UNIVERSIDADE FEDERAL DO CEARÁ CENTRO DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA E RECURSOS NATURAIS
LUCAS FIGUEIREDO SOARES
COMO AS MUDANÇAS CLIMÁTICAS PODEM INFLUENCIAR A DISTRIBUIÇÃO DE ESPÉCIES XERÓFITAS?
FORTALEZA 2019
LUCAS FIGUEIREDO SOARES
COMO AS MUDANÇAS CLIMÁTICAS PODEM INFLUENCIAR A DISTRIBUIÇÃO DE ESPÉCIES XERÓFITAS?
Dissertação apresentada ao Programa de Pós-Graduação em Ecologia e Recursos Naturais da Universidade Federal do Ceará, como requisito parcial à obtenção do título de mestre em Ecologia e Recursos Naturais. Área de concentração: Ecologia e Recursos Naturais.
Orientador: Profa. Dra. Maria Iracema Bezerra Loiola.
FORTALEZA 2019
LUCAS FIGUEIREDO SOARES
COMO AS MUDANÇAS CLIMÁTICAS PODEM INFLUENCIAR A DISTRIBUIÇÃO DE ESPÉCIES XERÓFITAS?
Dissertação apresentada ao Programa de Pós-Graduação em Ecologia e Recursos Naturais da Universidade Federal do Ceará, como requisito parcial à obtenção do título de mestre em Ecologia e Recursos Naturais. Área de concentração: Ecologia e Recursos Naturais.
Aprovada em: 10/04/2019.
BANCA EXAMINADORA
________________________________________ Profa. Dra. Maria Iracema Bezerra Loiola (Orientadora)
Universidade Federal do Ceará (UFC)
_________________________________________ Profa. Dra. Andréa Pereira Silveira
Universidade Estadual do Ceará (UECE)
________________________________________ Prof. Dr. Sebastião Medeiros Filho
AGRADECIMENTOS
À CAPES, pelo apoio financeiro com a concessão da bolsa de auxílio;
À Profa. Dra. Maria Iracema Bezerra Loiola, pela excelente orientação e por confiar no meu trabalho;
Aos professores participantes da banca examinadora, Dr. Sebastião Medeiros Filho, Dra. Andréa Pereira Silveira e Dra. Ingrid Koch pelas valiosas colaborações e sugestões;
Ao Marcelo Oliveira Teles de Menezes, pela colaboração no manuscrito e ideias sugeridas;
À Luciana Silva Cordeiro, por toda a ajuda durante a elaboração dos modelos e do manuscrito;
Aos demais amigos do Laboratório de Sistemática e Ecologia Vegetal (LASEV): Valéria Sampaio, Fernanda Melo Gomes, Rayane Ribeiro, Edenilce Peixoto, Carlos Píffero, Tatiane Nojosa, Natanael Pereira, Francisco Yago, Kyhara Soares e Diego Costa;
Aos amigos da pós-graduação: Luana Guimarães, Elvis Franklin, Gabriela Ramires, Sérgio Lucas, Sabrina Moura, Margarida Xavier, James Castro, Antônio Xavier, Mônica Santana, Robson Victor, Hélio Coelho, Frede Lima e os demais da turma de 2017;
Aos professores da pós graduação, em especial Roberta Zandavalli, Rogério Parentoni, Roberto Feitosa, Lorenzo Zanette e Rafael Carvalho pelas reflexões, críticas e sugestões recebidas;
À toda minha família, em especial minha vó Zuila Figueiredo e minha irmã Livia Figueiredo;
Ao Mikael Mendes e aos amigos Raquel Castro e Marcelle Yanari;
“They say that dreaming is free, but I wouldn’t care what it cost me.”
RESUMO
As mudanças climáticas transformam as condições ambientais, e consequentemente, afetam a distribuição dos organismos em todo o planeta. Objetivamos com este estudo biogeográfico compreender a probabilidade de ocorrência futura de cinco espécies xerófitas do gênero Tacinga Britton & Rose (Cactaceae), distribuídas no semiárido brasileiro, em domínios fitogeográficos de caatinga e cerrado. Para tal, utilizamos variáveis bioclimáticas que derivaram os modelos futurísticos presentes no manuscrito. Nossa hipótese é que devido ao aquecimento global previsto para os próximos anos, espécies xerófitas terão a distribuição geográfica favorecida e expandida mesmo em áreas com risco de desertificação. No entanto, nossos resultados sugerem que este fator deve ser analisado de acordo com cada táxon, pois nem todas as espécies irão expandir sua distribuição. Verificamos que no território brasileiro existem locais estratégicos para a preservação dessas espécies como a Chapada Diamantina na Bahia, considerado um refúgio biológico do gênero. Concluímos que espécies com probabilidade de ocorrência mais restritas, como T. funalis e T. saxatilis precisam ser conservadas, devido uma possível restrição geográfica em tempos futuros, mais precisamente em 2050.
ABSTRACT
Climate change transforms environmental conditions, and consequently, affects the distribution of organisms around the planet. We aim with this biogeographic study to understand the probability of future occurrence of five xerophyte species of the genus Tacinga Britton & Rose (Cactaceae), distributed in the Brazilian semi-arid, in phytogeographic domains of caatinga and cerrado. For this, we used bioclimatic variables that derived the futuristic models present in the manuscript. Our hypothesis is that due to global warming predicted for the coming years, xerophytic species will have the geographical distribution favored and expanded even in areas at risk of desertification. However, our results suggest that this factor should be analyzed according to each taxon, since not all species will expand their distribution. We verified that in the Brazilian territory there are strategic locations for the preservation of these species such as the Chapada Diamantina in Bahia, considered a biological refuge of the genus. We conclude that species with a more restricted probability of occurrence, such as T. funalis and T. saxatilis need to be conserved, due to a possible geographical restriction in future times, more precisely in 2050.
LISTA DE FIGURAS
Figura 1- Detalhe do hábito das espécies de Tacinga (Cactaceae) estudadas. (a) T. funalis, (b) T. inamoena, (c) T. palmadora e (d) T. werneri.
Fotos por Marcelo Oliveira Teles de Menezes... 25 Figura 2- Distribuição atual das espécies de Tacinga: (a) T. funalis, (b) T.
inamoena, (c) T. palmadora, (d) T. saxatilis e (e) T. werneri ...
... 26 Figura 3- Distribuição potencial das espécies Tacinga (Cactaceae) no Brasil.
(a) T. funalis, (b) T. inamoena, (c) T. palmadora, (d) T. saxatilis e (e) T. werneri para 2050, com o aumento da temperatura em 1,5 graus, utilizando variáveis bioclimáticas (Isotermalidade,
Temperatura Média do Bairro Mais Seco, Média Temperatura do Trimestre Mais Quente, Precipitação Anual, Precipitação do Mês Mais Molhado, Precipitação do Mês Mais Seco e Precipitação do Trimestre Mais Úmido) ...
LISTA DE TABELAS
Tabela 1- Projeção dos domínios fitogeográficos e tipos de solos das espécies
SUMÁRIO
1 INTRODUÇÃO GERAL ... 13
2 MANUSCRITO 1. HOW DOES CLIMATE CHANGE INFLUENCE THE DISTRIBUTION OF XEROPHYTIC SPECIES? ... 17
3 INTRODUCTION ... 19
4 MATERIAL AND METHODS ... 21
4.1 Data Collection ... 21 4.2 Niche modeling ... 21 4.3 Biological models ... 22 5 RESULTS ... 23 6 DISCUSSION ... 29 7 CONCLUSIONS ... 31 8 ACKNOWLEDGMENTS ... 31 9 CONSIDERAÇÕES FINAIS ... 32 REFERÊNCIAS ... 34
ANEXO A - NORMAS DA REVISTA JOURNAL OF PLANT ECOLOGY ... 39
1 INTRODUÇÃO GERAL
Os estudos biogeográficos possibilitam entender os processos ecológicos envolvidos na distribuição das espécies nas mais diferentes escalas (GILLUNG, 2011). Com base na Biogeografia, podemos inferir sobre a distribuição potencial das espécies, a história biogeográfica, o cálculo de riqueza, o ordenamento atual dos táxons, dentre outros (TABARELLI; MANTOVANI, 1999; ABREU; PINTO; MEWS, 2014; MA et al., 2016).
