, Y. Yang, Y. Han & B. Liu. 2019. Mechanisms underpinning the onset of seed coat impermeability and dormancy-break in Astragalus adsurgens. Scientific Reports 9: 9695.

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson, C.D. 1970. Biosystematics of the Arizona, California, and Oregon species of the seed beetle genus Acanthoscelides Schilsky (Coleoptera: Bruchidae). University of California Publications in Entomology 59: 1-116.

    Google Scholar 

  • Johnson, G.N., A.J. Young, J.D. Scholes & P. Horton. 1993. The dissipation of excess excitation energy in British plant species. Plant, Cell & Environment 16: 673-679.

    Article  CAS  Google Scholar 

  • Johnston, I.M., 1947. Astragalus in Argentina, Bolivia and Chile. Journal of the Arnold Arboretum 28: 336-374.

    Article  Google Scholar 

  • Jones T.A., D.A. Johnson, B.S. Bushman, K.J. Connors & R.C. Smith. (2016) Seed dormancy mechanism in basalt milkvetch and western prairie clover. Rangeland Ecology and Management 69: 117-122.

    Article  Google Scholar 

  • Jordano, D., J.F. Haeger & J. Rodríguez. 1990. The effect of seed predation by Tomares ballus (Lepidoptera: Lycaenidae) on Astragalus lusitanicus (Fabaceae): determinants of differences among patches. Oikos 57: 250-256.

    Article  Google Scholar 

  • Juncosa, A.M. & B.D. Webster. 1989. Pollination in Lupinus nanus subsp. latifolius (Leguminosae). American Journal of Botany 76: 59-66.

    Article  Google Scholar 

  • Karron, J.D. 1987a. A comparison of levels of genetic polymorphism and self-compatibility in geographically restricted and widespread plant congeners. Evolutionary Ecology 1: 47-58.

    Article  Google Scholar 

  • Karron, J.D., 1987b. The pollination ecology of co-occuring geographically restricted and widespread species of Astragalus (Fabaceae). Biological Conservation 39: 179-193.

    Article  Google Scholar 

  • Karron, J.D. 1989. Breeding systems and levels of inbreeding depression in geographically restricted and widespread species of Astragalus (Fabaceae). American Journal of Botany 76: 331-340.

    Article  Google Scholar 

  • Karron, J.D. 1991. Patterns of genetic variation and breeding systems in rare plant species. In: Falk, D.A. & K.E. Holsinger (eds). Genetics and conservation of rare plants. Oxford University Press, New York & Oxford. pp. 87-98.

    Google Scholar 

  • Karron, J.D., Y.B. Linhart, D.A. Chaulk & C.A. Robertson. 1988. Genetic structure of populations of geographically restricted and widespread species of Astragalus (Fabaceae). American Journal of Botany 75: 1114-1119.

    Article  Google Scholar 

  • Kaye, T.N. 1999. From flowering to dispersal: reproductive ecology of an endemic plant, Astragalus australis var. olympicus (Fabaceae). American Journal of Botany 86: 1248-1256.

    Article  CAS  PubMed  Google Scholar 

  • Kazempour Osaloo S., A.A. Maassoumi & N. Murakami. 2003. Molecular systematics of the genus Astragalus L. (Fabaceae): phylogenetic analyses of nuclear ribosomal DNA internal transcribed spacers and chloroplast gene ndhF sequences. Plant Systematics and Evolution 242: 1–32.

    Article  Google Scholar 

  • Kazempour Osaloo, S., A.A. Maassoumi & N. Murakami. 2005. Molecular systematics of Old World Astragalus (Fabaceae) as inferred from nrDNA ITS sequence data. Brittonia 57: 367–381.

    Article  Google Scholar 

  • Kildisheva, O.A., T.E. Erickson, M.D. Madsen, K.W. Dixon & D.J. Merritt. 2019. Seed germination and dormancy traits of forbs and shrubs important for restoration of North American dryland ecosystems. Plant Biology 21: 458-469.

    Article  CAS  PubMed  Google Scholar 

  • Kim, S.Y., S.H. Oh, W.H. Hwang, S.M. Kim, K.J. Choi & H.W. Kang. 2008. Physical dormancy in seeds of Chinese milk vetch (Astragalus sinicus L.) from Korea. Korean Journal of Crop Science 53: 421-426.

    CAS  Google Scholar 

  • King, T.L., M.J. Springmann & J.A. Young. 2012. Tri- and tetra-nucleotide microsatellite DNA markers for assessing genetic diversity, population structure, and demographics in the Holmgren milk-vetch (Astragalus holmgreniorum). Conservation Genetic Resources 4: 39–42.

    Article  Google Scholar 

  • Komarov, V.L. (ed.) 1965. Flora of the USSR. Vol. XII. Leguminoseae: Astragalus. (Translated from the Russian by the Israel Program for Scientific Translations for the Smithsonian Institution).

  • Kondo, T. & S. Takeuchi. 2004. Breaking seed dormancy and growth after germination of Astragalus adsurgens (Leguminosae), a rare species in Hokkaido. Journal of the Japanese Society of Revegetation Technology 29: 495-502.

    Article  Google Scholar 

  • Kozuharova, E. & D.H. Firmage. 2007. On the pollination ecology of Astragalus alopecurus Pallas (Fabaceae) in Bulgaria. Comptes Rendus de l’Académie Bulgare de L’Académie des Sciences 60: 863-870.

