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Zamia

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For the three species commonly called Zamia that are endemic to Western Australia, see Macrozamia riedlei, Macrozamia fraseri, and Macrozamia dyeri.

Zamia
Zamia furfuracea
Scientific classification Edit this classification
Kingdom: Plantae
Clade: Tracheophytes
Clade: Gymnospermae
Division: Cycadophyta
Class: Cycadopsida
Order: Cycadales
Family: Zamiaceae
Subtribe: Zamiinae
Genus: Zamia
L.[1]
Type species
Zamia pumila
Synonyms[2]
  • Aulacophyllum Regel
  • Chigua D.W.Stev.
  • Palmifolium Kuntze
  • Palma-filix Adans.

Zamia is a genus of cycad of the family Zamiaceae, native to North America from the United States (in Georgia and Florida) throughout the West Indies, Central America, and South America as far south as Bolivia.[2][3][4][5] The genus is considered to be the most ecologically and morphologically diverse of the cycads, and is estimated to have originated about 68.3 million years ago.[6]

Description

[edit]
Zamia furfuracea leaves

The genus comprises deciduous shrubs with aerial or subterranean circular stems, often superficially resembling palms. They produce spirally arranged, pinnate leaves which are pubescent, at least when young, having branched and simple, transparent and coloured hairs. The articulated leaflets lack a midrib, and are broad with subparallel dichotomous venation. Lower leaflets are not reduced to spines, though the petioles often have prickles. The emerging leaves of many Zamia species are striking, some emerging with a reddish or bronze cast (Z. roezlii being an example). Z. picta is even more distinctive, being the only truly variegated cycad (having whitish/yellow speckles on the leaves).[7]

Like all Zamiaceae, Zamia plants have "coralloid" (coral-shaped) roots which host nitrogen-fixing cyanobacteria. Stems are 3 to 25 centimetres (1.2 to 9.8 in) in diameter, and when arborial, up to 5 metres (16 ft) tall. Leaves vary from 2 to up to 15 in number, and have an even number (5 to 60 pairs) of leaflets. petioles (leaf stalks) and rachis (leaf axis, to which leaflets are attached) may be smooth, or have prickles on the petiole and lower part of the rachis. Leaflets are linear to ovate and may be directly attached to the rachis, or may be on short petiolules. The edges of leaflets may be smooth, or may be toothed partly or around the whole leaflet.[8] The morphology of leaflets is highly varied between even closely related species of Zamia, and within species and even within populations of a species. Studies have found that the amount of sun a plant is exposed to is responsible for differences in leaflet length, width, surface area, width ratio, shape, and density and thickness of leaflets. There is also significant morphological variation in leaflets between male and female plants in some species.[9][10]

Reproduction

[edit]

Zamia sporophylls are born in vertical rows in cones, and the megasporophyll apices are faceted or flattened, not spinose. The fleshy seeds are subglobular to oblong or ellipsoidal, and are red, orange, yellow or rarely white. The endosperm is haploid, derived from the female gametophyte. The embryo is straight, with two cotyledons that are usually united at the tips and a very long, spirally twisted suspensor. The sperm of members from the genus are large, as is typical of cycads, and Z. roezlii is an example; its sperm are approximately 0.4 mm long and can be seen by the unaided eye.[11]

It was long believed that Zamia plants, like all cycads, relied completely on wind pollination. In the 1980s it was discovered that at least some Zamia species were pollinated by beetles of the Pharaxonotha and Rhopalotria genera. Further studies have found that pollination by beetles is widespread in Zamia and other cycads.[12]

Seed-dispersal in Zamia is poorly documented for most species, but there are reports of birds and/or small to medium-sized mammals dispersing the seeds of a few Zamia species.[13]

Habitats

[edit]

With one exception, Zamia species are found only in the Neotropical realm in the Americas. The exception is Z. integrifolia, which has a range that extends into the Nearctic realm in northern Florida, and formerly into the southeastern corner of Georgia.[14]

Toxicity

[edit]

