UNIVERSIDADE FEDERAL DO RIO GRANDE DO NORTE
PROGRAMA DE PÓS-GRADUAÇÃO EM ECOLOGIA
ALINA ROCHA PIRES BARBOZA
INVERTEBRADOS BENTÔNICOS DE RECIFES ARENÍTICOS
TROPICAIS: AVALIAÇÃO DE MÉTODOS E ESTRUTURAÇÃO DA
COMUNIDADE INTERTIDAL
Natal/RN 2019
ALINA ROCHA PIRES BARBOZA
Invertebrados bentônicos de recifes areníticos tropicais: avaliação de
métodos e estruturação da comunidade intertidal
Tese apresentada ao Programa de
Pós-Graduação em Ecologia da Universidade
Federal do Rio Grande do Norte, como
requisito parcial para obtenção do grau de
Doutora em Ecologia.
Orientadora: Dra. Tatiana Silva Leite
Co-orientador: Dr. Fúlvio Aurélio de Morais Freire
Aprovada em 01/02/2019.
BANCA EXAMINADORA
Dra. Juliana Deo Dias (Presidente - UFRN)
Dra. Cristiane Xerez Barroso (UFC)
Dr. Carlos Eduardo Rocha Duarte Alencar (UERN)
Dr. Edson Aparecido Vieira Filho (UFRN)
Dra. Rosângela Gondim D’Oliveira (UFRN)
Natal/RN 2019
Universidade Federal do Rio Grande do Norte - UFRN Sistema de Bibliotecas - SISBI
Catalogação de Publicação na Fonte. UFRN - Biblioteca Central Zila Mamede
Barboza, Alina Rocha Pires.
Invertebrados bentônicos de recifes areníticos tropicais: avaliação de métodos e estruturação da comunidade intertidal / Alina Rocha Pires Barboza. - 2019.
163f.: il.
Tese (Doutorado)-Universidade Federal do Rio Grande do Norte, Centro de Biociências, Programa de Pós-Graduação em Ecologia, Natal, 2019.
Orientadora: Dra. Tatiana Silva Leite.
Coorientador: Dr. Fúlvio Aurélio de Morais Freire.
1. Bentos - Tese. 2. Moluscos - Tese. 3. Equinodermos - Tese. 4. Recifes sedimentares - Tese. 5. Métodos de levantamento - Tese. 6. Cienciometria - Tese. I. Leite, Tatiana Silva. II. Freire, Fúlvio Aurélio de Morais. III. Título.
RN/UF/BCZM CDU 574
À minha família, que participa ativamente de todas as
minhas conquistas. Meu porto seguro.
“Uns confiam em carros e outros em cavalos, mas
nós faremos menção do nome do Senhor nosso
Deus.”
AGRADECIMENTOS
A Deus, que tem me sustentado a cada dia e permitido a concretização de projetos, como essa tese, e tem me permitido estudar as maravilhas de Sua criação.
Aos meus pais, Bezaliel e Cássia, e minha irmã, Glice, que oraram por mim e forneceram todo o apoio, amor, conforto e carinho necessários para eu encontrar forças e seguir em frente diante das dificuldades surgidas no caminho. Agradeço também por todo o apoio material e logístico na compra e confecção de artefatos para os campos e na coleta de dados. Sou grata ao meu pai, que testou e me ensinou a melhor forma de fazer a marcação das minhas áreas amostradas e me ensinou a medir o perfil dos recifes; e à minha irmã, que editou a maioria dos gráficos desta tese.
Ao meu amado esposo, Ted Manassés, que tem me incentivado, apoiado e ajudado de perto em toda minha jornada acadêmica, desde a participação em campo à tabulação de dados, e no cuidado comigo nos mínimos detalhes no dia-a-dia. Seu companheirismo e suporte foram fundamentais para a realização dessa tese.
À profa. Tatiana (Taty), agradeço pelos anos de orientação acadêmica, pelo exemplo de profissionalismo e competência, pela amizade, pelas broncas, pelo conforto e por desejar e lutar por um mundo melhor. Principalmente, agradeço por ter continuado me orientando nesta tese mesmo em meio a tantos problemas que surgiram pelo caminho. Não foi fácil, mas estamos aqui.
Ao prof. Fúlvio, agradeço imensamente por ter me acolhido como sua co-orientanda e ter me assistido quando precisei.
A todos que me ajudaram em campo, um agradecimento muito especial! Gostaria de citar o nome de todos, mas foram mais de 50 pessoas que me acompanharam nas praias nesses quatro anos de trabalho. Aos alunos dos cursos de graduação de Ciências Biológicas, Ecologia e Aquicultura, que me permitiram transmitir um pouco do que sei e que me ensinaram tantas coisas. Todos foram muito importantes para a coleta de dados, mas agradeço especialmente a Mariana, Alana, Géssyca e Pedro, que foram os primeiros a me dar o suporte na fase mais delicada de início de coletas, e a Geovane Oliveira, que participou de incontáveis campos e conseguiu inúmeros voluntários para nos ajudar. Obrigada aos familiares, amigos e amigos dos amigos que não são da minha área de estudo, mas mesmo assim foram para cima dos recifes ajudar da forma que puderam.
Um agradecimento especial a Mariana Lisboa, que contribuiu em inúmeras etapas deste trabalho, e ao seu irmão Matheus Lisboa, pela ajuda com os mapas.
À minha amiga Larissa Nascimento, por todo apoio, pelas sugestões e por tirar minhas dúvidas de estatística domingo à noite.
Aos professores que contribuíram para condução do trabalho: Guilherme Longo, Alexandre Fadigas e Adriano Calimam.
À professora Rosângela Gondim, pelos incentivos de sempre e por conseguir vários alunos para participar das coletas.
Ao professor Marcos Nascimento, pela contribuição com informações geológicas da área de estudo.
Aos amigos do departamento de Oceanografia e Limnologia e do departamento de Ecologia, pelos momentos de trocas de ideias e de descontração.
Aos amigos e colegas que em algum momento contribuíram com considerações pertinentes para o desenvolvimento da tese, em especial Maiara Menezes, Nádia, Priscila Cruz, Helder Espírito-Santo, Guilherme Pierri, Bruno Wanderley e Carla Milanez.