    Google Scholar 

  • Kozuharova, E. & D.H. Firmage. 2009. Notes on the reproductive biology of Astragalus dasyanthus Pall. (Fabaceae) a rare plant for Bulgaria. Comptes Rendus de L’Académie Bulgare des Sciences 62: 1079-1088.

    Google Scholar 

  • Kudo, G. 1991. Effects of snow-free period on the phenology of alpine plants inhabiting snow patches. Arctic and Alpine Research 23: 436-443.

    Article  Google Scholar 

  • Kundo, G. & L.D. Harder. 2005. Floral and inflorescence effects on variation in pollen removal and seed production among six legume species. Functional Ecology 19: 245-254.

    Article  Google Scholar 

  • Kudo, G. & U. Molau. 1999. Variations in reproductive traits at inflorescence and flower levels of an arctic legume, Astragalus alpinus L.: comparisons between a subalpine and an alpine population. Plant Species Biology 14: 181-191.

    Article  Google Scholar 

  • Ladyman, J.A.R. 2003. Astragalus molybdenus Barneby (Leadville milkvetch): a technical conservation assessment. [Online]. USDA Forest Service, Rocky Mountain Region. Available: http://www.fs.fed.us/r2/projects/scp/assessments/astragalusmolybdenus.pdf. [3 May 2020].

  • Ladyman, J.A.R. 2006. Astragalus barrii Barneby (Barr’s milkvetch): a technical conservation assessment. [Online]. USDA Forest Service, Rocky Mountain Region. Available: http://www.fs.fed.us/r2/projects/scp/assessments/astragalusbarrii.pdf.

  • Lalonde, R.G. & B.D. Roitberg. 1989. Resource limitation and offspring size and number trade-offs in Cirsium arvense (Asteraceae). American Journal of Botany 76: 1107-1113.

    Article  Google Scholar 

  • Langran, X. & D. Podlech. 2010. Flora of China: 139. Astragalus Linnaeus. Species Plantarum 2, 755-1753. In: ‘eFloras (2008). Published on the Internet http://www.efloras.org [accessed 18 Novemeber 2020]’ Missouri Botanical Garden, St. Louis, MO & Harvard University Herbaria, Cambridge, MA.

  • Lee, Y.H., S.H. Hong, B.H. Kang, J.K. Lee, S.I. Shim & W. Kim. 2006. Effect of stratification on the dormancy of Chinese milk vetch seeds (Astragalus sinicus L.). Korean Journal of Plant Breeding 38: 250-254.

    Google Scholar 

  • Leppik, E.E. 1966. Floral evolution and pollination in the Leguminosae. Annales Botanici Fennici 3: 299-308.

    Google Scholar 

  • Lersten, N.R. 1983. Suspensors in leguminosae. The Botanical Review 49: 233-257.

    Article  Google Scholar 

  • Lesica, P. 1994. Demographic monitoring of Astragalus scaphoides at two sites in Montana and Idaho. Final report to USDI Bureau of Land Management, Butte District. Montana Natural Heritage Program, Helena.

  • Lesica, P. & B.M. Steele. 1994. Prolonged dormancy in vascular plants and implications for monitoring studies. Natural Areas Journal 14: 209-212.

    Google Scholar 

  • Lesica, P. 1995. Demography of Astragalus scaphoides and effects of herbivory on population growth. The Great Basin Naturalist 55: 142-150.

    Google Scholar 

  • Li, X. 2015. Distribution of rare psammophyte Astragalus lehmannianus (Fabaceae) and the effect of the cocoon-shaped calyx on sexual reproduction and seed dispersal. M.S. thesis, Xinjiang Agricultural Universtiy. Urümqi. (in Chinese with 2-page English abstract)

  • Liston, A & Wheeler, J.A. 1994. The phylogenetic position of the genus Astragalus (Fabaceae): evidence from the chloroplast genes rpoC1 and rpoC2. Biochemical Systematics and Ecology 22: 377–388

  • Liston, A. 1992. Isozyme systematics of Astragalus sect. Leptocarpi subsect. Californici (Fabaceae). Systematic Botany 17: 367-379.

    Article  Google Scholar 

  • Liu, H., B. Abudureheman, L. Zhang, J.M. Baskin C.C. Baskin & D. Zhang. 2017. Seed dormancy-breaking in a cold desert shrub in relation to sand temperature and moisture. AoB Plants 9: plx003.

  • Liu, Y., X. Feng, P. Gao, Y. Li, M.J. Christensen & T. Duan. 2018. Arbuscular mycorrhiza fungi increased the susceptibility of Astragalus adsugens to powdery mildew caused by Erysiphe pisi. Mycology 9: 223-232.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Long, Y., D.Y. Tan, C.C. Baskin & J.M. Baskin. 2012. Seed dormancy and germination characteristics of Astragalus arpilobus (Fabaceae, subfamily Papilionoideae), a central Asian desert annual ephemeral. South African Journal of Botany 83: 68-77.

    Article  Google Scholar 

  • Looman, J. 1974. Biological flora of the Canadian prairie provinces. II. Astragalus vexilliflexus Sheld. Canadian Journal of Plant Science 54: 291-300.

    Article  Google Scholar 

  • Loria, M. & I. Noy-Meir. 1979/80. Dynamics of some annual populations in a desert loess plain. Israel Journal of Botany 28: 211-225.

