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Long-Term Survey of Key Macrobenthic Species in a Temperate Eutrophic

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Long-Term Survey of Key Macrobenthic Species in a Temperate Eutrophic Long-term survey of key macrobenthic species in a temperate eutrophic estuary and the influence of trematode parasites Susana Margarida de Freitas Ferreira Coimbra, 2005 Susana Margarida de Freitas Ferreira Long-term survey of key macrobenthic species in a temperate eutrophic estuary and the influence of trematode parasites Coimbra 2005 Long-term survey of key macrobenthic species in a temperate eutrophic estuary and the influence of trematode parasites Susana Margarida de Freitas Ferreira IMAR - Institute of Marine Research Department of Zoology Faculty of Sciences and Technology University of Coimbra 3004-517 coimbra, Portugal Telephone: (+351) 239 837 797 / 239 836 386 Fax: (+351) 239 823 603 E-mail: [email protected] Photographs, drawings, book marker and cover designed by the author. Photos from the book marker in sequential order from top to bottom: 1 - Hydrobia ulvae (Gastropoda); 2 & 3 - Maritrema subdolum (Digenea); 4 & 5 - Microphallus claviformis (Digenea); 6 & 7 - Levinseniella brachyosoma (Digenea); 8 - Cyathura carinata (Isopoda); 9- flamingos in an abandoned salina; 10, 11 & 12 - Zostera noltii bed; 13, 14 & 15 - eutrophic area; 16 - a functional salina in the Mondego Estuary. Doctoral dissertation in Biology (Scientific Area of Ecology) presented to the University of Coimbra. Dissertação apresentada à Universidade de Coimbra para prestação de provas de Doutoramento em Biologia (Especialidade em Ecologia). This thesis is based on the following manuscripts: Jensen KT, Ferreira SM, Pardal MA (2004). Trematodes in a Cyathura carinata population from a temperate intertidal estuary: infection patterns and impact on host. Journal of the Marine Biological Association of the United Kingdom 84, 1151-1158. Ferreira SM, Jensen KT, Pardal MA (2005). Infection characteristics of a trematode in an estuarine isopod: influence of substratum. Hydrobiologia 539, 149-155. Ferreira SM, Jensen KT, Martins PA, Sousa SF, Marques JC, Pardal MA (2005). Impact of microphallid trematodes on the survivorship, growth and reproduction of an isopod (Cyathura carinata). Journal of Experimental Marine Biology and Ecology 318, 191-199. Ferreira SM, Cardoso PG, Lillebø AI, Marques JC, Jensen KT, Pardal MA. Digenean trematodes in a southern European population of the estuarine gastropod Hydrobia ulvae. (In preparation). Ferreira SM, Jensen KT, Pardal MA. Infection characteristics and transmission strategies of two digenetic trematodes (Maritrema subdolum and Levinseniella sp.) infecting the isopod Cyathura carinata. (In preparation). Ferreira SM, Brandão A, Baeta A, Neto JM, Lillebø AI, Marques JC, Jensen KT, Pardal MA. Effects of restoration management on the estuarine isopod Cyathura carinata: mediation by trematodes and habitat change. Marine Biology (submitted). i This thesis was supported by: The Portuguese Foundation for Science and Tecnology, through the PhD grant SFRH/BD/5392/2001; IMAR - Institute of Marine Research (Interdisciplinary Center of Coimbra); Department of Zoology from the University of Coimbra; Department of Marine Ecology (Institute of Biological Sciences) from the University of Aarhus. There were many people that accompanied me during the long ride that has culminated in the elaboration of this work. To all of them… my sincere gratitude. To Professor Miguel Ângelo Pardal for the trust that he has confided in me, for all the advices, guidance, support and friendship that were always an asset along the progress developed during all this work. To Professor Kurt Thomas Jensen, who has introduced me to the new exciting world of parasites, for all his patience, advices, supervision, assistance and friendship. To Professor João Carlos Marques, for the possibility that he has granted me to join and work with a fabulous team, as the one from IMAR - Coimbra. To Dr. Patricia Cardoso, for her constant collaboration, friendship and sisterhood that have prevailed for such a long time, as well as for her capacity to be always available to listen and to help in all occasions. To Dr. Ana Lillebø, Dr. João Neto and Dr. Joana Patrício for their patient in putting up with all my questions, for their advices and friendship. To Drª. Maria Gabriel Fontes for her readiness in helping with all the paper work and for her many “healthy” advices. To all the team of IMAR (Coimbra) and collegues from the “Hidrobiologia” unit: Dr. Alexandra Baeta, Dr. Andrea Brandão, Dr. Sílvia Gonçalves, Dr Marina Dolbeth, Dr. Filipe Martinho, Dr. Ricardo Leitão, Dr. Tiago Verdelhos, Dr. Pedro Coelho, Dr. Ricardo Lopes, Dr. Tiago Múrias, Dr. Irene Martins, Dr. Paulo Maranhão, Dr. Elsa Rodrigues, Dr. Heliana Teixeira, Dr. Aranzazú Marcotegui, Dr. Fuensanta