The need for multidisciplinary conservation: a case study of Ceratozamia (Zamiaceae, Cycadales) in eastern Mexico
L ILÍ M ARTÍNEZ-DOMÍNGUEZ,FERNANDO N ICOLALDE-MOREJÓN D ENNIS W M .STEVENSON,QUIYARI J. SANTIAGO-JIMÉNEZ O CTAVIO R OJAS-SOTO and F RANCISCO V ERGARA-SILVA
Abstract As an evolutionary lineage cycads are rare, and Keywords Ceratozamia, cycads, ecological niche model- the extinction risk is high for many species. The genus ling, Mexico, multidisciplinary approach, protected areas, Ceratozamia, one of the most diverse in Mexico, is experi- socio-cultural perceptions encing drastic reductions of its habitat. Ceratozamia is wide- Supplementary material for this article is available at ly distributed along the Sierra Madre Oriental, a complex doi.org/./S mountain range, in a region characterized by high ecological and cultural diversity. Since , various conservation and management strategies have been applied to this taxon in Introduction Mexico but evidence for the effectiveness of these mea- sures is lacking. Ceratozamia in the Mexican Sierra Madre he genus Ceratozamia (Zamiaceae: Cycadales) is wide- Oriental is highly diverse and endemic, offering a model Tly distributed and highly diverse in Mexico, with for analysing geographical distribution patterns with eco- species occurring in the country (Calonje et al., ). logical niche modelling. It also presents an opportunity Nearly %ofCeratozamia species are endemic to the for assessing the success of conservation and management Sierra Madre Oriental, a complex mountain range that strategies that have been implemented in this area. Here, harbours the greatest diversity of species belonging to we examined three aspects that are considered fundamental this genus. Given the threatened status of Ceratozamia for the development and evaluation of conservation strat- (the genus is listed on CITES Appendix I, and several spe- egies: ( ) taxonomy, ( ) ecology and ( ) sociocultural an- cies are categorized as threatened on the IUCN Red List; thropology. Our findings suggest a pessimistic outlook for CITES, ), there is an urgent need to develop conserva- the long-term survival of Ceratozamia species in their nat- tion strategies, but this is hampered by a paucity of infor- ural environment, indicating the need to review the current mation on cycad distribution. IUCN Cycad Action Plan for the genus. To improve the Cycads grow slowly, can live for several hundred years protection of Ceratozamia and other taxonomic and/or and struggle to survive in disturbed habitats, making them ecological assemblages, we encourage a multidisciplinary important indicators of habitats in good conservation status approach, with increased collaboration between natural (Norstog & Nicholls, ). Assessing cycad distribution and social scientists. could thus contribute to the mapping of priority areas for ecosystem conservation in Mexico. The most threatened vegetation types in Mexico are oak, pine–oak and cloud for- ests, which occur widely in the Sierra Madre Oriental and are characteristic habitats for most species of Ceratozamia LILÍ MARTÍNEZ-DOMÍNGUEZ* and FERNANDO NICOLALDE-MOREJÓN (Corresponding (Contreras-Medina, ). author, orcid.org/0000-0003-1423-7474) Laboratorio de Taxonomía Integrativa, Instituto de Investigaciones Biológicas, Universidad Veracruzana, The Cycad Action Plan (Donaldson, ) is an inter- Xalapa, 91190, Veracruz, Mexico. E-mail [email protected] national initiative of the IUCN Cycad Specialist Group fo-
DENNIS WM.STEVENSON The New York Botanical Garden, New York, USA cusing on sustainable use and ex situ conservation. These
QUIYARI J. SANTIAGO-JIMÉNEZ Facultad de Biología, Universidad Veracruzana, approaches have led to a number of international initiatives Xalapa, Veracruz, Mexico (Graham et al., ; Griffith et al., ), with the main
OCTAVIO ROJAS-SOTO Laboratorio de Bioclimatología, Red de Biología Evolutiva, focus being on the cultivation of cycads in nurseries. This Instituto de Ecología, Xalapa, Veracruz, Mexico is also the case in Mexico, where the most frequently pro- FRANCISCO VERGARA-SILVA Laboratorio de Sistemática Molecular, Jardín posed conservation action has been the establishment of Botánico, Instituto de Biología, Universidad Nacional Autónoma de México, Coyoacán, Mexico nurseries to support sustainable management of cycads, which are often planted for ornamental purposes (Vovides *Also at: Centro de Investigaciones Tropicales, Universidad Veracruzana, Xalapa, Veracruz, Mexico & Iglesias, ; Vovides et al., ). Received July . Revision requested September . The conservation of Ceratozamia is hampered by poor Accepted March . taxonomic curation of botanical specimens deposited in
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, Downloadeddistribution, from https://www.cambridge.org/core and reproduction in any medium,. IP address: provided 170.106.202.226 the original work, ison properly 24 Sep 2021 cited. at 02:46:45, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, Page 1 of 10 © The Author(s),. https://doi.org/10.1017/S0030605320000204 2021. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000204 2 L. Martínez‐Domínguez et al.
