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A review of geocarpy and amphicarpy in angiosperms, with special reference to their ecological adaptive significance
Received date: 2009-05-25
Accepted date: 2009-07-13
Online published: 2010-01-01
Geocarpy and amphicarpy are two special types of fruiting modes in angiosperms, and they occur mostly in terrestrial herbaceous plants. Geocarpous and amphicarpous species often occur in unstable habitats, where water or light is limiting, soil disturbance is frequent and environmental fluctuations are high. These two types of fruiting modes are important plant ecological adaptations that evolved via natural selection. The adaptive advantages of geocarpy include high survivorship of offspring in the favorable parental microhabitats, maintenance of seed viability in extreme environments, escape from herbivory and damage by fire and increase length of the developmental period of fruits. Amphicarpy is ecologically significant in that it reduces competition among siblings within the population, maintains and increases the size of the population in situ and increases the adaptability and evolutionary plasticity of the species. Thus, these two fruiting modes are considered adaptive strategies of species to biotic and abiotic factors of the environment. However, their potential evolutionary disadvantages include limitation of seed or fruit dispersal, influence on gene transfer and thus population genetic structure and increase of population fragmentation and of reproductive costs, all of which can greatly impact the distribution of species, population increase, migration, fitness and life history evolution. Geocarpy has been reported in about 24 families and 57 genera and amphicarpy in 13 families and 34 genera of angiosperms. Moreover, both types of fruiting modes occur in species of Asteraceae, Brassicaceae, Fabaceae and Scrophulariaceae. Phylogenetically, geocarpy occurs in the magnoliids, monocots and eudicots and amphicarpy in both monocots and eudicots, but neither mode has been reported in the basalmost angiosperms (ANITA clades).
TAN Dun-Yan, ZHANG Yang, WANG Ai-Bo . A review of geocarpy and amphicarpy in angiosperms, with special reference to their ecological adaptive significance[J]. Chinese Journal of Plant Ecology, 2010 , 34(1) : 72 -88 . DOI: 10.3773/j.issn.1005-264x.2010.01.011
[1] | Alinoglu N, Durlu N (1970). Subterranean vetch seed enhances persistence under grazing and severe climates. Journal of Range Management, 23, 61-63. |
[2] | Al-Shehbaz IA, Arai K, Ohba H (2000). A revision of the genus Lignariella (Brassicaceae). Harvard Papers in Botany, 5, 113-121. |
[3] | APG II (2003). An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society, 141, 399-436. |
[4] | Barker NP (2005). A review and survey of basicarpy, geocarpy, and amphicarpy in the African and Madagascan flora. Annals of the Missouri Botanical Garden, 92, 445-462. |
[5] | Bruhl JJ (1994). Amphicarpy in the Cyperaceae, with novel variation in the wetland sedge Eleocharis caespitosissima Baker. Australian Journal of Botany, 42, 441-448. |
[6] | Burtt BL (1970). The evolution and taxonomic significance of a subterranean ovary in certain monocotyledons. Israel Journal of Botany, 19, 77-90. |
[7] | Campbell CS, Quinn JA, Cheplick GP, Bell TJ (1983). Cleistogamy in grasses. Annual Review of Ecology and Systematics, 14, 411-441. |
[8] | Chen HB (陈汉斌), Zheng YJ (郑亦津), Li FZ (李法曾) (1997). Flora of Shandong (山东植物志) Vol. 2. Qingdao Press, Qingdao. 407. (in Chinese) |
[9] | Chen G (陈刚), Min HY (闵海燕), Zhu CL (朱春来), Sun GR (孙国荣), Zhang B (张彪), Du K (杜坤), Liang JS (梁建生) (2006). Reproductive strategy and reproductive cost in Commelina benghalensis. Acta Ecologica Sinica (生态学报), 26, 521-527. (in Chinese with English abstract) |
