Migrating birds rapidly increase constitutive immune function during stopover

Eikenaar, Cas; Hessler, Sven; Hegemann, Arne

doi:10.1098/rsos.192031

Cited by 27 publications

(34 citation statements)

References 55 publications

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“…Additionally, we found SESA that refuelled at RWR had faster northbound migrations of greater than 50 km/day, which is an important indicator of fitness in migrants and suggests that SESA were able to get fatter at RWR compared to GI (Bayly et al, 2016; Gómez et al, 2017; Lindström et al, 2019; Pomeroy et al, 2008; Sjöberg et al, 2015; Warnock, 2010). Although GI potentially had fewer foraging opportunities for SESA, it still provided necessary resting habitat after crossing the GOM allowing individuals to physiologically recover, which is likely true for other barrier islands (Curtiss & Pierce, 2016; Eikenaar, Hessler, & Hegemann, 2020; Eikenaar, Winslott, et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Migration tactics and connectivity of a Nearctic–Neotropical migratory shorebird

Herbert

Mizrahi

Taylor

2022

Journal of Animal Ecology

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During long‐distance spring migrations, birds may rest and refuel at numerous stopover sites while minimizing the time to reach the breeding grounds. If habitat is limited along the migration route, pre‐breeding birds optimize flight range by having longer stopovers at higher quality sites compared to poorer quality sites. Stopover duration also depends on distance remaining to breeding grounds, ecological barriers and individual characteristics. We assessed spring migration tactics and connectivity of a Nearctic–Neotropical migratory shorebird, the semipalmated sandpiper Calidris pusilla, at two sites with known relative habitat quality on the northern Gulf of Mexico (NGOM) coast, the first land encountered after crossing the Gulf of Mexico (GOM). We used automated radio telemetry (Motus) to estimate stopover duration and probability of departure. Migration speed was estimated for individuals detected at subsequent receivers on the Motus network. To measure migratory connectivity, we used morphometrics and the Motus network to assign general breeding regions. Additionally, feather stable isotope ratios of C and N provided coarse information about overwintering regions. Stopover duration declined with higher fuel loads at capture as expected under a time‐minimizing strategy. After accounting for fuel load, stopover duration was approximately 40% longer at the higher quality site. We found no detectable effect of age, sex or breeding location on stopover behaviour. The probability of departure was strongly affected by humidity and also by tailwind and weather conditions. Birds stopping at the higher quality site had earlier apparent arrival to the breeding grounds. The Louisiana coast is an apparent stopover hub for this species, since the individuals were departing to range‐wide breeding regions and isotope values suggested birds were also using widespread wintering regions. Our study shows how high‐quality, coastal wetlands along the NGOM coast serve a critical role in the annual cycle of a migratory shorebird. Stopover behaviour indicated that high‐quality habitat may be limited for this species during spring migration. As threats to the GOM coast increase, protection of these already limited wetlands is vitally important.

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Section: Discussionmentioning

confidence: 99%

Migration tactics and connectivity of a Nearctic–Neotropical migratory shorebird

Herbert

Mizrahi

Taylor

2022

Journal of Animal Ecology

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“…Eikenaar, Isaksson & Hegemann (2018) provided data that support the presence of a physiological trade-off during stopover in migratory common blackbirds (Turdus merula Linnaeus). In these birds, microbial killing capacity (a constitutive immune function) was negatively correlated with non-enzymatic antioxidant capacity and positively associated with oxidative damage to lipids, whereas these correlations were absent in resident conspecifics sampled at the same location and time (Eikenaar et al, 2018). This suggests that migrants during stopover may trade off recovery of oxidative balance against recovery of constitutive immune function.…”

Section: (F) Trade-offs In the Recovery Of Physiological Functionsmentioning

confidence: 92%

“…That an organism needs to rest and recover physiologically after a period of endurance exercise seems a plausible explanation for stopping over. However, what exactly is meant by ‘rest and recovery’ is often not clearly defined (but see Biebach, 1998; Karasov & Pinshow, 1998; Guglielmo, Piersma & Williams, 2001; Schwilch et al ., 2002b; Aborn & Moore, 2004; Skrip et al ., 2015; Ferretti et al ., 2019), and actual evidence for specific recovery processes is still scarce (Skrip et al ., 2015; Eikenaar, Hessler & Hegemann, 2020b; Eikenaar et al ., 2020c). Here we present several physiological processes and systems on which migratory endurance flight can have an adverse effect with potential fitness costs, from which the bird may need to recover during stopover.…”

Section: The Multiple Functions Of Stopovermentioning

confidence: 99%

“…Red knots ( Calidris canutus rufa Linnaeus) that were in protein recovery, and hence presumably had recently interrupted their endurance flight, had lower constitutive immune function than conspecifics that were storing fat and thus presumed present for a longer time at stopover (Buehler, Tieleman & Piersma, 2010). These cross‐sectional results were later supported by a longitudinal study showing improved constitutive immune function in northern wheatears temporarily caged at stopover, indicating a recovery from lower levels during flights (Eikenaar et al ., 2020b).…”