Mexican herbaria and elsewhere, lack of taxonomic revi- Methods sions and limited knowledge of the taxonomic relationships of species within the genus. To study the biology of spe- Species data cies, delimit species distributions and assess extinction risk, correct identification and naming of species is im- We obtained occurrence records for Ceratozamia by review- portant (Wheeler et al., ; Mota-Vargas & Rojas-Soto, ing the specimens available in the following herbaria: ), but the distribution of the various species of Cera- CHAPA, CIB, ENCB, FCME, FTG, GH, HEM, IEB, K, LE, tozamia in the Sierra Madre Oriental remains poorly LSU, MB, MICH, MEXU, MO, NY, P, SERO, SLPM, U, known. Some Ceratozamia species occur within desig- UAT, US, XAL, and XALU (acronyms according to Index nated protected areas, but how many or which ones is Herbariorum; Thiers, ). This review was based on the unknown. taxonomic concepts of species proposed by Nicolalde- Ecological niche modelling predicts the distribution of Morejón et al. ( ) and Martínez-Domínguez et al. ( ). species using spatial analysis of environmental variables We also included information collected in the field during – (Holt, ). It is a valuable tool for the development and . We conducted fieldwork on Ceratozamia evaluation of conservation strategies (Peterson et al., ) populations throughout the Mexican Sierra Madre Oriental, and has been shown to be effective in studies of the distribu- to corroborate existing records and/or obtain new localities tion of many taxa (Mota-Vargas & Rojas-Soto, ; Peterson for species. Because of the clustered distribution of species, & Soberón, ), but has rarely been used in analyses of we used preliminary information on distribution and eco- the distribution of cycads. logical requirements to locate Ceratozamia populations. Evidence of the effectiveness of current conservation In localities we interviewed local people, showing them actions for Mexican Ceratozamia species is lacking. Out- photographs and describing the morphological characters comes of ongoing conservation programmes, which involve representative of the genus, and asking about potential participation of local communities in the propagation and sites in the vicinity that may have suitable habitat for cycads, care of nursery plants, have not been evaluated (Vovides such as karstic rocks. We recorded the geographical coordi- et al., ), and potential conceptual and methodological nates of each site where we located cycad plants and com- shortcomings that could restrict their success have not been piled this information in a database in ArcMap . (Esri, considered (Bottrill & Pressey, ). In addition, there is a Redlands, USA). Records without precise locality data, or disconnect between conservation policies and management with coordinates that could not be corroborated during strategies recommended by biologists and the needs and fieldwork, were omitted. To examine the distribution of activities of local communities. This calls for collaborative, Ceratozamia in the Sierra Madre Oriental, we superimposed multidisciplinary approaches, with the aim to implement the points of occurrence on the biogeographical province conservation strategies in partnership between local com- proposed by Paniagua & Morrone ( ). munities and conservation biologists/managers (Orlove & Brush, ). Environmental layers, ecological niche modelling and Here, we evaluate the conservation and management distribution strategies for Ceratozamia in the Sierra Madre Oriental, using multidisciplinary methods from both natural and We used interpolated climatic layers of bioclimatic vari- social sciences (Halme et al., ;Bennett,). Specifically, ables from WorldClim (Hijmans et al., ) at a spatial we examine the taxonomy and biogeographical characteris- resolution of " (c. km cell size) to characterize ecological tics of the genus, and local perceptions of, and attitudes niches. We reduced dimensionality and collinearity between towards, existing conservation programmes. We also dis- the bioclimatic layers by applying principal component cuss prospects for additional multidisciplinary approaches analysis (PCA) with the function PCARaster in the R .. for the conservation of cycads. package ENMGadgets (Barve & Barve, ; R Development Core Team, ). We retained the first six components Study area for modelling because they explained c. % of the overall variance in environments for all species. Niche modelling The Sierra Madre Oriental is a mountain