As espécies possuem limites de distribuição, que muitas vezes são aleatórios ou ainda não conhecidos (HAUSDORF, 2002). Fazem interações com o meio, e sua continuidade depende de fatores abióticos (como por exemplo, água, luz, umidade, temperatura, tipo de solo, etc.) e bióticos (associações, competição, dispersão) favoráveis à sua existência. É aí que as mudanças climáticas podem atuar, pois estas alteram as condições terrestres, e consequentemente, modificam o ordenamento das espécies (KERR et al., 2015; PACIFICI et. al., 2015).
Vários estudos indicam que as mudanças climáticas podem trazer consequências desastrosas para nosso planeta, como a oscilação nos índices pluviométricos, o aumento da temperatura, a ampliação de áreas desérticas, a elevação do nível do mar, a diminuição da diversidade de diferentes grupos de plantas e animais, extinção de espécies endêmicas e o aumento de CO2 na atmosfera (HUGHES, 2000; URBAN, 2015; HUGHES et al., 2017). Ainda segundo alguns especialistas, o aumento da temperatura do planeta é um fenômeno considerado normal, porém, está sendo intensificado por atividades humanas (STEFFEN et al., 2015; MIAO; JIN; CUI, 2016).
Em eras geológicas passadas, a terra presenciou o aumento da aridez ou glaciações. O que acarretou no aumento e diminuição de tipos vegetacionais de climas úmidos e estacionalmente secos (HUGHES et al., 2013), este último predominante no nordeste do Brasil. Deste modo, surgiram algumas áreas de refúgios nas quais as plantas mantiveram sua diversidade (HAFFER, 1969; WERNECK et al., 2011; MENEZES et al., 2016; CORDEIRO, 2017). É o caso dos remanescentes de vegetação florestal serrana presentes no semiárido brasileiro (AZEVEDO, 2017), em locais onde a altitude é elevada, variando entre 400 e 1.154 m (FAJARDO; TIMOFEICZYK JUNIOR, 2015).
Estudos têm evidenciado que na região Neotropical existem várias áreas de endemismo (HAROLD; MOOI, 1994; LIMA et. al., 2018), devido às interações ecológicas e estabilidade climática (ARITA; VAZQUEZ-DOMINGUEZ, 2008; ANTONELLI; SANMARTIN, 2011). Pesquisadores de diferentes áreas da Ciência propõem a preservação desses locais para que haja a manutenção dessas espécies e dos serviços ecossistêmicos que as mesmas oferecem para diversos grupos de animais, incluindo a população humana (FONSECA; SILVA, 2010; LEAL; LOPES; MACHADO; TABARELLI, 2018).
O aumento de diversidade na região Neotropical está frequentemente associado à especiação por vicariância (ANTONELLI; SANMARTIN, 2011). A vicariância é um mecanismo evolutivo (ROSEN, 1978; LUEBERT et al., 2017), onde, por exemplo, algumas populações devido à quebra do fluxo gênico em decorrência da fragmentação de sua área de ocorrência vão apresentar diferenças morfológicas, o que poderá resultar em especiação alopátrica ao longo do tempo (SOUZA; RIBEIRO, 2017). Assim, cabe ao organismo se adaptar ao ambiente, ocupar novas áreas ou limitar sua distribuição.
A modelagem de nicho é uma ferramenta que possibilita a elaboração de modelos probabilísticos de distribuição de espécies. É comumente utilizada em estudos sobre a origem das espécies - biogeografia histórica (GELVIZ-GELVEZ et al., 2015; KOLÁŘ et al., 2016; LI; THOMAS; SAUNDERS, 2017), ou em um contexto de mudanças climáticas, já que estas alteram a paisagem e a diversidade de espécies (HAFFER, 2008). Pode ainda ser usada na inferência sobre a probabilidade de ocorrência, principalmente para espécies endêmicas (CORDEIRO et al., 2017), em extinção (MOAT et al., 2019) ou exóticas, que causam desequilíbrio no ecossistema (DESCOMBES et al., 2018). Essa ferramenta também foi usada em pesquisas com espécies xerófitas (ZHANG; ZHANG; SANDERSON, 2016; OSSA et al., 2019), a fim de compreender seu ordenamento passado.
Atualmente, existe ainda um conjunto de dados online sobre a distribuição de espécies vegetais, como por exemplo GBIF, SiBBr, speciesLink e Reflora. Essas informações dão subsídios à formulação de diversas perguntas e hipóteses ecológicas, e buscam preencher as lacunas do conhecimento científico (MILLINGTON, 2013). Com a tecnologia e os Sistemas de Informações Geográficas - SIGs, podemos obter informações mais exatas especialmente sobre a distribuição dos táxons (HIJMANS et al., 2005).
No presente estudo, nos utilizamos da modelagem de nicho com o intuito de entender como a distribuição de um grupo de plantas pode ser influenciada mediante as mudanças climáticas previstas. Para analisarmos a distribuição potencial de espécies xerófitas, tivemos como modelo biológico representantes do gênero Tacinga Britton & Rose, pertencente à família Cactaceae. Esse gênero é constituído por oito espécies, das quais sete (T. braunii Esteves, T. funalis (Britton & Rose), T. inamoena (K.Schum.) N.P.Taylor & Stuppy, T. palmadora (Britton & Rose) N.P.Taylor & Stuppy, T. saxatilis (Ritter) N.P.Taylor & Stuppy subsp., T. inamoena subsp. subcylindrica M.Machado & N.P.Taylor e T. werneri (Eggli) N.P.Taylor & Stuppy) são endêmicas do leste do Brasil (ZAPPI & TAYLOR, BFG, 2015), e uma (Tacinga lilae Trujillo & Marisela Ponce) é endêmica do Nordeste da Venezuela (MAJURE; PUENTE, 2014).
Tacinga compreende espécies arbustivas, subarbustivas e lianas, com cladódios complanados ou cilíndricos, geralmente segmentados, com abundantes gloquídios em suas aréolas, frutos globosos ou alongados com gloquídios e poucas sementes (TAYLOR & ZAPPI, 2004). Seus representantes são importantes componentes da flora do semiárido brasileiro, ocorrendo preferencialmente em vegetação de caatinga (ZAPPI & TAYLOR, 2004; BFG, 2015) e apenas uma espécie foi registrada no cerrado (T. saxatilis). Além disso, têm papel destacado na ecologia e sustentabilidade desses ecossistemas em diferentes aspectos como, por exemplo, constituem fonte de alimento e água para diversos animais; contribuem para a formação de solo sobre inselbergues, permitindo o estabelecimento de vários outros grupos de plantas (TAYLOR & ZAPPI, 2004). Merece destacar que Tacinga braunii Esteves foi enquadrada como espécie ameaçadas de extinção, categoria vulnerável (ZAPPI et al., 2013).
Para o presente trabalho, selecionamos cinco espécies que possuem no mínimo 10 pontos de ocorrência. Esse valor mínimo é necessário para obtermos modelos com resultados mais robustos. Partimos do seguinte questionamento: Como as mudanças climáticas influenciam a distribuição de espécies xerófitas? A partir dessa pergunta, buscamos compreender o ordenamento futuro dessas espécies, utilizando algorítimos de probabilidade de ocorrência, a fim de elucidar respostas sobre o porquê dessas espécies estarem ocorrendo nessas manchas dos modelos. Esta é uma pesquisa inovadora para o gênero Tacinga, por se tratar da elaboração de modelos onde o foco está na distribuição futura.
acordo com as mudanças climáticas, a fim de elucidar os fatores que poderão influenciar na redução ou aumento de áreas de distribuição de suas populações. Considerando que o habitat de espécies xerófitas incluem ambientes onde existem altas temperaturas, solos rasos e pedregosos, baixa precipitação e clima semiárido, nossa hipótese é que esses táxons maximizarão sua distribuição nos próximos anos, pois estamos vivenciando um aquecimento global diante das flutuações climáticas, já que de acordo com especialistas, a temperatura irá aumentar em cerca de 1 a 5º C em 2050, acarretando em áreas de desertificação no nordeste do Brasil.
A dissertação foi elaborada no formato de um capítulo, intitulado “How can climate change influence the distribution of xerophytic species? O manuscrito foi submetido para a revista Journal of Plant Ecology, B1 em biodiversidade, de acordo com critérios da CAPES, com fator de impacto 1.937.
