| 1. |
- Eikenaar, Cas, et al.
(författare)
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A hidden cost of migration? Innate immune function versus antioxidant defense
- 2018
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Ingår i: Ecology and Evolution. - : Wiley. - 2045-7758. ; 8:5, s. 2721-2728
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Tidskriftsartikel (refereegranskat)abstract
- Migration is energetically demanding and physiologically challenging. Migrating birds, for example, need to boost their antioxidant defenses to defeat the pro-oxidants produced during high energetic activity. The enhanced antioxidant defense possibly withdraws limited resources (e.g., energy or micronutrients) from other physiological functions, such as immune defense. Such a trade-off might not occur outside the migration seasons or in resident individuals. Here, we investigate whether there is a negative relationship between innate immune function and antioxidant defense by sampling both migrating and resident blackbirds (Turdus merula) at the same location during the same period of the annual cycle. We show that in migrating blackbirds microbial killing capacity (BKA), an integrative measure of baseline innate immune function was negatively correlated with total nonenzymatic antioxidant capacity. In contrast, in resident conspecifics, sampled at the same time and location, these two physiological measures were not correlated. This suggests that migrating birds trade off innate immune function and antioxidant defense. Furthermore, and likely a consequence of this trade-off, in migrant blackbirds BKA was positively correlated with oxidative damage to lipids. In resident blackbirds BKA and degree of lipid oxidation were uncorrelated. The mechanism and currencies of the supposed trade-off are currently unknown, but energetic investments or micronutrients are likely candidates. Future experimental studies could provide more conclusive evidence for this trade-off; yet, our results open up a new level of thinking about the physiological costs of migration.
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| 2. |
- Eikenaar, Cas, et al.
(författare)
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Can differential fatty acid composition help migrating birds to limit oxidative lipid damage?
- 2022
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Ingår i: Physiology and Behavior. - : Elsevier BV. - 0031-9384. ; 249
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Tidskriftsartikel (refereegranskat)abstract
- During migratory endurance flights, which are energetically very demanding, migrants have to deal with prolonged elevated generation of reactive oxygen species (ROS). To limit the damaging actions that ROS have on lipids and proteins, migrating birds are known to upregulate their antioxidant defence system. However, there may be additional ways to limit oxidative damage incurred from flying. Migratory endurance flights are fuelled mainly with fatty acids (FAs), and the risk of their peroxidation (resulting in oxidative lipid damage) increases with the number of double bonds in a FA, with polyunsaturated FAs (2 or more double bonds, PUFAs) being most peroxidation-prone. By fuelling their flights with relatively few PUFAs, migratory birds could thus limit oxidative lipid damage. Within migratory birds, there is considerable variation in the length of their flights, with nocturnal migrants making lengthier flight bouts, thus more likely to experience lengthier periods of elevated ROS production, than diurnal migrants. However, whether migrants making lengthier flights incur more oxidative lipid damage is unknown. Neither is it known whether flight length and FA composition are associated. Therefore, we determined plasmatic malondialdehyde level, a marker of oxidative lipid damage, and FA composition of three nocturnal and two diurnal migrant species caught at an autumn stopover site. We found little inter-specific variation in malondialdehyde level, indicating that the amount of oxidative lipid damage was comparable across the species. In contrast, the species strongly differed in their plasmatic FA composition. The nocturnal migrants had significantly lower relative PUFA levels than both diurnal migrants, an effect mainly attributable to linoleic acid, an essential (strictly dietary) FA. Consequently, the susceptibility of plasmatic FAs to lipid peroxidation was significantly lower in the nocturnal than diurnal migrants. Because in birds, energy expenditure during flight decreases with the degree of FA unsaturation, we interpret our observation of lower PUFA levels in nocturnal migrants as support for the idea that utilizing PUFA-poor fuel can help migrating birds to curb oxidative lipid damage.
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| 3. |
- Eikenaar, Cas, et al.