Many of the Zamia species are, or have been, gathered to process the stem and/or seeds into starch for use as food or laundry starch. However, almost the entire plant is very toxic and the starch must be repeatedly washed to remove the toxins. Only the sarcotesta, the pulpy covering of the seeds, is relatively free of toxins.[15] The primary toxin in Zamia plants is cycasin, a carcinogenic and neurotoxic glucoside. Other glucoside toxins present include macrozamin (de) and several neocycasins.[16] BMAA, a neurotoxin that is produced by cyanobacteria living in roots of the plants, is also present in most Zamia plants.[17]

Consumption of cycads by livestock has resulted in two forms of cycad toxicosis. Hepato-gastrointestinal toxicosis results from damage to the liver and gastrointestinal tracts of affected animals causing depression, anorexia, and weight loss. Neurologic toxicosis, known as Zamia staggers, is the result of damage to brain, spinal cord, and dorsal root ganglia tissue causing weight loss, swaying of hind quarters, and weakness and other defects in rear limbs.[18]

Phylogeny

[edit]

Despite the ancient history of cycads, species diversity in Zamia is geologically recent. Calonje et al. found a stem age for Zamia of 68.28 million years ago (mya), and a crown age of 9.54 mya.[19]

Geographic groups

[edit]

As early as the 1930s, authors recognized three biogeographic groups in Zamia, Caribbean, Mesoamerican, and Central and South America. In the 21st century, phylogenies of Zamia based on molecular phylogenetic analyses have found stronger correlation with geographic regions than with morphological features.[20]

Zonneveld and Lindström (2016) measured genome size in 71 species of Zamia and found support for three geographical groupings. Variation in genome size of Zamia species is fairly small compared to many other genera, with the ratio of largest to smallest just 1.36, but the authors found significant differences in genome sizes between three geographical areas. Species in Mega Mexico, including the northern part of Central America, had the largest average genome size. Species in South America, plus Costa Rica and Panama, had the smallest average genome size, while species in the Caribbean Islands and Florida had an intermediate genome size.[21]

Zamia tree based on DNA[22]
Zamia

Caribbean and Florida 8 sp.

Mesoamerica 21 sp.

Zamia soconuscensis

Isthmus 16 sp.

South America 28 sp.

Calonje, et al. (2019) analyzed the DNA from 70 species of Zamia, finding support for four geographically distinct clades (plus a single isolated species). A clade including the species found on the Caribbean islands and in Florida is sister to the rest of the genus. The species of the Caribean clade have diverged within the last 1.9 million years. The Mesoamerica clade includes all species found in Mesoamerica (north of Nicaragua), except for the single species Z. soconuscensis. It has a divergence age of 5.79 mya. The Isthmus clade includes species found in southernmost Nicaragua, Costa Rica and Panama, and has a divergence age of 2.35 mya. The species in South America form another clade, which is sister to the Isthmus clade. It has a divergence age of 2.62 mya.[22]

Zamia tree based on transcriptomes[23]
Zamia
I

Caribbean islands 7 sp.

Florida  Zamia integrifolia

II 

Fischeri clade 3 sp.

III
III‑A 

Mega Mexico A 14 sp.

III‑B 

Mega Mexico B 7 sp.

IV 

 Zamia soconuscensis

V 

Isthmus 15 sp.

VI 

West of the Andes 12 sp.

VII

Northern Colombia

(Manicata clade) 4 sp.

East of the Andes 13 sp.

Lindstrom et al. (2024) analyzed transcriptomes from 77 species of Zamia finding support for seven clades of the genus occupying distinct geographical ranges. Clade I is a strongly monophyletic clade that includes eight of the species of the Caribbean islands and Florida. Clade II (the Fischeri clade), consists of three species found in Veracruz, Hidalgo, Querétaro, San Luis Potosí, and Tamaulipas states in Mexico. This clade is a sister to Clade I, with the group of Clade I and Clade II being sister to the rest of the genus. Clade III (Mega Mexico) is divided into the sub-clades III-A and III-B. Clade III-A includes 14 species found in Mexico and northern Central America. Clade III-B consists of seven species found in Honduras, Guatemala, and Belize. Clade IV consists of the single species Z. soconuscensis found in cloud forests in Chiapas state in Mexico. Clade V (the Isthmus clade) includes 15 species found in southern Nicaragua, Costa Rica, and Panama. Clade VI includes 12 species found in southernmost Panama and west of the Andes in Colombia and Ecuador. Clade VII consists of four closely related species in northern Columbia (the Manicata clade) and 13 species east of the Andes in Venezuela, Colombia, Ecuador, Peru, Brazil, and Bolivia.[23]

