Eduardo Bessa Pereira da Silva Efeito do turismo de natureza sobre o comportamento de peixes em riachos de cabeceira São José do Rio Preto 2013 Eduardo Bessa Pereira da Silva Efeito do turismo de natureza sobre o comportamento de peixes em riachos de cabeceira Tese apresentada como parte dos requisitos para obtenção do título de Doutor em Biologia Animal, junto ao Programa de Pós-Graduação em Biologia Animal, Área de Concentração – Ecologia e Comportamento, do Instituto de Biociências, Letras e Ciências Exatas da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de São José do Rio Preto. Orientadora: Profª. Drª. Eliane Gonçalves de Freitas São José do Rio Preto 2013 Bessa, Eduardo Efeito do turismo de natureza sobre o comportamento de peixes em riachos de cabeceira / Eduardo Bessa Pereira da Silva. - São José do Rio Preto: [s.n.], 2013. 71 f. : 7 il. ; 30 cm. Orientador: Eliane Gonçalves de Freitas Tese (doutorado) - Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Biociências, Letras e Ciências Exatas 1. Comportamento animal. 2. Peixes de riacho. 3. Conservação. I. Gonçalves-de-Freitas, Eliane. II. Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Biociências, Letras e Ciências Exatas. III. Título. CDU - 597 Eduardo Bessa Pereira da Silva Efeito do turismo de natureza sobre o comportamento de peixes em riachos de cabeceira Tese apresentada como parte dos requisitos para obtenção do título de Doutor em Biologia Animal, junto ao Programa de Pós-Graduação em Biologia Animal, Área de Concentração – Ecologia e Comportamento, do Instituto de Biociências, Letras e Ciências Exatas da Universidade Estadual Paulista “Júlio de Mesquita Filho”, Campus de São José do Rio Preto. Comissão Examinadora Profª. Drª. Eliane Gonçalves de Freitas UNESP – São José do Rio Preto Orientadora Profª. Drª. Eleonora Trajano USP – São Paulo Prof. Dr. Gilson Volpato UNESP – Botucatu Profª. Drª Lilian Casatti UNESP – São José do Rio Preto Profª. Drª. Patrícia Izar USP – São Paulo São José do Rio Preto Junho de 2013 À Cristina, minha esposa e companheira de todas as horas nesse processo conturbado que é a aquisição de um título de doutor. “A verdade sobre a natureza é muito mais bela do que nossos maiores poetas poderiam cantar.” Konrad Lorenz “Se naturalistas vão para o céu (coisa de que tenho consideráveis dúvidas eclesiásticas), espero que lá eu receba um bando de papagaios para me entreterem, em vez de uma televisão.” Gerald Durrell SUMÁRIO RESUMO ..................................................................................................................... 1 ABSTRACT ................................................................................................................... 2 AGRADECIMENTOS ................................................................................................. 3 INTRODUÇÃO GERAL ............................................................................................. 6 Os valores da biodiversidade ........................................................................................ 6 A humanidade busca a natureza ................................................................................... 7 Ecoturismo e impactos ambientais ............................................................................... 8 Ferramentas para monitoramento e manejo do ecoturismo .......................................... 9 O comportamento no manejo do ecoturismo em ambientes aquáticos ...................... 11 Desafios do uso do comportamento no manejo do ecoturismo .................................. 12 O conteúdo desta tese ................................................................................................. 13 Referências ................................................................................................................. 14 Microhabitat use and activity period do not indicate impacts from aquatic nature tourism on fish ........................................................................................................... 21 Abstract ...................................................................................................................... 21 Introduction ................................................................................................................ 22 Materials and Methods .............................................................................................. 23 Results......................................................................................................................... 26 Discussion ................................................................................................................... 26 References .................................................................................................................. 30 Monitored tourism conserves territorial fish .............................................................. 44 Acknowledgements .................................................................................................... 44 Abstract ....................................................................................................................... 45 Keywords .................................................................................................................... 45 Highlights ................................................................................................................... 45 1. Introduction ............................................................................................................ 48 2. Materials and Methods ........................................................................................... 52 3. Results .................................................................................................................... 56 4. Discussion ............................................................................................................... 56 References .................................................................................................................. 60 Table and table caption ............................................................................................... 66 Figure captions ........................................................................................................... 67 CONCLUSÃO ............................................................................................................ 71 APÊNDICE ................................................................................................................ 73 1 RESUMO 1 2 3 O turismo de natureza tem sido apontado como solução para o dilema entre 4 conservar o ambiente ou lucrar com ele. No entanto, o turismo de natureza 5 também causa impactos, o que ainda é pouco estudado. Meu objetivo foi 6 avaliar como o turismo afeta o comportamento dos peixes testando se os 7 peixes evitarão os turistas ou mudarão seu comportamento social em resposta 8 à visitação a longo prazo, mesmo na ausência do turista, uma abordagem 9 inovadora. Dividi riachos de Nobres, Mato Grosso em três tratamentos: Áreas 10 Referência (RA nos artigos em Inglês), Áreas de Visitação Monitorada (MVA) e 11 Áreas de Visitação Não-Monitorada (NMVA). Comparei uso de microhabitats, 12 período de atividade, agressividade e nidificação nesses três tratamentos. As 13 dez espécies de peixes analisadas não mudaram o uso dos microhabitats nem 14 o período de atividade. Como os ambientes estão degradados pelo turismo, 15 isso me levou a considerar inadequados estes indicadores. Os 16 comportamentos sociais (agressividade e nidificação) responderam apenas à 17 falta de monitoramento. Assim, o monitoramento do turista é fundamental para 18 a conservação. Em conclusão, o turismo de natureza pode aliar conservação e 19 exploração econômica, desde que use indicadores de impactos funcionais e 20 que o comportamento dos turistas seja monitorado. 21 22 Palavras-chave: Conservação. Cichlidae. Characiformes. Territorialidade. 23 Nidificação. Uso de microhabitats. Período de atividade. 24 25 2 ABSTRACT 1 2 3 Nature-based tourism has been touted as a solution to the dilemma between 4 conserving the environment or taking profit from it. However, nature tourism 5 also causes impacts, which is still understudied. My objective was to evaluate 6 how tourism affects fish behavior by testing whether the fish avoid tourists or 7 change their social behavior in response to visitation in the long term, after 8 visitors have left, an innovative approach. I divided the streams of Nobres, Mato 9 Grosso, Brazil, in three treatments: Reference Areas (RA), Monitored Visitation 10 Areas (MVA) and Non-Monitored Visitation Areas (NMVA). I compared 11 microhabitat use, activity period, aggressiveness and nesting in these three 12 treatments. The ten fish species analyzed did not change microhabitat use or 13 activity periods. Since the environment is degraded by tourism, I considered 14 these inadequate indicators. Differently, social behaviors (aggression and 15 nesting) responded only to lack of monitoring. Thus, monitoring the tourists is 16 fundamental for conservation. In conclusion, nature tourism can combine 17 conservation and economic exploitation, provided you use functional impacts 18 indicators and monitor tourists’ behavior. 