[10] | Chen JM (陈建民), Qin QL (秦秋琳), Tang T (汤廷页), Jin YG (金银根), Wan JM (万建民) (2004). Studies on chromosomal karyotype and ribosome genes in Bengal dayflower (Commelina benghalensis L.) by flurescent in situ hybridization. Weed Science (杂草科学), 1, 1-4. (in Chinese) |
[11] | Cheplick GP (1983). Differences between plants arising from aerial and subterranean seeds in the amphicarpic annual Cardamine chenopodifolia (Cruciferae). Bulletin of the Torrey Botanical Club, 110, 442-448. |
[12] | Cheplick GP (1987). The ecology of amphicarpic plants. Trends in Ecology and Evolution, 2, 97-101. |
[13] | Cheplick GP (1988). Influence of environment and population origin on survivorship and reproduction in reciprocal transplants of amphicarpic peanutgrass ( Amphicarpum purshii). American Journal of Botany, 75, 1048-1056. |
[14] | Cheplick GP (1994). Life history evolution in amphicarpic plants. Plant Species Biology, 9, 119-131. |
[15] | Cheplick GP, Quinn JA (1982). Amphicarpum purshii and the “pessimistic strategy” in amphicarpic annuals with subterranean fruit. Oecologia, 52, 327-332. |
[16] | Cheplick GP, Quinn JA (1983). The shift in aerial/subterranean fruit ratio in Amphicarpum purshii: causes and significance. Oecologia, 57, 374-379. |
[17] | Cheplick GP, Quinn JA (1987). The role of seed depth, litter, and fire in the seedling establishment of amphicarpic peanutgrass ( Amphicarpum purshii). Oecologia, 73, 459-464. |
[18] | Cheplick GP, Quinn JA (1988). Subterranean seed production and population responses to fire in Amphicarpum purshii. Journal of Ecology, 76, 263-273. |
[19] | Corner EJH (1966). Debunking the new morphology. New Phytologist, 65, 398-404. |
[20] | Dafni A, Werker E (1982). Pollination ecology of Sternbergia clusiana (Ker-Gawler) Spreng. (Amaryllidaceae). New Phytologist, 91, 571-577. |
[21] | Dakora FD, Atkins CA, Pate JS (1992). Effect of nitrate on nitrogen fixation and nitrogenous solutes of xylem in two nodulated West African geocarpic legumes, Kersting’s bean ( Macrotyloma geocarpum L.) and Bambara groundnut (Vigna subterranea L.). Plant and Soil, 140, 255-262. |
[22] | de Clavijo ER (1995). The ecological significance of fruit heteromorphism in the amphicarpic species Catananche lutea (Asteraceae). International Journal of Plant Sciences, 156, 824-833. |
[23] | Dieterle JVAA (1974). New geocarpic genus from Mexico: Apatzingania (Cucurbitaceae). Brittonia, 26, 129-132. |
[24] | Ellner S, Shmida A (1981). Why are adaptations for long-range seed dispersal rare in desert plants? Oecologia, 51, 133-144. |
[25] | Evenari M, Kadouri K, Gutterman Y (1977). Ecophysiological investigations on the amphicarpy of Emex spinosa (L.) Campd. Flora, 166, 223-238. |
[26] | Ferguson ME, Jarvis A, Stalker HT, Williams DE, Guarino L, Valls JFM, Pittman RN, Simpson CE, Bramel PJ (2005). Biogeography of wild Arachis (Leguminosae): distribution and environmental characterisation. Biodiversity and Conservation, 14, 1777-1798. |
[27] | Friedman WE, Ryerson KC (2009). Reconstructing the ancestral female gametophyte of angiosperms: insights from Amborella and other ancient lineages of flowering plants. American Journal of Botany, 96, 129-143. |
[28] | Gamm R (1983). Notes on amphicarpy shown by the annual species Cardamine chenopodiifolia Pers. (Brassicaceae). Acta Botanica Neerlandica, 32, 346. |
[29] | Gao LX (高乐旋), Chen JK (陈家宽), Yang J (杨继) (2008). Phenotypic plasticity: eco-devo and evolution. Journal of Systematics and Evolution (植物分类学报), 46, 441-451. (in Chinese with English abstract) |
