A Trait-Based Approach to the Conservation of Threatened Plant Species

A trait-based approach to the conservation of threatened plant species

J UAN C. ÁLVAREZ-YÉPIZ,ALBERTO B ÚRQUEZ A NGELINA M ARTÍNEZ-YRÍZAR and M ARTIN D OVCIAK

Abstract Traditionally the vulnerability of threatened environment, genetics and population dynamics (Gilpin & species to extinction has been assessed by studying their Soulé, ), hereafter referred to as the traditional ap- environment, genetics and population dynamics. A proach. In this context, the study of environment includes more comprehensive understanding of the factors pro- investigating the quality and quantity of available and po- moting or limiting the long-term persistence of threa- tential habitat, and thus all aspects of species’ relationships tened species could be achieved by conducting an with abiotic and biotic factors. Genetic studies focus on the analysis of their functional responses to changing envir- genetic diversity of species and populations (including onments, their ecological interactions, and their role in adaptation to change) and population bottlenecks from ecosystem functioning. These less traditional research small effective population sizes. Research on population dy- areas can be unified in a trait-based approach, a recent namics investigates species’ demography and persistence in methodological advance in ecology that is being used to a given environment manifested via population structure, link individual-level functions to species, community fecundity and, ultimately, fitness. The traditional approach and ecosystem processes to provide mechanistic explana- has proved successful in studies of threatened and non- tions of observed patterns, particularly in changing environ- threatened plant and animal species (e.g. Oostermeijer ments. We illustrate how trait-based information can be et al., ; Conard, ; Kalkvik, ). However, other translated into well-defined conservation strategies, using components of a more comprehensive assessment of the the example of Dioon sonorense, an Endangered cycad en- viability of populations (some of these originally proposed demic to north-western Mexico. Scientific information by Gilpin & Soulé, ), such as species’ functional re- yielded by trait-based research, coupled with existing knowl- sponses to a changing environment, their ecological interac- edge derived from well-established traditional approaches, tions, and their role in ecosystem functioning, have not been could facilitate the development of more integrative conser- formally incorporated into conservation research, particu- vation strategies to promote the long-term persistence of in- larly regarding threatened taxa (Schemske et al., ). dividual threatened species. A comprehensive database of These additional research areas can be unified in a trait- functional traits of threatened species would be of value in as- based approach, a recent methodological advance in ecology sisting the implementation of the trait-based approach. that is being used to link individual-level functions (measured with functional traits) to species, community and eco- Keywords Biodiversity loss, conservation strategies, cycad, system processes, to provide mechanistic explanations for Dioon sonorense, Endangered species, Mexico, plant the observed patterns, particularly in changing environ- conservation, rarity ments (McGill et al., ; Violle et al., ; Garnier & Navas, ; Shipley et al., ). ‘ Introduction From the perspective of trait-based ecology, a trait is any morphological, physiological or phenological feature meas- he vulnerability of species to extinction has traditional- urable at the individual level, from the cell to the whole- Tly been assessed within three major areas of study: organism level, without reference to the environment or any other level of organization’ (Violle et al., ). These traits are called functional traits when they influence fitness through their effects on growth, reproduction and survival, † JUAN C. ÁLVAREZ-YÉPIZ* (Corresponding author), ALBERTO BÚRQUEZ and which are the three components of individual performance ANGELINA MARTÍNEZ-YRÍZAR Instituto de Ecología, Universidad Nacional Autónoma de México, Colosio y Sahuaripa, Col. Los Arcos, Hermosillo, (Violle et al., ). Species traits are usually assessed as Sonora 83250, Mexico. E-mail [email protected] mean values of individual traits per population, and such MARTIN DOVCIAK State University of New York College of Environmental Science values can vary with the environment. Thus, information and Forestry, Syracuse, New York, USA on the local environment of populations is needed to inter- *Also at: State University of New York College of Environmental Science and pret the ecological and evolutionary meaning of measured Forestry, Syracuse, New York, USA †Also at: Instituto Tecnológico de Sonora, Obregón, Sonora, Mexico traits and to make useful predictions under changing envir-   Received  August . Revision requested  January . onmental conditions (McGill et al., ; Violle et al., ; Accepted  June . First published online  February . Garnier & Navas, ; Shipley et al., ).

