UNIVERSIDADE FEDERAL DE PERNAMBUCO
CENTRO DE TECNOLOGIA E GEOCIÊNCIAS
DEPARTAMENTO DE OCEANOGRAFIA
Felipe Monteiro Gomes de Mattos
Uso de habitat e padrões comportamentais do peixe Stegastes
fuscus nos recifes costeiros de Porto de Galinhas (PE)
RECIFE
2016
Felipe Monteiro Gomes de Mattos
Uso de habitat e padrões comportamentais do peixe Stegastes
fuscus nos recifes costeiros de Porto de Galinhas (PE)
Orientadora: Profa. Dra. Maria Elisabeth de Araújo
Dissertação apresentada à Coordenação do Programa de pós-graduação em Oceanografia da Universidade Federal de Pernambuco, como um dos requisitos para a obtenção do título de Mestre em Ciências, na área de Oceanografia Biológica.
RECIFE
2016
Catalogação na fonte
Bibliotecária Valdicea Alves, CRB-4 / 1260
M435u
Mattos, Felipe Monteiro Gomes de.Uso de habitat e padrões comportamentais do peixe Stegastes fuscus nos recifes costeiros de Porto de Galinhas (PE) / Felipe Monteiro Gomes de Mattos - 2016.
87 folhas, Il., e Tabs.
Orientadora: Profa. Dra. Maria Elisabeth de Araújo.
Dissertação (Mestrado) – Universidade Federal de Pernambuco. CTG. Programa de Pós-Graduação em Oceanografia, 2016.
Inclui Referências.
1. Oceanografia. 2. Comportamento de peixes recifais. 3. Espécie Stegastes fuscus. 4. Montastrea sp. I. Araújo, Maria Elisabeth de(.Orientadora). II. Título.
UFPE
Felipe Monteiro Gomes de Mattos
Uso de habitat e padrões comportamentais do peixe Stegastes
fuscus nos recifes costeiros de Porto de Galinhas (PE)
Dissertação apresentada à Coordenação do Programa de pós-graduação em Oceanografia da Universidade Federal de Pernambuco, como um dos requisitos para a obtenção do título de Mestre em Ciências, na área de Oceanografia Biológica.
Apresentado e aprovada pela banca examinadora em: 31/05/2016
_____________________________________
Profa. Dra. Maria Elisabeth De Araújo (Orientadora)
Departamento de Oceanografia – UFPE
_____________________________________
Profa. Dra. Beatrice Padovani Ferreira (Membro Interno)
Departamento de Oceanografia – UFPE
_____________________________________
Prof. Dr. João Lucas Leão Feitosa (Membro Externo)
Departamento de Zoologia - UFPE
_____________________________________
Profa. Dra. Caroline Vieira Feitosa (Suplente)
Universidade Federal do Ceará - UFC
_____________________________________
Prof. Dr. José Souto Rosa Filho (Suplente)
Departamento de Oceanografia – UFP
AGRADECIMENTOS
Em primeiro lugar agradeço à Terra, e ao mar. Pois sempre nos esquecemos de agradecer a eles.
A toda minha família que sempre acreditou em mim, sempre me apoiou e soube que eu rumaria por este caminho. Principalmente aos meus pais, que não só me apoiaram como me colocaram nesta área desde pequeno. Graças a eles, e os constantes documentários, hoje realizo o sonho que tive desde que me lembro, seguindo os passos do meu pai, cursando o mesmo mestrado que ele.
Agradeço à minha grande orientadora Maria Elisabeth de Araújo, por tudo que me ensinou nestes anos, pela paciência, atenção, confiança e toda a orientação que tornou possível este trabalho. Mas acima de tudo, pela amizade que só se fortaleceu. Obrigado Beth.
Aos membros da banca examinadora, Profa. Dra. Beatrice Ferreira, e futuro Professor Dr. João Lucas Feitosa, Profa. Dra. Caroline Feitosa e Dr. José Souto, por aceitarem o convite e pelas contribuições.
Ao meu namorado, Davi, pela paciência em tempos de dedicação exclusiva ao trabalho. Por me apoiar e me animar sempre que precisei. E pelos desenhos, sem eles o artigo do Etograma não teria saído.
A toda equipe de amigos e pesquisadores do Grupo de Ictiologia Marinha Tropical (IMAT), Cabelo, Daniel, Walter, Danise, Carol, Zé, Jaque, Rafael Dantas e Rafael Bispo, Ályssa, Nicole, Demétrio, Vinny, Henrique, Sidney. A Felipe Bastos. Em especial aos meus companheiros que me ajudaram em campo, Cabelo, Daniel, Rafael Dantas, Rafael Bispo, Bárbara, Patrícia, Carol, meu pai e principalmente Walter, que nunca me negou um auxilio.
Às Professoras Beatrice e Beth pela oportunidade de pesquisa na Universidad de Murcia, Espanha, participando de um projeto internacional. Ao professor Jose Charton por todo o amparo e auxilio que me ofereceu durante minhas duas estadias em Murcia. Aos integrantes do Grupo de Ecología y Conservación Marina, que me auxiliaram na execução do projeto, em especial para Ramón, Pereñiguez, Antonio e Gabi, pela ajuda em campo.
Aos amigos de turma do mestrado e Oceanografia, especialmente Cíntia, Hedyane e Walter.
Aos professores e funcionários do Departamento de Oceanografia da UFPE, em especial à secretária da pós-graduação Myrna Lins, sempre muito solícita com os alunos do departamento.
Ao Programa de Pós-Graduação em Oceanografia por todo apoio fornecido, ao CNPq pela concessão da bolsa de mestrado.
Sumário
Lista de Figuras 7
Lista de Tabelas
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INTRODUÇÃO GERAL
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Capítulo 1
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Etograma e classificação comportamental de Stegastes fuscus (Pomacentridae) nos recifes costeiros de Porto de Galinhas (Brasil) 13
INTRODUCTION 15
METHODOLOGY 16
RESULTS 17
DISCUSSION 26
Capítulo 2
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Uso de habitat e comportamento agonístico de Stegastes fuscus em condições naturais e experimentais (in loco) nos recifes costeiros de Porto de Galinhas (PE) 44
INTRODUÇÃO 46
ÁREA DE ESTUDO 48
51 Em cada um dos pontos estudados foram feitos 3 censos visuais, estimando-se o número total de indivíduos da espécie estudada, a fim de obter a densidade total de
S. fuscus por ponto de estudo. 51
METODOLOGIA 52
DISCUSSÃO 64
REFERÊNCIAS BIBLIOGRÁFICAS 75
CONSIDERAÇÕES FINAIS 84
LISTA DE FIGURAS
FIGURA 1: RECIFES DA PRAIA DE PORTO DE GALINHAS COM EVIDÊNCIA PARA OS PONTOS AMOSTRAIS. ... 48 FIGURA 2: CARACTERÍSTICAS AMBIENTAIS DO PONTO DO FUNDO RECIFAL (P1) EM PORTO DE
GALINHAS (PE). ... 49 FIGURA 3: CARACTERÍSTICAS AMBIENTAIS DO PONTO DA PRAIA (P2) EM PORTO DE GALINHAS (PE). 50 FIGURA 4: CARACTERÍSTICAS AMBIENTAS DO PONTO DO TOPO RECIFAL (P3) EM PORTO DE GALINHAS (PE). ... 51 FIGURA 5: MARCADORES (RETÂNGULOS) E TRENA UTILIZADOS NA MEDIÇÃO DE TERRITÓRIOS DE S.
