Chemical Element Concentrations of Cycad Leaves: Do We Know Enough?

Abstract

The literature containing which chemical elements are found in cycad leaves was reviewed to determine the range in values of concentrations reported for essential and beneficial elements. We found 46 of the 358 described cycad species had at least one element reported to date. The only genus that was missing from the data was Microcycas. Many of the species reports contained concentrations of one to several macronutrients and no other elements. The cycad leaves contained greater nitrogen and phosphorus concentrations than the reported means for plants throughout the world. Magnesium was identified as the macronutrient that has been least studied. Only 14 of the species were represented by data from in situ locations, with most of the data obtained from managed plants in botanic gardens. Leaf element concentrations were influenced by biotic factors such as plant size, leaf age, and leaflet position on the rachis. Leaf element concentrations were influenced by environmental factors such as incident light and soil nutrient concentrations within the root zone. These influential factors were missing from many of the reports, rendering the results ambiguous and comparisons among studies difficult. Future research should include the addition of more taxa, more in situ locations, the influence of season, and the influence of herbivory to more fully understand leaf nutrition for cycads.

1. Background

Effective horticultural management of economic crops or threatened plant taxa requires an adequate understanding of essential nutrient accumulation, partitioning among organs, and remobilization prior to organ senescence. These biological phenomena influence many issues such as attractiveness to herbivores, the speed of litter decomposition, and soil changes within the zone of root proliferation and leaf litterfall. Knowledge of the concentrations of essential elements in plant organs is useful for determining plant health, diagnosing the cause of an observable problem, and measuring the efficacy of a fertilizer program [1,2,3]. Therefore, plant tissue analysis has been part of the traditional toolbox to meet management goals in agronomy, horticulture, and silviculture or to improve knowledge about the ecology of tree species.

In any testing procedure designed to determine the presence or absence of a measurable component from a sample, adherence to protocols that were developed through verifiable research is mandatory for achieving unambiguous results [4]. Moreover, recording and reporting the biological and environmental factors which are known to influence plant nutrient concentrations are necessary for methods to become standardized and repeatable, engender trust in the results, and to justify comparisons among studies.

The group of gymnosperm plants known as cycads is comprised of the mono-generic Cycadaceae family with 117 species and the Zamiaceae family with nine genera and 241 described species [5]. Research in applied sciences such as horticulture has been insufficient for members of this plant group [6,7]. For example, the global agenda of understanding how leaf element concentrations correlate with leaf functional traits has not sufficiently included cycad species [8]. This research agenda has expanded substantially in the past six years, and the subject has never been reviewed to date.

The aim of our review is to report which taxonomic groups have been most studied, to compile a listing of the published chemical element concentration data for cycad leaves, and to establish protocols for continued research to ensure the results are comparable among the various laboratories that contribute to the agenda in the future. Moreover, we conclude with a discussion of possible future research directions with the hope of inspiring more demanding protocols to better meet horticulture and conservation goals.

2. Species Studied

The literature search identified 18 publications in the primary literature in which the concentration of at least one chemical element was reported as a constituent of leaf tissue for at least one cycad species. Our primary focus was the essential nutrients, those chemical elements that are directly involved in plant function and are required by plants to complete the life cycle. Macronutrients are required in greater quantities, and micronutrients are required in small amounts. We also report beneficial nutrients, those chemical elements that may stimulate growth in some plants but do not meet the requirements of being essential. Other chemical elements which were reported in some studies were not included in this review. The numerical concentrations of elements which were presented in figures were estimated. Some reports used logarithmic data to meet parametric statistical requirements or to smooth regression modeling. In order to standardize our reported data into one format, we transformed these data to numerical concentrations. Misspelled species names were corrected and included if the mistake was easily diagnosed. Data were not included if misspelled species names could not be determined to be a currently accepted species. Synonyms or other obsolete names with an accepted binomial [5] were reported for the currently accepted binomial. These methods identified a total of 46 cycad species from the literature search (

Table 1. Forty-six cycad species with reported leaf element concentrations.

Species	Family	Taxonomic Authority	Native Range
Bowenia serrulata	Zamiaceae	(W. Bull) Chamb.	Australia
Bowenia spectabilis	Zamiaceae	Hook. ex Hook.f.	Australia
Ceratozamia mexicana	Zamiaceae	Brongn.	Mexico
Cycas armstrongii	Cycadaceae	Miq.	Australia
Cycas debaoensis	Cycadaceae	Y.C.Zhong & C.J.Chen	China
Cycas diannanensis	Cycadaceae	Z.T.Guan & G.D. Tao	China
Cycas elongata	Cycadaceae	(Leandri) D.Yue Wang	Vietnam
Cycas fairylakea	Cycadaceae	(Leandri) D.Yue Wang	China
Cycas media	Cycadaceae	R.Br.	Australia
Cycas micholitzii	Cycadaceae	Dyer	Laos, Vietnam
Cycas micronesica	Cycadaceae	K.D. Hill	Guam, Rota, Palau, Yap
Cycas nitida	Cycadaceae	K.D.Hill & A.Lindstr.	Philippines
Cycas nongnoochiae	Cycadaceae	K.D.Hill	Thailand
Cycas panzhihuaensis	Cycadaceae	L.Zhou & S.Y.Yang	China
Cycas revoluta	Cycadaceae	Thunb.	China, Japan
Cycas rumphii	Cycadaceae	Miq.	Australia, Indonesia, Papua New Guinea
Cycas sexseminifera	Cycadaceae	F.N.Wei	China, Vietnam
Cycas siamensis	Cycadaceae	Miq.	Cambodia, Laos, Myanmar, Thailand, Vietnam
Cycas szechuanensis	Cycadaceae	W.C.Cheng & L.K.Fu	China
Cycas thouarsii	Cycadaceae	R.Br. ex Gaudich	Comoros, Kenya, Madagascar, Mozambique, Seychelles, Tanzania
Cycas wadei	Cycadaceae	Merr.	Philippines
Dioon edule	Zamiaceae	Lindl.	Mexico
Dioon mejiae	Zamiaceae	Standl. & L.O.Williams	Honduras
Dioon sonorense	Zamiaceae	(De Luca, Sabato & Vázq.Torres) Chemnick, T.J.Greg. & Salas-Mor.	Mexico
Dioon spinulosum	Zamiaceae	Dyer ex Eichler	Mexico
Encephalartos cupidus	Zamiaceae	R.A.Dyer	South Africa
Encephalartos ferox	Zamiaceae	G.Bertol	Mozambique, South Africa
Encephalartos gratus	Zamiaceae	Prain	Malawi, Mozambique
Lepidozamia hopei	Zamiaceae	Regel	Australia
Lepidozamia peroffskyana	Zamiaceae	Regel	Australia
Macrozamia communis	Zamiaceae	L.A.S.Johnson	Australia
Macrozamia lucida	Zamiaceae	L.A.S.Johnson	Australia
Macrozamia macleayi	Zamiaceae	Miq.	Australia
Macrozamia moorei	Zamiaceae	F.Muell.	Australia
Macrozamia mountperriensis	Zamiaceae	F.M.Bailey	Australia
Macrozamia parcifolia	Zamiaceae	P.I.Forst. & D.L.Jones	Australia
Macrozamia reidlei	Zamiaceae	(Gaudich.) C.A.Gardner	Australia
Macrozamia serpentina	Zamiaceae	D.L.Jones & P.I.Forst	Australia
Stangeria eriopus	Zamiaceae	(Kunze) Baill.	South Africa
Zamia erosa	Zamiaceae	O.F.Cook & G.N.Collins	Cuba, Jamaica, Puerto Rico
Zamia fischeri	Zamiaceae	Miq.	Mexico
Zamia furfuracea	Zamiaceae	L.f.	Mexico
Zamia integrifolia	Zamiaceae	L.f.	Bahamas, Cayman Islands, Cuba, United States
Zamia portoricensis	Zamiaceae	Urb.	Puerto Rico
Zamia splendens	Zamiaceae	Schutzman	Mexico
Zamia standleyi	Zamiaceae	Schutzman	Guatemala, Honduras
Zamia vazquezii	Zamiaceae	D.W.Stev., Sabato & De Luca	Mexico

). In addition to the taxonomic authority, we also included the countries in which each species is considered endemic or indigenous. Leaf sampling from plants growing within natural habitat were considered “in situ” and leaf sampling from plants that were growing in managed gardens were considered “ex situ.”

3. Green Leaf Elements

3.1. The Elements

Laboratory methods have varied among the years and among laboratories. The oldest articles in our review quantified nitrogen with Kjeldahl digestion, and most contemporary articles employ dry combustion approaches for nitrogen. The other minerals and metals are digested from the tissue, with nitric acid being used most often. Quantification is done with spectrometry most common in the earliest publications and spectroscopy being used more often in recent years. Macronutrient concentrations in cycad leaf tissue were highly variable among the elements. The total carbon found in cycad leaves was less variable than the other elements and ranged from 438–566 mg·g⁻¹ among taxa of nine genera (

Table 2. Published ranges in green leaf concentrations of macronutrients, micronutrients, and beneficial elements for cycad plants.

