Reintroduction of illegally extracted Melocactus violaceus (Cactaceae) in Brazil
H AISSA DE A BREU C AITANO,VALQUÍRIA F ERREIRA D UTRA R ODRIGO T HEÓFILO V ALADARES and L UANA S ILVA B RAUCKS C ALAZANS
Abstract Cactaceae is one of the most threatened plant fam- of the declines of these species (Machado et al., ; ilies, in part as a result of the illegal extraction of plants for Cardoso et al., ). ornamental use. However, reports of the seizure and reintro- Melocactus violaceus Pfeiff., popularly known as coroa-de- duction of cacti are scarce and do not include species of frade, is endemic to eastern Brazil (Taylor & Zappi, ). The Melocactus, the genus of Cactaceae in Brazil that has the species occurs in the Caatinga and Atlantic Forest, in the car- highest number of threatened species. The coroa-de-frade rasco, campo rupestre and resting a phytophysiognomies Melocactus violaceus is endemic to Brazil and categorized (The Brazil Flora Group, )onthesedimentarycoastal as Vulnerable on the IUCN Red List. We report the seizure plain, and is categorized as Vulnerable on state, national of individuals of coroa-de-frade extracted illegally from and global Red Lists (Simonelli & Fraga, ; Machado their natural habitat, the results of their reintroduction et al., ; Braun et al., ). Although the species is legally to Paulo César Vinha State Park, in Espírito Santo state, protected, it is often sold in urban centers of coastal Brazil Brazil, and provide information for environmental monitor- (authors, pers. obs., ). Extraction is mainly of reproduc- ing agencies regarding how to proceed in seizure cases, with tively mature individuals, which have a developed cephalium the goal of minimizing the impacts of this illegal practice on (reproductive branch) that increases the species’ ornamental the species. After seizure, individuals were cultivated in a value. Although monitoring results in the seizure of speci- greenhouse and were reintroduced in restinga, the natural mens destined for the clandestine market, technical guidance area of occurrence of the species. After months, survival on replantation of cacti into the wild is limited (e.g. Jasper was % for those individuals cultivated in the greenhouse et al., ). Providing guidance for the reintroduction of and % for those planted in restinga, showing that rapid this endemic, threatened species is essential to guarantee its reintroduction of species with ornamental appeal, prefer- conservation (e.g. Godefroid et al., ; Fenu et al., ) entially in their natural habitat, can reduce the impacts of through the proper management of seized specimens. illegal extraction. This reintroduction protocol can be used Here, we report the first exploratory study to test condi- by managers of conservation units, contributing to the tioning and reintroduction of M. violaceus in restinga vege- maintenance of threatened cactus species in their natural tation, identify health indicators and discuss effects on the habitat. conservation of the species. For this we used adult in- dividuals illegally extracted from Paulo César Vinha State Keywords Atlantic Forest, Brazil, Cactaceae, conservation, Park in Espírito Santo state, Brazil (Fig. ), a priority area coroa-de-frade, globose cacti, Melocactus violaceus, restinga for conservation of threatened species in eastern Brazil (Brasil, ). The plants were being sold by street vendors and were seized by the environmental monitoring agency he family Cactaceae is one of the most threatened plant Instituto Estudual de Meio Ambiente e Recursos Hídricos – Tfamilies, with % of its species threatened to some in September (Plates a d). At the time of seizure, degree (Goettsch et al., ). In Brazil, c. %of cacti the plants were bundled together in a box; the roots of species are threatened (Machado et al., ; The Brazil some individuals were cut or tied (to facilitate sale), without Flora Group, ). The principal threats are fragmentation rhizosphere. After seizure, in view of the lack of a standard- and loss of habitat quality, mining and illegal commercial- ized protocol for reintroducing the species into the wild, ization (Ribeiro-Silva et al., ). The extraction and illegal the Park staff asked us to help, and permitted an exploratory trade of globose cacti (e.g. species of Discocactus Pfeiff., experiment to reintroduce individuals into the Park. Melocactus Link & Otto, Parodia Speg.) are the main drivers A few days after seizure, two experiments were started and monitored for months: () individuals were con- ditioned in containers (c. cm tall and cm diameter) containing sand enriched with organic substrate, in a propa- HAISSA DE ABREU CAITANO (Corresponding author, orcid.org/0000-0003-2319- 5288), VALQUÍRIA FERREIRA DUTRA ( orcid.org/0000-0003-1547-1377), RODRIGO gation shelter covered by netting with % luminosity, THEÓFILO VALADARES ( orcid.org/0000-0002-6528-2278) and LUANA SILVA no horticultural treatments and only irrigated when there BRAUCKS CALAZANS ( orcid.org/0000-0002-3308-3725) Universidade Federal . do Espírito Santo, Vitória, Brazil. E-mail [email protected] were days without rain; and ( ) individuals were planted directly in a non-inundated open shrub formation Received October . Revision requested December . Accepted April . of restinga (Pereira, ) were the species naturally occurs,
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike licence (http://creativecommons.org/licenses/by-nc-sa/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the same Creative Commons licence is included and the original work is properly cited. The Downloadedwritten from https://www.cambridge.org/core permission of Cambridge University. IP Press address: must be170.106.33.22 obtained for, on commercial 26 Sep 2021 re-use. at 22:10:12, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/termsOryx, Page 1 of 4 © The Author(s),. https://doi.org/10.1017/S0030605320000344 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605320000344 2 H. d. A. Caitano et al.