    Google Scholar 

  • Lovas-Kiss, Á., J. Sonkoly, O. Vincze, A.J. Green, A. Takács & A.V. Molnár. 2015. Strong potential for endozoochory by waterfowl in a rare, ephemeral wetland plant species, Astragalus contortuplicatus (Fabaceae). Acta Societatis Botanicorum Poloniae 84: 321–326

    Article  Google Scholar 

  • Luo, M.C., K.K. Hwu & T.C. Huang. 2000. Taxonomic study of Taiwan Astragalus based on genetic variation. Taxon 49: 35-46.

    Article  Google Scholar 

  • Maassoumi, A.A. 1998. Astragalus in the Old World, check-list. Research Institute of Forests and Rangelands, Tehran. (in Persian)

  • Maassoumi, A.A. 2018. Fabaceae: Astragalus III. 766 pp. In: Assadi et al. (eds.) Flora of Iran, No. 145–Research Institute of Forests and Rangelands, Tehran. (in Persian)

  • Mabberley, D.J. 2008. Mabberley’s plant-book. A portable dictionary of plants, their classification and uses. Third edition. Cambridge University Press, Cambridge.

  • Macior, L.W. 1974. Pollination ecology of the Front Range of the Colorado Rocky Mountains. Melanderia 15: 1-59.

    Google Scholar 

  • Martin, E.F. 2010. Reproduction, demography, and habitat characterization of Astragalus peckii (Fabaceae), a rare central Oregon endemic. Ph.D. dissertation, Oregon State University, Corvallis.

  • Martínez-Sánchez, J.J., F. Segura, M. Aguado, J.A. Franco & M.J. Vicente. 2011. Life history and demographic features of Astragalus nitidiflorus, a critically endangered species. Flora 206: 423-432.

    Article  Google Scholar 

  • Maschinski, J., R. Frye & S. Rutman. 1997. Demography and population viability of an endangered plant species before and after protection from trampling. Conservation Biology 11: 990-999.

    Article  Google Scholar 

  • Maxwell, K. & G.N. Johnson. 2000. Chlorophyll fluorescence—a practical guide. Journal of Experimental Botany 51: 659-668.

    Article  CAS  PubMed  Google Scholar 

  • Mazer, S.J. & S. Travers. 1992. Baseline monitoring study of a rare plant, the fish slough milkvetch (Astragalus lentiginosus var. piscinensis [Fabaceae]): sources of variation in reproduction, herbivory and growth. A grant report prepared in the Department of Biological Sciences of the University of California, Santa Barbara.

  • Mehrnia, M., S. Zarre & A. Sokhan-Sanj. 2005. Intra-and inter-specific relationships within the Astragalus microcephalus complex (Fabaceae) using RAPD. Biochemical Systematics and Ecology 33: 149-158.

    Article  CAS  Google Scholar 

  • Meinke, R., K. Amsberry & R. Currin. 2009. Continuing assessement of recovery requirements for Astragalus lentiginosus var. coachellae: evaluating the potential effects of disturbance, habitat fragmentation, and exotic species. A report prepared for the California Department of Fish and Wildlife. Eureka Field Office, Eureka, CA.

  • Meinke, R., S. Meyers, K. Amsberry, C. Wilson, M. Groberg, R. Woolverton & J. Brown. 2013. Assessing the population genetics, taxonomy, reproductive ecology, and life history traits of Humboldt milk-vetch (Astragalus agnicidus) in relation to conservation and management. A report prepared for the California Department of Fish and Wildlife. Eureka Field Office, Eureka, CA.

  • Meinke, R.J. & T.N. Kaye. 1992. Taxonomic assessment of Astragalus tegetarioides (Fabaceae) and a new related species from northern California. Madroño 39: 193-204.

    Google Scholar 

  • Meinke, R.J., K. Amsberry, R.E. Currin, S.C. Meyers & B. Knaus. 2007. Evaluating the biological conservation status of the Coachella valley milkvetch (Astragalus lentiginosus var. coachellae). Native Plant Conservation Program, Oregon Department of Agriculture and Department of Botany & Plant Pathology, Oregon State University, Corvallis.

  • Melgoza-Castillo, A. 1995. Ecology of locoweed (Astragalus mollissimus) in Chihuahua, Mexico. Ph.D. dissertation. New Mexico State University, Las Cruces.

  • Miklas, P.N., C.E. Townsend & S.L. Ladd. 1987. Seed coat anatomy and the scarification of cicer milkvetch seed. Crop Science 27: 766-772.

    Article  Google Scholar 

  • Miller, M.E., R.K. Mann, R. Lieberg, C. Decker, K. Davidson, H. Goldstein & J.D. Yount. 2009. An update on ecological investigations of the Shivwits milk-vetch (Astragalus ampullarioides), Washington County, Utah. Poster presentation, Fifth Southwest Rare Plant Conference. Salt Lake City, Utah.

  • Molau, U., B. Eriksen & J.T. Knudsen. 1989. Predispersal seed predation in Bartsia alpina. Oecologia 81: 181-185.

    Article  PubMed  Google Scholar 

  • Molnár, V.A., J. Sonkoly, Á. Lovas-Kiss, R. Fekete, A. Takacs, L. Somlyay & P. Toeroek. 2015. Seed of the threatened annual legume, Astragalus contortuplicatus, can survive over 130 years of dry storage. Preslia 87: 319-328.

