UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL
POPULATION ECOLOGY OF TWO SPECIES OF CAVE-DWELLING BATS (Miniopterus schreibersii and Myotis myotis)
Maria Luísa Sequeira Viana Rodrigues
DOUTORAMENTO EM BIOLOGIA (Ecologia)
2008
UNIVERSIDADE DE LISBOA FACULDADE DE CIÊNCIAS DEPARTAMENTO DE BIOLOGIA ANIMAL
POPULATION ECOLOGY OF TWO SPECIES OF CAVE-DWELLING BATS (Miniopterus schreibersii and Myotis myotis)
Maria Luísa Sequeira Viana Rodrigues
Tese orientada pelo Professor Doutor Jorge M. Palmeirim
DOUTORAMENTO EM BIOLOGIA (Ecologia)
2008
This dissertation should be cited as: Rodrigues L. (2008) Population ecology of two species of cave-dwelling bats (Miniopterus schreibersii and Myotis myotis). PhD Thesis. University of Lisboa, Portugal.
À minha Mãe, à Inês, à Sara e ao Henrique
Nota prévia
Na elaboração desta dissertação, e nos termos do n.º 1 do Artigo 40 do Regulamento de Estudos Pós-Graduados da Universidade de Lisboa, publicado no Diário da República – II Série N.º 153, de 5 de Julho de 2003, esclarece-se que foi efectuado o aproveitamento total dos resultados de trabalhos já publicados ou submetidos para publicação em revistas indexadas de circulação internacional, os quais integram os capítulos da presente tese. Tendo os referidos trabalhos sido realizados em colaboração com Jorge M. Palmeirim, Ana Rainho e Andreas Zahn, a candidata esclarece que participou activamente no planeamento, obtenção, análise e discussão dos resultados, bem como na redacção dos manuscritos. Devido à integração de vários artigos científicos, o padrão de formatação é variável consoante as normas de cada revista.
Lisboa, Janeiro de 2008
Maria Luísa Sequeira Viana Rodrigues
Contents
Agradecimentos/Acknowledgments ix Resumo xi Abstract xix
1. Introduction 1 1.1 Aims 5 1.2 Studied species 5 1.3 Studied topics 11 1.4 Thesis structure 16 1.5 References 17
2. Migratory behaviour 23 Paper I - Rodrigues L. & Palmeirim J.M. (in press) Migratory behaviour 25 of the Schreiber’s bat: when, where, and why do cave bats migrate in a Mediterranean region? Journal of Zoology doi:10.1111/j.1469- 7998.2007.00361.x 3. Spatial behaviour and Gene flow 35 Paper II - Rodrigues L., Ramos Pereira M.J., Rainho A. & Palmeirim 37 J.M. (submitted) Behavioural factors determining potential gene flow among colonies of the Schreiber’s bat Miniopterus schreibersii. Behavioral Ecology and Sociobiology. 4. Critical times 53 Paper III - Zahn A., Rodrigues L., Rainho A. & Palmeirim J.M. (2007) 55 Critical times of the year for Myotis myotis, a temperate zone bat: roles of climate and food resources. Acta Chiropterologica 9: 115-125. 5. Roosting behaviour and Phenology 67 Paper IV - Rodrigues L., Zahn A., Rainho A. & Palmeirim J.M. (2003) 69 Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67: 321-335. 6. General Discussion: the results in the context of bat 85 conservation in Portugal 6.1 Migratory behaviour 87 6.2 Spatial behaviour and Gene flow 91 6.3 Critical times 94 6.4 Roosting behaviour and Phenology 96 6.5 Future work 98 6.6 References 100
vii
Agradecimentos/Acknowledgments
Queria desde já agradecer às muitas pessoas que tornaram possível este trabalho. Ao Professor Doutor Jorge Palmeirim agradeço o ter-me escolhido como estagiária em 1987, permitindo a minha entrada no mundo extraordinário dos morcegos e das grutas! A confiança e amizade demonstradas ao longo destes já muitos anos deram-me o incentivo para me atirar ao mestrado e agora ao doutoramento! Agradeço igualmente ao Dr. Carlos Magalhães o ter acreditado que eu daria conta do recado e ter-me aberto as portas do Instituto da Conservação da Natureza e da Biodiversidade (ICNB) mesmo antes de ter acabado o curso. O desenvolvimento de estudos de ecologia aplicada à conservação, que têm constado dos planos de actividades do ICNB desde 1987, só foi possível com o apoio de todos os chefes que passaram pela nossa Divisão: Dr. Carlos Magalhães, Dra. Maria João Cabral, Dra. Elisa Oliveira, Eng. Carlos Romão, Dra. Márcia Pinto, Dra. Anabela Trindade, Dr. Mário Silva e Arq. Maria da Glória Araújo. A todos agradeço o facto de acreditarem que o nosso trabalho tem ajudado a conservar os morcegos portugueses! Ao ICNB (nomeadamente, à Dra. Lurdes Carvalho e ao Prof. João Rosmaninho de Menezes) agradeço a licença de três meses com vencimento, que facilitou a preparação desta tese. À amiga Ana Rainho, companheira de luta pelos morcegos, agradeço as inúmeras e variadas ajudas (muitas, muitas, muitas dicas de computadores, auxílio no campo, leitura do texto,…). Aos morcególogos Hugo Rebelo, Sofia Lourenço, Maria João Pereira e Tiago Marques, quero agradecer o companheirismo e boa disposição sempre presentes nas muitas saídas de campo. Os disparates ditos ao longo de tantos milhares de quilómetros transformaram as intermináveis viagens em momentos de paródia… À Sofia agradeço também a ajuda no alindamento da tese… À Patrícia Salgueiro agradeço muitas dicas para a tese. Tendo em conta que o trabalho de campo não podia ser realizado sozinha, só foi possível fazer tantas centenas de saídas de campo ao longo destes anos com a ajuda de muitos amigos e familiares. Entre eles destacam-se Nuno Vieira, Francisco Rasteiro e Gabriel Mendes, que comigo partilharam muitas horas de grutas e anilhagem.
ix Agradecimentos/Acknowledgments
I thank Andreas Zahn for his enthusiasm and perseverance in the preparation of two papers, and especially for his friendship. Ao Francisco Rasteiro agradeço as fotografias lindas que me emprestou para ilustrar como estes animais são bonitos. Não se percebe como há tantas pessoas que os acham feios; provavelmente nunca viram fotografias como estas… Aos colegas espanhóis agradeço toda a cooperação, em particular ao Godfried Schreur, Ana Cordero, Juan Quetglas, Elena Migens, Carlos Ibáñez e Óscar de Paz. Obrigada por terem enviado os dados das recapturas! Peter Lina, Hugo, Luzia Sousa, José Garrido Garcia, Oscar de Paz, Godfried, Carlos and Marie-Jo Dubourg-Sauvage provided many papers. Thanks for this enormous help! Besides anonymous referees, the manuscripts were reviewed by Allen Kurta, Paul Racey, Jens Rydell, Sólveig Thornsteinsdóttir, Tony Hutson, Luka Clarke, and Tony Mitchell-Jones (a very special thank to Tony, who really helped a lot in the paper about migration!). Thanks a lot for all suggestions! Aos eternos amigos Rec´s da melhor casta da FCUL (83-87) (em particular à Mena, Pedro Beja, António, Lino, João e Pedro Raposo) e aos colegas do ICNB (em particular à Margarida, Mónica, Júlia e D. Conceição) agradeço o permanente incentivo.
Por fim, os agradecimentos (ainda) mais especiais… Às minhas sobrinhas Sónia e Rita, pelo “babysitting” da Sara, que me deu mais paz para acabar a tese. À minha Mãe, que me passou a sua coragem e garra de vida! A sua presença e todo o apoio que nos dá são essenciais nas nossas vidas… As muitas tardes que passou com a Sara facilitaram a escrita dos capítulos finais. À minha “filha grande” Inês, que já me acompanha muitas vezes nas idas às grutas e que tanto gosta de fazer os registos dos dados da anilhagem, obrigada por seres como és e me fazeres tão feliz… À minha “filha pequenina” Sara, que apareceu nas nossas vidas há poucos meses e que é um bebé adorável, obrigada por seres tão calminha, o último artigo foi escrito durante as tuas sestas… Ao meu marido Henrique, com quem tenho partilhado os últimos anos, pelo seu amor para além da muita ajuda (no campo, na preparação dos últimos artigos, na leitura do texto...). Esta tese é também um bocadinho tua!
x Resumo
Contexto A Ordem Chiroptera inclui mais de 1000 espécies e tem uma ampla distribuição a nível mundial. Para além de terem um papel de destaque em termos de biodiversidade, os morcegos têm enorme importância científica, ecológica e económica. Muitas espécies de morcegos apresentam uma situação preocupante, reflectida no número crescente de espécies que têm vindo a ser classificadas como ameaçadas pela UICN à escala global (pertencendo às categorias criticamente em perigo, em perigo ou vulnerável). As principais ameaças a que estas espécies estão sujeitas são a perda ou alteração do habitat, a destruição e/ou perturbação dos abrigos (sobretudo nas épocas de hibernação e maternidade), o uso excessivo de pesticidas e a perseguição directa. Estas causas de ameaça podem ainda ser agravadas por factores intrínsecos, tais como a raridade e uma taxa reprodutora reduzida. Das 26 espécies de morcegos inventariadas em Portugal, 24 ocorrem no continente e muitas são consideradas ameaçadas. Tendo em conta que todas as espécies reconhecidamente ameaçadas ocupam abrigos subterrâneos durante pelo menos parte do ano, torna-se óbvio que as espécies cavernícolas apresentam uma situação particularmente difícil no nosso país. É, no entanto, de notar que situações semelhantes ocorrem em muitos outros países da Europa e de outras regiões do Mundo. É aceite que a principal causa de ameaça da maior parte das espécies cavernícolas é a perturbação dos abrigos durante os dois períodos mais sensíveis, correspondentes à hibernação e à maternidade, sendo a maioria destas espécies particularmente vulnerável porque se concentra num número muito reduzido de abrigos. A grande concentração destas espécies deve-se ao facto de algumas terem hábitos coloniais e de existirem poucos abrigos com as condições microclimáticas adequadas para cada estação do ano. Os morcegos portugueses estão protegidos por legislação nacional e internacional, tendo sido publicado em 1992 o Plano Nacional de Conservação dos Morcegos Cavernícolas. Decorrentes da implementação do Plano e da legislação, várias medidas de conservação foram tomadas no nosso país nas últimas duas décadas. Embora estas medidas tenham sido importantes, devem ser tomadas medidas adicionais para alterar a situação desfavorável que as espécies cavernícolas têm em Portugal. No entanto, para o planeamento destas medidas são necessários
xi
Resumo mais conhecimentos sobre a biologia das espécies de morcegos, como a sua ecologia populacional. Neste contexto, foi decidido estudar vários aspectos da biologia relevantes para a definição de padrões populacionais, utilizando como modelo as duas espécies cavernícolas mais abundantes no país: Miniopterus schreibersii e Myotis myotis.
Objectivos Foram estabelecidos quatro objectivos fundamentais a alcançar por esta tese: (1) estudar os padrões de migração e as suas causas, (2) determinar como o comportamento espacial (dispersão e migrações) influencia a estrutura das populações e o fluxo genético potencial entre maternidades, (3) determinar se existem épocas críticas ao longo do ciclo anual, e (4) estudar como o comportamento nos abrigos (sociabilidade e preferências térmicas) e a fenologia se relacionam com o clima.
Comportamento migratório Este estudo foi realizado usando Miniopterus schreibersii como espécie-modelo e baseou-se em dados de captura-recaptura recolhidos entre 1987 e 2005. Foram anilhados mais de 36000 indivíduos e registadas mais de 8000 recapturas, tornando estes dados sobre migrações provavelmente os mais completos já alguma vez recolhidos com morcegos. As principais conclusões podem resumir-se da seguinte forma: - Nos Invernos com temperatura e precipitação médias M. schreibersii hiberna, tendo sido registados poucos movimentos nesta época do ano. No fim da hibernação as fêmeas migram para os abrigos intermédios de Primavera e, mesmo antes dos nascimentos (no início de Junho), para as maternidades; esta chegada tardia pode ser uma estratégia para evitar uma acumulação prejudicial de parasitas. Logo após a independência dos jovens, as fêmeas adultas migram para os abrigos onde vão passar o Outono e, por vezes, também o Inverno. Os jovens permanecem nas maternidades até mais tarde, provavelmente porque as temperaturas mais elevadas a que aí estão sujeitos aceleram o seu crescimento. O padrão de migração dos machos é semelhante ao das fêmeas, mas o abandono dos abrigos de hibernação dá-se mais tarde e trocam mais frequentemente de abrigo durante a época de maternidade; chegam também mais tarde aos abrigos de hibernação, possivelmente porque necessitam de mais tempo para acumular reservas para o Inverno, depois de terem perdido muita energia na época das cópulas.
xii Resumo
- Os indivíduos das várias maternidades passam o seu ciclo anual em áreas vitais bem definidas (média=19030 km2), existindo frequentemente sobreposição de áreas vitais de colónias distintas. A época do ano em que os morcegos estão mais longe dos abrigos de maternidade é a hibernação, mas mesmo nessa fase 80% dos indivíduos não se afasta mais que 90 km. Cada abrigo de hibernação é ocupado por morcegos de várias maternidades, numa área de influência de cerca de 10770 km2. - O maior deslocamento detectado de M. schreibersii foi de 306 km. - Comparando duas possíveis razões para a existência de migrações regionais em M. schreibersii (nomeadamente, temperatura no abrigo e nas áreas de alimentação), concluímos que a temperatura do abrigo e as vantagens metabólicas que lhe estão associadas são a causa principal para as migrações regionais observadas.
Comportamento espacial e Fluxo genético Para este estudo utilizámos os dados de captura-recaptura de Miniopterus schreibersii referidos anteriormente. As conclusões alcançadas incluem os seguintes pontos: - Comparando as três fontes potenciais de fluxo genético entre as maternidades analisadas (nomeadamente, dispersão de jovens para outras colónias, troca de colónia por adultos, e cópulas entre indivíduos de diferentes colónias), concluímos que o principal mecanismo de fluxo genético entre maternidades de M. schreibersii é a ocorrência de cópulas entre indivíduos de colónias diferentes. As recapturas sugerem que o impacto desta mistura nas oportunidades de cópula é tal que fêmeas de algumas colónias têm maior probabilidade de se cruzar com machos de colónias diferentes do que com machos da sua própria colónia. - Apesar de não terem sido registados casos de dispersão de jovens, não significa que estes não conhecem outros abrigos de maternidade; fora da época de maternidade, foram recapturados vários jovens em abrigos de maternidade diferentes daquele onde nasceram. - Relativamente aos adultos, foram observados muito poucos casos de dispersão de fêmeas e mesmo os machos mostraram uma forte ligação à colónia em que nasceram. No entanto, apesar desta ligação às suas colónias durante a época de maternidade, os morcegos adultos de ambos os sexos conhecem outras maternidades e visitam-nas regularmente fora desta época. - O fluxo genético entre maternidades está limitado pela distância entre as colónias e pela existência de abrigos de cópula entre elas. É assimétrico, sendo a direcção do fluxo dominante das colónias maiores para as menores.
xiii Resumo
- As nossas observações da filopatria e migrações sazonais e a tabela de fluxo genético potencial resultante, são compatíveis com a estrutura genética da população recentemente estudada por Ramos Pereira et al. (submetido), tanto para o ADN mitocondrial como para o ADN nuclear. Este facto corrobora a ideia de que os parâmetros comportamentais descritos são em grande parte responsáveis pela definição da estrutura genética observada. O estudo genético tinha encontrado diferenças evidentes entre colónias ao nível do ADN mitocondrial; como este tipo de ADN só pode ser transferido pelas fêmeas, estas diferenças podem ser explicadas pela falta de dispersão que observámos nas fêmeas jovens e adultas, que elimina a possibilidade de o fluxo genético ser mediado pelas fêmeas. No estudo genético tinha também sido observado que a estrutura ao nível do ADN nuclear, que é disperso pelas fêmeas e pelos machos, era muito menos marcada que a do ADN mitocondrial; esta homogeneidade pode ser explicada pela elevada probabilidade de cópulas potenciais que calculámos entre machos e fêmeas pertencentes a maternidades diferentes. Outra conclusão da análise genética foi a evidência de algum isolamento pela distância ao nível do ADN nuclear; o mesmo fenómeno foi encontrado por nós nas estimativas de cópulas potenciais entre colónias calculadas com dados de captura-recaptura. A forte correlação entre as nossas estimativas de cópulas potenciais entre colónias e a distância genética, sugere que o comportamento espacial é em grande parte responsável por essas distâncias. - A população das sete maternidades estudadas parece estar dividida em três subpopulações: Norte (apenas com a colónia Miranda Douro), Centro-Oeste (incluindo Alcanena, Tomar, Sesimbra I, Marvão e Moura I) e Sul (apenas com a colónia Loulé I). As subpopulações apresentam-se com um nível de isolamento variável: a do Norte parece estar completamente isolada, e as colónias do Centro-Oeste e do Sul parecem também estar bastante isoladas entre si. No entanto, a situação das colónias Marvão e Moura I é menos clara: Marvão tem uma pequena ligação às outras colónias da subpopulação do Centro-Oeste, e Moura I parece estar ainda mais isolada destas colónias; de facto, Moura I encontra-se mais próxima de Loulé I, tanto ao nível genético como geográfico. Numa perspectiva precaucionária, considerámos que Marvão devia ser considerada uma subpopulação à parte.