A Felipe Oliveira, por ser sempre tão solícito e pelas ajudas e incentivos.
À profa. Eliane Marinho (Laboratório de Macroalgas Marinhas da UFRN), agradeço pela ajuda na identificação de algas e por me receber sempre com tanto carinho e motivação.
Aos professores Alexandre Pimenta (Museu Nacional/UFRJ), Helena Matthews-Cascon (UFC) e Paula Spotorno (IEAPM) pela ajuda na identificação de moluscos; e ao professor Renato Ventura (Museu Nacional/UFRJ), pela ajuda na identificação de equinodermas.
À Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), pela concessão de bolsa de estudo.
Ao Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), pela concessão de licença para coleta.
Enfim, a todos que de alguma forma contribuíram, participaram, oraram e torceram para que eu conseguisse terminar esta tese.
RESUMO
Ambientes intertidais de substrato rochoso servem como área de alimentação, crescimento e reprodução de uma diversidade de organismos bentônicos. Esses ecossistemas são encontrados no mundo todo e características ambientais e biológicas influenciam na composição e nos padrões temporais e espaciais de distribuição do bentos. A maioria dos trabalhos tem se concentrado em ambientes de costões rochosos de regiões temperadas e subtropicais. Por outro lado, há uma carência de estudos em outras formações rochosas e de ambientes tropicais, que testem metodologias que sejam adequadas à maior heterogeneidade de substrato e menor inclinação. O presente estudo teve três objetivos principais: 1) identificar os principais tipos de métodos que vêm sendo empregados para o levantamento de organismos bentônicos sésseis e móveis, por meio de uma análise cienciométrica; e, em recifes areníticos tropicais: 2) testar métodos de levantamento bentônico que melhor representem a riqueza destes organismos neste ambiente, testando abordagens aleatórias e estratificadas, com quadrados e com transectos com quadrados aninhados; 3) e, a partir do método de coleta definido com o objetivo anterior, testar quais os fatores ambientais mais influenciam a ocorrência, abundância e riqueza desses organismos, além de testar se há variação sazonal na abundância dos táxons. A mobilidade de organismos foi um dos principais fatores determinantes na escolha do método de levantamento bentônico nos artigos analisados. Quadrados e transectos com quadrados aninhados foram os principais métodos utilizados para delimitar áreas de contagem do número de indivíduos da fauna móvel e estimativa de porcentagem de cobertura da fauna séssil. Nos recifes tropicais escolhidos para os testes metodológicos, uma abordagem de levantamento bentônico aleatória, com uso de transectos com quadrados aninhados de forma sistematizada, incluindo a amostragem embaixo de rochas, quando presentes, contemplou a maior riqueza de espécies da área com menor esforço de coleta. Tipo de cobertura de substrato, tipologia de recife (com blocos de rochas e abrigados do embate de ondas ou em platô rochoso exposto a embate de ondas), índice de complexidade do hábitat e tempo de exposição foram os principais fatores estruturadores da comunidade no hábitat em cima das rochas. Tipo de substrato debaixo das rochas, o índice de complexidade e o tempo de exposição foram os principais fatores estruturadores da comunidade no hábitat embaixo das rochas. Quanto à abundância dos organismos nos diferentes períodos, Pugilina tupiniquim, Holothuria grisea e Cerithium sp. são táxons indicadores da estação chuvosa e Aplysia dactylomela, da estação seca em recifes de tipologia com blocos rochosos e abrigados.
Palavras-chave: bentos, moluscos, equinodermas, recifes sedimentares, métodos de levantamento, cienciometria
ABSTRACT
Rocky intertidal environments are important feeding, growth and reproduction areas to a variety of benthic organisms. These ecosystems can be found worldwide and their benthos’ composition and temporal and spatial patterns are influenced by environmental and biological factors. Most studies on these environments have focused on rocky shores of temperate and subtropical regions. On the other hand, there is a lack of studies in other rocky formations and tropical regions, specially testing proper methodologies that are suitable for greater substrate heterogeneity and lower slope. This study had three main objectives: 1) to identify the main types of method used for quantifying benthonic organisms, using scientometric analysis; and, in tropical sedimentary reefs: 2) to test random and stratified quadrats and transects with quadrats to test the survey method that best represent richness of molluscs and echinoderms in these environments; 3) and, after determining the most suitable survey method, to test which environmental factors influence occurrence, abundance and richness of these organisms, and test whether there is seasonal variation of abundance of taxa. The organisms’ mobility was one of the determinant factors when choosing benthonic survey method in the analyzed papers. Quadrats and transects with quadrats were the main methods used to delimit areas for counting of mobile individuals and estimation of sessile cover. On the selected tropical reefs for the methodological tests, random transects with quadrats showed better richness results with less sampling effort, including sampling under boulders when they were present. Substrate cover, reef typology, habitat complexity and exposure time were the main environmental factors determining the structure of communities over the reefs. Substrate cover, habitat complexity and exposure time were the main factors structuring communities under boulders. Regarding organisms’ abundance between the different seasons, Pugilina tupiniquim, Holothuria grisea and Cerithium sp were indicative taxa of the rainy season and Aplysia dactylomela was indicative taxa of the dry season in sheltered reefs with rocky blocks.