19 20 Keywords: Conservation. Cichlidae. Characiformes. Territoriality. Nidification. 21 Microhabitat use. Activity period. 22 23 3 AGRADECIMENTOS 1 2 3 Tornar-se doutor é aprender. Aprender muito mesmo! Então usarei essa 4 seção para agradecer meus professores. 5 Preciso começar agradecendo a principal professora desse projeto, Eliane 6 Gonçalves de Freitas, minha orientadora. Por muito tempo vi com admiração os 7 trabalhos que a Eliane fazia, então ter finalmente trabalhado com ela foi um 8 privilégio e uma realização pessoal. Entrei nesse doutorado com algumas 9 metas pessoais paralelas à questão do título, graças ao convívio agradável e 10 ao aprendizado posso dizer que as considero plenamente satisfeitas. Mais do 11 que trabalhar, conviver com a Eliane me mostrou que não é preciso trocar a 12 vida pessoal pela acadêmica, e que é possível ter um vínculo de amizade e 13 respeito e manter o senso crítico em alta ainda assim. 14 Já conheço os professores Francisco Langeani e Lilian Casatti há algum 15 tempo, mas conviver com eles como coordenadores do meu programa de pós 16 foi um prazer. Ainda me tornei verdadeiramente aluno deles nas disciplinas que 17 cursei, providencialmente condensadas. Obrigado ainda pelo feedback na 18 banca de qualificação. Espero ter sido um bom garoto e ajudado a subir o 19 conceito CAPES do nosso programa. 20 Se avó é mãe duas vezes, o que seria o orientador de sua orientadora? 21 Um avô acadêmico? Orientador ao quadrado? Desde 1999 aprendo com o 22 Gilson Volpato através de seus cursos e livros. Foi um raro privilégio tê-lo por 23 uma semana inteira no curso de Jaboticabal, ouvir suas ideias e contar as 24 minhas também. Inspirador. 25 Mais alguns colegas foram meus professores à medida que me ensinaram 26 a paixão pelos peixes. O José Sabino esteve desde o início envolvido com 27 esse projeto, me ajudou a idealizá-lo e a colocá-lo em prática. Tem sido um 28 parceiro de pesquisa incrível e aberto tantas oportunidades legais que jamais 29 terei como retribuir ou agradecer o suficiente. Outra colega tem tanto a ver com 30 4 esse projeto que tem Nobres até no nome. A Professora Lucélia Nobre 1 Carvalho é excelente companhia em campo e tornou-se a pessoa mais próxima 2 para as conversas e colaborações científicas em história natural de peixes. 3 Todo esse projeto foi financiado pela Fundação de Amparo à Pesquisa de 4 Mato Grosso, FAPEMAT. Também contei com o apoio de diversas pessoas em 5 Nobres para realizar essa pesquisa. O Seu Isaías de Almeida sempre me 6 hospedou com o conforto merecido depois de um trabalho de campo puxado. O 7 ‘Klebinho’ Oliveira, ‘Toninho’ Campos e a Dona Joana Lambert me abriram as 8 portas para alguns dos lugares mais bonitos em que mergulhei. Sem a 9 compreensão deles esse trabalho não teria nem começado. 10 Há alguns outros professores a quem preciso agradecer. Em 2006 tomei 11 uma decisão pouco usual para um cientista. Decidi tentar um concurso público 12 numa universidade antes de ter um doutorado. Passei. Tornei-me professor da 13 Universidade do Estado de Mato Grosso, um campus pequeno, no interior, 14 cheio de jovens colegas recém-contratados como eu e de alunos curiosos. 15 Obrigado a todos os colegas que me ensinaram muito nesses anos iniciais da 16 docência superior. Foi nesses anos que duvidei que um dia seria um bom 17 professor. Agora tenho certeza de que não serei. Meu muito obrigado especial 18 aos colegas mais próximos: A Ana Arnt e seu jeito ‘do contra’, a Alessandra e 19 seu jeito efusivo, o Anderson Fernandes e seu jeito mineiro, o Marco 20 Gottschalk e a Monica Blauth e seus jeitos acolhedores e o Diogo Andrade 21 Costa e seu jeito... Bom, só ‘seu jeito’. Agradeço ainda todos os colegas 22 professores que passaram nalgum momento por cargos de gestão e 23 participaram da minha peleja para conseguir concluir meu doutorado na 24 modalidade ‘kamikaze’, sem afastamento. 25 Ensinar é uma experiência interessante porque há momentos em que 26 duvidamos de quem é o aprendiz e quem é o mestre. Assim, obrigado a todos 27 os meus alunos de Zoologia de Vertebrados e outras disciplinas. Muito 28 obrigado especialmente a todos os estagiários do LECR, o Laboratório de 29 Ecologia Comportamental da Reprodução, que coordeno na UNEMAT. Vocês 30 5 me ajudaram em campo, discutiram os projetos e artigos comigo, tiveram 1 paciência com minhas ausências, cuidaram de mim e até ficaram ansiosos 2 junto comigo. Às vezes mais que eu! Tenham certeza de que aprendi muito 3 com vocês todos. 4 Tenho quatro professores especiais, desses que nunca mais deixam de 5 nos ensinar coisas bem mais importantes que o melhor indicador 6 comportamental dos impactos do turismo. A primeira é minha esposa, uma 7 mulher inteligentíssima. O mais legal é que ela sabe muita coisa de áreas 8 totalmente diferentes da minha, por isso não paro de aprender com ela. Ela 9 também tem aprendido tanta Biologia que, aparte sua aversão por sapos e 10 lagartos, ainda vai se tornar minha doutora honoris causa. Meu pai, José 11 Renato Leite Pereira da Silva, tem uma curiosidade insaciável, espero ter 12 aprendido um pouco disso com ele. Estudar, estudar e estudar. Ler, ler e ler. 13 Ele é meu pai, meu confidente, meu companheiro. Aprendi muito com minha 14 mãe, Maria Thereza Fontes Bessa. Alguns diriam que em 2008 ela parou de 15 ensinar. Eu discordo, continuo aprendendo até hoje. Eis aí a verdadeira vida 16 eterna. Obrigado ao meu padrasto, Fernando Tamanini, pelo interesse nos 17 assuntos naturalísticos, tanto os meus quanto os que ele colhe no Discovery 18 Channel. Obrigado por continuar por perto. Meu agradecimento, por fim, aos 19 meus irmãos, Ana Bessa, Pedro Tamanini e.Lucas Fragomeni. Eram eles que 20 estavam por perto quando descobri que era biólogo nos costões rochosos de 21 Três Praias. 22 23 6 INTRODUÇÃO GERAL 1 2 3 Os valores da biodiversidade 4 5 O termo biodiversidade foi cunhado por Edward O. Wilson para incluir três 6 níveis da diversidade biológica (Wilson, 1988): o nível molecular, ou genético; o 7 nível orgânico, ou taxonômico; e o nível da paisagem. Todos os três níveis 8 apresentam seu valor para a humanidade, mas estão ameaçados por nosso 9 modelo econômico naquela que já é considerada uma nova era geológica, o 10 Antropoceno (Zalasiewicz et al., 2011). 11 Um dilema entre o desenvolvimento econômico mundial e a conservação 12 da biodiversidade foi preconizado, embora ele seja, de fato, um falso dilema 13 (Sabino et al., 2012). Considero esse dilema falso por dois motivos que se 14 localizam nas duas pontas do processo econômico: a matéria prima e o 15 mercado consumidor. Primeiro porque toda atividade humana tem na sua base 16 matéria prima natural. Deixar de se preocupar com a biodiversidade é abrir 17 mão da matéria prima que move a economia. Segundo porque toda a 18 economia depende de um mercado consumidor. Esse mercado, composto por 19 nós humanos, compõe uma delicada rede de interações que depende em certo 20 grau de estabilidade ecológica. Caso a economia degrade demais o ambiente, 21 seus consumidores serão penalizados, afetando-a por consequência. 22 Vivendo numa sociedade capitalista, atribuir valor à biodiversidade é 23 interessante (Kopnina, 2012) e, ao mesmo tempo, uma tarefa complexa. De 24 forma a pautar a atribuição de valor à biodiversidade, esse valor foi dividido em 25 três (Sabino et al., 2012). O valor de mercado considera como valioso aquilo 26 que gera recursos concretos. Quando um rio produz grande quantidade de 27 peixes próprios para o consumo humano, esse rio possui valor de mercado. 28 Considera-se valor de amenidade aquele proporcionado pela experiência que 29 um item da biodiversidade nos causa. É o valor de amenidade que leva um 30 turista a deslocar-se de sua casa para um ambiente natural para fazer 31 7 ecoturismo. Por fim, todos os integrantes da biodiversidade são o produto de 1 um processo evolutivo de bilhões de anos e atuam em funções chave em seus 2 ecossistemas. No valor moral, considera-se que por isso todas as espécies têm 3 o direito de existir. 4 5 A humanidade busca a natureza 6 7 A hipótese da biofilia pode ser definida como nosso vínculo inato com a 8 natureza (Wilson, 1984). A humanidade evoluiu num panorama natural, por 9 isso, a presença de elementos naturais desencadeia a sensação de bem-estar 10 em nosso organismo. Humanos buscam instintivamente o contato com a 11 natureza, o que nos causa bem-estar físico e psicológico (Heinsch, 2012). 