Element	Genera	Species Studied	Species in Genus	Range	Reference
Aluminum	Cycas	1	117	22–60 mg·kg−1	[23]
Boron	Cycas	2	117	11.6–43.4 mg·kg−1	[11,12,13,14,20]
Calcium	Bowenia	2	2	5.0–6.1 mg·g−1	[9]
Calcium	Ceratozamia	1	32	7.1 mg·g−1	[9]
Calcium	Cycas	14	117	1.2–23.7 mg·g−1	[9,11,12,13,14,17,18,20,24]
Calcium	Dioon	3	16	7.6–8.4 mg·g−1	[9]
Calcium	Encephalartos	3	65	4.5–14.3 mg·g−1	[9]
Calcium	Lepidozamia	2	2	3.6–5.0 mg·g−1	[9]
Calcium	Macrozamia	4	41	1.4–7.1 mg·g−1	[9,23]
Calcium	Stangeria	1	1	7.1 mg·g−1	[9]
Calcium	Zamia	5	81	3.0–7.7 mg·g−1	[9]
Carbon	Bowenia	2	2	508–519 mg·g−1	[9]
Carbon	Ceratozamia	1	32	514 mg·g−1	[9]
Carbon	Cycas	13	117	463–509 mg·g−1	[9,10,11,12,13,14,17]
Carbon	Dioon	3	16	485–496 mg·g−1	[9]
Carbon	Encephalartos	3	65	490–505 mg·g−1	[9]
Carbon	Lepidozamia	2	2	438–566 mg·g−1	[9,16]
Carbon	Macrozamia	5	41	512–524 mg·g−1	[9,16]
Carbon	Stangeria	1	1	479 mg·g−1	[9]
Carbon	Zamia	7	81	477–491 mg·g−1	[9,15]
Chloride	Cycas	1	117	0.5–2.3 mg·g−1	[24]
Copper	Cycas	2	117	2.0–17.9 mg·kg−1	[11,12,13,14,18,20]
Copper	Macrozamia	1	41	2.1–2.8 mg·kg−1	[22]
Iron	Bowenia	2	2	189–207 mg·kg−1	[9]
Iron	Ceratozamia	1	32	106 mg·kg−1	[9]
Iron	Cycas	14	117	27–410 mg·kg−1	[9,11,12,13,14,18,19,20,24]
Iron	Dioon	3	16	117–163 mg·kg−1	[9]
Iron	Encephalartos	3	65	93–363 mg·kg−1	[9,19]
Iron	Lepidozamia	2	2	166–176 mg·kg−1	[9]
Iron	Macrozamia	3	41	83–253 mg·kg−1	[9]
Iron	Stangeria	1	1	228 mg·kg−1	[9]
Iron	Zamia	6	81	142–1700 mg·kg−1	[9,19]
Magnesium	Cycas	4	117	1.4–8.2 mg·g−1	[11,12,13,14,17,18,20,24]
Magnesium	Macrozamia	1	41	1.1–1.9 mg·g−1	[22]
Manganese	Cycas	3	117	20–152 mg·kg−1	[11,12,13,14,18,20,24]
Manganese	Macrozamia	1	41	6–57 mg·kg−1	[22]
Nitrogen	Bowenia	2	2	24–41 mg·g−1	[9,16]
Nitrogen	Ceratozamia	1	32	13 mg·g−1	[9]
Nitrogen	Cycas	17	117	16–44 mg·g−1	[9,10,11,12,13,14,15,16,17,18,19,20,21]
Nitrogen	Dioon	4	16	14–17 mg·g−1	[9,22]
Nitrogen	Encephalartos	3	65	15–19 mg·g−1	[9,19]
Nitrogen	Lepidozamia	2	2	17–31 mg·g−1	[9,16]
Nitrogen	Macrozamia	8	41	8–55 mg·g−1	[9,16,21,23]
Nitrogen	Stangeria	1	1	22 mg·g−1	[9]
Nitrogen	Zamia	8	81	12–30 mg·g−1	[9,15,19]
Phosphorus	Bowenia	2	2	1.0–1.1 mg·g−1	[9]
Phosphorus	Ceratozamia	1	32	0.8 mg·g−1	[9]
Phosphorus	Cycas	14	117	0.7–3.4 mg·g−1	[9,10,11,12,13,14,17,18,19,20]
Phosphorus	Dioon	3	16	0.8–1.5 mg·g−1	[9]
Phosphorus	Encephalartos	3	65	1.0–1.3 mg·g−1	[9,19]
Phosphorus	Lepidozamia	2	2	0.8–1.2 mg·g−1	[9]
Phosphorus	Macrozamia	4	41	0.5–1.2 mg·g−1	[9,21]
Phosphorus	Stangeria	1	1	1.1 mg·g−1	[9]
Phosphorus	Zamia	6	81	0.7–1.3 mg·g−1	[9,19]
Potassium	Bowenia	2	2	5.5–6.2 mg·g−1	[9]
Potassium	Ceratozamia	1	32	4.9 mg·g−1	[9]
Potassium	Cycas	15	117	3.1–23.7 mg·g−1	[9,10,11,12,13,14,17,18,20,24]
Potassium	Dioon	3	16	5.7–11.5 mg·g−1	[9,19]
Potassium	Encephalartos	3	65	6.2–8.9 mg·g−1	[9]
Potassium	Lepidozamia	2	2	9.5–10.6 mg·g−1	[9]
Potassium	Macrozamia	4	41	5.1–11.3 mg·g−1	[9,23]
Potassium	Stangeria	1	1	8.0 mg·g−1	[9]
Potassium	Zamia	6	81	4.6–18.0 mg·g−1	[9]
Selenium	Cycas	2	117	0.41–0.58 mg·kg−1	[11,12]
Sodium	Cycas	2	117	0.2–1.2 mg·g−1	[12,24]
Sodium	Macrozamia	1	41	0.3–1.0 mg·g−1	[23]
Sulfur	Bowenia	2	2	1.9 mg·g−1	[9]
Sulfur	Ceratozamia	1	32	1.4 mg·g−1	[9]
Sulfur	Cycas	12	117	0.8–2.6 mg·g−1	[9,17,19,20]
Sulfur	Dioon	3	16	1.1–1.4 mg·g−1	[9]
Sulfur	Encephalartos	3	65	0.8–2.2 mg·g−1	[9,19]
Sulfur	Lepidozamia	2	2	1.4–1.6 mg·g−1	[9]
Sulfur	Macrozamia	4	41	0.8–1.9 mg·g−1	[9,23]
Sulfur	Stangeria	1	1	2.3 mg·g−1	[9]
Sulfur	Zamia	5	81	0.6–13.7 mg·g−1	[9,19]
Zinc	Bowenia	2	2	19–21 mg·kg−1	[9]
Zinc	Ceratoamia	1	32	24 mg·kg−1	[9]
Zinc	Cycas	14	117	6–70 mg·kg−1	[9,11,12,13,14,18,20,24]
Zinc	Dioon	3	16	12–23 mg·kg−1	[9]
Zinc	Encephalartos	3	65	11–22 mg·kg−1	[9]
Zinc	Lepidozamia	2	2	23–25 mg·kg−1	[9]
Zinc	Macrozamia	4	41	4–22 mg·kg−1	[9,22]
Zinc	Stangeria	1	1	53 mg·kg−1	[9]
Zinc	Zamia	6	81	11–38 mg·kg−1	[9]

) [9,10,11,12,13,14,15,16,17]. The range in nitrogen concentration in the cycad leaf tissue was considerable, with a 6.9-fold difference among the species and studies and considerable overlap among the nine genera [9,10,11,12,13,14,15,16,17,18,19,20,21,22,23]. The phosphorus concentration of the cycad leaf tissue was less variable than nitrogen, with a 4.9-fold difference among the species and studies represented by nine genera [9,10,11,12,13,14,17,18,19,20]. Potassium concentration was highly variable with a 7.6-fold difference among the nine genera studied [9,10,11,12,13,14,17,18,19,20,23,24]. Magnesium was determined for only two genera, yet the range in concentration was substantial with a 7.5-fold difference among the studies [11,12,13,14,17,18,20,22,24]. The calcium concentration of cycad leaf tissue was more variable than the other macronutrients, with a 19.8-fold difference among the nine genera and studies [9,11,12,13,14,17,18,20,23,24]. Sulfur concentration in cycad leaf tissue was also highly variable with a 22.8-fold difference among the nine genera and studies [9,17,19,20,23].

Micronutrient concentrations in cycad leaf tissue were also highly variable among the elements and studies. Iron and zinc were the only micronutrients included in numerous articles, with nine genera represented among the studies for each element (Table 2). Iron was also the only element exhibiting one extreme outlier species, with Zamia fischeri [9,18] exhibiting iron concentrations more than 4-fold greater than the range of the remaining 33 species that have been studied [9,11,12,13,14,18,19,20,24]. The remaining micronutrients have not been observed adequately. Leaf chloride concentrations were reported for a single Cycas species [24], boron concentrations were reported for only two species [11,12,13,14,20], copper concentrations were reported for three species [11,12,13,14,18,20,22], and manganese concentrations were reported for four species [11,12,13,14,18,20,22,24]. The cycad leaf content of the micronutrients molybdenum and nickel have not been reported for any cycad species.

Several beneficial elements have been reported from cycad leaf tissue (Table 2). Aluminum concentration has been reported for one species [23], selenium has been reported for two species [11,12], and sodium has been reported for three species [12,23,24]. The remaining beneficial nutrients have not been studied in the context of cycad leaf physiology.

3.2. The Taxa

Bowenia, Lepidozamia, and Stangeria contain only one or two species each, and every one of these species was included in the literature review (Table 2,

Table A1. Published ranges for green leaf element concentrations of cycad plants. Misspellings of species were corrected if identity was obvious, species that were misspelled were not included if identity was not obvious. Taxonomic synonyms were corrected. Data were estimated for reports displaying data as figures and transformed if data were presented in log format.