LISTA DE FIGURAS
CAPÍTULO I - Patterns of methodological approach to evaluate the structure of rocky intertidal benthic communities: 40 year of surveys
Figure 1 -Temporal trends in the number of published papers on rocky intertidal zoobenthos, between 1979 and May 2018. ... 27
Figure 2 - Percentage of published articles on benthic organisms of rocky intertidal ecosystems, from 1979 to 2018, considering a) research approaches and b) target taxa. ... 28
Figure 3 - Relative frequency of articles on benthic organisms of rocky intertidal ecosystems published between 1979 and May 2018 that described important environmental features, per type of research approach……….. .. 29
Figure 4 - Percentage of published articles surveying rocky intertidal benthic fauna, from 1979 to 2018, regarding type of used method and animals’ mobility. ... 30
Figure 5 - Correspondence analysis diagrams showing ordination of: a) methods used for counting zoobenthos and the type of animals’ mobility, b) methods and research approaches, and c) research approaches and period of study………..……….31
Figure 6 - Percentage of published articles on benthic organisms of rocky intertidal ecosystems, from 1979 to 2018, considering a) used methods for assessing benthic fauna, b) type of environment and c) climate region where the study took place………... 33
Figure 7 - Locations where studies on benthic organisms of rocky intertidal ecosystems were conducted between 1979 and May 2018………...34
CAPÍTULO II - Comparação entre métodos de levantamento bentônico em recifes areníticos intertidais tropicais de diferentes tipologias
Figura 1 - Mapa de localização dos recifes estudados, nas praias de Santa Rita e do Meio, em relação à costa do estado do Rio Grande do Norte, Brasil ... 57
Figura 2 - Fotos dos recifes estudados: Praia de Santa Rita (esquerda), com recife de Tipologia com Blocos Rochosos e Abrigado (TBRA), e Praia do Meio (direita), recife de Tipologia Platô Rochoso e Exposto (TPRE). ... 58
Figura 3 - Aplicação em capo do método de Quadrados Aleatórios (esquerda) e esquema representativo da disposição dos quadrados (direita) ... 60
Figura 4 - Amostragem de macroinvertebrados bentônicos embaixo de rochas ... 60
Figura 5 - Aplicação do método de Transectos: a) transecto em cinto utilizado para levantamento da megafauna; b) quadrados alocados dentro do transecto para levantamento de macrofauna maior e macrofauna menor; c) desenho esquemático do método de Transectos...61
Figura 6 -Manchas de hábitats identificadas no recife de Tipologia Platô Rochoso Exposto (TPRE): a) Borda; b) Platô; c) Braquidontes; c) Craca...62
Figura 7 -Manchas de hábitats identificadas no recife de Tipologia com Blocos Rochosos Abrigado (TBRA): a) Rocha; b) Rocha com areia; c) Borda; c) Borda com areia...63
Figura 8 -Curvas de rarefação (linhas contínuas) e extrapolação (linhas tracejadas) da riqueza para cada método aplicado nos recifes estudados. Áreas pintadas em torno das linhas representam seus respectivos intervalos de confiança (0,95). TPRE = tipologia platô e exposto; TBRA = tipologia com blocos rochosos e abrigados. TA = transecto aleatório; TM = transecto em manchas; QA = quadrado aleatório...66
CAPÍTULO III - Fatores ambientais determinantes na estruturação da comunidade de invertebrados bentônicos em recifes areníticos intertidais tropicais
Figura 1 - Mapa de localização da área de estudo em relação à costa do Rio Grande do Norte, Brasil ... 82
Figura 2 - Imagens dos recifes areníticos nas praias amostradas: A) Santa Rita (TBRA), B) Búzios (TBRA), C) Praia do Meio (TPRE) e D) Tabatinga (TPRE) ... 83
Figura 3 - Perfil topográfico dos recifes amostrados no Rio Grande do Norte. Santa Rita e Búzios = recifes de tipologia de blocos rochosos e abrigados; Praia do Meio e Tabatinga = recifes com tipologia de platô rochoso e exposto. Linha contínua = recife rochoso; linha tracejada = porção da praia de areia ... 90
Figura 4 - Análise de Componentes Principais com dados ambientais de cima das rochas dos recifes estudados, apresentados nas dimensões 1 e 2 e 1 e 3 (A e B, respectivamente), somando 47,6% da explicação. Círculos menores correspondem aos pontos de coleta de dados, com seus respectivos centroides indicados pelos círculos maiores. TBRA = recifes de tipologia com blocos rochosos e abrigados; TPRE = recifes de tipologia platô rochoso e exposto ... 92
Figura 5 - Análise de Componentes Principais com dados ambientais debaixo das rochas dos recifes de Tipologia com Blocos de Rochas e Abrigados estudados, apresentados nas dimensões 1 e 2 e 1 e 3 (A e B, respectivamente), somando 37,2% da explicação ... 94
Figura 6 - Distribuição dos dados de riqueza da megafauna, macrofauna móvel e macrofauna séssil, coletados em seus respectivos amostradores: transecto 10 m x 1m, quadrado de 0,25cm2 e quadrado de 0,04cm2, respectivamente, em cada recife amostrado. Boxplot: base e topo do retângulo = 1° e 3° quartis, respectivamente; linha atravessando o retângulo = mediana; barra acima do retângulo = valor máximo; círculos = valores discrepantes. TBRA = tipologia com blocos rochosos e abrigados; TPRE = tipologia platô rochoso e exposto...97
Figura 7 - Distribuição dos dados de abundância (número de indivíduos) da megafauna e da macrofauna móvel e de porcentagem de cobertura da macrofauna séssil, coletados em seus respectivos amostradores: transecto 10 m x 1m, quadrado de 0,25cm2 e quadrado de 0,04cm2, respectivamente, em cada recife amostrado. Boxplot: base e topo do retângulo = 1° e 3° quartis, respectivamente; linha atravessando o retângulo = mediana; barra acima do retângulo = valor máximo; círculos = valores discrepantes. TBRA = tipologia com blocos rochosos e abrigados; TPRE = tipologia platô rochoso e exposto ... 98