range that emerges was performed with Maxent (Phillips et al., ) because from the coastal plain of the Gulf of Mexico towards the of its high predictive capability with presence-only data central high plateau of Mexico. It is km long and – (Elith et al., ), and the dismo package (Hijmans et al., km wide (Eguiluz de Antuñano et al., ). Ceratozamia )inR. Because the seeds of cycads are dispersed mainly species occur at an altitude of –, m on karstic rocks. by gravity (rarely by rodents, and then only over short People living in this area are ethnically diverse and prac- distances), watersheds could be barriers to the dispersion tice subsistence- and market-oriented production (Toledo of the species. We calibrated models within the accessible et al., ). area (i.e. the area where the species could occur considering
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dispersion barriers and the historic conditions in the region) (). In addition, we identified two nurseries for Ceratoza- for each species (Barve et al., ). We used polygons re- mia in the Sierra Madre Oriental (Vovides et al., ), in the presenting the watershed system of Mexico, and selected municipality of Coacoatzintla (Veracruz State): Tachinola and those polygons where at least one record was present. Dos Cerros. Both nurseries grew C. tenuis. Because of the small number of records, we used %of To examine local perceptions of the nurseries, we in- occurrences for calibration. Models included five bootstrap- terviewed people with varying degrees of involvement in type replicas, and we selected those with the highest value the management and running of these conservation facili- for the area under the receiver operating characteristic ties (Supplementary Table ). We identified four groups curve (AUC). We transformed the predictions obtained of participants: () representatives of local municipal insti- into a binary map ( = absence, = presence), including tutions, () researchers who promoted and implemented the total number of records in all cases corresponding to Ceratozamia conservation through nurseries, () members the lowest presence threshold (i.e. the minimum training of the community who participated in nursery activities presence of Maxent). We validated model predictions for and () community members who did not participate species with , presence records through jackknife tests (Supplementary Table ). We also asked members of local (Pearson et al., ); for species with $ records, communities about their understanding, interpretation analyses were conducted with PartialROC (Barve, ; and evaluation of conservation strategies (Bennett, ). Peterson et al., ; Supplementary Table ). During May–August we interviewed local residents (nine men and one woman) from different socio-economic backgrounds. The semi-structured interviews lasted – Evaluation of current conservation and management minutes, and six were audio-recorded. Four participants strategies did not consent to audio recordings; we took detailed notes in these cases. We asked about the participants’ The binary models were summed using the Algebra map knowledge of the nursery, their level of participation and tool in ArcMap, and then reclassified to produce a richness perceived effects of the nursery on the community (includ- accumulation map. Although this method could potentially ing benefits and conflicts arising during project manage- overestimate species richness in some areas, we believe it is ment). All participants gave oral consent for the use of suitable here because it did not predict areas that would the information, and their anonymity was preserved. We not be suitable for Ceratozamia (e.g. Calabrese et al., ; analysed the interviews qualitatively following standard D’Amen et al., a,b). To visualize areas potentially practices in sociocultural anthropology and ethnobiology, affected by anthropogenic land-use changes, we clipped using the characteristics of the content to detect any trends. species richness maps using the most recent series of data During the analysis, we attempted to identify any temporal on land use and vegetation coverage provided by the changes in the development of the nurseries (Bernard, ; Mexican Instituto Nacional de Geografía y Estadística Albuquerque et al., ). (INEGI, ). To assess the role of protected areas pro- grammes, we evaluated species richness in areas of four protection categories: State, Municipal, Common Land Results and Private Natural Protected Areas, following the Mexican