[30] | Gao R (高蕊), Wei Y (魏岩) (2007). Amphicarpy of Ceratocarpus arenarius (Chenopodiaceae) in Junggar Desert. Acta Botanica Yunnanica (云南植物研究), 29, 300-302. (in Chinese with English abstract) |
[31] | Garbari F (1975). The genus Allium L. in Italy. V. Allium subgen. chamaeprason (F. Hermann), stat. nov. Taxon, 24, 541-542. |
[32] | Goldblatt P, Manning JC (1993). Ixia acaulis, a new acaulescent species of Iridaceae: Ixioideae from the Knersvlakte, Namaqualand, South Africa. Novon, 3, 148-153. |
[33] | Goldblatt P, Manning JC (2006). Radiation of pollination systems in the Iridaceae of sub-Saharan Africa. Annals of Botany, 97, 317-344. |
[34] | Gopinathan MC, Babu CR (1986). A unique growth pattern associated with cleistogamy in a tropical legume, Vigna minima (Roxb.) Ohwi & Ohashi (Leguminosae). Botanical Journal of the Linnean Society, 92, 263-268. |
[35] | Gopinathan MC, Babu CR (1987). Breeding systems and pollination in Vigna minima (Leguminosae, Papilionoideae). Plant Systematics and Evolution, 156, 117-126. |
[36] | Grisona L, Edwards AA, Hossaert-McKey M (1999). Interspecies variation in floral fragrances emitted by tropical Ficus species. Phytochemistry, 52, 1293-1299. |
[37] | Guo XM (郭学民), Qiao YK (乔亚科), Liu YJ (刘永军), Liu JZ (刘建珍), Li Q (李强), Cao CH (曹晨华), Li SH (李素红), Gao H (高红), Wang Y (王艳) (2003). Observation of the flower of Amphicarpaea edgeworthii Beath. with SEM and test of pollen vigor. Journal of Hebei Vocation-Technical Teachers College (河北职业技术师范学院学报), 17(1), 30-34. (in Chinese with English abstract) |
[38] | Guo XM (郭学民), Qiao YK (乔亚科), Liu YJ (刘永军), Zhou YG (周永国) (2002). Comparative study on the testa and pericarp of Amphicarpaea edgeworthii Beath. of different habitat under SEM observation. Journal of Hebei Vocation-Technical Teachers College (河北职业技术师范学院学报), 16(3), 61-64. (in Chinese with English abstract) |
[39] | Hedberg O (1970). Evolution of the afroalpine flora. Biotropica, 2, 16-23. |
[40] | Hollmann J, Myburgh S, van Wyk B (1995). Aardvark and cucumber—A remarkable relationship. Veld & Flora, 95, 108-109. |
[41] | Imber E (2002). Ecological consequences and ontogeny of seed heteromorphism. Perspectives in Plant Ecology, Evolution and Systematics, 5, 13-36. |
[42] | Inglis GJ (2000). Disturbance-related heterogeneity in the seed banks of a marine angiosperm. Journal of Ecology, 88, 88-99. |
[43] | Kaul V, Koul AK, Sharma MC (2000). The underground flower. Current Science, 78, 39-44. |
[44] | Kaul V, Sharma N, Koul AK (2002). Reproductive effort and sex allocation strategy in Commelina benghalensis L., a common monsoon weed. Botanical Journal of the Linnean Society, 140, 403-413. |
[45] | Kawano S, Hara T, Hiratsuka A, Matsuo K, Hirota I (1990). Reproductive biology of an amphicarpic annual, Polygonum thunbergii (Polygonaceae): spatio-temporal changes in growth, structure and reproductive components of a population over an environmental gradient. Plant Species Biology, 5, 97-120. |
[46] | Keighery GJ (1982). Geocarpy in Tribulopsis R. Br. (Zygophyllaceae). Flora, 172, 329-333. |
[47] | Koller D, Roth N (1964). Studies on the ecological and physiological significance of amphicarpy in Gymnarrhena micrantha (Compositae). American Journal of Botany, 51, 26-35. |
[48] | Konuma A, Terauchi R (2001). Population genetic structure of the self-compatible annual herb: Polygonum thunbergii. The American Midland Naturalist, 146, 122-127. |
[49] | Kubitzki K (2003). The Families and Genera of Vascular Plants, Vol. 5. Flowering Plants, Dicotyledons: Malvales, Capparales, and Non-betalain Caryophyllales. Springer- Verlag, Berlin. |
[50] | Lawn RJ, Holland AE (2003). Variation in the Vigna lanceolata complex for traits of taxonomic, adaptive or agronomic interest. Australian Journal of Botany, 51, 295-308. |