Épocas críticas A existência de épocas críticas foi estudada em Myotis myotis, tendo o estudo sido realizado em duas áreas climaticamente diferentes, Portugal e Alemanha. Foi estudada a variação sazonal na condição corporal dos morcegos (equivalente à razão entre o peso e o comprimento do antebraço), medida em 2100 indivíduos em Portugal
xiv Resumo e em 1950 indivíduos na Alemanha, capturados entre 1987 e 2002. Relativamente a este estudo, concluímos: - Em Portugal, foi encontrada uma época crítica, correspondendo ao verão (Junho a Setembro). No entanto, foi considerado que a hibernação (meio de Dezembro ao fim de Fevereiro) poderá também ser um período difícil para os morcegos portugueses. Na Alemanha, as épocas críticas incluem a longa hibernação (Novembro a Março/Abril) e, por vezes, o início da Primavera (Abril) devido à dificuldade de alimentação nos anos em que o mau tempo se prolonga. - A variação na condição corporal nas duas áreas estudadas demonstrou diferenças nas várias fases do ciclo anual, sugerindo que o ambiente influencia as duas populações de forma diferente. Depois dos nascimentos, as fêmeas adultas portuguesas apresentam uma condição corporal baixa e só aumentam de peso no Outono, enquanto que as alemãs mantêm uma boa condição nesta fase. Embora na Alemanha as fêmeas iniciem a hibernação em melhores condições do que as portuguesas, no fim desta época apresentam uma condição corporal pior, visto o Inverno ser mais longo no norte. Embora os recursos alimentares sejam abundantes quando os animais saem da hibernação, a condição das fêmeas alemãs permanece baixa durante mais um mês. Os padrões dos machos são muito semelhantes aos das fêmeas nos dois países. - Os morcegos portugueses nunca atingiram condições corporais tão baixas nem tão altas como as dos morcegos alemães. - M. myotis é fortemente dependente de artrópodes do solo, especialmente Carabidae e outros Coleoptera. No entanto, a dieta é mais diversa em Portugal, onde inclui uma grande proporção de Gryllidae (item não consumido na Alemanha).
Comportamento nos abrigos e Fenologia Tal como o tema anterior, este estudo foi conduzido em Portugal e na Alemanha, usando Myotis myotis como espécie-modelo. A análise foi realizada com 821 indivíduos capturados em Portugal e 2241 capturados na Alemanha, entre 1997 e 1999; adicionalmente, foram também incluídas observações realizadas desde 1987 em Portugal e desde 1991 na Alemanha. As conclusões atingidas são as seguintes: - Em Portugal, a maioria das maternidades de M. myotis utiliza abrigos subterrâneos. Nestes abrigos, mais frios e com uma temperatura mais estável que os usados pela espécie na Alemanha, as fêmeas reprodutoras e alguns machos organizam-se em grandes grupos compactos, que permanecem nos mesmos locais por longos períodos. As colónias podem mudar de lugar dentro do mesmo abrigo,
xv Resumo frequentemente ficando na mesma sala ou galeria. Os machos que se juntam às colónias de maternidade tendem a ser mais jovens e a ter epidídimos mais pequenos do que os que permanecem isolados. As colónias são em geral maiores que as observadas na Alemanha, e por vezes estão associadas a outras espécies como Myotis blythii, Rhinolophus mehelyi e, sobretudo, a M. schreibersii. Os nascimentos ocorrem mais cedo no nosso país. Na Alemanha todas as maternidades utilizam edifícios, em particular sótãos. Nestes abrigos observam-se grandes variações térmicas ao longo do dia e da época de maternidade, que provocam alterações na densidade e localização dos grupos de morcegos. As colónias são compostas quase exclusivamente por fêmeas, e não se conhecem colónias mistas com outras espécies. - Em Portugal há concentração de territórios de cópula de machos de M. myotis em áreas específicas dos abrigos, situação nunca observada na Alemanha. - O início da época das cópulas de M. myotis é síncrono em Portugal e na Alemanha, mas em Portugal as cópulas prolongam-se até mais tarde. - Em Portugal a hibernação de M. myotis inicia-se mais tarde e termina mais cedo, durando apenas cerca de dois meses, em contraste com a situação na Alemanha, onde dura cinco meses. Durante o Inverno, nos dois países, os morcegos desta espécie dispersam-se, sendo a maioria dos abrigos utilizados desconhecida. - A maturidade sexual de M. myotis é atingida mais cedo em Portugal, onde a maioria dos jovens dos dois sexos se reproduz no primeiro ano. Na Alemanha, as fêmeas e a maioria dos machos reproduzem-se apenas no segundo ano.
Aplicação dos resultados à conservação Os resultados obtidos permitem dar suporte científico a algumas medidas de conservação que têm vindo a ser tomadas nos últimos anos e espera-se que contribuam para a aplicação de medidas adicionais para a conservação de morcegos cavernícolas em regiões mediterrânicas. Neste contexto, é apresentada uma discussão detalhada da aplicação dos resultados a medidas de conservação, dando particular ênfase às populações de Miniopterus schreibersii e Myotis myotis em Portugal. Em particular, são discutidas: (i) as épocas do ano em que os abrigos de M. schreibersii e M. myotis não devem ser perturbados, (ii) a preferência térmica dos abrigos de M. schreibersii nas várias épocas do ano e de M. myotis nas épocas de criação e de hibernação, importante no caso de haver alterações no uso sazonal dos abrigos e no planeamento de abrigos de substituição que venham a ser criados, (iii) a rede de abrigos associados a cada colónia de criação de M. schreibersii, que devem ser monitorizados e protegidos, (iv) a grande filopatria das fêmeas de M. schreibersii às suas colónias de criação, e as implicações na sua gestão como unidades
xvi Resumo demograficamente autónomas, (v) a divisão da população das sete colónias de criação de M. schreibersii estudadas em quatro subpopulações, que devem ser tratadas como diferentes Unidades de Gestão, (vi) a importância dos abrigos de cópula de M. schreibersii, que devem continuar a ser inventariados e, se possível, protegidos, e (vii) a disponibilidade de recursos alimentares ser um factor limitante para M. myotis durante algumas épocas do ano, o que implica que as áreas de alimentação em redor das colónias mais importantes sejam geridas de forma a fomentar a utilização de práticas agrícolas ambientalmente adequadas e amigáveis para os morcegos. Dada a existência de migrações entre Portugal e Espanha e a provável existência de subpopulações transfronteiriças, não podemos esquecer que a situação dos morcegos migradores portugueses beneficiaria da cooperação com Espanha, tanto ao nível de acções de investigação como de conservação.
Tendo em conta que é desejável continuar a investigação para clarificar e fortalecer alguns padrões e estudar tópicos adicionais, são apresentadas as linhas de trabalho que seria importante desenvolver no futuro.
Esperamos que a conservação dos morcegos no Mediterrâneo, e em particular em Portugal, beneficie dos resultados desta tese. A necessidade de obter conhecimentos que permitam a implementação de medidas apoiadas em estudos científicos sólidos esteve sempre na base do planeamento deste trabalho. Apenas estudámos parte dos aspectos da biologia relevantes para a conservação, e apenas para duas espécies, ainda que os resultados sejam também relevantes na gestão de outras espécies ecologicamente próximas. No entanto, tendo em conta que os morcegos são organismos pouco conhecidos e difíceis de estudar, sentimos que é uma adição significativa ao trabalho que tem vindo a ser realizado por outros investigadores de países mediterrânicos; juntos estamos a construir o conhecimento que permite uma conservação eficaz dos morcegos nesta região, numa altura em que as alterações da paisagem e as políticas europeias trazem novos desafios, responsabilidades e oportunidades de conservação no continente europeu.
Palavras-chave: Morcegos, conservação, migrações, comportamento espacial, fluxo genético, épocas críticas, comportamento nos abrigos, fenologia
xvii
Abstract
Many bat species, particularly cave-dwellers, present an unfavourable conservation status on a global level. All bats presently considered as threatened in Portugal are cave-dwellers, which shows that the conservation of this group of species requires an active management programme. However, the planning of management measures requires a good knowledge of some aspects of the biology of species, including their population ecology. Much of this critical knowledge is still missing, as bats are among the least studied of vertebrates. To contribute to overcome this limitation, we planned four general objectives for this thesis: (1) understand bat migration patterns and their causes, (2) determine how spatial behaviour influences population structure and potential gene flow among maternity colonies, (3) determine if there are critical times during the yearly cycle of bats, and (4) understand how roosting behaviour and phenology relate to ambient and roost climate. The two first objectives were studied with Miniopterus schreibersii and the latter with Myotis myotis. We discussed the results in the perspective of planning of management measures, particularly in the Portuguese context. Our results increased the understanding of the biology of the two studied species, gave scientific support to some conservation measures that are already being taken, and will hopefully serve as a base for the application of additional management measures to protect cave-dwelling bats in Portugal and other Mediterranean areas. Finally, we indicate possible avenues or the continuation of the work done in this thesis, which we find to be both scientifically interesting and important for the planning of technically sound conservation programmes.
Key-Words: Bats, conservation, migrations, spatial behaviour, gene flow, critical times, roosting behaviour, phenology
xix
1
Introduction
1
1. Introduction Bats belong to the order Chiroptera, which traditionally is divided in two suborders – the Megachiroptera (often known as Old World fruit bats) and the Microchiroptera (including all European species). Other classifications have been suggested (e.g., Van den Bussche & Hoofer 2004; Jones & Teeling 2006), but no consensus has been reached. They are present throughout most of the World, except the Arctic and Antarctic and a few isolated oceanic islands (Mickleburgh et al. 2002). The capacity of flight and the sophistication of the echolocation system that many species have, make them unique and of major scientific importance (Hill & Smith 1986). With more than 1000 species (Mickleburgh et al. 2002), they are also an important part of the mammalian biodiversity. Moreover, this huge number of species is reflected in a great ecological diversity, for example in terms of roosting and feeding behaviour. Bats use multiple types of roosting habitats, such as trees, caves and mines, buildings, bridges and cliffs, and some species even choose different types of roosts along their annual cycle. Their feeding habits are also very diverse, as they can be, for example, insectivorous, carnivorous, piscivorous, frugivorous, nectarivorous or pollinivorous. They often play a crucial role in the maintenance of the ecosystems, as predators of arthropods, prey to other vertebrates, seed dispersers or pollinators (Altringham 1996). Cave-dwelling species have the additional ecological function of importing organic matter to caves, which supports communities of invertebrates that thrive in these underground ecosystems (Palmeirim & Rodrigues 1992). Bats can also be of significant economic relevance for a variety of reasons. In some tropical countries the large deposits of guano which build up under bat colonies are still an economically important agricultural fertilizer (Altringham 1996). In addition, insectivorous bats control insects that are important agricultural pests or vectors of diseases, thus avoiding major economic damages (Palmeirim & Rodrigues 1992). Finally, they are of importance in medical research, which takes advantage of some unique aspects of their biology, such as their mechanism of thermoregulation, the anticoagulant protein in vampire’s saliva, and their orientation system (Yalden & Morris 1975; Hill & Smith 1986; Liberatore et al. 2003). There is evidence that bat populations in many parts of the world are in decline and that the range of many species has contracted (Altringham 1996). This unfavourable conservation status is reflected in the increasing number of species included in the IUCN categories of threat at a global level (Racey & Entwistle 2003). In 2007 it was estimated that 24% of the bat fauna was listed as threatened (critically endangered, endangered or vulnerable) (IUCN 2007a). Intrinsic factors, such as low
3
Chapter 1 reproductive rate and rarity, for some species, may exacerbate the consequences of the threats that affect bats (Racey & Entwistle 2003). It is considered that the most general threats to bats are habitat loss or modification, roost loss or disturbance (especially during hibernation and maternity seasons), excessive use of pesticides, and deliberate persecution (Mickleburgh et al. 2002). However, there are other threats that are becoming increasingly important, such as the mortality caused by cars and wind turbines (Cabral et al. 2005). Twenty-six species of bats are known in Portugal, 24 of which in the continental part of the territory. Presently, 38% of the species occurring in Continental Portugal are classified as threatened (Cabral et al. 2005). Cave-dwelling bats have a particularly unfavourable situation in the country, and all threatened species are cave-dwellers at least during part of the year. It is considered that the problem of these species is the disturbance of underground roosts during the two most sensitive seasons, hibernation and maternity (Cabral et al. 2005). Most cave-dwelling species are highly colonial, and few underground sites provide suitable seasonal microclimatic characteristics to harbour bat colonies. The consequent concentration of the populations of some species in a reduced number of sites increases their vulnerability (Palmeirim & Rodrigues 1992). In this thesis we consider cave-dwelling species those that regularly hibernating and/or breed in underground roosts in Portugal: Miniopterus schreibersii, Myotis myotis, M. blythii, M. nattereri, M. emarginatus, Rhinolophus ferrumequinum, R. hipposideros, R. euryale and R. mehelyi. In addition, seven other species are occasionally found in this type of roost: Myotis bechsteinii, M. mystacinus, M. daubentonii, Eptesicus serotinus, Plecotus auritus, P. austriacus and Barbastella barbastellus. Portuguese bats are protected by legislation, namely EU Habitats & Species Directive (Decreto-Lei nº 140/99, de 24 de Abril), Bonn Convention (Decreto-Lei nº 103/80, de 11 de Outubro), EUROBATS – The Agreement on the Conservation of Populations of European Bats (Decreto-Lei nº 31/95, de 18 de Agosto) and Bern Convention (Decreto-Lei nº 316/89, de 22 de Setembro). In 1992 a Conservation Plan for Cave-dwelling Species was published (Palmeirim & Rodrigues 1992), which included a list of management actions per roost. In the sequence of this conservation plan and of the existing legislation a number of conservation measures have been implemented, such as: (1) inclusion of most important roosts in Special Areas of Conservation designated for Natura 2000 network, (2) an annual monitoring programme of the most important hibernation and maternity roosts, in course since 1987, (3) fencing of five important roosts to minimize disturbance, (4) stabilization of
4 Chapter 1 the ceiling of one roost, (5) construction of two replacement roosts to compensate the destruction of two underground galleries that harboured bats, (6) regular trimming of the vegetation around roost entrances to keep the passage free for bats, and (7) closing off abandoned mines that pose security threats with methods that are compatible with the continuation of their use by bats. Although these measures have been important to protect Portuguese cave- dwelling bats, additional measures need to be taken to reverse the unfavourable situation of these species in the country. However, the correct planning of these measures requires more background information, especially on population ecology of bats. In this context, we aimed to study several aspects of the ecology of cave-dwelling species which are relevant to understand their population patterns and conservation requirements.
1.1 Aims Using Miniopterus schreibersii and Myotis myotis as models, this dissertation aims at contributing to four major issues that are relevant for the conservation of bats: (1) understand bat migration patterns and their causes (2) determine how spatial behaviour influences population structure and potential gene flow among maternity colonies (3) determine if there are critical times during the yearly cycle of bats (4) understand how roosting behaviour and phenology relate to climate
1.2 Studied species The two most abundant cave-dwelling species were used in these studies, Miniopterus schreibersii for objectives (1) and (2), and Myotis myotis for objectives (3) and (4). A brief description of the aspects of their biology that are most relevant for the studied topics is presented.
Miniopterus schreibersii (Kuhl, 1817) - Schreiber’s bat The classification of the genus Miniopterus is still controversial; while some authors include it in the family Vespertilionidae others classify it as a separate family, Miniopteridae. Identification - M. schreibersii is a median size bat: head-body 50-62 mm; tail 56-64 mm; forearm 45-48 mm; wingspan 305-342 mm; weight 9-16 g (Schober & Grimmberger 1989). The fur is greyish, silky and very dense, the underparts are slightly lighter than the back, the basal half of the hair is much darker then the terminal half, the
5 Chapter 1 long and narrow wings are a little darker than the fur, and the ears are very short and have a characteristic square shape (Palmeirim 1990) (Fig. 1.1).
Fig. 1.1 – Miniopterus schreibersii (Photo: Francisco Rasteiro).
