Unveiling the 'hidden' effects of subclinical infection - a movement ecology perspective

Parasitism is one of the most ubiquitous strategies across ecosystems. Yet, wildlife researchers often assume animals are healthy and performing optimally. In reality, many carry 'hidden' infections with masked symptoms that nevertheless affect movement capacity, potentially impacting host fitness.
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Parasites, by definition, deplete host resources, leaving hosts with fewer resources for fitness-enhancing activities. Based on this principle, we argued that, regardless of the mechanisms at play, host movement behaviour should serve as a reliable indicator of host performance, as behavioural changes are likely to occur first, before fitness losses become evident. To test this, we focused on a widespread group of parasites—avian blood parasites—which naturally occur at high prevalences in many passerine species. Avian blood parasites have complex life cycles, with an obligate two-host lifecycle (heteroxeneous), infecting the red blood cells of the host. During the acute phase, red blood cells are eventually destroyed, leading to reduced oxygen transport to muscles and organs - an ideal study system to explore physiological constraints of infection.

We utilised ultra-high-resolution tracking (ATLAS, with one localisation every 8 seconds) to monitor the local movement behaviour of barn swallows (Hirundo rustica) and house martins (Delichon urbicum) during the breeding season. Working in a resource-depleted landscape, where high-quality habitats are patchily distributed, we expected the feedbacks of parasites on foraging behaviour and resource selection to be particularly pronounced.

Atlas receiver set up in the Uckermark area close to a natural habitat patch that is embedded in the agricultural crop fields
Atlas receiver in the Uckermark area located at a natural habitat patch that is embedded in a crop field (photo: J. Pufelski)

We coupled our analyses with a structured capture-mark-recapture study,  monitoring the entire population across multiple breeding seasons. We systematically sampled blood and morphological measurements, revealing conclusive insights into the disease dynamics of the population. Across years, we observed considerable variation in parasite prevalence, ranging from 11% to 76% across three genera: Plasmodium, Haemoproteus, and Leucocytozoon. We used population models that allowed us to reliably assess the role of blood parasites in fitness proxies such as survival and body condition. 

Blood sampling of house martin (Delichon urbicum) (photo: E. Sánchez Arribas)

In short, infected individuals of both swallow species exhibited smaller activity ranges than their non-infected counterparts. By classifying behavioural states using high-resolution movement data, we demonstrated that infected birds rested more and foraged less. These combined effects led infected swallows to forage in habitat types generally lower in insect abundance. Specifically, infected birds, likely limited by physiological constraints, reduced foraging range and duration, and foraged on agricultural crop fields closer to their colony. In contrast, non-infected individuals showed a clear avoidance of these habitat types when foraging. On the population level, we found lower survival in infected individuals raising the question of whether this depletion is related to the reduced movement behaviour we observed in the infected individuals.

House martin (Delichon urbicum) equipped with lightweight ATLAS tag, recording localisations at second intervals (photo: Marie Klett)

In conclusion, subclinical infections can manifest in altered movement behaviour and researcher may detect such pathogen-induced alteration by studying them at appropriate spatiotemporal scales, aided by recent technological advancements. Although subtle, and traditionally often neglected, these behavioural effects may amplify over time or during energetically demanding life-history stages such as the breeding period, influencing population dynamics. Unlike previous studies focusing primarily on pathogen impacts on migration, we were able to establish direct links of behavioural alterations with potential fitness outcomes. We argue that pathogens should be more thoughtfully considered as key drivers of variation in individual movement behaviour. With global change potentially heightening the role of pathogens, the bi-directional relationship highlights the value of such analyses in future disease surveillance during outbreaks, as the movement behaviour does not only respond to infection but also facilitates pathogen transport.

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Ecology
Life Sciences > Biological Sciences > Ecology
Parasite Biology
Life Sciences > Biological Sciences > Microbiology > Parasitology > Parasite Biology

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