Clades and species complexes

[edit]

Fischeri clade

[edit]

The Fischeri clade consists of three closely related species of Zamia found near the Gulf coast of central Mexico. The three species, Z. fischeri, Z. inermis, and Z. vazquezii, share various morphological features, including the near or total absence of prickles on leaf stalks. The analysis of DNA by Calonje, et al. found strong support for the Fischeri clade as sister to all of the mainland Zamia species (i.e., everything except the Caribbean and Florida clade.[24] The analysis of transcriptomes by Lindstrom et al. found strong support for the Fischeri clade as sister to the Caribbean-Florida clade, with the combined Caribbean-Florida and Fischeri clade sister to the rest of Zamia. The Fischeri and Caribbean-Florida clades share several morphological traits, including the lack or near-lack of prickles on leaf stalks and simlarities in reproductive characters. The genome sizes of the species in the Fischeri clade are among the smallest in Zamia.[25]

Manicata clade

[edit]

The Manicata clade is a group of closely related species found in northern Colombia. It consists of Zamia manicata, Z. disodon, Z. melanorrhacis, Z. restrepoi, Z. imbricata, and Z. sinuensis. Z. manicata was described in 1876. The other species in the clade have been described more recently, with Z. restrepoi described in 1990 (as Chigua restrepoi, reclassified as Z. restrepoi in 2009), Z. disodon and Z. melanorrhacis in 2001, and Z. imbricata and Z. sinuensis in 2021. The monophyly of the clade is strongly supported by molecular phylogenetic studies. Calonje, et al. (2019) found Z. manicata, Z. disodon, Z. melanorrhacis, and Z. restrepoi to form a clade.[26] Lindstrom et al. (2024) found Z. manicata, Z. disodon, Z. restrepoi, and Z. sinuensis to form a clade.[27] While Z. imbricata was not included in either analysis, it shares several morphological features with the rest of the clade, including subterranean or semi-subterranean stems, strongly toothed margins on leaflets, strobili (cones) on very long stalks, small seeds with very thin sarcotesta (coats), and very small pollen (male) cones. Leaf morphology varies strongly among the members of the clade.[28]

Zamia pumila species complex

[edit]
Zamia pumila species complex tree based on transcriptomes[23]
Zamia

All of the species in the Caribbean plus Florida grouping/clade are also in the Zamia pumila species complex. The classification of the populations in the Greater Antilles, Bahamas, and Florida has been controversial. In 1980, Eckenwalder included all the Zamia populations in the Caribbean and Florida in the single species Z. pumila, incorporating 27 previously described species (not all of which were valid or accepted) into the subspecies Z. pumila subsp. pumila, and five such species from Cuba into the subspecies Z. pumila subsp. pygmaea.[29] Eckenwalder's classification is no longer generally accepted, and a monophyletic species complex consisting of nine species is now accepted, including Z. pumila, seven other species corresponding to combinations of the species subsumed into Eckenwalder's Z. pumila subsp. pumila, and Z. pygmaea, consisting of the former species placed by Eckenwalder in Z. pumila subsp. pygmaea.[30][31]

Zamia skinneri species complex

[edit]
Z. skinneri species complex based on transcriptomes[23]
Zamia

Zamia skinneri has been regarded as a highly variable species. Z. neurophyllidia was described as a new species in 1993, based on a population of what had been regarded as a dwarf form of Z. skinneri. A study published in 2004 proposed that Z. neurophyllidia and Z. skinneri were a "hybrid species complex", and noted that Z. skinneri included several morphologically distinct populations. In 2008, Taylor B. et al. described three sub-populations of Z. skinneri as Z. hamannii, Z. imperialis, and Z. nesophila.[32] All five of the species in this complex are found in Bocas del Toro Province, at least three of the species are endemic to that Province, and all of them have plicate leaves, a trait that occurs elsewhere in Zamia only in Z. dressleri in Colon and San Blas provinces in Panama, and in Z. roezlii and Z. wallisii in Colombia. Taylor B. et al. (2012) suggest that Z. skinneri is the central species of the complex, and that the other species have evolved rapidly from Z. skinneri on the periphery of its range due to geographic or other isolation.[33]