12 Existem evidências disso na velocidade de recuperação de doentes 13 (Annerstedt e Wahrborg, 2011) e na resiliência ao sofrimento (Tidball, 2012). 14 Talvez devido a esse desejo de estar com a natureza o homem busque o 15 ecoturismo. 16 O ecoturismo como vemos hoje surgiu na década de 1980 e é o 17 segmento do turismo que mais cresce (Hawkins & Lamoureux, 2001). As 18 definições de ecoturismo são dissonantes (Donohoe & Needham, 2006), 19 algumas definem ecoturismo pelo foco: locais de natureza preservada. Outras 20 pelo modo: turismo que não oferece, ou oferece minimamente, impactos 21 ambientais. Talvez a definição ideal esteja numa junção das duas: visitação a 22 locais preservados causando o menor impacto possível (Blamey, 2001, Tabela 23 1.1). 24 A Organização Mundial do Turismo estima um crescimento cerca de três 25 vezes maior para o ecoturismo do que o da indústria turística como um todo, 26 cerca de 7% de todos os gastos com viagens internacionais no mundo (Shum, 27 2007). Segundo projeções, o ecoturismo pode passar a movimentar nos 28 próximos anos cerca de US$ 473 bilhões por ano (World Tourism Organization, 29 2010). Os dados disponíveis para o Brasil são menos completos, mas destinos 30 ecoturísticos constam de diversos relatórios e perspectivas de aumento da 31 8 importância econômica do turismo brasileiro (Barbosa, 2010). Dos 184 destinos 1 turísticos vinculados pela EMBRATUR à Copa de 2014, por exemplo, 140 são 2 destinos voltados para o ecoturismo (Ministério do Turismo, 2012). 3 Essa busca por contato com a natureza não é diferente nos ambientes 4 aquáticos. Da mesma forma que grandes símios incluem fontes de água em 5 seus territórios, a proximidade da água nos conforta (Wilson, 1984), tornando-a 6 um elemento comum no paisagismo (Mador, 2008), mas também um ambiente 7 a ser visitado. O ecoturismo tem crescido principalmente no mar, mas também 8 em grandes rios, lagos e riachos de cabeceira. Esses últimos têm recebido 9 turistas para a prática do mergulho livre, a chamada flutuação (Sabino & 10 Andrade, 2003). Nobres, em Mato Grosso, área de estudo desta tese, é um 11 ponto de ecoturismo em água doce cuja importância vem crescendo. 12 13 Ecoturismo e impactos ambientais 14 15 O ecoturismo tem aparecido como uma grande esperança na valorização 16 da natureza e na geração de renda sem a degradação ambiental (United 17 Nations Environmental Program, 2005). No entanto, fica claro que essa mesma 18 atividade tem potencial de degradar o ambiente onde ocorre (McKercher, 19 1993). Sendo o ecoturismo a busca pela interação com um ambiente natural 20 preservado, temos um paradoxo para a sustentabilidade econômica dessa 21 atividade: o turismo degrada, mas o turista busca paisagens preservadas. 22 Assim, é primordial desenvolver estratégias de monitoramento e mitigação dos 23 impactos causados pelo ecoturismo, especialmente estratégias baseadas em 24 dados científicos. 25 Estudos anteriores apontaram impactos do ecoturismo sobre a fauna. 26 Turistas frequentemente afastam a fauna de grandes animais (Rogala et al., 27 2011). Mesmo acostumar-se à presença humana pode ser prejudicial (Higham 28 & Shelton, 2011), podendo resultar, por exemplo, no contágio da fauna por 29 doenças humanas (Muehlenbein et al., 2010). O ruído produzido pelos turistas 30 9 é outra forma de impacto (Davenport & Davenport, 2006; Constantine et al., 1 2004). 2 Em ambiente recifal ocorre a simplificação estrutural do habitat pelo 3 turismo nos recifes de coral (Rouphael & Inglis, 2001; Daby, 2003) e a oferta de 4 alimento (Ilarri et al., 2008). Em rios são conhecidos os impactos causados pela 5 pesca amadora (Catella et al., 1997). Mais recentemente alguns estudos 6 enfocaram o turismo de flutuação nos riachos de cabeceira. A perda de 7 complexidade do habitat e o pisoteio do substrato (Teresa et al., 2011), e a 8 oferta de alimento (Obs. Pess.) são alguns fatores que começaram a ser 9 explorados, embora os estudos ainda sejam incipientes. Ainda não existe, por 10 exemplo, uma ferramenta clara de monitoramento e mitigação dos impactos 11 turísticos em riachos. 12 13 Ferramentas para monitoramento e manejo do ecoturismo 14 15 O ecoturismo pode ser uma alternativa viável para lucrar com ambientes 16 preservados, desde que realizado de maneira sustentável (United Nations 17 Environmental Program, 2005). Alguns manuais de boas práticas em 18 ecoturismo foram propostos (Drumm & Moore, 2003; Higginbottom, 2004; 19 Ministério do Meio Ambiente, 2006; Tapper, 2006). Protocolos de avaliação de 20 impactos também são essenciais. 21 O primeiro protocolo de sustentabilidade turística baseou-se na 22 capacidade de carga. Essa medida diz respeito ao número de visitantes que 23 uma área pode suportar. A capacidade de carga, no entanto, não considera 24 especificidades do ambiente nem o comportamento do visitante (McCool & 25 Lime, 2001). 26 Alternativas incluem indicadores mensuráveis selecionados pelo gestor do 27 turismo para cada atração. Foi o caso do monitoramento de impacto da 28 visitação, VIM na sigla em inglês (Graefe et al., 1990), o protocolo de limites 29 aceitáveis de alteração (Stankey et al., 1984) e o protocolo de experiência do 30 visitante e proteção dos recursos (Manning et al., 1995). 31 10 1 2 11 O comportamento no manejo do ecoturismo em ambientes aquáticos 1 2 Muitos protocolos de gerenciamento do ecoturismo se pautam em 3 indicadores escolhidos pelo próprio gestor da atividade ou órgão de regulação 4 ambiental ou turística. Seria interessante usar indicadores embasados em 5 argumentos empíricos (Tarlow & Blumstein, 2007). É comum usar espécies ou 6 a estrutura da comunidade como indicadores (Casatti et al., 2010), mas o 7 comportamento ainda é pouco explorado na conservação (Caro & Sherman, 8 2011). 9 Respostas comportamentais já são conhecidas para diversos tipos de 10 impactos como poluição química (Craig & Laming, 2004), sonora (Schwemmer 11 et al., 2011; Rolland et al., 2012), introdução de espécies invasoras (Mattos & 12 Orrock, 2010), iluminação artificial (Witherington, 1992) e mudança na 13 disponibilidade de sítios de nidificação (Semel & Shermann, 2001). Isso indica 14 que o comportamento pode ser uma importante ferramenta para o diagnóstico 15 de novos impactos ambientais (Wingfield, 2003), desde que informações 16 básicas e empíricas subsidiem sua aplicação. De acordo com Semeniuk et al., 17 (2011), três níveis comportamentais devem ser considerados para avaliação de 18 impactos ambientais: 1) História de vida; 2) Socialidade e reprodução; e 3) 19 Alimentação e interação predador-presa. Assim, esses níveis podem servir 20 como base para estudos sobre impactos do ecoturismo. 21 Alguns esforços já foram feitos para encontrar indicadores 22 comportamentais de impactos do turismo em ambientes aquáticos. A resposta 23 de golfinhos nariz de garrafa (Tursiops truncatus) aos barcos turísticos serviu 24 de base para a regulação da observação de golfinhos na Nova Zelândia 25 (Constantine et al., 2004). Milazzo e colaboradores (2006) apresentam dados 26 sobre alterações comportamentais de peixes recifais em decorrência da oferta 27 de alimento. Esses autores são tolerantes com a prática, desde que restrita a 28 uma área só, devido ao seu valor na interação entre peixes e turistas. Em 29 riachos, o comportamento alimentar de peixes na relação nuclear-seguidor é 30 12 afetado indiretamente pelo turismo, por meio da simplificação do habitat 1 (Teresa et al., 2011). 2 3 Desafios do uso do comportamento no manejo do ecoturismo 4 5 Ainda há alguns entraves para a aplicação do comportamento animal na 6 conservação (Caro, 2007). Conhecer as espécies de peixes de cabeceiras 7 tropicais nos dará bases para entender padrões comportamentais naturais e 8 alterados por impactos humanos como o turismo. Serão esses padrões 9 alteráveis que funcionarão como indicadores (Tarlow & Blumstein, 2007). Esse 10 conhecimento precisa transcender a taxonomia, um início necessário, mas que 11 demanda complementação. Com uma base teórica robusta, muitas vezes 12 puramente descritiva, fica mais fácil usar o comportamento no manejo do 13 ecoturismo e comparar comportamentos naturais com respostas aos impactos. 14 Outra necessidade reside na busca por padrões de resposta. 15 Compreender todos os ambientes onde o ecoturismo possa se instalar será 16 impossível. Dessa maneira, conhecer padrões de respostas comportamentais 17 por meio da integração de dados de diferentes ambientes pode ser a chave 18 para o manejo. Mesmo situações diferentes como a resposta comportamental à 19 oferta de alimento numa ilha do Mediterrâneo (Milazzo et al., 2006) num recife 20 do nordeste brasileiro (Ilarri et al., 2008) e num riacho de cabeceira (Obs. 21 Pess.) têm características em comum e a solução encontrada para um pode 22 ser aplicada aos outros. Uma massa crítica de pesquisas será necessária para 23 permitir as extrapolações necessárias ao uso do comportamento no controle de 24 impactos do turismo. 