Inserting cycads into global nutrient relations data sets

ABSTRACT

Global research agendas on plant nutrient relations attempt to illuminate biotic and abiotic factors that mediate nutrient relations. We contend that cycad species are not adequately represented in these global agendas. Little is known about how various cycad traits such as phylogenetics, growth form, latitudinal range, or ecological niche influence concentration, stoichiometry, and resorption dynamics of leaf nutrients. The addition of cycad species data to the global research dataset will address a critical knowledge gap and benefit global research needs to improve our systemic understanding of biotic and abiotic influences on plant nutrition.

Cycads are ancient gymnosperms that have survived mass extinction events.¹ Cycads are the most endangered group of plants worldwide according to the International Union for Conservation of Nature, with more than 63% of the described taxa listed under one of the threatened categories.² Cycads are part of a geologically ancient lineage of seed plants whose origins can be traced back to the late Paleozoic era.¹ Their perseverance and documented fossil history provide research with the opportunity to gain insight into plant evolution and biology.³ Cycads are unique among the living seed plants by having motile spermatozoids which are linked to some of the earliest seed plants.¹

Most cycad research has focused on taxonomy and phylogeny, and research into other areas of cycad biology has been lacking.⁴ An explicit result of this phenomenon is that cycad conservationists often lack the information that is needed to inform management decisions.^5,6 An inadvertent result of these developments is that cycads are conspicuously missing from worldwide data sets that have been compiled to explain universal patterns among plants.

Global research agendas on plant nutrient relations help us to understand biotic and abiotic factors that mediate plant nutrient cycling. The manner in which Cycas micronesica K.D. Hill, a representative arborescent cycad tree, influenced in-situ plant-soil feedback processes has been described.⁷ Plant-soil feedback relations are partly mediated by leaf and litter nutrient relations, illuminating the need to gain more knowledge about cycad leaf nutrient relations. The number of publications on cycad leaf nutrients has been accumulating, but attempts to place cycad data into the worldwide research agendas has been lacking.^8–15 Here we outline some of the research that would benefit from adding cycad species to the global dataset for biotic and abiotic influences on plant nutrition.

Phylogenetics

The role of phylogenetics in leaf nutrient concentrations has been well studied.¹⁶ About 350 cycad species have been described in 10 genera.¹⁷ Only nine of these genera have been included in publications on leaf nutrient concentrations. This should be completed for ex-situ settings where sampled plants have been cultivated in a common garden setting to enable taxa comparisons under homogeneous growing conditions. Phylogenetic differences should also be studied for in-situ habitats because many agendas such as latitudinal effects cannot be studied in ex-situ settings. The relationships among the hundreds of cycad taxa within phylogenetic tree revisions are evolving as more molecular protocols are employed. As more species are added to the global database of nutrient relations, more formal comparisons among the phylogenetic variations of this plant group will be enabled in tandem with greater understanding of the phylogenetic relations.

Functional and growth forms

The traits that explain plant functional groups have also been invoked to study variations in leaf nutrient concentrations among plants.^18–20 For example, deciduous species construct leaves with much greater leaf nutrient concentrations than evergreen species.^21–23 This functional group trait could be directly tested with cycad species that lose their leaves annually versus species that sustain leaf longevity in the order of years (Figure 1), a comparison that has been done with several species.^12,15 One of the broad classifications of cycads is robust, arborescent versus diminutive, subterranean growth forms (Figure 2).¹ To our knowledge, Zamia pseudoparasitica J. Yates is the only cycad species that is obligately epiphytic,¹ although others may be facultatively epiphytic.²⁴ For example, the differences of water and nutrient stress for epiphytic versus terrestrial species create interesting physiological phenomena to study. Representatives from these and other highly contrasting cycad growth forms should be studied to enable large-scale comparisons among the cycad taxa.

Figure 1.

Leaf longevity is highly variable among cycad species. (A) Cycas siamensis Miq. from south east Asia produce short-lived leaves that are replaced at least annually. (B) Cycas elephantipes A.Lindstr. & K.D.hill from central Thailand produces evergreen long-lasting leaves. (Photo credit: A. Lindstrom).

Figure 2.

Cycad species vary from diminutive species to robust arborescent species. (A) Zamia pygmaea Sims from central Cuba is one of the smallest cycad species described with subterranean stems. (B) Microcycas calocoma (Miq.) A.DC. from western Cuba grows to 10-m in height. The genus Microcycas has not been included in any publications on leaf nutrients. (Photo credit: A. Lindstrom).

Ecological variation

The study of ecotypic variation of leaf nutrient status is a research agenda often discussed in the context of environmental adaptation and climate change. For example, plants from arid regions allocate more nitrogen (N) to leaves than plants from more wet regions, presumably to improve photosynthesis to increase water use efficiency.^25,26 As a group, the native habitats for cycads exhibit remarkable heterogeneity for ecological niche (Figure 3). To date, no robust attempts have been made to directly compare leaf nutrients of cycad species that are adapted to and originate from contrasting ecological conditions.

