ECR feature: Letícia Soares on migratory birds and their pathogens

Letícia Soares is a postdoc at the Advanced Facility for Avian Research, University of Western Ontario, and is interested in disease ecology and evolution. In her recently published paper in Journal of Biogeography, Letícia studied the malarial parasites in North American migratory bird species in their Hispaniola over-wintering range. She shares her findings from her temporally stratified collections and the differences between migrant and co-occurring resident bird species.

Letícia during field work in Bruce Peninsula (Canada), working on yellow-rumped warblers during their fall migration.

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Institute. Advanced Facility for Avian Research, University of Western Ontario

Academic life stage. Postdoc

Major research themes. Disease Ecology & Evolution, Biogeography

Current study system. Most of my current research focuses on determining the drivers of geographical and temporal variation in the occurrence of malarial parasites in birds (order Haemosporida). In birds, malarial parasites have a relevant regulatory role in populations, as infections can reduce the reproductive success, life span, and survival of hosts. Moreover, bird malaria is biologically similar and evolutionary related to human malaria, making this the perfect study system to understand the ecology and evolution of malaria parasites in natural populations.

Recent paper in Journal of Biogeography. Soares L., Latta S. and Ricklefs R. (2020) Neotropical migratory and resident birds occurring in sympatry during winter have distinct haemosporidian parasite assemblages. Journal of Biogeography, 47(3):748–759.

Motivation behind this research. Neotropical migratory birds have a life history strategy that most would envy: they spend their summers breeding in North America, and when days become shorter and food supplies start to diminish, they make their way southwards to their wintering grounds, where migrants will spend up to five months co-occurring with year-round resident bird species. Most migratory birds are infected with malarial parasites prior to travelling to wintering areas, but we do not know the effects of these parasites on host survival during North Hemisphere winters. We additionally have very little understanding of the fate of parasitic infections during wintering. For migratory birds, infections likely confer negative effects that can carry over to future breeding and migratory seasons. Hence, we wanted to quantify how often birds that reside year-round in the Tropics exchange parasite strains with migratory birds. We also wanted to assess the potential of migratory birds as vehicles for parasite dispersal across large geographical scales. For example, picture a Cape May warbler during the breeding season in Maine, USA: this bird gets bit by a mosquito that transmits a malarial strain to it. When this bird travels to Hispaniola for the winter, it will co-occur with birds that reside there year-round. If this particular Cape May warbler brings this North American malarial strain to Hispaniola, it has the potential of transmitting that parasite to local resident species via mosquito vectors. 

Two common migratory species caught while mistnetting in the Caribbean. (left) Cape May Warbler. (right) Black and White Warbler.

Methodology. Consistent sampling was important in collecting high quality data. This was only possible thanks to Dr. Steven Latta and collaborators in the Dominican Republic. Capturing, banding, and taking blood samples from birds in remote areas is no easy task and always deserves to be acknowledged and appreciated. It was a game changer to be able to demonstrate that migratory birds are rarely detected with infections across multiple years, even on years of high prevalence among resident species. Before this study, we worked with resident bird species in more than 20 islands of the West Indies, demonstrating that infection prevalence exhibits dynamic fluctuations on short time frames (2–3 years). Thus, our sampling allowed us to demonstrate that even though migratory and resident birds might face similar ecological conditions in Hispaniola, migrant populations seem refractory to what happens to resident populations, at least when it comes to malarial parasites.

Unexpected outcomes. Our data show a very strong and multi-year pattern of low prevalence of malarial infections among migratory birds, even in years when co-occurring populations of resident birds have infection prevalence as high as 78%. My a priori expectation was that migratory birds would be found infected with parasite lineages that commonly occur in the wintering grounds, which was not the case. Elaborating biologically meaningful hypotheses to explain these findings was quite challenging, given that very little is known about the winter ecology of malarial parasites in migratory and resident bird populations, and the information on vector biology for this system is also scarce.

Major results. We have demonstrated that during midwinter on Hispaniola, populations of 14 over-wintering migratory bird species are rarely infected with malarial parasites. In all five sampled years (2001, 2002, 2014, 2015, and 2017), we found that, on average, 27% of 1,780 resident birds were infected with malarial parasites, but infections were detected in only 2.8% of 901 over-wintering migratory individuals. While previous studies provided the valuable insight that parasite dispersal by migratory birds is limited, they were focused on determining the prevalence of infections at breeding, migration stop-over and wintering areas of single species of migratory birds. Hence, prior studies lacked multi-year sampling and data on other resident bird species that co-occur with these migrants during different phases of their life-cycles. What makes our study stand out is that we expanded sampling from populations to communities to focused on assemblages of migratory and resident birds occurring in sympatry during North Hemisphere winters, with considerable temporal replication. We inferred that malarial parasite seldom use migratory birds as vehicles for dispersal, and that migratory birds rarely exchange parasite strains with resident birds of Hispaniola.

(left) Broad billed tody, a Hispaniola endemic species. (right) Haemosporidian parasites have complex life cycles. Within the vertebrate hosts, these parasites replicate clonally and produce transmission stages (highlighted by the arrows) that infect red blood cells.

Next steps. Like human malarial parasites, bird malarial parasites are transmitted by blood-feeding insects. To fully understand what determines the ability of a vector-transmitted parasite to disperse and establish transmission cycles in a novel geographic region, we need to describe the communities of insects that prefer to feed on bird blood, and determine whether these blood feeding insects are suitable vectors for the parasites. Diminished vector populations during North Hemisphere winters is among the hypotheses we proposed to explain the low frequency of parasite exchange between resident and migratory birds. We also tend to intuitively think of blood-feeding insects as being opportunistic feeders, when in reality many do present feeding preferences. Thus, we cannot rule out the possibility that insect vectors in Hispaniola are not suitable vectors for North American parasite strains, or that these insects are just not fond of drinking blood from migratory birds.  

If you study any organism on Earth, what would it be and why? I would love to study bird species that seem refractory to commonly occurring parasites. For example, malaria parasites have been found infecting most bird species that have been sampled, with the exception of shorebirds.  Why shorebirds are rarely detected with malaria infections is not understood, but it is possible that shorebirds are incompatible hosts for these parasites. Most shorebirds that breed at high latitudes in the Northern Hemisphere undertake long-distance migration to wintering areas in South America. Infections likely increase the costs of migration, and, over time, natural selection would have favored individuals with effective immune response against infections that increase the costs and affect the energetic budget of migration. Understanding the mechanisms regulating disease susceptibility and resistance in birds can inform research into human malaria, as many strategies of host exploitation by the parasite and immune response by the host are similar across the avian and mammalian malaria parasite systems.

Anything else you would like to share? In my capacity as a postdoc at the University of Western Ontario, I am experimentally determining the effects of malaria parasites on the migratory performance of yellow-rumped warblers. I am using experimental infection and simulated migration in a wind tunnel to determine whether malaria parasites affect migratory flight performance by integrating metrics of flight behavior, infection intensity, and costs of infection with a direct association to host longevity and physiology. The results from this experiment could help us explain the low prevalence of malaria infections in migratory birds during wintering. Migration is physiologically strenuous for the birds, and we hypothesize that oxidative stress resulting from endurance exercise during migration could have a negative effect on within-host parasite survival.

Published by jbiogeography

Contributing to the growth and societal relevance of the discipline of biogeography through dissemination of biogeographical research.

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