2 MANUSCRITO 1. HOW CAN CLIMATE CHANGE INFLUENCE THE DISTRIBUTION OF XEROPHYTIC SPECIES?
Lucas Figueiredo Soares¹*, Marcelo Oliveira Teles de Menezes², Luciana Silva Cordeiro³ and Maria Iracema Bezerra Loiola¹
Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal do Ceará (UFC), Centro de Ciências, Departamento de Biologia, Av. Mr. Hull, s/n, Pici, Fortaleza, Ceará, Brasil.¹
Departamento de Educação, Instituto Federal de Educação, Ciência e Tecnologia do Ceará (IFCE), Av. Treze de Maio, 2081, Benfica, Fortaleza, Ceará, Brasil.²
Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri (URCA), Rua Cel. Antônio Luís, 1161, Pimenta, Crato, Ceará, Brasil.³ *Correspondence address. Programa de Pós-graduação em Ecologia e Recursos Naturais, Universidade Federal do Ceará (UFC), Centro de Ciências, Departamento de Biologia, Av. Mr. Hull, s/n, Pici, 60440-900, Fortaleza, Ceará, Brasil; Telefone: +5585 336698126; E-mail: lucasfigueiredosoares@gmail.com
ABSTRACT Aims
The distribution of plants is constantly influenced by climatic fluctuations. We had as objective to make probabilistic models and examine the future distributions of endemic xerophytic species in semiarid environments and in areas potentially subject to desertification. Methods
We used niche modeling to simulate the probable occurrences of five species of the genus Tacinga Britton & Rose (Cactaceae Juss.) using simulation data according to IPCC’s information for the year 2050 with scenarios variations in ambient conditions over a temperature range of 1 to 5°C.
Important findings
We observed that not all xeromorphic species would be favored with growth distributions due to increasing temperatures and declining annual precipitation. Indicating that not all biological models showed all members of the Cactaceae family maximizing future distributions. Our research suggests the need to conserve strategic dispersal sites, such as the Chapada Diamantina (Bahia State, northeastern Brazil) and protect species that show more restricted probabilities of why occurrence (T. saxatilis and T. werneri), as they are important sources of resources for local animal populations (food and water).
3 INTRODUCTION
The environmental conditions of the Neotropics have favored overall plant diversity (ANTONELLI et al., 2015). Brazil, for example, currently has a great diversity of species of plants and a high incidence of endemism. Of a total of 33,243 species of plants registered in the Brazilian territory, 18,643 are endemic (BFG, 2015), corresponding to approximately 56% of recorded taxa.
The current distributions of its taxa, and those of past and future times, must be considered within the context of constant climatic change (COX, 2016). Those distribution processes are essential to understanding how different biotic, abiotic, edaphic, and stochastic factors will influence the biogeographic patterns of caatinga (Brazilian Seasonally Deciduous Tropical Forests – SDTF (caatinga) vegetation (MORO et al., 2016), with 2.232 species, which 327 are endemic (BFG, 2015).
The response time for changes in vegetation following abrupt shifts in climate is currently unknown. Recently, several studies tried to explain the dry vegetation of South America on the past (HUGHEN et al., 2004; WERNECK et al., 2011; JARA-ARANCIO et al., 2014; CORDEIRO et al., 2017). They found that these plants originated during the Miocene-Eucene, and also in the Pleistocene. However, studies that seek to predict the behavior of dry vegetation in the face of future changes are still scarce for these vegetations.
Xerophytic species are highly representative of Brazilian Seasonally Deciduous Tropical Forests – SDTF (caatinga), originating after the Eocene-Oligocene (HERNÁNDEZ-HERNÁNDEZ et al., 2014). They adapted to the expansion of aridity in the Americas at the end of the Miocene – a scenario that favored the emergence of new habitats favorable to their expansion (JARA-ARANCIO et al., 2014). In that context, they used dispersal strategies in the past to expand their range (TAYLOR; ZAPPI, 2004).
Representatives of Cactaceae family have significant economic importance to human populations living in semiarid regions who exploit the ecosystem services of those species, including as food resources. The fruits of the cacti are an important source of resources for several species of animals in the Caatinga, especially the fruits of the species that bear fruit during an extended period of the year, especially in the drier months (ZAPPI et al., 2011). Additionally, cacti are pollinated by several bird species of the Brazilian semiarid
region (KIILL et al., 2012). Therefore, the cacti species has an important role in the ecological maintenance of arid and semi-arid ecosystems such as the Caatinga.
Georeferenced data has been used in different approaches to biodiversity studies. Programs using that type of information have aided ecological research, as some are able to project past and future scenarios and delete predict reductions of vegetation cover in certain areas. Those projections can be extremely important for studying the dispersal of organisms in different ecosystems (RIBEIRO-SILVA et al., 2016), and can be used to examine semiarid environments in Brazil having high levels of biodiversity (ROSSATO et al., 2017). Such information can also provide support for natural resource conservation (WHITTAKER et al., 2007).
To evaluate plant diversity and species distribution, it is advisable to use tools to observe and investigate the factors that influence them (GENTRY, 1992; HAFFER, 2008). Thus, ecological niche modeling emerges as an extremely useful tool for researchers seeking to investigate that approach, as it produces models that project accurate probabilities of species occurrences (PETERSON, 2001; BRITO et al., 2011). This method can be used in different studies, depending on the desired application, such as conservation (ELITH et al., 2011).
Approximately 15% of the semiarid region of Brazil is susceptible to desertification caused by climatic changes and/or anthropogenic factors (LI et al., 2016). Desertification can lead to reductions in populations of endemic plant species, and represents a serious concern for environmental conservation (CUNHA; GUERRA, 1996) as endemic species are highly adapted to specific geographic areas.
We evaluated here the influence of temperature increases and precipitation decreases on the distribution of species adapted to semiarid climates, focusing on species of the genus Tacinga (Cactaceae) recorded in the eastern portion of the Brazilian semiarid domain, in SDTF and savanna vegetation. The choice of representatives of Tacinga for the present study was to highlight important components of the Brazilian semiarid vegetation (Nobel and Bobich, 2002) that have prominent roles in the ecology and sustainability of those ecosystems, serve as sources of food and habitat for many animals, and contribute to the formation of soils that allow the establishment of other plants (TAYLOR; ZAPPI, 2004). The present study had as objective to examine the future distributions of five Tacinga Britton & Rose (Cactaceae) species.
4 MATERIAL AND METHODS
4.1 Data Collection
To elaborate the models predicting the probability of species occurrences in the future, georeferenced information was extracted from the Reference Center on Environmental Information CRIA site (2018) and Global Biodiversity Information Facility site (2018) (https://www.gbif.org/). The bioclimatic variables for the current climate were obtained from the Worldclim 1.4 database (2005) (http://www.worldclim.org/), while the IPCC (2014) (http://www.ipcc.ch/) variables were use to model future scenarios.
The collections at eight herbaria were consulted: ASE (Universidade Federal de Sergipe); CEN (EMBRAPA Recursos Genéticos e Biotecnologia - DF); CEPEC (Centro de Pesquisas do Cacau - BA); EAC (Universidade Federal do Ceará – CE); HUEFS (Universidade Estadual de Feira de Santana - BA); MOSS (Universidade Federal Rural do Semiárido - RN); UESC (Universidade Estadual de Santa Cruz - BA); UFP (Universidade Federal de Pernambuco - PE); and UNEB (Universidade do Estado da Bahia) – acronyms according to Thiers (2018, continuously updated). Specimens collected and identified by specialists such as Daniela C. Zappi, Marlon C. Machado, Marcelo O. T. de Menezes, and Nigel P. Taylor were mainly considered. We developed this study by combining a minimum of 10 occurrence points for each species and taxonomic identification by specialists.
4.2 Niche modeling
Simulations of future climate scenarios were run considering projected temperature ranges of from 1 to 5 degrees in 50 years, acoording to IPCC. The selection of variables was performed by PCA (Principal Components Analysis) in the R (R Development Core Team 2010) program to detect useful environmental variables related to temperature and precipitation and quarterly variations during the year (ELITH et al., 2011). The objective was to exclude correlated variables that have lower utility for determining the spatial distributions of the genus. In that way, the following bioclimatic variables (BIO) were chosen: BIO3 = Isothermality (BIO2/BIO7) (* 100), BIO9 = Mean Temperature of Driest Quarter, BIO10 = Mean Temperature of Warmest Quarter, BIO12 = Annual Precipitation, BIO13 = Precipitation of Wettest Month, BIO14 = Precipitation of Driest Month, and BIO16 = Precipitation of
Wettest Quarter.