FUSCUS EM PORTO DE GALINHAS (PE). FOTO DO AUTOR. ... 53 FIGURA 6: EXEMPLAR ADULTO DE STEGASTES FUSCUS REGISTRADO EM PORTO DE GALINHAS (PE) . 55 FIGURA 7: DENSIDADES DE S. FUSCUS POR M² ENTRE OS PONTOS AMOSTRAIS EM PORTO DE GALINHAS
(PE). LINHAS VERTICAIS INDICAM O DESVIO PADRÃO. LINHAS VERTICAIS INDICAM DESVIO
PADRÃO. LETRAS DIFERENTES INDICAM DIFERENÇA SIGNIFICATIVA. ... 56 FIGURA 8: COMPARAÇÃO ENTRE AS SEGUINTES VARIÁVEIS NOS PONTOS AMOSTRADOS: ÁREAS DOS
TERRITÓRIOS (A) E COMPRIMENTOS DE S. FUSCUS (B), NÚMERO DE LOCAS POR TERRITÓRIO (C), PORCENTAGEM DE COBERTURA ALGAL NO TERRITÓRIO (D). CIRCULOS VAZIOS REPRESENTAM OS VALORES DISCREPANTES . LETRAS DIFERENTES REPRESENTAM DIFERENÇA SIGNIFICATIVA. ... 57 FIGURA 9: CORRELAÇÕES ENTRE OS COMPRIMENTOS DE INDIVÍDUOS DE S. FUSCUS E AS ÁREAS DO
TERRITÓRIO (A), A PORCENTAGEM DE COBERTURA (B) E O NÚMERO DE LOCAS NO TERRITÓRIO (C). ... 58 FIGURA 10: NÚMERO MÉDIO DE INTERAÇÕES AGONÍSTICAS POR AMOSTRAGEM (5 MIN) (A) E NÚMERO
MÉDIO DE ATOS ALIMENTARES POR AMOSTRAGEM (B) NOS PONTOS DE ESTUDO. CÍRCULOS VAZIOS E ASTERISCO MOSTRAM OS OUTLIERS. ... 59 FIGURA 11: DISTRIBUIÇÃO POR PERÍODO DO DIA. TAXA DE ALIMENTAÇÃO (A). INTERAÇÕES
AGONÍSTICAS EXERCIDAS POR S. FUSCUS DURANTE AS OBSERVAÇÕES (5MIN) (B) ... 61 FIGURA 12: CORRELAÇÃO ENTRE O NÚMERO DE INTERAÇÕES AGONÍSTICAS REALIZADAS POR S.
FUSCUS E A TAXA DE ALIMENTAÇÃO INDIVIDUAL A CADA 5MIN (A) E AS VARIAÇÕES NA TAXA DE ALIMENTAÇÃO (POR MINUTO) (B). LETRAS DIFERENTES INDICAM DIFERENÇA SIGNIFICATIVA. ... 61 FIGURA 13: CORRELAÇÃO ENTRE OS COMPRIMENTOS TOTAIS DOS PEIXES DE STEGASTES FUSCUS E A
LISTA DE TABELAS
TABELA 1: FREQUÊNCIAS RELATIVAS DOS COMPRIMENTOS TOTAIS DE S. FUSCUS OBSERVADOS EM
PORTO DE GALINHAS (PE) 55
TABELA 2: NÚMERO DE INTERAÇÕES AGONÍSTICAS INTRAESPECÍFICAS E INTERESPECÍFICAS
EXERCIDAS POR PEIXES DE S. FUSCUS NOS TRÊS PONTOS DE ESTUDO. 59 TABELA 3: NÚMERO DE INTERAÇÕES AGONÍSTICAS INTERESPECÍFICAS E INTRAESPECÍFICAS ENTRE AS
DIFERENTES POSTURAS APRESENTADAS POR INDIVÍDUOS DE STEGASTES FUSCUS EM PORTO DE
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RESUMONo Brasil os estudos um dos principais focos dos estudos etológicos com peixes recifais é a espécie Stegastes fuscus (Cuvier, 1830); a mais representativa em abundância e frequência nos recifes rasos de Pernambuco. Neste contexto, este estudo teve por objetivos; (1) descrever o repertório comportamental de S. fuscus, criando etogramas descritivos e ilustrados com todos os comportamentos observados, e (2) analisar o comportamento de defesa territorial da espécie. Dez horas de observações preliminares e 68h de observações ad libitum e animal focal, e 20h de experimento in situ foram realizadas nos recifes naturais da praia de Porto de Galinhas, Ipojuca. Três áreas foram escolhias por suas características diferentes: (1) ponto do Fundo Recifal, (2) ponto da Praia, (3) ponto do Topo Recifal. As observações geraram um etograma com nove categorias comportamentais motoras: natação, alimentação, defecação, limpeza de território, limpeza do corpo, saída do território, interação social, abrigo, agonístico; e duas sonoras: pop e burr. O ponto do fundo recifal foi o de menor densidade de S. fuscus, com 0,3 peixes/m², e onde se encontraram os maiores territórios (1,45 m² em média). Os maiores valores de densidade, cobertura e locas foram encontrados no ponto da Palythoa. As regressões obtidas para o comprimento dos indivíduos e as variáveis avaliadas mostraram tendência para a relação entre o comprimento dos indivíduos e o número de locas, no ponto do fundo. Provavelmente neste pontoo mais importante para os peixes é a presença de abrigo. Foram registrados peixes afastando-se quase 10 m de seus territórios. Pode-se afirmar que área de vida da espécie está associada ao ambiente ao redor. A taxa de alimentação diminuiu conforme aumentou o número de interações agonística. O número de atos alimentares por minuto só diminuiu de forma significativa quando houve mais de dois atos agonísticos. Este ponto representa um limiar que define até onde é vantajoso para o peixe manter a defesa de territórios. Durante as observações experimentaisforam identificados sete padrões de reação aos objetos. São elas: evitar, não interagir, observar e sair, observar e aproximar-se aos poucos, observar e examinar, observar e ameaçar com display, e observar e expulsar. As diferentes respostas demonstram como o comportamento territorialista da espécie está tão associado às variações individuais e às ambientais. O presente estudo identificou três padrões comportamentais que não foram descritos anteriormente em estudos comportamentais com a família Pomacentridae.