Comisión Nacional para el Uso y Conservación de la Taxonomy of Ceratozamia species in the Sierra Madre Biodiversidad (CONABIO, ) and the Federal Natural Oriental Protected Areas of the Mexican Comisión Nacional de Áreas Naturales Protegidas (CONANP, ). We also The distribution of Ceratozamia species in the Sierra Madre considered Priority Terrestrial Regions (CONABIO, ) Oriental is confined to a narrow eco-climatic zone. In herb- and main regions and subregions of the cloud forest in aria and during our fieldwork, we found a total of unique Mexico (CONABIO, ). In addition, we overlaid species records, with geographical coordinates, of the species richness concentrations upon a cultural map (Boege, ), that occur in this Mexican province. Six species are micro- to evaluate the geographical correspondence of Ceratozamia endemic, of which five are located in the south of the region: diversity with the distribution of ethnic groups. C. brevifrons, C. morettii and C. tenuis occur in the Sierra To evaluate ex situ conservation efforts, we consulted Norte de Puebla-Chiconquiaco region, and C. mexicana is with the curators or directors of the major botanical gardens present in the south in a part of the Antigua Basin and, to in Mexico, either by visiting the collections or via e-mail. a lesser extent, in the Huatusco-Coscomatepec area (Fig. ). To assesses the contribution of botanical gardens to Cera- Ceratozamia decumbens is distributed in the Huautla- tozamia conservation, we confirmed the species identities Zongolica region and in a small part of the Orizaba region of live specimens kept in botanical garden collections, (Fig. ), and C. zaragozae is endemic to the Sierra de Álvarez using the taxonomic key by Martínez-Domínguez et al. (San Luis Potosí).
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five species with wide distributions converge, and for which the model predicted suitable ecological conditions for the presence of up to three additional species. The se- cond area was in the south, with mainly micro-endemic spe- cies (Fig. ). Of the total range of Ceratozamia, % has been converted to anthropogenic environments (Fig. ). Species with the smallest potential range occur in the southern area, which has been largely transformed. Agriculturally driven environmental degradation is most severe within the range of C. mexicana (Table ); in contrast, undisturbed natural habitats persist in the northern area. Ceratozamia latifolia and C. hildae have a greater potential range in areas with original vegetation (Figs & ).
Assessment of conservation status and management strategies
Most Ceratozamia species (%) are under ex situ conser- vation in botanical gardens (Table ). These species occur in seven protected areas (Table ). The Sierra Gorda Bio- sphere Reserve contains three species (C. chamberlainii, C. sabatoi and C. hildae). According to their potential range, C. kuesteriana and C. fuscoviridis could occur in the Altas Cumbres Federal Reserve, in the Chicamole ecological pres- FIG. 1 Modelled potential geographical range of two species of Ceratozamia: the widely distributed C. fuscoviridis and the ervation municipal area (Fig. a), but we were unable to micro-endemic C. tenuis. confirm this during fieldwork. The distribution of Ceratozamia mostly overlaps with several priority areas for conservation, including areas of The remaining eight Ceratozamia species, occurring high species richness in the northern part of the study from the central area to the northern extreme of the region, area. This area is thus of particular importance for the con- have a wider distribution (Fig. ). The species with the servation of the genus (Fig. b). The range of Ceratozamia northernmost distribution, C. kuesteriana, occurs widely in the mountains of the north and central Sierra Madre in two regions: El Cielo, and Canyons of Nuevo Leon and Oriental, and the southern part of the range of the genus, Tamaulipas. In the latter location, we did not locate this spe- overlap with three priority biological and cultural areas cies during fieldwork. Ceratozamia fuscoviridis and C. toto- for conservation and development (Fig. ). Forests are less nacorum occur in the cloud forest between San Bartolo affected by anthropogenic pressures in two of these areas Tutotepec (Hidalgo State) and Cuetzalan (Puebla State), (Fig. ). According to their current categorization in the and in the north-west from Hidalgo to Huayacocotla in IUCN Red List (IUCN, ) and the Mexican list of