Distribution - It was once considered the most widespread bat in the world (Palmeirim & Rodrigues 1995), but recent molecular studies have demonstrated that this taxon is a paraphyletic assemblage comprising several species. Following the latest taxonomic studies we use the name M. schreibersii for Mediterranean, Miniopterus fuliginosus for Asian, Miniopterus oceanensis for Australian (Tian et al. 2004), and Miniopterus natalensis for South African (Miller-Butterworth et al. 2005) populations. In this context, M. schreibersii is present in North Africa and from Portugal to the Caucasus (Rodrigues 1999). It occurs throughout the Portuguese mainland, where 15 major hibernation sites (i.e. used regularly by more than 100 individuals) and 12 maternity roosts are presently known (Fig. 1.2). Habitat - It roosts almost exclusively underground, especially in caves and abandoned mine galleries (Palmeirim & Rodrigues 1992). Isolated individuals or small groups are sometimes found in other types of shelters, such as attics (Rodrigues 1999). It is a gregarious species, forming large colonies throughout most of the year (Rodrigues 1999). During winter colonies are normally monospecific, but during summer they are often mixed with other species such as M. myotis, M. blythii, Rhinolophus mehelyi and R. euryale. It is the most abundant cave-dwelling species in the country, and one of the largest maternity colonies known in Europe occurs in Portugal, comprising around 20000 bats (Palmeirim & Rodrigues 1992).
6 Chapter 1
Fig. 1.2 – Maternity and hibernation roosts (black and white, respectively) of Miniopterus schreibersii known in Portugal.
Annual cycle – Few roosts present morphological and microclimatic characteristics suitable for the full annual cycle of these bats. Therefore, bats are forced to make seasonal movements between roosts, so most of these are only occupied during part of the year. Adult females often settle in maternity roosts just before giving birth. Some males and non-breeding females can also be found with them, but most remain in other shelters. After fledging, most maternity roosts are abandoned and the animals disperse to mating roosts. In colder winters most bats assemble again in a reduced number of roosts and hibernate; in milder winters bats may remain active and scattered in many roosts. In spring, bats leave the hibernation shelters and, after a period of frequent movements, move to maternity roosts (Palmeirim & Rodrigues 1992, 1995). Migration – It performs regional migrations of usually less than 100 km but occasional long movements are known. The longest movement, 833 km, was recorded in Spain (Benzal pers comm in Hutterer et al. 2005). In Portugal, the longest detected movement was 260 km (Palmeirim & Rodrigues 1992). Reproduction – Both females and males are sexually mature in their second
7 Chapter 1 year. Mating takes place mainly in autumn. Ovulation occurs about the time of mating and fertilization occurs immediately. The fertilized egg undergoes its first few cell divisions but embryonic development is arrested in its early stages and the embryo is not implanted in the uterus (delayed implantation). Embryonic development resumes again in spring (Altringham 1996). In Portugal births occur in beginning of June and one young, exceptionally two, are born (Palmeirim et al. 1999). Hunting and feeding – It emerges from the roosts shortly after sunset. The flight is very fast, 50-70 km/h (Constant & Cannonge 1957). Generally hunts at a long distance from the roost (Rainho 2005), in open areas particularly over freshwaters (Russo & Jones 2003). It preys on moths, gnats and beetles (Whitaker & Black 1976). Maximum age - The maximum age recorded is 19 years and 1 month for a male, and 16 years and 7 months for a female (Avril 1997). Status – It is considered as least concern on a global level (IUCN 2007a), as near threatened on a European level (IUCN 2007b) and as vulnerable in Portugal (Cabral et al. 2005). Although there are still some very large colonies in some regions of the range, the species has declined markedly. This decline is particularly evident in the northern part of the European range, from Romania to France (Rodrigues 1999). In Portugal, it seems to be relatively stable (Rodrigues et al. 2003). Recently, in Portugal, Spain and France there was a mass mortality of this species with unknown cause.
Myotis myotis (Borkhausen, 1797) – Greater mouse-eared bat This species belongs to the family Vespertilionidae. Identification - It is one of the largest European bats and the largest of its genus: head-body 67-79 mm; tail 45-60 mm; forearm 54-68 mm; wingspan 350-450 mm; weight 28-40 g (Schober & Grimmberger 1989). The fur is greyish-brown dorsally, contrasting with whitish-grey underparts that often have a buffy tinge. The hair is clearly bicoloured, the basal half being dark slaty-grey and the terminal half light brown or greyish-brown, becoming darker near the tips on the back. The wings are broad and both the ears and patagium are brown, varying in tone (Palmeirim 1990) (Fig. 1.3). Distribution - It occurs throughout Europe from the Iberian Peninsula to the Ukraine, and into Turkey, Israel, Lebanon and Syria, but excluding Iceland and most Scandinavia (Stutz 1999). Although it was considered to be present in North Africa, Castella et al. (2000) concluded that the populations south of the Mediterranean belong to a separate species. It is a relatively common cave-dwelling species in central and northern Portugal but it is rare in the south; apparently it does not breed in Algarve (Palmeirim et al. 1999). One hibernation shelter (used regularly by more than 100 individuals) and 12 maternity roosts are presently known (Fig. 1.4). Furthermore, there
8 Chapter 1 are two roosts that harbour maternity colonies of either M. myotis or M. blythii, or both (Mogadouro II and Odemira I); it has not been possible to know which of the two species occupies those roosts because their ceilings are very high and these two species are virtually undistinguishable without being captured and measured.
Fig. 1.3 – Myotis myotis (Photo: Francisco Rasteiro).
Fig. 1.4 – Maternity and hibernation roosts (black and white, respectively) of Myotis myotis known in Portugal.
9 Chapter 1
Habitat – In southern Europe generally breeds in caves and mines; during winter scatters through numerous types of roosts, and only isolated individuals or small groups are normally found in underground roosts (Palmeirim & Rodrigues 1992). In Portugal, only one small maternity colony in a non-underground roost is known. This colony uses a stone clock tower, with temperatures during the maternity season fairly similar to those observed in underground roosts. In northern Europe maternity colonies are found in buildings, mostly in attics; hibernates in caves, mines and cellars, rarely in bridges (Stutz 1999). It is a gregarious species, that often forms large colonies, particularly during summer, but it is not uncommon to find isolated individuals, especially males. Sometimes occurs in mixed colonies with M. schreibersii, R. mehelyi and its sibling species M. blythii (Palmeirim & Rodrigues 1992). Annual cycle – Adult females often settle in maternity roosts at the end of March. After the fledging of the young-of-the-year, maternity roosts are abandoned and the animals disperse to mating roosts. During winter bats disperse through many types of roosts, including non-underground sites (Palmeirim & Rodrigues 1992). Migration – It is a regional migrant (Hutterer et al. 2005). The longest movement known in Europe is 436 km (Simon et al. 2004). In Portugal, the longest detected movement is 100 km (Palmeirim & Rodrigues 1992). Reproduction – Normally these bats are sexually mature in their second year although a small percentage of females may reproduce in their first year (Haensel 1980). Mating takes place at the end of summer and autumn. During the mating season males have territories where they are visited by several females (Zahn & Dippel 1997). Sperm is stored and possibly nourished in the oviduct or the uterus right through the winter, and ovulation and fertilization occur in late winter/early spring (delayed fertilization) (Altringham 1996). In Portugal births occur mainly in April and one young, occasionally two, are born (Palmeirim et al. 1999). Hunting and feeding – It emerges only in darkness and flies slowly. It hunts in forest-rich landscapes, both inside forests and on adjoining cultivated but open areas (Stutz 1999). It preys on large insects (mainly beetles and crickets) (Ramos Pereira et al. 2002), which are often gleaned from the ground. It often lands on the ground to forage (Arlettaz 1995). Maximum age - The maximum age recorded is 28 years (Palmeirim et al. 1999). Status – It is considered as lower risk/near threatened on a global level (IUCN 2007a), as least concern on a European level (IUCN 2007c) and as vulnerable in Portugal (Cabral et al. 2005). It is widespread and regionally abundant. In the European Palaearctic the populations seems to have stabilized at relatively lower levels after a drastic decline from the 1950s to the 1970s (Stutz 1999). In Portugal,
10 Chapter 1 data from the last two decades show that the distribution area is stable, but there was a slight decline in the effectives, registered during the maternity season. It is not possible to confirm this tendency during the hibernation season because only one regular major hibernation roost is known (Rodrigues et al. 2003).
In Portugal, major threats to both M. schreibersii and M. myotis are roost destruction and disturbance (particularly during hibernation and maternity seasons), landscape change, and intensive use of pesticides (Cabral et al. 2005). Conservation measures listed in the Portuguese Red Data Book include the preparation of Action Plans, legal protection of the most important roosts, restriction to roost visits during the maternity and hibernation seasons, bat friendly management of the landscape surrounding important roosts, and continuation of the monitoring programme (Cabral et al. 2005). Another important measure is the promotion of public awareness to decrease roost disturbance.
1.3 Studied Topics
Migratory behaviour Migration can be defined as a seasonal, usually two-way, movement from one place or habitat to another to avoid unfavourable climatic conditions and/or to seek more favourable energetic conditions (Fleming & Eby 2003). Although most bats are sedentary, migration plays an important role for many species. Several species of temperate zone bats may undertake a variety of movements ranging from short distances between roosts and foraging areas to long-distance migrations between seasonally occupied regions (Hutson et al. 2001). For migratory behaviour to evolve, its benefits to individuals must exceed its costs. Possible benefits from migration include avoidance of unfavourable climatic conditions and food shortages, reduction of competition and predation, access to limiting nutrients, optimize mate selection, and reduced exposure to parasites or diseases (Richter & Cumming 2006). However, migration can be costly in terms of both time and energy, and can involve added risks of mortality due to predators, food shortage and inclement weather, particularly in the case of continental scale movements (Fleming & Eby 2003). Migration can have consequences at physiological, sociality, population genetic and community levels (Fleming & Eby 2003). Examples of physiological consequences include the increase of fat loads prior to migration and the need of regular dehydration while migrating. Mating systems and social stability are influenced by migratory
11 Chapter 1 behaviour, since it becomes less likely that bats will form year-round stable associations within and between groups of males and females. Migration may also have an important effect on genetic structure of bats populations; specifically, we expect to see lower levels of genetic subdivision in migrant species than in sedentary species. Finally, seasonal movements of large numbers of individuals from one region to another may result in important seasonal changes in rates of resource consumption in different communities, and in changes in the demand for adequate roost sites; if the availability of food or roost sites is limited, then the arrival of migrants could increase levels of competition between resident and migrant species. The study of the migratory behaviour of bats is very important not only because temporal and spatial patterns of migration are important parameters of their biology, but also because of its relevance for conservation. A migratory species may decline even if just one of the several areas that it uses during the yearly cycle is under pressure. Consequently, to preserve a migratory bat species it is usually necessary to protect the complete network of sites that it uses throughout the year, which requires a good knowledge of the migratory movements of the species. Besides the importance of knowing when and where bats migrate, it is also interesting to understand why they do so. In general, climate seasonality explains the long-distance two-way movements that follow a North-South pattern in the temperate zones (Fleming & Eby 2003), but the causes for the shorter regional migrations are less obvious. It is usually assumed that temperate zone bats make regional migrations to reach roosts that have microclimatic characteristics particularly suited for each season (McNab 1982; Baudinette et al. 1994). Some migrations are almost certainly caused by the need to move to roosts with temperatures suitable for hibernation, but the explanation for movements during other seasons is less clear. Roost temperatures may also be the drivers for these migrations, but there are other plausible hypotheses. Since some of the regional movements are long enough to place bats in areas with different climates, these migrations could be driven by the advantages of accessing foraging areas with better ambient temperatures. In general, higher night temperatures are more favourable for foraging insectivorous bats, because insect availability, within the same type of habitat, tends to increase with temperature (Jones et al. 1995). In this thesis three questions were addressed using M. schreibersii in Portugal as a model: (1) when do bats migrate, (2) where bats migrate to, and (3) what are the causes for regional migration.
Spatial behaviour and Gene flow The genetic structure of populations depends on a variety of historical factors
12 Chapter 1
(e.g., colonization processes and isolation in geographical refugia) and on elements of the biology of the species, such as its breeding structure and, most importantly, patterns of gene flow (Castella et al. 2001). It is, therefore, very important to identify the behavioural factors that control gene flow among populations. Several aspects of behaviour, such as migration and philopatry, have the potential to strongly influence patterns of gene flow. Although all bats are very mobile they range from highly migratory to sedentary species, and because migratory behaviour is an important enabler of gene flow, one would expect relatively low levels of genetic subdivision in the most migratory species, as previously referred (Fleming & Eby 2003). However, there are also species which have a strong population structure in spite of migrating extensively (Miller-Butterworth et al. 2003) and, consequently, there must be behavioural factors that are responsible for the preservation of this structure in spite of the massive long distance transportation of genes done by migrating animals. In the case of bats, philopatry seems to play a very important role in the preservation of geographic genetic structure. In fact, both migration and philopatry are likely to play important, but very different, roles in the determination of gene flow and population structuring in many bat species. Another important issue is the knowledge of the organization of maternity colonies in demes, because the planning of management actions should be based in conservation units, either Evolutionary Significant Units (ESUs) or Management Units (MUs). ESUs are geographically discrete groups of populations that evolved separately for a substantial amount of time, representing units reciprocally monophyletic for mitochondrial DNA and possessing significantly divergent allele frequencies at nuclear loci (Moritz 1994). MUs are demographically independent populations that correspond to the ecological components of the ESUs that must be monitored and managed (Moritz 1999). Although the concept of ESUs has been criticized on both semantic and practical grounds (e.g., Cracraft 1997; Crandall et al. 2000), MUs are more appropriate for short-term conservation situations, and have been used with populations of many species (e.g., Michaux et al. 2004; Holycross & Douglas 2007). The definition of these MUs is particularly relevant if re-introductions or translocations are ever needed for conservation or management purposes (e.g., to recover from drastic population crashes), to maintain current levels of genetic diversity (Salgueiro 2007). Using the results of a large scale ringing project of M. schreibersii, three potential sources of gene flow were assessed (the first two related to philopatry, and the third mostly dependent on the patterns of regional migrations during the mating season): (1) dispersal of juveniles to foreign colonies, (2) colony switching by adults, and (3) mating between individuals of different colonies. Additionally, results were
13 Chapter 1 related to the genetic structure of the Portuguese populations of this species, recently studied.
Critical times Most terrestrial species live in environments that are subject to profound rhythmic alterations in elements like light intensity, temperature and humidity, caused by seasonality. Many organisms adapted to these temporal changes in environmental conditions by developing endogenous diurnal rhythms with periods of approximately 24 hr, and in many cases circannual rhythms evolved in addition to daily rhythms. Biotic factors of concern to each individual, such as food supply and predator pressure, also vary on a daily, annual, or even lunar basis. Therefore, successful survival strategies should include a good adjustment of the rhythm of activity of animals to these environmental periodicities (Erkert 1982). Common timing cues used by animals for adjusting to daily and annual rhythms are, respectively, sunrise and sunset, and the length of the daylight period and its continual change over time (Neuweiller 2000). The dynamics of a population may not be just a function of the average environmental conditions, but of those occurring at critical times of the year when, due to specific constraints, the animal cannot fulfil its energy requirements (Racey 1982; Barclay 1991). The identification of such bottlenecks and of their determinants is very important to understand abundance and distribution of species, and also to direct management actions in order to halt and reverse population declines (Payne & Wilson 1999; Primack 2002). Temperate zone bats have a well-defined annual cycle, largely determined by climate, which may influence their energy balance in multiple ways. Body mass of bats shows seasonal fluctuations throughout the year, being explained by endogenous mechanisms (Beasley et al. 1984) and/or by seasonal variations in access to resources. Endogenous mechanisms should program bats to avoid a great accumulation of fat at times when it is not needed, because this may be costly during flight (Ransome 1990). Under optimal environmental conditions one would expect the body mass changes to be fully determined by the endogenous mechanisms. However, if resources are limited, the observed body condition of the bats will be a result of both the endogenous mechanisms and the environmentally-induced energetic constraints. In order to determine if there are seasonal resource bottlenecks that weaken body condition, it is necessary to ascertain if the seasonal body mass variations are not solely explained by endogenous mechanisms. Using M. myotis as a model, it was determined if there are critical times of the
14 Chapter 1 year for temperate zone bats in two climatically different regions (Portugal and Germany) and, additionally, it was studied the roles played by climate and food resources in the generation and timing of these potential bottlenecks.