[51] | Lev-Yadun S (2000). Why are underground flowering and fruiting more common in Israel than anywhere else in the world? Current Science, 79, 289. |
[52] | Li AR (李安仁), Gao ZJ (高作经), Mao ZM (毛祖美), Liu YL (刘玉兰) (1998). Polygonaceae. In: Li AR (李安仁) ed. Flora Reipublicae Popularis Sinicae (中国植物志), Tomus 25 (I). Science Press, Beijing. 70. (in Chinese) |
[53] | Liang ZC, Yang J, Rao GY (2007). Development of microsatellite markers in an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae). Molecular Ecology Notes, 7, 863-865. |
[54] | Liang ZC, Huang P, Yang J, Rao GY (2009). Population divergence in the amphicarpic species Amphicarpaea edgeworthii Benth. (Fabaceae): microsatellite markers and leaf morphology. Biological Journal of the Linnean Society, 96, 505-516. |
[55] | Lock JM, Hall JB (1973). Three new species of Aframomum K. Schum. (Zingiberaceae) from Ghana, with notes on spherical geocarpic fruits in the genus. Kew Bulletin, 28, 441-449. |
[56] | Maheshwari P, Maheshwari JK (1955). Floral dimorphism in Commelina forskalaei Vahl and C. benghalensis L. Phytomorphology, 5, 413-422. |
[57] | Mandák B (1997). Seed heteromorphism and the life cycle of plants: a literature review. Preslia, 69, 129-159. |
[58] | Mattatia J (1977). The amphicarpic species Lathyrus ciliolatus. Botaniska Notiser, 129, 437-444. |
[59] | Meney KA, Pate JS, Dixon KW (1990). Comparative morphology, anatomy, phenology and reproductive biology of Alexgeorgea spp. (Restionaceae) from south-western Western Australia. Australian Journal of Botany, 38, 523-541. |
[60] | Min HY (闵海燕), Chen G (陈刚), Sun GR (孙国荣), Wang C (王聪), Liu AP (刘爱平), Du K (杜坤), Zhang B (张彪) (2008). Resource allocation and reproductive cost of plants from four types of seedlings of Commelina benghalensis. Acta Ecologica Sinica (生态学报), 28, 1802-1809. (in Chinese with English abstract) |
[61] | Moctezuma E (2003). The peanut gynophore: a developmental and physiological perspective. Canadian Journal of Botany, 81, 183-190. |
[62] | Momose K, Inoue T (1993). Pollination and factors limiting fruit set of chasmogamous flowers of an amphicarpic annual, Polygonum thunbergii (Polygonaceae). Researches on Population Ecology, 35, 79-93. |
[63] | Nancy RM, Unger J (2003). Nyctaginaceae. In: Flora of North America Editorial Committee ed. Flora of North America North of Mexico, Vol. 4, Oxford University Press, New York. 16. |
[64] | Parker MA (1994). Evolution in natural and experimental populations of Amphicarpea bracteata. Journal of Evolutionary Biology, 7, 567-579. |
[65] | Pasquet RS, Mergeai G, Baudoin JP (2002). Genetic diversity of the African geocarpic legume Kersting’s groundnut, Macrotyloma geocarpum (Tribe Phaseoleae: Fabaceae). Biochemical Systematics and Ecology, 30, 943-952. |
[66] | Plitmann U (1973). Biological flora of Israel. 4 Vicia sativa subsp. amphicarpa (Dorth.) Aschers. & Graebn. Israel Journal of Botany, 22, 178-194. |
[67] | Qiao YK (乔亚科), Li GL (李桂兰), Gao SG (高书国), Liu W (刘微), Bi YJ (毕艳娟), Zhou YF (周印富), Li SG (李守刚), Jiang ZQ (蒋志强), Zhang Y (张怡), Liu DC (刘东昶) (2000). Preliminary study on the developmental speciality of seedling from subterraneous and plant’s seed of Amphicarpaea edgeworth Benth. Journal of Hebei Vocation-Technical Teachers College (河北职业技术师范学院学报), 14(4), 1-3. (in Chinese with English abstract) |
[68] | Real D, Rizza MD, Reyno R, Quesenberry KH (2007). Breeding system of the aerial flowers in an amphicarpic clover species: Trifolium polymorphum. Crop Science, 47, 1401-1406. |
[69] | Sadeh A, Guterman H, Gersani M, Ovadia O (2009). Plastic bet-hedging in an amphicarpic annual: an integrated strategy under variable conditions. Evolutionary Ecology, 23, 373-388. |