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ABSTRACTIn Brazil the major focus of ethological studies on reef fishes is Stegastes fuscus (Cuvier, 1830); the most representative fish species in abundance and frequency in the shallow reefs of Pernambuco. In this context, this study aimed; (1) describe the behavioral repertoire of S. fuscus, creating descriptive and illustrated ethograms with all the observed behaviors, and (2) to analyze the territorial defense behavior of the species. Ten hours of preliminary observations, 68h of ad libitum and focal animal observations and 20h of in situ experiment were performed on the natural reefs of Porto de Galinhas, Ipojuca. Three areas were chosen by their different characteristics: (1) Reef bottom site, (2) Beach site, (3) Reef flat site. The observations resulted in an ethogram with nine motor behavioral categories: swimming, feeding, defecation, territory maintenance, chafe, leaving the territory, social interaction, shelter antagonistic; and 2 sound: pop and burr. The point of the reef bottom has the lowest density of S. fuscus, with 0.3 fish / m², and where the larger territories were found (1.45 m² on average). The highest density, coverage and hollows values were found at the reef flat. The regressions obtained for the length of the individuals and the variables evaluated tended to find a relationship between the length of individuals and the number of hollows the reef bottom. Probably it’s more important for the fish the presence of shelter. Fish were recorded almost 10 m away of their territories. The home range of the species is associated with the environment around. The feed rate decreased as the number of agonistic interactions increased. The number of feeding acts per minute only decreased significantly when there were more than two agonistic actions per minute. This point is a threshold that defines how far it is advantageous for the fish to keep the protection areas. During the experiment it were identified seven reaction patterns to objects. They are: prevent, not interact, observe and leave, observe and approach slowly, observe and examine, observe and frontal display, and observe and leave. The different responses demonstrate how territorial behavior of the species is associated with individual and environmental variations. This study identified three behavioral patterns that have not been described previously in behavioral studies with the Pomacentridae family.
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INTRODUÇÃO GERAL
O estudo do comportamento animal é um dos mais importantes meios para compreender as interações entre animal e ambiente. A etologia é considerada um ramo da ecologia animal que trata dos padrões comportamentais tanto em nível de população como de indivíduo (Altmann, 1974; Dawkins, 2007; Del-Claro, 2004; Souto, 2003). A etologia moderna teve seu início na década de 50 (Dawkins, 2007; Tinbergen, 2009), quando se buscou primariamente descrever as posturas comportamentais e seus padrões através de ações realizadas pelos animais, para tentar entender os mecanismos que as causam, assim como a evolução destes mecanismos (Gould, 1982).
As primeiras pesquisas etológicas com peixes recifais datam do final da década de 50 e início dos 60 (Barlow, 1963; Davenport e Norris, 1958; Emery, 1968; Myrberg et al., 1967), possibilitadas pela facilitação do acesso a equipamentos de mergulho autônomo. No Brasil os estudos etológicos desses peixes tiveram início nos anos 80, sendo os trabalhos de Sazima os pioneiros no país (Sazima, 1986; Sazima e Uieda, 1980). As pesquisas descritivas nos recifes brasileiros evidenciaram a complexidade de comportamentos e hábitos alimentares, descrevendo padrões limpadores, lepidofágicos e seguidores (Francini–Filho et al., 2000; Sazima et al., 2006, 1999; Sazima e Uieda, 1980).
A partir do final dos anos 90, peixes da família Pomacentridae tornaram-se alvo do maior número de estudos comportamentais nos recifes de corais brasileiros (Ferreira et al., 1998; Souza et al., 2011), devido principalmente ao típico comportamento territorial adotado pelos seus representantes (Bessa e Sabino, 2012; Jones, 2005). Espécies dessa família defendem territórios de forma permanente em territórios alimentares (Stegastes spp., Microspathodon spp. Parma spp.), defesa de refúgios e formação de ninhos (Amphiprion spp. Dascyllus spp.) ou de forma sazonal em sistemas reprodutivos poligínicos a exemplo de Chromis spp.; Abudefduf spp. (Davenport e Norris, 1958; Albrecht, 1969; Fishelson, 1970; Sale, 1971; Norman and Jones, 1984; Menegatti et al., 2003; Picciulin et al., 2004; Sikkel e Kramer, 2006; Barneche et al., 2008; Bessa e Sabino, 2012).
Quatro gêneros pertencentes à família Pomacentridae são encontrados na província brasileira: Abudefduf, Chromis, Microspathodon e Stegastes. Três espécies representam este último gênero: Stegastes fuscus (Cuvier, 1830), Stegastes pictus (Castelnau, 1855), Stegastes variabilis (Castelnau, 1855). Consideradas de hábito
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alimentar herbívoro, estas espécies são conhecidas pelo comportamento territorial e por manter uma diversidade e produtividade algal maior em seus territórios quando comparados às áreas adjacentes (Feitosa et al, 2012; Hixon e Brostoff, 1996). Espécies deste gênero defendem territórios permanentes, excluindo peixes conespecíficos e heteroespecíficos ademais de invertebrados herbívoros como Pagurus sp. e ouriços, promovendo um crescimento mais abundante e diverso de algas em seus territórios (Itzkowitz, 1990; ; Hata e Kato, 2004; Osório et al., 2006Nos recifes do litoral nordestino, a espécie S. fuscus é a mais representativa considerando abundância e frequência de observações. Tem distribuição restrita à província brasileira, sendo encontrada do Ceará a Santa Catarina (Ferreira et al., 2004; Canan, 2007). Habitam áreas rasas até 15 metros de profundidade, formando seus territórios principalmente na crista e no topo recifal (Ferreira et al., 1995). Apesar de ser mais comum na crista das bancadas recifais, S. fuscus pode ser encontrada nas paredes e em manchas recifais com baixa cobertura de algas. Feitosa e colaboradores (2012) observaram que esta espécie controla o crescimento de algas, mantendo-as em estágios de sucessão finais, mantendo a dominância de algas calcáreas articuladas. Enquanto Ceccarelli, (2007) notou que, em seus territórios, S. fuscus mantêm maior riqueza e diversidade de invertebrados. Por tais motivos, estudos consideram S. fuscus como espécie chave para muitos recifes brasileiros, incluindo aqueles que se localizam na região nordeste oriental (Ceccarelli et al., 2005, 2001; Aued, 2012; Feitosa et al, 2012).
Por tanto, observar e descrever o comportamento da espécie, para além da ecologia alimentar e territorial, trará maior informação sobre as relações entre habitat, território e animal, permitindo que respostas populacionais às variações ambientais sejam inferidas a partir dos padrões de mecanismos comportamentais da espécie; vários deles nunca antes descritos. A presente pesquisa teve por objetivos descrever o repertório comportamental de S. fuscus, criando etogramas descritivos e ilustrados para analisar o uso de habitat, delimitar o território dos espécimes observados com base nas relações intraespecíficas e interespecíficas.
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Capítulo 1
Etograma e classificação comportamental de
Stegastes fuscus (Pomacentridae) nos recifes costeiros de
Porto de Galinhas (Brasil)
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Ethogram and behavioural classification of Stegastes fuscus
(Pomacentridae) in Porto de Galinhas (Brazil) coastal reefs
Felipe. M.G. Mattosª*, Maria E. De Araújo ª
ªUniversidade Federal de Pernambuco, Departamento de Oceanografia, Recife, Brazil *Correspondence: Felipe Mattos, Departamento de Oceanografia, Universidade Federal de Pernambuco, Av. dos Reitores, Recife, Brazil.