Oryx, 2019, 53(3), 429–435 © 2019 Fauna & Flora International doi:10.1017/S003060531800087X Downloaded from https://www.cambridge.org/core. IP address: 170.106.40.40, on 02 Oct 2021 at 10:30:42, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S003060531800087X 430 J. C. Álvarez-Yépiz et al.

Trait-based ecology is a relatively new discipline that is increasingly used in studies of community assembly (e.g. Ackerly & Cornwell, ), biotic interactions (e.g. Wardle et al., ) and ecosystem functioning (e.g. Díaz & Cabido, ), and in predicting species’ responses to climate warming (e.g. Diamond et al., ). Chown () presented a trait-based framework for use in conservation, specifically in conservation physiology, to forecast the risk of climate and habitat changes to species and higher ecological levels (communities, ecosystems). A major challenge of the trait- based approach to conservation is the identification and measurement of functional traits relevant to individual threatened species, particularly those traits related to responses to changing environments, species’ ecological interactions, and ecosystem functioning. Here we propose and FIG. 1 How the trait-based approach complements the illustrate how a functional trait-based approach can be traditional approach to the conservation of threatened species. used to increase our understanding of the vulnerability of The traditional approach focuses on species population threatened species to extinction. We introduce the steps dynamics, habitat suitability and genetic structure, and has and structure for implementing a trait-based approach in provided essential information for guiding conservation the conservation of threatened species, and illustrate this ap- strategies for threatened species. The trait-based approach has proach in a case study of Dioon sonorense, an Endangered been formally included in conservation research to a lesser cycad endemic to north-western Mexico, including a discus- extent, even though it can provide information on physiological sion of the potential applicability of the trait-based approach responses to environmental variability and ecological interactions of species, and their roles in ecosystem functioning in guiding the conservation of this species. (which may indirectly influence species persistence). Combining these approaches may lead to more integrative conservation strategies to promote the long-term persistence of target species A trait-based approach to the conservation of exposed to anthropogenic and natural threats. There is a threatened plant species dynamic feedback (double arrow) between conservation strategies and species persistence, as they can affect each other. By definition, threatened species are already at risk of extinction as a result of species-specific extrinsic and intrinsic factors. A more complete understanding of species’ vulner- to affect population fitness and species persistence, and thus ability to extinction requires knowledge not only of their en- facilitate science-based species conservation (Table ). vironment, genetics and demography but also of functional Although the collected information should be species- traits related to their responses to changing environments, specific, a multi-species framework by phylogenetic group their interactions and their role in ecosystem functioning may also be possible when related species display parallel (Gilpin & Soulé, ; Oostermeijer et al., ; Chown, responses to similar threats. ). This information can be translated into more in- Our case study illustrates how the trait-based approach tegrative management strategies to increase the viability of can provide information to understand () the individual threatened species (Fig. ). We focus on illustrating the con- physiological responses to environmental stress imposed by ceptual importance of studying functional traits to inform water, light and nutrient limitations that may be caused by the conservation of threatened species rather than on the the changing environment (e.g. Álvarez-Yépiz et al., a; methodological peculiarities of measurement and analysis Williams et al., ; Díaz-Álvarez et al., ; Urban, ), of functional traits, which can be found elsewhere (e.g. () the importance of maintaining species’ ecological inter- Díaz et al., ; Bernhardt‐Römermann et al., ; Kraft actions (e.g. plant–plant, plant–pollinator/seed disperser, & Ackerly, ; Pérez-Harguindeguy et al., ). and plant–herbivore), as the loss of these interactions usually We synthesized basic information from published stud- results in species extinctions (e.g. Tilman et al., ; ies for both the traditional approach and the trait-based Álvarez-Yépiz et al., b; Valiente-Banuet et al., ), approach, to illustrate how these approaches differ and and () the importance of the role of individual species in eco- how they can be useful in guiding the conservation of a tar- systems, because threatened species can increase carbon stor- get threatened species (Table ). The information for the age, biomass accumulation and ecosystem stability by trait-based approach can be formalized as a series of distinct increasing plant functional diversity, facilitating a broader and well-defined activities required to gather scientific use of available resources (Lyons et al., ; Mouillot et al., information on the functional traits and factors most likely ;Álvarez-Yépiz&Dovčiak, ; Leitão et al., ).