Salas, Dr. Adriana Medeiros, Dr. Patrícia Pedro, Dr. Nuno Coimbra, Dr. Maria João Feio, Dr. Manuela Abelho, Dr. Nélson Martins, Dr. Matilde Santos, Dr. Isabel Lopes, Professor Manuel Augusto Graça, Professor Rui Ribeiro, Professor Cristina Canhoto and Professor Jaime Ramos, for all their collaboration and fellowship. To Dr. Sara Sousa and Dr. Alexandre Martins for taking care of the experimental Cyathura carinata in my absence and for bearing my complaints about the lack of cooperation from my computer. To Dr. Majbritt Lassen, Dr. Rikke Warberg, Dr. Kathryn D. Nielsen and all the people from the Department of Marine Ecology, University of Aarhus, for all their help, welcoming and friendship. To Dª Teresa and Dª Helena for their sympathy and efficiency in keeping all the laboratorial material. To my family that, for better or for worst, has supported my decisions and suffered all the consequences. To Pantufa, Nixe, Eneias, “Pexinho”, GG and SMP for existing in my life and for motivating me to do what I love the most. Aknowledgments/ Agradecimentos iii Resumo Um dos principais objectivos deste trabalho é identificar e investigar a influência de tremátodes digenéticos na dinâmica populacional do isópode estuarino C. carinata, para além de descrever padrões temporais de prevalência e intensidade destes parasitas nas populações dos seus hospedeiros intermediários. Pretende-se também estudar o desenvolvimento de C. carinata ao longo de um período de quase 10 anos, num estuário eutrofizado, o estuário do Rio Mondego, onde foi implementado um programa de reabilitação ambiental. A presente dissertação será apresentada em vários capítulos, correspondentes a diferentes manuscritos em preparação, submetidos ou já publicados em revistas científicas. Inicialmente, é feita uma breve introdução à necessidade de desenvolver estratégias de gestão ambiental, com vista a uma utilização sustentável dos recursos costeiros. Nesta secção, são mencionados alguns dos tipos mais frequentes de pressão ambiental em zonas costeiras, nomeadamente processos de eutrofização. Neste cenário são abordados alguns dos problemas que afectam o estuário do Mondego, no qual o isópode C. carinata é uma das espécies-chave das comunidades bentónicas intertidais, e faz-se uma primeira abordagem à possível influência de tremátodes digenéticos. O primeiro capítulo é dedicado à identificação de tremátodes digenéticos que infectam C. carinata (segundo hospedeiro intermediário) e à descrição dos padrões destes parasitas em dois locais chave do estuário: um banco de Zostera noltii e uma zona arenosa eutrofizada. Duas espécies de tremátodes foram dominantes: Maritrema subdolum e uma espécie Levinseniella sp. ainda não descrita, sendo esta última a mais abundante. Geralmente, a prevalência destes parasitas culminou durante os meses de Inverno, quando as aves migratórias limícolas eram numerosas no estuário. Os isópodes do banco de Z. noltii alojaram mais infecções por espécime do que os da zona arenosa. Uma maior densidade de gastrópodes Hydrobia ulvae > 2 mm (primeiro hospedeiro intermediário) e uma fraca abundância de C. carinata naquele local foram apresentados como os motivos mais prováveis para justificar o padrão observado. O segundo capítulo refere-se a uma pequena experiência conduzida com o tremátode M. subdolum e ambos os seus hospedeiros intermediários: H. ulvae e C. carinata. Os resultados indicaram que factores de pequena escala, como diferenças de substrato e características associadas, poderão ter um impacto considerável nas infecções das populações de hospedeiros. C. carinata de um substrato de areia fina, com uma maior proporção de partículas < 125 µm, foram mais activos à superfície e alojavam mais larvas de M. subdolum do que os isópodes de outro tipo de sedimento, também de areia fina. Durante esta experiência de curto prazo, não foram observados quaisquer efeitos induzidos pelos parasitas nos seus hospedeiros. A distribuição de M. subdolum demonstrou que as cercárias penetraram em C. carinata através das estruturas de ventilação deste isópode e que se alojaram depois na zona médio-posterior do corpo do hospedeiro. O terceiro capítulo relata uma experiência laboratorial para avaliar o impacto de tremátodes Microphallidae na sobrevivência, crescimento e fecundidade de C. carinata. Durante quase 12 semanas, isópodes infectados e não infectados foram mantidos a 25ºC. Independentemente dos mecanismos envolvidos, os tremátodes Microphallidae demonstraram que podem ter consequências graves, afectando negativamente a sobrevivência, o crescimento e a fecundidade dos seus hospedeiros. Para espécies com desenvolvimento directo, como C. carinata, a impossibilidade de reprodução induzida por estes parasitas pode contribuir para flutuações de abundância. Por este motivo, recomenda-se que os parasitas sejam reconhecidos como um factor importante que influencia
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