E-mail address: felipemgmattos@hotmail.com
The behavioural patterns of animals are commonly grouped into ethograms. These are useful tools for better understanding and standardisation of terminologies in ethological studies. The first Brazilian work with reef fish’s behaviour began between the 70s and 80s. Since then a focus has been the territorial species Stegastes fuscus, due to their aggressive behaviour. The aim of this study was to describe the behavioural repertoire of S. fuscus, based on underwater observations, creating a descriptive and illustrated ethogram with all the observed behaviour. Eight hours of preliminary observations and 68 hours of observations ad libitum and focal animal were carried out on natural reefs of Porto de Galinhas, Ipojuca, Pernambuco, Brazil. Three areas were chosen for their different characteristics: one reef spot with two small patch reefs site 1 (reef bottom site), site 2 (shore site), and site 3 (reef flat site) was occupied by S. fuscus. The observations generated an ethogram with 9 motor behavioural categories: swimming, feeding, defecation, territory maintenance, chafe, leaving the territory, social interaction, shelter antagonistic; and 2 sound: pop and burr. The categories eating and agonistic behaviours were subdivided into distinguishable patterns. Most of the time fishes were actively "swimming". The most frequently recorded activity during observations was feeding. Specimens’ average length was similar to that previously observed in other studies. The behaviour described in this work as "leaving the territory", has no similar description in the previous literature studied, probably being the first time that such a category is described and discussed. Only the categories of chafe and defecation appear to have no connection with the territorial behaviour of the species. The behaviours herein registered are the first description for the whole behavioural repertoire of the species, comprising 3 new actions never before described for Pomacentridae.
Keywords: territorialism, dominant species, dusky damselfish, tropical beach, reef patches, herbivory
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INTRODUCTION
In Brazil, first records including reef fish behaviour into ethological research dated from the 70s and 80s, pioneered by Sazima and Uieda (1980) studies on reef fishes. Later, Sazima, (1986) makes a connection between coastal zones and wetland lakes habitats, by comparing feeding behaviours of fishes, finding similarities in fresh and salt waters niches. The first studies comprising the Stegastes genus date from the late 90s and early 2000s (Ferreira et al., 1998; Schwamborn and Ferreira, 2002). The delimitation of a habitat may be better evaluated if the fish species has a territoriality behaviour, as registered for Stegates fuscus (Cuvier, 1830), a species of Pomacentridae Family dominating the Pernambuco’s reefs (Ferreira et al., 1995, Araújo et al., in preparation).
Studies with Stegastes fuscus point it as key species on Brazilian reefs for carrying out maintenance of the diversity of algae inside their territories, keeping them in the final stages of ecological succession (Feitosa et al, 2012; Hixon and Brostoff, 1993, 1986). They are determinants in the structuring of a benthic community richer and more diverse in their territories. By changing the composition and amount of algae available in the environment, S. fuscus influences the zonation of coral and fish communities by modifying the behavior of the other herbivores, especially those of the Acanthuridae family and sub-family Scarinae (Hata et al., 2002; Jones, 2005; Menegatti et al. 2003; Souza et al. , 2011c).
The first Brazilian studies dealing with territorialism, agonistic and herbivory of S. fuscus were those of Ferreira et al., (1998) and Menegatti et al., (2012). This species is found in tropical and sub-tropical Brazilian reefs and rocky shores, inhabits shallow waters (up to 15 meters deep), colonizing and aggressively defending territories from 1 to 1.5 m² (Feitosa et al., 2012; Ferreira et al., 1995; Pacheco, 2008). But, for the territorialist behaviour to be beneficial as life strategy, the costs of defending an area should be outweighed by the benefits, either for reproduction or for feeding (Brown, 1964; Brown and Orians, 1970; Davies and Houston, 1981).
Research on feeding, fitness, and territorial behaviour comprising S. fuscus are now often found in the literature (Barneche et al., 2008; Souza et al., 2011, 2007). Nevertheless, there is a gap regarding the categorization of behavioural acts, and especially on the standardization of the used terminology. Ethograms are the basis to descriptive ethology (Dawkins, 2007; Souto et al., 2009; Tinbergen, 2009), allowing observers to clearly convey the range and structure of actions developed by animals,
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and provide standardized terminology to facilitate the comparison of results. Also, the in deep knowledge of a key-species behaviour brings important information for the studies of brazilian reefs and reef-fish communities, by allowing us to understand what is their natural behaviour, and what every action means. The main goal of the research is to describe, classify and represent behavioural patterns of S. fuscus in an ethogram’s descriptive form.METHODOLOGY
The research was conducted at Porto de Galinhas beach reefs formations (8°30'23 "S35°00'19"W), State of Pernambuco, Northeast Region of Brazil. The observations were made during summer (from December to April) of 2014-2015 and 2015-2016. During these months the water has the best conditions for fish observations. From May to August (wind months and rainy season), it was not possible to continue observations, due to poor visibility conditions (less than two meters), and all procedures were suspended. Observations were conducted between 07: 00h and 13: 00h, in order to avoid influence of reproductive behavior, which takes place in luscus fuscus.
For data collection, snorkelling was used in shallow waters areas (0-2 m), while SCUBA in deeper ones, up to 6 meters. Observations were taken during low tides (0.0m to 0.6m), when depths were measured. Through the research period, a single lens camera Canon Powershot G16 underwater case were used for general records of the study area, whilst an action camera, Go Pro 4, was chosen for photographic records and witness the developed performances and behaviour of Stegastes fuscus.
Three different sites were used for the observations, identified for local distinct characteristics: site 1 (reef bottom site), site 2 (shore site), and site 3 (reef flat site). All those areas are located in patch reefs and separated from the main reef, seeking the least possible interferences from other fish populations, ensuring the presence of the same fish in the studied areas. Site 1 (area of approximately 140m² and maximum depth of 6m) is the deepest among the three characterized by a reef bottom environment. Site 2 (area of 140 m², and 2m deep), where several nearby patch reefs are found also surrounded by sand, was the closest one to the shore. Site 3 was the larger patch reef (area 340 m², and 1.5 m deep), isolated from the main reef, and characterized by several colonies of Palythoa caribeorum, typical of a reef flat.
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All observations were made by the same diver using the ad libitum and focal animal methods as described in Altmann (1974). The focal animal method is recommended for observing detailed behaviour patterns of individuals. The ad libitum method consists on a free observation in which the researcher registers any possible behaviour that might seem important. In total, eight hours of trial observations were made, during December of 2014 and January of 2015. The observed behavioural patterns were listed and plotted on a cumulative curve until reaching the asymptote. Later, 47 hours of field observations were taken, being and 10 hours of focal-animal and 37 hours of ad libitum. Each sample taken by focal-animal method lasted 5 minutes, resulting in 600 minutes of acts sampled through this methodology. In each one of the samples, all acts performed by the specimen were recorded, in order to achieve a more detailed analysis.The sound patterns observed in this study, produced by S. fuscus, have written records through notes and video recordings made with the Canon G16 and GoPro cameras 4. This phase of the work is still in progress, and more detailed data are in collection process. The results described below are derived from primary data collected through ad libitum observations and analysis of the videos.
