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"Heavy metals in atlantic seabirds: current levels and possible impacts in fitness and behaviour of selected species"
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Abstract(s)
As aves marinhas são omnipresentes, predadores de topo no oceano, e estão sujeitas a
concentrações elevadas de metilmercúrio, mas as relações entre o mercúrio e o
comportamento continuam a ser mal compreendidas. O foco central desta tese é
determinar as concentrações de mercúrio e outros metais pesados em penas e sangue de
aves marinhas e avaliar os efeitos da presença de mercúrio sobre o comportamento e a
aptidão de algumas espécies de aves marinhas.
1. Os efeitos do mercúrio no comportamento das aves foram revistos no Capítulo 2. Os
relatos de efeitos detectáveis do mercúrio no comportamento das aves são, de facto,
poucos. Os efeitos detectáveis sobre o comportamento das aves são, na sua maioria,
descritos em indivíduos expostos a concentrações subletais em laboratórios. Os efeitos,
quando observados na natureza, são muitas vezes difíceis de descrever e quantificar. O
efeito do mercúrio é mais amplamente estudado em aves adultas do que em aves jovens.
Tanto quanto podemos verificar, o efeito do mercúrio no comportamento dos pintos das
aves marinhas nunca foi estudado.
2. No Capítulo 3 foi feita uma análise dos efeitos do mercúrio na sobrevivência das aves
marinhas. Apesar das provas de níveis elevados de mercúrio em aves marinhas, há muito
poucos estudos robustos que reportem uma relação deletéria entre as concentrações de
mercúrio em indivíduos e a sua aptidão. A sobrevivência da prole não parece ser afectada
no ninho, embora alguns estudos prevejam taxas reduzidas de pulgas. A exposição ao
mercúrio não parece causar alterações significativas na longevidade dos adultos, embora
os estudos a longo prazo que incorporam dados sobre o mercúrio sejam limitados. É
possível que as aves marinhas estejam adaptadas às concentrações relativamente elevadas
de mercúrio presentes no ecossistema marinho.
3. A concentração de mercúrio e arsénio nas penas do corpo de cinco espécies de aves
marinhas das Ilhas Falkland foi estudada no Capítulo 4. Neste estudo foram amostradas
diferentes espécies e localizações nas Malvinas, para avaliar a variabilidade inter-espécies
e espacial dentro desta região. Os pinguins roqueiros da Ilha Beauchene, tinham
concentrações mais elevadas de mercúrio e arsénico do que os de outras colónias. A
concentração de mercúrio em plumas de albatroz-de-sobrancelha-negra Thalassarche
melanophris aumentou desde 1986. Os resultados sugerem que o arsénico não se
biomagnifica da mesma forma que o mercúrio ao longo das teias alimentares.
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4. Também estudámos (Capítulo 5) a concentração de elementos vestigiais no sangue de
albatrozes de raça negra das Ilhas Falklands, que aqui mostramos, através do rastreio com
geolocadores, forragens sobre a maior parte da Plataforma Patagónica. As concentrações
de elementos vestigiais no sangue não foram significativamente diferentes entre ilhas, o
que é consistente com as observações de comportamentos de forragens revelando que as
aves de ambas as ilhas forragearam em geral as mesmas áreas nos meses que antecederam
a amostragem. As concentrações de arsénio e selénio nas fêmeas eram mais elevadas do
que nos machos. As diferenças relacionadas com o sexo na concentração destes elementos
podem estar relacionadas com ligeiras diferenças desconhecidas na dieta ou com
diferenças na assimilação entre os sexos.
5. A alma-negra Bulweria bulwerii (predadores aviários altamente especializados de
presas mesopelágicas) foram utilizados como biomonitores dos níveis de mercúrio no
domínio mesopelágico dos oceanos Pacífico e Atlântico no Capítulo 6. As colónias
atlânticas mostraram concentrações mais elevadas de mercúrio do que as do Pacífico. Os
níveis tróficos derivados da análise isotópica de compostos específicos para pintos eram
semelhantes entre as colónias, sugerindo que as diferenças entre os locais não se deviam
a diferenças no nível trófico dessas populações. Os níveis de mercúrio das penas
registados foram inferiores aos registados em 1992 para o Atlântico.
6. Os possíveis efeitos adversos do mercúrio em pintos de alma-negra Bulweria bulwerii
foram avaliados no Capítulo 7. A taxa de crescimento dos pintos foi negativamente
correlacionada com a contaminação por mercúrio. Os pintos com coeficientes de taxa de
crescimento reduzidos para a massa corporal apresentavam um crescimento retardado do
comprimento das asas. Altas concentrações de mercúrio foram associadas ao atraso no
crescimento dos pintos de alma-negra Bulweria bulwerii. O comportamento dos pintos
no ninho não foi influenciado pelos níveis de mercúrio.