Section: The Multiple Functions Of Stopovermentioning

confidence: 99%

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Understanding the ecological and evolutionary function of stopover in migrating birds

2022

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Global movement patterns of migratory birds illustrate their fascinating physical and physiological abilities to cross continents and oceans. During their voyages, most birds land multiple times to make so-called 'stopovers'. Our current knowledge on the functions of stopover is mainly based on the proximate study of departure decisions. However, such studies are insufficient to gauge fully the ecological and evolutionary functions of stopover. If we study how a focal trait, e.g. changes in energy stores, affects the decision to depart from a stopover without considering the trait(s) that actually caused the bird to land, e.g. unfavourable environmental conditions for flight, we misinterpret the function of the stopover. It is thus important to realise and acknowledge that stopovers have many different functions, and that not every migrant has the same (set of) reasons to stop-over. Additionally, we may obtain contradictory results because the significance of different traits to a migrant is context dependent. For instance, late spring migrants may be more prone to risktaking and depart from a stopover with lower energy stores than early spring migrants. Thus, we neglect that departure decisions are subject to selection to minimise immediate (mortality risk) and/or delayed (low future reproductive output) fitness costs. To alleviate these issues, we first define stopover as an interruption of migratory endurance flight to minimise immediate and/or delayed fitness costs. Second, we review all probable functions of stopover, which include accumulating energy, various forms of physiological recovery and avoiding adverse environmental conditions for flight, and list potential other functions that are less well studied, such as minimising predation, recovery from physical exhaustion and spatiotemporal adjustments to migration. Third, derived from these aspects, we argue for a paradigm shift in stopover ecology research. This includes focusing on why an individual interrupts its migratory flight, which is more likely to identify the individualspecific function(s) of the stopover correctly than departure-decision studies. Moreover, we highlight that the selective forces acting on stopover decisions are context dependent and are expected to differ between, e.g. K−/r-selected species, the sexes and migration strategies. For example, all else being equal, r-selected species (low survival rate, high reproductive rate) should have a stronger urge to continue the migratory endurance flight or resume migration from a stopover because the potential increase in immediate fitness costs suffered from a flight is offset by the expected higher reproductive success in the subsequent breeding season. Finally, we propose to focus less on proximate mechanisms controlling landing and departure decisions, and more on ultimate mechanisms to identify the selective forces shaping stopover decisions. Our ideas are not limited to birds but can be applied to any migratory species. Our revised definition of stopover and the proposed paradigm shi...

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“…Hegemann et al., 2012; Owen & Moore, 2006), evidence for rapid (within days or weeks) changes in these traits is scarce in wild birds (e.g. Eikenaar et al., 2020). Research on experimentally infected birds shows that IgY response usually starts to develop ca.…”

Section: Discussionmentioning

confidence: 99%

Immunocompetent birds choose larger breeding colonies

Drzewińska‐Chańko

Włodarczyk

Gajewski

et al. 2021

Journal of Animal Ecology

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1. Optimal size of social groups may vary between individuals, depending on their phenotypic traits, such as dominance status, age or personality. Larger social groups often enhance transmission rates of pathogens and should be avoided by individuals with poor immune defences. In contrast, more immunocompetent individuals are expected to take advantage of larger group sizes (e.g. better protection, information transfer) with smaller extra costs from pathogen or parasite pressure.2. Here, we hypothesized that immunocompetence may be a key determinant of group size choice and tested this hypothesis in a colonial waterbird, the common tern Sterna hirundo. We used a unique experimental framework, where formation of breeding colonies of different sizes was induced under uniform environmental conditions. For this purpose, different-size patches of attractive nesting substrate (artificial floating rafts) were provided at a single site with limited availability of natural nesting habitat.3. Colony size was identified as the only significant predictor of both innate (natural antibody-mediated complement activation) and adaptive (immunoglobulin concentrations) immunological traits in the common terns, as more immunocompetent birds settled in larger experimental colonies. In contrast, we found no significant associations between colony size and genetic diversity of key pathogenrecognition receptors, toll-like receptors (TLRs) and the Major Histocompatibility Complex (MHC) or genome-wide heterozygosity.4. We conclude that settlement decisions may be flexible within individuals and, thus, are likely to be primarily determined by the current immunological status, rather than fixed immunogenetic traits. Our study sheds new light on the complex interface between immunity and sociality in animals.

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Migrating birds rapidly increase constitutive immune function during stopover

Cited by 27 publications

References 55 publications

Migration tactics and connectivity of a Nearctic–Neotropical migratory shorebird

Migration tactics and connectivity of a Nearctic–Neotropical migratory shorebird

Understanding the ecological and evolutionary function of stopover in migrating birds

Immunocompetent birds choose larger breeding colonies

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