At the end of the data collection, our records were compared with those found in Fishelson (1970) and Myrberg (1972), followed by the choice of the best terminology to describe the variety of behaviours observed. Behaviours terms used and described in earlier work for Stegastes genus were kept, in order to maintain unifying descriptions, facilitating the comparison and communication between ethological studies.
RESULTS
Twenty campaigns were carried out, including four pilots, spending between 2 and 3 hours of diving in each of them, with visual and video-photographic records, the horizontal visibility ranged from 2 to 10 meters. In total, 90 individuals of the target species, distinguished by their different territories, were followed and had their behaviour recorded by the focal animal method. The average estimated length of the registered specimens was approximately 10 cm, and they spent, on average, 7 seconds per minute housed in hollows or cracks.
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Behavioural patterns observed in Porto de Galinhas resulted in nine main different motor categories: swimming, feeding, defecation, territory maintenance, chafe, leaving the territory, social interaction, shelter, agonistic. Two of them (feeding and agonistic) were divided into clearly distinguishable behavioural units. The categories and behavioural units Swimming, Feeding, Nip, Spitting-out material, Chafe, Agonistic, Display and Chase, were extracted from (Myrberg, 1972); the units Bite and Threat were based on (Fishelson, 1970) work. Behaviours with no correspondence in literature involving Pomacentridae were here designated based on other ethological fish studies. The behaviours of swimming and feeding are represented in Plate I. The categories of defecation to shelter are in Plate II. The agonistic patterns are represented in Plate III.A) Swimming:
It refers the behaviour of moving freely in the water, within the limits of the territory. During the act of swimming, fish does not interact with the substrate or with other animals, remaining a few centimetres above the substrate. Swimming can be displacements at different speed within the territory, remarkably slowly, or may consist in remaining static in the water column. The swimming pattern of Stegastes fuscus is characterized by using a combination of acts of the caudal fin, for propulsion, and the pectoral fins, for manoeuvring or remaining on static. B) Feeding:
Represents any action developed by the fish to feed through bites, usually on algae (nip, nibbling in torn portions, lateral tug, chewing, spitting-out material), followed by the ingestion of material, evidenced by movements of the mouth and operculum, after the act of biting. Sometimes this behaviour may be preceded by a long inspection of the substrate.
B.1) Nip:
Quick biting movements, taking small pieces of algae into his mouth. Hereby, the fish is positioned a few millimetres from the substrate, remaining on the water column, using the pectoral fins, keeping the head sloped slightly downwards and the mouth pointed at the target, and the nip is most often characterized by one single bite. The specimen then swims over, nibbling the substrate and eating a small piece of organic material.
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This behaviour is observed when the torn piece of food (algae) is too large to be snapped at once. To tear the algae in pieces the fish swims slowly near the substrate, using the pectoral fins, with the head tilted toward the target (bite) point, the fish pulls a big piece of algae and nibbles while it remains floating in the water column near its territory. Usually the algae piece is bitted from 3 to 6 times.B.3) Lateral tug:
During this behaviour, the fish oscillates the body laterally and accelerates at great speed using the caudal fin. The resulting impulse of this movement gives to the fish a chance to reach the food with much higher energy than a “nip”. Then the animal completes the act with a strong tug on algae, leading to its mouth a larger portion of food in relation to nipping. Fishes that have been sighted doing this behaviour had only one large bite from the substrate. In the eyes of a less careful observer this action can be confused with an agonistic nature act.
B.4) Chewing:
During this act, the fish performs various movements to open and close the jaws and operculum, after accumulating some food in its mouth. This behaviour is usually started after 3 or 4 followed bites directed to calcareous algae, especially Jania spp.. Such behaviour was mostly often observed in fishes from areas 1 and 2, after bites also directed to the sandy substrate.
B.5) Spitting-out:
This behaviour is directly associated and always succeeding the act of chewing. Fishes expels through the mouth or operculum the excess of material from their bites. Although mostly expelling is through the mouth, materials can be also expelled through the operculum when the fish nibbles on a thin substrate.
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C) Defecation:It includes all action of faeces elimination. Act rarely observed in this study, it generally occurs either inside or outside the territorial limits. In this behaviour fishes tend to swim 30 to 50 centimetres above the substrate within or outside the territorial limits, where they release their waste, without looking for any specific location where to defecate.
D) Territory maintenance:
Series of acts which S. fuscus performs to maintain it’s territory appearance. Can be either to prune and improve the cultivation of algae or simply to clean it, withdraw some object, which apparently bothers the fish. The cleanness was seen on several occasions, when the fish removed some rock or hollow shell of its territory, with no other clear reason.
E) Chafe:
To body cleansing, fishes swim near hard surfaces, and with one movement rubs its body laterally, from head to tail, against a hard surface like Jania sp., while performing rapid small undulations with the posterior region of the body. Those movements are held with intention to withdraw from the body surface potential parasites, particles that can cause illness or that simply annoy the animal.
F) Leaving the territory:
Refers to the act performed by the fish moving away some centimetres to several meters outside the limits of its territory, interacting with the surrounding environment, without being threatened by any other individual. Sometimes this behaviour was linked to social interaction, although at 80% of the times this behaviour relates with the fish apparent intention of feeding beyond territorial limits, often in neighbouring territories, or sometimes associated with social interaction.
G) Social interaction:
Behaviour in which one or more individuals of the studied species physically interacts, joining pairs or small groups, without any act of agonistic nature. Herein the fishes swims side by side, when small interactions occurs, such as a contact between pectoral fins or/and a quick touch of a fish's pectoral fin with
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another fish's body lateral. Stegastes fuscus, who live in closer territories, usually form groups of 2 to 6 individuals.H) Shelter:
Encompasses all acts performed by S. fuscus when remaining 5 or more seconds inside holes in their territories. Usually this position is held when the fish feels apparently threatened by some other fishes, mainly conspecifics, although on several occasions specimens were observed entering and staying in a shelter without a clear threat. The expended time was chosen as a standard to categorize the use of shelters. Since the observer could not see what the fish was doing inside the hole.
I) Agonistic:
Behaviour consisting of an act or a series of clearly aggressive actions directed to some other animal (included divers) or any object that arrive in its territory. This behaviour is mainly linked to the defence against invaders fishes that enter others territories limits, in order to drive them off. There are six different behaviour postures here identified: display, threat assault, persecution, bite and mouth fighting.
I.1) Display: It consists in showing the body, face to face or sideways, in order to intimidate the intruder. This behaviour is usually the first to be held by the fish, having as main objective frighten the opponent, avoiding other acts with greater energy expenditure. The fish can adopt the front or side threat, taking those postures by opening fins in order to show greater body surface, thus appearing larger to others animals. The frontal display is accompanied by expansion of the pelvic, pectoral and dorsal fins, as well as opening the mouth. The lateral threat is held with the expansion of the dorsal, anal, and pelvic fins. I.2) Charge: A very quick behaviour, usually performed in fractions of a second, in which Stegastes fuscus accelerates toward an intruder propelled by rapid and aggressive movements of the caudal fin. Despite the charge, the attacker does not actually touch or chase the attacked, changing the direction of swimming at the last moment and returning to the centre of the territory. This act is usually enough for most intruders to flee and leave the territorial limits of the defender.