TABLE 1 Summary of the main steps for implementing a trait-based approach (steps –) that complements the traditional approach (steps –) for the conservation of threatened plant species.

Step Description & goals (1) Reviewing literature on the life history & Existing information is a cost-effective means of directing research towards filling in ecology of the target species existing knowledge & data gaps; knowledge of the biology of the target species can be used to direct conservation & management & future conservation research, particularly information on (a) why the target species is threatened, rare or endemic, (b) the main extrinsic & intrinsic threats to the target species, & (c) the species’ responses to key biotic & abiotic environmental limiting factors. (2) Monitoring population dynamics Following populations & cohorts of individuals within populations through time helps to determine if populations are declining, stable or increasing, & to identify the life stages that contribute most to population growth (Álvarez-Yépiz et al., 2011). (3) Evaluating habitat suitability Typifying & analysing habitats across populations of various sizes can increase our understanding of resource limitations (e.g. soil nutrients, water, light) & identify new potentially suitable habitats for reintroduction (Álvarez-Yépiz et al., 2011). (4) Assessing genetic diversity Long-term population viability can be determined by population size, genetic structure & diversity. Genetic analysis of populations of various sizes & life stages (seed, seedling, juvenile & adult) can provide information about dispersal distances, gene flow, population history & the main population reservoirs of genetic diversity (González-Astorga et al., 2008). (5) Measuring functional responses Physiological traits can help to detect thresholds of species’ tolerance to resource limitations & environmental stressors (e.g. temperature, water or nutrient stress) at different life stages & improve the understanding & prediction of species’ responses to changing environments (Álvarez-Yépiz et al., 2014b). (6) Quantifying ecological interactions As species interactions occur throughout their life cycles it is important to identify the relationships between threatened species & other taxa (e.g. with pollinators, seed dispersers, herbivores or nurse plants) & quantify them at various demographic stages; it is also important to identify keystone threatened species & their cascade effects (Álvarez-Yépiz et al., 2014a). (7) Ascertaining the species’ role in ecosystem Functional trait analysis can be useful to identify the individual function of threatened functioning species & scale this up to the ecosystem level; e.g. the trait-based approach can help to determine the role of the target threatened species in ecosystem stability & resilience, or in other processes, such as carbon storage & nutrient cycling (Álvarez-Yépiz & Dovčiak, 2015).