We then generated models that simulated climatic conditions in 2050 using the most updated method indicated by ecologists to evaluate the limits of the geographic distribution of a species (SIQUEIRA, 2005). The present study used MaxEnt 3.3.3, the most widely used algorithm, which generates what are considered the most robust and accurate models (PETERSON et al., 2007), as the algorithm can fill in information gaps concerning the species and decrease the inclusion of false occurrence areas in the final model.
A minimum of 10 occurrence points were selected for each species, distributed evenly throughout the area, as recorded in the Flora do Brasil 2020 site. That minimum value of 10 was suggested by Phillips; Dudík (2008) to provide greater accuracy in the delimitation of the areas of most likely occurrence.
Niche modeling is designed to predict how climate changes will affect future species occurrence areas within the accuracy of the mathematical probability algorithm used by the program (ELITH et al., 2011). The models obtained display data referring to the geographic locations of species of the genus Tacinga, with darker tones indicating the highest probability of occurrence for the climatic scenario modeled. Soil data were extracted from the database of the Brazilian Institute of Geography and Statistics (IBGE, 2016).
4.3 Biological models
The genus Tacinga is represented in Brazil by nine taxa, including seven species and two subspecies. Five representatives of the genus were selected for this study, with the requirement that each taxon had at least ten occurrence records. We disregard the others. The species studied were:
Tacinga funalis Britton & Rose – Endemic to northeastern Brazil (Fig. 1a), occurring in the
states of Piauí, Pernambuco, and Bahia in caatinga and “carrasco” vegetation (ZAPPI; TAYLOR, 2018), usually associated with gneiss and granite rocks (TAYLOR; ZAPPI, 2004).
Tacinga inamoena ( K.Schum.) N.P.Taylor & Stuppy – Endemic to eastern Brazil (Hunt
2006, Fig. 1b). Occurring in all of the states in the northeastern region, and in northern Minas Gerais State (southeastern region) in caatinga, “carrasco” and rupestrian field vegetation (ZAPPI; TAYLOR, 2018). Often found on rock outcrops, although it occurs on a wide variety of substrates and at altitudes ranging from sea level to 1550 m (TAYLOR; ZAPPI, 2004; MENEZES et al., 2011).
Tacinga palmadora (Britton & Rose) N.P.Taylor & Stuppy – Endemic to northeastern
Brazil (Fig. 1c), being recorded in the states of Piauí, Ceará, Rio Grande do Norte, Paraíba, Pernambuco, Alagoas, Sergipe, and Bahia in caatinga and “carrasco” vegetation (Zappi; Taylor, 2018), at altitudes between 200 and 1020 m (Taylor; Zappi, 2004).
Tacinga saxatilis (Ritter) N.P.Taylor & Stuppy subsp. saxatilise – Endemic to Brazil,
with confirmed occurrences only in the states of Bahia (northeastern Brazil) and northern Minas Gerais (southeastern region) in caatinga vegetation and in deciduous and semideciduous seasonal forests, often on rock outcrops (Zappi; Taylor, 2018).
Tacinga werneri (Eggli) N.P.Taylor & Stuppy –Endemic to Brazil (Fig. 1d), with
distribution restricted to the states of Bahia (northeastern Brazil) and northern Minas Gerais (southeastern region), in drier environments such as caatinga (ss) and deciduous and semideciduous seasonal forests, often on rock outcrops (Zappi; Taylor, 2018).
5 RESULTS
We found that some species of the genus will have broad distributions in environments currently with less pronounced aridity.
Tacinga funalis is currently restricted to areas of Caatinga (STDF), mainly in the Chapada Diamantina region, in Bahia State (Fig. 2a). In the simulation for 2050 (Fig. 3a), its area of occurrence increased in the extreme northeastern region of Brazil, near the São Francisco River and Borborema Plateau, and near the coast (mainly in the states of Alagoas, Bahia, Pernambuco, and Sergipe). The distribution of the species was influenced mainly by BIOS referring to precipitation levels, such as Annual Precipitation and Isothermality.
Tacinga inamoena currently has wide distribution in Brazilian STDF, mainly in Caatinga vegetation (Fig. 2b). In the simulation for 2050, it was projected to be present over a large geographic area in the tropical region of eastern Brazil, mainly in the states of Alagoas, Bahia, Ceará, Paraíba, Rio Grande do Norte, and Sergipe (Fig. 3b). Some representatives would also be found in subtropical or humid areas, such as the Amazon (the states of Pará and Roraima), in cerrado savanna vegetation (Mato Grosso do Sul, Goiás, São Paulo, and Minas Gerais), and in Pampas (Rio Grande do Sul State). Most relevant to those analyses were Mean Temperature of Driest Quarter, Annual Precipitation, Precipitation of Wettest Month, and Precipitation of Wettest Quarter.
Figura 1 – Detail of the habit of the Tacinga (Cactaceae) species studied. (a) T. funalis, (b) T. inamoena, (c) T. palmadora e (d) T. Werneri.
Figura 2 – Current distribution of Tacinga (Cactaceae) in Brasil. (a). T.
funalis, (b). T. inamoena, (c) T. palmadora, (d) T. saxatilis and (e) T. werneri.
Figura 3 – Potential distribution of the species Tacinga (Cactaceae) in Brazil. (a) T. funalis, (b) T. inamoena, (c) T. palmadora, (d) T. saxatilis, and (e) T. werneri for 2050, with the increase of the temperature by 1.5 degrees, using bioclimatic variables
(Isothermality, Mean Temperature of Driest Quarter, Mean Temperature of Warmest Quarter, Annual Precipitation, Precipitation of Wettest Month, Precipitation of Driest Month and Precipitation of Wettest Quarter).
Fonte: Próprio autor.
Tacinga palmadora currently occurs widely in areas of southeastern STDF, in northeastern Brazil (Fig. 2c). In 2050, its distribution was predicted to extend, to a lesser
degree, to the savanna near Venezuela (Roraima State) and to the westernmost cerrado areas (the states of Mato Grosso, São Paulo, Minas Gerais, and Mato Grosso do Sul) throughout the central-western, southern, and southeastern regions of Brazil (Fig. 3c). Most relevant to the analyses were the BIOS Precipitation of Wettest Quarter, Annual Precipitation, and
Isothermality.
Tacinga saxatilis representatives currently grow exclusively in Chapada Diamantina and nearby regions, in the states of Bahia, Pernambuco, and Paraíba (Fig. 2d). In our simulations for the future, this species became widely distributed throughout the tropical region of Brazil, in current savanna and Caatinga vegetation in the states of Goiás, Ceará, and Bahia, among others (Fig. 3d), being influenced largely by the BIO Annual Precipitation.
Tacinga werneri is currently found along the São Francisco River and in the Chapada Diamantina, Bahia State (Fig. 2e), and will occupy those same areas in 2050, although with still wider distribution, reaching mainly the states of Rio Grande do Norte, Ceará, Pernambuco, and Paraíba (Fig. 3e), being influenced largely by Annual Precipitation and Mean Temperature of Warmest Quarter.
Another relevant factor found in our research was the influence of different soil types on future projections. Tacinga species are currently found growing predominantly in Luvisol soils, while our results suggest that, in the future, some of those plants will occupy habitats with, Ferralsol, planosol and cambisol (Table 1).
Tabela 1 – Projected phytogeographic domains and soil types of Tacinga species (Cactaceae).
Species Phytogeographical domain Type of soil Tacinga funalis Savanna STDF Non-calcic brown soils,
latosol Tacinga
inamoena
Savanna STDF, Rainforest, Seasonal Forest
Non-calcic brown soils, latosol, planosol, cambisol Tacinga palmadora Savanna STDF, Rainforest, Seasonal Forest
Non-calcic brown soils, latosol, planosol,
cambisol Tacinga
saxatilis
Savanna STDF, Rainforest Non-calcic brown soils, latosol, planosol,
cambisol Tacinga
werneri
Savanna STDF Non-calcic brown soils, latosol
Fonte: BFG (2015), WRB (1998) and IBGE (2016) databases.
6 DISCUSSION
Species of the genus Tacinga occur in semiarid regions, in environments with high temperatures, shallow soils, and low precipitation levels (ZAPPI; TAYLOR, 2018). Its distribution is exclusive to the phytogeographic domains of savanna STDF (caatinga and cerrado). Its species are found in eastern Brazil under similar edaphoclimatic and vegetation conditions. Our simulations sought to determine where their representatives will be distributed in the future in light of environmental changes.