Roosting behaviour and Phenology Bats spend more than half of their lives under the influence of the conditions in their roosting environment, so roosts necessarily play a key role in their ecology and evolution (Kunz 1982). Bats occupy a great diversity of roosts in both natural and man- made structures: most bat species use roosts exclusively or opportunistically in plants, but many others use shelters in caves, rock crevices, mines, tombs, buildings, bridges and other types of man-made structures (Kunz & Lumsden 2003). Choosing suitable roosts has important benefits such as: protection from the weather and predators, energetic savings, reduced costs to commute to foraging sites, increased mating opportunities, improved maternal care, information transfer between animals (e.g., knowledge of good foraging and roosting sites), and avoidance of competition (Altringham 1996). The roosting habits of bats are usually influenced by the diversity and abundance of available roosts, the distribution and abundance of food, and by an energy economy that is influenced by body size and the physical environment (Kunz & Lumsden 2003). On other hand, the roosting habits of bats influence their regional and global distributions and densities, foraging and mating strategies, social structure and seasonal movements, and in fact even the morphology and physiology of bats (Altringham 1996). Factors that are likely to promote high roost fidelity include large colony size, roost stability, low availability of vacant roosts, widely spaced colonies, intense competition, strong social segregation, high risk of settling in roosts unsuitable for colony, and intense social interdependence (Palmeirim & Rodrigues 1995). Phenology in bats is highly controlled by climate seasonality and by the reproductive rhythm. For example, bats have evolved a number of strategies to optimize the timing of birth in order to maximize the chances of survival to both the female and its young. For bats living at high latitudes, the summer is short and so the young should be born as early in the year as possible in order to maximise the time available for complete development before the start of the winter (Altringham 1996). The natural dependence on a good food supply during lactation makes rainfall a very important climatic factor influencing bat reproductive cycles in tropical regions, because it determines the phenology of insects and plants. In temperate latitudes, where rainfall is usually less seasonal, ambient temperature tend to be more important in determining
15 Chapter 1 the availability of food and reproductive phenology (Racey 1982). In the temperate zones most bats hibernate, presumably to avoid the limitation in the availability of their insect prey during the winter. As a consequence, the processes of fat storage, gestation, lactation, growth of young and, for some species, migration, all have to be accomplished in roughly half of the year (Racey 1982). Humphrey (1975) suggested that bats meet this challenge in part by selecting maternity shelters with a high survival value, by giving birth to few young, and by nurturing them until they reach an advanced state of development. The knowledge of roosting behaviour and phenology is very important to understand potential changes in roost occupancy and to plan when management measures should be taken. M. myotis faced a recent northward expansion, presumably caused by the availability of man-made roosts that can be used as maternity shelters, since underground roosts are too cold (Horáček 1985; Güttinger 1994). Environmental conditions encountered in Central Europe are quite different from those of its south European range, and M. myotis had to adjust to these conditions by altering various aspects of its biology (e.g., timing of birth and hibernation (Paz 1986; Pandurska 1993, 1998; Ibáñez 1997; Zahn 1999), diet (Arlettaz 1995; Ramos Pereira et al. 2002) and social structure (Zahn & Dippel 1997)). However, published information was still insufficient to understand important divergences in the responses of M. myotis to the different environmental conditions existing in the northern and southern parts of the range. Roosting behaviour and phenology were studied comparing various aspects of the biology of M. myotis in Mediterranean and Central Europe, specifically in Portugal and in Germany. Namely, it was studied: (1) roosting and clustering behaviour, (2) maternity and hibernation periods, (3) mating activity, and (4) sexual maturation.
1.4 Thesis Structure The thesis is organized in six chapters; chapters 2 to 5 are composed by four papers. Three of them are already published in international scientific journals, and one (chapter 3) has been submitted and is in the process of evaluation. Chapter 1 corresponds to the general introduction of this thesis. Chapter 2 describes the migration patterns of M. schreibersii, discussing when, where and why cave-dwelling bats migrate. Chapter 3 analyses the gene flow routes of M. schreibersii. Chapter 4 discusses the existence of critical times for M. myotis during the yearly cycle, analysing the potential role of climate and food resources. Chapter 5 describes the
16 Chapter 1 roosting behaviour and phenology of M. myotis, comparing the situation in its southern and northern distribution ranges. The results of this thesis give scientific support to some conservation measures that are already being taken and will hopefully serve as background for the implementation of additional management measures to protect cave-dwelling bats in Mediterranean areas. Chapter 6 comprises a discussion of the results in the context of these management measures, mostly focusing on the conservation of Portuguese bats, and the future work.
1.5 References Altringham J.D. (1996) Bats, Biology and Behaviour. Oxford University Press, New York .
Arlettaz R. (1995) Ecology of the sibling mouse-eared bats (Myotis myotis and Myotis blythii): zoogeography, niche, competition, and foraging. Horus Publ., Martigny.
Avril B.W.P. (1997) Le minioptère de Schreibers : analyse des résultats de baguages de 1936 à 1970. Thèse pour de Doctorat Vétérinaire. Ecole Nationale Vétérinaire de Toulouse, France.
Barclay R.M.R. (1991) Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. Journal of Animal Ecology 60: 165-178.
Baudinette R.V., Wells R.T., Sanderson K.J. & Clark B. (1994) Microclimatic conditions in maternity caves of the bent-wing bat, Miniopterus schreibersii: an attempted restoration of a former maternity site. Wildlife Research 21: 607-619.
Beasley L.J., Pelz K.M. & Zucker I. (1984) Circannual rhythms of body weight in pallid bats. American Physiological Society 246: 955-958.
Cabral M.J. (coord.), Almeida J., Almeida P.R., Dellinger T., Ferrand de Almeida N., Oliveira E., Palmeirim J.M., Queiroz A.I., Rogado L. & Santos-Reis M. (Eds.) (2005) Livro Vermelho dos Vertebrados de Portugal. Instituto da Conservação da Natureza, Lisboa.
Castella V., Ruedi M., Excoffier L., Ibanez C., Arlettaz R. & Hausser J. (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Molecular Ecology 9:1761-1772.
Castella V., Ruedi M., Excoffier L. (2001) Contrasted pattern of nuclear and mitochondrial genetic structure among nursery colonies of the bat Myotis myotis. Journal of Evolutionary Biology 14:708-720
Constant P. & Cannonge B. (1957) Evaluation de la vitesse de vol des Miniopteres. Mammalia 21: 301-302.
Cracraft J. (1997) Species concepts in systematics and conservation biology: an ornithological viewpoint. Pp. 325-339. In: Species: the units of biodiversity. Claridge M.F., Dawah A.H. & Wilson M.R. (Eds.) Chapman and Hall, London.
17 Chapter 1
Crandall K.A., Bininda-Emonds O.R.P., Mace G.M. & Wayne R.K. (2000) Considering evolutionary processes in conservation biology. Trends in Ecology & Evolution 15: 290-295.
Erkert H.G. (1982) Ecological aspects of bat activity. Pp. 201-242. In: Ecology of Bats. Kunz T.H. (Ed.). Plenum Press, New York.
Fleming T.H. & Eby P. (2003) Ecology of Bat Migration. Pp. 156-208. In: Bat ecology. Kunz T.H. & Fenton M.B. (Eds.) University of Chicago Press, Chicago.
Güttinger R. (1994) 1st in Mitteleuropa das Klima der primär begrenzende Faktor für das Vorkommen von Fortpflanzungskolonien des Grossen Mausohrs (Myotis myotis)? Berichte der St. Gallischen Naturwissenschaftlichen Gesellschaft 87: 87–92.
Haensel J. (1980) Wann werden Mausohren, Myotis myotis (Borkhausen, 1797), geschlechtsreif? Nyctalus 1: 235-245.
Hill J.E. & Smith J.D. (1986) Bats: a natural history. University of Texas Press, Austin.
Holycross A.T. & Douglas M.E. (2007) Geographic isolation, genetic divergence, and ecological nonexchangeability define ESUs in a threatened sky-island rattlesnake. Biological Conservation 134: 142-154.
Horáček I. (1985) Population ecology of Myotis myotis in Central Bohemia. Acta Universitatis Carolinae - Biologica 1981: 161-267.
Humphrey S.R. (1975) Nursery roosts and community diversity of Nearctic bats. Journal of Mammalogy 56: 321-346.
Hutson, A.M., Mickleburgh, S.P. & Racey, P.A. (compilers) (2001) Microchiropteran Bats: Global Status Survey and Action Plan.. IUCN/SSC Chiroptera Specialist Group, IUCN, Gland, Switzerland and Cambridge, UK.
Hutterer R., Ivanova T., Meyer-Cords C. & Rodrigues L. (2005) Bat Migrations in Europe: A Review of Banding Data and Literature. German Agency for Nature Conservation, Bonn.
Ibáñez C. (1997) Winter reproduction in the greater mouse-eared bat (Myotis myotis) in South Iberia. Journal of Zoology 243: 836-840.
IUCN (2007a) 2007 IUCN Red List of Threatened Species. Downloaded / Consulted on 20 December 2007 at http://www.iucnredlist.org
IUCN (2007b) Miniopterus schreibersii. In: IUCN 2007. European Mammal Assessment. Downloaded / Consulted on 20 December 2007 at http://ec.europa.eu/environment/nature/conservation/species/ema
IUCN (2007c) Myotis myotis. In: IUCN 2007. European Mammal Assessment. Downloaded / Consulted on 20 December 2007 at http://ec.europa.eu/environment/nature/conservation/species/ema
Jones G., Duvergé P.L. & Ransome R.D. (1995) Conservation biology of an endangered species: Field studies of greater horseshoe bats. Symposium of Zooogical Society of London 67: 309-324.
18 Chapter 1
Jones G. & Teeling E.C. (2006) The evolution of echolocation in bats. Trends in Ecology and Evolution 21: 149 - 156.
Kunz T.H. (1982) Roosting ecology of bats. Pp. 1-55. In: Ecology of Bats. Kunz T.H. (Ed.). Plenum Press, New York.
Kunz T.H. & Lumsden L.F. (2003) Ecology of cavity and foliage roosting bats. Pp. 3-89. In: Bat ecology. Kunz T.H. & Fenton M.B. (Eds.) University of Chicago Press, Chicago.
Liberatore G.T., Samson A., Bladin C., Schleuning W.-D. & Medcalf R.L. (2003) Vampire bat salivary plasminogen activator (Desmoteplase) - a unique fibrinolytic enzyme that does not promote neurodegeneration. Stroke 34: 537-543.
MacNab B.K. (1982) Evolutionary alternatives in the physiological ecology of bats. Pp. 151-200. In: Ecology of bats. Kunz T.H. (Ed.). Plenum Press, New York.
Michaux J.R., Libois R., Davison A., Chevret P. & Rosoux R. (2004) Is the western population of the European mink, (Mustela lutreola), a distinct Management Unit for conservation? Biological Conservation 115: 357-367.
Mickleburgh S.P., Hutson A.M. & Racey P.A. (2002) A review of the global conservation status of bats. Oryx 36: 18-34.
Miller-Butterworth C.M., Jacobs D.S., Harley E.H. (2003) Strong population structure is correlated with morphology and ecology in a migratory bat. Nature 424: 187-191.
Miller-Butterworth C.M., Eick G., Jacobs D.S., Schoeman M.C. & Harley E.H. (2005) Genetic and phenotypic differences between South African long-fingered bats, with a global miniopterine phylogeny. Journal of Mammalogy 86: 1121-1135.
Moritz, C. (1994) Defining "Evolutionary Significant Units" for conservation. Trends in Ecology and Evolution 9: 373-375.
Moritz C. (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130: 217-228.
Neuweiler G. (2000) The biology of bats. Oxford University, Oxford.
Palmeirim J.M. (1990) Bats from Portugal: zoogeography and systematics. Miscellaneous Publications of the Kansas University Museum of Natural History 82.
Palmeirim J.M. & Rodrigues L. (1992) Plano Nacional de Conservação dos Morcegos Cavernícolas. Estudos de Biologia e Conservação da Natureza 8. SNPRCN, Lisboa.
Palmeirim J.M. & Rodrigues L. (1995) Dispersal and philopatry in colonial animals: the case of Miniopterus schreibersii. Pp. 219-231. In: Ecology, Evolution and Behaviour of Bats. Racey P.A. & Swift S.M. (Eds.). Oxford University Press, Oxford.
Palmeirim J.M., Rodrigues L., Rainho A. & Ramos M.J. (1999) Chiroptera. Pp 41-95. In: Mamíferos terrestres de Portugal Continental, Açores e Madeira. Instituto da
19 Chapter 1
Conservação da Natureza & Centro de Biologia Ambiental (Eds.). Lisboa.
Pandurska R.S. (1993) Distribution and species diversity of cave-dwelling bats in Bulgaria and some remarks on the microclimatic conditions of the hibernation. Trav. Inst. Spéol. Emile Racovitza 32: 155-163.
Pandurska R.S. (1998) Reproductive behaviour of nursery colonies of Myotis myotis in Bulgaria. Myotis 36: 143-150.
Paz O. de (1986) Age estimation and postnatal growth in the greater mouse bat Myotis myotis (Borkhausen, 1797) in Guadalajara, Spain. Mammalia 50: 243–251.
Payne R.J.H. & Wilson J.D. (1999) Resource limitation in seasonal environments. Oikos 87: 303-314.
Primack R. (2002) Essentials of Conservation Biology. Sinauer Associates, Sunderland.
Racey P.A. (1982) Ecology of bat reproduction. Pp. 57-68. In: Ecology of Bats. Kunz T.H. (Ed.). Plenum Press, New York.
Racey P.A. & Entwistle A.C. (2003) Conservation ecology of bats. Pp. 680-743. In: Bat ecology. Kunz T.H. & Fenton M.B. (Eds.). University of Chicago Press, Chicago.
Rainho A. (2005) How does land use change affect colonial bats? A methodology to compare alternative land use scenarios. MSc Thesis on Geographical Information Science. School of GeoSciences, Edinburgh, U.K.
Ramos Pereira M.J., Rebelo H., Rainho A. & Palmeirim J.M. (2002) Prey selection by Myotis myotis (Vespertilionidae) in a Meditterranean region. Acta Chiropterologica 4: 183-193.
Ransome R.D. (1990) The natural history of hibernating bats. Christopher Helm, London.
Richter H.V. & Cumming G.S. (2006) Food availability and annual migration of the straw-colored fruit bat (Eidolon helvum). Journal of Zoology 268: 35-44.
Rodrigues L. (1999) Miniopterus schreibersii (Kuhl, 1817). Pp. 154-155. In: The Atlas of European Mammals. Mitchell-Jones A.J., Amori G., Bogdanowicz W., Kryštufek B., Reijnders P.J.H., Spitzenberger F., Stubbe M., Thissen J.B.M., Vohralík V. & Zima J. (Eds.). Academic Press, London.
Rodrigues L., Rebelo H. & Palmeirim J.M. (2003) Avaliação da tendência populacional de algumas espécies de morcegos cavernícolas. Relatório técnico final. Centro de Biologia Ambiental / Instituto da Conservação da Natureza, Lisboa.
Russo D. & Jones G. (2003) Use of foraging habitat by bats in a Mediterranean area determined by acoustic surveys: conservation implications. Ecography 26: 197- 209.
Salgueiro P. (2007) Genetic structure and gene flow of fragmented bat populations: consequences for conservation. PhD Thesis. University of Lisbon, Portugal.
Schober W. & Grimmberger E. (1989) A guide of bats of Britain and Europe. Hamlyn,
20 Chapter 1
London.
Simon M., Huttenbugel S. & Smit-Viergutz J. (2004) Ecology and conservation of bats in villages and towns. Bundesamt fur Naturschutz, Bonn.
Stutz H-P.B. (1999) Myotis myotis (Kuhl, 1817). Pp. 114-115. In: The Atlas of European Mammals. Mitchell-Jones A.J., Amori G., Bogdanowicz W., Kryštufek B., Reijnders P.J.H., Spitzenberger F., Stubbe M., Thissen J.B.M., Vohralík V. & Zima J. (Eds.). Academic Press, London.
Tian L., Liang B., Maeda K., Metzner W. & Zhang S. (2004) Molecular studies on the classification of Miniopterus schreibersii (Chiroptera: Vespertilionidae) inferred from mitochondrial cytochrome b sequences. Folia Zoologica 53: 303-311.
Van den Bussche R.A. & Hoofer S.R. (2004) Phylogenetic relationships among recent chiropteran families and the importance of choosing appropriate out-group taxa. Journal of Mammalogy 85: 321-330.
Whitaker J.O. & Black H. (1976) Food habits of cave bats from Zambia, Africa. Journal of Mammalogy 57: 199-204.
Yalden D.W & Morris P.A. (1975) The lives of bats. David & Charles, West Vancouver.
Zahn A. (1999) Reproductive success, colony size and roost temperature in attic- dwelling bat Myotis myotis. Journal of Zoology 247: 275-280.
Zahn A. & Dippel B. (1997) Male roosting habits and mating behaviour of Myotis myotis. Journal of Zoology 243: 659-674.