Figure 3.

Highly contrasting ecological niches are inhabited by cycads. (A) Zamia roezlii Linden grows in one of the wettest habitats on earth, colonizing coastal brackish sites in Colombia where up to 8000 mm of annual precipitation occurs. (B) Zamia encephalartoides D.W. Stev. is a second Colombian species adapted to dry exposed desert localities at about 800 meter above sea level. (Photo credit: A. Lindstrom).

Native range and latitude

A robust data set of 430 angiosperm species indicated that taxa with a wide indigenous range exhibited higher leaf N than taxa with a narrow endemic range.²⁷ The highly contrasting spatial occurrences of the ca. 350 described cycad species¹⁷ may be exploited to determine if this phenomenon applies to cycads. Comprehensive analyses of latitudinal and elevational distributions of cycads and how they fit into gymnosperms as a whole may inform the methods.²⁸ The traits of various in-situ settings also reveal limitations to sample collection protocols. For example, physical access to some localities may be inhibitory. Moreover, ongoing habitat conversion is creating extreme cases of habitat loss and poaching is preferentially eliminating segments of some populations. These phenomena illuminate the sense of urgency for adding more taxa to the leaf nutrient research agenda. Some species are known to occur in a single constricted endemic location, whereas other species exhibit a widespread indigenous range. For example, the Philippines is home to Cycas wadei Merrill which is known from a single endemic location less than 10 km², and Cycas edentata De Laub. which grows throughout numerous disjunct localities that span many countries (Figure 4).²⁹

Figure 4.

The native range is highly contrasting among the described cycad species. (A) Cycas wadei Merrill is known from a single endemic location less than 10 km² on Culion Island, Philippines. (B) Cycas edentata De Laub. has an extensive indigenous range spanning hundreds of islands and many countries. (Photo credit: T. Marler).

A global analysis of green leaf phosphorus (P) among ca. 4,500 species revealed a strong latitudinal effect, with leaf P lower near the equator and greater in high latitudes.²⁷ Similarly, N:P revealed a strong relationship with latitude.³⁰ Senesced leaf N and P also reveal global patterns that are largely defined by latitude.³¹ The latitudinal limits to contemporary cycad species are substantial (Figure 5), and the study of cycads within this context would provide a robust comparison.

Figure 5.

Latitudinal range contrasts many of the world’s cycad species. (A) Cycas revoluta Thunb. is from southern Japan at 29 °N latitude. (B) Cycas rumphii Miq. grows on the equator in Indonesia. (Photo credit: A. Lindstrom).

Leaf economic spectrum

Leaf nutrient variations among plant species have been compiled at the global level within the context of an economics spectrum.^21,22,32 This economics spectrum is discussed in the context of comparing covariation among leaf structure and function traits. For example, long-lived leaves with considerable construction costs tend to have lower leaf nutrient concentrations than short-lived leaves with relatively less construction costs. Attempts to place cycad species within this research agenda have begun using ex-situ data sets.^12,15 These efforts need to expand to include in-situ data among species with contrasting leaf longevity.

Green leaf stoichiometry

Stoichiometry of constituent elements in plant biomass is associated with many physiological and ecosystem processes.^21,33 The stoichiometric relations among N, P, and potassium (K) have been heavily studied for green leaves, and have proven invaluable for understanding macronutrient limitations of plant growth. Robust data sets assessing plant biomass production indicate that leaf N:P above 16 suggests P limitation, N:P below 14 suggests N limitation, and N:K above 2.1 or K:P below 3.4 indicate K limitation.^34–38

Only two cycad papers have explicitly discussed the stoichiometry between pairs of green leaf minerals. Green leaves of Cycas nitida K.D.Hill & A.Lindstr.¹¹ and C. wadei¹⁴ expressed N:P:K relationships that illuminated primarily P limitation, followed by K limitation. Nitrogen generally emerges as the most prevalent limiting nutrient in plants. That these two cycad species do not exhibit N limitation is explained by the employment of cyanobionts by cycads to access newly fixed N.¹ The manner in which other cycad species conform to these generalities has not been reported. Accumulating more data sets may illuminate generalities in mineral nutrition limitations for cycads as a group. This information may improve conservation management decisions.

Leaf litter stoichiometry

The stoichiometric relations among carbon (C), N, and P have been heavily studied for senesced leaves of many plants, and have proven valuable for predicting how leaf litter influences nutrient cycling in the ecosystem.^39,40 The decomposition speed of fresh litterfall is generally positively correlated with mineral contents and negatively correlated with C:nutrient quotients. These quotients are correlated with leaf construction costs, so leaves with greater longevity generally have greater construction costs and more C relative to nutrients in senesced leaves. In contrast, leaves with lower longevity generally have relative less construction costs and less C relative to nutrients in senesced leaves.