Figura 8 - db-RDA com dados ambientais e dados de presença e ausência da megafauna (A) e macrofauna em cima de rocha (B) nos recifes areníticos estudados no Rio Grande do Norte, com indicação dos centroides dos pontos referentes a dados coletados em recifes de Tipologia com Blocos Rochosos e Abrigados (I) e naqueles de Tipologia Platô Rochoso e Exposto (II) ... 100
Figura 9 - Ordenação por nMDS da fauna em cima de rocha (megafauna, macrofauna séssil e macrofauna móvel, respectivamente), associada a tipologia do recife e períodos seco e chuvoso ... 102
Figura 10 - Distribuição de dados de (A) riqueza (número de espécies) e (B) abundância (número de indivíduos) da macrofauna embaixo de cada rocha amostrada em recifes de Tipologia com Blocos Rochosos e Abrigados. Boxplot: base e topo do retângulo = 1° e 3° quartis, respectivamente; linha atravessando o retângulo = mediana; barra acima do retângulo = valor máximo; círculos = valores discrepantes ... 104
Figura 11 - db-RDA com dados ambientais e dados de presença e ausência da macrofauna embaixo de rocha nos recifes areníticos estudados no Rio Grande do Norte. I. bicolor = Isognomon bicolor; T. viridula = Tegula viridula; P. imbricata = Pinctada imbricata; L. subrugosa = Lottia subrugosa; L. nassa = Leucozonia nassa; E. lineolata = Echinolittorina lineolata; 1 a 8 = outras espécies sem correlações ... 105
Figura 12 - Ordenação por nMDS da fauna embaixo de rocha nos recifes de Tipologia com Blocos de Rocha e Abrigados, nos períodos seco e chuvoso ... 106
LISTA DE TABELAS
CAPÍTULO I - Patterns of methodological approach to evaluate the structure of rocky intertidal benthic communities: 40 year of surveys
Table 1 - Tabulated information from analyzed papers ... 25 Appendix 1 – References of the papers selected by the bibliographical survey…………...43
CAPÍTULO II - Comparação entre métodos de levantamento bentônico em recifes areníticos intertidais tropicais de diferentes tipologias
Tabela 1 - Número total de táxons registrados nos recifes de Tipologia Platô Rochoso e Exposto (TPRE) e de Tipologia com Blocos Rochosos e Abrigados (TBRA), em cada método testado. TA = transecto aleatório; TM = transecto em manchas; QA = quadrados....65
Tabela 2 - Tempo aproximado para aplicação de cada método testado nos recifes de Tipologia Platô Rochoso e Exposto (TPRE) e Tipologia com Blocos Rochosos e Abrigados (TBRA); estimativa por m2 e tempo gasto no presente estudo (200m2 amostrados). TA = transecto aleatório; TM = transecto em manchas; QA = quadrados aleatórios ... 67
ANEXO I
Tabela 1 - Relação de táxons com suas respectivas densidades – n° de indivíduos/m2 (D) e ocorrências (O) para cada tamanho de amostrador, em cada método, no recife de Tipologia Platô Rochoso e Exposto. C = comum, F = frequente; R = rara. ... 74
Tabela 2 - Relação de táxons com suas respectivas densidades – n° de indivíduos/m2 (D) e ocorrências (O) para cada tamanho de amostrador, em cada método, no recife de Tipologia com Blocos Rochosos e Abrigado. C = comum, F = frequente; R = rara. ... 75
CAPÍTULO III - Fatores ambientais determinantes na estruturação da comunidade de invertebrados bentônicos em recifes areníticos intertidais tropicais
Tabela 2 - Características físicas dos recifes amostrados. TBRA = tipologia com blocos rochosos e abrigados; TPRE = tipologia platô rochoso e exposto ... 90
Tabela 3 - Frequência de ocorrência dos táxons de moluscos e equinodermas amostrados nos recifes de Tipologia com Blocos Rochosos e Abrigados (TBRA) e Tipologia Platô Rochoso Exposto (TPRE). R = rara; F = frequente; C = comum ... 96
Tabela 4 - Frequência de ocorrência dos táxons de moluscos e equinodermas do hábitat embaixo de rochas dos recifes de Tipologia com Blocos Rochosos e Abrigados (TBRA). R = rara; F = frequente; C = comum ... 103
SUMÁRIO
INTRODUÇÃO GERAL ... 18
METODOLOGIA GERAL ... 19
REFERÊNCIAS GERAIS ... 20
CAPÍTULO 1 - PATTERNS OF METHODOLOGICAL APPROACH TO EVALUATE THE STRUCTURE OF ROCKY INTERTIDAL BENTHIC COMMUNITIES: 40 YEAR OF SURVEYS ... 22
1 INTRODUCTION ... 22
2 MATERIALS AND METHODS ... 24
3 RESULTS ... 27
4 DISCUSSION ... 34
5 REFERENCES ... 37
APPENDIX 1 - REFERENCES OF THE PAPERS SELECTED BY THE BIBLIOGRAPHICAL SURVEY. ... 43
CAPÍTULO 2 - COMPARAÇÃO ENTRE MÉTODOS DE LEVANTAMENTO BENTÔNICO EM RECIFES ARENÍTICOS INTERTIDAIS TROPICAIS DE DIFERENTES TIPOLOGIAS ... 55 1 INTRODUÇÃO ... 55 2 MATERIAIS E MÉTODOS ... 57 3 RESULTADOS ... 64 4 DISCUSSÃO ... 67 5 REFERÊNCIAS ... 69 ANEXO 1 ... 74
CAPÍTULO 3 - FATORES AMBIENTAIS DETERMINANTES NA ESTRUTURAÇÃO DA COMUNIDADE DE INVERTEBRADOS BENTÔNICOS EM RECIFES ARENÍTICOS INTERTIDAIS TROPICAIS ... 78
1 INTRODUÇÃO ... 78 2 MATERIAIS E MÉTODOS ... 81 3 RESULTADOS ... 89 4 DISCUSSÃO ... 106 5 REFERÊNCIAS ... 110 CONCLUSÃO GERAL ... 115
MATERIAL SUPLEMENTAR: MOLUSCOS E EQUINODERMAS DE RECIFES ARENÍTICOS INTERTIDAIS DO RIO GRANDE DO NORTE...116
INTRODUÇÃO GERAL
Ecossistemas rochosos intertidais estão distribuídos em todo o mundo sob uma diversidade de formas, podendo se apresentar, por exemplo, como costões rochosos de grandes inclinações, recifes planos, aglomerados de rochas, ou uma mistura de várias formações. Sua complexidade biológica e estrutural faz com que esses ecossistemas sirvam de hábitat para diversos seres vivos que estão adaptados aos ciclos diários de emersão e submersão, como consequência da variação do nível da maré. Dentre as espécies adaptadas a esta condição, então os organismos bentônicos, muito comuns nos intertidais rochosos e representados por vários táxons, tanto do fitobentos quanto do zoobentos (Little et al., 2010; Satyam & Thiruchitrambalam, 2018).
Dentre os representantes do zoobentos moluscos e equinodermas são exemplos de grupos de ocorrência frequente em áreas intertidais rochosas e que desempenham importantes papeis ecológicos, podendo atuar, por exemplo, como bioindicadores (moluscos, Gladstone, 2002), bioerodidores (equinodermos, Griffin et al., 2003) e reguladores populacionais de outras espécies (equinodermos, Wright et al., 2005).
