Soil seed bank

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The soil seed bank is the natural storage of seeds, often dormant, within the soil of most ecosystems. [1] The study of soil seed banks started in 1859 when Charles Darwin observed the emergence of seedlings using soil samples from the bottom of a lake. The first scientific paper on the subject was published in 1882 and reported on the occurrence of seeds at different soil depths. [2] Weed seed banks have been studied intensely in agricultural science because of their important economic impacts; other fields interested in soil seed banks include forest regeneration and restoration ecology.

Contents

Henry David Thoreau wrote that the contemporary popular belief explaining the succession of a logged forest, specifically to trees of a dissimilar species to the trees cut down, was that seeds either spontaneously generated in the soil, or sprouted after lying dormant for centuries. However, he dismissed this idea, noting that heavy nuts unsuited for distribution by wind were distributed instead by animals. [3]

The ecological importance of seed bank

The seed bank is one of the key factors for the persistence and density fluctuations of plant populations, especially for annual plants. [4] Perennial plants have vegetative propagules to facilitate forming new plants, migration into new ground, or reestablishment after being top-killed, which are analogus to seed bank in their persistence ability under disturbance. These propagules are collectively called the 'soil bud bank', and include dormant and adventitious buds on stolons, rhizomes, and bulbs. Moreover, the term soil diaspore bank can be used to include non-flowering plants such as ferns and bryophytes.[ citation needed ]

Soil seed bank is significant breeding source for vegetation restoration [5] and species-rich vegetation restoration, [6] as they provide memories of past vegetation and represent the structure of future population. [6] Moreover the composition of seed bank is often more stable than the vegetation to environmental changes, [7] although a chronic N deposition can deplete it. [8] [9] In many systems, the density of the soil seed bank is often lower than the vegetation, [4] and there are a large differences in species composition of the seed bank and the composition of the aboveground vegetation. [10] [11] [12] Additionally, it is a key point that the relationship between soil seed bank and original potential to measure the revegetation potential. [13] [14] In endangered habitats, such as mudflats, rare and critically endangered species may be present in high de, the composition of the seed bank is often more stable than the vegetation to environmental changes[7][7], [15]

Soil seed banks are a crucial part of the rapid re-vegetation of sites disturbed by wildfire, catastrophic weather, agricultural operations, and timber harvesting, a natural process known as secondary succession. Soil seed banks are often dominated by pioneer species, those species that are specially adapted to return to an environment first after a disturbance. [16] Forest ecosystems and wetlands contain a number of specialized plant species forming persistent soil seed banks.[ citation needed ]

The absence of a soil seed bank impedes the establishment of vegetation during primary succession, while presence of a well-stocked soil seed bank permits rapid development of species-rich ecosystems during secondary succession.[ citation needed ]

Seed longevity

Dried lotus seeds DriedLotusSeeds.jpg
Dried lotus seeds

Many taxa have been classified according to the longevity of their seeds in the soil seed bank. Seeds of transient species remain viable in the soil seed bank only to the next opportunity to germinate, while seeds of persistent species can survive longer than the next opportunity—often much longer than one year. Species with seeds that remain viable in the soil longer than five years form the long-term persistent seed bank, while species whose seeds generally germinate or die within one to five years are called short-term persistent. A typical long-term persistent species is Chenopodium album (Lambsquarters); its seeds commonly remain viable in the soil for up to 40 years and in rare situations perhaps as long as 1,600 years. [17] A species forming no soil seed bank at all (except the dry season between ripening and the first autumnal rains) is Agrostemma githago (Corncockle), which was formerly a widespread cereal weed.[ citation needed ]

Longevity of seeds is very variable and depends on many factors. Seeds buried more deeply tend to be capable of lasting longer. [18] However, few species exceed 100 years. [19] In typical soils the longevity of seeds can range from nearly zero (germinating immediately when reaching the soil or even before) to several hundred years. Some of the oldest still-viable seeds were those of Lotus (Nelumbo nucifera) found buried in the soil of a pond; these seeds were estimated by carbon dating to be around 1,200 years old. [20] One cultivar of date palm, the Judean date palm, successfully sprouted in 2008 after accidental storage for 2,000 years. [21]

The famous seed longevity experiments

One of the longest-running soil seed viability trials was started in Michigan in 1879 by James Beal. The experiment involved the burying of 20 bottles holding 50 seeds from 21 species. Every five years, a bottle from every species was retrieved and germinated on a tray of sterilized soil which was kept in a growth chamber. Later, after responsibility for managing the experiment was delegated to caretakers, the period between retrievals became longer. In 1980, more than 100 years after the trial was started, seeds of only three species were observed to germinate: moth mullein (Verbascum blattaria), common mullein (Verbascum thapsus) and common mallow (Malva neglecta). [22] Several other experiments have been conducted to determine the long-term longevity of seeds in soil seed banks.