    Google Scholar 

  • Morris, A.B., C. Scalf, A. Burleyson, L.T. Johnson & K. Trostel. 2016. Development and characterization of microsatellite primers in the federally endangered Astragalus bibullatus (Fabaceae). Applications in Plant Sciences 4: 1500126.

    Article  Google Scholar 

  • Morris, A.B., R.S. Baucom & M.B. Cruzan. 2002. Stratified analysis of the soil seed bank in the cedar glade endemic Astragalus bibullatus: evidence for historical changes in genetic structure. American Journal of Botany 89: 29-36.

    Article  PubMed  Google Scholar 

  • Murooka, Y., Y. Xu, K. Sanada, M. Araki, T. Morinaga & A. Yokota. 1993. Formation of root nodules by Rhizobium huakuii biovar. regne bv. nov. on Astragalus sinicus cv. Japan. Journal of Fermentation and Bioengineering 76: 38-44.

    Article  CAS  Google Scholar 

  • Na, C.S., Y.H. Lee, S.H. Hong, C.S. Jang, B.H. Kang, J.K. Lee, T.H. Kim & W. Kim. 2007. Changes of seed quality of Chinese Milk Vetch (Astragalus sinicus L.) during seed developmental stages. Korean Journal of Crop Science 52: 363-369.

    Google Scholar 

  • Nelson, D.M. and C.D. Johnson. 1983a. Stabilizing selection on seed size in Astragalus (Leguminosae) due to differential predation and differential germination. Journal of the Kansas Entomological Society 56: 169-174.

    Google Scholar 

  • Nelson, D.M. & C.D. Johnson. 1983b. Selenium in seeds of Astragalus (Leguminosae) and its effects on host preferences of bruchid beetles. Journal of the Kansas Entomological Society 56: 267-272.

    Google Scholar 

  • Noroozi, J., A. Talebi, M. Doostmohammadi, S. Manafzadeh, Z. Asgarpour & G.M. Schneeweiss. 2019. Endemic diversity and distribution of the Iranian vascular flora across phytogeographical regions, biodiversity hotspots and areas of endemism. Scientific Reports 9: 12991.

    Article  PubMed  PubMed Central  Google Scholar 

  • Nosrati, H., M. Noramideh, A.R. Haghighi & M. Nikniazi. 2015. Relationship between geographical distribution range and levels of genetic variations in Astragalus (Fabaceae). Analele Universităţii din Oradea, Fascicula Biologie, 22: 76-80.

    Google Scholar 

  • Owen, W.R. 1995. Growth and reproduction in an alpine cushion plant: Astragalus kentrophyta var. implexus. The Great Basin Naturalist 55: 117-123.

    Google Scholar 

  • Özbek, F., H.N. Büyükkartal, M. Ekici & M.U. Özbek. 2016. Seed coat ultrastructure of the genus Astragalus L. section Uliginosi Gray (Fabaceae). Gazi University Journal of Science 29: 279-283.

    Google Scholar 

  • Patanè, C. & F. Gresta. 2006. Germination of Astragalus hamosus and Medicago orbicularis as affected by seed-coat dormancy breaking techniques. Journal of Arid Environments 67: 165-173.

    Article  Google Scholar 

  • Pavlik, B.M. 1980. Patterns of water potential and photosynthesis of desert sand dune plants, Eureka Valley, California. Oecologia 46: 147-154.

    Article  PubMed  Google Scholar 

  • Pavlik, B.M. & M.G. Barbour. 1988. Demographic monitoring of endemic sand dune plants, Eureka Valley, California. Biological Conservation 46: 217-242.

    Article  Google Scholar 

  • Peet, M.M., S. Sato & R. G. Gardner. 1998. Comparing heat stress effects on male-fertile and male-sterile tomatoes. Plant, Cell & Environemnt 21: 225-231.

    Article  Google Scholar 

  • Penas, J., S. Barrios, J. Bobo-Pinilla, J. Lorite & M.M. Martínez-Ortega. 2016. Designing conservation strategies to preserve the genetic diversity of Astragalus edulis Bunge, an endangered species from western Mediterranean region. PeerJ 4: e1474.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pickart, A.J., A.E. Hiss & A.W. Enberg. 1992. Return from extinction: recovery of the Humboldt milk-vetch. In Proceedings of the symposium on biodiversity of northwest California. Santa Rosa, California, October 28-30, pp 255-261.

  • Platt, W.J., G.R. Hill & S. Clark. 1974. Seed production in a prairie legume (Astragalus canadensis L.). Oecologia 17: 55-63.

    Article  PubMed  Google Scholar 

  • Podlech D. 1990. Die Typifizierung der altweltlichen Sektionen der Gattung Astragalus L. (Leguminosae). Mitteilungen der Botanischen Staatssammlung München 29: 461–494.

    Google Scholar 

  • Podlech D. 1991. The systematics of the annual species of the genus Astragalus L. (Leguminosae). Flora et Vegetatio Mundi 9: 1–8.

    Google Scholar 

  • Podlech D. 1994. Revision der altweltlichen anuellen Arten der Gattung Astragalus L. (Leguminosae). Sendtnera 2: 39–170.

    Google Scholar 

  • Podlech, D. & S. Zarre. 2013. A taxonomic revision of the genus Astragalus L. (Leguminosae) in the Old World. Vienna: Naturhistorisches Museum.

  • POWO. 2019. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Published on the internet. http://www.plantsoftheworldonline.org/ [accessed 18th November 2020]

  • Ralphs, M.H. & E.H. Cronin. 1987. Locoweed seed in soil: density, longevity, germination, and viability. Weed Science 35: 792-795.