A complexidade e a diversidade dos ambientes e dos organismos intertidais leva a uma grande variedade de métodos aplicados para levantamento bentônico, dependendo principalmente do tipo de substrato e de características dos organismos, como tamanho e mobilidade (Murray et al., 2006; Underwood & Jackson, 2009).
A composição, estrutura e distribuição espacial e temporal da comunidade bentônica nos ambientes rochosos intertidais são influenciadas por um conjunto de fatores bióticos, físicos e ambientais, como interações ecológicas negativas e positivas (Bertness & Leonard, 1997; Cowan et al, 2016), tempo de emersão, grau de exposição às ondas, complexidade do hábitat, grau de estabilidade do substrato e cobertura do substrato (Connell, 1961; Lewis, 1964; Coutinho, 1995; Tomanek & Helmuth, 2002; Chapman & Bulleri, 2003; Araújo et al, 2005; Skinner & Coutinho, 2005; Wallenstain & Neto, 2006) e variações de grandes amplitudes nas condições climáticas (Underwood & Denley, 1984).
No Brasil, a costa é formada principalmente por dois tipos de formações rochosa intertidais (Short & Klein, 2016; Ghilardi et al, 2008): um deles são os costões rochosos, que correspondem aos afloramentos rochosos de áreas de transição terra-mar e se estendem até poucos metros abaixo do nível do mar. Esse tipo de formação está presente principalmente na região sudeste do país e em ilhas oceânicas. O segundo tipo, muitas
vezes denominado de recifes areníticos ou beach rocks, são formações areníticas que podem se apresentar geralmente como formações planas e contínuas e/ou em estruturas de blocos rochosos agregados, comuns na região nordeste.
Diante do exposto, os principais objetivos deste trabalho foram: 1) por meio de uma análise cienciométrica, identificar os principais tipos de métodos que vêm sendo empregados para o levantamento de organismos bentônicos; e, em recifes areníticos tropicais: 2) testar métodos de levantamento bentônico que melhor representem a riqueza de moluscos e equinodermas neste ambiente, testando abordagens aleatórias e estratificadas, com quadrados e com transectos com quadrados aninhados; 3) e, a partir do método de coleta definido com o objetivo anterior, testar quais os fatores ambientais mais influenciam a ocorrência, abundância e riqueza desses organismos, além de testar a influência da sazonalidade na ocorrência das espécies.
Metodologia geral
As atividades de campo deste trabalho foram realizadas em recifes sedimentares areníticos tropicais de quatro praias no estado do Rio Grande do Norte/Brasil (capítulo 3, figura 1): Santa Rita (Extremoz), Praia do Meio (Natal) e Búzios e Tabatinga (Nísia Floresta). Foram escolhidos recifes de duas tipologias diferentes para contemplar a diversidade dos recifes e se investigar se a comunidade bentônica responde da mesma forma às características ambientais de cada uma delas: 1) Tipologia com Blocos Rochosos e Abrigados (TBRA), com presença de blocos de rochas, que podem estar soltas sobre o sedimento ou sobre outras rochas ou podem estar cimentadas/aglomeradas, e abrigados da exposição às ondas; e 2) Tipologia Platô Rochoso e Exposto (TPRE), apresentando-se em forma de platô elevado, com declividade suave em direção ao mar, sujeito ao embate de ondas.
O limite da área amostrada em cada recife foi georreferenciado e os pontos foram plotados em mapa no programa GPS Trackmaker, onde foi criado o contorno de cada recife estudado. Para a aleatorização das áreas amostradas, foi criada uma nuvem de pontos (coordenadas geográficas) sobre cada recife e, posteriormente, foram sorteados os pontos que seriam amostrados. Caso os pontos ficassem sobrepostos, um deles era eliminado e outro ponto era sorteado.
Nesta tese de doutorado, optamos por adotar a estrutura de agregação de artigos científicos. São apresentados três capítulos em formato de artigos completos e uma introdução e uma conclusão integradoras.
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Patterns of methodological approach to evaluate the structure of rocky intertidal benthic communities: 40 year of surveys
ABSTRACT
Marine hard-bottom substrates are heterogeneous environments found as rocky shores, rocky reefs, loose rock formations or even as a mix of many rock types. The biological and structural complexity of these environments leads to a great variety of methods usage for quantifying benthic animals, which must be adapted to their size classes and mobility. This study aims to: i) evaluate the main methodological approaches used to assess the zoobenthic structure at rocky intertidal ecosystems and ii) identify temporal-spatial relationship among the methodologies and the hard-bottom types. We used online databases for bibliographical surveys considering only ecological studies involving zoobenthic organisms in natural rocky intertidal environments.A total of 201 scientific papers were selected for analyzes. The most common methods for mobile benthos counting were quadrats and quadrats associated with transects; and for sessile animals were visual estimation of percentage cover in the field and photoquadrats for further count. There are still some gaps in the publications, such as the lack of standardization of the used terms, the lack of environments’ description and the lack of studies at tropical areas and rocky reef and boulder environments.We suggest that the widely applied methodologies be tested in the less contemplated environments until now, such as reefs and boulders in tropical areas.
Key-words: benthos, rocky intertidal, survey methods, scientometrics.
1. Introduction
Rocky intertidal ecosystems are distributed worldwide, occurring from tropical (Sibaja-Cordero, 2008; Londoño-Cruz et al., 2014) to polar zones (Smith & Simpson, 2002; Valdivia et al., 2014), representing 75% of the world’s coast (Davis Jr & FitzGerald, 2009). Marine hard-bottom substrates are heterogeneous environments
(Danovaro & Fraschetti, 2002) and can be categorized as, for example, rocky shores with accentuated slope, rocky reefs presenting flat platforms or rough surfaces, loose rock formations made of boulders or even as a mix of many rock types. Likewise, these substrates may hold different micro-habitats such as tidepools, crevices and boulders’ undersurfaces (Little et al., 2010; Satyam & Thiruchitrambalam, 2018).