Soil seed bank longevity of seeds in experimental conditions
SpeciesTimeComments
Verbascum blattaria At least 142 years [23]
Verbascum thapsus At least 100 years [22]
Malva neglecta At least 100 years
Oenothera biennis 80 years [24] 10% of seeds sprouted after the 80-year mark
Rumex crispus 80 yearsOnly 2% of seeds survived to this point. [24]
Datura stramonium At least 39 yearsOver 90 percent germination rate was reported [25]
Phytolacca americana At least 39 years80-90 percent germination rate was reported [25]
Solanum nigrum At least 39 yearsOver 80 percent germination rate was reported [25]
Robinia pseudoacacia At least 39 years
Ambrosia artemisiifolia At least 39 years
Potentilla norvegica At least 39 years
Onopordum acanthium At least 39 years
Rudbeckia hirta At least 39 years
Cuscuta polygonorum At least 39 years
Lespedeza frutescens At least 39 years
Convolvulus sepium At least 39 years
Ipomoea lacunosa At least 39 years
Verbena hastata At least 39 years
Verbena urticifolia At least 39 years
Nicotiana tabacum At least 39 years
Arctium lappa At least 39 yearsOnly 1 percent germination was reported.
Boehmeria nivea At least 39 years
Setaria verticillata At least 39 years
Trifolium pratense At least 39 years
Rumex obtusifolius At least 39 years
Rumex salicifolius At least 39 years
Chenopodium album At least 39 years
Chenopodium hybridum At least 39 years
Abutilon theophrasti At least 39 years
Leucanthemum vulgare At least 39 years
Hibiscus militaris At least 39 years
Hypericum hypericoides At least 39 years
Sporobolus cryptandrus At least 39 years
Polygonum scandens At least 39 yearsGermination rate was very low throughout the experiment.
Poa pratensis At least 39 years
Setaria viridis At least 39 years
Phalaris arundinacea 30 yearsOnly 1 percent of seed survived.
Portulaca oleracea 30 years38 percent of the most deeply buried seeds were viable at 21 years, 1 percent of more shallowly buried seeds are reported sprouting after the 30 year mark.
Polygonum pensylvanicum 30 years
Polygonum persicaria 30 years
Cassia marilandica 30 years
Thlaspi arvense 30 years
Trifolium hybridum 30 years
Ambrosia trifida 21 years
Brassica nigra 21 years
Dracocephalum parviflorum 24.7 years [26]
Rorippa islandica 24.7 years
Matricaria discoidea 24.7 years
Polygonum aviculare 24.7 years
Helianthus annuus 17 years [18]
Setaria parviflora 17 years
Cirsium arvense 17 years
Cirsium flodmanii 17 years
Ipomoea hederacea 17 years
Persicaria amphibia 17 years
Amaranthus tuberculatus 17 years
Solanum sarrachoides 17 years
Ambrosia grayii 17 yearsOnly 1% of seed germinated.
Bassia scoparia 17 yearsOnly 1% of seed germinated.
Echinochloa crus-galli 17 yearsOnly 1% of seed germinated.
Amaranthus retroflexus 12 years [18]
Pyrus calleryana At least 11 years [27]

Other studies

Species of Striga (witchweed) are known to leave some of the highest seed densities in the soil compared to other plant genera; this is a major factor that aids their invasive potential. [28] Each plant has the capability to produce between 90,000 and 450,000 seeds, although a majority of these seeds are not viable. [29] It has been estimated that only two witchweeds would produce enough seeds required to refill a seed bank after seasonal losses. [30] Before the advent of herbicides, a good example of a persistent seed bank species was Papaver rhoeas , sometimes so abundant in agricultural fields in Europe that it could be mistaken for a crop.[ citation needed ]

Studies on the genetic structure of Androsace septentrionalis populations in the seed bank compared to those of established plants showed that diversity within populations is higher below ground than above ground.[ citation needed ]

Related Research Articles

<span class="mw-page-title-main">Annual plant</span> Plant which completes its life cycle within one growing season and then dies

An annual plant is a plant that completes its life cycle, from germination to the production of seeds, within one growing season, and then dies. Globally, only 6% of all plant species and 15% of herbaceous plants are annuals. The annual life cycle has independently emerged in over 120 different plant families throughout the entire angiosperm phylogeny.