7. Os pintos de alma-negra Bulweria bulwerii têm algumas das mais elevadas
concentrações de mercúrio no sangue relatadas entre as aves marinhas. Medimos o
mercúrio no sangue de cada animal adulto de alma-negra Bulweria bulwerii e avaliámos
o seu desempenho em termos de forragens. Não houve relação entre a contaminação por
mercúrio e o desempenho de forragem, medido através da duração da viagem de forragem
e do ganho diário de massa durante uma viagem de forragem. A alma-negra Bulweria
bulwerii parece ser altamente resistente à contaminação por mercúrio.
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Os resultados desta tese fornecem uma linha de referência para estudos de bioindicação
utilizando penas e sangue de espécies seleccionadas de aves marinhas no Oceano
Atlântico e Pacífico. Apesar dos níveis excepcionalmente elevados de mercúrio
acumulado pelas aves marinhas, o seu comportamento parece em grande parte não ser
afectado pelas concentrações de mercúrio em toda a gama aqui medida.
ABSTRACT: The effect of mercury is more widely studied in adult birds than in young birds. Seabirds are ubiquitous, top predators in ocean, and are subjected to elevated methylmercury concentrations, but relationships between mercury and behaviour remain poorly understood. The central focus of this thesis is to determine the concentrations of mercury and other heavy metals in feathers and blood of seabirds and to evaluate the effects of the presence of mercury on the behaviour and fitness of some seabird species. 1. The effects of mercury in the behaviour of birds was reviewed in Chapter 2. Reports of detectable effects of mercury on avian behaviour are, in fact, few. Detectable effects on avian behaviour are mostly described in individuals exposed to sub-lethal concentrations in laboratories. The effects, when observed in nature, are often difficult to describe and quantify. As far as we can ascertain, the effect of mercury on the behaviour of seabird chicks has never been studied. 2. A review of the effects of mercury on survival of seabirds was undertaken in Chapter 3. Despite evidence of elevated mercury levels in seabirds, there are very few robust studies reporting a deleterious relationship between mercury concentrations in individuals and their fitness. Survival of offspring does not appear to be affected in the nest, although some studies predict reduced fledging rates. Mercury exposure does not appear to cause significant changes in adult longevity, although long-term studies incorporating mercury data are limited. It is possible that seabirds are adapted to the relatively high concentrations of mercury present in the marine ecosystem. 3. The concentration of mercury and arsenic in body feathers of five species of seabirds of Falkland Islands was studied in Chapter 4. In this study we sampled different species and locations in the Falklands, to evaluate the inter-species and spatial variability within this region. Rockhopper penguins from Beauchene Island, had higher concentrations of mercury and arsenic than those from other colonies. The concentration of mercury in feathers of black-browed albatrosses increased since 1986. Results suggest that arsenic does not biomagnify the same way as mercury does along food webs. 4. We also studied (Chapter 5) the concentration of trace elements in blood of blackbrowed albatrosses Thalassarche melanophris from the Falklands Islands, which we here show, by tracking with geolocators, forage over most of the Patagonian Shelf. Blood concentrations of trace elements were not significantly different between islands, which is consistent with observations from foraging behaviour revealing that birds from both xii islands foraged in broadly the same areas in the months before sampling. Arsenic and selenium concentrations in females were higher than in males. Sex-related differences in the concentration of these elements may be related to unknown slight differences in diet or to differences in assimilation between sexes. 5. Bulwer's petrels Bulweria bulwerii (highly specialised avian predators of mesopelagic prey) were used as biomonitors of mercury levels in the mesopelagic domain of the Pacific and Atlantic oceans in Chapter 6. Atlantic colonies showed higher mercury concentrations than those from the Pacific. CSIA-AA-derived trophic levels for chicks were similar among colonies, suggesting that differences between locations were not due to differences in the trophic level of those populations. Feather mercury levels recorded were lower than those reported in 1992 for the Atlantic. 6. Possible adverse effects of mercury in chicks of Bulwer’s petrels Bulweria bulwerii were evaluated in Chapter 7. Chick growth rate was negatively correlated to mercury contamination. Chicks with reduced growth rate coefficients for body mass exhibited retarded growth of wing length. High mercury concentrations were associated with delayed fledging in Bulwer’s petrel Bulweria bulwerii chicks. The behaviour of chicks in the nest was not influenced by mercury levels. 7. Bulwer’s petrel have some of the highest reported blood mercury concentrations amongst seabirds. We measured mercury in the blood of individual adult Bulwer’s petrel and assessed their foraging performance. There was no relationship between mercury contamination and foraging performance, as measured through foraging trip duration and daily mass gain during a foraging trip. Bulwer’s petrels Bulweria bulwerii seem to be highly resilient to mercury contamination. The results of this thesis provide a reference line for bioindication studies using feathers and blood from selected seabird species on the Atlantic and Pacific Ocean. Despite the exceptionally high levels of mercury accumulated by seabirds, their behaviour seems largely unaffected by mercury concentrations across the range measured here