The highest biological and structural variety in these habitats are usually related to tropical shorelines (Satyam & Thiruchitrambalam, 2018), in function of greater diversity of biogenic cover such as corals and sponges, algae beds, bryozoans and ascidians (Bianchi et al., 2004). These organisms modify hard-bottoms, increasing environmental complexity and heterogeneity, thus providing habitats to the associated fauna (Parker et al., 2001; Monteiro et al. 2002; Cole, 2010).
Benthic communities in rocky intertidal ecosystems are structured by an interaction of biotic and abiotic factors (Stephenson & Stephenson, 1949; Lewis, 1964; Little et al., 2010), some of which includes predation (Paine, 1966; Cowan et al., 2016), competition (Stanley & Newman, 1980; Paine, 1984), positive interactions such as mutualism and facilitation (Bertness & Leonard, 1997; Molina-Montenegro et al, 2005), tide range (emersion and submersion periods) (Chappuis et al., 2014), wave action (Gutiérrez et al 2015; Mrowicki & O´Connor, 2015;), type of rock (petrography) (Schoch & Dethier, 1996) and substrate slope (Benedetti-Cecchi et al., 2000).
The complexity of these environments leads to a great variety of methods usage. It is important to standardize them, depending mainly on sampled substrate and organism characteristics (Underwood & Jackson, 2009). For instance, methods for quantifying benthic animals must be adapted to their size classes and mobility (Murray et al., 2006; Little et al., 2010).
The first studies on benthic ecology were carried out on rocky shores and focused on explaining zonation patterns. Kjellman (1877, 1878) explained zonation based on tidal levels in Russia, Stephenson and Stephenson (1949), proposed a universal system of patterns defined by organisms’ distribution along shores, and Lewis (1961, 1964) included wave exposure as an important factor determining zonation. Later, Connell (1961) and Paine (1966) conducted important studies on species interactions as drivers of diversity and population and community structure at rocky shores. Since then, different methods and approaches have been applied to evaluate diversity, distribution and other characteristics of benthic fauna, such as active search, line and belt transects, quadrats, scraping, etc.
In function of the wide variation of the hard-bottoms’ features throughout the world, and to understand how methods and approaches evolved across time and space, this study aimed to: i) evaluate the main methodological approaches used to assess the zoobenthic structure at rocky intertidal ecosystems and ii) identify temporal-spatial relationship among the methodologies and the hard-bottom types.
2. Materials and methods 2.1.Bibliographical survey
This survey considered only ecological studies involving zoobenthic organisms in natural rocky intertidal environments. Two online databases were used to search for published articles: the database of the Coordination for the Improvement of Higher Education Personnel (CAPES) (http://www.periodicos.capes.gov.br/), a virtual library that makes international papers available to education and research institutions in our country (Brazil), and the database of the Web of Science (accessed through the CAPES portal), a widely used international reference platform. No temporal criteria were used in the search.
The following terms were inserted at the search field “topic” in both websites: “reef”, “rocky shore”, “hard bottom” and “beach rock”. Each of these was combined with the set of words and codes “benth* OR macroinvertebrate OR macrofauna OR sampl* method* OR assessment”. In total, four arrangement of words were made in each database.
We selected the papers based on their title and abstracts. Some of the analyzed papers did not focus exclusively on natural rocky ecosystems, intertidal areas or zoobenthos, but we considered them in our research and only noted information regarding these criteria.
We compiled the selected papers in a spreadsheet gathering the information based on bibliographical data, climate domains, research approaches, environmental information, target taxa, organisms’ mobility, field methods and type of studied environment (Table 1). When one of the analyzed categories of information presented more than one answer in the same article, one additional line for that article was inserted in the spreadsheet in order to record all information contemplated in each article. When the required information was not available in the paper, or when it did not relate to the aim of our study, we completed the spreadsheet cell with “NA” (not applicable). We conducted the bibliographical survey and data compilation between April and July 2018.
Review articles were not included in the analyzes regarding type of used methods, once these articles are a compilation of many others that used different methods. For the same reason, they were not included in the descriptive analyzes which identified the most described environmental variables per research approach.
Table 1. Tabulated information from analyzed papers.
Tabulated information Description
Bibliographical data Authors; year of publication; paper name; journal; local of study
Climate domains
Based on the Köppen-Trewartha climate classification (Trewartha & Horn, 1980): tropical, dry, subtropical, temperate, boreal and polar.
Research approaches
a. Biodiversity - studies on more than one species, or on a group of organisms, emphasizing ecological indexes (e.g., richness, biodiversity and evenness); b. Observational - descriptive studies emphasizing ecological aspects; c. Experimental – studies used to answer questions or test scientific hypotheses, involving some type of sample or experimental design in the field; d. Methodological - studies with an emphasis on the establishment of or comparison between field sampling methodologies; e. Review - studies reviewing the existing literature on intertidal rocky bottoms zoobenthos, either on a taxon or local. Adapted from Coutinho et al, 2016.
Environmental information Tidal range, waves action, rock slope and rock type: whether the paper described this information or not.
Target taxa
The highest taxonomic levels were used as categories (such as class or phylum). Studies done with the benthic community were defined as “macrobenthic community” when including algae or “macrozoobenthic community”, when invertebrates only. When the paper focused on biological interactions between different taxa, the category used was “interaction” and the taxa were specified in another spreadsheet column.
Mobility “sessile”, “mobile” or “sessile and mobile”, when including both types of invertebrates.
Methods
When zoobenthic qualitative-quantitative assessments were performed; active search (e.g. Rivadeneira et al., 2002), aerial photography (e.g. Murfitt et al., 2017), belt transects (e.g. Fa & Fa, 2002), belt transects with quadrats (e.g. Flores-Rodríguez et al., 2007), collection (e.g. Le Hir & Hilly, 2005 and Quirós-Rodríguez et al., 2015), hoop (Eschweller et al., 2009), percentage cover estimation (e.g. Bertocci et al., 2010), photoquadrats (e.g. Chan et al., 2008), quadrats (e.g. Herbert et al., 2009 and Ramírez et al., 2009), rock sampling (e.g. Liversage et al., 2014 and Ríos & Mutschke, 1999), scraping (e.g. Izquierdo & Guerra-García, 2011) and transects with quadrats (e.g. Miloslavich et al., 2013). The method “aerial photography” occurred twice, but since the photos were further analyzed using digital frames, it was gathered together with photoquadrats category. The methods “hoop” and “belt transects with quadrats” occurred only once and twice, respectively, so they were considered outliers and excluded from the analyzes.