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I.3) Chase: Behaviour in which S. fuscus chases any other fish, swimming at high speed, aiming at driving it off its territory limits. Being applied explosively, the pursuit is mainly short, lasting only 1 or 2 seconds, although sometimes it can reach more than 10 seconds. Persecution is promptly interrupted when the pursued fish is expelled from the territory or when it is no longer able to continue the pursuit. For instance, it occurs with small juvenile fishes that hide in little holes too small for an adult S. fuscus to reach. In those cases the defender gives up chasing.I.4) Bite: S. fuscus uses this act when the three behaviours above described were not efficient repelling intruders. In such a case, the fish bites the body of the intruders in order to cause damage. Typically, the fish takes a bite and moves away from the opponent, watching it and, if necessary, strike again. Those postures can be observed toward much larger fishes such as large carnivores including species of the Lutjanidae family, or even against divers. I.5) Mouth fighting: With wide open mouths, fishes can perform this act in two different ways, simply touching on each other mouths without any further action, or when there is a more intense fight, the fish pushes the opponents mouth, trying to dislocate the whole body of the other S. fuscus. This act is the rarest observed and is usually accompanied by one or more bites on the opponent's body.
I.6) Escape: A run away behaviour when suffering aggression from another S.
fuscus. In this act, the individual uses all the posterior half of the body, bending it’s body like an S, in order to escape from an attack. The action ends when the tracker gives up or when the fish pursued can reach a shelter.
The swimming behaviour is the act that fishes spent in most of their time, representing almost 30% of the total time sampled. This was the second most performed behaviour. The most frequently recorded activity during observations was feeding. Within this category, "nip" is the most common pattern. The "social interaction" with other individuals, and "territory cleaning" were the less observed behaviours in this study.
The most attacked trophic group was the invertebrate eaters, followed by herbivores. Fishes of the Epinephelus adscensionis, Cephalopholis fulva and
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Holocentrus adscensionis species where fully tolerated, having only one record of charge against C. fulva.Sounds
Two types of sounds were recorded during field data collection. The descriptions and the names below were based on similar sound patterns found in Myrberg (1972) described for Stegates partitus because so far no publications were found recording sound production for the studied species.
Pop: Sound from jaw movements, possibly produced by a mechanism connected to the mouth and swim bladder. Registered during agonistic encounters, the sounds are usually associated with the defence of territory before an attacker, being more common in intraspecific conflicts. Usually it occurs simultaneously during threats, but it can happen at the time that precedes the act of biting. Occurring as individual sound pulses, the recorded sounds were executed by the defender to the attacker and never in an opposite way.
Burr: Rarer sound recorded always and exclusively in the presence of other S. fuscus, associated with a standard swimming movement with rapid flow rate, waving quickly the anal and caudal fins. It is characterized by several sound pulses like a roar, can be heard at least 5 meters apart, and apparently concerning social interactions, this sound can be a aggressive sign, or also an act of communication between neighbouring fishes. The collected data are still insufficient to determine whether this sound is produced agonistically, as part of territory defence, or have non-aggressive communication function. Overall, the sound was produced within the territorial limits, directed to the fish that have neighbouring territories. But it was possible to observe individuals who sometimes leave their territories, from 3 to 5 meters away, and then producing the burr sound in front of several other conspecifics territories distant to their own.
DISCUSSION
Many previous researches described fish behaviours on reef environments (Bshary and Schäffer, 2002; Gibran et al., 2004; Myrberg jr and Riggio, 1985; Sazima et al., 2006), some of them using species from the family Pomacentridae (Emery, 1968; Fishelson, 1970; Myrberg, 1972; Hourigan, 1986), but only Myrberg (1972) produced a
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complete ethogram of the categories observed in Stegastes partitus (Poey, 1868), and no previous study aimed to observe all S. fuscus behaviours. This research is the first attempt to classify and analyse their patterns producing a descriptive and illustrated ethogram. When comparing the results obtained with Myrberg (1972), there are clear similarities among the patterns found for these two species. Some categories, such as "exiting", "territory cleaning", "social interaction", and "output territory" had never been described for S. fuscus, but it is likely that other fish of the genus Stegastes have similar patterns of variable intensities and frequencies to be studied.Motor Patterns
The predominantly caudal swimming present on Stegastes fuscus follows the approach described to the genus (Emery, 1968; Myrberg, 1972). Its locomotion differs from the pattern observed in the most Pomacentridae family species, such as those belonging to the genus Chromis, Abudefduf and Amphiprion which mainly use the pectoral fins for swimming, reserving the caudal fin for emergency swimming in escaping situations (Myrberg et al., 1967; Fishelson, 1970; Russell, 1971; Prappas et al., 1991). Current observations on S. fuscus show various postures in which the pectoral fin has been widely used, mainly during feeding behaviours (nip and nibbling in torn pieces), agonistics (display and mouth fighting) and shelter, when the fish needs to remain relatively static.
Although several studies explored territorialism of S. fuscus (Aued, 2012; Ceccarelli et al., 2005, 2001; Menegatti et al., 2003; Souza et al., 2011c), none of them seems to notice the importance of time spent swimming. In fact, additionally to aggressive interactions among the necessary actions to territory maintenance against invaders, are the chemical (olfactory) and visual signals (Brown and Orians, 1970; Giuggioli et al., 2011). Therefore, even when no agonistic behaviour is registered, the simple fact of swimming in its territory for most of the time may indicate an act of marking territory.
The acts of chewing and expelling sediment show that the species is food-selective, eating red filamentous algae than calcareous, like Jania sp., dominant in S. fuscus territories (Ferreira et al., 1998; Menegatti et al., 2003). These observations explain why, despite having a high rate of nibbling in calcareous algae, this kind of feeding resource represents only 25% of the algae portion in S. fuscus stomachs (Ferreira et al., 1998). It is possible that S. fuscus specimens avoid excessive intake of calcareous material, as calcium carbonate acts as a buffer to their stomach’s pH
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(Lobel, 1981). While studying the feeding behaviour of that species, Ferreira (1998) noticed that these fishes have the lowest stomach’s pH among herbivorous fishes. This two combined information would explain why often pieces of Jania sp. calcareous algae are ingested and then expelled, as described in the act "spitting out".It is important to emphasize the need to standardize the terms used in behavioural studies with S. fuscus. In their work of foraging, Menegatti et al. (2003) refers to any feeding act as investee (lunge), while Aued (2012) does the same generalization using the term bite. Moreover, Bessa and Sabino (2012) studying 3 damselfish species (S. fuscus, C. multilineata and A. saxatilis) used the term feeding to represent all behavioural patterns inside this category.
In this study, there were few records related to waste elimination, as well, few publications refer such behaviour to Stegastes spp. (Lassuy, 1984; Polunin, 1988). Some species of the Caribbean, as S. partitus and S. lividus (Forster, 1801), choose in which part of the territory will defecate in order to fertilize the area and provide it with nitrogen (Polunin and Koike, 1987). Apparently S. fuscus differs from their counterparts of the Caribbean, eliminating their droppings anywhere in its territory (or even beyond), letting them fall on any kind of substrate. The observations discussed here are similar to those described by Ferreira (1998), which also observed defecating act of this fish species, and was also unable to observe any pattern as to where it was performed.