(författare)
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Migrating birds rapidly increase constitutive immune function during stopover
- 2020
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Ingår i: Royal Society Open Science. - : The Royal Society. - 2054-5703. ; 7:2
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Tidskriftsartikel (refereegranskat)abstract
- Migratory flight is physiologically highly demanding and has been shown to negatively affect multiple parameters of constitutive immune function (CIF), an animal’s first line of physiological defence against infections. In between migratory flights, most birds make stopovers, periods during which they accumulate fuel for the next flight(s). Stopovers are also commonly thought of as periods of rest and recovery, but what this encompasses is largely undefined. Here, we show that during stopover, northern wheatears Oenanthe oenanthe, a long-distance migratory bird, can rapidly increase constitutive innate immune function. We caught and temporarily caged birds under ad libitum food conditions at a stopover site in autumn. Within 2 days, most birds significantly increased complement activity and their ability to kill microbes. Changes in immune function were not related to the birds’ food intake or extent of fuel accumulation. Our study suggests that stopovers may not only be important to refuel but also to restore immune function. Additionally, the increase in CIF could help migrating birds to deal with novel pathogens they may encounter at stopover sites.
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| 4. |
- Eikenaar, Cas, et al.
(författare)
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Migratory common blackbirds have lower innate immune function during autumn migration than resident conspecifics
- 2016
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Ingår i: Biology letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 12
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Tidskriftsartikel (refereegranskat)abstract
- Animals need awell-functioning immune systemto protect themselves againstpathogens. The immune system, however, is costlyand resource trade-offs withother demands exist. For migratory animals several (not mutually exclusive)hypotheses exist. First, migrants reduce immune function to be able to allocateresources to migration. Second, migrants boost immune function to cope withmore and/or novel pathogens encountered during migration. Third, migrantsreallocate resources within the immune system.We tested these hypotheses bycomparing baseline immune function in resident and migratory commonblackbirds (Turdus merula), both caught during the autumn migration seasonon the island of Helgoland, Germany. Indices of baseline innate immune function(microbial killing capacity and haptoglobin-like activity) were lower inmigrants than in residents. There was no difference between the groups intotal immunoglobulins, a measure of baseline acquired immune function.Our study on a short-distance avian migrant supports the hypothesis thatinnate immune function is compromised during migration.
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| 5. |
- Eikenaar, Cas, et al.
(författare)
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Migratory refueling affects non-enzymatic antioxidant capacity, but does not increase lipid peroxidation.
- 2016
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Ingår i: Physiology & Behavior. - : Elsevier BV. - 1873-507X .- 0031-9384. ; 158, s. 26-32
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Tidskriftsartikel (refereegranskat)abstract
- All aerobic organisms are to some degree affected by oxidative stress, which is an imbalance between pro-oxidants and antioxidants in favor of the former. Pro-oxidants can damage DNA, proteins and lipids, and as such oxidative stress can carry considerably fitness costs. In mammals excessive calorie intake is a known cause of oxidative stress. We investigated whether in migrant birds, which typically engage in over-eating in between flights (refueling), high food intake causes oxidative stress. In an experiment we compared levels of plasmatic total non-enzymatic antioxidant capacity (AOX) and oxidative damage (lipid peroxidation) between migrants repeatedly fasted and refed (simulating the flight-refuel cycle of wild migrants), and migrants on ad libitum food. We found that refueling increased AOX, an effect mainly attributable to an increase in uric acid level, an antioxidant that is produced during protein metabolism. Accordingly, variation in AOX was mainly explained by the refueling birds' food intake. However, food intake in migrants on ad libitum food did not explain any variation in AOX. Refueling did not affect lipid peroxidation, nor were its levels explained by food intake. We propose that over-eating migrants retain uric acid, which might be a very low cost mechanism to forego oxidative damage.
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| 6. |
- Eikenaar, Cas, et al.
(författare)
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Not just fuel : energy stores are correlated with immune function and oxidative damage in a long-distance migrant.