25 O comportamento animal padece de um grave problema, muitas pessoas 26 acreditam fazer pesquisas e observações comportamentais sem dominarem as 27 técnicas relacionadas. Talvez por isso existam tantos trabalhos sobre métodos 28 em comportamento animal (Altmann, 1974; Lehner, 1998; Martin & Bateson, 29 2007). Para aplicar o comportamento ao manejo do turismo será necessário 30 formar observadores, sejam eles os gestores da atividade turística, cientistas, 31 13 ambientalistas ou até os turistas. Todos esses personagens podem ser 1 coletores dos dados necessários ao manejo, desde que sejam treinados. 2 Por fim, é necessário convencer os tomadores de decisão do valor das 3 pesquisas no embasamento das políticas públicas, incluindo o valor do 4 comportamento enquanto indicador de impactos (Buchholdz, 2007) e seu papel 5 no manejo de atrações turísticas. Indicadores fisiológicos (Sprague, 1971) e 6 ecológicos (Casatti et al., 2010) de impactos ambientais já são bem conhecidos 7 e utilizados na conservação. Indicadores comportamentais ainda são novidade, 8 portanto sua eficácia ainda precisa de aceitação. É só com o acúmulo de 9 pesquisas e de aplicações bem sucedidas que esse reconhecimento virá. 10 11 O conteúdo desta tese 12 13 Esta tese de doutorado busca apresentar indicadores comportamentais 14 dos impactos decorrentes do turismo de forma a torná-lo uma ferramenta de 15 conservação desse ambiente. Em outras palavras, a pergunta que norteou toda 16 essa pesquisa foi: Como a ocorrência de turismo altera o comportamento dos 17 peixes de cabeceira? Procurei avaliar a aplicabilidade de comportamentos dos 18 peixes que habitam esses riachos como medidas do grau de alteração causada 19 pelo ecoturismo. Uma das novidades desse estudo consiste na avaliação em 20 longo prazo dos impactos do turismo, ou seja, além do momento em que o 21 turista e o peixe estavam em contato direto (Bejder et al., 2006). 22 Há duas formas de abordar os efeitos do ecoturismo, uma abrange a 23 comunidade, a outra enfoca a espécie. Utilizei essas duas abordagens. Esses 24 são dois dos três comportamentos apontados como mais susceptíveis a 25 impactos por Semeniuck et al. (2011). Tais dados podem servir de base para 26 propostas de políticas públicas sobre a gestão de riachos de cabeceira 27 utilizados para turismo. 28 No primeiro capítulo avaliei como dez espécies de peixes abundantes 29 (veja apêndice para a lista completa de espécies) e importantes para o visitante 30 escolhem seus microhabitats e seu período de atividade em áreas sem 31 14 visitação, com visitação monitorada e com visitação não-monitorada. Previ uma 1 ocupação de ambientes mais crípticos e atividade em horários alternativos em 2 locais onde o turismo ocorria de modo mais impactante. Isso porque evitar o 3 contato direto com o visitante é um mecanismo de defesa comum entre animais 4 afetados pelo turismo (Bejder et al., 2006). O uso de dez espécies de 5 importância para os visitantes buscou atender aos requisitos propostos por 6 Caro (2007). Apesar do impacto do turismo ser visível (conforme diagnosticado 7 pelo monitoramento do impacto de visitação), os microhabitats ocupados e os 8 períodos de atividade não se alteraram, sinalizando que esses podem não ser 9 bons indicadores de impacto do ecoturismo. Os peixes têm adaptações fortes 10 para a ocupação de locais específicos do rio e para seu horário de atividade, 11 não lhes sendo facultado alterá-los em resposta ao turismo. Esse capítulo, já 12 em inglês, está formatado e será submetido ao Journal of Fish Biology. 13 No segundo capítulo avaliei como o ecoturismo afeta o comportamento de 14 nidificação e agressivo em uma espécie social, Crenicichla lepidota. Espécies 15 sociais têm um importante papel ecológico e são indicadores eficientes de 16 estressores ambientais, causando um controle da comunidade de baixo para 17 cima (Wong, 2012). 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Philosophical Transactions of 19 the Royal Society A, 1938, 835–841. doi: 10.1098/rsta.2010.0339 20 21 21 Microhabitat use and activity period do not indicate impacts from 1 aquatic nature tourism on fish 2 3 Eduardo Bessa1,2*, Eliane Gonçalves-de-Freitas2 4 5 1Laboratório de Ecologia Comportamental da Reprodução, Departamento de Ciências 6 Biológicas, Universidade do Estado de Mato Grosso, Tangará da Serra, Mato Grosso, 7 Brazil 8 2Departmento de Zoologia e Botânica, Universidade Estadual Paulista and Centro de 9 Aquicultura da UNESP, São José do Rio Preto, São Paulo, Brazil 10 *E-mail: edu_bessa@yahoo.com 11 12 Abstract 13 14 The maintenance of environmental integrity in headwater streams requires an effective 15 technique for evaluating impacts caused by nature tourism. Here we evaluated how useful 16 microhabitat use and activity period are for that purpose by predicting that tourism, especially 17 that done without monitoring, would alter where fish stay and when they are more active. We 18 divided the sampling points in reference areas, monitored tourism areas and non-monitored 19 tourism areas, then we evaluated each area’s conservation state with a visitation impact 20 monitoring protocol. We preformed underwater censuses evaluating microhabitat use and 21 activity by ten fish species in different hours of the day. The fish neither changed microhabitat 22 use, nor activity period in response to tourists. Since we ruled out that the river was not 23 impacted by tourism with the visitation impact monitoring protocol, we conclude that 24 microhabitat use and activity period are not appropriate indicators of the impacts caused by 25 nature-based tourism in headwater streams. This may be because these characteristics are 26 species-specific; fish are adapted to a certain microhabitat and activity period and cannot 27 inhabit other sites or be active in other periods. 28 29 30 22 Introduction 1 2 Nature tourism industry has been growing all over the world (Weaver and Lawton, 3 2007). Then research regarding the impact that such activity can cause in exploited places has 4 being growing accordingly (e.g. Praveena et al., 2012). To the moment results are dissonant, 5 sometimes pointing at a sustainable coexistence between conservation and touristic 6 exploitation (White et al., 2008), sometimes registering impacts (Uyarra & Côté, 2007). This 7 may reflect either that the indicators of impact used are not adequate to infer environment 8 impacts or that the nature tourism is not an impacting activity, this last being the most 9 unlikely. Therefore, attributing the responsibility for impacts to nature tourism is still a 10 conundrum and more effective means of impact evaluation are needed. 11 Many authors have used a single species to monitor visitation impacts, either because 12 the monitored species is a central touristic attraction (Quiros, 2007), because it pertains to a 13 better studied taxon (Müllner et al., 2004), or because it is considered a charismatic or flagship 14 species (Bejder et al., 2006). Contrastingly, Blumstein et al. (2005) suggest that a more precise 15 measure of the human effect on the wildlife should consist on the evaluation of numerous 16 species of that fauna. In this way, analysis of impacts from tourism on a larger array of species 17 by quantitative metrics would generate more efficient evaluation protocols, which could 18 conciliate tourism and conservation based on empiric evidence (Tarlow and Blumstein, 2007). 19 Touristic visitation is increasing in clear headwater streams where visitors can snorkel 20 along underwater trails. Such kind of environment is rich in animal and plant species, but still 21 understudied and subject to numerous impacts (Yates & Bailey, 2010). Moreover, due to the 22 agricultural expansion and their smaller volume, low-order streams are frequently more 23 affected by environmental impacts (Casatti et al., 2012). Altogether, touristic exploitation, lack 24 of information and environmental fragility make urgent the study of headwater streams. 25 Among the taxa that compose stream communities, fish are good candidates for 26 indicator species. Besides already being used as indicators for diverse ecologic impacts (Alyan, 27 2007), fish are efficient indicators of touristic impact on coral reefs (Milazzo et al., 2005) and 28 freshwater streams (Teresa et al., 2011a). They are also the most attractive species for tourists 29 during snorkeling, thus, their behavior should produce effective and practical evaluation 30 protocols. 