Element	Species	Range	Reference
Carbon	Bowenia serrulata	519 mg·g−1	[9]
Carbon	Bowenia spectabilis	508 mg·g−1	[9]
Carbon	Ceratozamia Mexicana	514 mg·g−1	[9]
Carbon	Cycas debaoensis	485 mg·g−1	[9]
Carbon	Cycas diannanensis	463 mg·g−1	[9] 1
Carbon	Cycas elongata	483 mg·g−1	[9]
Carbon	Cycas fairylakea	499 mg·g−1	[9]
Carbon	Cycas micholitzii	475 mg·g−1	[9]
Carbon	Cycas micronesica	479 mg·g−1	[12]
Carbon	Cycas micronesica	484–493 mg·g−1	[13]
Carbon	Cycas micronesica	480–505 mg·g−1	[14]
Carbon	Cycas micronesica	475–485 mg·g−1	[17]
Carbon	Cycas nitida	499–509 mg·g−1	[10]
Carbon	Cycas panzhihuaensis	466–504 mg·g−1	[9]
Carbon	Cycas sexseminifera	467 mg·g−1	[9]
Carbon	Cycas siamensis	469 mg·g−1	[9]
Carbon	Cycas szechuanensis	475–498 mg·g−1	[9]
Carbon	Cycas thouarsii	497 mg·g−1	[9]
Carbon	Cycas wadei	508 mg·g−1	[11]
Carbon	Dioon edule	496 mg·g−1	[9]
Carbon	Dioon mejiae	485 mg·g−1	[9]
Carbon	Dioon spinulosum	486 mg·g−1	[9]
Carbon	Encephalartos cupidus	490 mg·g−1	[9]
Carbon	Encephalartos ferox	494 mg·g−1	[9]
Carbon	Encephalartos gratus	497–505 mg·g−1	[9]
Carbon	Lepidozamia hopei	515 mg·g−1	[9]
Carbon	Lepidozamia peroffskyana	511 mg·g−1	[9]
Carbon	Lepidozamia peroffskyana	473–566 mg·g−1	[16]
Carbon	Macrozamia communis	512 mg·g−1	[9]
Carbon	Macrozamia communis	507–560 mg·g−1	[16]
Carbon	Macrozamia lucida	524 mg·g−1	[9]
Carbon	Macrozamia lucida	473–522 mg·g−1	[16]
Carbon	Macrozamia macleaya	438–508 mg·g−1	[16]
Carbon	Macrozamia moorei	519 mg·g−1	[9]
Carbon	Macrozamia riedlei	455–525 mg·g−1	[16]
Carbon	Stangeria eriopus	479 mg·g−1	[9]
Carbon	Zamia erosa	495 mg·g−1	[9] 2
Carbon	Zamia erosa	481 mg·g−1	[15]
Carbon	Zamia fischeri	458 mg·g−1	[9] 3
Carbon	Zamia furfuracea	477–489 mg·g−1	[9]
Carbon	Zamia integrifolia	490–491 mg·g−1	[9]
Carbon	Zamia portoricensis	484 mg·g−1	[15]
Carbon	Zamia splendens	483 mg·g−1	[9]
Carbon	Zamia vazquezii	488 mg·g−1	[9]
Nitrogen	Bowenia serrulata	24 mg·g−1	[9]
Nitrogen	Bowenia serrulata	41 mg·g−1	[16]
Nitrogen	Bowenia spectabilis	24 mg·g−1	[9]
Nitrogen	Ceratozamia mexicana	13 mg·g−1	[9]
Nitrogen	Cycas armstrongii	21 mg·g−1	[21]
Nitrogen	Cycas debaoensis	28 mg·g−1	[9]
Nitrogen	Cycas diannanensis	26 mg·g−1	[9] 1
Nitrogen	Cycas diannanensis	26 mg·g−1	[19] 1
Nitrogen	Cycas elongata	28 mg·g−1	[9]
Nitrogen	Cycas fairylakea	25 mg·g−1	[9]
Nitrogen	Cycas media	44 mg·g−1	[16]
Nitrogen	Cycas micholitzii	25 mg·g−1	[9]
Nitrogen	Cycas micholitzii	25 mg·g−1	[19]
Nitrogen	Cycas micronesica	29–30 mg·g−1	[15]
Nitrogen	Cycas micronesica	25 mg·g−1	[12]
Nitrogen	Cycas micronesica	14–30 mg·g−1	[18]
Nitrogen	Cycas micronesica	18–27 mg·g−1	[13]
Nitrogen	Cycas micronesica	18–29 mg·g−1	[14]
Nitrogen	Cycas micronesica	23–37 mg·g−1	[17]
Nitrogen	Cycas micronesica	17–30 mg·g−1	[20]
Nitrogen	Cycas nitida	24–28 mg·g−1	[10]
Nitrogen	Cycas nongnoochiae	26–30 mg·g−1	[20]
Nitrogen	Cycas panhihuaensis	16–21 mg·g−1	[9]
Nitrogen	Cycas panhihuaensis	16 mg·g−1	[19]
Nitrogen	Cycas rumphii	30–31 mg·g−1	[15]
Nitrogen	Cycas sexseminifera	19 mg·g−1	[9]
Nitrogen	Cycas sexseminifera	19 mg·g−1	[19] 4
Nitrogen	Cycas siamensis	18 mg·g−1	[9]
Nitrogen	Cycas siamensis	19 mg·g−1	[19]
Nitrogen	Cycas szechuanensis	21–25 mg·g−1	[9]
Nitrogen	Cycas szechuanensis	21 mg·g−1	[19]
Nitrogen	Cycas thouarsii	23 mg·g−1	[9]
Nitrogen	Cycas wadei	21 mg·g−1	[11]
Nitrogen	Dioon edule	15 mg·g−1	[9]
Nitrogen	Dioon mejiae	14 mg·g−1	[9]
Nitrogen	Dioon sonorense	14–17 mg·g−1	[22]
Nitrogen	Dioon spinulosum	15 mg·g−1	[9]
Nitrogen	Encephalartos cupidus	17 mg·g−1	[9]
Nitrogen	Encephalartos cupidus	18 mg·g−1	[19]
Nitrogen	Encephalartos ferox	15 mg·g−1	[9]
Nitrogen	Encephalartos gratus	18–19 mg·g−1	[9]
Nitrogen	Encephalartos gratus	18 mg·g−1	[19]
Nitrogen	Lepidozamia hopei	17 mg·g−1	[9]
Nitrogen	Lepidozamia peroffskyana	19 mg·g−1	[9]
Nitrogen	Lepidozamia peroffskyana	18–31 mg·g−1	[16]
Nitrogen	Macrozamia communis	20 mg·g−1	[9]
Nitrogen	Macrozamia communis	10–38 mg·g−1	[16]
Nitrogen	Macrozamia lucida	21 mg·g−1	[9]
Nitrogen	Macrozamia lucida	14–22 mg·g−1	[16]
Nitrogen	Macrozamia macleayi	8–43 mg·g−1	[16]
Nitrogen	Macrozamia moorei	20 mg·g−1	[9]
Nitrogen	Macrozamia mountperriensis	54–55 mg·g−1	[16]
Nitrogen	Macrozamia parcifolia	47–49 mg·g−1	[16]
Nitrogen	Macrozamia riedlei	14 mg·g−1	[21]
Nitrogen	Macrozamia riedlei	11–15 mg·g−1	[23]
Nitrogen	Macrozamia riedlei	8–38 mg·g−1	[16]
Nitrogen	Macrozamia serpentina	28–31 mg·g−1	[16]
Nitrogen	Stangeria eriopus	22 mg·g−1	[9]
Nitrogen	Zamia erosa	18 mg·g−1	[9] 2
Nitrogen	Zamia erosa	26 mg·g−1	[15]
Nitrogen	Zamia fischeri	28 mg·g−1	[9] 3
Nitrogen	Zamia fischeri	28 mg·g−1	[19] 3
Nitrogen	Zamia furfuracea	12–14 mg·g−1	[9]
Nitrogen	Zamia furfuracea	13 mg·g−1	[19]
Nitrogen	Zamia integrifolia	18–21 mg·g−1	[9]
Nitrogen	Zamia portoricensis	18 mg·g−1	[15]
Nitrogen	Zamia splendens	15 mg·g−1	[9]
Nitrogen	Zamia standleyi	19 mg·g−1	[15]
Nitrogen	Zamia vazquezii	30 mg·g−1	[9]
Phosphorus	Bowenia serrulata	1.0 mg·g−1	[9]
Phosphorus	Bowenia spectabilis	1.1 mg·g−1	[9]
Phosphorus	Ceratozamia mexicana	0.8 mg·g−1	[9]
Phosphorus	Cycas debaoensis	1.4 mg·g−1	[9]
Phosphorus	Cycas diannanensis	2.4 mg·g−1	[9] 1
Phosphorus	Cycas diannanensis	2.4 mg·g−1	[19] 1
Phosphorus	Cycas elongata	1.2 mg·g−1	[9]
Phosphorus	Cycas fairylakea	1.1 mg·g−1	[9]
Phosphorus	Cycas micholitzii	1.5 mg·g−1	[9]
Phosphorus	Cycas micholitzii	1.5 mg·g−1	[19]
Phosphorus	Cycas micronesica	2.9 mg·g−1	[12]
Phosphorus	Cycas micronesica	1.2–2.7 mg·g−1	[18]
Phosphorus	Cycas micronesica	0.9–2.5 mg·g−1	[13]
Phosphorus	Cycas micronesica	0.8–2.8 mg·g−1	[14]
Phosphorus	Cycas micronesica	2.6–2.9 mg·g−1	[17]
Phosphorus	Cycas micronesica	1.5–2.9 mg·g−1	[20]
Phosphorus	Cycas nitida	1.1–1.9 mg·g−1	[10]
Phosphorus	Cycas nongnoochiae	1.3–3.4 mg·g−1	[20]
Phosphorus	Cycas panzhihuaensis	1.0–1.1 mg·g−1	[9]
Phosphorus	Cycas panzhihuaensis	1.1 mg·g−1	[19]
Phosphorus	Cycas sexseminifera	1.5 mg·g−1	[9]
Phosphorus	Cycas sexseminifera	1.2–1.5 mg·g−1	[19] 4
Phosphorus	Cycas siamensis	1.2 mg·g−1	[9]
Phosphorus	Cycas siamensis	1.2 mg·g−1	[19]
Phosphorus	Cycas szechuanensis	1.0–1.2 mg·g−1	[9]
Phosphorus	Cycas thouarsii	1.2 mg·g−1	[9]