Farming, and weeding behaviours, are widely known in feeding ecology works on Stegastes species (Hata and Kato, 2002, 2004; Salemaa, 1987), although for S. fuscus there is no clear description of weeding (Feitosa et al., 2012), defending the territory characterizes the species behavior as extensive farming, as described in Hata and Kato (2004) . This kind of farming is meant to protect large areas where the fish allows the growth of various species of algae, unlike intensive farming, in which the territories are smaller and the fish allows growth of only one or two species of algae (Hata and Kato, 2004). The records show that S. fuscus remove both small pieces of seaweed, as other seemingly unwanted objects (Mattos et al., in preparation), small rocks, decapods of Pagurus spp., and small sea urchins, Lytechinus variegatus. The “territory maintenance” behaviour herein described might be the first records of weeding for the species, although the objective of such act is not yet clear enough to make such assumption.
For Stegastes genus, territorialism is not only associated with reproductive success, but also the territory maintenance can be linked with life quality of these organisms (Wilson and Wilson, 1992). According to these authors, territory owners
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simply protect their homes. Some studies reveal how females of other species, such as S. variabilis, S. partitus and S. leucostictus, even having their own territories, seek nests organized and guarded by males in other territories, to spawn (Emery, 1968; Myrberg, 1972). Although behaviours observed during this study (remove stones) may have reproductive function, the collected data and the choice of avoiding to register reproductive behaviours, do not allow us to validate this hypothesis. Since the gender of the observed fishes were not identified, it is impossible to say if only males perform such behaviour.Body health maintenance behaviours have long been observed in reef fishes (Grutter and Poulin, 1998; Sazima et al., 1997). The need to remove parasites from their bodies as well as cleaning wounds to prevent infection is a potential problem for demersal fishes with great interaction with the substrate (Cheney and Cote, 2003; Grutter, 1995; Grutter et al., 2011). Some reef fishes, like Haemulidae, Labridae, and Epinephelidae, are able to visit a cleaning station (Campos and Sá-Oliveira, 2011; Sazima et al., 1997), but territorial herbivores developed other cleaning strategies, such as rubbing against algal substrate, as Jania sp. or Halimeda sp. Moreover, Araújo et al. (2003) attribute the aggressiveness of S. fuscus as a factor which reduces the amount of clients in fish cleaning stations in Pernambuco’s reefs.
Since the dusky-damselfishes would have to leave its territory to visit cleaning stations, those fishes need to use another known strategy reef fishes use for cleaning their bodies. Thus the fish acts by rubbing its body surface against hard materials, as described in “chafe”. Those behaviours were described previously for S. partitus and S. variabilis (Emery, 1968; Myrberg, 1972). However, S. fuscus shows smaller, fewer and simpler range of those actions than their sisters’ species. The chafe behaviour of the Brazilian species consists in only one action (see “chafe”), in which the fish tries to clean the entire body surface, from the head to the caudal fin. Meanwhile, S. partitus and S. variabilis perform 3 to 5 different behaviours for different part of the body, like chafe, fin-flick and tail-down (Emery, 1968; Myrberg, 1972).
It was common to see S. fuscus specimens leaving their territories, like described in leaving the territory pattern, to feed in other areas, mostly territories of other fish species. Few works with fishes describe fortuitous postures like those with reef fishes, and this is the first description for Stegastes genus. Studies with Mediterranean fishes, like Chromis chromis (Pomacentridae), described behaviours where animals unnoticed invade other territorial nests for variables reasons, like fecundating others females eggs or stealing food, including eggs (Picciulin et al., 2004).
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A furtive behaviour has been clearly identified, but few times a fish swims up to 10m away from its territory to feed in a conspecific territory until being expelled. Thereafter, the same fish swims again to another territory repeating the action, and then finally returns to its own area, spending, sometimes, almost 2 minutes away. Stealing behaviours have been recorded since the beginning of ethological observations, on systems with limited resources and hierarchical system, where dominated individuals develop alternative behaviours to gain access to the resources of other animals (Slater et al., 2005; Tenaza, 1971).As an example, fishes from Batrachoididae family maintain a furtive behaviour in which small not dominant males, hide and sneak into the nest of other males, trying to impregnate a female’s spawning (Brantley and Bass, 1994). S. fuscus specimens live in constant competition for space and food, thus, leaving the territory with the objective of stealing some food from others territories seems to be another typical furtive behaviour. In this study, nearly 90% of bites performed in algae of neighbouring areas were performed by 10 cm or smaller fishes (equal to, or below the average). It is also possible that the animals seen leaving and coming back doing nothing more than swim, are unsuccessful in the attempt of stealing food.
Social groups are able to recognize each other in reef fish communities (Wilson and Wilson 1995), and Stegastes fuscus behaviours seem to follow this precept. The pattern observed by forming groups among neighbours fish of adjacent or close territories, should be described as a social interaction on this species. Often these groups make up 4 or 5 fish side by side driving to distant territories, which caused an aggressive reaction of the "owners” of these areas that can dissipate the group. The fact of S. fuscus forming groups with neighbours of adjacent territories, which sometimes are attacked by a fish from a distant area supports the hypothesis that these fish might recognize and tolerate their adjacent neighbours.
The acts performed inside a shelter are commonly described to reef fish, including territorial herbivores species (Myrberg, 1972; Myrberg and Riggio, 1985). Usually aggressive interactions or predators can induce the fishes to hide from their potential attackers to avoid encounters (Almany, 2004; Beukers and Jones, 1998). However, search for shelter does not seem to be necessarily associated with running away from a threat, but also a part of their resting behaviours, as registered in Bessa and Sabino (2012).
For fishes that live in shallow waters, more exposed to the waves and sunlight, the demand for shelter is often associated with the presence of more stable conditions;
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calmer waters and lower temperatures, since big temperature changes can affect the fish metabolism (Barlow, 1993; Morinière et al., 2003; Rosa et al., 1997) These two possibilities, refuge for better environmental conditions and hiding, also explain the variation (0 to 27s / min) found in the time spent in acts of this behaviour. Only in 2% of the time that individuals entered in hole was possible to see some kind of threat; as the presence of barracudas and sounds of boats approaching. Fish with more exposed areas, territories to unfavourable physical conditions, or more aggressive neighbours would tend to shelter longer, to prevent from spending more energy than their feeding input.The chemical marking may also explain why these individuals spend part of their time in shelters. These hollows are also used by juveniles who remain hidden in adults territories. Studies with species of the genus Dascyllus and Pomacentrus showed that recruits are able to identify adult fishes of the same species by the chemical cues (Coppock et al., 2016). This suggests that the time spent on shelter by some individuals might also result in chemical marking, and not only an act hiding or resting.
Acts of chase, display and threat were observed in previous studies with S. fuscus (Aued, 2012; Osório et al., 2006; Souza et al., 2011c) while the behaviour "bite", registered for S. variabilis and S. partitus (Emery, 1968), was still not described for S. fuscus. Mouth fighting behaviour, although is more often described for freshwater fishes (Vierke, 1988), is also widely described for species of the families Labridae and Haemulidae (DeLoach and Humann, 1999). The act "escaping" was quoted in Bessa and Sabino (2012), but it was not described. In the present work, this act was the lowest representation within the agonistic category. The threat and mouth fighting behaviours were exclusively intraspecific.