Tacinga species are currently widely distributed in the semiarid region of Brazil (REALINI et al., 2015), and their future distributions will aid us in understanding if they will still occupy those sites in environments prone to desertification, such as Rio Jaguaribe region. The aforementioned biological model of Tacinga is especially relevant to studies of semiarid areas in the Neotropics susceptible to desertification because its species (as well as cacti in general) are easily observed in the field (ARZABE et al., 2018).
Climate change can reduce the chances of regeneration of populations, influencing the distribution of plants. It is icreased by anthropogenic factors, as reported by Carrillo-Angeles et al. (2016) for the genus Astrophytum (Cactaceae). They verified the distribution of
the genus by 2020 and 2050, mainly using bioclimatic precipitation variables, which had greater biological weight, a result similar to the present study.
It was possible to observe that the species T. funalis conserved its location in the future in its current range due to their high climatic stability. This result suggests that the specie should have priority for conservation efforts because, as suggested by Saraiva et al. (2015), it is endemic to the semiarid region and helps protect the soil and avoid erosion.
Our results were similar to those of Ferreira et al. (2016), and indicated that Tacinga species would show the greatest distribution expansions in areas with high temperatures and rainfall rates below 1000 mm.y-1, although the results presented here (under the simulated climatic conditions used) indicated those species would be limited to semiarid areas.
Tacinga inamoena and T. saxatilis showed the suitable range enlargement in relation to the other taxa, and we attribute that increased occurrence to anthropogenic impacts on tropical and subtropical environments. Tacinga palmadora showed distribution displacements that apparently take advantage of natural biological refuges in mountainous areas of the Chapada Diamantina and near the São Francisco River. According to Franco and Manfrin (2013), those areas will function as dispersal centers for that species.
The probabilities of occurrence of those three species (Tacinga inamoena, T. saxatilis, and T. palmadora) were also expanded to regions north of the Amazonian domain, suggesting that even in areas currently having high annual precipitation levels there will be locations suitable for Cactaceae, a situation that does not exist today. That situation should have direct influences on the dynamics of their respective communities, as the projected environment will favor geographic expansion of xerophytic species.
We observed future species distributions in the area near Venezuela within the diagonal of dry vegetation that Prado; Gibbs (1993), Pennington et al. (2000), and Neves et al. (2015) discuss as supporting SDTFs during the Pleistocene. The species Tacinga inamoena, T. saxatilis, and T. palmadora were projected to grow in that territorial band, and we interpret those occurrences to exist due to remnants of plants found in the past, during that geological period.
It is important to highlight that this research focused on the desertification and climatic oscillations we are currently experiencing, but future biological changes are still unknown (such as the restricted distribution of species resistant to high temperatures, facilitation and competition) a problem likewise put forward by Bestelmeyer et al. (2015),
Vieira et al. (2015) and Wang et al. (2017). It was evident here that even Amazonian environments (for example), with their current high precipitation rates and dense arboreal vegetation, will be the habitat of cacti species in the future due to savannization resulting from the anthropogenic forest degradation of recent years, as described by Coe et al. (2017) and Monteiro et al. (2017).
7 CONCLUSIONS
We conclude that xerophytic species will be expanded mainly in their dispersal centers, and will be greatly benefited by global warming in relation to their arrangement, although not all of them extend their arrangement. We emphasize the importance of the permanent protected area of Chapada Diamantina for the preservation of xerophytic species that are currently widely distributed throughout the region, especially species at risk of extinction. We also emphasize the need for more extensive surveys of cacti to be able to generate models with greater accuracy.
8 ACKNOWLEDGMENTS
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. Maria Iracema Bezerra Loiola thanks CNPq for the productivity grant (Process n° 304099 / 2017-1), and Luciana Silva Cordeiro acknowledges the PNPD / CAPES grant (Process n° 1810203).
Conflict of interest statement. The authors declare that they have no conflict of interests.
9 CONSIDERAÇÕES FINAIS
Atualmente, todas as espécies do gênero Tacinga (Cactaceae) estão presentes na região semiárida do leste do Brasil, nos domínios fitogeográficos caatinga e cerrado. De acordo com as informações extraídas das bases de dados consultados têm-se registros desses táxons nos estados de Alagoas, Bahia, Ceará, Minas Gerais, Paraíba, Pernambuco, Piauí, Rio Grande do Norte e Sergipe. No entanto, com base nos resultados encontrados com a modelagem de nicho no presente estudo, em um futuro próximo, haverá uma maior concentração de espécies na Bahia. O local é também conhecido como “refúgio da Bahia” por ter sido uma área de estabilidade durante o período Pleistoceno e Holoceno.
Verificamos ainda que a maioria das espécies estudadas (T. inamoena, T. palmadora e T. saxatilis) serão beneficiadas com o aumento da temperatura e com a redução da precipitação, previstos para 2050, pois terão sua distribuição expandida para novas áreas, além da manutenção das áreas atualmente ocupadas. Apesar disso, algumas dessas plantas irão manter sua distribuição apenas próxima à Chapada Diamantina (T. funalis e T. werneri). O resultado similar também foi destacado em trabalhos anteriores com outras espécies xerófitas, o que vai de acordo com a hipótese que existem áreas de endemismo na região Neotropical, como o planalto da Borborema e nos depósitos residuais do rio São Francisco, que proporcionam a manutenção de algumas espécies.
Precisamos nos atentar para a preservação desse centro de endemismo, pois os mesmos possuem uma grande biodiversidade, necessária para que haja conservação ambiental. Além disso, os serviços ecossistêmicos são garantidos se essas plantas forem preservadas, principalmente as endêmicas de distribuição restrita. Assim, sugerimos que a manutenção da área de proteção permanente desse território é essencial, se quisermos atingir os objetivos previamente citados, que visam a sustententabilidade.
O presente trabalho fomenta outras perguntas ecológicas, como por exemplo, o estudo da história biogeográfica de representantes de Tacinga, a fim de promover um maior entendimento sobre essas plantas. Entender a origem desses táxons pode elucidar questões sobre como as espécies xerófitas se comportaram durante eras geológicas anteriores a essa. Existem lacunas do conhecimento científico as quais trabalhos com essa temática podem preencher, como por exemplo o ordenamento passado, atual ou futuro das espécies de plantas em diferentes partes do mundo.
REFERÊNCIAS
ABREU, T.A.; PINTO, J.R.R.; MEWS, H.A. Variações na riqueza e na diversidade de espécies arbustivas e arbóreas no período de 14 anos em uma Floresta de Vale, Mato Grosso, Brasil. Rodriguésia, v. 65, p. 73–88, 2014.
ANTONELLI, A.; SANMARTÍN, I. 2011. Why are there so many plant species in the Neotropics? Taxon, v. 60, p. 403–414, 2011.
ANTONELLI, A.; ZIZKA, A.; SILVESTRO, D.; SCHARN, R.; CASCALES-MIÑANA, B.; BACON, C.D. An engine for global plant diversity: highest evolutionary turnover and emigration in the American tropics. Frontiers in Genetics, v. 6, p. 1–14, 2015.
ARZABE, A. A.; AGUIRRE, L.F.; BALDELOMAR, M.P.; MOLINA-MONTENEGRO, M.A. Assessing the geographic dichotomy hypothesis with cacti in South America. Plant Biology, v. 20, n. 2, p. 399–402, 2018.
AZEVEDO, J.P.S. Ecofisiologia de Erythroxylum pauferrense em uma floresta de brejo de altitude, nordeste do brasil. Universidade Federal da Paraíba. Trabalho de Conclusão de Curso, 2017.
BESTELMEYER, B.T., OKIN, G.S.; DUNIWAY, M.C.; ARCHER, S.R.; SAYRE, N.F.; WILLIAMSON, J.C.; HERRICK, J.E. Desertification, land use, and the transformation of global drylands. Frontiers in Ecology and the Environment, v. 13, n. 1, p. 28–36, 2015.
BFG - THE BRAZIL FLORA GROUP. Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia, v. 66, p. 1085–1113, 2015.
BRASIL. Ministério da Educação. Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior. Portaria nº 206, de 4 de setembro de 2018. Diário Oficial da União, Brasília, nº 172, 5 set. 2018. Seção 1, p. 22. Disponível
em:
http://www.imprensanacional.gov.br/materia/- /asset_publisher/Kujrw0TZC2Mb/content/id/39729251/do1-2018-09-05-portaria-n-206-de-4-de-setembro-de-2018-39729135. Acesso em: 19 mar. 2018.