Phosphorus	Cycas wadei	1.1 mg·g−1	[11]
Phosphorus	Dioon edule	0.8 mg·g−1	[9]
Phosphorus	Dioon mejiae	1.5 mg·g−1	[9]
Phosphorus	Dioon spinulosum	0.8 mg·g−1	[9]
Phosphorus	Encephalartos cupidus	1.2 mg·g−1	[9]
Phosphorus	Encephalartos cupidus	1.2 mg·g−1	[19]
Phosphorus	Encephalartos ferox	1.0 mg·g−1	[9]
Phosphorus	Encephalartos gratus	1.1–1.3 mg·g−1	[9]
Phosphorus	Encephalartos gratus	1.1 mg·g−1	[19]
Phosphorus	Lepidozamia hopei	0.8 mg·g−1	[9]
Phosphorus	Lepidozamia peroffskyana	1.2 mg·g−1	[9]
Phosphorus	Macrozamia communis	1.0 mg·g−1	[9]
Phosphorus	Macrozamia lucida	1.2 mg·g−1	[9]
Phosphorus	Macrozamia moorei	0.9 mg·g−1	[9]
Phosphorus	Macrozamia riedlei	0.5 mg·g−1	[21]
Phosphorus	Stangeria eriopus	1.1 mg·g−1	[9]
Phosphorus	Zamia erosa	1.0 mg·g−1	[9] 2
Phosphorus	Zamia fischeri	1.7 mg·g−1	[9] 3
Phosphorus	Zamia fischeri	1.7 mg·g−1	[19] 3
Phosphorus	Zamia furfuracea	0.7–0.8 mg·g−1	[9]
Phosphorus	Zamia furfuracea	0.7 mg·g−1	[19]
Phosphorus	Zamia integrifolia	1.3 mg·g−1	[9]
Phosphorus	Zamia splendens	0.8 mg·g−1	[9]
Phosphorus	Zamia vazquezii	0.7 mg·g−1	[9]
Potassium	Bowenia serrulata	5.5 mg·g−1	[9]
Potassium	Bowenia spectabilis	6.2 mg·g−1	[9]
Potassium	Ceratozamia mexicana	4.9 mg·g−1	[9]
Potassium	Cycas debaoensis	4.4 mg·g−1	[9]
Potassium	Cycas diannanensis	9.9 mg·g−1	[9] 1
Potassium	Cycas elongata	9.8 mg·g−1	[9]
Potassium	Cycas fairylakea	5.8 mg·g−1	[9]
Potassium	Cycas micholitzii	7.0 mg·g−1	[9]
Potassium	Cycas micronesica	15.3 mg·g−1	[12]
Potassium	Cycas micronesica	6.9–23.0 mg·g−1	[18]
Potassium	Cycas micronesica	3.8–22.1 mg·g−1	[13]
Potassium	Cycas micronesica	3.1–23.7 mg·g−1	[14]
Potassium	Cycas micronesica	14.9–16.4 mg·g−1	[17]
Potassium	Cycas micronesica	10.5–18.9 mg·g−1	[20]
Potassium	Cycas nitida	6.4–16.6 mg·g−1	[10]
Potassium	Cycas nongnoochiae	4.4–18.3 mg·g−1	[20]
Potassium	Cycas panzhihuaensis	5.8–7.7 mg·g−1	[9]
Potassium	Cycas revoluta	4.9–11.9 mg·g−1	[24]
Potassium	Cycas sexseminifera	4.3 mg·g−1	[9]
Potassium	Cycas siamensis	10.2 mg·g−1	[9]
Potassium	Cycas szechuanensis	3.7–5.7 mg·g−1	[9]
Potassium	Cycas thouarsii	8.8 mg·g−1	[9]
Potassium	Cycas wadei	7.4 mg·g−1	[11]
Potassium	Dioon edule	5.7 mg·g−1	[9]
Potassium	Dioon mejiae	11.5 mg·g−1	[9]
Potassium	Dioon spinulosum	7.9 mg·g−1	[9]
Potassium	Encephalartos cupidus	6.2 mg·g−1	[9]
Potassium	Encephalartos ferox	6.7 mg·g−1	[9]
Potassium	Encephalartos gratus	7.2–8.9 mg·g−1	[9]
Potassium	Lepidozamia hopei	9.5 mg·g−1	[9]
Potassium	Lepidozamia peroffskyana	10.6 mg·g−1	[9]
Potassium	Macrozamia communis	9.8 mg·g−1	[9]
Potassium	Macrozamia lucida	11.3 mg·g−1	[9]
Potassium	Macrozamia moorei	5.1 mg·g−1	[9]
Potassium	Macrozamia riedlei	6.5–9.2 mg·g−1	[23]
Potassium	Stangeria eriopus	8.0 mg·g−1	[9]
Potassium	Zamia erosa	10.0 mg·g−1	[9] 2
Potassium	Zamia fischeri	6.6 mg·g−1	[9] 3
Potassium	Zamia furfuracea	4.6–10.2 mg·g−1	[9]
Potassium	Zamia integrifolia	9.3–9.5 mg·g−1	[9]
Potassium	Zamia splendens	8.1 mg·g−1	[9]
Potassium	Zamia vazquezii	18.0 mg·g−1	[9]
Magnesium	Cycas micronesica	2.3 mg·g−1	[12]
Magnesium	Cycas micronesica	1.7–8.2 mg·g−1	[18]
Magnesium	Cycas micronesica	2.5–4.8 mg·g−1	[13]
Magnesium	Cycas micronesica	2.9–5.1 mg·g−1	[14]
Magnesium	Cycas micronesica	2.2–2.4 mg·g−1	[17]
Magnesium	Cycas micronesica	3.1–7.0 mg·g−1	[20]
Magnesium	Cycas nongnoochiae	2.4–2.6 mg·g−1	[20]
Magnesium	Cycas revoluta	1.9–3.1 mg·g−1	[24]
Magnesium	Cycas wadei	1.4 mg·g−1	[11]
Magnesium	Macrozamia reidlei	1.1–1.9 mg·g−1	[23]
Calcium	Bowenia serrulata	6.1 mg·g−1	[9]
Calcium	Bowenia spectabilis	5.0 mg·g−1	[9]
Calcium	Ceratozamia mexicana	7.1 mg·g−1	[9]
Calcium	Cycas debaoensis	11.8 mg·g−1	[9]
Calcium	Cycas diannanensis	11.4 mg·g−1	[9]
Calcium	Cycas elongata	11.6 mg·g−1	[9]
Calcium	Cycas fairylakea	3.9 mg·g−1	[9]
Calcium	Cycas micholitzii	2.7 mg·g−1	[9]
Calcium	Cycas micronesica	2.8 mg·g−1	[12]
Calcium	Cycas micronesica	7.1–23.7 mg·g−1	[18]
Calcium	Cycas micronesica	1.2–8.6 mg·g−1	[13]
Calcium	Cycas micronesica	7.8–10.6 mg·g−1	[14]
Calcium	Cycas micronesica	2.5–3.1 mg·g−1	[17]
Calcium	Cycas micronesica	3.1–19.9 mg·g−1	[20]
Calcium	Cycas nongnoochiae	3.2–7.0 mg·g−1	[20]
Calcium	Cycas panzhihuaensis	6.6–7.0 mg·g−1	[9]
Calcium	Cycas revoluta	7.7–15.6 mg·g−1	[24]
Calcium	Cycas sexseminifera	8.6 mg·g−1	[9]
Calcium	Cycas siamensis	9.9 mg·g−1	[9]
Calcium	Cycas szechuanensis	1.4–2.8 mg·g−1	[9]
Calcium	Cycas thouarsii	6.3 mg·g−1	[9]
Calcium	Cycas wadei	2.51 mg·g−1	[11]
Calcium	Dioon edule	7.7 mg·g−1	[9]
Calcium	Dioon mejiae	8.4 mg·g−1	[9]
Calcium	Dioon spinulosum	7.6 mg·g−1	[9]
Calcium	Encephalartos cupidus	4.5 mg·g−1	[9]
Calcium	Encephalartos ferox	14.3 mg·g−1	[9]
Calcium	Encephalartos gratus	4.7–6.2 mg·g−1	[9]
Calcium	Lepidozamia hopei	5.0 mg·g−1	[9]
Calcium	Lepidozamia peroffskyana	3.6 mg·g−1	[9]
Calcium	Macrozamia communis	1.4 mg·g−1	[9]
Calcium	Macrozamia lucida	2.8 mg·g−1	[9]
Calcium	Macrozamia moorei	4.7 mg·g−1	[9]
Calcium	Macrozamia riedlei	3.1–7.1 mg·g−1	[23]
Calcium	Stangeria eriopus	7.1 mg·g−1	[9]
Calcium	Zamia erosa	3.0 mg·g−1	[9] 2
Calcium	Zamia fischeri	7.7 mg·g−1	[9] 3
Calcium	Zamia furfuracea	4.9–7.0 mg·g−1	[9]
Calcium	Zamia integrifolia	4.2–4.3 mg·g−1	[9]
Calcium	Zamia splendens	4.4 mg·g−1	[9]
Calcium	Zamia vazquezii	6.7 mg·g−1	[9]
Chloride	Cycas revoluta	0.5–2.3 mg·g−1	[24]
Sodium	Cycas micronesica	0.5 mg·g−1	[12]
Sodium	Cycas revoluta	0.2–1.2 mg·g−1	[24]
Sodium	Macrozamia reidlei	0.3–1.0 mg·g−1	[23]
Sulfur	Bowenia serrulata	1.9 mg·g−1	[9]
Sulfur	Bowenia spectabilis	1.9 mg·g−1	[9]
Sulfur	Ceratozamia mexicana	1.4 mg·g−1	[9]
Sulfur	Cycas debaoensis	2.6 mg·g−1	[9]
Sulfur	Cycas diannanensis	1.6 mg·g−1	[9] 1
Sulfur	Cycas diannanensis	1.6 mg·g−1	[19] 1
Sulfur	Cycas elongata	2.0 mg·g−1	[9]
Sulfur	Cycas fairylakea	1.7 mg·g−1	[9]
Sulfur	Cycas micholitzii	1.4 mg·g−1	[9]
Sulfur	Cycas micholitzii	1.4 mg·g−1	[19]
Sulfur	Cycas micronesica	1.2–1.6 mg·g−1	[17]
Sulfur	Cycas micronesica	1.1 mg·g−1	[20]
Sulfur	Cycas nongnoochiae	1.4 mg·g−1	[20]
Sulfur	Cycas panzhihuaensis	0.9–1.4 mg·g−1	[9]
Sulfur	Cycas panzhihuaensis	0.8 mg·g−1	[19]
Sulfur	Cycas sexseminifera	1.0 mg·g−1	[9]