31 23 We measured microhabitat use and activity period changes by ten fish species as 1 indicators of touristic disturbances. The behavior is expected to respond faster to 2 environmental changes than other biological factors, such as population or community 3 structure (Wingfield, 2003). It is known that animals respond to the presence of humans as 4 they respond to predators (Frid & Dill, 2002), so they were expected to occupy the 5 environment in a different fashion where tourists are present (Rogala et al., 2011; Lusseau, 6 2004). Tourists might also influence fish activity period, inhibiting activity during visitation 7 periods, what was already observed in mammals (Duchesne et al., 2000; Lusseau, 2004). 8 With this study we aimed to evaluate if fish microhabitat use and their activity period are 9 disturbed by tourism. First we guaranteed that tourism is damaging the environment with a 10 visitation impact monitoring protocol. Next we predicted that: i) fish that prefer open 11 substrate and the water column would move to more cryptic microhabitats in the presence of 12 visitors, especially if managers do not monitor the touristic activity; and ii) the period when 13 fish are more active would change to periods before or after the tourists were present, more 14 markedly where tourism is not monitored. We also evaluated if analyzing more species gives a 15 more complete scenario of the environment status by observing if species response varied. By 16 studying environments without visitors and with controlled visiting we depicted good 17 comparison to non-monitored visiting areas. 18 19 Materials and Methods 20 21 Study areas 22 Good representative areas to test tourism indicators occur in Nobres, in Mato Grosso, 23 Brazil (14° 43’ 13”S; 56° 19’ 39”W; Fig. 1). Many touristic attractions are located there receiving 24 around 5 thousand visitors every month, according to the touristic agencies operating there. 25 Government and particular investments are improving the tourism in the area and attracting 26 more visitors. Nobres is placed on the Brazilian Central Plateau on limestone soil, there are 27 streams with visibility beyond 20 m due to the flocculation of sediments caused by the calcium 28 carbonate provided by the soil (Strahler, 1952). Those streams sustain rich fauna and flora with 29 strong aesthetic appeal. All these characteristics makes of Nobres an ideal site for aquatic 30 nature tourism, especially in the rivers Estivado, Triste and Salobra, where tourists practice 31 underwater trails. 32 24 In that environment, we could define three treatments, according to the intensity of the 1 tourism: Reference areas (RA), natural areas where visitation does not occur; monitored 2 visitation areas (MVA), where touristic attraction manager strictly monitor tourism (controlled 3 number of tourists, floatation equipment and presence of a guide); and non-monitored 4 visitation area (NMVA), in which the tourism occurs without any sort of regulation. We 5 controlled river depth, diversity of water velocity and depth, combination of pool-riffle-run, 6 substrate coverage, fish abundance and predator abundance (Table 1). 7 To evaluate fish microhabitat preference, we sampled the proportion occupied by each 8 substrate microhabitat with eight 5 m² quadrants randomly placed in each treatment. We 9 identified seven types of microhabitats (Fig. 2) common to the three treatments based on 10 Romero and Casatti (2012): large wood pieces (LW), hard substrate (HS), unconsolidated 11 substrate (US), channel surface (CS), channel center (CC), macrophytes and roots (MR) and 12 litter (LI). Macrophytes and roots were considered two distinct microhabitats by Romero and 13 Casatti (2012), but since macrophytes commonly occurred amidst the roots in our study area, 14 we considered it a single microhabitat. 15 16 Evaluation of the nature tourism impact 17 To test if our treatments are under tourism pressure, we used a visitation impact 18 monitoring protocol (Graefe et al., 1990), which is based on qualitative and quantitative 19 physical, biological and social factors influencing the environment, summarized in Table I. 20 21 Data collection 22 We conducted the in situ study applying snorkeling techniques. Collects occurred from 23 June 2010 to September 2011, always during the dry season. We focused ten species chosen 24 according to their visibility, easiness of identification, abundance and attractiveness to the 25 tourists and diurnal activity period during tourist visitation: Astyanax asuncionensis, Brycon 26 hilarii, Characidium zebra, Cichlasoma dimerus, Crenicichla lepidota, Hyphessobrycon eques, 27 Leporinus friderici, Leporinus striatus, Prochilodus lineatus and Salminus brasiliensis (Fig. 2, see 28 appendix too for the complete species list). Testimony specimens of the smaller species are 29 deposited in the Coleção de Peixes (DZSJRP numbers 14789-14810). 30 For the analysis of microhabitat use we did 30 visual censuses (Labrosse et al., 2002) in 31 10 m transects randomly placed in the treatment area. For 5 min the diver swam along the 32 25 transect at a continuous speed of 2 m.min-1 to avoid bias. We registered the number of 1 individuals of each species, the microhabitat they were at and how exposed or hidden they 2 were. We considered in hidden substrate fish amidst plants, inside wood pieces, buried under 3 the litter or beneath large rocks; on the opposite, we considered in open substrates fish at the 4 surface or mid water, on the litter, sand or rocks. The records along transects were done from 5 08:00 to 12:00 with intervals between sessions of no less than 4 h and no more than 20 days to 6 avoid temporal autocorrelation and seasonal interference, respectively. 7 For the activity period we performed five visual censuses in each treatment, logging if 8 individuals of the ten studied species were active (feeding, moving, outside the shelters) or 9 inactive (immobile by the river bed, inside shelters). The censuses were performed before the 10 arrivals of tourists (06:00), during the morning visitation period (09:00), during the afternoon 11 visitation period (15:00), after visitation period (18:00) and at night (20:00). At night we used 12 indirect light with a red filter to avoid disturbing the animals. Similarly, the censuses did not 13 start before a 10 min adjustment period during which the diver stood still. 14 15 Data analysis 16 A chi-square test was applied to compare the frequency of occurrence of each species in 17 each microhabitat and in open or closed substrate between the treatments. The same test 18 compared the frequency of active versus inactive fish in the three treatments. We considered 19 as expected the values found for the reference areas and as observed the values for monitored 20 visitation areas and non-monitored visitation areas. Significant values were set at α > 0.05. 21 The connectance is a measure generally used to evaluate predators’ specialization, but 22 we used it here to evaluate microhabitat use according to Romero and Casatti (2012). 23 Connectance is the ratio between the number of possible connections and the number of 24 observed connections. The connectance was compared between treatments to check for 25 preference for a microhabitat due to tourism. We used variance to check how much variation 26 occurred between the treatments. We also correlated connectance and microhabitat 27 proportion using a Spearman ranks test (Zar, 1999). 28 29 30 26 Results 1 2 The visitation impact monitoring results demonstrate that the tourism in its current form 3 has already impacted the environment (Table I). As expected, non-monitored visitation areas 4 are the most disturbed environment, with a minor touristic effect on monitored visitation 5 areas. Marginal erosion and modification, riparian forest degradations, nests of C. lepidota, 6 number of visitors and presence of rubbish were the factors that varied the most between 7 non-monitored visitation areas and reference areas. We also registered the hybrid tambacu 8 (Piaractus mesopotamicus x Colossoma macropomum) in both visited areas, an invasive 9 species. 10 Each studied species preferred a microhabitat in the streams (Fig. 2 and 3). Nevertheless, 11 the preference for an open or closed microhabitat was not altered by the touristic use of the 12 area. Microhabitat use was similar between reference, monitored and non-monitored 13 visitation areas (Table II). 14 The fish were generally connected to the same microhabitats, despite how impacted by 15 the tourism the area was. Connectance was not correlated to substrate abundance in any of 16 the treatments (Reference areas: Spearman’s ρ = 0.243; p = 0.600; Monitored visitation areas: 17 ρ = 0.572; p = 0.180; Non-monitored visitation areas: ρ = 0.724; p = 0.066;). The connectance 18 between fish species and microhabitats were similar and had little variation (Reference areas = 19 0.70; Monitored visitation areas = 0.59; Non-monitored visitation areas = 0.61; Variance = 20 0.035) in the three treatments (Fig. 3). 21 All the studied species were more active during the morning and afternoon (Fig. 4). The 22 fish were not more active right before or after the touristic visiting, activity period did not 23 change in response to tourism. 