21
2
Migratory behaviour
Paper I Rodrigues L. & Palmeirim J.M. (in press) Migratory behaviour of the Schreiber’s bat: when, where, and why do cave bats migrate in a Mediterranean region? Journal of Zoology doi:10.1111/j.1469-7998.2007.00361.x
23
Chapter 2
25 Chapter 2
26 Chapter 2
27 Chapter 2
28 Chapter 2
29 Chapter 2
30 Chapter 2
31 Chapter 2
32 Chapter 2
33 Chapter 2
34
3
Spatial behaviour and Gene flow
Paper II Rodrigues L., Ramos Pereira M.J., Rainho A. & Palmeirim J.M. (submitted) Behavioural factors determining potential gene flow among colonies of the Schreiber’s bat Miniopterus schreibersii. Behavioral Ecology and Sociobiology.
35
Chapter 3
Behavioural factors determining potential gene flow among colonies of the Schreiber’s bat Miniopterus schreibersii
Luísa Rodrigues1, Maria João Ramos Pereira2, Ana Rainho1 and Jorge M. Palmeirim2
1Instituto da Conservação da Natureza e da Biodiversidade, Rua de Santa Marta 55, 1150-294 Lisboa, Portugal; 2Departamento de Biologia Animal and Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, 1749-016 Lisboa, Portugal.
Key words Miniopterus schreibersii, dispersal, philopatry, gene flow, migrations
Abstract Dispersal and migratory behaviours are often important determinants of gene flow in wild species, and we have studied their role using mark-recapture data in the Portuguese population of Miniopterus schreibersii, a cave dwelling bat that forms large maternity colonies. Juvenile dispersal, usually a major agent of gene flow, was found to be negligible, as young females never settled to give birth in foreign colonies. Likewise, there was virtually no dispersal of adult females to foreign maternity colonies. This strong philopatry virtually eliminated female mediated gene flow, but we found a great potential for male mediated gene flow among colonies, as regional migrations temporarily joined both sexes from different colonies in the same roosts, during the mating season. In fact, females from some colonies were more likely to mate with males from foreign colonies than from their own, thus bringing home genes of foreign males. In spite of this abundant gene flow, we found a pattern of isolation by distance and even separate demes, which is explained by the fact that migrations were usually too short to allow direct flow among distant colonies. We concluded that potential gene flow is influenced by the distance between colonies and the availability of mating roosts between them. In addition, we found this flow to be asymmetrical, with a dominant direction from the largest to the smallest colonies. Our mark-recapture estimates of potential gene flow based on dispersal and migratory behaviour are compatible with the genetic structure of the population for both nuclear and mitochondrial DNA.
Introduction Gene flow, the transfer of alleles between populations, is a key factor in the
37 Chapter 3 structuring of the populations of a species (McCracken 1987). High rates of gene flow among populations tend to combine their gene pools, resulting in geographically homogeneous species (Frankham et al. 2002). In contrast, low rates allow populations to differentiate as a consequence of drift and local adaptations, resulting in geographically structured species. Genetic analyses have demonstrated that even species that are phenotypically homogeneous can have genetically structured populations. To understand how this structuring arises and is maintained it is important to know the behavioural factors that control gene flow among populations. Several aspects of behaviour, such as migration and philopatry, have the potential to strongly influence patterns of gene flow. Although all bats are very mobile they range from highly migratory to sedentary species, and because migratory behaviour is an important enabler of gene flow, one would expect relatively low levels of genetic subdivision in the most migratory species (Fleming and Eby 2003). Supporting this prediction, genetic studies have found little geographic differentiation in long distance migrants like Leptonycteris curasoae (Wilkinson and Fleming 1996), Nyctalus noctula (Petit and Mayer 1999) and Pteropus scapulatus (Sinclair et al. 1996), and in regional migrants like Myotis lucifugus (Fenton and Thomas 1985), Myotis myotis (Castella et al. 2000) and Carollia perspicillata (Fleming 1988). In contrast, high levels of genetic subdivision have been reported in sedentary species, such as Macroderma gigas (Worthington Wilmer et al. 1994), Myotis bechsteinii (Kerth et al. 2000) and Plecotus auritus (Burland et al. 1999). However, there are also bats, such as Miniopterus natalensis, which have a strong population structure (Miller-Butterworth et al. 2003) in spite of migrating extensively. Consequently, there must be behavioural factors that are responsible for the preservation of this structure in spite of the massive long distance transportation of genes done by migrating animals. In the case of bats, philopatry seems to play a very important role in the preservation of geographic genetic structure. If bats return to their birth colonies, rather then disperse to new or foreign colonies, then this reduces gene flow and favours the maintenance of structure. A number of migratory bat species have been found to have a highly philopatric behaviour, i.e. low levels of dispersal (e.g. Myotis grisescens (Tuttle 1976) and M. natalensis (Miller-Butterworth et al. 2003)). Consequently, both migration and philopatry are likely to play important, but very different, roles in the determination of gene flow and population structuring in many bat species. Intensive ringing-recapture studies are the best way to learn about the dispersal and migratory behaviours of bats, but to our knowledge none has objectively included a quantitative assessment of the potential role of each of these behaviours on gene flow. In this paper we use the results of a large scale ringing project of a colonial bat
38 Chapter 3
Miniopterus schreibersii in Portugal to assess three potential sources of gene flow. Two of them are related to philopatry: dispersal of juveniles to foreign colonies, and colony switching by adults. The third, mating between individuals of different colonies, is mostly dependent on the patterns of regional migrations during the mating season. Finally, we relate our results to the genetic structure of the Portuguese populations of this species, which has recently been studied (Ramos Pereira et al. submitted).
Methods Following the latest taxonomic revisions (Tian et al. 2004; Miller-Butterworth et al. 2005), we consider that the range of M. schreibersii is restricted to the Mediterranean region, and we refer to the southern African form as M. natalensis. M. schreibersii occurs throughout the Portuguese mainland and roosts almost exclusively underground, especially in caves and abandoned mine galleries. It is a gregarious species, forming large colonies throughout most of the year (Rodrigues 1999). Twelve maternity colonies and 15 important hibernation roosts (i.e. used regularly by more than 100 individuals) are known in Portugal. Since the country has been thoroughly surveyed since 1987 it is unlikely that large colonies, particularly nurseries, remain unknown. Over 36000 bats were marked with 4.2 mm smoothed metal lipped rings (made initially by Lambournes and later by Porzana (U.K.)), designed to minimise the risk of damage to the wing. This is the ring size recommended by Resolutions 4.6 and 5.5 of EUROBATS. The impact of ringing on bats in this study was monitored and was apparently minor (Rodrigues and Palmeirim in press), but the same low incidence of problems can not be assumed for other bat species or ring types. The ringing programme had two phases: from 1987 to 1992 about 27000 bats were ringed throughout the whole country, mainly to map migration routes and obtain information to establish a network of protected sites. From 1993 to 2005 ringing was limited to a few roosts, to obtain long-term data on the population dynamics of their colonies. We obtained a total of over 8000 recaptures of ringed bats. We required a minimum of two recaptures to validate a connection between two roosts, thus minimizing the effects of unusual behaviour and of possible errors reading the rings. Bats were normally captured while emerging from roosts, using harp-traps (Palmeirim and Rodrigues 1993). When that was not possible, they were captured inside the roosts by hand or hand-net. To minimise disturbance, bats were not trapped in maternity roosts until after all the young-of-the-year were already flying. The numbers of bats assigned to each roost are the result of direct daytime counts or visual estimates. When the animals formed compact clusters their number was estimated
39 Chapter 3 using the approximate surface area covered by the clusters and a reference density of 2000 individuals/m2 (Rodrigues and Palmeirim in press). Any maternity colony other than the one where a bat was born is referred to as a “foreign colony”. We assumed that the females found in a maternity colony during the maternity season had given birth there, because we have previously determined that they very seldom change roost during this period (Rodrigues and Palmeirim in press). We considered two age classes for both females and males: adults (at least one year old) and young-of-the-year (henceforth referred to as “juveniles”). Age was determined by the ossification of the carpal joints, development of nipples and testis (e.g., Dwyer 1963a; Baagøe 1977), and the patterns of moult (Dwyer 1963b). The annual cycle was divided in four periods: hibernation (mid December to end of February), spring (beginning of March to end of May), maternity (beginning of June to end of July) and autumn (end of July to mid December). M. schreibersii is known to make seasonal migratory movements of usually a few dozen kilometres, but up to several hundred kilometres (Rodrigues 1999). These movements bring together, during the mating season, males and females from different maternity colonies. Using the recaptures of ringed bats we determined which mating roosts were used by the animals from each colony, and quantified their relative importance for each colony. In each of those mating roosts we then estimated the probability of a bat from a particular colony mating with animals from each of the colonies represented in the roost. For example, if 70% of the bats in a mating roost were from colony A, 20% from B, and 10% from C, the probability of a bat from colony A mating with an animal from colonies A, B, and C was 70%, 20%, and 10% respectively. Pooling this information for all the mating roosts used by animals from colony A, we estimated their mating potential with animals from each of the studied colonies. We also assumed that in mating roosts harbouring bats from different maternity colonies, the probability that two bats mate is independent of their origin. While there are no behavioural observations confirming this assumption, there are several genetic studies demonstrating that bats often mate with foreign animals (e.g. M. bechsteinii (Kerth et al. 2003), P. auritus (Veith et al. 2004), and N. noctula (Petit and Mayer 2000)). Mating in M. schreibersii occurs mainly in autumn (Serra-Cobo 1989), but since normally these bats remain in the mating roost through the winter (Rodrigues and Palmeirim in press), we pooled the recaptures from both seasons to make more robust estimates the usage of each mating roost by bats from different colonies. We analysed mating potential using only data from the first phase of the ringing programme, to avoid biases resulting from the very uneven sampling during the second
40 Chapter 3 phase. We only analysed seven maternity colonies (Miranda do Douro, Tomar, Alcanena, Marvão, Sesimbra I, Moura I and Loulé I; Figure 1) because data for the remaining five Portuguese colonies were considered insufficient.
Fig. 1 - Map of potential mating opportunities between individuals of the maternity colonies. Connections between roosts are proportional to the mating potential between them, estimated using the recovery in the mating roosts of ringed animals (lines correspond to values multiples of 10%).
Ramos Pereira et al. (submitted) amplified five microsatellite loci (Miller- Butterworth et al. 2002) from tissues obtained from 407 bats of 11 Portuguese maternity colonies of M. schreibersii (including the seven colonies analysed in this study). We used the data in that paper to calculate genetic relationships between pairs of colonies with F-statistics (Weir and Cockerham 1984) using SPAGeDi 1.2 (Hardy and Vekemans 2002). These relationships were then compared with the mating potential between colonies calculated using the results of the ringing study. The use of nuclear markers is ideal for comparing with mark-recapture data because, unlike mitochondrial markers, they reflect the contribution of both males and females to the genetic structuring of populations.
41 Chapter 3
Results Juvenile dispersal No cases of juvenile dispersal were registered. In fact, during the maternity season, all the recaptures of bats that had been marked in the roost where they were born (n=283), took place in that same roost: 51 bats (31 females, 20 males) were recaptured there in their second year and 232 bats (136 females, 96 males) in later years. So all the females returned to give birth in the colony where they were born, demonstrating strict natal philopatry. The fact that these young bats do not move to other maternity roosts is not a consequence of not knowing their location. In fact, juvenile M. schreibersii often made temporary visits to roosts of foreign nurseries. Of the 75 juveniles (females and males) recaptured in roosts of maternity colonies outside the maternity season, 23% were in the roosts of foreign colonies. However, these are just temporary users, as only bats found with foreign colonies during the maternity season can be considered true dispersers.
Adult dispersal We observed very few cases of adult female dispersal, i.e. females that switched colonies during the course of their reproductive life. During the maternity season 99.5% of recaptured adult females (n=1120) were in the same maternity roost where they had given birth before. Most males do not spend the maternity season in the nurseries, and they do not have any known role in them. However, the males that are with the maternity colonies also show a high degree of attachment to them. The great majority (93.7%; n=327) of the recaptures in such colonies were of males that had been ringed in them. In spite of this attachment to their colonies during the maternity season, adult bats of both sexes know the location of foreign maternity roosts and regularly visit them. In fact, 28% of the females and males recaptured outside the maternity season (n=629), were visiting roosts that harbour foreign maternity colonies.
Mating with individuals of foreign colonies Table 1 shows the mating potential between the maternity roosts, estimated using the mark-recapture data. It is interesting to note that while some colonies show maximum mating potential with themselves (e.g., Loulé I), in other colonies bats seem to have more opportunities to mate with animals from foreign colonies (e.g., bats from Tomar seem to have twice the opportunities to mate with bats from Alcanena than with bats from their own colony).
42 Chapter 3
Table 1 – Potential mating opportunities (in percentage) between individuals of the seven analysed maternity colonies, estimated using the recovery in the mating roosts of ringed animals. Each line represents one maternity colony. The values are the proportion of females from that colony that are likely to mate with males from the colonies indicated in the columns. Alcanena Tomar Sesimbra I Marvão Moura I Loulé I M. Douro Alcanena 52,3 16,4 29,5 1,3 0,4 0,0 0,0 Tomar 44,9 21,1 24,1 6,7 3,1 0,0 0,0 Sesimbra I 38,0 11,4 50,6 0,0 0,0 0,0 0,0 Marvão 9,2 17,1 0,0 61,4 12,3 0,0 0,0 Moura I 1,0 2,7 0,0 4,2 91,9 0,1 0,0 Loulé I 0,0 0,0 0,0 0,0 1,0 99,0 0,0 M. Douro 0,0 0,0 0,0 0,0 0,0 0,0 100,0
The representation of potential mating opportunities between maternity colonies on a map (Fig. 1) shows that, in general, there should be greater genetic interchange between the closest colonies. Mating opportunities between colonies are indeed negatively correlated with the distance between them (Fig. 2, R=-0.65, df=47, p < 0.0001).
Fig. 2 – Potential mating opportunities between maternity roosts vs distance between them.
The data shows that, in spite of the potential of gene flow through mating with individuals from different colonies, the population is divided into demes, although the level of isolation among them is variable (Table 1 and Fig. 1). The northern deme seems to be very isolated from the rest, and the colonies in the west-centre and in the south of the country are also very isolated from each other. The situation of the colonies of Marvão and Moura I is less clear. Marvão has relatively few links to the west-centre deme, and Moura I seems to be even more isolated.
43 Chapter 3
Plotting the genetic distance between maternity colonies against the potential mating opportunities between them (Fig. 3), shows that the colonies with a greater mating potential are genetically more similar (Rs=-0.78, df=26, p < 0.0001).
Fig. 3 – Potential mating opportunities between maternity roosts vs genetic distances between them.
Discussion Juvenile dispersal makes virtually no contribution to gene flow Juvenile dispersal is usually the single largest (and often only) long-distance movement made by individual animals of many species (Dice and Howard 1951), and is generally accepted as the major agent of gene flow among populations (Wiklund 1996). It has been observed in several bat species: juveniles of both sexes of Lophostoma silvicolum (Dechmann et al. 2007) and Phylostomus hastatus (McCracken 1987) dispersed before their first birthdays, and juvenile males of Desmodus rotundus dispersed before reaching sexual maturity (McCracken 1987). However, we did not observe any case of juvenile dispersal to foreign nurseries in this study, and since our sample was quite large we can establish that such events, if they occur, are very rare. Low rates of juvenile dispersal have also been reported for some bat species, such as P. auritus (Burland et al. 2006) and M. lucifugus (Humphrey and Cope 1976), and for females of D. rotundus (McCracken 1987) and M. grisescens (Tuttle 1976). Consequently, we can conclude that, in spite of the long distance movements that juveniles of M. schreibersii make in their first year of life, juvenile dispersal is a very minor agent of gene flow among populations.
Adult dispersal contribution to gene flow also minor Bats can live for many years and reproduce throughout most of their lives. Consequently, during the reproductive life of a female bat there are plenty of
44 Chapter 3 opportunities for it to switch the maternity colony where it gives birth, and this switch would result in a female mediated transfer of genes between colonies, with the addition of a new matriline to the receiving colony. However, in the case of M. schreibersii we found that such events are extremely rare. Even the observed 0.5% of recaptures of females in foreign colonies during the maternity season may not correspond to real switches between colonies, as some of these females could be in the wrong colony because of unusual circumstances. In one instance we found several adult females in a foreign maternity during the nursing season, but immediately after that we checked their original colony and discovered that its animals had dispersed prematurely because almost all the juveniles had died, for some unknown reason. Presumably, as their young died they no longer had any reason to remain in the roost and so dispersed. These females were not quantified as dispersers in our study, but there may have been other similar events that we did not detect and that may explain the presence of a few recaptures in foreign maternity colonies. Males also showed a high level of philopatry, but they were somewhat more likely to disperse to roosts harbouring foreign nurseries than females. Presumably, such male dispersal events are of little consequence for gene flow because females do not mate with the males in the maternity roosts. Our findings confirmed the strictly philopatric behaviour of M. schreibersii during the maternity season, already described by Palmeirim and Rodrigues (1995) using a smaller dataset. Female philopatry to maternity roosts is common in temperate bats, but its strength varies among species; colony switching was not observed in an intensive mark-recapture study of M. bechsteini (Kerth et al. 2002), but was not rare in M. myotis (Zahn 1998). The combination of natal philopatry in juvenile females, and reproductive philopatry in adult females, makes female mediated gene transfer virtually non-existent, and this has an impact on the genetic structure of population at the mtDNA level, as discussed below. In this study we only measured the potential dispersal to sites already harbouring maternity colonies. However, some artificial roosts (e.g. mine galleries), have been colonised by M. schreibersii, so some amount of dispersal to new sites must occur. But because new colonies are very seldom formed, we assume that either the number of animals dispersing in this way is very small or their success getting established is extremely low.