    Article  Google Scholar 

  • Ralphs, M.H. & V.L. Bagley. 1988. Population cycles of Wahweap milkvetch on the Henry Mountains and seed reserve in the soil. The Great Basin Naturalist 48: 541-547.

    Google Scholar 

  • Ralphs, M.H., J.A. Pfister, S.L. Welsh, J.D. Graham, J. Purvines, D.T. Jensen & L.F. James. 2003. Locoweed population cycles. Rangelands 25: 14-18.

    Article  Google Scholar 

  • Ranjbar, M. & B. Mahmoudian. 2015. An overview on cytogenetics of the genus Astragalus subgenus Hypoglottis (Fabaceae). Caryologia 68: 109-124.

    Article  Google Scholar 

  • Ranjbar, M., A. Assadi & R. Karamian. 2010. Systematic study of Astragalus chrysostachys Boiss. (Fabaceae) in Iran, with the description of a new species. Annalen des Naturhistorischen Museums in Wien. Serie B für Botanik und Zoologie 112: 221-237.

    Google Scholar 

  • Reynolds, R.J.B., R.R. Jones, J. Heiner, K.M. Crane & E.A.H. Pilon-Smits. 2020. Effects of selenium hyperaccumulators on soil selenium distribution and vegetation properties. American Journal of Botany 107: 970-982.

    Article  CAS  PubMed  Google Scholar 

  • Riahi, M. & S. Zarre. 2009. Seed development in Astragalus cemerinus and A. ruscifolius (Fabaceae), and its systematic implications. Acta Biologica Cracoviensia, Series Botanica 51: 111-117.

    Google Scholar 

  • Riahi, M., S. Zarre, A. Chehregani & B. Shahsavan-Behboudi. 2003. Seed development in two species of medifixed hairy Astragalus (Fabaceae). Flora 198: 211-219.

    Article  Google Scholar 

  • Richards, K.W. 1986. Pollination requirements of cicer milkvetch, Astragalus cicer L. Rangeland Ecology & Management 39: 457-459.

    Article  Google Scholar 

  • Richards, K.W. 1987. Diversity, density, efficiency, and effectiveness of pollinators of cicer milkvetch, Astragalus cicer L. Canadian Journal of Zoology 65: 2168-2176.

    Article  Google Scholar 

  • Rodríguez-Riano, T., A. Ortega-Olivencia & J.A. Devesa. 1999. Types of androecium in the Fabaceae of SW Europe. Annals of Botany 83: 109-116.

    Article  Google Scholar 

  • Rominger, K.R., S.E. Meyer, R. Van Buren & A.B. Searle. 2019. Phenological patterns in the desert spring ephemeral Astragalus holmgreniorum Barneby (Fabaceae). Western North American Naturalist 79: 308-322.

    Article  Google Scholar 

  • Rosbakh, S., E. Pacini, M. Nepi & P. Poschlod. 2018. An unexplored side of regeneration niche: seed quantity and quality are determined by the effect of temperature on pollen performace. Frontiers in Plant Science 9: 1036.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rose, A.L. 1981. Vesicular-arbuscular endomycorrhizal associations of some desert plants of Baja California. Canadian Journal of Botany 59: 1056-1060.

    Article  Google Scholar 

  • Rundel, P.W., B. Prigge & M.R. Sharifi. 2007. The effect of amount and frequency of precipitation on seedling establishment and survival of Lane Mountain milkvetch (Astragalus jaegerianus Munz). Final report. U.S. Army Research Office, P. O. Box 12211, Research Triangle Park, NC.

  • Rundel, P.W., T.R. Huggins, B.A. Prigge & M. Rasoul Sharifi. 2012. Community dynamics and soil seed bank ecology of the Lane Mountain milkvetch (Astagalus jaegerianus Munz). Final report. U.S. Army Research Office. P. O. Box 12211. Research Triangle Park, NC.

  • Rundel, P.W., T.R. Huggins, B.A. Prigge & M. Rasoul Sharifi. 2015. Rarity in Astragalus: a California perspective. Aliso 33: 111-120.

    Article  Google Scholar 

  • Sanderson, M.J. & M.F. Wojciechowski. 2000. Improved bootstrap confidence limits in large-scale phylogenies, with an example from Neo-Astragalus (Leguminosae). Systematic Biology 49: 671-685.

    Article  CAS  PubMed  Google Scholar 

  • Sankary, M.N. 1971. Comparative plant ecology of two Mediterranean-type arid areas in Syria and California, with emphasis on the autecology of 20 dominant species. Ph.D. dissertation, University of California, Davis.

  • Sankary, M.N. & M.G. Barbour. 1980. Germination, growth, and water relations of Astragalus lentiginosus var. nigricalycis (Fabaceae). Madroño 27: 90-96.

    Google Scholar 

  • Scheetz, J.G. 1971. Estimates of cross- and self-fertility of cicer milkvetch (Astragalus cicer L.). M.Sc. thesis, Montana State University, Bozeman.

  • Scherson, R.A., R. Vidal & M.J. Sanderson. 2008. Phylogeny, biogeography, and rates of diversification of New World Astragalus (Leguminosae) with an emphasis on South American radiations. American Journal of Botany 95: 1030-1039.