24 25 Discussion 26 27 Against our predictions, the fish did not move from the microhabitats they originally 28 occupied when exposed to tourism, even though this activity is certainly causing impacts, as 29 evidenced by the visitation impact management protocol. Similarly, no change in activity 30 period was observed, taking to the rejection of our second prediction. The species showed 31 27 high connectance to their microhabitats, allowing us to conclude that they are not plastic in 1 relation to this resource. 2 Our behavioral results suggest two possibilities: i) that the tourism was not impacting 3 the streams; or ii) that, although an impact is occurring, our indicators are not efficient at 4 pointing it. We relied on visitation impact management to decide between these possibilities. 5 Visitation impact monitoring is a protocol widely used by tourism managers that applies 6 specific factors to evaluate visitation impacts (Graefe et al., 1990). How arbitrary this protocol 7 is depends heavily on the choice of these factors, but it is considered a better choice than 8 concurrent protocols such as cargo capacity (McCool & Lime, 2001) and recreation opportunity 9 spectrum (Higginbottom, 2004). Thus, we carefully chose the factors used in our visitation 10 impact management protocol. 11 The physical factors we applied refer to structural changes in the habitat due to 12 visitation. The marginal erosion occurs due to an increase in water turbulence and transit of 13 tourists both in the river and by the margins. Building stairs and timbering may serve the 14 touristic activity, but results in changes in habitat structure. Tourists frequently hang on 15 sunken objects and end up breaking those (Rouphael & Inglis, 2001), thus, this is a common 16 indicator used on land protocols. Land protocols also frequently use unofficial tracks and 17 shortcuts (Li et al., 2005), a similar impact occurs when the tourist decides to enter or exit the 18 floatation in unofficial points. 19 Biological factors include impacts to the fauna and flora. Riparian forest can be put down 20 to facilitate tourist access to the river, but at a devastating cost to the environment (Teresa & 21 Casatti, 2010). Unnatural behaviors, such as fish swimming towards the visitors begging for 22 food is a sign of human impact (Milazzo et al., 2006). Invasive species, such as the tambacu 23 hybrid found in the study area, are indicative of impacted areas (Casatti et al., 2010). We also 24 used the presence of reproductive couples of the pike cichlid Crenicichla lepidota as indicator 25 of quality (Pers. Obs.). 26 The social factors involve visitors’ perception and direct impact on the environment. 27 Although the cargo capacity paradigm has failed to protect visited areas (McCool & Lime, 28 2001), the number of visitors per meter of floatation track is an important adjuvant 29 measurement. We also asked five visitors how conserved they recognize the area in a scale of 30 1 to 5 (one being very degraded and 5 being very conserved) and if they could report any 31 inadequate behavior by other people. Finally, we recorded two inadequate visitors’ behaviors: 32 28 feeding the fish (Ilarri et al. 2008) and the presence of rubbish in the water. It is widely 1 accepted that tourism can disturb the environment (McKercher, 1993), including in headwater 2 streams (Teresa et al., 2011b) and in our own study area (Bessa & Gonçalves-de-Freitas, in 3 prep.). Thus, the visitation impact monitoring protocol confirmed that the studied streams are 4 under tourism impacts, especially those in non-monitored visitation areas; ruling out the 5 environmental integrity and confirming that microhabitat use and activity period are not good 6 indicators of tourism impacts. 7 The species we observed were recorded for microhabitats and activity periods that 8 mostly agree with previous studies (Romero & Casatti, 2012 for A. asuncionensis; Sabino & 9 Sazima, 1999 for B. hilarii; Zuanon et al., 2006 for C. zebra; Romero & Casatti, 2012 for C. 10 dimerus; Sazima, 1986 for C. lepidota; Carvalho & Del-Claro, 2004 for H. eques; Bizzotto et al. 11 2009 for L. friderici; Romero & Casatti, 2012 for L. striatus; Teresa et al., 2011a for P. lineatus; 12 and finally Bessa, et al., 2011 for S. brasiliensis). At least two fish species occupied all the 13 microhabitats in our treatments. Microhabitat use is consistent across different study sites and 14 day hour. 15 Fish usually present site fidelity (Zuanon & Sabino, 1998; Cetra et al., 2011; but see 16 Grossman & Ratajczak Jr., 1998 for contrasting data). One of the predictions from the 17 ecomorphological hypothesis (Bock & von Wahlert, 1965; Casatti & Castro, 2006) is that the 18 use of a given microhabitat is determined by each species’ morphological aspects. Considering 19 that a microhabitat puts selective pressures on its inhabitants, it follows that the fish’s body 20 responds to the pressures of that specific microhabitat, making them unsuitable to others. 21 Microhabitat fidelity was previously linked to reducing competition among species with dietary 22 overlap (Cetra et al., 2011). In fact, the predominant plastic diet with high niche overlap of 23 most freshwater fish (Hartley, 1948) may be possible only due to microhabitat fidelity. Thus, 24 occupying a microhabitat is not just a matter of refuge from a threat, but a much more 25 enduring relation, even when threatened by predators. For instance, L. friderici does not 26 shelter under rocks or amidst the vegetation when threatened by predators, but flee within 27 the same microhabitat (Lima et al., 2012). The same can occur in response to human visitors, 28 changing microhabitats seems not to be an option. 29 Because fish species are not leaving their microhabitats, it is likely that with the loss of 30 microhabitat diversity, many species should go extinct. The most connected microhabitats in 31 our study were the channel center, hard substrate and unconsolidated substrate, while 32 29 Romero and Casatti (2012) report marginal vegetation, fine roots, and hard substrate as the 1 most important microhabitats in their cross-watershed study. The low correlation between 2 microhabitat occurrence and fish occupying them in our study may reflect the small fish 3 communities in rheophilic streams (Belliard et al., 1997). This means low competition for space 4 so that the species could move to another microhabitat in response to tourism, which 5 reinforces that a morphological limitation, not competition, prevented the fish from moving. 6 Being restricted to certain microhabitats, the spatial conservation of streams should be a 7 concern in aquatic management programs. 8 Fish did not respond to the presence of the tourists by shifting their activity period 9 either. Cronobiology is the science that studies how organisms cope with time. According to it, 10 every animal, including fish, has an endogenous activity rhythm which is mostly innate, but 11 may be dragged by environmental cues (zeitgebers) such as light-dark cycles (Volpato & 12 Trajano, 2006). We expected that the presence of tourists could function as a zeitgeber, as has 13 been shown for competition (Cetra et al., 2011) and predation (Metcalf et al., 1998), but our 14 results show this is not the case. Even when some plasticity is recognized in the activity period, 15 this is not an immediate response, depending on the exposure to a consistent zeitgeber during 16 critical parts of the fish’s life history (Metcalf et al., 1998). At least the eye morphology has 17 been considered a morphological constrain to activity period plasticity in fish (Schmitz & 18 Wainwright, 2011). The time-budget of the studied species may not allow them to reduce 19 activity during the visitation period or anticipate or delay their active period simply because 20 the fish are not physiologically adapted to being active in a different period. 21 Staying in the same microhabitat and being active in the same period can be interpreted 22 as habituation, but this does not mean lack of impact. The term ‘habituation’ is frequently 23 misused (Bejden et al., 2009), resulting in tourists and managers considering that the animals 24 are well and receptive. Even when habituation does occur, it can harm an animal by reducing 25 its defense behaviors and altering the time spent in other behaviors (Shackley, 1996). Thus, 26 habituation is not a sign of impact cessation, but a reduction of the overall fitness of the 27 species (Higham & Shelton, 2011). 28 Even though our data did not present significant variation among the studied species, 29 this is more likely due to the inefficiency of our metrics than to multiple species analyses being 30 unimportant. Previous studies demonstrate that species respond differently to visitation 31 impact depending on numerous aspects of their biology (reviewed by Blumstein et al., 2005). 