Chigua

[edit]

Chigua was described as a new genus with two species in Zamiaceae in 1990, but was reclassified as Zamia restrepoi in 2009.[34]

Species

[edit]
Accepted species[α] Clade:[23] distribution IUCN status
Zamia acuminata Oerst.ex Dyer V (Isthmus): Costa Rica, Nicaragua, Panama Vulnerable
Zamia amazonum D.W.Stev. VII (East of Andes): Brazil, Colombia, Ecuador, Peru, Venezuela Least concern
Zamia amplifolia Hort.Bull ex Mast. VI (West of Andes): Colombia Endangered
Zamia angustifolia Jacq. I (Caribbean): Bahamas, Cuba Vulnerable
Zamia boliviana (Brongn.) A.DC. VII (East of Andes): Bolivia, Brazil (Mato Grosso) Least concern
Zamia brasiliensis Calonje & Segalla (unknown): Brazil (Mato Grosso, Rondônia) Not evaluated
Zamia chigua Seem. VI (West of Andes): Colombia Near threatened
Zamia cremnophila Vovides, Schutzman & Dehgan III-A (Mega Mexico): Mexico (Tabasco) Endangered
Zamia cunaria Dressler & D.W.Stev. VI (West of Andes): Panama Endangered
Zamia decumbens Calonje, Meerman, M.P. Griff. & Hoese III-B (Mega Mexico) Belize Endangered
Zamia disodon D.W.Stev. & Sabato VII (Manicata): Colombia Endangered
Zamia dressleri D.W.Stev. V (Isthmus): Panama Endangered
Zamia elegantissima Schutzman, Vovides & R.S.Adams V (Isthmus): Panama Endangered
Zamia encephalartoides D.W. Stev. VII (East of Andes): Colombia Endangered
Zamia erosa O.F.Cook & G.N.Collins I (Caribbean): Cuba, Jamaica, Puerto Rico Vulnerable
Zamia fairchildiana L.D.Gómez V (Isthmus): Panama, Costa Rica Near threatened
Zamia fischeri Miq. ex Lem. II (Fischeri): Mexico (Hidalgo, San Luis Potosí, Querétaro, Tamaulipas, Veracruz) Endangered
Zamia furfuracea L.f. III-A (Mega Mexico): Mexico (Veracruz) Endangered
Zamia gentryi Dodson VI (West of Andes): Ecuador Endangered
Zamia gomeziana R.H.Acuña (unknown): Costa Rica Near threatened
Zamia grijalvensis Pérez-Farr., Vovides & Mart.-Camilo III-A (Mega Mexico): Mexico (Chiapas) Critically endangered
Zamia hamannii A.S.Taylor, J.L.Haynes & Holzman V (Isthmus): Panama Vulnerable
Zamia herrerae Calderón & Standl. III-A (Mega Mexico): Mexico (Chiapas), El Salvador, Guatemala, Honduras, Nicaragua Vulnerable
Zamia huilensis Calonje, H.E.Esquivel & D.W.Stev. VII (East of Andes): Colombia Endangered
Zamia hymenophyllidia D.W.Stev. VII (East of Andes): Colombia, Peru Least concern
Zamia imbricata[β] Calonje & J.Castro VII (Manicata): Colombia[10] Not evaluated
Zamia imperialis A.S.Taylor, J.L.Haynes & Holzman V (Isthmus): Panama Endangered
Zamia incognita A.Lindstr. & Idárraga (unknown): Colombia Endangered
Zamia inermis Vovides, J.D.Rees & Vázq.Torres II (Fischeri): Mexico (Veracruz) Critically endangered
Zamia integrifolia L.f. I (Caribbean): Bahamas, Cayman Islands, Cuba, Puerto Rico, United States (Florida, Georgia) Near threatened
Zamia ipetiensis D.W.Stev. VI (West of Andes): Panama Endangered
Zamia katzeriana (Regel) E.Rettig III-A (Mega Mexico): Mexico Critically endangered
Zamia lacandona Schutzman & Vovides III-A (Mega Mexico): Mexico (Chiapas) Endangered
Zamia lawsoniana[γ]' Dye (unknown): Mexico (Chiapas, Oaxaca, Tabasco, Veracruz) Not evaluated
Zamia lecointei Ducke VII (East of Andes): Brazil (Pará), Colombia, Peru, Venezuela Least concern
Zamia lindenii Regel ex André VI (West of Andes): Ecuador, Peru Endangered
Zamia lindleyi Warsz. ex A.Dietr. V (Isthmus): Panama Endangered
Zamia lindosensis Stevenson, Cárdenas & Castaño (unknown): Colombia Not evaluated
Zamia loddigesii Miq. III-A (Mega Mexico): Belize, El Salvador, Honduras, Mexico (Campeche, Chiapas, Veracruz, Puebla, Oaxaca, Hidalgo, Tabasco, Tamaulipas, Quintana Roo, Yucatán) Near threatened
Zamia lucayana Britton I (Caribbean): Bahamas Critically endangered
Zamia macrochiera D.W.Stev. (unknown): Peru Endangered
Zamia magnifica[δ] Pérez-Farr., Gutt-Ortega & Calonje (unknown): Mexico (Oaxaca) Not evaluated