- 2019
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Ingår i: Current Zoology. - : Oxford University Press (OUP). - 1674-5507 .- 2396-9814.
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Tidskriftsartikel (refereegranskat)abstract
- In many animals, catabolic and anabolic periods are temporally separated. Migratory birds alternate energy expenditure during flight with energy accumulation during stopover. The size of the energy stores at stopover affects the decision to resume migration and thus the temporal organization of migration. We now provide data suggesting that it is not only the size of the energy stores per se that may influence migration scheduling, but also the physiological consequences of flying. In two subspecies of the northern wheatearOenanthe oenanthe, a long-distance migrant, estimated energy stores at a stopover during autumn migration were positively related with bothconstitutive innate and acquired immune function, and negatively related with oxidative damage to lipids. In other words, migrants’ physiological condition was associated with their energetic condition. Although time spent at stopover before sampling may have contributed to this relationship, our results suggest that migrants have to trade-off the depletion of energy stores during flight withincurring physiological costs. This will affect migrants’ decisions when to start and when to terminate a migratory flight. The physiological costs associated with the depletion of energy stores may also help explaining why migrants often arrive at and depart from stopover sites with larger energy stores than expected. We propose that studies on the role of energy stores as drivers of the temporal organization of (avian) migration need to consider physiological condition, such as immunological and oxidative states.
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| 7. |
- Eikenaar, Cas, et al.
(författare)
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Oxidative challenges of avian migration : A comparative field study on a partial migrant
- 2017
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Ingår i: Physiological and Biochemical Zoology. - : University of Chicago Press. - 1522-2152 .- 1537-5293. ; 90:2, s. 223-229
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Tidskriftsartikel (refereegranskat)abstract
- Most avian migrants alternate flight bouts, characterized by high metabolic rates, with stopovers, periods of fuel replenishment through hyperphagia. High-energy metabolism and excessive calorie intake shift the balance between damaging prooxidants and antioxidants toward the former. Hence, migration likely affects the oxidative balance of birds. Migratory flight indeed appears to cause oxidative damage; however, whether migration affects the oxidative state of birds at stopover is unclear. Therefore, we compared total nonenzymatic antioxidant capacity (AOX) and malondialdehyde concentration (MDA; a measure of lipid peroxi-dation) in the plasma of migrant and resident common blackbirds. We also determined plasmatic uric acid (UA) and fatty acid (FA) concentrations and calculated a FA peroxidation index. Birds were sampled during autumn migration at a stopover site that also supports a sedentary blackbird population. Migrants had higher AOX than residents, also after correcting for UA concentration. Migrants tended to have higher FA peroxidation indexes than residents, indicating that the energy source of migrants contains higher concentrations of peroxidizable FAs. However, the two groups did not differ in MDA concentration, also not after correcting for peroxidation index. Peroxidation-corrected MDA concentration was negatively correlated with UA-corrected AOX. In other words, individuals with low nonenzymatic AOX suffered more from lipid peroxidation than individuals with high nonenzymatic AOX. These results together indicate that migrant blackbirds invest in antioxidant defenses to reduce oxidative damage to lipids, likely representing an adaptation to diminish the physiological costs of migration.
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| 8. |
- Eikenaar, Cas, et al.