Species that most suffer from S. fuscus attacks were: Pseudopeneus maculatus, Coryphopterus glaucofraenum, Halichoeres brasiliensis, Acanthurus coeruleus and Acanthurus bahianus. These observations differ from (Aued, 2012; Feitosa, 2010), for whom species of the families Scarinae and Acanthuridae are the ones that suffered more agonistic actions from S. fuscus. However, the results resemble with those found by Myrberg (1972), which indicates the substrate feeders Thalasoma, Halichoeres and Pseudopeneus species, as generally most attacked by S. partitus. That might indicate that the rate of agonistic behaviours depends mostly on the abundance of the invader species.
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The assumptions made by Ferreira (1998), argue that S. fuscus is a key species for reef community, because it can maintain high diversity and richness of small invertebrates that live in the surrounding areas. This idea is supported by the fact that the two most often species attacked by S. fuscus in this study – Pseudupeneus maculatus and Halichoeres brasiliensis - are mobile invertebrates feeders (Ferreira et al., 2004a).The similarities between the herein results for S. fuscus and those found by Myrberg (1972) can be explained mainly by the similarity of areas 1 and 2 of this study with the environments occupied by S. partitus. The latter species tends to occupy mainly isolated patch reef, characterized by low tops in relation to the sandy matrix (Cervigón, 1991; DeLoach and Humann, 1999; Myrberg, 1972). The environment formed by the reef spots in Porto de Galinhas’s sampling points 1 and 2 are closer to the habitat described above, characterized by small hilltops surrounded by sandy substrate, facilitating interaction between bottom and top reef fishes (see Ferreira, 1995). Those characteristics attract mobile invertebrate feeders, thus being more abundant in the habitats found on areas 1 and 2, therefore this is the main trophic group attacked by S. fuscus in this study. No agonistic encounter with the species H. brasilienis, P. macullatus and C. glaucofraenum was registered in point 3.
Two studies on different reefs, in Pernambuco State also pointed mobile invertebrates predators among the most attacked by S. fuscus (Leal et al., 2015a, 2013). In these studies, the specimens defended territories established in Millepora sp colony. As some territories in the present study, the substrate was different from predominantly dominated by macro algae, which consequently attracts invertebrates eaters, for example. The variation in the substrate defended causes the differences between the main invasive species. In areas with greater coverage of algae, most of the interactions will be against roving herbivores. And, in areas with presence of corals as Millepora sp., most interactions will be against predators of small invertebrates (Leal et al., 2013; Pereira, 2011).
Observations made in Pernambuco reefs, point Cephalopholis fulva (Linnaeus, 1758) as frequently present in S. fuscus territories, being fully tolerated, recording one single act of aggression against this species. The same behaviour occurs when these two species are using the colonies of Millepora sp. as habitat (Pereira et al., 2012). It is possible that the presence of C. fulva in damselfish territories bring benefits to the species, possibly driving away potential invaders as small crustaceans and juvenile fish of Blenniidae, Acanthuridae and Labridae Families. The mutualistic relation between S.
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fuscus and Epinephelus marginatus shows fitness increasing of dusky-damselfish due to the presence of the grouper (Bessa and Sabino, 2012). The last one helps keep predators away from eggs of S. fuscus territories, eventually feeding on potential invaders and decreasing nest defence efforts for S. fuscus (Bessa, 2011). Myrberg (1972) also found tolerance by two species of the genus Serranus (evolutionarily close to Epinephaelidae Family) on territories of S. partitus.Sound Patterns
The sounds recorded here fall within the categories observed for reef fishes, such as cutting behaviors and agonistic (Myrberg, 1981, 1972; Winn, 1972). The sound production by S. diencaeus during reproductive periods was registered in Florida by Emery (1968). The pop sound performed by S. fuscus is very similar to what Myrberg (1972) described for S. partitus. This behaviour is understood as an agonistic sound jointly performed with acts of chase and threat. For S. partitus, the pop sound was also produced while performing the behaviour "circle" described by Myrberg when opponents swim drawing a small circle, as the head of one individual pursues the tail of the other.
The burr sound was rarely observed and is still difficult to determine its function. It is possible that this pattern is associated with reproductive behaviour, similarly to the "drumming sounds" described by Emery (1968). The sound here registered is very similar the one described in Myrberg (1972), not only by the sound itself but when it comes to the situation when the sound was performed. It was always registered in front of another conspecific, and associated with the fish moving rapidly in water column. The fact of being perfomed only for conspecifics might indicate a kind of communication between male-female, or simply some kind of hierarchical demonstration. Nevertheless, it might explain why Myrberg (1972) was unable to register those sounds in laboratory.
Although there are differences in the description of the latter to the sound recognized in the present study, we can address a specific variation, and deeper observations with S. fuscus are necessary to validate this hypothesis. Therefore, research should be expanded with the use of appropriate equipment, such as hydrophones, to understand the type, duration, frequency, speed and range of these sounds. This work is in progress, aiming at providing a more complete study of this species sound production.
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ConclusionFrom the patterns herein observed, it is clear that resources and territory defence is the main factor influencing S. fuscus behaviour, since only the patterns of chafe and defecation appear to have no connection with the territorial behaviour of this species. Three behaviours described in this work; nibbling in torn pieces, lateral tug and leaving the territory; have no matching records in the literature for reef fishes, probably being the first time that such patterns are described and discussed. The first two behaviours represent wider feeding activities compared to another Stegastes species. While, leaving the territory shows how those fishes expand their home range beyond territory limits, continuously interacting with the surrounding individuals and environment.
Many reef fish behaviour studies, although having the intention to create an ethological research, rarely describe their behaviour patterns in details, highlighting ecological interpretation and the numerical approaches of the actions. Those studies of observations in loco are important in order to learn about the behaviour of this species and how they interact with the environment. In addition to acquiring in-depth knowledge about the species behaviour, the standardization of terms and concepts create an interdisciplinary basis. The organization and categorization facilitates communication between different areas of scientific knowledge, promoting dialogue between areas such as physiology and conservation.
A behavioral repertoire similar to Caribbean Stegastes species was identified, although behaviour variations and different acts found in S. fuscus differ from those described earlier for species of this genus. Body cleansing has a different pattern when compared to that described for S. partitus, once the behavior of the specie herein studied is much simpler, comprising one single movement. In addition, 3 new recorded behaviors were never before described in Caribbean Pomacentridae, namely: biting in torn pieces, lateral tug and leaving the territory. Thus S. fuscus, although resembling to its congeners, proved to have a sole behavioral pattern, different from the fishes studied in the Caribbean.
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ACKNOWLEDGEMENTSWe would like to thank the researches of the Ichthyology Marine Tropical Group (IMAT). To the CNPq, for the scholarship, essential for the implementation of this work. And especially Sergio Mattos, for the contribution to the text, the translation and the assistance in all phases of the work, and to David Moraes, author of the illustrations.
REFERENCES