A trait-based approach for the cycad Dioon the northernmost tropical dry forest of the Americas and is sonorense valued as an ornamental plant (Plate ). There are five confirmed localities where this species still occurs, in c.  sub- Description of the target species populations, mostly restricted to subtropical vegetation (Fig. ). Each locality contains – subpopulations, usually Cycads are one of the most threatened groups of vascular with – mature individuals each but frequently with plants (Donaldson, ; IUCN, ). These gymnosperms ,  (González-Astorga et al., ; Álvarez-Yépiz et al., evolved c.  million years ago and were widespread during ). The total estimated population size is c. , mature the Jurassic but declined dramatically during the mass ex- individuals, with an apparent decreasing population trend tinction of the Cretaceous, when they apparently contracted since the s (Chemnick & Gregory, ). Dioon sonor- to rocky or nutrient-poor marginal habitats (Norstog & ense is dioecious, and female plants under optimal condi- Nicholls, ; Crisp & Cook, ;IUCN,). Many tions produce a single cone (strobilus) every  years, cycad species occur in small, isolated populations in tropical which restricts its regeneration potential and population and subtropical regions, often in marginal rocky habitats, persistence (Norstog & Nicholls, ; Álvarez-Yépiz et al., where they can obtain nitrogen through symbiotic N-fixing ). It is categorized as Endangered on the IUCN Red List cyanobacteria (Norstog & Nicholls, ;Lindblad&Costa, (Chemnick & Gregory, ). This species is exposed to ; Álvarez-Yépiz et al., a). () extrinsic threats, including illegal collecting (seeds, Dioon sonorense (De Luca, Sabato & Vasquez Torres, whole plants), land-use change (land clearing, grazing), Zamiaceae) is a cycad species endemic to the arid lands of and extreme natural events (hurricanes, fires, frosts), and north-western Mexico (essentially to the state of Sonora, () intrinsic threats, including small adult population Fig. ). It is an evergreen, long-lived understorey species of sizes, little or no recruitment to the adult stage, and a

information or insight it yields relative to the traditional (or previously used) research approaches. For example, the traditional approach has produced key scientific insights about D. sonorense population dynamics, habitat suitability and genetic structure. A matrix analysis indicated decreasing finite population growth rates (λ , ) for small populations (,  adults; Álvarez-Yépiz et al., ), with larger population sizes ($  adults) required for population stability (λ c. ) or growth (λ . ). Values of λ of .–. have been reported for other, more abundant cycad species (Raimondo & Donaldson, ; Pérez- Farrera et al., ). Elasticity analysis indicated that adults contribute most to population growth rates (Álvarez- Yépiz et al., ), similar to other cycads and long- lived plant species in general (Silvertown et al., ; Raimondo & Donaldson, ). Habitat analyses indicated that D. sonorense may occur in low abundance on poor soils FIG. 2 The five confirmed localities (black dots) of the cycad where angiosperm competition is low, but it can reach high- Dioon sonorense in the state of Sonora, Mexico, and one (San er abundance, recruitment and population growth on more Javier) where it is locally extinct; and the potential distribution of fertile soils where nurse plants can ameliorate heat stress –  the species (hatched, following elevations of , m), based and poor soil conditions (Bertness & Callaway, ; on past and present known occurrences (González-Astorga et al., Álvarez-Yépiz et al., , b). Genetic analyses indicated ; Álvarez-Yépiz et al., ). The species does not occur in the wild elsewhere. that the species has a robust genetic structure (high genetic diversity, slightly positive global inbreeding and zero local inbreeding; González-Astorga et al., ), and thus a good genetic baseline for conservation. The traditional approach to conservation has not, however, provided detailed information on the species functional or physiological responses to environmental variability, ecological interactions or the species roles in ecosystem functioning that may influence its persistence. As discussed below, some key traits of D. sonorense that have been iden- tified as important because of their effect on population vital rates and broader ecosystem functions include physiological (e.g. high water-use efficiency and symbiotic N fixation, which