FIG. 1 Location of Paulo César Vinha State Park, Espírito Santo state, Brazil.
PLATE 1 (a) Natural habitat of Melocactus violaceus in restinga, (b) location where the seizure was made, (c) seized individuals bundled inside a box, (d) roots tied to facilitate commercialization, (e) individuals cultivated in the greenhouse, and (f) individual reintroduced into the wild.
up to cm from the borders of thickets, which, according health. Indicators of good health included maintenance of to field observations and the literature (Hughes et al., ), the greenish epidermis (Plate a), formation of new spines is the environment in which the species normally occurs. To (Plate b) and production of flowers and fruits (Plate c). accommodate the roots, a hole – cm deep was dug, de- Indicators of poor health included changes in epidermis pending on the length of the individual plant’s roots. If colour, varying from yellowish to darkened (Plate d)afew the roots were tangled, they were untangled and planted weeks before death, and susceptibility to pests (Plates e,f). in the containers (Plate e) or soil (Plate f), and then abun- Of the individuals cultivated in the greenhouse, % sur- dantly watered. vived, with the death of % plants – months after plant- Based on our observations of the seized individuals over ing, and of the plants reintroduced in the restinga, % months, and field observations of natural populations of survived, with the death of % of plants after months. M. violaceus made during –, we identified macro- The production of reproductive structures in both experi- scopic indicators (IUCN, ; Fenu et al., ) of plant ments was no different from that in natural populations.
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PLATE 2 Macroscopic indicators used to evaluate the health of individuals: (a) maintenance of greenish epidermis, (b) formation of new spines, (c) flower and fruit production, (d) colour change of epidermis, and (e, f) susceptibility to pests.
Some of the plants that died included those that had roots ornamental under inadequate environmental conditions, damaged during extraction or a cut primary root. There was something that often occurs when individual plants are no production of vegetative propagules in either group. commercialized illegally. Survival rate was similar to that for species of Cereus The success of both cultivation in the greenhouse and re- Mill., Lepismium Pfeiff., Rhipsalis Gaertn., Parodia Speg. introduction may serve as a model for other globose cacti and Opuntia Mill. (Jasper et al., ). The greater mortality that are extracted illegally and then seized by law enforce- rate of the individuals in the greenhouse suggests that ex situ ment officials. Our results indicate that in cases of seizure cultivation may not be as reliable as in situ reintroduction. the individuals need to be planted as quickly as possible, As mortality only occurred c. months after planting, the preferentially in the habitat where they naturally occur, species could be kept in a temporary environment, such as which for M. violaceus is along the edges of thickets in rest- a greenhouse, if it is not possible to immediately reintroduce inga. The hole made needs to adequately accommodate the the plant to its natural environment. Although there were roots and establishment needs to be monitored using indi- no changes in development of reproductive branches, this cators of health. When plants cannot be planted immedi- may probably be related to stress from extraction in the ately into the wild, they could be maintained in containers initial months after planting (Schmalenbach et al., ). in a greenhouse until reintroduction is feasible. Subsequent For both experiments, most of the seized individuals that monitoring should evaluate recruitment amongst the re- still had roots with a thin layer of rhizosphere survived, introduced plants (Cogoni et al., ; Fenu et al., ). which indicates that the integrity of the roots is an Natural populations produce small vegetative propagules important factor for successful plantation. that are wind dispersed (Ribeiro et al., ). This character- Although survival was relatively high, it was lower under istic, along with the monitoring of health indicators, will controlled conditions than when plants were reintroduced contribute to the maintenance of the relictual populations into the wild. In a broader context, this suggests a lower of M. violaceus. Our findings indicate how rapid and effective chance of survival when the plant is cultivated as an actions can support the maintenance of a plant species
