The genus comprises deciduousshrubs 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
Zamiasporophylls 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
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
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
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
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]
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]
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
Fischeri clade
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
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]
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 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
Chigua was described as a new genus with two species in Zamiaceae in 1990, but was reclassified as Zamia restrepoi in 2009.[34]
^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.
^Z. imbricata is accepted in WLC, Kew, and Tropicos.
^Z. lawsoniana is accepted in WLC, Kew, and Tropicos.
^Z. magnifica is accepted in WLC, Kew, and Tropicos.
^Z. multidentata is accepted in WLC, Kew, and Tropicos.
^"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.
^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.
^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. JSTOR43782788.
^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. PMID12216856 – via Springer Link.
^Calonje, M.; Stevenson, Dennis; Osborne, Roy (2024). "About the World List of Cycads". World List of Cycads. Retrieved October 14, 2024.
^Calonje, Michael; Meerow, Alan W.; Knowles, Lindy; Knowles, David; Griffith, M. Patrick; Nakamura, Kyoko; Francisco-Ortega, Javier (April 2013). "Cycad biodiversity in the Bahamas Archipelago and conservation genetics of the threatened Zamia lucayana (Zamiaceae)". Oryx. 47 (2). Introduction. doi:10.1017/S0030605312000129.
Lindstrom, Anders; Nabib, Sadaf; Dong, Shanshan; Dong, Yiqing; Liu, Jiang; Calonje, Michael; Stevenson, Dennis; Zhang, Shouzhou (2024). "Transcriptome sequencing data provide a solid base to understand phylogenetic relationships, biogeography and reticulated evolution of the genus Zamia L. (Cycadales, Zamiaceae)". Annals of Botany. XX (5): 747–768. doi:10.1093/aob/mcae065. PMC 11560380. PMID38900840.