threat- Veracruz (Fig. ). The distribution of C. totonacorum includes ened species, NOM--SEMARNAT- (SEMARNAT, part of the Sierra Norte de Puebla-Chiconquiaco region. Cera- ), the species with the highest risk of extinction are tozamia hildae and C. latifolia are located in north-west those that have experienced less habitat loss. For example, Hidalgo and as far as Huayacocotla, with vestiges in the San C. kuesteriana has a relatively broad distribution but is Luis Potosí region; the potential distributions for these two categorized as Critically Endangered on the IUCN Red species overlap almost completely. Ceratozamia delucana List. In contrast, C. mexicana is categorized as Vulnerable but is restricted to the Sierra Norte de Puebla-Chiconquiaco occurs in an area with rapid loss of habitat (Supplementary region and to a small cloud forest area in north-west Table , Figs c & ). This suggests that the extinction Hidalgo and Huayacocotla, whereas C. chamberlainii and risk of these species should be re-evaluated to align the C. sabatoi inhabit a single forest area (Fig. ). categorization with actual threat levels. In our survey of the two nurseries, we found that although Species richness and land use approaches varied, outcomes were similar. Tachinola nursery is an Ejidal organization (a form of communal property/ We observed two areas of particularly high species richness. territory common in rural Mexican regions) in operation One was in the northern part of the study area, where since , whereas Dos Cerros nursery is a private initiative
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FIG. 2 Modelled potential geographical distribution for Ceratozamia: (a) northern area, (b) southern area, (c) central area, (d) Ceratozamia species and subregions of cloud forest in Sierra Madre Oriental.
that started in and ceased to operate around . to our questions about future development and further In the case of Tachinola nursery, the conservation actions outcomes of nursery management, most community infor- taken involved seed collections in the wild and transplanting mants recognized the failure of these initiatives. We found of parental plants from wild populations, to protect them three additional problems: () organizational difficulties from potential destruction of their habitat. Both nurseries caused by lack of agreements between technical researchers had three goals: () conservation of C. tenuis,() awareness- and members of the community regarding the sale of plants, raising through social outreach and () contribution to the () lack of direct involvement of the communities in the community’s economy. Economically, Tlachinola provided management and operation of nurseries, and () absence benefits in the form of cash payments to community mem- of a marketing strategy to commercialize the cycad plants bers who participated in cultivation and plant care, and Dos grown in nurseries. Several conflicts within and outside the Cerros provided cash payments to community members for community affected the work. For example, information on helping to transplant Ceratozamia plants, and to nursery the progress of plant sales was not shared with all members managers for carrying out organizational tasks. of the community, and restrictions on the use of natural In both Tlachinola and Dos Cerros, local informants re- resources were imposed by authorities (use of the species ported difficulties in the commercialization of plants (few or is prohibited, except as ornaments on Catholic altars, and no sales of cycads) as a cause for the decline of the nurseries. the use of seeds for food). Other reasons included low prices of plants sold, and exces- Our interviews showed that community members and sive investment of time in relation to perceived benefits, the conservation researchers promoting and implementing which is in part because of the slow growth of the spe- conservation through nurseries differed in their concep- cies. Overall, attitudes of local people towards Ceratozamia tual framing of Ceratozamia conservation. Local people per- conservation through nurseries were negative. In response ceived conservation as protection of the natural resources
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FIG. 3 Modelled potential species richness of Ceratozamia and FIG. 4 Modelled potential species richness of Ceratozamia in the priority biocultural regions for conservation and development. Sierra Madre Oriental (inset: potential geographical distribution of Ceratozamia).