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threatened with extinction, and will be of value for decision FENU, F., COGONI,D.&BACCHETTA,G.() The role of fencing in makers in the processes of environmental licensing, guid- the success of threatened plant species translocation. Plant Ecology, – ing conservation actions in accordance with the Brazilian , . GODEFROID, S., PIAZZA, C., ROSSI, G., BUORD, S., STEVENS, A.D., Alliance for Zero Extinction (Brasil, ). AGURAIUJA, R. et al. () How successful are plant species reintroductions? Biological Conservation, , –. Acknowledgements We thank Weverson Cardoso for his com- GOETTSCH, B., HILTON-TAYLOR, C., CRUZ-PIÑÓN, G., DUFFY, J.P., ments on the text, and the manager and staff of Parque Estadual FRANCES, A., HERNÁNDEZ, H.M. et al. () High proportion of Paulo Cesar Vinha and Instituto Estadual de Meio Ambiente e cactus species threatened with extinction. Nature Plants, , . Recursos Hídricos for their encouragement and logistical support. HUGHES, F.M., JACOB, C.M. & BORBA, E.L. () Fate of cohorts in This study was financed in part by the Coordenação de Aper- Melocactus (Cactaceae) species is affected by rainfall uncertainty — feiçoamento de Pessoal de Nível Superior Finance Code 001 (MSc and microrelief structures. Brazilian Journal of Botany, , –. scholarship to HAC and PhD scholarship to RTV). IUCN () IUCN Guidelines for Re-Introductions. IUCN/Species Survival Commission Reintroduction Specialist Group, IUCN, Author contributions Study design: HdAC, VFD, RTV; fieldwork: Gland, Switzerland and Cambridge, UK. HdAC, RTV, LSBC; data analysis: HdAC, RTV; writing: HdAC, VFD, JASPER, A., FREITAS, E.M., MUSSKOPF, E.L. & BRUXEL,J.() RTV, LSBC. Metodologia de salvamento de Bromeliaceae, Cactaceae e Orchidaceae na pequena central hidrelétrica (pch) salto forqueta— Conflicts of interest None. São José do Herval/Putinga—RS—Brasil. Pesquisas, Botânica, , –. Ethical standards All activities conducted during the study were MACHADO, M., MENEZES, M.O.T., SANTOS, M.R., PIETRO, P.V., approved by the manager of Parque Estadual Paulo Cesar Vinha. This HERING, R.L.O., BARROS, F.S.M. et al. () Cactaceae. In Livro research was authorized by Instituto Estudual de Meio Ambiente Vermelho da Flora do Brasil (eds G. Martinelli & M.A. Moraes), e Recursos Hídricos under license GRN 028R-2015 (process pp. –. Andrea Jakobsson, Instituto de Pesquisas Jardim 71911308), and otherwise abided by the Oryx guidelines on ethical Botânico do Rio de Janeiro, Rio de Janeiro, Brazil. standards. PEREIRA, O.J. () Restinga. In Atlas de ecossistemas do Espírito Santo (ed. J.L. Lani). pp. . SEMA, Viçosa, Brazil. RIBEIRO, E.M.S., MEIADO, M.V. & LEAL, I.R. () The role of clonal References and sexual spread in cacti species dominance at the Brazilian Caatinga. Gaia Scientia, , –. RASIL B ( ) Reconhece os Sítios da Aliança Brasileira para Extinção RIBEIRO-SILVA, S., ZAPPI, D.C., TAYLOR, N.P. & MACHADO, M.C. () — Zero Sítios-BAZE. Portaria de de julho de . Diária Plano de Ação Nacional para a Conservação das Cactáceas. Instituto Oficial da União, , . Chico Mendes de Conservação da Biodiversidade, Brasília, Brazil. RAUN ACHADO AYLOR APPI B , P., M , M., T , N.P. & Z , D.C. ( ) SCHMALENBACH, I., ZHANG, L., REYMOND,M.&JIMÉNEZ-GÓMEZ, Melocactus violaceus (amended version of assessment). In The J.M. () The relationship between flowering time and growth IUCN Red List of Threatened Species : e.T A . responses to drought in the Arabidopsis Landsberg erecta x dx.doi.org/ . /IUCN.UK. - .RLTS.T A .en Antwerp- population. Frontiers in Plant Science, , . [accessed July ]. SIMONELLI,M.&FRAGA, C.N. () Espécies da Flora Ameaçadas de CARDOSO, W.C., CALVENTE, A., DUTRA,V.F.&SAKURAGUI, C.M. Extinção do Espírito Santo. IPEMA, Vitória, Brazil. ( ) Anthropic pressure on the diversity of Cactaceae in a region TAYLOR,N.&ZAPPI, D.C. () Additions and corrections to ‘Cacti – of Atlantic Forest in eastern Brazil. Haseltonia, , . of eastern Brazil’. Bradleya, , –. OGONI ENU ONCAS ACCHETTA C , D., F , G., C ,E.&B ,G.( ) The THE BRAZIL FLORA GROUP () Brazilian Flora : innovation effectiveness of plant conservation measures: the Dianthus and collaboration to meet target of the Global Strategy for Plant – morisianus reintroduction. Oryx, , . Conservation (GSPC). Rodriguésia, , –.
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