32 30 In general, species whose feeding and social habits are impacted by the tourism should be 1 closely watched (Medeiros et al., 2007; Ilarri et al., 2008; Teresa et al., 2011a; Bessa & 2 Gonçalves-de-Freitas, in prep.). 3 Social behavior has a knock-on effect on community structure (Wong, 2012) with direct 4 influence on microhabitat use. When humans affect abiotic variables, which may disturb social 5 stability (Gonçalves-de-Freitas et al., 2008), they also alter group and population structure. In 6 turn, social-species’ populations will influence the community (Waldie et al., 2011). Finally, 7 community structure and microhabitat use are connected; community was responsible for 60 8 to 80% of microhabitat distribution between coral reef fish (Robertson & Gaines, 1986). 9 Visitation impacts on Nobres’ streams are still in the base of this cascade with no measurable 10 impacts on the microhabitat use and activity period. Measuring more base-level changes, like 11 territoriality and other social behaviors, should be more effective. 12 We conclude that microhabitat use and activity period are not good indicators of 13 impacts caused by nature tourism visitation. Further studies should evaluate trophic 14 interactions, sensitive species’ abundance and social behavior as potential indicators. 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Neotropical Ichthyology 4: 107–118. doi: 10.1590/S1679-6 62252006000100012 7 8 37 Table I – Visitation Impact Management (VIM) results demonstrating the effect of tourism on 1 the treatments, but the similarity between the environments in other aspects that could 2 influence microhabitat use and activity period controlled by us. VIM includes both qualitative 3 and quantitative factors, Diversity of water velocity and depth, and Combination of pool-riffle-4 run in accordance with Casatti et al. (2006) scale. RA = Reference Area; MVA = Monitored 5 Visitation Area; NMVA = Non-monitored visitation Area. 6 Factors Measure RA MVA NMVA Ph ys ic al fa ct or s Visible points of marginal erosion m per 100 m 0.86 1.17 5 Visible points of modified margins m per 100 m 0 3.2 12 Broken trunks or roots unities per 100 m 0 1.78 4.25 Non-official exits along the floatation m per 100 m - 2 4 Bi ol og ic al fa ct or s Riparian forest coverage % of forest coverage 80 70 10 Fish swimming towards the visitors Presence or absence Absence Presence Presence Invasive species Presence or absence Absence Presence Presence Nesting Crenicichla lepidota Presence or absence Presence Presence Absence So ci al fa ct or s Cargo capacity visitors per m - 0.04 0.5 Visitors perception of conservation 1 very degraded - 5 very conserved - 5 3.67 Reports of inadequate behavior reports per 5 visitors - 1 3 Artificial fish feeding Presence or absence Absence Absence Presence Rubbish unities per 100 m 0 3 12 U na ffe ct ed fa ct or s Depth m (mean±standard deviation) 1.5±0.3 1.8±0.5 1.4±0.5 Diversity of water velocity and depth Good – Very poor Good Good Good Combination of pool-riffle-run Good – Very poor Good Good Good Total abundance of fish mean±standard deviation 138.1±144.25 135.0±178.64 142.5±47.14 Predator abundance mean±standard deviation 0.5±0.58 1.0±0.81 0.3±0.50 7 8 38 Table II – The fish did not alter their spatial distribution in response to tourism. Microhabitat 1 use by ten species in relation to exposure. N is the sample size. RA = reference area; MVA = 2 monitored visitation area; NMVA = non-monitored visitation Area; E is the expected value and 3 O1 and O2 are the observed values. 4 Species N Individuals in open microhabitats/individuals recorded Analysis RA (E) MVA (O1) NMVA (O2) Highest χ² value Lowest p value Astyanax asuncionensis 114 1 1 1 0 1 Brycon hilarii 274 0.977 0.783 0.467 8.842 0.452 Characidium zebra 71 1 0.955 1 2 0.991 Cichlasoma dimerus 95 0 0 0 0 1 Crenicichla lepidota 69 1 1 0.95 0 1 Hyphesobrycon ecques 24 0 0 0 0 1 Leporinus friderici 257 0.833 0.729 0.809 1.263 0.998 Leporinus striatus 43 0.357 0.197 0.098 2 0.991 Prochilodus lineatus 120 1 0.923 1 2 0.991 Salminus brasiliensis 11 1 1 1 5 0.834 5 Figure 1 – Map of the study area. Location of Nobres (black rectangle) within Mato Grosso 6 (grey area) and Brazil (white) (14º 43’ 13”S; 56º 19’ 39”W), studied rivers and sample sites for 7 the three treatments: Reference Areas (RA); Monitored Visitation Areas (MVA); and Non-8 Monitored Visitation Areas (NMVA). 9 10 Figure 2 – Representation of a stream microhabitats. The fish, which are out of scale, are 11 represented in their preferred microhabitat. LW = Large Wood pieces; HS = Hard Substrate; US 12 = Unconsolidated Substrate; CS = Channel Surface; CC = Channel Center; MR = Macrophytes 13 and Roots; and LI = Litter. Aa = Astyanax asuncionensis; Bh = Brycon hilarii, Cz = Characidium 14 zebra; Cd = Cichlasoma dimerus; Cl = Crenicichla lepidota; He = Hyphesobrycon ecques; Lf = 15 Leporinus friderici; Ls = Leporinus striatus; Pl = Prochilodus lineatus; Sb = Salminus brasiliensis. 16 17 Figure 3 – Frequency of the fish occupying each microhabitats within touristic impact 18 treatments. The fish did not occupy different microhabitats according to the visitation impact. 19 RA = Reference Area; MVA = Monitored Visitation Area; NMVA = Non-monitored visitation 20 Area. LW = Large Wood pieces; HS = Hard Substrate; US = Unconsolidated Substrate; CS = 21 Channel Surface; CC = Channel Center; MR = Macrophytes and Roots; and LI = Litter. 22 23 39 Figure 4 – Activity period of the ten studied species in the three treatments (tourism impact) 1 mostly overlap. RA = Reference Area; MVA = Monitored Visitation Area; NMVA = Non-2 monitored visitation Area; χ² = chi-square test result; p = probability of type I error. 3 4 40 1 Fig. 1 2 3 41 1 Fig. 2 2 3 42 1 2 3 4 5 Fig. 3 6 43 1 2 3 4 5 Fig. 4 6 7 N = 202 χ² = 0.011 p = 0.999 N = 161 χ² = 0.560 p = 0.967 N = 105 χ² = 0.099 p = 0.998 N = 74 χ² = 1.021 p = 0.906 N = 26 χ² = 1.000 p = 0.910 N = 80 χ² = 0.133 p = 0.997 N = 402 χ² = 0.451 p = 0.978 N = 76 χ² = 0.292 p = 0.990 N = 27 χ² = 0.082 p = 0.999 N = 161 χ² = 0.084 p = 0.999 44 Monitored tourism conserves territorial fish 1 2 Eduardo Bessaa,b*, Eliane Gonçalves-de-Freitasb 3 4 aLaboratório de Ecologia Comportamental da Reprodução, Universidade do Estado de 5 Mato Grosso, Rod MT 358, km 7. Tangará da Serra, Mato Grosso, Brazil 6 bDepartmento de Zoologia e Botânica, Universidade Estadual Paulista and Centro de 7 Aquicultura da UNESP, São José do Rio Preto, São Paulo, Brazil 8 * Corresponding author. Tel.: 5565 3311-4918; fax: 5565 3311-4900. Rod MT 358, km 9 7, Jd. Aeroporto PO Box 287 CEP 78300-000. Tangará da Serra, Mato Grosso, Brazil 10 E-mail address: edu_bessa@yahoo.com (E. Bessa). 11 12 Acknowledgements 13 14 We thank Mrs. Joana Lambert, Messrs. Kleber Oliveira, Antônio Campos and Isaías de 15 Almeida for the access to the study sites. We are also thankful to Paola Tomazzelli, 16 Monise Lima, Giliard Balduíno, Ralskd Cariagas and Nathália Szimanski for help 17 during data collection. Fundação de Amparo à Pesquisa de Mato Grosso (FAPEMAT) 18 funded this study. English editing was provided by Nature Publishing Group and funded 19 by Fundunesp. 20 21 22 45 Abstract 1 2 Nature tourism is a growing industry frequently noted as the solution to the conflict 3 between preservation and economic exploitation. Nevertheless, it is known to cause 4 several effects. Here, we address for the first time the idea that monitored tourism 5 avoids triggering the emergency life history strategy in the social cichlid fish, 6 Crenicichla lepidota, in the long term. We studied the aggression toward territorial 7 intruders and the number of nests built in pristine reference areas, in monitored visiting 8 areas and in non-monitored visiting areas. We observed suppressed aggressive behavior 9 and suppressed nesting, presumed fear responses, only in the non-monitored area. We 10 conclude that by monitoring visitations, including the avoidance of stepping on the river 11 bed, artificial fish feeding and a reduced number of visitors, it is possible to avoid the 12 emergency life history strategy that indicates damage caused by nature tourism, even in 13 the long term. 14 15 Keywords 16 17 River snorkeling. Ecotourism. Cichlidae. Emergency life history theory. Sustainable 18 tourism. Social Behavior. Mato Grosso, Brazil. Tourism monitoring techniques. 