<span class="mw-page-title-main">Seed</span> Embryonic plant enclosed in a protective outer covering

In botany, a seed is a plant embryo and food reserve enclosed in a protective outer covering called a seed coat (testa). More generally, the term "seed" means anything that can be sown, which may include seed and husk or tuber. Seeds are the product of the ripened ovule, after the embryo sac is fertilized by sperm from pollen, forming a zygote. The embryo within a seed develops from the zygote and grows within the mother plant to a certain size before growth is halted.

<span class="mw-page-title-main">Seed bank</span> Backup seed storage

A seed bank stores seeds to preserve genetic diversity; hence it is a type of gene bank. There are many reasons to store seeds. One is to preserve the genes that plant breeders need to increase yield, disease resistance, drought tolerance, nutritional quality, taste, etc. of crops. Another is to forestall loss of genetic diversity in rare or imperiled plant species in an effort to conserve biodiversity ex situ. Many plants that were used centuries ago by humans are used less frequently now; seed banks offer a way to preserve that historical and cultural value. Collections of seeds stored at constant low temperature and low moisture are guarded against loss of genetic resources that are otherwise maintained in situ or in field collections. These alternative "living" collections can be damaged by natural disasters, outbreaks of disease, or war. Seed banks are considered seed libraries, containing valuable information about evolved strategies to combat plant stress, and can be used to create genetically modified versions of existing seeds. The work of seed banks often span decades and even centuries. Most seed banks are publicly funded and seeds are usually available for research that benefits the public.

<span class="mw-page-title-main">Germination</span> Process by which an organism grows from a spore or seed

Germination is the process by which an organism grows from a seed or spore. The term is applied to the sprouting of a seedling from a seed of an angiosperm or gymnosperm, the growth of a sporeling from a spore, such as the spores of fungi, ferns, bacteria, and the growth of the pollen tube from the pollen grain of a seed plant.

<span class="mw-page-title-main">Weed control</span> Botanical component of pest control for plants

Weed control is a type of pest control, which attempts to stop or reduce growth of weeds, especially noxious weeds, with the aim of reducing their competition with desired flora and fauna including domesticated plants and livestock, and in natural settings preventing non native species competing with native species.

<i>Bromus tectorum</i> Species of grass

Bromus tectorum, known as downy brome, drooping brome or cheatgrass, is a winter annual grass native to Europe, southwestern Asia, and northern Africa, but has become invasive in many other areas. It now is present in most of Europe, southern Russia, Japan, South Africa, Australia, New Zealand, Iceland, Greenland, North America and western Central Asia. In the eastern US B. tectorum is common along roadsides and as a crop weed, but usually does not dominate an ecosystem. It has become a dominant species in the Intermountain West and parts of Canada, and displays especially invasive behavior in the sagebrush steppe ecosystems where it has been listed as noxious weed. B. tectorum often enters the site in an area that has been disturbed, and then quickly expands into the surrounding area through its rapid growth and prolific seed production.

<i>Onopordum acanthium</i> Species of flowering plant in the daisy family Asteraceae

Onopordum acanthium is a flowering plant in the family Asteraceae. It is native to Europe and Western Asia from the Iberian Peninsula east to Kazakhstan, and north to central Scandinavia, and widely naturalised elsewhere, with especially large populations present in the United States and Australia. It is a vigorous biennial plant with coarse, spiny leaves and conspicuous spiny-winged stems.

<span class="mw-page-title-main">Perennial</span> Plant that lives for more than two years

In botany, a perennial plant or simply perennial is a plant that lives more than two years. The term is often used to differentiate a plant from shorter-lived annuals and biennials. The term is also widely used to distinguish plants with little or no woody growth from trees and shrubs, which are also technically perennials. Notably, it is estimated that 94% of plant species fall under the category of perennials, underscoring the prevalence of plants with lifespans exceeding two years in the botanical world.