    Article  PubMed  Google Scholar 

  • Schurr, L., L. Affre, F. Flacher, T. Tatoni, L.L.M. Pecheux & B. Geslin. 2019. Pollination insights for the conservation of a rare threatened plant species, Astragalus tragacantha (Fabaceae). Biodiversity and Conservation 28: 1389-1409.

    Article  Google Scholar 

  • Schwegman, J.A. 1998. Some aspects of the life history and population dynamics of Astragalus tennesseensis A. Gray in Illinois. Castanea 63, 63-67.

    Google Scholar 

  • Searle, A.B. 2011. Reproductive success and soil seed bank characteristics of Astragalus ampullarioides and A. holmgreniorum (Fabaceae): two rare endemics of southwestern Utah. M. S. thesis. Brigham Young University, Provo, UT.

  • Segura, F., J.J. Martínez-Sánchez, M. Aguado, J.A. Franco & M.J. Vicente. 2014. Could recently locally extinct population patches of Astragalus nitidiflorus regenerate from the soil seed bank? Journal of Arid Environments 110: 75-78.

    Article  Google Scholar 

  • Selyutina, I.Y.E., E.S. Konichenko, O.V. Dorogina & D.V. Sandanov. 2016. Genetic diversity of the endangered endemic milkvetch Astragalus sericeocanus Gontsch., Fabaceae from the Lake Baikal region. Biochemical Systematics and Ecology 68: 163-169.

    Article  CAS  Google Scholar 

  • Sharifi, J.A.B.E.R., A.A. Shahmoradi & A.A. Imani. 2010. An ecological study on some characteristics of Astragalus brachyodontus in rangelands of Ardabil province, Iran. Iranian Journal of Range and Desert Research 17: 221-233. (in Persian)

    Google Scholar 

  • Shearer, G., D.H. Kohl, R.A. Virginia, B.A. Bryon, J.L. Skeeters, E.T. Nilsen, M.R. Sharifi & P.W. Rundel. 1983. Estimates of N2-fixation from variation in the natural abundance of 15N in Sonoran Desert ecosystems. Oecologia 56: 365-373.

    Article  CAS  PubMed  Google Scholar 

  • Shefferson, R.P. 2009. The evolutionary ecology of vegetative dormancy in mature herbaceous perennial plants. Journal of Ecology 97: 1000-1009.

    Article  Google Scholar 

  • Shemetova, T., A. Erst, W. Wang, K. Xiang, C. Vural & Z. Aytac. 2018. Seed morphology of the genus Astragalus L. from North Asia. Turkish Journal of Botany 42: 710-721.

    Article  CAS  Google Scholar 

  • Shi, Z.Y., G. Feng, P. Christie & X.L. Li. 2006. Arbuscular mycorrhizal status of spring ephemerals in the desert ecosystem of Junggar Basin, China. Mycorrhiza 16: 269-275.

    Article  CAS  PubMed  Google Scholar 

  • Shim, S.I. & B.H. Kang. 2004. Ecophysiology of seed germination in Chinese milk vetch (Astragalus sinicus L.). Korean Journal of Crop Science 49: 19-24.

    Google Scholar 

  • Smoliak, S., A. Johnston & M.R. Hanna. 1972. Germination and seedling growth of alfalfa, sainfoin, and cicer milkvetch. Canadian Journal of Plant Science 52: 757-762.

    Article  Google Scholar 

  • Soltani, E., J.M. Baskin, C.C. Baskin & F. Benakashani. 2020. A meta-analysis of the effects of treatments used to break dormancy in seeds of the megagenus Astragalus (Fabaceae). Seed Science Research 30: 224-233.

    Article  CAS  Google Scholar 

  • Song, B., S. Niu & S. Wan. 2016. Precipitation regulates plant gas exchange and its long-term response to climate change in a temperate grassland. Journal of Plant Ecology 9: 531-541.

    Article  Google Scholar 

  • Spellenberg, R. 1976. Chromosome numbers and their cytotaxonomic significance for North American Astragalus (Fabaceae). Taxon 25: 463-476.

    Article  Google Scholar 

  • Spellenberg, R. 1993. Astragalus. pp. 583-605. In J.C. Hickman (ed.), The Jepson Manual. University of California Press, Berkeley.

    Google Scholar 

  • Stark, K.E., A. Arsenault & G.E. Bradfield. 2006. Soil seed banks and plant community assembly following disturbance by fire and logging in interior Douglas-fir forests of south-central British Columbia. Canadian Journal of Botany 84: 1548-1560.

    Article  Google Scholar 

  • Strickler, G.S. & P.J. Edgerton. 1976. Emergent seedlings from coniferous litter and soil in eastern Oregon. Ecology 57: 801-807.

    Article  Google Scholar 

  • Sugden, E.A. 1985. Pollinators of Astragalus monoensis Barneby (Fabaceae): new host records; potential impact of sheep grazing. The Great Basin Naturalist 45: 299-312.

    Google Scholar 

  • Symonides, E. 1986. Seed bank in old-field successional ecosystems. Ekologia Polska 34: 3–29.

    Google Scholar 

  • Syvertsen, J.P., G.L. Nickell, R.W. Spellenberg & G.L. Cunningham. 1976. Carbon reduction pathways and standing crop in three Chihuahuan Desert plant communities. The Southwestern Naturalist 21: 311-320.

    Article  Google Scholar 

  • Szentesi, Á. & T. Jermy. 1995. Predispersal seed predation in leguminous species: seed morphology and bruchid distribution. Oikos 73: 23-32.