ABSTRACT: The effect of mercury is more widely studied in adult birds than in young birds. Seabirds are ubiquitous, top predators in ocean, and are subjected to elevated methylmercury concentrations, but relationships between mercury and behaviour remain poorly understood. The central focus of this thesis is to determine the concentrations of mercury and other heavy metals in feathers and blood of seabirds and to evaluate the effects of the presence of mercury on the behaviour and fitness of some seabird species. 1. The effects of mercury in the behaviour of birds was reviewed in Chapter 2. Reports of detectable effects of mercury on avian behaviour are, in fact, few. Detectable effects on avian behaviour are mostly described in individuals exposed to sub-lethal concentrations in laboratories. The effects, when observed in nature, are often difficult to describe and quantify. As far as we can ascertain, the effect of mercury on the behaviour of seabird chicks has never been studied. 2. A review of the effects of mercury on survival of seabirds was undertaken in Chapter 3. Despite evidence of elevated mercury levels in seabirds, there are very few robust studies reporting a deleterious relationship between mercury concentrations in individuals and their fitness. Survival of offspring does not appear to be affected in the nest, although some studies predict reduced fledging rates. Mercury exposure does not appear to cause significant changes in adult longevity, although long-term studies incorporating mercury data are limited. It is possible that seabirds are adapted to the relatively high concentrations of mercury present in the marine ecosystem. 3. The concentration of mercury and arsenic in body feathers of five species of seabirds of Falkland Islands was studied in Chapter 4. In this study we sampled different species and locations in the Falklands, to evaluate the inter-species and spatial variability within this region. Rockhopper penguins from Beauchene Island, had higher concentrations of mercury and arsenic than those from other colonies. The concentration of mercury in feathers of black-browed albatrosses increased since 1986. Results suggest that arsenic does not biomagnify the same way as mercury does along food webs. 4. We also studied (Chapter 5) the concentration of trace elements in blood of blackbrowed albatrosses Thalassarche melanophris from the Falklands Islands, which we here show, by tracking with geolocators, forage over most of the Patagonian Shelf. Blood concentrations of trace elements were not significantly different between islands, which is consistent with observations from foraging behaviour revealing that birds from both xii islands foraged in broadly the same areas in the months before sampling. Arsenic and selenium concentrations in females were higher than in males. Sex-related differences in the concentration of these elements may be related to unknown slight differences in diet or to differences in assimilation between sexes. 5. Bulwer's petrels Bulweria bulwerii (highly specialised avian predators of mesopelagic prey) were used as biomonitors of mercury levels in the mesopelagic domain of the Pacific and Atlantic oceans in Chapter 6. Atlantic colonies showed higher mercury concentrations than those from the Pacific. CSIA-AA-derived trophic levels for chicks were similar among colonies, suggesting that differences between locations were not due to differences in the trophic level of those populations. Feather mercury levels recorded were lower than those reported in 1992 for the Atlantic. 6. Possible adverse effects of mercury in chicks of Bulwer’s petrels Bulweria bulwerii were evaluated in Chapter 7. Chick growth rate was negatively correlated to mercury contamination. Chicks with reduced growth rate coefficients for body mass exhibited retarded growth of wing length. High mercury concentrations were associated with delayed fledging in Bulwer’s petrel Bulweria bulwerii chicks. The behaviour of chicks in the nest was not influenced by mercury levels. 7. Bulwer’s petrel have some of the highest reported blood mercury concentrations amongst seabirds. We measured mercury in the blood of individual adult Bulwer’s petrel and assessed their foraging performance. There was no relationship between mercury contamination and foraging performance, as measured through foraging trip duration and daily mass gain during a foraging trip. Bulwer’s petrels Bulweria bulwerii seem to be highly resilient to mercury contamination. The results of this thesis provide a reference line for bioindication studies using feathers and blood from selected seabird species on the Atlantic and Pacific Ocean. Despite the exceptionally high levels of mercury accumulated by seabirds, their behaviour seems largely unaffected by mercury concentrations across the range measured here
Description
Thesis presented in fulfilment of the degree of
PhD in Behavioural Biology, presented at
Ispa - Instituto Universitário in the year of
Keywords
Comportamento alimentar Comportamento no ninho Mercúrio Oligoelementos Aves marinhas Oceano Biomonitorização Nível trófico Aptidão física Foraging behaviour Behaviour in the nest Mercury Trace elements Seabirds Ocean Biomonitoring Trophic level Fitness