<i>Coprosma robusta</i> Species of tree

Coprosma robusta, commonly known as karamū, is a flowering plant in the family Rubiaceae that is endemic to New Zealand. It can survive in many climates, but is most commonly found in coastal areas, lowland forests, or shrublands. Karamū can grow to be around 6 meters tall, and grow leaves up to 12 centimeters long. Karamū is used for a variety of purposes in human culture. The fruit that karamū produces can be eaten, and the shoots of karamū are sometimes used for medical purposes.

<span class="mw-page-title-main">Fire ecology</span> Study of fire in ecosystems

Fire ecology is a scientific discipline concerned with the effects of fire on natural ecosystems. Many ecosystems, particularly prairie, savanna, chaparral and coniferous forests, have evolved with fire as an essential contributor to habitat vitality and renewal. Many plant species in fire-affected environments use fire to germinate, establish, or to reproduce. Wildfire suppression not only endangers these species, but also the animals that depend upon them.

<i>Striga</i> Genus of flowering plants belonging to the broomrape family

Striga, commonly known as witchweed, is a genus of parasitic plants that occur naturally in parts of Africa, Asia, and Australia. It is currently classified in the family Orobanchaceae, although older classifications place it in the Scrophulariaceae. Some species are serious pathogens of cereal crops, with the greatest effects being in savanna agriculture in Africa. It also causes considerable crop losses in other regions, including other tropical and subtropical crops in its native range and in the Americas. The generic name derives from Latin strī̆ga, "witch".

Seed dormancy is an evolutionary adaptation that prevents seeds from germinating during unsuitable ecological conditions that would typically lead to a low probability of seedling survival. Dormant seeds do not germinate in a specified period of time under a combination of environmental factors that are normally conducive to the germination of non-dormant seeds.

<span class="mw-page-title-main">Revegetation</span>

Revegetation is the process of replanting and rebuilding the soil of disturbed land. This may be a natural process produced by plant colonization and succession, manmade rewilding projects, accelerated process designed to repair damage to a landscape due to wildfire, mining, flood, or other cause. Originally the process was simply one of applying seed and fertilizer to disturbed lands, usually grasses or clover. The fibrous root network of grasses is useful for short-term erosion control, particularly on sloping ground. Establishing long-term plant communities requires forethought as to appropriate species for the climate, size of stock required, and impact of replanted vegetation on local fauna. The motivations behind revegetation are diverse, answering needs that are both technical and aesthetic, but it is usually erosion prevention that is the primary reason. Revegetation helps prevent soil erosion, enhances the ability of the soil to absorb more water in significant rain events, and in conjunction reduces turbidity dramatically in adjoining bodies of water. Revegetation also aids protection of engineered grades and other earthworks.

<span class="mw-page-title-main">Oldest viable seed</span> Oldest seed known to have grown into a full plant

There have been several seeds known at different times as the oldest viable seed.

<i>Brassica tournefortii</i> Species of flowering plant

Brassica tournefortii is a species of plant known by the common names Asian mustard, pale cabbage, African mustard, and Sahara mustard, and is well known as an invasive species, especially in California.

<i>Amaranthus tuberculatus</i> Species of flowering plant

Amaranthus tuberculatus, commonly known as roughfruit amaranth, rough-fruited water-hemp, tall waterhemp, or common waterhemp, is a species of flowering plant. It is a summer annual broadleaf with a germination period that lasts several months. Tall waterhemp has been reported as a weed in 40 of 50 U.S. states.

<i>Taeniatherum</i> Genus of grasses

Taeniatherum is a genus of Eurasian and North African plants in the grass family.

<span class="mw-page-title-main">Riparian-zone restoration</span> Ecological restoration of river banks and floodplains

Riparian-zone restoration is the ecological restoration of riparian-zonehabitats of streams, rivers, springs, lakes, floodplains, and other hydrologic ecologies. A riparian zone or riparian area is the interface between land and a river or stream. Riparian is also the proper nomenclature for one of the fifteen terrestrial biomes of the earth; the habitats of plant and animal communities along the margins and river banks are called riparian vegetation, characterized by aquatic plants and animals that favor them. Riparian zones are significant in ecology, environmental management, and civil engineering because of their role in soil conservation, their habitat biodiversity, and the influence they have on fauna and aquatic ecosystems, including grassland, woodland, wetland or sub-surface features such as water tables. In some regions the terms riparian woodland, riparian forest, riparian buffer zone, or riparian strip are used to characterize a riparian zone.