    Article  Google Scholar 

  • Tanner, D.A., C. Clark & J.P. Pitts. 2013. Pollination biology of Astragalus phoenix (Fabaceae) with notes on the natural history of its pollinator, Anthophora porterae (Hymenoptera: Apidae). Western North American Naturalist 73: 373-382.

    Article  Google Scholar 

  • Tekpinar, A., S.K. Erkul, Z. Aytac & Z. Kaya. 2016. Phylogenetic relationships between Oxytropis DC. and Astragalus L. species native to an Old World diversity center inferred from nuclear ribosomal ITS and plastid matK gene sequences. Turkish Journal of Biology 40: 250-263.

    Article  CAS  Google Scholar 

  • Templeton, A.R. & D.A. Levin. 1979. Evolutionary consequences of seed pools. The American Naturalist 114: 232-249.

    Article  Google Scholar 

  • Tepedino, V.J. 2005. Reproduction and pollination of two rare species of Astragalus from Washington County, southern Utah: A. holmgreniorum and A. ampullarioides. USDA-ARS Bee Biology and Systematics Laboratory, Department of Biology, Utah State University, Logan.

  • The Plant List. 2013. Version 1.1. Published on the Internet; http://www.theplantlist.org/ (accessed 18th November 2020).

  • Tian, C., Shi, Z., Chen, Z. & Feng, G. 2006. Arbusculr mycorrhizal associations in the Gurbantunggut Desert. Chinese Science Bulletin 51: 140-146.

    Article  Google Scholar 

  • Townsend, C.E. 1971. Self-compatibility studies with Astragalus cicer L. Crop Science 11: 769-770.

    Article  Google Scholar 

  • Townsend, C.E. 1972. Comparison of S1 and open-pollination progenies of Astragalus cicer L. for certain agronomic characters. Crop Science 12: 793-795.

    Article  Google Scholar 

  • Townsend, C.E. 1981. Vernalization and photoperiod requirements for maximum flowering of cicer milkvetch. Crop Science 21: 917-921.

    Article  Google Scholar 

  • Townsend, C.E. & W.J. McGinnies. 1973. Factors influencing vegetative growth and flowering in Astragalus cicer L. Crop Science 13: 262-264.

    Article  Google Scholar 

  • Travis, S.E., J. Maschinski & P. Keim. 1996. An analysis of genetic variation in Astragalus cremnophylax var. cremnophylax, a critically endangered plant, using AFLP markers. Molecular Ecology 5: 735–745.

    Article  CAS  PubMed  Google Scholar 

  • Trelease, S.F. & H.M. Trelease. 1937. Toxicity to insects and mammals of foods containing selenium. American Journal of Botany 24: 448-451.

    Article  CAS  Google Scholar 

  • Tutin, T.G., V.H. Heywood, N.A. Burges, D.M. Moore, D.H. Valentine, S.M. Walters & D.A. Webb. 1968. Flora Europaea. Volume 2. Rosaceae to Umbelliferae. Cambridge University Press, Cambrige.

  • Ueki, C. & I. Suetsugu. 1958. The identification of hard seeds in some leguminous forage crops. I. Genge (Astragalus sinicus L.). Proceeding of the International. Seed Testing Association 23: 69-72.

    Google Scholar 

  • Van Buren, R. & K.T. Harper. 2003. Demographic and environmental relations of two rare Astragalus species endemic to Washington County, Utah: Astragalus holmgreniorum and A. ampullarioides. Western North American Naturalist 63: 236-243.

    Google Scholar 

  • Vural, C., M. Ekici, H. Akan & Z. Aytaç. 2008. Seed morphology and its systematic implications for genus Astragalus L. sections Onobrychoidei DC., Uliginosi Gray and Ornithopodium Bunge (Fabaceae). Plant Systematics and Evolution 274: 255-263.

    Article  Google Scholar 

  • Walker, G.F. & A.E. Metcalf. 2008. Genetic variation in the endangered Astragalus jaegerianus (Fabaceae, Papilionoideae): a geographically restricted species. Bulletin, Southern California Academy of Sciences 107: 158-177.

    Article  Google Scholar 

  • Wall, W.A., N.A. Douglas, W.A. Hoffmann, T.R. Wentworth, J.B. Gray, Q.Y.J. Xiang, B.K. Knaus & M.G. Hohmann. 2014. Evidence of population bottleneck in Astragalus michauxii (Fabaceae), a narrow endemic of the southeastern United States. Conservation Genetics 15: 153-164.

    Article  Google Scholar 

  • Walters, C., L.M. Wheeler & J.M. Grotenhuis. 2005. Longevity of seeds stored in a genebank: species characteristics. Seed Science Research 15: 1-20.

    Article  CAS  Google Scholar 

  • Wang, A., W. Wujisguleng, Y. Liu, Y. Liu & C. Long. 2013. Isolation and characterization of polymorphic microsatellite loci for the valuable medicinal plant Astragalus mongholicus. Open Journal of Genetics 3: 89–92.

    Article  Google Scholar 

  • Wang, N., J.Y. Jiao, Y.F. Jia & D.L. Wang. 2011. Seed persistence in the soil on eroded slopes in the hilly-gullied Loess Plateau region, China. Seed Science Research 21: 295-304.

    Article  Google Scholar 

  • Wang, R.Z., X.Q. Liu & Y. Bai. 2006. Photosynthetic and morphological functional types for native species from mixed prairie in Southern Saskatchewan, Canada. Photosynthetica 44: 17-25.

