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
2
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
3
4
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
Universidade Federal do Ceará (UFC)
5
A Deus e minha família.
6
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;
À minha turma da Geografia 2012.1 da Universidade Estadual do Ceará – UECE.
7
“They say that dreaming is free, but I wouldn’t
care what it cost me.”
(Hayley Williams, Taylor York)
8
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.
Palavras-chave: Cactaceae. Modelagem de nicho. Tacinga. Xeromorfismo.
9
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.
Keywords: Cactaceae. Niche modelling. Tacinga. Xeromorphism.
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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) .................................................................
........................................................................................................... 27
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LISTA DE TABELAS
Tabela 1- Projeção dos domínios fitogeográficos e tipos de solos das espécies
de Tacinga Britton & Rose (Cactaceae) ............................................. 29
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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
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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).
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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).
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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.
O objetivo do estudo foi definir as áreas de ocorrência dessas espécies xerófitas de
16
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.
17
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:
18
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).
Key words: Tacinga, biogeography, geographic distribution, ecological niche modeling.
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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
20
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.
21
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
22
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).
23
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.
24
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.
Fonte: Marcelo Oliveira Teles de Menezes.
25
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.
Fonte: Próprio autor.
26
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
27
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).
28
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
29
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),
30
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.
31
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.
32
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39
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)
(b) the name(s) of the author(s)
40
(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
41
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.
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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.
Chapter in book:
43
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.
44
Colour figures should be CMYK (Cyan-Magenta-Yellow-Black). All figures must be supplied
in electronic format as .TIF.
Line drawings should be clear: faint shading or stippling will be lost upon reproduction and
should be avoided and heavy shading or stippling may appear black. Lines and symbols
should be drawn boldly enough to stand reduction to the desired size. For graphs where
reduction to one-half in linear dimensions is intended, a suitable thickness for the axis would
be 0.3 mm and for the other lines 0.4 or 1.0 mm depending on the complexity of the graph.
The preferred symbols are closed circle, open circle, closed square, open square, closed
triangle, and open triangle and should be no smaller than 2 mm (height/diameter) for
reduction to one-half. The symbols x and + should be avoided.
Photographs not supplied electronically, must be of high quality, printed on glossy paper and
mounted neatly on a thin white card base, leaving a narrow gap between each print. Irregular
and asymmetrically distributed groups of photographs will not be accepted. Individual figures
should be lettered, a, b, c, etc. on the photograph using a lettering set. Other lettering, arrows,
etc. may be put on the photograph by the author; otherwise they should be indicated in the
exact position required on a transparent or translucent self-locating overlay. On no account
should any marks be made on the photograph itself.
Colour figures: If the manuscript is accepted for publication, authors will be asked to cover
the cost of reproduction, which is ¥1500/£170/$240/€200 per colour figure. Colour plates
should be combined to make a single composite figure whenever possible. A scale should be
included; otherwise the scale of the original should be stated in the legends so that the final
scale can be calculated.
Legends: A separate typewritten, double-spaced list of legends of all figures must be supplied
and included in the text file. Each legend should contain sufficient explanation to be
meaningful without cross-referencing. A scale of the original should be included in the legend
unless already indicated in the picture. A description of the symbols used in the figures should
be written out in full. (Please do not include the character symbol in the legend.)
Please be aware that figure legends may be used by search engines for figure searches.
Figure font requirements (see the sample copy for format): Typeface: Arial Figure labels (a, b,
45
c, etc.) font size: 12 pt, bold Figure caption font size: 12 pt, no bold X-axis, y-axis labels font
size: 12 pt, no bold X-axis, y-axis units: 10 pt, no bold All other text inside figures: 10 pt, no
bold
Cover illustrations will be taken from, or be associated with, an article that appears in the
journal, where possible. Authors wishing to submit a potential cover illustration should
indicate it at the time of submission. The potential cover illustration figures must be supplied
in electronic format as .TIF, and resolution must be above 300 dpi at publication size. Please
supply a short concise caption to appear inside the journal.
For useful information on preparing your figures for publication, go
to http://cpc.cadmus.com/da. Please note that all labels used in figures should be in lower case
in both the figure and the legend. The journal reserves the right to reduce the size of
illustrative material. All micrographs must carry a magnification bar.
Supplementary data
There are facilities for publishing data on the Internet (e.g. appendices, additional tables,
graphics and other material useful for enhancing the understanding of the manuscript) as
supplementary data. This section should include all the legends of the supplementary
materials.
Submission of manuscripts
Manuscripts should be submitted via the web-based submission system.
Suggesting reviewers
Please also include the names of 3–5 individuals that are qualified to review your manuscript.
Indicate the name, institution and email address of each individual. We will try to have at
least one reviewer from the set that you have requested. You may also request a member of
the editorial team that you think is best suited to handle your manuscript.