Sulfur	Cycas sexseminifera	0.9 mg·g−1	[19] 4
Sulfur	Cycas siamensis	1.3 mg·g−1	[9]
Sulfur	Cycas siamensis	1.3 mg·g−1	[19]
Sulfur	Cycas szechuanensis	1.1–1.4 mg·g−1	[9]
Sulfur	Cycas szechuanensis	1.1 mg·g−1	[19]
Sulfur	Cycas thouarsii	1.4 mg·g−1	[9]
Sulfur	Dioon edule	1.4 mg·g−1	[9]
Sulfur	Dioon mejiae	1.4 mg·g−1	[9]
Sulfur	Dioon spinulosum	1.1 mg·g−1	[9]
Sulfur	Encephalartos cupidus	1.2 mg·g−1	[9]
Sulfur	Encephalartos cupidus	1.2 mg·g−1	[19]
Sulfur	Encephalartos ferox	1.3 mg·g−1	[9]
Sulfur	Encephalartos gratus	0.9–2.2 mg·g−1	[9]
Sulfur	Encephalartos gratus	0.8 mg·g−1	[19]
Sulfur	Lepidozamia hopei	1.6 mg·g−1	[9]
Sulfur	Lepidozamia peroffskyana	1.4 mg·g−1	[9]
Sulfur	Macrozamia communis	1.2 mg·g−1	[9]
Sulfur	Macrozamia lucida	1.9 mg·g−1	[9]
Sulfur	Macrozamia moorei	1.0 mg·g−1	[9]
Sulfur	Macrozamia riedlei	0.8–1.2 mg·kg−1	[23]
Sulfur	Stangeria eriopus	2.3 mg·g−1	[9]
Sulfur	Zamia erosa	1.0 mg·g−1	[9] 2
Sulfur	Zamia fischeri	2.7 mg·g−1	[9] 3
Sulfur	Zamia fischeri	2.7 mg·g−1	[19] 3
Sulfur	Zamia furfuracea	0.6–1.5 mg·g−1	[9]
Sulfur	Zamia furfuracea	0.6 mg·g−1	[19]
Sulfur	Zamia integrifolia	13.6–13.7 mg·g−1	[9]
Sulfur	Zamia splendens	1.1 mg·g−1	[9]
Sulfur	Zamia vazquezii	2.9 mg·g−1	[9]
Iron	Bowenia serrulata	189 mg·kg−1	[9]
Iron	Bowenia spectabilis	207 mg·kg−1	[9]
Iron	Ceratozamia mexicana	106 mg·kg−1	[9]
Iron	Cycas debaoensis	114 mg·kg−1	[9]
Iron	Cycas diannanensis	406 mg·kg−1	[9] 1
Iron	Cycas diannanensis	406 mg·kg−1	[19] 1
Iron	Cycas elongata	149 mg·kg−1	[9]
Iron	Cycas fairylakea	98 mg·kg−1	[9]
Iron	Cycas micholitzii	340 mg·kg−1	[9]
Iron	Cycas micholitzii	345 mg·kg−1	[19]
Iron	Cycas micronesica	43.5 mg·kg−1	[12]
Iron	Cycas micronesica	38.5–88.6 mg·kg−1	[18]
Iron	Cycas micronesica	39.6–46.8 mg·kg−1	[13]
Iron	Cycas micronesica	26.8–56.9 mg·kg−1	[14]
Iron	Cycas micronesica	71.4 mg·kg−1	[20]
Iron	Cycas nongnoochiae	76.4 mg·kg−1	[20]
Iron	Cycas panzhihuaensis	134–215 mg·kg−1	[9]
Iron	Cycas panzhihuaensis	225 mg·kg−1	[19]
Iron	Cycas revoluta	31 mg·kg−1	[24]
Iron	Cycas sexseminifera	311 mg·kg−1	[9]
Iron	Cycas sexseminifera	300 mg·kg−1	[19] 4
Iron	Cycas siamensis	218 mg·kg−1	[9]
Iron	Cycas siamensis	225 mg·kg−1	[19]
Iron	Cycas szechuanensis	234–304 mg·kg−1	[9]
Iron	Cycas szechuanensis	300 mg·kg−1	[19]
Iron	Cycas thouarsii	166 mg·kg−1	[9]
Iron	Cycas wadei	71.3 mg·kg−1	[11]
Iron	Dioon edule	163 mg·kg−1	[9]
Iron	Dioon mejiae	117 mg·kg−1	[9]
Iron	Dioon spinulosum	123 mg·kg−1	[9]
Iron	Encephalartos cupidus	363 mg·kg−1	[9]
Iron	Encephalartos cupidus	355 mg·kg−1	[19]
Iron	Encephalartos ferox	93 mg·kg−1	[9]
Iron	Encephalartos gratus	121–339 mg·kg−1	[9]
Iron	Encephalartos gratus	340 mg·kg−1	[19]
Iron	Lepidozamia hopei	176 mg·kg−1	[9]
Iron	Lepidozamia peroffskyana	166 mg·kg−1	[9]
Iron	Macrozamia communis	83 mg·kg−1	[9]
Iron	Macrozamia lucida	197 mg·kg−1	[9]
Iron	Macrozamia moorei	253 mg·kg−1	[9]
Iron	Stangeria eriopus	228 mg·kg−1	[9]
Iron	Zamia erosa	142 mg·kg−1	[9] 2
Iron	Zamia fischeri	1697 mg·kg−1	[9] 3
Iron	Zamia fischeri	1700 mg·kg−1	[19] 3
Iron	Zamia furfuracea	194–272 mg·kg−1	[9]
Iron	Zamia furfuracea	260 mg·kg−1	[19]
Iron	Zamia integrifolia	211–270 mg·kg−1	[9]
Iron	Zamia splendens	160 mg·kg−1	[9]
Iron	Zamia vazquezii	478 mg·kg−1	[9]
Manganese	Cycas micronesica	23.8 mg·kg−1	[12]
Manganese	Cycas micronesica	19.5–44.7 mg·kg−1	[18]
Manganese	Cycas micronesica	26.1–77.5 mg·kg−1	[13]
Manganese	Cycas micronesica	25.4–95.6 mg·kg−1	[14]
Manganese	Cycas micronesica	36.6 mg·kg−1	[20]
Manganese	Cycas micronesica	68.6 mg·kg−1	[20]
Manganese	Cycas revoluta	27.1–73.7 mg·kg−1	[24]
Manganese	Cycas wadei	152 mg·kg−1	[11]
Manganese	Macrozamia riedlei	6-57 mg·kg−1	[22]
Boron	Cycas micronesica	13.6 mg·kg−1	[12]
Boron	Cycas micronesica	11.6–14.3 mg·kg−1	[13]
Boron	Cycas micronesica	13.6–15.9 mg·kg−1	[14]
Boron	Cycas micronesica	43.4 mg·kg−1	[20]
Boron	Cycas micronesica	25.6 mg·kg−1	[20]
Boron	Cycas wadei	17.2 mg·kg−1	[11]
Copper	Cycas micronesica	4.2 mg·kg−1	[12]
Copper	Cycas micronesica	6.5–17.9 mg·kg−1	[18]
Copper	Cycas micronesica	3.1 mg·kg−1	[13]
Copper	Cycas micronesica	2.0–4.0 mg·kg−1	[14]
Copper	Cycas micronesica	7.7 mg·kg−1	[20]
Copper	Cycas micronesica	9.7 mg·kg−1	[20]
Copper	Cycas wadei	3.9 mg·kg−1	[11]
Copper	Macrozamia riedlei	2.1–2.8 mg·kg−1	[23]
Zinc	Bowenia serrulata	19.2 mg·kg−1	[9]
Zinc	Bowenia spectabilis	21.4 mg·kg−1	[9]
Zinc	Ceratozamia mexicana	24.4 mg·kg−1	[9]
Zinc	Cycas debaoensis	18.6 mg·kg−1	[9]
Zinc	Cycas diannanensis	18.9 mg·kg−1	[9] 1
Zinc	Cycas elongata	19.8 mg·kg−1	[9]
Zinc	Cycas fairylakea	26.6 mg·kg−1	[9]
Zinc	Cycas micholitzii	14.1 mg·kg−1	[9]
Zinc	Cycas micronesica	19.0 mg·kg−1	[12]
Zinc	Cycas micronesica	15.2–70.2 mg·kg−1	[18]
Zinc	Cycas micronesica	20.4–45.7 mg·kg−1	[13]
Zinc	Cycas micronesica	18.1–59.8 mg·kg−1	[14]
Zinc	Cycas micronesica	32.5 mg·kg−1	[20]
Zinc	Cycas nongnoochiae	28.0 mg·kg−1	[20]
Zinc	Cycas panzhihuaensis	13.1–15.1 mg·kg−1	[9]
Zinc	Cycas revoluta	5.7–68.5 mg·kg−1	[24]
Zinc	Cycas sexseminifera	13.6 mg·kg−1	[9]
Zinc	Cycas siamensis	11.1 mg·kg−1	[9]
Zinc	Cycas szechuanensis	13.6–18.3 mg·kg−1	[9]
Zinc	Cycas thouarsii	14.2 mg·kg−1	[9]
Zinc	Cycas wadei	10.3 mg·kg−1	[11]
Zinc	Dioon edule	22.6 mg·kg−1	[9]
Zinc	Dioon mejiae	12.3 mg·kg−1	[9]
Zinc	Dioon spinulosum	16.4 mg·kg−1	[9]
Zinc	Encephalartos cupidus	10.5 mg·kg−1	[9]
Zinc	Encephalartos ferox	17.8 mg·kg−1	[9]
Zinc	Encephalartos gratus	14.9–22.2 mg·kg−1	[9]
Zinc	Lepidozamia hopei	23.2 mg·kg−1	[9]
Zinc	Lepidozamia peroffskyana	25.2 mg·kg−1	[9]
Zinc	Macrozamia communis	21.5 mg·kg−1	[9]
Zinc	Macrozamia lucida	21.0 mg·kg−1	[9]
Zinc	Macrozamia moorei	18.2 mg·kg−1	[9]
Zinc	Macrozamia riedlei	3.6–6.6 mg·kg−1	[23]
Zinc	Stangeria eriopus	53.3 mg·kg−1	[9]
Zinc	Zamia erosa	13.9 mg·kg−1	[9] 2
Zinc	Zamia fischeri	20.0 mg·kg−1	[9] 3
Zinc	Zamia furfuracea	10.5–13.7 mg·kg−1	[9]
Zinc	Zamia integrifolia	15.5–16.1 mg·kg−1	[9]
Zinc	Zamia splendens	13.8 mg·kg−1	[9]
Zinc	Zamia vazquezii	38.4 mg·kg−1	[9]
Aluminum	Cycas revoluta	22.0–59.6 mg·kg−1	[24]
Selenium	Cycas micronesica	0.58 mg·kg−1	[12]
Selenium	Cycas wadei	0.41 mg·kg−1	[11]