BRITO, J.C.; Fahd, S.; Geniez, P.; Martínez-Freiría, F.; Trape, J.F. Biogeography and conservation of viperids from North-West Africa: an application of ecological niche-based models and GIS. Journal of Arid Environments, v. 75, n. 11, p. 1029–1037, 2011.
CARRILLO-ANGELES, I.G.; SUZÁN-AZPIRI, H.; MANDUJANO, M.C.; GOLUBOV, J.; MARTÍNEZ-ÁVALOS, J.G. Niche breadth and the implications of climate change in the conservation of the genus Astrophytum (Cactaceae). Journal of Arid Environments, v. 124, p. 310–317, 2016.
CNCFLORA. Tacinga inamoena. In: Lista Vermelha da flora brasileira versão 2012. Centro Nacional de Conservação da Flora. Disponível em: http://cncflora.jbrj.gov.br/portal/pt-br/profile/Tacinga inamoena. Acesso em: 10 fev. 2019.
COE, M.T.; BRANDO, PM; DEEGAN, L.A.; MACEDO, M.N.; NEILL, C.; SILVERIO, D.V. The forests of the Amazon and Cerrado moderate regional climate and are the key to the future. Tropical Conservation Science, v. 10, p. 1–6, 2017.
CORDEIRO, L.S.; ARAÚJO, F.S.; KOCH, I.; SIMÕES, A.O.; MARTINS, F.R.; LOIOLA, M.I.B. Paleodistribution of Neotropical species of Erythroxylum (Erythroxylaceae) in humid and dry environments. Acta Botanica Brasilica, v. 31, p. 645–656, 2017.
COX, C.B.; MOORE, P.D.; LADLE, R. Biogeography: an ecological and evolutionary approach. John Wiley & Sons, 2016.
CUNHA, S.B.; GUERRA, A.J.T. Degradação ambiental. Geomorfologia e meio ambiente, v. 4, p. 337–379, 1996.
DESCOMBES, P.; PETITPIERRE, B.; MORARD, E.; BERTHOUD, M.; GUISAN, A.; VITTOZ, P. 2016. Monitoring and distribution modelling of invasive species along riverine habitats at very high resolution. Biological invasions, v. 18, p. 3665–3679, 2016.
ELITH, J.; HASTIE, T.; DUDÍK, M.; YUNG, E.C.; YATES, J.C. A statistical explanation of MaxEnt for ecologists. Diversity and distributions, v. 17, n. 1, p. 43-57, 2011.
FAJARDO, A.M.P.; TIMOFEICZYK JUNIOR, R. 2015. Financial Feasibility of Carbon Sequestration in Serra de Baturité, Ceara state, Brazil in 2012. Floresta e Ambiente, v. 22, p. 391–399.
FERREIRA, P.S.M; LOPES, S.F.; TROVÃO, D.M.B.M. Patterns of species richness and abundance among cactus communities receiving different rainfall levels in the semiarid region of Brazil. Acta Botanica Brasilica, v. 30, n. 4, p. 569-576, 2016.
FONSECA, V.L.I.; SILVA, P.N. 2010. As abelhas, os serviços ecossistêmicos e o Código Florestal Brasileiro. Biota Neotropica, v. 10, p. 60–62.
FRANCO, F.F.; MANFRIN, M.H. Recent demographic history of cactophilic Drosophila species can be related to Quaternary palaeoclimatic changes in South America. Journal of Biogeography, v. 40, n. 1, p. 142-154, 2013.
GELVIZ-GELVEZ, S.M.; PAVÓN, N.P.; ILLOLDI-RANGEL, P.; BALLESTEROS-BARRERA, C. Ecological niche modeling under climate change to select shrubs for
ecological restoration in Central Mexico. Ecological Engineering, v. 74, p. 302–309, 2015.
GENTRY, A.H. Tropical forest biodiversity: distributional patterns and their conservational significance. Oikos, v. 63, p. 19–28, 1992.
GILLUNG, J.P. Biogeografia: a história da vida na Terra. Revista da Biologia, v. 7, p. 1–5, 2018.
HAFFER, J. Hypotheses to explain the origin of species in Amazonia. Brazilian Journal of Biology, v. 68, p. 917–947, 2008.
HAROLD, A.S; MOOI, R.D. Area of endemism: definition and recognition criteria. Systematic Biology, v. 43, p. 261–266, 1994.
HAUSDORF, B. Units in biogeography. Systematic Biology, v. 51, p. 648-652, 2002.
HERNÁNDEZ-HERNÁNDEZ, T.; BROWN, J.W.; SCHLUMPBERGER, B.O.; EGUIARTE, L.E.; MAGALLÓN, S. Beyond aridification: multiple explanations for the elevated
diversification of cacti in the New World Succulent Biome. New Phytologist, v. 202, p. 1382–1397, 2014.
HIJMANS, R.J.; CAMERON, S.; PARRA, J.; JONES, P.; JARVIS, A.; RICHARDSON, K. WorldClim, version 1.3. University of California, Berkeley, USA, 2005.
HIJMANS, R.J.; CAMERON, S.E.; PARRA, J.L.; JONES P.G.; JARVIS, A. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, v. 25, p. 1965–1978, 2005.
HUGHEN, K.A.; EGLINTON, T.I.; XU, L.; MAKOU, M. Abrupt tropical vegetation response to rapid climate changes. Science, v. 304, p. 1955-1959, 2004.
HUGHES, L. Biological consequences of global warming: is the signal already apparent? Trends in Ecology & Evolution, v. 15, p. 56–61, 2000.
HUGHES, C.E.; PENNINGTON, R.T.; ANTONELLI, A. Neotropical plant evolution: assembling the big picture. Botanical Journal Linnean Society, v. 171, p. 1–18, 2013. HUGHES, T.P.; KERRY, J.T.; ÁLVAREZ-NORIEGA, M.; ÁLVAREZ-ROMERO, J.G.; ANDERSON, K.D.; BAIRD, A.H.; BRIDGE, T.C. Global warming and recurrent mass bleaching of corals. Nature, v. 543, p. 373–377, 2017.
IBGE. Base de dados de informação sobre solos. Disponível em: https://www.ibge.gov.br/ Acesso em: 06 mar. 2019.
IPCC Climate Change. Mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, 2014. JARA-ARANCIO, P.; ARROYO, M.T.; GUERRERO, P.C.; HINOJOSA, L.F.; ARANCIO, G.; MÉNDEZ, M.A. Phylogenetic perspectives on biome shifts in Leucocoryne (Alliaceae) in relation to climatic niche evolution in western South America. Journal of biogeography, v. 41, p. 328–38, 2014.
KERR, J.T.; PINDAR, A.; GALPERN, P.; PACKER, L.; POTTS, S.G.; ROBERTS, S.M.; WAGNER, D.L.. Climate change impacts on bumblebees converge across continents. Science, v. 349, p. 177–180, 2015.
KIILL, L.H.P.; SANTOS, A.P.B.; MARTINS, C.T.V.D.; SILVA, N.B.G.; SILVA, T.A. Pollination ecology of the cactus Arrojadoa rhodantha in a seasonal hiper-xerophilous tropical forest. Sitientibus, v. 12, p. 303–312, 2012.
KOLÁŘ, F.; FUXOVÁ, G.; ZÁVESKÁ, E.; NAGANO, A. J.; HYKLOVÁ, L.; LUČANOVÁ, M.; MARHOLD, K. Northern glacial refugia and altitudinal niche divergence shape
genome‐wide differentiation in the emerging plant model Arabidopsis arenosa. Molecular Ecology, v. 25, p. 3929–3949, 2016.
LEAL, I.R.; LOPES, A.V.; MACHADO, I.C.; TABARELLI, M. Interações planta-animal na Caatinga: visão geral e perspectivas futuras. Ciência e Cultura, v. 70, p. 35–40, 2018.
LI, Q.; ZHANG, C.; SHEN, Y.; JIA, W.; LI, J. Quantitative assessment of the relative roles of climate change and human activities in desertification processes on the Qinghai-Tibet Plateau based on net primary productivity. Catena, v. 147, p. 789–796, 2016.
LI, P.S.; THOMAS, D. C.; SAUNDERS, R. M.K. Historical biogeography and ecological niche modelling of the Asimina-Disepalum clade (Annonaceae): role of ecological
differentiation in Neotropical-Asian disjunctions and diversification in Asia. BMC Evolutionary Biology, v. 17, p. 1–18, 2017.