    Article  CAS  Google Scholar 

  • Watrous, K.M. & J.H. Cane. 2011. Breeding biology of the threadstalk milkvetch, Astragalus filipes (Fabaceae), with a review of the genus. The American Midland Naturalist 165: 225-241.

    Article  Google Scholar 

  • Weeks, S.C. 2004. Factors limiting growth in Astragalus michauxii (sandhills milk-vetch). Ph.D. dissertation. North Carolina State University, Raleigh.

  • Wells, G.G. 2006. Life history and reproductive biology of Astragalus crassicarpus var. trichocalyx. M.S. thesis. Southern Illinois University Edwardsville,

  • Wiens, D. 1984. Ovule survivorship, brood size, life history, breeding systems, and reproductive success in plants. Oecologia 64: 47-53.

    Article  PubMed  Google Scholar 

  • Wiens, D., L. Allphin, D.H. Mansfield & G. Thackray. 2002. Developmental failure and loss of reproductive capacity as a factor in extinction: a nine-year study of Dedeckera eurekensis (Polygonaceae). Aliso 21: 55-63.

    Article  Google Scholar 

  • Wilson, J.K. & C.-H. Chin. 1947. Symbiotic studies with isolates from nodules of species of Astragalus. Soil Science 63: 119-128.

    Article  CAS  Google Scholar 

  • Wojciechowski M.F., M.J. Sanderson, B.G. Baldwin & Donoghue M.J. 1993. Monophyly of aneuploid Astragalus (Fabaceae): evidence from nuclear ribosomal DNA internal transcribed spacer sequences. American Journal of Botany 80: 711–722.

    Article  CAS  Google Scholar 

  • Wojciechowski M.F., M.J. Sanderson & J.M. Hu. 1999. Evidence on the monophyly of Astragalus (Fabaceae) and its major subgroups based on nuclear ribosomal DNA, ITS and chloroplast DNA trnL introndata. Systematic Botany, 24, 409-437.

    Article  Google Scholar 

  • Wojciechowski, M.F. 2005. Astragalus (Fabaceae): a molecular phylogenetic perspective. Brittonia 57: 382–396.

    Article  Google Scholar 

  • Wu, M., X. Shi & D. Tan. 2019. Development of SSR markers for Astragalus lehmannianus, a vulnerable species from northwestern China. Applications in Plant Sciences 7: e11297.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, B.C., X.P. Deng, S.Q. Zhang & L. Shan. 2010. Biomass partition, leaf gas exchange and water relations of alfalfa and milkvetch seedlings in response to soil drying. Photosynthetica 48: 481-487.

    Article  Google Scholar 

  • Youtie, B.A. & R.F. Miller. 1986. Insect predation on Astragalus filipes and A. purshii seeds. Northwest Science 60: 42-46.

    Google Scholar 

  • Zalamea, P.-C., J.W. Dalling, C. Sarmiento, A.E. Arnold, C. Delevich, M.A. Berhow, A. Ndobegang, S. Gripenberg & A.S. Davis. 2018. Dormancy-defense syndromes and tradeoffs between physical and chemical defenses in seeds of pioneer species. Ecology 99: 1988-1998.

    Article  PubMed  Google Scholar 

  • Zarre, S., Z. Khodaei, Z. Karamali, V. Niknam & M. Mirmasoumi. 2007. Isoenzyme variation patterns and species concept in Astragalus gossypinus and Astragalus persicus complexes (Fabaceae) in Iran. Biochemical Systematics and Ecology 35: 757-763.

    Article  CAS  Google Scholar 

  • Zhang, D.Q., J. Yang & B. Jiang. 2013. Isolation and characterization of 23 microsatellite loci in Astragalus camptodontus (Leguminosae), a traditional medicinal plant in Yunnan province. Biochemical Systematics and Ecology 50: 448–451.

    Article  CAS  Google Scholar 

  • Zhao, B., A. Trouvelot, S. Gianinazzi & V. Gianinazzi-Peasron. 1997. Influence of two legume species on hyphal production and activity of two arbuscular mycorrhizal fungi. Mycorrhiza 7: 179-185.

    Article  Google Scholar 

  • Ziegler, H., K.H. Batanouny, N. Sankhla, O.P. Vyas & W. Stichler. 1981. The photosynthetic pathway types of some desert plants from India, Saudi Arabia, Egypt, and Iraq. Oecologia 48: 93-99.

    Article  CAS  PubMed  Google Scholar 

  • Zinn, K.E., M. Tunc-Ozdemir & J.F. Harper. 2010. Temperature stress and plant sexual reproduction: uncovering the weaket links. Journal of Experimental Botany 61: 1959-1968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Agronomy and Plant Breeding Sciences, College of Aburaihan, University of Tehran, Tehran, Iran

    Elias Soltani & Fatemeh Benakashani

  2. Department of Biology, University of Kentucky, Lexington, KY, 40506-0225, USA

    Jerry M. Baskin & Carol C. Baskin

  3. Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, 40546-0312, USA

    Carol C. Baskin

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Soltani, E., Benakashani, F., Baskin, J.M. et al. Reproductive biology, ecological life history/demography and genetic diversity of the megagenus Astragalus (Fabaceae, Papilionoideae). Bot. Rev. 87, 55–106 (2021). https://doi.org/10.1007/s12229-020-09243-x

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