Zamia manicata Linden ex Regel VII (Manicata): Colombia, Panama Near threatened
Zamia meermanii Calonje III-A (Mega Mexico): Belize Endangered
Zamia melanorrhachis D.W.Stev. VII (Manicata): Colombia[10] Endangered
Zamia montana A.Braun VI (West of Andes): Colombia Critically endangered
Zamia monticola Chamb. III-B (Mega Mexico): Guatemala Critically endangered
Zamia multidentata[ε] Calonje, Segalla & R.S.Pimenta (unknown): Brazil (Acre) Not evaluated
Zamia muricata Willd. VII (East of Andes): Colombia, Venezuela Least concern
Zamia nana[ζ] A.Lindstr., Calonje, D.W.Stev. & A.S.Taylor V (Isthmus): Panama Endangered
Zamia nesophila A.S.Taylor, J.L.Haynes & Holzman V (Isthmus): Panama Critically endangered
Zamia neurophyllidia D.W.Stev. V (Isthmus): Costa Rica, Nicaragua, Panama Least concern
Zamia obliqua A.Braun V (Isthmus): Colombia Least concern
Zamia oligodonta E.Calderón & D.E.Stev. (unknown): Colombia Critically endangered
Zamia onan-reyesii C.Nelson & Sandoval III-B (Mega Mexico): Honduras Endangered
Zamia oreillyi C.Nelson III-B (Mega Mexico): Honduras Critically endangered
Zamia orinoquiensis[η] Calonje, Betancur & A.Linstr. VII (East of Andes): Colombia Not evaluated
Zamia paucifoliolata Calonje VI (West of Andes): Colombia Not evaluated
Zamia paucijuga Wieland III-A (Mega Mexico): Mexico (Guerrero, Jalisco, Colima, Michoacán, Nayarit, Oaxaca) Near threatened
Zamia poeppigiana Mart. & Eichler VII (East of Andes): Bolivia, Brazil (Acre) Least concern
Zamia portoricensis Urb. I (Caribbean): Puerto Rico Endangered
Zamia prasina W.Bull III-A (Mega Mexico): Belize, Mexico (Tabasco, Yucatán) Least concern
Zamia pseudomonticola L.D.Gómez V (Isthmus): Costa Rica, Panama Least concern
Zamia pseudoparasitica Yates V (Isthmus): Panama Near threatned
Zamia pumila L. I (Caribbean): Hispaniola (Dominican Republic), possibly Cuba; possibly extirpated in Puerto Rico and Haiti Vulnerable
Zamia purpurea Vovides, J.D.Rees & Vázq.Torres III-A (Mega Mexico): Mexico (Veracruz, Oaxaca) Critically endangered
Zamia pygmaea Sims I (Caribbean): Cuba Endangered
Zamia pyrophylla Calonje, D.W.Stev. & A.Lindstr. VI (West of Andes): Colombia Critically endangered
Zamia restrepoi (D.W.Stev.) A.Lindstr. VII (Manicata): Colombia Critically endangered
Zamia roezlii Regel ex Linden VI (West of Andes): Colombia, Ecuador Least concern
Zamia sandovalii C.Nelson III-B (Mega Mexico): Honduras Endangered
Zamia sinuensis[θ] Calonje & J.Castro VII (Manicata): Colombia Not evaluated
Zamia skinneri Warsz. ex A.Dietr. V (Isthmus): Panama Endangered
Zamia soconuscensis Schutzman, Vovides & Dehgan IV: Mexico (Chiapas) Endangered
Zamia spartea A.DC. in A.P.de Candolle III-A (Mega Mexico): Mexico (Oaxaca) Critically endangered
Zamia splendens[ι] Schutzman III-A (Mega Mexico): Mexico (Chiapas, Tabasco, Veracruz) Endangered
Zamia standleyi Schutzman III-B (Mega Mexico): Guatemala, Honduras Not evaluated
Zamia stenophyllidia Nicolalde-Morejón, Martínez-Domínguez & Stevenson (unknown): Mexico (Michoacán) Not evaluated
Zamia stevensonii A.S.Taylor & Holzman V (Isthmus): Panama Endangered
Zamia stricta Miq. I (Caribbean): Cuba Vulnerable
Zamia tolimensis Calonje, H.E.Esquivel & D.W.Stev VII (East of Andes): Colombia Endangered
Zamia tuerckheimii Donn.Sm. III-B (Mega Mexico) Guatemala Near threatened
Zamia ulei Dammer VII (East of Andes): Brazil, Colombia, Ecuador, Peru, Venezuela Least concern
Zamia urep B.Walln. VII (East of Andes): Peru Endangered
Zamia variegata Warsz. III-A (Mega Mexico): Belize, Guatemala, Mexico (Chiapas) Endangered
Zamia vazquezii D.W.Stev., Sabato & De Luca II (Fischeri): Mexico (Veracruz) Critically endangered
Zamia verschaffeltii Miq. (unknown): Mexico Not evaluated[κ]
Zamia wallisii H.J.Veitch VI (West of Andes): Colombia Critically endangered