¹ Reported as Cycas parvula S.L. Yang ex D.Y. Wang; ² Reported as Zamia amblyphyllidia D.W. Stev.; ³ The name Z. fischeri is widely misapplied to the species Z. vazquezii in cultivation. The real Z. fischeri is extremely rare in cultivation, and it is probable that the taxon sampled was Z. vazquesii; ⁴ Reported as Cycas miquelii Warb.

). Cycas contains more species than any other cycad genus and also is the genus with most species represented in this research agenda. However, on a percentage basis only 16% of Cycas species have been studied, compared with 20% of Macrozamia species. Other speciose genera are Encephalartos with 5% of the species studied and Zamia with 10% of the species studied. The monotypic Microcycas was the only cycad genus that has not been included in this research agenda to date. The reported ranges in nutrient concentration did not appear to be constrained within each genus. For example, the least and greatest concentrations for some nutrients were reported within a single genus (Table 2).

The number of genera and species that have been studied for each element was greatest for most of the macronutrients, as would be expected. These are the chemical elements that are needed in greatest quantity by plants, and they comprise the core constituents of most commercial fertilizers that are manufactured to increase plant growth and productivity. Nitrogen was the most studied element with nine genera and 46 of the 358 described cycad species [5] being represented among 14 reports (Table 2). For unknown reasons, the inclusion of the macronutrient magnesium in cycad leaf tissue studies has been minimal, with only five species and two genera included. The micronutrients were much less represented in the literature. Iron and zinc were the only micronutrients that received considerable attention in this agenda. The remainder of the micronutrients have been mostly ignored during past research, with one to four Cycas and Macrozamia species included for each micronutrient. The leaf concentrations for only three of the six beneficial nutrients have been reported to date (Table 2), and each of these were represented by one or two Cycas or Macrozamia species.

Only two species have had more than 10 essential or beneficial elements reported, and both were Cycas species (Figure 1a). Ten of the 46 species had only one or two leaf elements reported. The most heavily studied species was Cycas micronesica, and five of the eight studies for this species included in situ data (Figure 1b). Only 14 of the 45 species were represented with in situ data. About two-thirds of the species were represented by only one study.

The original heavily cited description of the global leaf economic spectrum known as GLOPNET [21] compiled data from 2548 species and included nitrogen and potassium among the leaf traits that were built into the model. Their global average for leaf nitrogen was 19.4 mg·g⁻¹. Our mean of leaf nitrogen concentration for cycad leaves was 22.8 mg·g⁻¹, the greater value possibly occurring because of the nitrogen-fixing cyanobacteria endosymbionts for cycads [6]. The GLOPNET data included 155 species identified as having nitrogen-fixing endosymbionts, including one Cycas and one Macrozamia species [21]. The nitrogen mean for this subset was 25.7 mg·g⁻¹, indicating cycad leaves contain less nitrogen on average than angiosperm plants that associate with nitrogen-fixing endosymbionts. The global average for leaf phosphorus was 1.1 mg·g⁻¹, less than our mean of 1.3 mg·g⁻¹ for cycad species with reported phosphorus values. Overall, our findings indicated the reported values for nitrogen and phosphorus in cycad leaves were greater than the global average. However, this direct comparison suffers from procedural ambiguities. The compilers of the GLOPNET data were careful to restrict their methods to natural settings where the plants received no management of any type (Peter Reich, personal communication). Most of the published cycad reports included leaf data from managed plants in botanic gardens, and many of the studies failed to describe irrigation and fertilization protocols that preceded the sampling dates. Moreover, the explicit comparisons of cycads to leaf economic spectrum fundamentals [9,19,25] were based exclusively on managed botanic garden plants. Managed garden plants of two Cycas species were compared with in situ plants to indicate the managed plants produced leaves with macronutrient concentrations that were not similar to the unmanaged plants [20]. For example, C. nongnoochiae leaves from garden plants contained 2.6-fold greater phosphorus and 4.1-fold greater potassium than in situ plants. This species grows in one locality in central Thailand and exhibits an extreme small endemic range. Clearly, most published leaf element data from cycad species are not currently useful for comparison to GLOPNET.

4. Leaf Litter Elements

The elemental constituents of leaf litter interplay with many cascading ecosystem phenomena, such as plant soil feedback [26,27,28,29], the home field advantage in decomposition [30,31], and the soil food web [32,33,34]. Moreover, an understanding of leaf litter nitrogen is critically important for plant species in Fabaceae because these plants enter into symbiotic relationships with nitrogen-fixing bacteria (Rhizobium) and Cycadales because these plants enter into symbiotic relationships with nitrogen-fixing cyanobacteria (Nostoc) [35]. Therefore, some of the nitrogen released during litter decomposition for these plant groups represents new contributions to the bulk soil. Other plant groups that do not have nitrogen-fixing endosymbionts must absorb the required nitrogen from the edaphic substrates, then their litterfall contains that same nitrogen that is returned to the same edaphic substrates. Direct measurement of leaf litter chemistry is required for each species because translocation of green leaf elements back into the stem tissue occurs during the dismantling of a leaf’s machinery as senescence commences. The percentage of resorption of each element is species-specific [36,37].

A literature review of cycad leaf litter chemistry reveals the definition of generalities is impossible because so few species have been studied. Leaf litter content of carbon and nitrogen has been determined for four Cycas [10,11,18,20,35,38] and two Macrozamia [16] species (

Table 3. Published ranges in leaf litter concentrations of macronutrients, micronutrients, and beneficial elements for cycad plants.

Element	Genera	Species Studied	Species in Genus	Range	Reference
Carbon	Cycas	3	117	475–534 mg·g−1	[10,11,18,35,38]
Carbon	Macrozamia	2	41	502–546 mg·g−1	[16]
Nitrogen	Cycas	4	117	15–22 mg·g−1	[10,11,18,35,38]
Nitrogen	Macrozamia	2	41	11–24 mg·g−1	[16]
Phosphorus	Cycas	4	117	0.3–2.0 mg·g−1	[10,11,18,38]
Potassium	Cycas	4	117	1.0–14.2 mg·g−1	[10,11,18,38]
Magnesium	Cycas	3	117	1.32–7.54 mg·g−1	[11,17,38]
Calcium	Cycas	3	117	2.5–32.3 mg·g−1	[11,18,38]
Sulfur	Cycas	1	117	1.20–1.38 mg·g−1	[38]
Iron	Cycas	2	117	28–547 mg·kg−1	[11,18,38]
Manganese	Cycas	2	117	25–141 mg·kg−1	[11,18,38]
Boron	Cycas	2	117	29.5–51.6 mg·kg−1	[11,38]
Copper	Cycas	2	117	1.3–5.9 mg·kg−1	[11,18,38]
Zinc	Cycas	2	117	4.48–31.21 mg·kg−1	[11,18,38]
Selenium	Cycas	1	117	0.48 mg·kg−1	[11]

). One to four Cycas species have been studied for other essential and beneficial elements (

Table A2. Published ranges for leaf litter element concentrations of cycad plants. Misspellings of species were corrected if identity was obvious, species that were misspelled were not included if identity was not obvious. Taxonomic synonyms were corrected. Data were estimated for reports displaying data as figures and transformed if data were presented as log.