on which they depend, whereas researchers viewed conser- the main conservation challenges are in the southern region, vation primarily as a means of protecting wildlife from which was not evaluated in that study. Species in the south- extinction. ern area have restricted ranges, leaving them vulnerable to habitat destruction and extinction (Fig. ). Across the state of Veracruz, where both diversity and endemism of Discussion Ceratozamia species are high, the areas with the highest concentrations of species richness are unprotected (Fig. ). Through a multidisciplinary approach that links ecological and Despite occurring within a protected area, species such as social aspects, we explored current conservation strategies for C. delucana and C. decumbens have lost more than half of Ceratozamia, a genus of cycads in Mexico. Our data contribute their potential habitat to destruction (Table ). to the understanding of the limits of conservation efforts, and Anthropogenic land-use changes affect protected areas demonstrate challenges for future studies. We combined an in the study region (Fig. ); the southern zone of the exhaustive review of occurrence records in herbaria with the Sierra Madre Oriental is one of the most threatened, with taxonomic concepts proposed by Martínez-Domínguez et al. severely transformed vegetation (Fig. ). Therefore, species () and found that reliable taxonomic information on in the southern zone of the restricted distribution of Cerato- Ceratozamia is lacking, which creates difficulties for the zamia require urgent conservation planning. There is con- assignment of threat categories (Supplementary Table ). siderable overlap between the distribution of Ceratozamia and the main Priority Terrestrial Regions for Conservation Limitations of current conservation strategies (Fig. ) defined by Mexican authorities. These areas are con- sidered relevant for the conservation of many other plant Current protected areas cover only a part of the northern and animal taxa, but forest cover continues to decline. area of the Sierra Madre Oriental, the area with the high- This suggests that current protected areas are ineffective est potential suitability for Ceratozamia (Fig. a). This in conserving species endemic to Mexico. In this context, corresponds with a recent evaluation of the diversity of cycads could serve as biogeographical and ecological model endemic species in the northern part of the study area species in conservation biology studies, as they occur in het- (Salinas-Rodríguez et al., ); however, we found that erogeneous habitats and are frequently associated with other
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TABLE 1 The area where each species is predicted to be present, area transformed to anthropogenic landscapes, whether the area is considered a biocultural priority region (Boege, ), and conservation strategies for Ceratozamia species in the Sierra Madre Oriental, Mexico.
Predicted area Transformed Biocultural Species (km2) habitat (km2) priority region Conservation category C. brevifrons 817 558 No Ex situ: botanical garden C. chamberlainii 3,604 2,762 Yes Ex situ: botanical garden In situ: Biosphere Reserve Sierra Gorda C. decumbens 1,084 836 Yes Ex situ: botanical garden In situ: State Reserve Metlac-Río Blanco C. delucana 1,642 1,118 Yes Ex situ: botanical garden In situ: State Reserve Río Filolobos & surroundings C. fuscoviridis 6,674 3,593 Yes Ex situ: botanical garden In situ: Los Mármoles National Park C. hildae 6,631 2,206 Yes Ex situ: botanical garden In situ: Biosphere Reserve Sierra Gorda C. kuesteriana 19,599 8,748 Yes Ex situ: botanical garden In situ: Biosphere Reserve El Cielo C. latifolia 8,148 2,729 Yes Ex situ: botanical garden C. mexicana 737 647 No Ex situ: botanical garden C. morettii 782 535 No Ex situ: botanical garden C. sabatoi 1,447 524 Yes Ex situ: botanical garden In situ: Biosphere Reserve Sierra Gorda, Los Mármoles National Park C. tenuis 258 203 No Ex situ: botanical garden, nursery Tlachinola (inactive), nursery Dos Cerros (closed) C. totonacorum 4,345 1,073 Yes In situ: hydrological basin of River Necaxa C. zaragozae Not available Not available No Ex situ: botanical garden In situ: El Potosí National Park
endemic species. In situ conservation actions are required and are characterized by high levels of biological, agrobio- to mitigate the loss of diversity in these cloud forests, which logical and cultural diversity (Boege, ). The fact that comprise highly diverse and productive ecosystems in Mexico these areas harbour a large number of Ceratozamia species (Gual-Díaz & González-Medrano, ). could be a result of the past activities of diverse Meso- Ex situ conservation initiatives have dominated the american peoples, who have managed natural resources with- preservation of cycads in Mexico, with botanic gardens play- out destroying or severely damaging the forest (Toledo et al., ing an important role (Griffith et al., ). However, species ). Our findings suggest that, in addition to considering that occur in a narrow geographical area, and/or are strictly the biology of the target taxa, successful conservation and dioecious, tend to have