Species table notes

[edit]
  1. ^ Almost all of the species in this table are accepted as valid in at least four of the following databases, including The World List of Cycads (WLC),[35] the USDA-ARS Germplasm Resources Information Network (GRIN),[36] the Kew Gardens Plants of the World Online (Kew),[37] the World Flora Online (WFO).[38] and Tropicos.[39] A few species accepted in only two or three of the five databases are noted individually.
  2. ^ Z. imbricata is accepted in WLC, Kew, and Tropicos.
  3. ^ Z. lawsoniana is accepted in WLC, Kew, and Tropicos.
  4. ^ Z. magnifica is accepted in WLC, Kew, and Tropicos.
  5. ^ Z. multidentata is accepted in WLC, Kew, and Tropicos.
  6. ^ Z. nana is accepted in WLC, Kew, and Tropicos.
  7. ^ Z. orinoquiensis is accepted in WLC and Kew, and listed as "unchecked" in WFO.
  8. ^ Z. sinuensis is accepted in WLC, Kew, and Tropicos.
  9. ^ Z. splendens is accepted in WLC, WFO, and Tropicos.
  10. ^ Z. verschaffeltii may be extinct.[40]

References

[edit]
  1. ^ "Genus: Zamia L." Germplasm Resources Information Network. United States Department of Agriculture. 2007-10-05. Archived from the original on 2009-08-27. Retrieved 2011-01-12.
  2. ^ a b Kew World Checklist of Selected Plant Families
  3. ^ Hill, K.D. & Stevenson, D.W. (1999). A world list of Cycads, 1999. Excelsa 19: 67-72.
  4. ^ Flora of North America, vol 2, Zamia integrifolia Linnaeus f. in Aiton, Hort. Kew. 3: 478. 1789.
  5. ^ Standley, P. C. & J. A. Steyermark. 1958. Cycadaceae. In Standley, P.C. & Steyermark, J.A. (Eds), Flora of Guatemala - Part I. Fieldiana, Bot. 24(1): 11–20.
  6. ^ Monteza-Moreno, Claudio M.; Rodriguez-Castro, Lilisbeth; Castillo-Caballero, Pedro L.; Toribio, Edgar; Saltonstall, Kristin (2022). "Arboreal camera trapping sheds light on seed dispersal of the world's only epiphytic gymnosperm: Zamia pseudoparasitica". Ecology and Evolution. 12 (3): e8769. Bibcode:2022EcoEv..12E8769M. doi:10.1002/ece3.8769. PMC 8948316. PMID 35356569.
  7. ^ Nicolalde-Morejón, F., A. P. Vovides & D. W. Stevenson. 2009. Taxonomic revision of Zamia in Mega-Mexico. Brittonia 61(4): 301–335.
  8. ^ Stevenson 2004, p. 197, 202.
  9. ^ Lindstrom 2009, pp. 269–270.
  10. ^ a b c Calonje et al. 2021, p. 1.
  11. ^ Armstrong, W.P. (2008-04-03). "Botanical Record-Breakers (Part 1 of 2)". Wayne's Word. Archived from the original on 2010-12-19. Retrieved 2011-01-12.