19 20 Highlights 21 22 � This is a long-term study of nature tourism impact on fish behavior 23 � This study focuses underwater snorkeling trails in rivers 24 � Fish respond to nature tourism changing their social and nesting behavior 25 46 � Monitoring tourism avoids impacts 1 � Floating equipment, time of exposure to visitor and fish feeding should be 2 monitored3 47 Monitored tourism conserves territorial fish 1 2 Abstract 3 Nature tourism is a growing industry frequently noted as the solution to the conflict 4 between preservation and economic exploitation. Nevertheless, it is known to cause 5 several effects. Here, we address for the first time the idea that monitored tourism 6 avoids triggering the emergency life history strategy in the social cichlid fish, 7 Crenicichla lepidota, in the long term. We studied the aggression toward territorial 8 intruders and the number of nests built in pristine reference areas, in monitored visiting 9 areas and in non-monitored visiting areas. We observed suppressed aggressive behavior 10 and suppressed nesting, presumed fear responses, only in the non-monitored area. We 11 conclude that by monitoring visitations, including the avoidance of stepping on the river 12 bed, artificial fish feeding and a reduced number of visitors, it is possible to avoid the 13 emergency life history strategy that indicates damage caused by nature tourism, even in 14 the long term. 15 16 Keywords 17 Ecotourism 18 Cichlidae 19 Emergency life history theory 20 Sustainable tourism 21 Social Behavior 22 Tourism monitoring techniques 23 48 1. Introduction 1 2 All types of natural environments are liable to unpredictable disturbances, and 3 animals must cope with this. These disturbances include natural catastrophes, variations 4 in the predator population or food items and also the impact of human activities. The 5 latter one has become a major concern, and the immediate form of coping with such 6 disturbances is by behavioral responses called emergency life history strategies 7 (Wingfield, 2003). Among human impacts, one recently considered as a potential 8 disturbance is nature tourism. Although about half of the human population lives in 9 cities (Lederbogen et al., 2011), mankind finds comfort in nature, seeking it frequently 10 (Wilson, 1984). The definitions of nature tourism and ecotourism have long been argued 11 (Wallace & Pierce, 1996). Ecotourism is defined as any type of tourism regarding the 12 conservation of natural resources, whereas nature tourism is defined as the visitation to 13 natural landscapes, not necessarily in a sustainable manner (Drumm & Moore, 2003). 14 Accordingly, we will refer to “nature tourism” to describe the act of visiting natural 15 places. 16 Whereas the nature tourism business benefits from human visitations to pristine 17 environments, this activity can result in environmental impacts, causing a dilemma. On 18 one hand, more visits will increase the profits; on the other hand, more visits will 19 degrade what the visitors are attracted to (Machado, 2005). Undoubtedly, nature tourism 20 can disturb the environment by consuming resources, building structures and leaving 21 debris behind (McKercher, 1993). The solution to this dilemma lies in the planned 22 exploitation of natural resources, but empirical data to support this idea are still weak. 23 49 In aquatic environments, non-monitored, nature-based tourism has caused impacts 1 in many places. For instance, tourists capture more fish than all of the local fishing 2 industry (Catella et al., 1997). Populations of turtles were reported to decline in 3 response to human recreation (Garber & Burger, 1995). The number of omnivorous fish 4 increased and the community evenness decreased in a coral reef during visitations (Ilarri 5 et al., 2008). Because of such undesirable effects, it is necessary to evaluate how to 6 monitor activities that were previously established so that nature tourism is sustainable. 7 Fish are potential models for this purpose because they respond to diverse human 8 impacts and they are easy to observe (Amundsen, 2003); it is worth deepening the 9 knowledge of emergency life histories in this group (Wingfield, 2003); they are the 10 main attraction of several aquatic touristic activities, such as diving, fishing and 11 underwater tracks. 12 Aquatic nature tourism is frequently related to coral reefs. However, a less 13 charismatic, but equally important, environment is that of clear water streams. The 14 streams of Nobres, in Mato Grosso, Brazil, are appropriate environments for evaluating 15 the effects caused by non-monitored tourism. The different streams are subject to an 16 array of visitation and monitoring styles, which could be used as treatments to test 17 whether adequate monitoring can prevent visitation impacts. In our case, monitoring is 18 any technique that is used to prevent impacts on the river bed from stepping on it, to 19 protect riparian vegetation and to reduce the fish’s exposure to visitors. 20 Among the various fish species that occur in headwater streams, some are very 21 good models for addressing certain questions. This is the case for cichlids because they 22 tend to stay in within a certain area and do not move along the river (Hert, 1992), thus 23 providing more detailed information about a particular locality. Within the cichlids, a 24 50 behavioral repertoire consisting of territoriality and parental care are characteristic of 1 the group (Keenleyside, 1991; Teresa & Gonçalves-de-Freitas, 2011). Thus, we chose 2 the cichlid Crenicichla lepidota as our model because it is locally abundant, easy to 3 observe and there is available knowledge about its behavior. 4 Behavior is a good way to assess environmental effects because it is the most 5 immediate way that an animal can cope (Wingfield, 2003), it has previously been used 6 as an environmental quality indicator (Teresa et al., 2011a) and it is also considered a 7 key to improving conservation (Caro & Sherman, 2011). Previous studies focused on 8 the acute effects of visitors on fish behavior, i.e., the effects during the presence of 9 visitors (e.g., Duchesne, Côtè, & Barrette, 2000; Constantine, Brunton, & Dennis 2004; 10 White et al., 2008). However, long term effects (i.e., those occurring after the visitors 11 leave) tend to be more informative (Bejder et al., 2006). The long term can be 12 considered because remembering aversive stimuli is known to occur in cichlids 13 (Moreira & Volpato, 2004) and salmonids (Moreira, Pulman, & Pottinger, 2004). Thus, 14 ours is the first study focusing on chronic behavioral effects and relating them to two 15 different levels of monitored visiting. 16 Behavioral changes allow fish to intensify or reduce behaviors, such as 17 territoriality and nesting, in response to visitors. Animals can respond to the sight of 18 visitors (Frid & Dill, 2002), to the food they offer (Milazzo, Anastasi, & Willis, 2006), 19 or to the noise they make (Codarin et al., 2009), resulting in stress and, therefore, in 20 emergency life history strategies. Animals frequently respond to humans like they 21 respond to predators, hiding more during visitation (Frid & Dill, 2002). Thus, non-22 monitored visitation is expected to reduce territorial aggression and reproductive 23 51 behavior because defending a territory and building a nest means expending energy and 1 time and exposure to risks, such as predation (Candolin & Voigt, 2001). 2 One of the ways territoriality may be defined is the defense of an area containing a 3 restrictive resource through aggression (Maher & Lott, 1995). Crenicichla lepidota 4 guards territories containing suitable nest sites which are those with no feeding 5 importance, as is common among cichlids. Territory is, then, part of the reproductive 6 behavior of cichlids, and it is the place where nests are built. Reproduction is the most 7 vulnerable part of the life cycle (Barlow, 1991) and promoting reproduction is an 8 important part of the maintenance of a population. In cichlids, there is evidence that 9 approximately 40% of the individuals die during the egg phase and another 40% die in 10 the larval phase (Cacho, Chellappa, & Yamamoto, 2006). Part of this risk is mitigated 11 by females choosing males with safer nests (Candolin & Voigt, 2001). Likewise, a non-12 monitored area should result in less couples nesting if visitors are considered to be 13 threats. 14 We hypothesized that areas without visitation monitoring will trigger emergency 15 life history strategies, causing the fish to be less proactive (i.e., exposing themselves 16 less to territorial intruders) (Wingfield, 2003), altering the territorial and reproductive 17 behaviors of C. lepidota, whereas reference areas and areas with visitation monitoring 18 will not differ. This introduces three predictions: 1) territorial individuals will not attack 19 invaders as much in non-monitored visitation areas as they will in reference areas or 20 monitored areas; 2) the fish will take longer to attack; 3) fewer nests are expected in the 21 non-monitored visitation areas than in the other areas. We did not predict a gradient of 22 response to tourism from reference areas to non-monitored areas because we trusted and 23 desired to test if monitoring is sufficient for pres