LUEBERT, F.; COUVREUR, T. L.; GOTTSCHLING, M.; HILGER, H. H.; MILLER, J. S.; WEIGEND, M. Historical biogeography of Boraginales: West Gondwanan vicariance followed by long‐distance dispersal? Journal of Biogeography, v. 44, p. 158–169, 2017. MA, K.Y.; CRAIG, M.T.; CHOAT, J.H.; VAN HERWERDEN, L. The historical biogeography of groupers: Clade diversification patterns and processes. Molecular Phylogenetics and Evolution, v. 100, p. 21–30, 2016.
MACHADO, M.C.; MENEZES, M.O.T.; SANTOS, M.R.; PRIETO, P.V.; HERING, R.L.O.; BARROS, F.S.M.; BORGES, R.A.X. Cactaceae. Plantas Raras do Brasil. Conservação Internacional, Belo Horizonte, p. 118-126, 2009.
MAJURE L.C.; PUENTE, R. Phylogenetic relationships and morphological evolution in Opuntia s.str. and closely related members of tribe Opuntieae. Succulent Plant Research, v. 8, p. 9–30, 2014.
MENEZES, M.O.T.; ZAPPI, D.C.; MORAES, E.M.; FRANCO, F.F.; TAYLOR, N.P.; COSTA, I.R.; LOIOLA, M.I.B. Pleistocene radiation of coastal species of Pilosocereus (Cactaceae) in eastern Brazil. Journal of Arid Environments, v. 135, p. 22–32, 2016.
MIAO, Y.; JIN, H.; CUI, J. Human activity accelerating the rapid desertification of the Mu Us Sandy Lands, North China. Nature Scientific Reports, v. 6, p. 1–6, 2016.
MILLINGTON, A.C.; WALSH, S.J.; OSBORNE, P. E. GIS and remote sensing
MOAT, J.; GOLE, T.W.; DAVIS, A.P. Least Concern to Endangered: Applying climate change projections profoundly influences the extinction risk assessment for wild Arabica
coffee. Global change biology, v. 25, p. 390–403, 2019.
MONTEIRO, Marko. Science and Policies of Deforestation in the Amazon: Reflecting Ethnographically on Multidisciplinary Collaboration. In: Intercultural Communication and Science and Technology Studies. Palgrave Macmillan, Cham, p. 79–103, 2017.
MORO, M.F.; LUGHADHA, E.M.; ARAÚJO, F.S.; MARTINS, F.R. A phytogeographical metaanalysis of the semiarid Caatinga domain in Brazil. The Botanical Review, v. 82, p. 91– 148, 2016.
NEVES, D.M.; DEXTER, K.G.; PENNINGTON, R.T.; BUENO M.L.; OLIVEIRA FILHO, A.T. Environmental and historical controls of floristic composition across the South American Dry Diagonal. Journal of Biogeography, v. 42, p. 1566–1576, 2015.
NOBEL, P.S.; BOBICHE, E.G. Environmental Biology. Los Angeles, CA: University of California Press, 2002.
OSSA, C.G.; MONTENEGRO, P.; LARRIDON, I.; PÉREZ, F. Response of xerophytic plants to glacial cycles in southern South America. Annals of Botany, v. 10, p. 1–11, 2019.
PACIFICI, M.; FODEN, W.B.; VISCONTI, P.; WATSON, J.E.; BUTCHART, S.H.; KOVACS, K.M.; CORLETT, R. T. Assessing species vulnerability to climate change. Nature Climate Change, v. 5, p. 215–224, 2015.
PEIXOTO, M.R.; ZAPPI D.C.; SILVA, S.R.; COSTA, G.M.; AONA, L.Y. Cactus survey at the Floresta Nacional of Contendas do Sincorá, Bahia, Brazil. Bradleya, v. 34, p. 38–54, 2016.
PENNINGTON, R.T.; PRADO, D.E.; PENDRY, C.A. Neotropical seasonally dry forests and Quaternary vegetation changes. Journal of Biogeography, v. 27, p. 261–73, 2000.
PETERSON, A.T.; PAPEŞ, M.; EATON, M. Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography, v. 30, p. 550– 560, 2007.
PHILLIPS, S.J.; DUDÍK, M. Modeling of species distributions with Maxent: new extensions and acomprehensive evaluation. Ecography, v. 31, p. 161–175, 2008.
PRADO, D.E.; GIBBS, P.E. Patterns of species distributions in the dry seasonal forests of South America. Annals Missouri Botanical Garden, v. 80, p. 902–27, 1993.
PETERSON, A.T. Predicting SPECIES'Geographic Distributions Based on Ecological Niche Modeling. The Condor, v. 103, p. 599–605, 2001.
R CORE TEAM. Data from R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Disponível em: https://www.r-project.org/ Acesso em:
09 fev. 2019.
REALINI, M.F.; GONZÁLEZ, G.E.; FONT, F.; PICCA, P.I.; POGGIO, L.; GOTTLIEB, A.M. Phylogenetic relationships in Opuntia (Cactaceae, Opuntioideae) from southern South
America. Plant Systems Evolution, v. 301, p. 1123–1134, 2015.
RIBEIRO-SILVA, S.; MEDEIROS, M.B.; LIMA, V.V.F.; PEIXOTO, M.R.; AONA, L.Y.S. Patterns of Cactaceae species distribution in a protected area in the semiarid Caatinga biome of north-eastern Brazil. Edinburgh Journal of Botany, v. 73, p. 157–170, 2016.
ROSEN, D.E. Vicariant patterns and historical explanation in biogeography. Systematic Zoology, v. 27, p. 159–188, 1978.
ROSSATO, L.; ALVALÁ, R.C.; MARENGO, J.A.; ZERI, M.; CUNHA, A.P.; PIRES, L.; BARBOSA, H.A. Impact of soil moisture on crop yields over Brazilian semiarid. Frontiers in Environmental Sciences, v. 5, p. 1–16, 2017.
SARAIVA, D.D.; SOUSA, K.S.; OVERBECK, G.E. Multiscale partitioning of cactus species diversity in the South Brazilian grasslands: Implications for conservation. Journal for nature conservation, v. 24, p. 117–122, 2015.
SIQUEIRA M.F.D. Uso de modelagem de nicho fundamental na avaliação do padrão de distribuição geográfica de espécies vegetais. Tese (Doutorado em Ciências da Engenharia Ambiental). Universidade de São Paulo, Brasil, 2005.
SOUZA, T.S.; RIBEIRO, M.S.L. De volta ao passado: revisitando a história biogeográfica das florestas neotropicais úmidas. Oecologia Australis, v. 21, p. 93–107, 2017.
STEFFEN, W.; BROADGATE, W.; DEUTSCH, L.; GAFFNEY, O.; LUDWIG, C. The trajectory of the Anthropocene: the great acceleration. The Anthropocene Review, v. 2, p. 81–98, 2015.
TABARELLI, M.; MANTOVANI, W. A regeneração de uma floresta tropical montana após corte e queima (São Paulo-Brasil). Revista Brasileira de Biologia, v. 59, p. 239–250, 1999.
TAYLOR, N.P.; ZAPPI, D.C. Cacti of Eastern Brazil. Kew: Royal Botanic Gardens, 2004.
THIERS B (continuously updated) Index herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium.
URBAN, M. C. Accelerating extinction risk from climate change. Science, v. 348, n. 6234, p. 571–573, 2015.
VIEIRA, R.D.S.P.; TOMASELLA, J.; ALVALÁ, R.C.S.; SESTINI, M.F.; AFFONSO, A.G.; RODRIGUEZ, D.A.; OLIVEIRA, S.B.P. Identifying areas susceptible to desertification in the Brazilian northeast. Solid Earth, v. 6, p. 347–360, 2015.
WANG, X.; HUA, T.; LANG, L.; MA, W. Spatial differences of aeolian desertification responses to climate in arid Asia. Global and Planetary Change, v. 148 p. 22–28, 2017.
WERNECK, M.D.S.; SOBRAL, M.E.G.; ROCHA, C.T.V.; LANDAU, E.C.; STEHMANN, J. R. Distribution and endemism of angiosperms in the Atlantic Forest. Natureza &
Conservação, v. 9 p. 188–193, 2011.
WHITTAKER, R.J.; FERNÁNDEZ-PALACIOS, J.M. Island biogeography: ecology, evolution, and conservation. Oxford, UK. Oxford University Press, 2007.