45 Chapter 3
Male mediated gene flow is strong, thanks to seasonal migrations that allow them to mate with females of foreign colonies Regional migrations thoroughly mix males and females from different maternity colonies during the mating season and this creates conditions for abundant gene flow. In fact, our mark-recapture data suggests that the impact of this mixture on the mating opportunities is such that females from some colonies were far more likely to mate with males from foreign colonies than with males from their own colony. Genetic paternity studies done in other temperate bats found low numbers of juveniles fathered by within-colony males ((e.g. in M. myotis (Petri et al. 1997), P. auritus (Burland et al. 2001) and M. bechsteinii (Kerth and Morf 2004)). Consequently, we can conclude that regional migrations, rather than dispersal, are the main agent of gene flow between colonies of M. schreibersii. Despite this facilitation of inter-colony mating by regional migrations, it is clear from the values in Table 1 that the frequency of inter-changes varies substantially among the studied colonies; 79% of the females from Tomar presumably mate with foreign males, but the connections between some other pairs of colonies is nil (which does not mean that they are completely isolated, as they may mate with colonies in Spain, which we did not study). So what are the factors that are behind these major variations in potential gene flow? It is clear that distance between maternity colonies plays an important role in the determination of the amount of potential gene flow among them (Fig. 2). This influence of distance occurs because most regional migrations tend to be just a few dozen kilometres long, and in the study area many colonies are separated by greater distances (Rodrigues and Palmeirim in press). Consequently, most migrations are only likely to bring together animals from the closest maternity colonies (such as the various colonies of central Portugal). But distance alone does not fully explain the observed variations in mating potential. For example, the Tomar colony is closer to Marvão than to Sesimbra I, but its females are four times as likely to mate with males from the latter colony. Regional differences in the availability of potential mating roosts explain this discrepancy; the region between Tomar and Sesimbra I includes limestone areas with caves, whereas there are none between Tomar and Marvão. Rossiter et al. (2000) also suggested that inter-colony gene flow in Rhinolophus ferrumequinum is probably limited by both the distances travelled by bats during the mating period and the availability of suitable mating sites. Another fact that stands out from Table 1 is that potential gene flow is not symmetrical. For example, a female from Tomar has a 45% chance of mating with a
46 Chapter 3 male from Alcanena, but the probability of the reverse is only 16%. This is due to the fact that Alcanena is a larger colony, so it has more males in the mating sites used by both colonies. As virtually all gene flow is female mediated, this asymmetry in mating should result in an asymmetry in gene flow. It seems clear that in general the dominant direction of gene flow is from the largest to the smallest colonies. In summary, regional migrations created opportunities for intensive gene flow, but this was limited by the distance between nurseries, and by the availability of mating roosts between them. In addition, this potential flow was asymmetrical, with greater flow from the larger to the smaller colonies. This scenario probably applies to many other temperate zone cave-dwelling species, as they often make regional migrations that mix animals from different maternity colonies in mating roosts (e.g. Myotis myotis (Zahn and Dippel 1997) and M. nattereri (Rivers et al. 2006)). However, as these migrations become longer, relative to the distance between roosts, isolation by distance should become less relevant and there should be an increasing tendency for unstructured populations, as those observed in some bat species (e.g. Leptonycteris curasoae (Wilkinson and Fleming 1996) and Nyctalus noctula (Petit and Mayer 1999)).
Patterns of spatial behaviour explain genetic structure of population Our observations on philopatry and seasonal migrations of M. schreibersii and the resulting table of potential gene flow are congruent with the genetic information recently made available for the same population (Ramos Pereira et al. submitted). In the remaining of this paper we discuss how the behavioural patterns here described may have shaped the genetic structure of this population. Ramos Pereira et al. (submitted) found clear inter-colony differences at the mtDNA level in our study region. As mtDNA can only be transferred by females these differences are easily explained by the observed lack of dispersal by both juvenile and adult females, which eliminated the opportunities for female mediated gene flow. Similar explanations have been used to justify marked mtDNA structuring in other bats (Kerth et al. 2000). Ramos Pereira et al. (submitted) also reported that the structure in nuclear DNA, which is dispersed by both males and females, is much less marked than that of the mtDNA. This relative homogeneity can be explained by the regional migratory patterns here described, which resulted in a high mating potential between males and females of different colonies. As a consequence, females often bring home the genes of foreign males, thus weakening inter-colony differences at the nuclear DNA level. In spite of this abundant male mediated gene flow, Ramos Pereira et al. (submitted) found nuclear DNA evidence of some isolation by distance. The clear
47 Chapter 3 correlation between our mark-recapture based estimates of mating potential among colonies (Fig. 2) and the nuclear DNA distances (Fig. 3) suggests that spatial behaviour is responsible for those distances. This isolation by distance apparently developed because, as the mark-recapture results demonstrated, the regional migrations that make inter-colony gene flow possible were usually too short to make direct links between distant colonies. Isolation by distance is apparently not common in bats (Burland and Worthington Wilmer 2001), but has also been found in Rhinolophus monoceros (Chen et al. 2006), P. auritus (Burland et al. 1999), Myotis septentrionalis (Arnold 2007) and in autosomal genes of M. bechsteinii (Kerth and Petit 2005). Finally, the structuring in multiple demes that was inferred from the genetic data (Ramos Pereira et al. submitted) was confirmed by our mark-recapture data (Fig 1), as we found few opportunities for gene flow between those demes (Table 1). This seems to be a consequence of the rarity of potential mating roosts between them, which results in gaps of strong resistance to gene flow. Our results have several implications for the conservation of this species, which has a status of “Vulnerable” (Cabral et al. 2005). The confirmation with the behavioural data of the existence of separate demes, underlines the need to treat them as independent management units, in order to preserve the full variability of the species and any potential local adaptations. In addition, the confirmation of the strict philopatry to the maternity colonies shows that it is important to monitor and avoid declines in each of them, as one can not count on a rescue effect of immigrants to help colonies recover. Finally, we have demonstrated the importance of preserving mating roosts, as they are key in the maintenance of the existing gene flow among colonies.
Acknowledgements We would like to thank the many colleagues who provided help in the field, especially to Hugo Rebelo, Sofia Lourenço, Tiago Marques, Gabriel Mendes, Francisco Rasteiro, Nuno Vieira and Henrique Vicêncio. Several Spanish colleagues have been kindly reporting the ring numbers of bats that were found in their working areas. Peter Lina helped to find bibliography, and Luka Clarke made useful comments on earlier versions of the manuscript. Bats were ringed under licence from the “Instituto da Conservação da Natureza e da Biodiversidade”.
References Arnold BD (2007) Population structure and sex-biased dispersal in the forest dwelling vespertilionid bat, Myotis septentrionalis. Am Midl Nat 157:374-384
48 Chapter 3
Baagøe HJ (1977) Age determination in bats (Chiroptera). Vidensk Meddr dansk naturh Foren 140:53-92
Bengtsson BO (1978) Avoiding inbreeding: at what cost? J theor Biol 73:439-444
Burland TM, Barratt EM, Beaumont MA, Racey PA (1999) Population genetic structure and gene flow in a gleaning bat, Plecotus auritus. Proc R Soc Lond B 266:975-980
Burland TM, Barratt EM, Nichols RA, Racey PA (2001) Mating patterns, relatedness and the basis of natal philopatry in the. brown long-eared bat, Plecotus auritus. Mol Ecol 10:1309-1321
Burland TM, Worthington Wilmer J (2001) Seeing in the dark: molecular approaches to the study of bat populations. Biol Rev 76:389-409
Burland TM, Entwistle AC, Racey PA (2006) Social and population structure in the brown long-eared bat Plecotus auritus. In: Zubaid A, MacCracken GF, Kunz TH (eds) Functional and evolutionary ecology of bats. Oxford University Press, New York, pp 185-198
Cabral MJ (coord.), Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira E, Palmeirim JM, Queiroz AI, Rogado L & Santos-Reis M (Eds.) (2005) Livro Vermelho dos Vertebrados de Portugal. Instituto da Conservação da Natureza, Lisboa
Castella V, Ruedi M, Excoffier L, Ibanez C, Arlettaz R, Hausser J (2000) Is the Gibraltar Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertilionidae)? Mol Ecol 9:1761-1772
Chen S, Rossiter SJ, Faulkes CG, Jones G (2006) Population genetic structure and demographic history of the endemic Formosan lesser horseshoe bat (Rhinolophus monoceros). Mol Ecol 15:1643-1656
Dechmann DKN, Kalko EKV, Kerth G (2007) All-offspring dispersal in a tropical mammal with resource defense polygyny. Behav Ecol Sociobiol 61:1219-1228
Dice LR, Howard WE (1951) Distance of dispersal by prairie deermice from birthplaces to breeding sites. Contrib Lab Vert Biol Univ Mich 50:1-13
Dwyer PD (1963a) The breeding biology of Miniopterus schreibersi blepotis (Temmick) (Chiroptera) in north-eastern New South Wales. Aust J Zool 11:219-240
Dwyer PD (1963b) Seasonal changes in pelage of Miniopterus schreibersi blepotis (Chiroptera) in north-eastern New South Wales. Aust J Zool 11:290-300
Fenton MB, Thomas DW (1985) Migrations and dispersal in bats (Chiroptera). Contrib Mar Sci 27:409-424
Fleming TH (1988) The short-tailed fruit bat: a study in plant-animal interactions. University of Chicago Press, Chicago
Fleming TH, Eby P (2003) Ecology of bat migration. In: Kunz TH, Fenton MB (eds.) Bat ecology. University of Chicago Press, Chicago, pp 156-208
49 Chapter 3
Frankham R, Ballou JD, Briscoe DA (2002) Introduction to Conservation Genetics. Cambridge University Press.
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618- 620
Humphrey SR, Cope JB (1976) Population ecology of the little brown bat, Myotis lucifugus, in Indiana and north-central Kentucky. American Society of Mammalogy Special Publication 4:1-88
Kerth G, Mayer F, König B (2000) Mitochondrial DNA (mtDNA) reveals that female Bechstein’s bats live in closed societies. Mol Ecol 9:793-800
Kerth G, Safi K, König B (2002) Mean colony relatedness is a poor predictor of colony structure and female philopatry in the communally breeding Bechstein's bat (Myotis bechsteinii). Behav Ecol Sociobiol 52:203-210
Kerth G, Kiefer A, Trappmann C, Weishaar M (2003) High gene diversity at swarming sites suggest hot spots for gene flow in the endangered Bechstein's bat. Cons Gen 4:491-499
Kerth G, Morf L (2004) Behavioural and genetic data suggest that Bechstein’s bats predominantly mate outside the breeding habitat. Ethology 110:987-999
Kerth G, Petit E (2005) Colonization and dispersal in a social species, the Bechstein’s bat (Myotis bechsteinii). Mol Ecol 14:3943-3950
McCracken GF (1987) Genetic structure of bat social groups. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 281-298
Miller-Butterworth CM, Jacobs DS, Harley EH (2002) Isolation and characterization of highly polymorphic microsatellite loci in Schreibers' long fingered bat, Miniopterus schereibersii (Chiroptera: Vespertilionidae). Mol Ecol Notes 2:139-141
Miller-Butterworth CM, Jacobs DS, Harley EH (2003) Strong population structure is correlated with morphology and ecology in a migratory bat. Nature 424:187-191
Miller-Butterworth CM, Eick G, Jacobs DS, Schoeman MC, Harley EH (2005) Genetic and phenotypic differences between South African long-fingered bats, with a global miniopterine phylogeny. J Mamm 86:1121-1135
Palmeirim JM, Rodrigues L (1993) The 2-minute harp trap for bats. Bat Res News 34:60-64
Palmeirim JM, Rodrigues, L (1995) Dispersal and philopatry in colonial animals: the case of Miniopterus schreibersii. In: Racey PA, Swift SM (eds). Ecology, Evolution and Behaviour of Bats. Oxford University Press, Oxford, pp 219-231
Petit E, Mayer F (1999) Male dispersal in the noctule bat (Nyctalus noctula): where are the limits? Proc R Soc Lond B 266:1717-1722
Petit E, Mayer F (2000) A population genetic analysis of migration: the case of the noctule bat (Nyctalus noctula). Mol Ecol 9:683-690
50 Chapter 3
Petri B, Paabo S, Von Haeseler A, Tautz D (1997) Paternity assessment and population subdivision in a natural population of the larger mouse-eared bat Myotis myotis. Mol Ecol 6:235-242
Ramos Pereira MJ, Salgueiro P, Rodrigues L, Coelho MM, Palmeirim JM (submitted) Population structure of a cave-dwelling bat, Miniopterus schreibersii: Does it reflect history and social organization? J Hered
Rivers NM, Butlin RK, Altringham JD (2006) Autumn swarming behaviour of Natterer’s bats in the UK: Population size, catchment area and dispersal. Biol Conserv 127:215- 226
Rodrigues L (1999) Miniopterus schreibersii. In: Mitchell-Jones AJ, Amori G, Bogdanowicz W, Krystufek B, Reijnders PJH, Spintzenberger F, Stubbe M, Thissen JBM, Vohralik V, Zima J (eds) The Atlas of European Mammals. Academic Press, London, pp 154-155
Rodrigues L, Palmeirim JM (in press) Migratory behaviour of Miniopterus schreibersii (Chiroptera): when, where, and why do cave bats migrate in a Mediterranean region? J Zool DOI 10.1111/j.1469-7998.2007.00361.x
Rossiter SJ, Jones G, Ransome RD, Barratt EM (2000) Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc R Soc Lond B 267:545-551
Serra-Cobo J (1989) Biological and ecological study of the Miniopterus schreibersii. PhD thesis. Barcelona, University of Barcelona
Sinclair EA, Webb NJ, Marchant AD, Tidemann CR (1996) Genetic variation in the Little Red Flying-fox, Pteropus scapulatus (Chiroptera: Pteropodidae): implications for management. Biol Conserv 76:45-50
Tian L, Liang B, Maeda K, Metzner W, Zhang S (2004) Molecular studies on the classification of Miniopterus schreibersii (Chiroptera: Vespertilionidae) inferred from mitochondrial cytochrome b sequences. Folia Zool 53:303-311
Tuttle MD (1976) Population Ecology of the Gray Bat (Myotis grisescens): Philopatry, Timing, and Patterns of Movement, Weight Loss during Migration, and Seasonal Adaptive Strategies. Occas Pap Mus Nat Hist Univ Kans 54:1-38
Veith M, Beer N, Kiefer A, Johannesen J, Seitz, A (2004): The role of swarming sites for maintaining gene flow in the brown long-eared bat (Plecotus auritus). Heredity 93:342-349
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358-1370
Wiklund CG (1996) Determinants of dispersal in breeding merlins (Falco columbarius). Ecology 77:1920-1927
Wilkinson GS, Fleming TH (1996) Migration and evolution of lesser long-nosed bats Leptonycteris curasoae, inferred from mitochondrial DNA. Mol Ecol 5:329-339
Worthington Wilmer J, Moritz C, Hall L, Toop J (1994) Extreme population structuring in
51 Chapter 3 the threatened ghost bat, Macroderma gigas: evidence from mitochondrial DNA. Proc R Soc Lond B 257:193-198
Zahn A (1998) Individual migration between colonies of Greater mouse-eared bats (Myotis myotis) in Upper Bavaria. Z Säugetierkd 63:321-328
Zahn A, Dippel B (1997) Male roosting habits, mating system and mating behaviour of Myotis myotis. J Zool 243:659-674
52
4
Critical times
Paper III Zahn A., Rodrigues L., Rainho A. & Palmeirim J.M. (2007) Critical times of the year for Myotis myotis, a temperate zone bat: roles of climate and food resources. Acta Chiropterologica 9: 115-125.
53
Chapter 4
55 Chapter 4
56 Chapter 4
57 Chapter 4
58 Chapter 4
59 Chapter 4
60 Chapter 4
61 Chapter 4
62 Chapter 4
63 Chapter 4
64 Chapter 4
65
5
Roosting behaviour and Phenology
Paper IV Rodrigues L., Zahn A., Rainho A. & Palmeirim J.M. (2003) Contrasting the roosting behaviour and phenology of an insectivorous bat (Myotis myotis) in its southern and northern distribution ranges. Mammalia 67: 321-335.