Only three cycad species have been discussed in the context of leaf litter C:N:P:K stoichiometry. The range in C:N was constrained among species and soil types compared to C:P or C:K for C. nitida,¹¹ C. wadei,¹⁴ and Cycas micronesica K.D.Hill.⁴¹ Moreover, leaf damage by invasive specialist pests altered these leaf litter traits for C. micronesica.⁴¹ To date, no other cycad species has been studied in this context, limiting our understanding of how cycad populations affect local biogeochemical cycles.

Green leaf nutrients and resorption

Nutrient resorption as leaves senesce is a critical behavior among plants enabling an internal recycling of limiting elements.^42,43 This behavior affects many plant and habitat components of the biogeochemical cycle. Large-scale syntheses indicate that plants withdraw 50% to 60% of leaf N and P prior to leaf abscission, and withdraw about 70% of the leaf K prior to leaf abscission.^{30,41,44–46} Evaluation of a global database of 297 species revealed N and P resorption efficiency decreased as green leaf N and P increased among plants.⁴⁷ This relationship was consistent for inter- and intra-specific resorption efficiency. The few publications that include cycad leaf nutrient concentrations ^8–15 revealed considerable inter-specific variation in green leaf nutrients. This limited amount of published cycad data indicates the relationship between green leaf nutrient status and nutrient resorption efficiency could be studied with substantial amplitude.

The only available cycad data related to this subject are for C. nitida and C. wadei.^11,14 Nitrogen resorption efficiency was much lower than global values but P and K resorption efficiencies were greater than global values. Four habitats were compared for C. nitida,¹¹ and the variation in green leaf N did not covary with N resorption efficiency, but the variation in green leaf P did covary with P resorption efficiency. The plants exhibited P resorption efficiency of 73% in the habitat with leaf P of 1.0 mg· g⁻¹ and 53% in the habitat with leaf P of 1.6 mg· g⁻¹.

Soil nutrients and leaf resorption efficiency

Leaf P resorption has been studied in relation to soil P availability, and resorption tends to increase as background soil P decreases.⁴⁸ However, resorption does not always track soil nutrient status, making determination of the effectors and effects on nutrient resorption complex. The only publication comparing leaf nutrient resorption among more than one soil type included a comparison of four soil types for Cycas nitida.¹¹ For this species, P resorption efficiency declined with increases in soil P resources as expected.

Plant size

Nutrient concentrations in green leaf tissues generally decrease with increased plant size.^27,49–51 Moreover, small plants generally exhibit lower N:P ratio than large plants.²⁷ These reports underscore three important issues with regard to cycads. First, only three of the published cycad reports containing leaf nutrient concentration data reported some measure of plant size.^8,10,14 This oversight should be corrected during ongoing studies designed to expand this research agenda so that methods can be adequately repeated. Second, the known record height for cycads is ca. 18-m.¹ The species that exhibit the capacity to attain these extreme heights lend themselves to detailed allometric approaches to study height versus leaf nutrient pools. Third, the direct comparison of diminutive cycad species to arborescent cycad species (Figure 2) would improve our knowledge about the applicability of plant size in mediating cycad leaf nutrients.

The course ahead

This paper illuminates several issues concerning cycads. First, we have clearly shown that all of the above research agendas would benefit by adding representative cycad species. There are about 350 described cycad species available for applied research.¹⁷ Compiling leaf nutrient data from all published papers indicates at least one nutrient has been quantified and reported for about 10% of the described taxa. The examples where only one, two, or three cycad species have been studied within a global research agenda indicate that less than 1% of contemporary cycad taxa have been included. Second, many of the global research agendas have compared angiosperms and gymnosperms, yet the gymnosperm data sets were comprised entirely of conifer species. A more permanent fix would pursue the publication of data from Representatives of the Cycadidae, Ginkgoidae, and Gnetidae need to be added to the published conifer database. Third, several cycad publications contain data sets that were not used to discuss global issues such as stoichiometry, but the published raw data remain available in the literature for further development in future reviews.^8,9,12,15 With contemporary access to online publication of supplementary information, there is no reason to collect data then leave it unreported even if the raw data do not directly inform the authors’ primary objectives. Fourth, the points that we have illuminated reveal that cycad leaf nutrient studies need to be conducted appropriately with covarying factors such as plant size and soil nutrient status quantified and reported. These details will improve our ability to fully compare the results that are added from ongoing research.

Acknowledgments

Support provided by Mr. Kampon Tansacha, Director of Nong Nooch Tropical Botanical Garden.