ZAPPI, D.C.; RIBEIRO-SILVA, S.; AONA, L.; TAYLOR N. Aspectos ecológicos e Biologia reprodutiva. In: Ribeiro-Silva S et al. (ed). Plano de Ação Nacional para a Conservação das Cactáceas - Série Espécies Ameaçadas. Instituto Chico Mendes de Conservação da Biodiversidade. Brasília, Brasil, 2011.
ZAPPI, D.C.; TAYLOR N. 2018. Cactaceae in Flora do Brasil 2020 em construção. Rio de Janeiro, Brasil. Jardim Botânico do Rio de Janeiro. Disponível em:
http://floradobrasil.jbrj.gov.br/reflora/floradobrasil/ FB1758. Acesso em: 06 mar. 2019.
ZHANG, H.X.; ZHANG, M.L.; SANDERSON, S.C. Spatial genetic structure of forest and xerophytic plant species in arid Eastern Central Asia: insights from comparative
phylogeography and ecological niche modelling. Biological Journal of the Linnean Society, v. 120, p. 612–625, 2016.
ANEXO A - NORMAS DA REVISTA JOURNAL OF PLANT ECOLOGY General information
Journal of Plant Ecology (JPE) is a peer-reviewed international journal of plant ecology, which serves as an important medium for Chinese and international ecologists to present research findings and discuss challenging issues in the broad field of plant ecology. Research and review articles published in JPE will be of interest to all types of plant ecologists. JPE includes special issues/features focusing on the frontiers in plant ecology with invited reviews written by the leading ecologists in the field.
Thank you for your interest in Journal of Plant Ecology. Please read the complete Author Guidelines carefully prior to submission, including the section on copyright. To ensure fast peer review and publication, manuscripts that do not adhere to the following instructions will be returned to the corresponding author for technical revision before undergoing peer review.
Manuscript preparation
Original manuscripts must be provided as Microsoft Word. References, Figure Legends and Tables should be included in the Word file. The main text should be typewritten using size 12 Times New Roman on one side only of A4 size, aligned left and double-spaced with margins of at least 3 cm. All pages should be numbered sequentially. Each line of the text should also be numbered consecutively. Manuscripts should be written in clear, concise and scientific language, nomenclature and standard international units should be used. Authors are advised to follow the JPE style carefully (see the sample copy for format). Manuscripts that do not meet these standards will be returned to authors without reviewing.
Please organize your manuscripts in the following order:
Title page, Abstract, Introduction, Materials and methods, Results, Discussion, Funding, Acknowledgments, References, Tables, Figures and figure legends, Supplementary data, Title page
The title page should contain:
(a) the title (not exceeding 100 characters)
(c) the name(s) and address(es) of the institution(s) where the work was carried out, followed by the contact details of the author to whom correspondence should be sent (address, telephone, fax, and e-mail).
Any acknowledgements or any footnotes referring to the title, including sources of financial support, should be inserted into the Acknowledgements section, which precedes the References. Authors should also supply a running title which will appear at the top of the page, this should not exceed 50 characters, including spaces.
Abstract
Each paper must begin with a structured abstract of no more than 450 words, including three parts: Aims, Methods and Important Findings (reviews and forums should omit Methods). Aimsshould briefly state the context and primary objectives of the study. Methods should concisely state the location (for field studies) and major techniques and procedures used in the study. Important Findings should take up no more than half of the abstract and summarize only the most important results and their significance. Three to five Key Words should be supplied after the abstract for indexing purposes.
Text
The body of the text should be subdivided into the following main headings:
(a) Introduction should be concise and define the scope of the work in relation to other work
done in the same field.
(b) Materials and methods should be brief but informative enough for reproduction of the work; when methods published in standard journals are followed without any modification, a
reference to the work should be listed.
(c) Results and Discussion should be presented with clarity and precision.
Funding
This section should list funding sources. The following rules should be followed:
(a) The sentence should begin: ‘This work was supported by …’ (b) The full official funding agency name should be given, i.e. ‘the National Cancer Institute
at the National Institutes of Health’ or simply 'National Institutes of Health' not ‘NCI' (one of the 27 subinstitutions) or 'NCI at NIH’ – see the full RIN-approved list of UK funding
agencies for details
(c) Grant numbers should be complete and accurate and provided in brackets as follows:
‘[grant number ABX CDXXXXXX]’
(d) Multiple grant numbers should be separated by a comma as follows: ‘[grant numbers ABX
CDXXXXXX, EFX GHXXXXXX]’
(e) Agencies should be separated by a semi-colon (plus ‘and’ before the last funding agency) (f) Where individuals need to be specified for certain sources of funding the following text should be added after the relevant agency or grant number 'to [author initials]'.
An example is given here: This work was supported by the National Institutes of Health [P50 CA098252 and CA118790 to R.B.S.R.] and the Alcohol & Education Research Council [HFY GR667789].
Oxford Journals will deposit all NIH-funded articles in PubMed Central. See Depositing articles in repositories – information for authors for details. Authors must ensure that manuscripts are clearly indicated as NIH-funded using the guidelines above.
Acknowledgements
This section may acknowledge contributions from non-authors, and it should include a statement of any conflicts of interest. Amendments or corrections are not allowed after publication.
References
We highly recommend the use of a reference software such as EndNote (http://www.endnote.com) for reference management and formatting (click to download the JPE Endnote reference style file).
For review articles, there is no limitation on the number of references cited, although we strongly suggest citing only publications in which original knowledge was presented. For other types of articles, the maximum number of cited references is 50.
All references in the text should have the authors immediately followed by the date to facilitate the electronic linkages which are available on-line, for example: (Shen and Ma 2001) or Shen and Ma (2001). If several papers by the same author in the same year are cited, they should be lettered in sequence (2000a, 2000b), etc. When papers are by more than two authors they should be cited thus: (Shen et al. 2001).
Only papers published or in press should be cited in the literature list. Unpublished results, including submitted manuscripts and those in preparation, should be cited as unpublished in the text. Citation of articles from e-journals and journal articles published ahead of print should have the author names, year, title, journal title followed by the assigned digital object identifier (DOI). All citations mentioned in the text, tables or figures must be listed in the reference list
Names of journals should be abbreviated according to the Serial Sources for the Biosis Data Base, available in most libraries or from http://www.biosis.org. The list of reference must be typed double-spaced throughout and checked thoroughly before submission. If the list is not in the correct form it will be returned to the author for amendment and publication of the paper may be delayed.
Journals:
Kennedy T, Jones R (1985) Effect of obesity on esophageal transit. Am J Surg 149:177–81.
Chen MJ, Fu YW, Zhou QY, et al. (2015) Simulation of Cd2+ and Zn2+ migration among water, soil and Paspalum distichum. Environ Sci Technol 38:65–70.
Book:
Long HC, Blatt MA, Higgins MC, et al. (1997) Medical Decision Making. Boston, MA: Butterworth-Heinemann.
Manners T, Jones R, Riley M (1997) Relationship of overweight to haitus hernia and reflux oesophagitis. In Newman W (ed). The Obesity Conundrum. Amsterdam, The Netherlands: Elsevier Science, 352–74.
Articles published online but not yet in print:
Qiao D, Chen W, Stratagoules E, et al. (2000) Bile acid-induced activation of activator protein-1 requires both extracellular signal-regulated kinase and protein kinase C signaling. J Biol Chem, doi:10.1074/jbc.M908890199.
Conference proceedings:
Hou Y, Qiu Y, Vo NH, et al. (2003) 23-O derivatives of OMT: highly active against H. influenzae. In: Programs and Abstracts of the Forty-third Interscience Conference on Antimicrobial Agents and Chemotherapy, Chicago, IL. Abstract F-1187, p.242. American Society for Microbiology, Washington, DC.
Thesis:
N'tchobo H (1998) Sucrose unloading in tomato fruits. II. Subcellular distribution of acid invertase and possible roles in sucrose turnover and hexose storage in tomato fruit. PhD thesis. Laval University, Canada.
Tables
Tables should be self-contained and complement, but not duplicate information in the text. Tables should be on a separate page, and should be numbered in Arabic numerals with an appropriate legend at the head. All tables should have three horizontal lines, with the upper and the lower lines in bold. No vertical lines are allowed (see the sample copy for format). They should be included in the text file (in the Word file).
Figures
Figures should be self-explanatory and contain as much information as is consistent with clarity. All figures must carry the figure number in Arabic numerals. Citation in the text should take the form Fig. 1a etc. The minimum resolution for the figures is 300 dpi (dots per inch) for tone or colour, 1200 dpi for line art at approximately the correct size for publication.