Cover letters
All authors must include a cover letter when submitting a manuscript to JPE. Cover letters
should include the following sections:
46
(a) Title, names of authors, and numbers of tables, figures and pages in the main text, and
supplementary materials;
(b) The importance and novelty of the research findings in the study;
(c) Authors need to promise that manuscripts submitted to JPE are considered on the
understanding that they have not been published elsewhere, nor are under consideration for
publication;
(d) In addition, agreement for submission and email address from all the authors are needed.
Language Editing
Particularly if English is not your first language, before submitting your manuscript you may
wish to have it edited for language. This is not a mandatory step, but may help to ensure that
the academic content of your paper is fully understood by journal editors and reviewers.
Language editing does not guarantee that your manuscript will be accepted for publication.
For further information on this service, please click here.
Revised manuscripts
Revised manuscripts should be returned via the online submission system within three months
(major revision) or one month (minor revision) of the date from when the invitation was sent;
revised manuscripts received after this time will be considered as new submissions. Revised
manuscripts should be accompanied by a detailed response letter on how all the concerns of
the editor and referees have been addressed. Please give the exact page number(s),
paragraphs(s) and line number(s) where each revision was made. Please copy this letter in
“Response to reviews” during submission and as well as upload a word file of your response.
Format: Original source files are required to avoid delays if the manuscript is accepted. The
main text must be provided as Microsoft Word. All the changes should be highlighted (in red
colour or with track changes using the “revision mode” in Microsoft Word). References,
Figure Legends and Tables should be included in the Word file.
Figures should be provided as .TIF files. The minimum resolution for the figures is 300 dpi
for tone or colour, 1200 dpi for line art at approximately the correct size for publication.
Colour figures should be CMYK (Cyan-Magenta-Yellow-Black).
47
Supplementary material for online-only publication
Supplementary data may be submitted for online only publication if it adds value for potential
readers. The hard copy of the manuscript should stand alone, but it should be indicated at an
appropriate point in the text that supplementary material is available on-line. Please name
your supplementary material and cite it within the manuscript as Figure S1, Table S1, Video
S1, etc, and provide a detailed legend.
Electronic files of supplementary material are preferable as one complete .PDF file. If images
are supplied as .GIFs or .JPEGs, the minimum acceptable resolution for viewing on screen is
120 dpi.
Videos: The preferred formats for video clips are .MOV, .MPG, .AVI, and animated .GIF
files. Authors are advised to use a readily available program to create movies so that they can
be viewed easily with e.g., Windows Media Player or QuickTime.
Authors should carefully check the supplementary data as this information is not
professionally copy edited or proofread. Once the manuscript is accepted and has been sent to
production, Authors are no longer allowed to revise the supplementary materials, including at
the proof stage.
Manuscript style
Abbreviations
Standard chemical symbols may be used in the text where desirable in the interests of
conciseness. For long chemical names and other cumbersome terms, widely accepted
abbreviations may be used in the text (e.g. ATP, DNA); the list of standard abbreviations
published by The Biochemical Journal (http://www.biochemj.org/bj/bji2a.htm) is an
acceptable guide. Abbreviations for the names of less common compounds may be used, but
the full term should be given on first mention. It is confusing and unnecessary to use
abbreviations for common English words (e.g. L for light).
Scientific names
The complete scientific name (genus, species, and authority, and cultivar where appropriate)
must be cited for every organism at the first mention. The generic name may be abbreviated to
the initial thereafter except where intervening references to other genera with the same initial
48
could cause confusion. If vernacular names are employed, they must be accompanied by the
correct scientific name on first use.
Chemical and molecular biology nomenclature
Follow Chemical Abstracts and its indexes for chemical names. The IUPAC and IUBMB
recommendations on chemical, biochemical, and molecular biology nomenclature should be
followed (see http://www.chem.qmw.ac.uk/iupac and http://www.chem.qmw.ac.uk/iubmb).
Units of measurement
The metric system is adopted as standard. The system of units known as 'SI' should be used. If
non-standard abbreviations must be used they should be defined in the text. Units of
measurement should be spelled out except when preceded by a numeral, when they should be
abbreviated in the standard form: g, mg, cm3, etc. and not followed by full stops. Use negative
exponents to indicate units in the denominator (i.e. mmol m-2 s-1).
Numbers up to ten should be spelled out in the text except when referring to measurements.
Numbers higher than ten are to be represented as numerals except at the beginning of a
sentence. Fractions are to be expressed as decimals.
Dates should be cited thus: 7 June 2001 and the 24 hour clock should be used.
Sequence data
Deposition of amino acid sequences of proteins or nucleotide sequences is required before
publication, and the database accession number must be given in the text of the manuscript.
Microarray Gene Expression Data should comply with the minimum information about
microarray experiments standard (MIAME; see http://fged.org/projects/miame/ for more
information.)
Equations
If equations require more than one level of subscript or superscript, please use either
'Microsoft Equation Editor' or 'Math Type'. If anything else is used, the equation has to be re-
typed which makes it vulnerable to errors.