  12. ^ Segalla, Rosane; Telles, Francismeire Jane; Pinhiero, Fabio; Morellato, Patricia (October 22, 2019). "A Review of Current Knowledge of Zamiaceae, with Emphsis on Zamia From South America". Tropical Conservation Science. 12. Mutualistic Interaction: Plant-Pollinators. doi:10.1177/1940082919877479.
  13. ^ Segalla, Rosane; Telles, Francismeire Jane; Pinhiero, Fabio; Morellato, Patricia (October 22, 2019). "A Review of Current Knowledge of Zamiaceae, with Emphsis on Zamia From South America". Tropical Conservation Science. 12. Mutualistic Interaction: Seed Dispersers and Consumers. doi:10.1177/1940082919877479.
  14. ^ Calonje et al. 2019, p. 286.
  15. ^ Stevenson, Dennis Wm. (1991). "The Zamiaceae of the Southeastern United States". Journal of the Arnold Arboretum, Supplementrary Series. 1: 381. doi:10.5962/p.315947. JSTOR 43782788.
  16. ^ Schneider, Dietrich; Wink, Michael; Sporer, Frank; Lounibos, Philip (July 2002). "Cycads: their evolution, toxins, herbivores and insect pollinators". Naturwissenschaften. 89 (7): 283. Bibcode:2002NW.....89..281S. doi:10.1007/s00114-002-0330-2. PMID 12216856 – via Springer Link.
  17. ^ Holtcamp, Wendee (1 March 2012). "The Emerging Science of BMAA: Do Cyanobacteria Contribute to Neurodegenerative Disease?". Environmental Health Perspectives. 120 (3): a110–a116. doi:10.1289/ehp.120-a110. PMC 3295368. PMID 22382274.
  18. ^ Reams, Rachel Y.; Janovitz, Evan B.; Robinson, Farrel R.; Sullivan, John M.; Casanova, Carlos Rivera; Más, Edwin (July 1993). "Cycad (Zamia Puertoriquensis) Toxicosis in a Group of Dairy Heifers in Puerto Rico". Journal of Veterinary Diagnostic Investigation. 5 (3): 488–494. doi:10.1177/104063879300500337. ISSN 1040-6387. PMID 8373871.
  19. ^ Calonje et al. 2019, p. 294.
  20. ^ Calonje et al. 2019, pp. 287–288.
  21. ^ Zonneveld, B. J. M.; Lindström, A. J. (26 May 2016). "Genome sizes for 71 species of Zamia (Cycadales: Zamiaceae) correspond to three different biogeographic regions". Nordic Journal of Botany. 34 (6): 744–751. doi:10.1111/njb.01094.
  22. ^ a b Calonje et al. 2019, pp. 287–294.
  23. ^ a b c d e Lindstrom et al. 2024, pp. 10 (chart), 16–17.
  24. ^ Calonje et al. 2019, p. 301.
  25. ^ Lindstrom et al. 2024, p. 762.
  26. ^ Calonje et al. 2019, pp. 296 (tree).
  27. ^ Lindstrom et al. 2024, pp. 10 (tree), 19.
  28. ^ Calonje et al. 2021, pp. 1, 5, 9.
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Sources

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