Element	Species	Range	Reference
Carbon	Cycas micronesica	475–486 mg·g−1	[35]
Carbon	Cycas micronesica	501–534 mg·g−1	[18]
Carbon	Cycas micronesica	509 mg·g−1	[36]
Carbon	Cycas nitida	494–519 mg·g−1	[10]
Carbon	Cycas wadei	513 mg·g−1	[11]
Carbon	Macrozamia communis	515–546 mg·g−1	[16]
Carbon	Macrozamia riedlei	502–534 mg·g−1	[16]
Nitrogen	Cycas micronesica	16–22 mg·g−1	[35]
Nitrogen	Cycas micronesica	21–22 mg·g−1	[18]
Nitrogen	Cycas micronesica	20 mg·g−1	[36]
Nitrogen	Cycas nitida	17–22 mg·g−1	[10]
Nitrogen	Cycas wadei	19 mg·g−1	[11]
Nitrogen	Macrozamia communis	11–24 mg·g−1	[16]
Nitrogen	Macrozamia riedlei	11–20 mg·g−1	[16]
Phosphorus	Cycas micronesica	0.5–0.9 mg·g−1	[18]
Phosphorus	Cycas micronesica	1.3–2.0 mg·g−1	[35]
Phosphorus	Cycas nitida	0.3–0.9 mg·g−1	[10]
Phosphorus	Cycas wadei	0.5 mg·g−1	[11]
Potassium	Cycas micronesica	1.0–1.9 mg·g−1	[18]
Potassium	Cycas micronesica	2.2–14.2 mg·g−1	[35]
Potassium	Cycas nitida	1.2–4.5 mg·g−1	[10]
Potassium	Cycas wadei	3.2 mg·g−1	[11]
Magnesium	Cycas micronesica	3.39–6.52 mg·g−1	[18]
Magnesium	Cycas micronesica	3.38–5.82 mg·g−1	[35]
Magnesium	Cycas wadei	1.32 mg·g−1	[11]
Calcium	Cycas micronesica	4.2–15.1 mg·g−1	[18]
Calcium	Cycas micronesica	11.9–32.3 mg·g−1	[35]
Calcium	Cycas wadei	2.5 mg·g−1	[11]
Sulfur	Cycas micronesica	1.20–1.38 mg·g−1	[35]
Iron	Cycas micronesica	64–272 mg·kg−1	[35]
Iron	Cycas micronesica	28–547 mg·kg−1	[18]
Iron	Cycas wadei	37 mg·kg−1	[11]
Manganese	Cycas micronesica	24.5–86.1 mg·kg−1	[18]
Manganese	Cycas micronesica	23.0–37.3 mg·kg−1	[35]
Manganese	Cycas wadei	141 mg·kg−1	[11]
Boron	Cycas micronesica	29.5–51.6 mg·kg−1	[35]
Boron	Cycas wadei	9.9 mg·kg−1	[11]
Copper	Cycas micronesica	2.4–4.4 mg·kg−1	[35]
Copper	Cycas micronesica	1.3–5.9 mg·kg−1	[18]
Copper	Cycas wadei	3.3 mg·kg−1	[11]
Zinc	Cycas micronesica	4.5–31.2 mg·kg−1	[18]
Zinc	Cycas micronesica	11.0–23.8 mg·kg−1	[35]
Zinc	Cycas wadei	5.9 mg·kg−1	[11]
Selenium	Cycas wadei	0.48 mg·kg−1	[11]

).

5. Biotic Factors

The direct influence of leaf age on nutrient concentration has been reported for three cycad species [13,16]. A 33% decline in leaf nitrogen occurred from youngest to oldest C. micronesica leaves [13], a 12% decline in leaf nitrogen occurred from youngest to oldest M. communis leaves [16], and a 13% increase in leaf nitrogen occurred from youngest to oldest M. riedlei leaves [16]. The leaf crown on a cycad plant is comprised of several cohorts of leaves with disparate age, each of which is separated by persisting cataphylls. The determination of the youngest cohort and the oldest cohort of leaves is unambiguous due to the persisting cataphylls. These contrasting results for three species were unexpected and point out the need to determine how leaf age influences leaf elements for more cycad species. The increase in nitrogen with leaf age for M. riedlei is in sharp contrast to the robust literature on the subject of nutrient resorption. Moreover, the description of which leaves were sampled from the plants in most cycad reports reviewed herein was not included. This oversight must be corrected in future studies. The persistence of cataphylls in cycad leaf crowns enables an unmistakable demarcation that separates the youngest leaf cohort from older leaves.

The influence of plant size on leaf nutrients has been reported for two cycad species [18,22]. Leaf nitrogen concentration declined with plant size for C. micronesica [18] and D. sonorense [22]. The results point out the need to determine the influence of plant size on leaf nutrients for more cycad species. Both of these species produce arborescent stem growth. We suggest the results were under control of allometric relations rather than height per se. Therefore, cycad species which produce stem growth that is mostly subterranean may require a different variable to quantify stem growth, such as diameter of the stem clump or number of apices per plant.

The influence of leaflet sampling position along the leaf rachis has been reported for two cycad species [14,16]. Cycas micronesica leaf nitrogen concentration increased linearly for young leaves and non-linearly for old leaves with distance from the petiole [14]. A non-linear increase in leaf nitrogen concentration occurred for M. riedlei with distance from the petiole [16]. The leaf age was not reported. The majority of papers that we reviewed did not include a description of sampling location along the pinnately compound cycad leaf rachis. As with leaf age and plant size, this oversight must be corrected in future studies.

6. Environmental Factors

The direct influence of incident light on C. micronesica leaf element concentrations has been reported [13]. Nitrogen, phosphorus, and potassium concentrations were greater in shaded plants than in full sun plants. Differences in C. micronesica leaf element concentrations were reported between homogeneous shade conditions supplied by commercial shadecloth and heterogeneous shade conditions supplied by wood slats [17]. These results reveal the dangers in relying on data from managed gardens without augmenting the results with data from natural settings. A quantification of incident light or the general level of shade has not been reported for most of the cycad studies from the literature. A comparison of two Cycas species between garden and in situ settings revealed the nutrient concentrations of leaves from the garden plants were dissimilar from those of leaves from habitat [20]. The benign level of competition in the gardens versus robust competition with sympatric plants in habitat was considered a causal mechanism. The use of multiple sites with contrasting soil nutrient relations has revealed that cycad leaf concentrations of some leaf nutrients track with the differences soil concentrations [10,20]. Many of the cycad studies in this review did not include a description of soil nutrient concentrations accompanying the sampled plants. Other studies reported general soil characteristics but did not include measurements of the nutrients within soils subtending the sampled cycad plants. The differences of soil chemistry directly beneath cycad plants versus away from the plants [39,40] indicate soil nutrition within the root zone of the sampled cycad plants is a metric that should be determined in order to interpret leaf nutrient results accurately.

7. Future Directions

We consider three issues as the greatest needs within this agenda as more research accumulates. First, adherence to accepted binomials for every taxon included in this research is of paramount importance. Some reports included taxa names that did not conform to any known published species names, and these data were not included herein and should not be used in future meta-analyses and reviews. Careful adherence to accepted binomials [5] in future research would mitigate this ambiguity. Moreover, as changes in cycad classification and nomenclature will continue to occur, including specific provenance or pedigree data for samples included in studies, or preparing herbarium specimens representing these samples will help researchers compiling data for future meta-analyses and reviews.

Second, more species must be added to the data before large-scale generalities will become accurate for the Cycadales. Priority should be given to taxonomic groups that have not been studied adequately. The genus Microcycas is missing from the published data. However, the speciose genera are also not adequately represented in the literature. For example, only 3% of Ceratozamia, 5% of Encephalartos, 10% of Zamia, 16% of Cycas, and 20% of Macrozamia species have been studied to date.

Third, an increase in focus on natural habitats and reduction in focus on botanic garden settings is needed. The leaf nutrient relations of only 14 of the 358 described species [5] have been determined in situ, and most of those reports included a single locality. In situ leaf sampling of Cycas micronesica has occurred among numerous insular habitats across four geopolitical island groups. No other species has been studied with this level of focus on in situ sampling methods. This paucity of data from natural habitats renders the current cycad literature of little value for comparing to GLOPNET. Moreover, the genetic × environmental control over leaf nutrient concentrations cannot be determined until multiple localities are included for indigenous species with an extensive native range.

Seasonal variation in leaf element concentrations may be considerable and modulated by biotic factors. For example, the influence of season on Actinidia arguta var. arguta (Siebold and Zucc.) Planch. ex Miq. leaf nutrient concentrations differed for male and female plants [41]. Moreover, the influence of season on Olea europaea L. leaves interacted with intraspecific genotypic variation [42]. These results indicate that research to determine the influence of season on cycad leaf nutrient relations should include multiple provenances and the distinction of male and female sampled plants. Until this is determined for numerous cycad species, the approach used by Marler and Lindström [20] is recommended for comparing more than one location, whereby one season is used to compare locations.

Zhang et al. [9,19] reported iron concentrations of Zamia fischeri leaves that were extreme outliers when compared with other species studied in two botanic garden locations. This observation should be confirmed in natural settings in Mexico and greater attention to iron variation among other closely related Zamia species may be warranted.