Permission to reproduce figures
Please note that if your manuscript includes any data in tables or figure(s) modified or re-
drawn from another publication, you will need permission from the original publisher to
49
reproduce it before your manuscript can be published. This includes figures adapted in any
way from other publications. Permission to reproduce figures or data from other publications
must be sought by authors at the time of acceptance. Please note that obtaining copyright
permission could take some time. A copy of the permission document should be sent to the
Production Editor, Journal of Plant Ecology, Oxford University Press, Great Clarendon Street,
Oxford OX2 6DP. Email: [email protected].
To seek copyright permission please contact the copyright permission department of the
relevant journal/publisher.
Proofs
Proofs will be sent electronically to the corresponding author as a .PDF file. The author
should reply to the proof email with their corrections, and should send an annotated PDF.
Corrections should be limited to typographical errors and corrections should be returned
within three days of receipt; otherwise the Editor reserves the right to correct the proofs and to
send the material for publication. This is essential if all the material in a given issue is not to
be delayed by the late receipt of one corrected proof.
Page charges
Manuscripts that are more than ten pages in length when typeset will incur a charge
of £120/$192/€156 per extra page after the tenth page. The first ten pages are free of charge.
Unique URL
On publication of an article, the corresponding author will receive a unique URL that gives
access to both PDF and HTML versions of the paper. The URL links visitors to the JPE site
and the complete version of the paper online with all functionality retained is accessible
regardless of subscription status.
If you would like to subscribe in print, please contact the JPE editorial office
Licence to publish
50
It is a condition of publication in the journal that authors grant an exclusive licence to the
Institute of Botany, Chinese Academy of Sciences (IBCAS) and the Botanical Society of
China (BSC). This ensures that requests from third parties to reproduce articles are handled
efficiently and consistently and will also allow the article to be as widely disseminated as
possible. In assigning the licence, authors may use their own material in other publicat ions
provided that the journal is acknowledged as the original place of publication, and Oxford
University Press, on behalf of the Institute of Botany, Chinese Academy of Sciences (IBCAS)
and the Botanical Society of China (BSC), is notified in writing and in advance.
Upon receipt of accepted manuscripts at Oxford Journals authors will be invited to complete
an online copyright licence to publish form.
Please note that by submitting an article for publication you confirm that you are the
corresponding/submitting author and that Oxford University Press ("OUP") may retain your
email address for the purpose of communicating with you about the article. You agree to
notify OUP immediately if your details change. If your article is accepted for publication
OUP will contact you using the email address you have used in the registration process.
Please note that OUP does not retain copies of rejected articles.
Oxford Open articles are published under Creative Commons licences. Authors publishing in
Journal of Plant Ecology can use the following Creative Commons licences for their articles:
Creative Commons Attribution licence (CC-BY)
Creative Commons Non-Commercial licence (CC-BY-NC)
Creative Commons non-Commercial No Derivatives licence (CC-BY-NC-ND)
Please click here for more information about the Creative Commons licences.
Author self-archiving/public access policy
For information about this journal's policy, please visit our Author Self-Archiving policy
page.
Conflict of interest
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Journal policy also requires that all authors sign a conflict of interest statement. If the
manuscript is published, such information may be communicated in a note following the text
and reference.
Open access option for authors
Journal of Plant Ecology authors have the option to publish their paper under the Oxford
Open initiative; whereby, for a charge, their paper will be made freely available online
immediately upon publication. After your manuscript is accepted the corresponding author
will be required to accept a mandatory licence to publish agreement. As part of the licensing
process you will be asked to indicate whether or not you wish to pay for open access. If you
do not select the open access option, your paper will be published with standard subscription-
based access and you will not be charged.
Oxford Open articles are published under Creative Commons licences. Authors publishing in
the journal can use the following Creative Commons licences for their articles:
Creative Commons Attribution licence (CC-BY)
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Please click here for more information about the Creative Commons licences.
You can pay Open Access charges using our Author Services site. This will enable you to pay
online with a credit/debit card, or request an invoice by email or post. Open Access charges
for Journal of Plant Ecology are:
Standard charge: £1900/ $3040 / €2470
Reduced rate developing country charge*: £950/ $1520 / €1235
Free developing country charge*: £0 / $0 / €0
*A list of qualifying developing countries can be found here.
Please note that these charges are in addition to any page charges that may apply.
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Please provide a VAT number for yourself or your institution and ensure you account for your
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Third-party content in open access papers
If you will be publishing your paper under an Open Access licence but it contains material for
which you do not have Open Access re-use permissions, please state this clearly by supplying
the following credit line alongside the material:
Title of content Author, Original publication, year of original publication, by permission of
[rights holder] This image/content is not covered by the terms of the Creative Commons
licence of this publication. For permission to reuse, please contact the rights holder
Crossref funding data registry
In order to meet your funding requirements authors are required to name their funding
sources, or state if there are none, during the submission process. For further information on
this process or to find out more about the CHORUS initiative please click here.
Crossref funding data registry
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please contact the editorial office at [email protected]. The cost per issue is ¥150, or ¥900 for
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