increase the efficiency of resource use), morphological (e.g. sclerophylly, which decreases water loss and increases protection against herbivory), and phenological traits (e.g. evergreen leaves, which increase nutrient retention). PLATE 1 A male individual of the Endangered cycad Dioon Functional traits related to water conservation and nutri- sonorense, a long-lived species with a narrow geographical ent acquisition are particularly important in D. sonorense range in north-western Mexico (Fig. ). Photograph by J.C. because they can affect population vital rates in the water- Álvarez-Yépiz. and nutrient-limited habitats where this species occurs. Dioon sonorense seems to be able to access more atmospher- ic nitrogen at sites with low soil fertility through symbiotic distribution restricted to marginal habitats (Norstog & associations with cyanobacteria, and this ability increases   Nicholls, ; González-Astorga et al., ; Chemnick & with ontogeny (Álvarez-Yépiz et al., a). Seedlings of   Gregory, ; Álvarez-Yépiz et al., ). D. sonorense (and other species in this genus) are especially vulnerable to seasonal drought, with higher water loss lead- Description of the trait-based approach ing to lower water-use efficiency (i.e. the ratio of photosyn- thesis to transpiration rates) and subsequently higher Any contributions of a trait-based approach (or any other seedling mortality as a result of desiccation (Álvarez-Yépiz new approach) should be evaluated in terms of what new et al., a; but see also Yáñez-Espinosa et al., ;

Yáñez-Espinosa & Flores, ). Sclerophylly in leaves of D. attributed to this species (Álvarez-Yépiz & Dovčiak, ). sonorense seedlings is a trait that helps them to reduce water In addition, D. sonorense may facilitate the survival of loss (by transpiration) and, at least in seedlings, requires  other species by providing permanent shade as a result of days to develop fully (Álvarez-Yépiz et al., a). Therefore, its evergreen nature, reducing heat and drought stress, reducing light intensity through artificial shading or protec- thus contributing to the maintenance of biodiversity in tion from nurse plants should increase seedling survival, es- tropical dry forests (Álvarez-Yépiz et al., a,b). pecially during the first few months of development. Important ecological interactions of D. sonorense with other species include facilitation by angiosperms, which Discussion can be especially important at the seedling stage, when the angiosperm canopy provides shade that reduces tran- The trait-based research approach can provide key infor- spiration and increases water-use efficiency and seedling mation to better understand the persistence mechanisms survival (Álvarez-Yépiz et al., a,b; but see also Yáñez- of a threatened species. Examples of relevant trait-based Espinosa et al., ; Yáñez-Espinosa & Flores, ). information in our D. sonorense case study highlight that However, the growth and survival of D. sonorense at () seedlings (especially those with immature leaves, ,  different life stages vary with the identity of neighbouring days old) rather than juveniles or adults are most sensitive plants (Álvarez-Yépiz et al., b); for example, intraspecif- to resource limitation and environmental conditions, mak- ic competition is strongest at the seedling stage, especially in ing seedling functional responses particularly important sheltered microsites densely colonized by cycad seedlings, for species range shifts as a result of changing climate whereas interspecific competition is strongest at the adult (Álvarez-Yépiz et al., a,b); () relatively low water-use stage. The type of neighbour (conspecific vs heterospecific) efficiency of seedlings coupled with the lack of microclimat- and associated neighbourhood interactions (competition, ic amelioration by nurse plants contributes to high seedling facilitation) have important conservation implications, as mortality rates, reduced adult recruitment and consequently they can be used to guide the selection of appropriate micro- reduced population viability (Álvarez-Yépiz et al., a,b; sites for seedling establishment for species restoration or Yáñez-Espinosa et al., ; Yáñez-Espinosa & Flores, reintroduction. For example, rocky areas with conspecific ); and () large populations with many mature indivi- canopies tend to facilitate the survival of D. sonorense seed- duals contribute locally to the maintenance of ecosystem lings by reducing interspecific competition (Álvarez-Yépiz