Type of environment
a. rocky shore – when the authors used this term; b. rocky reef - when the authors used this term or a related name such as “rocky platform”, “flattened platform”, and “bedrock”; c. boulders - when the authors used this term or a similar name such as “boulder field” and “boulder reef”; d. hard bottom - when the authors used this term, when the study area was made of more than one type of rocky environment (e.g., reef, boulders and pebbles), and when the name was too general (e.g., “rocky coast”, “rocky substrates”, “rocky surface” and “rocky intertidal habitats”);
2.2. Data analysis
In order to evaluate temporal trends on publications, we plotted the number of references by year of publications in a scatterplot. We calculated descriptive statistics of the investigated variables after data from the previously constructed spreadsheet. Chi-square tests were performed to identify relationships among some analyzed variables: methods and benthos mobility, methods and research approach, year of publication and research approach, period and type of method, method and type of rock environment, method and climate zones and method and country of study. Three correspondence analysis were conducted based, respectively, on: i) mobility and methods, ii) methods and research approaches, and iii) year of publication and research approaches. The information regarding year of publication was divided into periods in order to balance data and transformed into a categorical variable with four levels depending on the time of publication: I (from 1979 to 2005), II (from 2006 to 2010), III (from 2011 to 2014) and
IV (from 2015 to 2018). All analyzes were performed in R (R Core Development Team, 2017) and in Excel®. A map with the relative frequency of published papers per studied country were constructed in Excel®.
3. Results
A total of 198scientific papers were selected for analyzes based on our exclusion criteria (appendix 1). An increasing trend of number of published papers per year was found (Fig. 1), with production reaching its highest peak in 2014 (18 published papers). A study on echinoderms in Africa, published in the journal Marine Biology in 1979, was the oldest paper found in the databases (Sloan, 1979). The main approaches of studies about rocky benthic community were categorized as field experimental studies, followed by observational ones, studies on biodiversity, literature reviews and methodological studies (Fig. 2a).
Figure 1. Temporal trends in the number of published papers on rocky intertidal zoobenthos,
Regarding the studied taxa (Fig. 2b), Mollusca and Crustacea were the most studied ones, although there were also studies that contemplated ecological aspects of the entire benthic community as well as the zoobenthic community only, and biological interactions between two or more taxa. In relation to the environmental information of the studied areas, not all articles described the abiotic variables within the studied area (Fig. 3).Observational, experimental and biodiversity approaches have focused mainly on describing wave and tidal range conditions from the sampled area, while methodological approaches also described slope. The rock type of the studied area was described in less than 32% of the papers in each category of approaches.
A total of 12 types of methodologies were registered, but only nine were included in the analyzes (Table 1). Some methods showed great correlation with benthos mobility (X2, p<0.01): the most common methods for mobile benthos counting were quadrats and quadrats associated with transects (Fig. 4a). The most used methods in studies on sessile animals were percentage cover estimation in the field and photoquadrats for further count (Fig. 4b). Studies that used the same sampler to sessile and mobile animals (Fig. 4c) preferred quadrats, quadrats associated with transects and collection (inside a quadrat or by active search) of the animals. These relationships between the methodology and zoobenthic mobility are emphasized by the correspondence analysis at Figure 5a.
Figure 2: Percentage of published articles on benthic organisms of rocky intertidal ecosystems, from 1979 to
2018, considering a) research approaches and b) target taxa.
Correspondence analysis between methods and research approach (X2, p<0,001)
showed that methodological studies were associated with the usage of photoquadrats and with visual estimation of percentage cover for counting organisms (Fig. 5b). Observational studies used mainly belt transects, quadrats associated with transects and active search. Studies on biodiversity were associated with organisms’ collection and rock sampling, while experimental studies were mainly associated with the usage of quadrats and scraping.
Figure 3: Relative frequency of articles on benthic organisms of rocky intertidal ecosystems published between
Figure 4: Percentage of published articles surveying rocky intertidal benthic fauna, from 1979
to 2018, regarding type of used method and animals’ mobility. C
B A
Figure 5: Correspondence analysis diagrams showing ordination of: a) methods used for counting
zoobenthos and the type of animals’ mobility, b) methods and research approaches, and c) research approaches and period of study.
A
B
The relationship between the year of publication and the research approach (X2, p<0,05) was emphasized by the correspondence analyses (Fig. 5c). During the period I (from 1979 to 2005), there was a higher concentration of review studies and studies about biodiversity in comparison to the other periods. The periods II (from 2006 to 2010) and III (from 2011 to 2014) were related to studies on biodiversity, methodology and experiments, while the period IV (from 2015 to 2018) is mainly related to methodological and observational studies. Although experimental and observational studies were frequent in periods II and III and periods I and IV, respectively, these approaches were the only ones found during the entire time span (from 1979 to 2018). The experimental ones were the most frequent per year. Methodological studies were frequent only since 2006 and were the less studied type during the whole research period. There was no relationship between period and type of method (X2, p>0.05). For the entire period, including articles
that were published from 1979 to 2018, the most used methods were quadrats (alone or associated with transects) and visual estimation of percentage cover in the field (Fig. 6a).
Regarding the spatial relationships, the applied methods for quantifying macrozoobenthic organisms showed dependence with type of rock environment (X2, p = 0.04) and with the climate zones (X2, p=0.02), but no dependence with the country of study (X2, p = 0.33). Intertidal studies have mostly focused on hard bottom environments and rocky shores, while few studies were conducted on rocky reefs and boulders fields (Fig. 6b).
Concerning climate (Fig. 6c), studies have been more frequent in subtropical and temperate areas, followed by tropical, dry, boreal and polar ones. The countries with the highest publication percentage according to our search criteria were Chile (26 papers), Brazil (22 papers), Australia (19 papers) and United States of America (18 papers) (Fig. 7).
Figure 6: Percentage of published articles on benthic organisms of rocky intertidal ecosystems, from 1979 to
2018, considering a) used methods for assessing benthic fauna, b) type of environment and c) climate region where the study took place.