67
Chapter 5
69 Chapter 5
70 Chapter 5
71 Chapter 5
72 Chapter 5
73 Chapter 5
74 Chapter 5
75 Chapter 5
76 Chapter 5
77 Chapter 5
78 Chapter 5
79 Chapter 5
80 Chapter 5
81 Chapter 5
82 Chapter 5
83
6
General Discussion: the results in the context of bat conservation in Portugal
85
6. General Discussion: the results in the context of bat conservation in Portugal The main results of these studies have been discussed in the papers presented in Chapters 2 to 5. The results give scientific support to some of the conservation measures that have been implemented in the past few years and will hopefully serve as background for the implementation of additional management measures to protect cave-dwelling bats in Mediterranean areas. In this final chapter, the main research questions of this thesis are discussed and integrated with specific management measures. Particular emphasis is given to the management of populations of Miniopterus schreibersii and Myotis myotis in Portugal, but this discussion is relevant to bat conservation elsewhere, especially in the Mediterranean.
6.1 Migratory behaviour Three main issues were addressed using M. schreibersii as a model: (1) timing of migrations, (2) where bats migrate to, and (3) the causes for regional migrations.
Timing of migrations The knowledge of the temporal patterns of bat migrations among roosts is essential to plan when roost management measures should be taken. Examples of measures that should not take place while bats are more vulnerable, namely during hibernation and maternity periods, are removal of garbage, stabilization of ceiling or walls, and allowing organized visits (e.g., speleological courses). Prior to our work, there were a few publications on the migratory behaviour of M. schreibersii (e.g., Aellen 1983; Rodrigues 1989; Serra-Cobo & Balcells 1991; Palmeirim & Rodrigues 1992; Avril 1997; Serra-Cobo et al. 1998; Serra-Cobo et al. 2000), but to our knowledge none described it with the detail of this dissertation. Like the above cited papers, our data showed that M. schreibersii performs seasonal migrations, which result in major population shifts. Migratory movements were least frequent during winter, as bats generally hibernated and seldom changed roost. After hibernation, most females migrated to new sites and most changed roost at least once during each spring. Some of these caves used by bats in the spring will later harbour nurseries, but at this time females are often still not in their own maternity roost. As spring ended, the great majority of females made migrations to reach their maternity sites, often just before giving birth, in early June. Soon after juveniles were weaned, females moved to caves where most spent the autumn and where they sometimes also remained throughout the winter. Males showed a broadly similar
87
Chapter 6 migratory pattern, but differed in that they left the hibernacula later than females and made more frequent inter-roosts movements throughout the maternity season. Taking into account this pattern, maternity roosts of M. schreibersii should not be disturbed especially between the beginning of June and the end of July, and hibernation roosts should not be disturbed especially between mid December and the end of February. However, since there are inter-annual variations, it is reasonable to recommend that maternity roosts of M. schreibersii should not be disturbed especially between mid May and mid August, and hibernation roosts should not be disturbed especially between beginning of December and mid March. These recommendations corroborate in general those included in Palmeirim & Rodrigues (1992), which were drawn up using a smaller dataset; the major difference concerns the beginning of the hibernation season, which previously was assumed to start earlier, in mid November. Taking into consideration the high number of recaptures used in the definition of this pattern (n=1139), we consider that it is a good representation of the reality. However, it would be important to increase to number of recaptures of M. schreibersii in the autumn, which is the season with fewest recaptures.
Where bats migrate to In the case of migratory species, the knowledge of the migration map is necessary to protect them, since it may be necessary to protect the network of roosts used throughout the yearly cycle (Fleming & Eby 2003). Before the preparation of this thesis, only a very preliminary map of the migrations of M. schreibersii in Portugal was available (Rodrigues 1989; Palmeirim & Rodrigues 1992). The new data now collected allows a much more complete definition of the roosts that have links to each of the maternity colonies (Table 6.1). This information is of critical importance in the monitoring and conservation of each colony. Home ranges of the seven best known maternity roosts are presented in Figure 3 of Chapter 2 (from North to South, Tomar, Alcanena, Marvão, Sesimbra I, Moura I, Santiago Cacém, and Loulé I). The effective protection of each maternity roost implies the protection of the entire network of roosts from which it is dependent. The great majority of the most important roosts are now included in the list of Special Areas of Conservation designated for Natura 2000 network. However, there are still two important roosts of M. schreibersii that should receive protected status: the hibernation roost Mogadouro I and the maternity roost Óbidos.
88 Chapter 6
Table 6.1 - Network of roosts associated to each maternity colony of M. schreibersii. Maternity roost Associated network of roosts Miranda Douro Mogadouro I Mogadouro II Mogadouro I, Figueira Castelo Rodrigo I Figueira Castelo Rodrigo I Marvão Tomar Alcanena, Porto Mós I, Cadaval, Vila Nova Ourém, Marvão, Montemor-o-Novo I, Óbidos, Alcobaça I, Moura I, Pombal I, Sesimbra I, Sesimbra II, Sesimbra III, Torres Novas II Alcanena Óbidos, Cadaval, Montemor-o-Novo I, Tomar, Alcobaça I, Porto Mós I, Vila Nova Ourém, Marvão, Coimbra I, Sesimbra II Marvão Moura I, Montemor-o-Novo I, Seia, Spanish I Óbidos Cadaval Sesimbra I Cadaval, Óbidos, Montemor-o-Novo I, Lisboa, Santiago Cacém, Sesimbra IV, Sesimbra III, Porto Mós I, Sesimbra II Moura I Moura III, Marvão, Loulé I, Serpa, Loulé II Santiago Cacém Sesimbra II, Loulé II, Loulé I III, Loulé I, Grândola I, Odemira VII, Sesimbra I, Aljezur II Odemira I none (no movements detected) Loulé I Loulé II, Loulé IV, Aljezur II, Santiago Cacém, Moura I, Odemira VII, Montemor-o-Novo I, Spanish II, Spanish III, Spanish IV
Although the roost networks of the majority maternity colonies is already well known, there are still some gaps concerning some colonies of M. schreibersii less visited and where less bats were ringed (mostly because they have a difficult and dangerous access, or because they were found more recently): Miranda Douro, Mogadouro II, Figueira Castelo Rodrigo I, Óbidos and Odemira I. It would be important to intensify the work in these roosts. Many of our populations of M. schreibersii are shared with Spain, as bats migrate among roosts located in the two countries. Although we already have a large number of recaptures of Portuguese rings in Spain, thanks to the kind collaboration of several Spanish colleagues, the picture of these international migrations is still quite incomplete. This is a handicap for the planning of monitoring and conservation measures of several important Spanish and Portuguese maternity colonies. Further integration of bats research and conservation between the two countries is, therefore, highly desirable.
Causes for regional migration In order to understand the phenomenon of migration by bats it is important to learn about the factors that motivate this behaviour, thus determining what its adaptive advantages are. In general it is assumed that, as for other long distance vertebrate migrants, climate seasonality induces the long-distance two-way movements that follow
89 Chapter 6 a North-South pattern in the temperate zones (Fleming & Eby 2003). However, the motivation for the regional migrations that do not follow clear geographic trends, which in fact are the most common in bats, is less obvious. It is generally accepted that regional migrations are related to the search for roosts with microclimatic conditions particularly suited for each season (McNab 1982; Baudinette et al. 1994), and some movements towards hibernation roosts with distinctive microclimates corroborate this hypothesis. However, the explanation for movements at other seasons is not always obvious. The comparison of two potential drivers for migration of M. schreibersii (temperature in the roosts and at the foraging areas) demonstrated that these bats made migrations to reach roosts that had internal temperatures particularly suited for each phase of their annual cycle. This strongly corroborates the idea that the temperature of roosts and associated advantages at metabolic level, are major drivers for regional migrations in cave-dwelling species. Migration, even at a regional level, is a behaviour often associated to important costs. In general there is an increase in mortality associated to the travel between roosts. But in regional migrations the main costs of inter-roost migrations are probably associated to the need to learn how to exploit the new environment for roosting, foraging, getting water, avoiding predation, etc. With all these costs it is natural that bats only migrate between roosts if there are advantages associated to the roost changes that more than compensate the costs. Our conclusion that the main reason why M. schreibersii migrates is the search for roosts with particular thermal characteristics suitable for each time of the year, highlights the need to maintain a network of roosts with suitable temperatures for the different phases of the annual cycle. In Portugal we recorded this species in roosts with the following temperatures along the annual cycle: Hibernation season – 11.4ºC, on average (minimum: 3.3ºC; maximum: 18.5ºC) Spring – 16ºC, on average (minimum: 12.6ºC; maximum: 19.5ºC) Maternity season – 19.4ºC, on average (minimum: 16.8ºC; maximum: 23.6ºC) Autumn – 12.9ºC, on average (minimum: 12.5ºC; maximum: 13.5ºC) Knowledge of the thermal preferences of bats in roosts and the monitoring of their temperatures are important from a conservation perspective because it they may help understanding any changes in the way a roost is used by bats (e.g., the abandonment of roosts). In fact, although underground temperatures tend to be quite stable, there are factors that may change them in both natural and artificial underground roosts. For example, the internal topography of a cave or mine gallery can change as a result of rock falls, and this can result in changes in airflow patterns and,
90 Chapter 6
consequently, on microclimatic conditions. The total or partial closure of mine chimneys for safety reasons, or their blockage by natural vegetation, can have similar consequences. The knowledge of these thermal preferences is also important if new replacement roosts are to be constructed. The design of such roosts should aim at achieving the temperatures most suitable for the times of the year when the bats are expected to use them. In fact, the configuration of the underground roosts can determine the internal microclimate; for example, domes in the roof can collect and hold rising warm air, leading to an elevated temperature, whereas low parts of systems can act as sinks for cold air, leading to a lower temperature (Mitchell-Jones et al. 2007). Likewise, descending galleries will tend to accumulate cold air, and ascending galleries warm air. Finally, chimneys can also be used to manipulate the temperatures of galleries and chambers. In Portugal these principles and the knowledge of the thermal preferences of several species of bats have already been used to design two replacement roosts for cave-dwelling bats. Both are located in the valley of the Guadiana, where they were built as compensation for roosts flooded by the Alqueva and Pedrogão dams, and the older is already being used by good numbers of bats (Rainho et al. 2006). Knowledge of the thermal preferences of roosting bats can also be essential in the few circumstances when it is desirable, and possible, to manipulate roost temperature artificially. Experimental heating of a maternity roost already improved the reproduction success of R. ferrumequinum, via the growth and survival of the young (Ransome 1998).
6.2 Spatial behaviour and Gene flow Determining the behavioural factors that control gene flow among populations is important to understand how the genetic structure of each species arose and is maintained. Intensive ringing-recapture studies are the best way to learn about the philopatric and migratory behaviours of bats (e.g., Dwyer 1966; Tuttle 1976), but to our knowledge no study of this nature has made a quantitative assessment of the potential impact of each of these behaviours on gene flow. Another important issue related to the study of gene flow is the knowledge of the organization of maternity colonies in demes, since the planning of management actions should be based in conservation units, either Evolutionary Significant Units or Management Units. Ramos Pereira et al. (submitted) studied the genetic structure of the Portuguese populations of M. schreibersii analysing bats from 11 out of the 12
91 Chapter 6 known maternity colonies. Four major demes were found, with a relatively high differentiation level among them: North East (includes three colonies: Miranda Douro, Mogadouro II and Figueira Castelo Rodrigo I), West-Centre (includes three colonies: Tomar, Alcanena and Sesimbra I), East-Centre (includes only Marvão) and South (includes four colonies: Moura I, Santiago Cacém, Odemira I and Loulé I). Using the results of our large scale ringing project of M. schreibersii, three potential sources of gene flow were assessed (the first two related to philopatry, and the third mostly dependent on the patterns of regional migrations during the mating season): (1) dispersal of juveniles to foreign colonies, (2) colony switching by adults, and (3) mating between individuals of different colonies. Additionally, results were related to the genetic structure of the Portuguese populations of this species, recently studied. The analysis of the recaptures showed no cases of juvenile dispersal. Regarding adults, very few cases of female dispersal were observed and the males that were found with the maternity colonies also showed a high degree of attachment to them (although most males do not spend the maternity season in the nurseries and do not have any known role in them). Since the two potential sources of gene flow related to philopatry seemed to be minimal, it seemed that gene flow should be almost exclusively dependent of the mating opportunities between individuals of the different maternity colonies. In fact, it was demonstrated that the gene flow potentiated by regional migrations was intense and we concluded that regional migrations, rather than dispersal, are the main agent of gene flow between colonies of M. schreibersii. It was also found that gene flow was limited by the distance between nurseries and by the availability of mating roosts between them, and that it was asymmetrical (being the dominant direction from the largest to the smallest colonies). Taking into consideration the strict philopatric behaviour presented by females to their maternity colonies, it is essential to manage each colony as a demographically autonomous unit. This because managers can not count on the potential rescue effect of immigrant animals to help colonies recover, which would be more likely if bats were more willing to disperse to alternative roosts. The monitoring of the 12 known maternity colonies should continue, in order to detect any decline. If any problem is detected (such as a significant decline in the number of bats present, confirmation of non- reproduction in a particular year, or presence of signs of major disturbance by visitors), the situation should be closely monitored and appropriate measures should be taken. On other hand, since gene flow in maternity colonies is almost exclusively dependent on the mating opportunities between individuals of the different maternity colonies, it is very important to preserve mating roosts, as they are very important to
92 Chapter 6
keep the existing gene flow among colonies. While in the case of Portuguese M. schreibersii, many important mating roosts are already known and protected, this is the time of the year in which the whereabouts of these bats are least known. In the light of our results, which reinforced the importance of autumn roosts for the maintenance of population connectivity, we conclude that it is very important to continuing surveying these roosts and, whenever possible, protect them. Our observations on philopatry and seasonal migrations of M. schreibersii and the resulting table of potential gene flow are compatible with the genetic structure of the population for both nuclear and mitochondrial DNA recently made available for the same population (Ramos Pereira et al. submitted), corroborating the idea that the described behaviour parameters are key in the shaping of its genetic structure. Particularly, it was analysed how potential gene flow relates to the deme structure. Using the data of ringing-recapture, the Portuguese population of M. schreibersii of the seven studied colonies seems to be divided in three demes: North East (includes only Miranda Douro), Centre (includes five colonies: Alcanena, Tomar, Sesimbra I, Marvão e Moura I) and South (includes only Loulé I). However, the level of isolation among them is variable: the North East deme seems to be very isolated from the rest, and the colonies in the West-Centre (namely, Tomar, Alcanena and Sesimbra I) and in the South of the country are also very isolated from each other. The situation of the colonies of Marvão and Moura I is less clear; Marvão has relatively few links to the colonies of the West-Centre and Moura I seems to be even more isolated. Figure 6.1 represents the demes found using ringing-recapture and genetic techniques. The discrepancy in the deme structure found with the two different techniques, particularly regarding Moura I, may be explained by the fact that we analysed the mating potential using only data from the first phase of the ringing programme (1987- 1992). Although this restriction was necessary to avoid biases resulting from the very uneven sampling during the second phase (after 1992), as explained in Chapter 3, the used dataset did not include movements between Moura I and Loulé I, only detected later. In fact, Moura I is genetically and geographically closer to Loulé I. Concerning the organization of the population in demes, in order to preserve the full genetic variability of the species and any potential local adaptations, they should be treated as distinct Management Units. If re-introductions or translocations would be needed to recover from a regional catastrophic population reduction, these Management Units should be taken into consideration. We believe that the deme
93 Chapter 6 structure used for conservation purposes should follow the most conservative approach, so Marvão should be treated as an independent deme.
Fig. 6.1 – Demes of Miniopterus schreibersii found with ringing-recapture and genetic techniques (grey and black, respectively).
It is important to note that the intensive ringing study, as well as the genetic study, only covered the Portuguese populations of M. schreibersii. However, it is almost certain that some of the maternity colonies are likely to maintain strong gene flow with some colonies in Spain, and therefore form transfrontier demes. This reinforces the idea, advanced above, that the conservation of this species, as well as that of other migratory bats, is best deal with cooperative efforts between Portugal and Spain.