function and stability by augmenting long-term carbon et al., b), and thus they may be suitable sites for success- storage and functional diversity (Álvarez-Yépiz & ful conservation or reintroduction efforts attempting to in- Dovčiak, ). crease the number of populations. Conservation strategies The information gathered from the trait-based research accounting for species interactions may include maintaining approach coupled with existing knowledge derived from or promoting greater canopy cover to protect seedlings from the traditional approach can help us define more integrative heat and drought stress. However, subsequent management conservation actions. For example, () guarding the most fa- should reduce canopy cover (e.g. via silviculture) to decrease vourable habitats, especially where D. sonorense co-occurs interspecific competition and promote recruitment of juve- with appropriate nurse plants; () protecting adult plants niles into adults, especially in productive sites with denser across all populations, given their importance for maintain- canopies. Other biotic interactions that are important in cy- ing long-term population viability, genetic and functional cads but unknown for D. sonorense include relationships diversity, and ecosystem functioning; () increasing seedling with herbivores, pollinators, seed dispersers and N-fixing survival to larger size classes by augmenting canopy shading cyanobacteria (Norstog & Nicholls, ; Pérez-Farrera during early seedling development; () managing for lower et al., ; Snow & Walter, ; Hall & Walter, ). canopy cover at the juvenile and adult stages to reduce the Key ecosystem functions such as carbon storage can be negative effects of interspecific competition; and () produ- disproportionately enhanced locally by threatened species cing seedlings of both the threatened target species and its such as D. sonorense (e.g. Álvarez-Yépiz & Dovčiak, ; nurse plant species (if necessary) for their reintroduction Leitão et al., ) because rare species often possess unique into suitable habitats, or for augmenting their small natural combinations of functional traits that increase functional di- populations. It may also be necessary to identify and assess versity and resource use (Lyons et al., ; Mouillot et al., the role of local and long-distance dispersers of pollen and ; Álvarez-Yépiz et al., ). The evergreen and long- seeds, to protect them. All of the above guidelines could be lived habit of D. sonorense implies the species contributes implemented in all five tropical dry forest localities where to the regional carbon pool and cycling through longer-term D. sonorense occurs in Mexico (Fig. ). However, the habitat carbon storage (for hundreds of years) and slow carbon of this species is under official protection in only release. In tropical dry forest stands where D. sonorense one of the localities, Alamos (through the federal ecological occurs, up to % of the above-ground biomass has been reserve Sierra de Alamos–Rio Cuchujaqui, which is also

included in UNESCO’s Man and the Biosphere References Programme). Paradoxically, the populations that require  ‐ more active conservation management do not have perman- ACKERLY, D.D. & CORNWELL, W.K. ( ) A trait based approach to community assembly: partitioning of species trait values into ent monitoring, as they occur outside the reserve, thus em- within‐ and among‐community components. Ecology Letters, , phasizing the need to designate new protected areas and to –. work with local communities to increase public awareness ÁLVAREZ-YÉPIZ, J.C., BÚRQUEZ,A.&DOVČIAK,M.(a) in unprotected areas. Ontogenetic shifts in plant–plant interactions in a rare cycad The steps used to implement a trait-based approach within angiosperm communities. Oecologia, , –. coupled with the traditional approach for conservation ÁLVAREZ-YÉPIZ, J.C., BÚRQUEZ, A., MARTÍNEZ-YRÍZAR, A., TEECE, M., YÉPEZ, E.A. & DOVCIAK,M.() Resource partitioning by of D. sonorense may be applicable to other cycads, espe- evergreen and deciduous species in a tropical dry forest. Oecologia, cially those of the genus Dioon;the species of Dioon , –. in Mexico exhibit similar population dynamics, habitat ÁLVAREZ-YÉPIZ, J.C., CUEVA, A., DOVČIAK, M., TEECE,M.&YEPEZ, preferences and responses to threats (Vovides, ; E.A. (b) Ontogenetic resource-use strategies in a rare long-lived  Norstog & Nicholls, ; Yáñez-Espinosa et al., ). cycad along environmental gradients. Conservation Physiology, , cou. The value of including the trait-based approach as an add- ÁLVAREZ-YÉPIZ, J.C. & DOVČIAK,M.