<i>Striga hermonthica</i> Species of flowering plant

Striga hermonthica, commonly known as purple witchweed or giant witchweed, is a hemiparasitic plant that belongs to the family Orobanchaceae. It is devastating to major crops such as sorghum and rice. In sub-Saharan Africa, apart from sorghum and rice, it also infests maize, pearl millet, and sugar cane.

<i>Salix alaxensis</i> Species of flowering plant

Salix alaxensis is a species of flowering plant in the willow family known by the common names Alaska willow and feltleaf willow. It is native to northern North America, where it occurs throughout Alaska and northwestern Canada.

References

  1. ↑ Jack Dekker (1997). "The Soil Seed Bank". Agronomy Department, Iowa State University. Retrieved 10 December 2015.
  2. ↑ Christoffoleti, P. J.; Caetano, R. S. X. (July 17, 1998). "Soil seed banks". Scientia Agricola. 55: 74–78. doi: 10.1590/S0103-90161998000500013 – via SciELO.
  3. ↑ Mcartney, Eugene S. (1931). "Forest Succession and Folklore". The Classical Weekly. 25 (6): 47–48. doi:10.2307/4389644. JSTOR   4389644.
  4. 1 2 DeMalach, Niv; Kigel, Jaime; Sternberg, Marcelo (2023-03-01). "Contrasting dynamics of seed banks and standing vegetation of annuals and perennials along a rainfall gradient". Perspectives in Plant Ecology, Evolution and Systematics. 58: 125718. arXiv: 2301.12696 . doi:10.1016/j.ppees.2023.125718. ISSN   1433-8319.
  5. ↑ Lu, Z.J., Li, L.F., Jiang, M.X., Huang, H.D., and Bao, D.C., Can the soil seed bank contribute to revegetation of the drawdown zone in the Three Gorges reservoir region? Plant Ecol., 2010, vol. 209, no. 1, pp. 153–165.
  6. 1 2 Fisher, Judith L.; Loneragan, William A.; Dixon, Kingsley; Veneklaas, Erik J. (2009-02-01). "Soil seed bank compositional change constrains biodiversity in an invaded species-rich woodland". Biological Conservation. 142 (2): 256–269. doi:10.1016/j.biocon.2008.10.019. ISSN   0006-3207.
  7. ↑ DeMalach, Niv; Kigel, Jaime; Sternberg, Marcelo (March 2021). Dalling, James (ed.). "The soil seed bank can buffer long‐term compositional changes in annual plant communities". Journal of Ecology. 109 (3): 1275–1283. arXiv: 2010.15693 . doi:10.1111/1365-2745.13555. ISSN   0022-0477.
  8. ↑ Eskelinen, Anu; Elwood, Elise; Harrison, Susan; Beyen, Eva; Gremer, Jennifer R. (December 2021). "Vulnerability of grassland seed banks to resource‐enhancing global changes". Ecology. 102 (12). doi: 10.1002/ecy.3512 . ISSN   0012-9658.
  9. ↑ Basto, Sofía; Thompson, Ken; Phoenix, Gareth; Sloan, Victoria; Leake, Jonathan; Rees, Mark (2015-02-04). "Long-term nitrogen deposition depletes grassland seed banks". Nature Communications. 6 (1): 6185. doi: 10.1038/ncomms7185 . ISSN   2041-1723.
  10. ↑ Sanderson, M.A., Goslee, S.C., Klement, K.D., and Soder, K.J., Soil seed bank composition in pastures of diverse mixtures of temperate forages, Agron. J., 2007, vol. 99, no. 6, p. 1514.
  11. ↑ White, S.; Bork, E.; Karst, J.; Cahill, J. (2012-11-21). "Similarity between grassland vegetation and seed bank shifts with altered precipitation and clipping, but not warming". Community Ecology. 13 (2): 129–136. doi:10.1556/comec.13.2012.2.1. ISSN   1588-2756.
  12. ↑ Hopfensperger, K.N., A review of similarity between seed bank and standing vegetation across ecosystems, Oikos, 2007, vol. 116, pp. 1438–1448.
  13. ↑ Lu, Z.J., Li, L.F., Jiang, M.X., Huang, H.D., and Bao, D.C., Can the soil seed bank contribute to revegetation of the drawdown zone in the Three Gorges reservoir region? Plant Ecol., 2010, vol. 209, no. 1, pp. 153–165