reduced ranges and populations management of threatened species must enable active and when their habitats are fragmented by human activities. direct participation of local communities. This community This leaves them more vulnerable to extinction than spe- engagement should not be limited to the provision of eco- cies with a broader distribution. Conserving Ceratozamia nomic benefits during the implementation of conservation species and other cycad genera such as Dioon and Zamia projects, but should start during the planning phase, to requires improved conservation strategies and careful selec- avoid negative perceptions of, and attitudes towards, con- tion of the best strategy depending on the characteristics servation and management strategies. of the species and the area in which it occurs. We detected a series of conflicts in the nurseries studied, such as a lack of dialogue between members of the com- Improving conservation strategies through munity and researchers, discontent and distrust within the multidisciplinary approaches community, difficulty selling the plants, and organiza- tional problems (lack of agreements). In both nurseries, The best preserved areas for Ceratozamia in the Sierra Thachinola and Dos Cerros, members of local communities Madre Oriental, which potentially include the highest num- were considered as employees, rather than principal parti- ber of cycad species (except the range of C. decumbens; cipants. The nature of these conflicts could vary regionally Fig. ), correspond with priority biocultural regions. These because of diverse factors (e.g. social values, socio-economic are territories with long-term occupation by Indigenous status). Our work could serve as a starting point for a com- peoples and peasant communities of Mesoamerican origin, prehensive analysis of nurseries management. Development
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FIG. 5 Modelled potential species richness of Ceratozamia and (a) protected areas, and (b) Priority Terrestrial Regions for Conservation (CONABIO, ).
of a more complex socio-environmental framework is ne- conservation, several studies have pointed out the need to cessary to plan any further establishment of cycad nurseries combine approaches from basic and applied and/or social in the communities in the study area. We recommend that science, and to apply a holistic perspective to complex pro- communities should be involved in conservation planning blems (Lindenmayer & Hunter, ). Biodiversity conser- from the start, as principal actors, in coordination with the de- vation requires both information on species’ biology, and velopers of planning processes. In addition, the current practice acceptance of science-based programmes by communi- of cultivating a single species could be replaced with diversified ties, whose priorities and viewpoints need to be considered. models featuring a range of products and practices, such as cul- Conservation strategies thus need to be evaluated from a tivation of cycads and other species with faster growth rates, or multidisciplinary perspective, through assessment of eco- inclusion of recreational activities such as tourist trails. logical and taxonomic issues combined with an examination Overall, our findings suggest that the conservation status of social perceptions. Such collaborative approaches have of most Ceratozamia species needs to be re-evaluated. In the potential to improve the effectiveness of ex situ con- particular, the threat categories used in Mexican legislation servation strategies for Ceratozamia and other taxa. need to be updated (Figs & ). Considering that most cycad species in this area have cultural importance as religious Acknowledgements This research was supported in part by Consejo symbols (Bonta et al., ), a re-evaluation of the relation- Nacional de Ciencia y Teconología under grant 134960 to FNM, and ship between cycads and people is important for the conser- National Science Foundation grants BSR-8607049 and EF-0629817 to DWS. LMD thanks CONACYT for the award of a Masters degree vation of this group. We recommend community-managed scholarship. We thank C. Yañez-Arenas and S. Jiménez-García for ad- protected areas to improve conservation effectiveness, and vice on ecological niche modelling and the socio-cultural anthropology the incorporation of traditional knowledge in the planning aspects, respectively; the curators of all herbaria; the communities in and implementation of conservation actions (Berkes, ; the municipality of Coacoatzintla for their cooperation; the anony- Shahabuddin & Rao, ). This is particularly applicable in mous reviewers for their constructive critiques; and the editors for priority areas for biocultural conservation and development their extensive help in finalizing the text. that have a high species richness, such as those harbouring Author contributions Study design: LMD, FNM, FVS; data collec- C. sabatoi, C. hildae, C. kuesteriana, C. zaragozae and C. tion: LMD, FNM; data analysis: LMD, FNM, ORS; writing and revi- fuscoviridis (Fig. ). Working at the scale of ecosystem sions: all authors.
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