() Enhancing ecosystem itional conservation tool is particularly important consid- function through conservation: threatened plants increase local ering that, despite the long history of conservation efforts, carbon storage in tropical dry forests. Tropical Conservation Science, % of all known vascular plant species are currently con- , –.  sidered to be threatened with extinction (RBG Kew, ; ÁLVAREZ-YÉPIZ, J.C., DOVČIAK,M.&BÚRQUEZ,A.( ) Persistence  of a rare ancient cycad: effects of environment and demography. IUCN, ). Some taxonomic groups are particularly at Biological Conservation, , –.   risk; for example, %ofcycadspeciesand %ofcacti BERNHARDT‐RÖMERMANN, M., RÖMERMANN, C., NUSKE, R., PARTH, are categorized as threatened on the IUCN Red List A., KLOTZ, S., SCHMIDT,W.&STADLER,J.() On the (Donaldson, ;Goettschetal.,). The trait-based identification of the most suitable traits for plant functional trait  – approach can be a valuable methodology for guiding the analyses. Oikos, , . BERTNESS, M.D. & CALLAWAY,R.() Positive interactions in conservation of threatened species (sensu IUCN, ), es- communities. Trends in Ecology & Evolution, , –. pecially given the freely accessible, extensive global data- CHEMNICK,J.&GREGORY,T.() Dioon sonorense.InThe IUCN bases of functional traits available for many plant species Red List of Threatened Species : e.TA. Http://dx. (Kattge et al., ). A comprehensive database of func- doi.org/./IUCN.UK.-.RLTS.TA.en. tional traits of threatened species would be particularly [accessed  August ].  helpful in assisting the implementation of the trait-based CHOWN, S.L. ( ) Trait-based approaches to conservation ’ physiology: forecasting environmental change risks from the approach. This approach goes beyond species intrinsic va- bottom up. Philosophical Transactions of the Royal Society B, , lues, as it emphasizes the responses of functional species to –. changing environments, and species’ functions within CONARD, J.M. () Genetic variability, demography, and habitat ecosystems, providing useful new information that com- selection in a reintroduced elk (Cervus elaphus) population. PhD plements traditional research approaches to species thesis. Kansas State University, Manhattan, USA. CRISP, M.D. & COOK, L.G. () Cenozoic extinctions account for the conservation. low diversity of extant gymnosperms compared with angiosperms. New Phytologist, , –. Acknowledgements JCÁY is grateful for the support from DIAMOND, S.E., NICHOLS, L.M., MCCOY, N., HIRSCH, C., PELINI, S.L., Fulbright-Garcia Robles (#15086997), and Doctoral (#214564) and SANDERS, N.J. et al. () A physiological trait-based approach to Postdoctoral (#179045) fellowships from Consejo Nacional de predicting the responses of species to experimental climate Ciencia y Tecnología. Additional funding was provided by warming. Ecology, , –. PROFAPI-ITSON, Dence Fellowship, PLACA and Pack summer re- DÍAZ,S.&CABIDO,M.() Vive la différence: plant functional search grants to JCÁY, and by PAPIIT DGAPA-UNAM #IN207315 diversity matters to ecosystem processes. Trends in Ecology & to AMY. ABM and AMY thank the Dirección General de Asuntos Evolution, , –. – del Personal Académico Programa de Apoyos para la Superación DÍAZ, S., LAVOREL, S., DE BELLO, F., QUÉTIER, F., GRIGULIS,K.& del Personal Académico de la Universidad Nacional Autónoma de ROBSON, T.M. () Incorporating plant functional diversity México for a sabbatical fellowship at the University of Arizona. effects in ecosystem service assessments. Proceedings of the National Enriquena Bustamante provided technical assistance. Academy of Sciences of the United States of America, , – . Author contributions Formulation of original idea, writing and re- DÍAZ-ÁLVAREZ, E.A., LINDIG-CISNEROS,R.&DE LA BARRERA,E. vision of article: JCÁY; writing and revision: MD; contribution of () Responses to simulated nitrogen deposition by the ideas, revision of article: AB and AMY. neotropical epiphytic orchid Laelia speciosa. PeerJ, ,e. DONALDSON, J.S. () Cycads. Status Survey and Conservation Conflicts of interest None. Action Plan IUCN/SSC. Cycad Specialist Group, IUCN, Gland, Switzerland. Ethical standards This research complied with the Oryx Code of GARNIER,E.&NAVAS, M.L. () A trait-based approach to Conduct for authors. comparative functional plant ecology: concepts, methods and

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