Marler and Lindström [20] reported that leaf magnesium concentration was constrained among Cycas plants from one provenance even when they were grown in different soils with substantial variation in soil magnesium concentrations. For example, C. nongnoochiae plants growing in Thailand habitat exhibited leaf magnesium concentration that did not differ from the plants growing in a managed cultivated garden, even though the garden soils contained magnesium that was only 14% of that in the habitat soils. Similarly, C. micronesica plants growing in Yap habitat exhibited leaf magnesium concentration that did not differ from the plants growing in a managed cultivated garden, even though the garden soils contained magnesium that was only 11% of that in the habitat soils. The maintenance of magnesium homeostasis in cycad leaves deserves further study. Some of the known roles of magnesium include maintenance of chlorophyll concentration, promotion of non-structural carbohydrate export from leaves, and control of ionic currents across membranes [43,44]. The observed homeostasis for two Cycas species is not unexpected, given this partial list of roles for this macronutrient. The observations need to be confirmed with other cycad species using multiple localities.

The nutrients which have been studied by more than one laboratory have revealed disparity in reported concentrations among the studies that may be explained by dissimilar methods. For example, green leaf nitrogen concentration reported by Kipp et al. [16] was more than double that reported by Grove et al. [23] for Macrozamia riedlei and almost double that reported by Zhang et al. [9] for Bowenia serrulata. Explanations for these differences among laboratories are difficult to consider because many of the co-varying factors discussed in Section 5 and Section 6 were not reported. Effort should be made during every future study to record and report all sources of variation to improve our understanding of reported differences among studies.

Marler and Dongol [35] reported the only study that we are aware of which determined the influence of insect herbivory on cycad leaf nutrients. All three insects were invasive non-native pests. Many cycad taxa coevolved with folivorous insects, and these should be studied in a similar manner to determine how leaf nutrients are altered by the herbivory of these native sympatric insects.

The influence of C. micronesica leaf litter on decomposition speed, soil respiration, and mineralization dynamics has been reported [38]. This study revealed the speed of these leaf after-life phenomena was slower for the cycad leaves than for two Fabaceae species. The results indicated that the presence of cycad plants in biodiverse settings may influence community-level litter decomposition even if they are limited in incidence [45].

The long-term changes in soil nutrient concentrations beneath the canopy of cycad plants have been determined for C. micronesica and Z. integrifolia [39,40]. To our knowledge, the influences of cycad plants on the soils within the dripline of their canopy have not been studied for any other species. However, the two species that have been studied revealed that the presence of a cycad plant in unmanaged settings is valuable for introducing soil heterogeneity at the fine scale, potentially increasing biodiversity in soil organisms and increasing ecosystem health. We propose two phenomena that deserve direct study. First, rainfall rarely reaches the soil surface without first being intercepted by plant structures [46,47,48,49,50,51]. This intercepted rainfall is lost through evaporation or transferred to the soil as throughfall or stemflow. The relative proportions of these processes are affected by canopy and leaf traits, and strongly influence the spatial components of the hydrologic and chemical cycles beneath mixed stands of plants [46,47,48,49,50]. Throughfall is the precipitation component that drips from numerous plant surfaces, and stemflow is the precipitation component that drains along the plant stems to reach the soil. The percentage of precipitation that reaches the soil via stemflow and the concentration of solutes and suspensions of particulates in stemflow are strongly linked to leaf traits and canopy architecture traits [46,47,48,49,50,51]. Stemflow influences essential minerals and metals near the base of trees, but also influences soil carbon by the transfer of dissolved organic matter in the stem flow [51]. To our knowledge, no studies of stemflow have included a cycad representative. However, arborescent palm species exhibit stem and leaf shapes and orientations that are similar to cycads, and many palm trees are skilled at increasing soil nutrients in their root zone by maximizing stemflow [52,53,54]. The diameter of the C. micronesica leaf crown is up to 4 m for healthy trees, but the diameter of the Z. intergrifolia leaf crown is less than 2 m, illuminating a highly contrasting ability to intercept rainfall for the individual plant. Projected canopy area is highly influential of stemflow volume [55]. The relative diameters of leaflets and rachis surfaces are also much greater for C. micronesica than for Z. integrifolia, and these organ traits directly influence how precipitation is intercepted by an individual plant. The inclusion of a range of cycad taxa in the stemflow research agenda would add greatly to our knowledge of how cycad plants directly affect soil chemistry, but would also improve our understanding of carbon, hydrologic, and nitrogen cycles by adding this unique gymnosperm plant group to the stemflow literature.

Second, some plants may influence the biogeochemical cycle by litter trapping. The leaf and stem traits of these plants increase the volume of litterfall that is trapped in the plant’s canopy, and this trapped litter becomes a privatized slow compost pile that releases nutrients over time [56]. As with stemflow, we are not aware of any cycad taxa that have been studied for litter-trapping abilities. However, palm species [52,56,57,58] and fern species [56,59] are highly effective at trapping litter, and the plant traits that enable this ability for palms and ferns are similar to the plant traits of cycads. Trapped litter may further magnify nutrient accumulation by attracting animals which may bring food materials and add feces directly to the litter mass [52,56]. The need to study the litter trapping traits of cycad plants is clear, as this may explain the increases in carbon and nitrogen that we have documented beneath two cycad species. Two cycad leaf traits should be considered in this line of work. First, the size, shape, and insertion angle of spines and prickles on cycad petioles vary greatly among species [6,60], and these petiole traits may directly influence how much of the incoming litterfall is trapped. Second, some cycad species produce leaves that are replaced annually, while other species produce leaves that are retained for many years. Undoubtedly, the amount of trapped litter that can accumulate over time is under the direct influence of leaf longevity, and this leaf trait should be considered in future studies on litter trapping of cycad plants.

Plants employ multiple defensive strategies against herbivores that have been studied within the context of various models [61], and plant defensive strategies are generally classified as structural or chemical. Structural defenses include leaf toughness and the construction of modified organs such as thorns, spines, and prickles. Chemical defenses include metabolites that alter the taste of the tissues to deter herbivory or that act as animal toxins. Cycads employ both defensive strategies, and cycad plants have been the subject of myriad medical and biochemical studies because of the number of known toxins that are synthesized by the plants [6,62]. Structural defenses are important after leaf expansion and maturation, but chemical defenses are important during leaf expansion [63]. The azoxyglycosides cycasin and macrozamin are among the most studied acute cycad toxins, and these nitrogenous compounds have been reported in all 10 genera and most species that have been studied [64,65]. These toxins may occur in greater concentrations in young cycad plants than in adult plants [66], which parallels the decline in leaf nitrogen concentration with plant size [18,22]. In general, elemental concentrations of plant tissues mediate defensive mechanisms [67]. These issues of secondary compounds in cycad biology suggest the individual plants with greater nutritive content are better protected with higher azoxyglycosides [66]. In consideration of the relevance of cycad toxins to human health research, continued research on element accumulation and partitioning in cycad plants may contribute substantially to toxicology research.

The elemental components of plant tissues cannot be studied in the absence of recognizing the contributions of root traits and symbionts. Cycad roots have not been adequately studied but these gymnosperms produce roots that appear typical of other seed-bearing plants, and although little is known about their general physiology, they are believed to function similarly to angiosperm roots [6 (p. 60)]. Seedlings initially produce a robust taproot which over time is augmented or replaced by similarly thick and fleshy branching secondary roots. Root hairs, which function in other plants to increase the volume of soil that plants area able to mine for nutrients, are rare in cycads and only irregularly formed in the thinnest of feeder roots. Cycads also produce specialized clusters of roots known as coralloid roots which typically grow upward above the soil surface and host nitrogen-fixing cyanobacteria which fix nitrogen for use by the plant [6,68,69,70]. Moreover, cycads roots are known to harbor arbuscular mycorrhizal fungi which enhance phosphorus uptake in low phosphorus soils and enhance water availability in seasonally dry habitats [71,72]. The incidence and diversity of these symbionts may contrast sharply between natural habitats where sympatric species of soil biota exist and botanic gardens where the soil biota that interacts with a cycad plant are novel to the plant More studies are needed to understand cycad root traits and to tease apart the influences of these symbiotic relationships on leaf element concentrations in various cycad taxa.

Finally, many areas of occupancy for various cycad species are characterized by edaphic characteristics that most plant species would not consider as suitable for plant growth. We highlight three examples that deserve a dedicated look during future research on cycad plant nutrition. First, multiple cycad species thrive in littoral habitats where roots are exposed to saline substrates and leaves must contend with aerosol salt deposits. Second, some cycad species flourish on limestone mountain surfaces or karst outcrops where mineral soils are scarce and drought stress is extreme. Third, cycad populations also occur on either highly acidic volcanic substrates or ultramafic habitats, where the plants must cope between the spectrum of extreme acidity and high alkalinity compounded by calcium deficiencies and metal toxicities. This group of plants is ideal for studying the mechanisms that plants exploit to compete in these extreme habitats. Moreover, some species are endemic to one of these extreme habitat types while other species are indigenous and can be found in various ecological niche habitats. Comparing these two types of cycad species may tease apart the stress physiology mechanisms that indicate facultative versus obligate approaches for tolerating extreme edaphic conditions.

8. Conclusions

Cycad species are highly prized in the horticulture trade. We have reviewed the available literature on elemental concentrations in cycad leaves. A total of six gardens were included with two in China, one in Florida, one in Thailand, one in Philippines, and one in Guam. These results were discussed along with in situ data from Australia, Guam, Mexico, Palau, Philippines, Rota, Thailand, and Yap. The review illuminates the scant research landscape of this agenda. By highlighting the unexpected results that most papers reported data from botanic gardens and the authors failed to describe the irrigation and fertilization protocols of the managed plants, we aimed to inspire an adoption of more demanding protocols for expanding this research agenda. In part, this should include measurement and reporting of plant size, leaf age, or position within the canopy, position of leaflets along the rachis, the shade level of the sampled leaves, and the soil element concentrations within the root zone of the sampled plants.