A
4. Discussion
This study highlighted that research on benthic organisms of rocky intertidal areas are mostly concentrated on hard bottom and rocky shores environments at temperate and subtropical climates. The most common methods for quantifying the benthic fauna were quadrats (alone or associated with transects) and visual estimation of percentage cover in the field, regardless of studied period. The method choice is mainly related to features of the studied organism, such as mobility. Mobile organisms are preferably counted inside quadrats, while sessile organisms are measured by percentage cover.
Some studies questioned the usage of traditional methodologies, such as transects. For instance, the Physiognomic Assessment of Hard Bottom Benthic Communities (Berchez et al., 2005; Ghilardi et al., 2008) has suggested a more efficient approach for rocky shores, based on landscape ecology theories. Nevertheless, this approach has been tested only on rocky shores, thus it should be tested other environments such as sandstone and biogenic reefs in order to confirm its efficiency.
Figure 7. Locations where studies on benthic organisms of rocky intertidal ecosystems were conducted
The increasing trend in publications from 1979 to April 2018 and the growth of experimental and observational studies reflect a rising interest in understanding processes and patterns of benthic ecology. It is also a consequence of the increase in the number of international partnerships (Moreno & Rocha, 2012). For instance, the long-term Census of Marine Life Program increased marine research effort worldwide during its execution between 2000 and 2010 (Longo & Amado-Filho, 2014).
Regardless of used method, most studies have been carried out at temperate and subtropical areas. Studies at tropical areas were less frequent and, generally, used the same methods of temperate and subtropical regions, although without prior testing. Tropical areas are supposed to present greater habitat and species diversities (Satyam & Thiruchitrambalam, 2018) and exhibit different climatic characteristics, which are known to be determinant factors of ecological patterns (Menge & Lubchenco, 1981). Thus, it is expected to study these areas with effectively tested methodologies.
Likewise, regardless of used method, we found a great number of studies on hard bottoms and on rocky shores (environments where the firsts studies of rocky bottom literature were conducted) comparing to other categories of environments. We highlight a lack of standardization of the terms used to characterize each category. The category hard bottom was the most frequently studied, probably because it was considered as a broad category for rocky environments in this study. Among the other categories, rocky shores stood out from the rocky reefs and boulders. Although we considered rocky shores only when this term was used by authors’, this terminology has been applied as a common term to define shores which present hard rocky material in general. This includes different types of rocky substrates (Satyam & Thiruchitrambalam, 2018), such as steep rocks, rocky platforms and boulders. It is also important to highlight that we restrict our search only to rocky reefs environments and did not include coral reefs. Despite presenting different features regarding formation and species composition, coral and rocky reefs are often considered as coral reef in some studies. This may have underestimated our results for “rocky reef” environments.
Rocky reefs were also found to be less studied. This might be because greater research efforts are indeed still necessary in this kind of environment. Although boulder fields occur throughout the world (Denn et al., 2018), we emphasize a gap of studies in these environments compared to studies in the other rock environments. This was already reported in 2004 (Grayson & Chapman, 2004). Boulders are important to be studied once they house an unique community, structured especially over small spatial scales,
presenting different organisms’ composition (Chapman, 2005) and abundance (Waller, 2013) when compared to communities on the upside of rocks.
The heterogeneity of hard bottoms and the lack of a specification of the used terms emphasize the need to describe the environmental features of the studied area in the papers. Only about 55% of the papers have described the wave conditions of the study area, and less than 45% have described tidal range, the substratum slope and rock type. These are important factors that influence the benthic communities’ composition and distribution in the environment, making previsions and patterns identification possible. Once factors are not described, it is not possible to know whether determined studies might be compared in ecological terms.
Regarding the most studied taxon, the Mollusca phylum is considered a good ecological and biological indicator. It has been used, for instance, as an environmental indicator for pollution (Velez et al., 2016), stress (Levin et al., 2002) and climate change (Saupe et al., 2014) and as an indicator taxon for biodiversity and conservation (Gladstone, 2002). Most benthic studies have focused on mollusks, once these animals have noticeable ecological importance, are very common and abundant on rocky intertidal ecosystems, have low mobility and are easier to identify when compared to other taxa (Smith, 2005).
The difference between the number of publications among the countries can be due to differences in the hard-bottom distribution along the world coast. Disproportional amounts financing research in each country might also be a reason for this. Furthermore, studies generally are concentrated where there are traditional researchers’ groups. For instance, in Brazil, where there is a great variety of hard bottoms (such as rocky shores, coral reefs, sandstone reefs and boulders), institutions and specialists on rocky shore environments are concentrated at the southeast coast, a subtropical area dominated by rocky shores. On the other hand, there are proportionately fewer studies at the northeast cost, which is a tropical area dominated by sandstone reef (Ghilardi et al., 2008; Coutinho et al., 2016). This highlights the need for studies in other environments.
In order to standardize terms for rocky environments we propose the following nomenclatures to each condition: “rocky coast” – a coastal zone that is mainly composed of rock, regardless its composition and geological settings (Davis Jr & Fitzgerald, 2004); “hard bottom” - a generic name for rocky coastal environments (Bianchi et al, 2004), also including a variety of types occurring together; “rocky shore” - a name to coastal intertidal rock outcrops that occurs at the transition area between land and sea, which can extend
many meters above and below the sea level (Satyam & Thiruchitrambalam, 2018; Moreno & Rocha, 2012); “rocky reef” – inshore rocky outcrops that generally occur in shallow water (intertidal or infralittoral zones) and may vary in size and shape (Davis Jr & Fitzgerald, 2004; Langmead et al., 2008); “boulders” – a loose rock mass with more than 256 mm of diameter (Wentworth, 1922); an accumulation of boulders in an area consists of a “boulder field”, that may also include some cobble, which are smaller than 256 mm. We also suggest that the widely applied methodologies to be tested in the less contemplated environments until now, such as reefs and boulders in tropical areas.
Acknowledgements - This study was financed in part by the Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. We
thank professors from the Post Graduate Program in Ecology - Federal University of Rio Grande do Norte (UFRN) for helping with useful discussions. We also thank Matheus Lisboa Nobre da Silva for providing support in mapping.
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