  14. ↑ Wang, Yongcui; Jiang, Deming; Toshio, Oshida; Zhou, Quanlai (2013-09-01). "Recent advances in soil seed bank research". Contemporary Problems of Ecology. 6 (5): 520–524. doi:10.1134/S1995425513050181. ISSN   1995-4263. S2CID   255553677.
  15. ↑ Poschlod, Peter; Rosbakh, Sergey (2018). "Mudflat species: Threatened or hidden? An extensive seed bank survey of 108 fish ponds in Southern Germany". Biological Conservation. 225: 154–163. doi:10.1016/j.biocon.2018.06.024. S2CID   91872044.
  16. ↑ Tang, Yong; Cao, Min; Fu, Xianhui (2006). "Soil Seedbank in a Dipterocarp Rain Forest in Xishuangbanna, Southwest China". Biotropica. 38 (3): 328–333. doi:10.1111/j.1744-7429.2006.00149.x. S2CID   53974012.
  17. ↑ "Iowa State University: College of Agriculture and Life Science: Lambsquarters".
  18. 1 2 3 Burnside, Orvin C.; Wilson, Robert G.; Weisberg, Sanford; Hubbard, Kenneth G. (1996). "Seed Longevity of 41 Weed Species Buried 17 Years in Eastern and Western Nebraska". Weed Science. 44 (1): 74–86. doi:10.1017/S0043174500093589. S2CID   82721189.
  19. ↑ Ken Thompson, Jan P. Bakker, and Renée M. Bekker. 1997. The soil seed banks of north west Europe : methodology, density and longevity. New York : Cambridge University Press. p. 276
  20. ↑ J. Derek Bewley; Michael Black; Peter Halmer (2006). The Encyclopedia of Seeds: Science, Technology and Uses. CABI. pp. 14–15. ISBN   978-0-85199-723-0.
  21. ↑ Fountain, Henry (2008-06-17). "Date Seed of Masada is Oldest Ever to Sprout". New York Times. Retrieved December 9, 2021.
  22. 1 2 Frank W. Telewski. "Research & Teaching". Department of Plant Biology, Michigan State University. Retrieved 10 December 2015.
  23. ↑ "Unearthing a scientific mystery". msutoday.msu.edu. Michigan State University.
  24. 1 2 Darlington, H.T.; Steinbauer, G.P. (1961). "THE EIGHTY-YEAR PERIOD FOR DR. BEAL'S SEED VIABILITY EXPERIMENT". American Journal of Botany. 48 (4): 321–325. doi:10.1002/j.1537-2197.1961.tb11645.x.
  25. 1 2 3 Brown, E.; Toole, E.H. (1946). "Final Results of the Duvel Buried Seed Experiment". Journal of Agricultural Research. 72 (6).
  26. ↑ Conn, Jeffrey S.; Werdin-Pfisterer, Nancy R. (2010). "Variation in Seed Viability and Dormancy of 17 Weed Species after 24.7 Years of Burial: The Concept of Buried Seed Safe Sites". Weed Science. 58 (3): 209–215. doi:10.1614/WS-D-09-00084.1. S2CID   9103710.
  27. ↑ Serota, Tziporah H.; Culley, Theresa M. (2019). "Seed Germination and Seedling Survival of Invasive Callery Pear (Pyrus calleryana Decne.) 11 Years After Fruit Collection". Castanea. 84 (1): 47. doi:10.2179/0008-7475.84.1.47. S2CID   191180173.
  28. ↑ Ross, Merrill A.; Lembi, Carole A. (2008). Applied Weed Science: Including the Ecology and Management of Invasive Plants. Prentice Hall. p. 22. ISBN   978-0-13-502814-8.
  29. ↑ Faiz F. Bebawi; Robert E. Eplee; Rebecca S. Norris (March 1984). "Effects of Seed Size and Weight on Witchweed (Striga asiatica) Seed Germination, Emergence, and Host-Parasitization". Weed Science. 32 (2): 202–205. doi:10.1017/S0043174500058811. JSTOR   4043831. S2CID   89078686.
  30. ↑ Daniel M. Joel; Jonathan Gressel; Lytton J. Musselman (2013). Parasitic Orobanchaceae: Parasitic Mechanisms and Control Strategies. Springer Science & Business Media. p. 394. ISBN   978-3-642-38146-1.
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