6.3 Critical times Bats that live in the temperate zones have a marked seasonal cycle, and so their energy requirements are likely to vary along it. At the same time, the availability of the food resources of which most temperate bats depend, insects, are know to vary seasonally (Arletazz et al. 2001). This raises the possibility that in the temperate zones
94 Chapter 6
bats may be subjected to critical periods, i.e., periods of the year in which animals have difficulty fulfilling their energy requirements (Racey 1982; Barclay 1991). The identification of these seasonal resource bottlenecks, and the understanding of their determinants, can be important to understand the distribution and abundance of species, and to plan management actions that benefit threatened species (Payne & Wilson 1999; Primack 2002). To our knowledge, a study that analysed this problem in temperate zone bats was never carried out. Using M. myotis as a model, we determined if there may be critical times of the year for temperate zone bats in two climatically different regions (Portugal and Germany). In addition, we studied the potential roles played by climate and food resources in the origin and timing of these potential bottlenecks. The comparison of the patterns of seasonal fluctuation of body mass of M. myotis in Portugal and Germany showed differences in the various phases of the annual cycle. In Germany, after giving birth females remained in good condition, whereas Portuguese females showed a deteriorated condition and only gained body mass in autumn. In Germany, females reached hibernation in better condition but suffered a more marked overall body mass loss during winter. Even though food is abundant after ending hibernation, the condition of German females remained poor for about one month after that. The patterns of body mass changes of males of both regions were very similar to those observed for females. The study of seasonal prey availability indicated a fall in prey abundance during the summer in Portugal. Taking into consideration that this relative scarcity of food resources resulted in a worse body condition, we concluded that food resources were indeed a limiting factor for M. myotis, so summer (June to September) was considered as a critical time for Portuguese bats. Furthermore, it was concluded that the period of hibernation (mid December to end of February) was also a potentially difficult time for our bats. The situation in Germany was very different, as it was found that critical times included the long hibernation period (November to March/April) and sometimes the early spring (April), because bad weather made foraging difficult. Since food resources can act as a limiting factor for M. myotis, feeding areas near important colonies need to be managed in order to avoid changes in practices that accentuate resource bottlenecks. In the case of Portugal, we now know that the main concern should be the maintenance of the quality of the summer foraging habitats. This species forages mostly in agricultural and open forest habitats (Güttinger 1997; Zahn et al. 2005), and in Portugal particularly in oak woodlands and other open habitats (Rainho 2007). The maintenance of these habitats could be achieved with agri-
95 Chapter 6 environment schemes, which are expected to be set up all over Europe with the objective of reversing the trend of agriculture intensification. Such schemes will involve the payment of compensations to stakeholders that voluntarily practise environmentally friendly farming methods (Rainho 2007). Bats will benefit from them if their foraging needs at critical times are taken into consideration when drawing the local regulations of the agri-environmental schemes. Particularly, extensive livestock grazing should also be maintained, since dung beetles are a common prey of M. myotis (Ramos Pereira et al. 2002). Furthermore, the maintenance of oak woodlands should also be assured by the implementation of the EU Habitats Directive (92/43/EEC), since it is a habitat requiring the classification of Special Areas of Conservation designated for the Natura 2000 network. Portuguese colonies whose feeding areas need to be properly managed for M. myotis are: Figueira Castelo Rodrigo I, Miranda Douro, Mação, Tomar, Torres Novas, Alcanena, Marvão, Arronches, Montemor-o-Novo I, Grândola I, Moura I, Alandroal, and Porto Mós IV. If breeding of M. myotis is confirmed in Mogadouro II and Odemira I, then these two colonies should also be included in the previous list. The feeding areas of two important colonies of M. myotis in southern Portugal (Montemor-o-Novo I and Moura I) have been studied (Rainho 1995; Rainho & Palmeirim 1999), and there is now information to give advice for the compatibilization of the foraging needs of those colonies and the use of land around them. The foraging ecology of other colonies known in Portugal has not been studied, but the knowledge obtained in the studies so far carried out can help delineating conservation measures for them. This is mostly valid for the colonies in southern Portugal, as the habitats available around the colonies in the north of the country are often different.
6.4 Roosting behaviour and Phenology The knowledge of roosting behaviour and phenology is important to understand potential changes in roost occupancy and to plan when management measures should be taken. M. myotis is well studied in its northern range, but little data was available in the south, particularly in Iberia. Besides data on distribution and movements, there are few papers on ecological characteristics of this species in this region (e.g., Paz 1985, 1986; Garrido García 1997; Ibáñez 1997; Ramos Pereira et al. 2002). Knowledge on roosting behaviour and phenology of bats in the Mediterranean region is needed because the information made available by studies done in central Europe often does not apply here. Consequently, it would be erroneous to base decisions about conservation measures on the results of those studies.
96 Chapter 6
Roosting behaviour and phenology of M. myotis were studied comparing them in Mediterranean and Central Europe. Namely, we studied: (1) roosting and clustering behaviour, (2) maternity and hibernation periods, (3) mating activity, and (4) sexual maturation.
Roosting and clustering behaviour The comparison of the roosting and clustering behaviour of M. myotis in Portugal and Germany revealed several differences. In the south, maternity colonies occur mainly in underground roosts, whereas in the north they occur in buildings, mostly in attics. Southern roosts presented stable temperatures, and nursing bats formed tight clusters and remained in the same location for long periods. Maternity colonies usually used multiple roosting locations within the same cave, often within the same chamber or gallery, well inside the roosts. Nursery clusters were in general larger and were often associated with other species, particularly with M. schreibersii. Sometimes these clusters were joined by males, who were younger and had smaller epididymes than those that remained separated from the nursing colonies. Northern roosts presented much greater daily and seasonal fluctuations of temperature, and the density and location of clusters frequently changed in response to temperature variations over the day. Males rarely joined nursery clusters. It was found that in Portugal M. myotis chooses roosts with the following temperatures: Hibernation season – 12.7ºC, median (minimum: 8.4ºC; maximum: 18.2ºC) Maternity season – 15ºC, median (minimum: 11.7ºC; maximum: 19.5ºC) As referred above for M. schreibersii, a good knowledge of the thermal requirements of roosting M. myotis can be important to understand rises or drops in the occupancy of roosts. In addition, such knowledge is also very important to manage natural and artificial roosts, and in the design of new replacement roosts, such as those that have been built as compensatory measures for the constructions of the Alqueva and Pedrogão dams.
Maternity and hibernation periods, and mating activity In Portugal M. myotis started clustering at the maternity roosts in March, and the maximum number of adults was reached in the beginning of April. Depending on the years, young were born between the beginning of April and mid May. Adult females started to abandon the maternity clusters after fledging in June or July. The first observations of male/female pairs at male roosts were recorded in late July. Although
97 Chapter 6 the peak of occurrence of such pairs in Portugal was in September-October, they were present through autumn and winter. Bats were usually active in Portuguese roosts until about mid December, although this varied with weather conditions. Only in January and February most bats were found in deep torpor, although in mid February some were already active. Overall, hibernation in Portugal was short, usually lasting two months or less. Taking into account the pattern of the annual cycle of M. myotis, maternity roosts of this species should not be disturbed especially between mid March and the end of July, and hibernation roosts should not be disturbed especially between mid December and the end of February. However, since there are inter-annual variations in phenology, it is reasonable to recommend that maternity roosts of M. myotis should not be disturbed especially between the beginning of March and mid August, and hibernation roosts should not be disturbed especially between the beginning of December and mid March. These recommendations corroborate those included in Palmeirim & Rodrigues (1992), which were drawn up using a smaller dataset.
6.5 Future Work The effective conservation of Portuguese cave-dwelling bats requires the continuation of field work to clarify and strength of some reported patterns and the investigation of several additional topics. Throughout this thesis we referred monitoring and research activities that are required to improved our capacity to preserve and manage the two study species. It would be difficult to list here all research projects potentially interesting and important for their conservation, but we would like to highlight some that would be a logical sequence of the work that we carried out:
- Study the seasonal occupation of the lesser known roosts. While most key roosts for both study species have been identified, the patterns of seasonal occupation of some of them are poorly known. The scientific interest of this study would be minimal, but it would provide important data for conservation, as lack of knowledge on this issue hinders the planning of the conservation and management of some key roosts. - Study the population dynamics of M. schreibersii. Data from the ringing programme that we carried out for many years in some colonies of this species should be suitable to do a very complete study of its population dynamics. The results could shed light on issues like generation time, duration of reproductive life, and major mortality factors, which could be important for conservation planning.
98 Chapter 6
- Study the migration patterns and deme structure of M. myotis. As explained above, information on migration patterns is very useful to plan conservation. The existing data from the past ringing activities and some additional ringing efforts could provide a good picture of these patterns, which to our knowledge is still not available for any Mediterranean region. A genetic study, apparently never carried out in cave-dwelling populations of M. myotis, would be a complement to refine the definition of demes and of Management Units. - Study the roosting behaviour and phenology of M. schreibersii. This study would fulfil an important gap in our knowledge of the species, which may be important for the proper management of existing roosts and, whenever required, the construction of replacement roosts. - How to minimize critical times of the year for M. myotis. We determined that in the case of southern Portugal the long dry summer is a critical time for the survival of M. myotis, apparently due to the relative scarcity of prey. To be able to minimize the risks associated to this resource bottleneck it may be necessary to manage the land around the endangered colonies to optimize the availability of prey. It would be important to carry out the research needed to learn how land management can be used to optimize prey availability at the identified critical times of the year. A similar study focused on M. schreibersii and its prey would also be both interesting, as this species feeds on completely different prey types, and useful for its conservation. - Monitoring programme. Portugal was a pioneer in the monitoring of populations of cave-dwelling bats, and now has one of the longest time series of monitoring data in Europe. This programme is critical to identify declines that may require intervention, and now is also needed to respond to the requirements of European legislation.
Studies similar to these, as well as to those included in this thesis, would be scientifically interesting and useful for conservation if carried out on most of our cave- dwelling bat species. It should be a priority to devote research efforts to some of the most threatened species, in particular Myotis blythii, Rhinolophus euryale, and R. mehelyi. These species have a threatened status and there is already evidence that their populations in Portugal are declining (Rodrigues et al. 2003). In addition, they have a relatively small geographic range, mostly restricted to the Mediterranean region, which leaves Portugal with an important share in the responsibility to preserve them.
While research is critical for conservation, we should never forget that bat
99 Chapter 6 conservation is heavily dependent on public image and awareness. It is essential to maintain educational activities and continue the cooperation with speleological associations and other potential collaborators, such as the media, teachers, NGOs and relevant governmental agencies.
We very much hope that bat conservation in the Mediterranean in general, and in Portugal in particular, will benefit from the results of the studies reported in this thesis. The need to obtain the knowledge to implement scientifically sound conservation measures was always behind the planning of this work. Only part of the aspects of the biology of bats relevant for conservation was covered, and even then only for two species. However, as bats are organisms poorly known and difficult to study, we feel that this is a significant addition to the work that is being carried out by other bat researchers in Mediterranean countries. Together we are building up the knowledge that is making possible the planning of bat conservation, at a time when landscape changes and European policies are posing new challenges, responsibilities, and opportunities across our Continent.
6.6 References Aellen V. (1983) Migration of bats in Switzerland. Bonner zoologische Beitrage 34: 3- 27.
Arlettaz R., Christe P., Lugon A., Perrin N. & Vogel, P. 2001. Food availability dictates the timing of parturition in insectivorous mouse-eared bats. Oikos 95: 105–111.
Avril B.W.P. (1997) Le minioptère de Schreibers: analyse des résultats de baguages de 1936 à 1970. These pour de Doctorat Veterinaire. Ecole Nationale Veterinaire de Toulouse, France.
Barclay R.M.R. (1991) Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. Journal of Animal Ecology 60: 165-178.
Baudinette R.V., Wells R.T., Sanderson K.J. & Clark, B. (1994) Microclimatic conditions in maternity caves of the bent-wing bat, Miniopterus schreibersii: an attempted restoration of a former maternity site. Wildlife Research 21: 607-619.
Dwyer P.D. (1966) The population pattern of Miniopterus schreibersii (Chiroptera) in north-eastern New South Wales. Australian Journal of Zoology 14: 1073-1137.
Fleming T.H. & Eby P. (2003) Ecology of Bat Migration. Pp. 156-208. In: Bat ecology. Kunz T.H. & Fenton M.B. (Eds.) University of Chicago Press, Chicago.
Garrido García J.A. (1997) La alimentación de Myotis myotis (Borkh, 1797) (Chiroptera, Vespertilionidae) en la cuenca del río Guadix (sureste de España). Doñana Acta Vertebrata 24: 27-38.
100 Chapter 6
Güttinger R. (1997) Jagdhabitate des Großen Mausohrs (Myotis myotis) in der modernen Kulturlandschaft. Buwal-Schriftenreihe Umwelt 288.
Ibáñez C. (1997) Winter reproduction in the greater mouse-eared bat (Myotis myotis) in South Iberia. Journal of Zoology 243: 836-840.
MacNab B.K. (1982) Evolutionary alternatives in the physiological ecology of bats. Pp. 151-200. In: Ecology of bats. Kunz T.H. (Ed.). Plenum Press, New York.
Mitchell-Jones A.J., Bihari Z., Masing M. & Rodrigues L. (2007) Protecting and managing underground sites for bats. EUROBATS Publication Series nº 2.
Palmeirim J.M. & Rodrigues L. (1992) Plano Nacional de Conservação dos Morcegos Cavernícolas. Estudos de Biologia e Conservação da Natureza 8. SNPRCN, Lisboa.
Payne R.J.H. & Wilson J.D. (1999) Resource limitation in seasonal environments. Oikos 87: 303-314.
Paz O. de (1985) Contribución al estudio eco-etológico de los quirópteros cavernícolas de 'La Canaleja', Abanades, Guadalajara. Boletin Estacion Central Ecología 14: 77-87.
Paz O. de (1986) Age estimation and postnatal growth in the greater mouse bat Myotis myotis (Borkhausen, 1797) in Guadalajara, Spain. Mammalia 50: 243–251.
Primack R. (2002) Essentials of Conservation Biology. 3rd edition. Sinauer Associates, Sunderland.
Racey P.A. (1982) Ecology of bat reproduction. Pp. 57-68. In: Ecology of Bats. Kunz T.H. (Ed.). Plenum Press, New York.
Rainho A. & Palmeirim J.M. (1999) Foraging behaviour and habitat selection in Myotis myotis. Pp. 53-54. In: Bats & Man. Million Years of Coexistence. Cruz M. & Kozakiewicz K. (Eds.). Abstracts VIIIth European Bat Research Symposium, 23- 27 August 1999, Poland.
Rainho A. (1995) Biótopos de alimentação de algumas espécies de morcegos presentes em quatro regiões a Sul do Tejo. Relatório de Estágio. Universidade de Lisboa, Portugal.
Rainho A., Lourenço S., Rebelo H. & Freitas A. (2006) Bats and Dams - Conservation Actions in the Region of the Reservoirs of Alqueva and Pedrógão. Instituto da Conservação da Natureza, Lisboa.
Rainho A. (2007) Summer foraging habitats of bats in a Mediterranean region of the Iberian Peninsula. Acta Chiropterologica 9: 171-181.
Ramos Pereira M.J., Rebelo H., Rainho A. & Palmeirim J.M. (2002) Prey selection by Myotis myotis (Vespertilionidae) in a Mediterranean region. Acta Chiropterologica 4: 183-193.
Ramos Pereira M.J., Salgueiro P., Rodrigues L., Coelho M.M., Palmeirim J.M.
101 Chapter 6
(submitted) Population structure of a cave-dwelling bat, Miniopterus schreibersii: Does it reflect history and social organization? Journal of Heredity
Ransome R.D. (1998) The impact of maternity roost conditions on populations of greater horseshoe bats. English Nature Research Reports 292.
Rodrigues L. (1989) Ciclo anual de Miniopterus schreibersii (Chiroptera: Miniopteridae): abrigos, migrações e peso. Relatório de Estágio. Universidade de Lisboa, Portugal.
Rodrigues L., Rebelo H. & Palmeirim J.M. (2003) Avaliação da tendência populacional de algumas espécies de morcegos cavernícolas. Relatório técnico final. Centro de Biologia Ambiental / Instituto da Conservação da Natureza, Lisboa.
Serra-Cobo J. & Balcells E. (1991) Migraciones de quirópteros en España. Pp. 181- 209. In: Los murciélagos de España y Portugal. Benzal J. & PAZ O. de (Eds.). ICONA, Madrid.
Serra-Cobo J., Sanz-Trullén V. & Martínez-Rica J.P. (1998) Migratory movements of Miniopterus schreibersii in the north-east of Spain. Acta Theriologica 43: 271- 283.
Serra-Cobo J., López-Roig M., Marquès-Lopez T. & Lahuerta, E. (2000) Rivers as possible landmarks in the orientation flight of Miniopterus schreibersii. Acta Theriologica 45: 347-352.
Tuttle M.D. (1976) Population ecology of the Gray Bat (Myotis grisescens): philopatry, timing, and patterns of movement, weight loss during migration, and seasonal adaptive strategies. Occasional Papers of the Museum of Natural History University of Kansas 54: 1-38.
Zahn A., Haselbach H. & Güttinger R. (2005) Foraging activity of central European Myotis myotis in a landscape dominated by spruce monocultures. Mammalian Biology 70: 265–270.
102