[70] | Schnee BK, Waller DM (1986). Reproductive behavior of Amphicarpaea bracteata (Leguminosae), an amphicarpic annual. American Journal of Botany, 73, 376-386. |
[71] | Schoen DJ (1984). Cleistogamy in Microlaena polynoda (Gramineae): an examination of some model predictions. American Journal of Botany, 71, 711-719. |
[72] | Sharma SK, Babu CR, Johri BM (1981). Fruit dimorphism in Phaseolus sublobatus (Fabaceae) and its evolutionary significance. Plant Systematics and Evolution, 137, 67-72. |
[73] | Small E, Brookes B (1984). Reduction of the geocarpic Factorovskya to Medicago. Taxon, 33, 622-635. |
[74] | Smith BW (1950). Arachis hypogaea, aerial flower and subterranean fruit. American Journal of Botany, 37, 802-815. |
[75] | Totland ?, Matthews I (1998). Determinants on pollinator activity and flower preference to the early spring blooming Crocus vernus. Acta Oecologica, 19, 155-166. |
[76] | Trapp EJ (1988). Dispersal of heteromorphic seeds in Amphicarpaea bracteata (Fabaceae). Amercan Journal of Botany, 75, 1535-1539. |
[77] | Trapp EJ, Hendrix SD (1988). Consequences of a mixed reproductive system in the hog peanut, Amphicarpaea bracteata (Fabaceae). Oecologia, 75, 285-290. |
[78] | van Rheede, van Oudtshoorn K, van Rooyen MW (1999). Dispersal Biology of Desert Plants: Adaptations of Desert Organisms. Springer, Berlin. |
[79] | Walker SR, Evenson JP (1985a). Biology of Commelina benghalensis L. in south-eastern Queensland. 1. Growth, development and seed production. Weed Research, 25, 239-244. |
[80] | Walker SR, Evenson JP (1985b). Biology of Commelina benghalensis L. in south-eastern Queensland. 2. Seed dormany, germination and emergence. Weed Research, 25, 245-250. |
[81] | Webb CJ (1998). The selection of pollen and seed dispersal in plants. Plant Species Biology, 13, 57-67. |
[82] | Wei YZ (韦裕宗) (1995). Leguminosae. In: Li SG (李树刚) ed. Flora Reipublicae Popularis Sinicae (中国植物志), Tomus 41. Science Press, Beijing. 257-258. (in Chinese) |
[83] | Weiss PW (1980). Germination, reproduction and interference in the amphicarpic annual Emex spinosa (L.) Campd. Oecologia, 45, 244-251. |
[84] | Zamski E, Ucko O, Koller D (1983). The mechanism of root contraction in Gymnarrhena micrantha, a desert plant. New Phytologist, 95, 29-35. |
[85] | Zeide B (1978). Reproductive behavior of plants in time. The American Naturalist, 112, 636-639. |
[86] | Zhang Y, Yang J, Rao GY (2005). Genetic diversity of an amphicarpic species, Amphicarpeae edgeworthii Benth. (Leguminosae) based on RAPD markers. Biochemical Systematices and Ecology, 33, 1246-1257. |
[87] | Zhang Y, Yang J, Rao GY (2006). Comparative study on the aerial and subterranean flower development in Amphicarpaea edgeworthii Benth. (Leguminosae: Papilionoideae), an amphicarpic species. International Journal of Plant Sciences, 167, 943-949. |
[88] | Zhang Y (张洋), Tan DY (谭敦炎) (2009). Breeding system and pollination biology of Crocus alatavicus (Iridaceae), a geocarpic subalpine plant of western Tianshan Mountains. Biodiversity Science (生物多样性), 17, 468-475. (in Chinese with English abstract) |
[89] | Zhao YT, Woltie HJ, Mathew B (2000). Iridaceae. In: Wu ZY, Raven PH eds. Flora of China, Vol. 24. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. 312-313. |
[90] | Zhou TY, Lu LL, Yang G, Al-Shehbaz IA (2001). Brassicaceae. In: Wu ZY, Raven PH eds. Flora of China, Vol. 8. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. 1-193. |
[91] | Zhou ZK, Michael GG (2003). Moraceae. In: Wu ZY, Raven PH, Hong DY eds. Flora of China, Vol. 5. Science Press, Beijing, and Missouri Botanical Garden Press, St. Louis. 37-71. |
[92] | Zohary M (1962). Plant Life of Palestine, Israel and Jorden. Ronald, New York. |
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