(författare)
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Oxidative damage to lipids is rapidly reduced during migratory stopovers
- 2020
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Ingår i: Functional Ecology. - : Wiley. - 0269-8463 .- 1365-2435. ; 34:6, s. 1215-1222
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Tidskriftsartikel (refereegranskat)abstract
- Most migrating birds need to stopover in between flights in order to refuel. Lately, additional purposes of stopover have been suggested, including physiological recovery from metabolically demanding migratory flight. One apparently unavoidable, but harmful physiological effect of migratory flight is increased oxidative damage to lipids and proteins. We here, for the first time, tested whether migrating birds are able to reduce their oxidative damage during stopover. To be able to collect longitudinal data on a large number of individual birds, we temporarily caged wild northern wheatears, a long-distance migrant which does not suffer stress when caged during migration. Around noon on the first and third day at stopover, the birds were blood-sampled to determine malondialdehyde (MDA) concentration, a commonly used marker of oxidative damage to lipids. We found that MDA concentrations significantly decreased during stopover, a result unchanged when correcting for the peroxidizability of the substrate. The extent of the decrease was unrelated to the amounts of food consumed or of fuel accumulated. Our findings support the hypothesis that stopovers serve reduction of oxidative damage, warranting re-thinking of how birds accomplish their migrations. They also highlight the need to include physiological recovery as a driver of the (temporal) organization of migration. A free Plain Language Summary can be found within the Supporting Information of this article.
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| 9. |
- Eikenaar, Cas, et al.
(författare)
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Recovery of constitutive immune function after migratory endurance flight in free-living birds
- 2023
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Ingår i: Biology letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 19:2
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Tidskriftsartikel (refereegranskat)abstract
- Strenuous physical activity can negatively affect constitutive innate immune function (CIF), the always present first line of defence against pathogens. CIF is non-specific, and thus vital when encountering novel pathogens. A lowered CIF likely increases the risk of infection and disease. Migratory birds engage in truly extreme physical activity during their endurance flights, however, little is known about how they deal with the negative impact this has on their immune function. By collecting both between- and within-individual data we show, for the first time, that free-flying migratory birds can recover several parameters of CIF during stopovers, which are stationary periods in between migratory flights. With this, we provide an important piece of the puzzle on how migrating birds cope with the physiological challenges they face on their biannual journeys. Furthermore, our study stresses the importance of migratory stopovers beyond fuel accumulation.
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| 10. |
- Eikenaar, Cas, et al.
(författare)
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Stopover departure decisions in autumn are not associated with constitutive immune function in Northern Wheatears Oenanthe oenanthe
- 2019
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Ingår i: Journal of Ornithology. - : Springer Science and Business Media LLC. - 2193-7192 .- 2193-7206. ; 160:3, s. 813-817
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Tidskriftsartikel (refereegranskat)abstract
- Stopover periods in between migratory flights determine the speed of migration and as such may affect birds’ fitness. The decision to leave a stopover site is affected by, for example, energy stores and weather conditions. We investigated whether immunological state influences autumn stopover departure decisions in Northern Wheatear (Oenanthe oenanthe), a nocturnal long-distance migrant. We measured three parameters of constitutive immune function: microbial killing capacity, haptoglobin, and total immunoglobulins. None of them explained variation in departure probability, minimum stopover duration, or departure time within the night. Thus, we did not find an effect of the birds’ immunological state on stopover departure decisions.
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| 11. |
- Eikenaar, Cas, et al.
(författare)
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Stopovers Serve Physiological Recovery in Migratory Songbirds
- 2023
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Ingår i: Physiological and Biochemical Zoology. - 1522-2152. ; 96:5, s. 378-389
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Tidskriftsartikel (refereegranskat)abstract
- Migrating birds perform extreme endurance exercise when fly-ing. This shifts the balance between the production of reactive oxygen species and the antioxidant defense system toward the former, potentially generating oxidative damages. In between migratory flights, birds make stopovers, where besides accumulat-ing fuel (mainly fats), they are assumed to rest and recover from the strenuous flight. We performed a series of studies on both temporarily caged (northern wheatears) and free-flying (northern wheatears and European robins) migrants to investigate whether migrants recover during stopover by decreasing the amount of oxidative lipid damage (malondialdehyde [MDA]) and/or increasing the total nonenzymatic antioxidant capacity (AOX). In caged wheatears, MDA decreased within a single day. These birds were able to simultaneously accumulate considerable amounts of fuel. Also, in the free-flying wheatears, there was a decrease in MDA during stopover; however, this process seemed incompatible with refueling. The reason for this difference could relate to constraints in the wild that are absent in caged birds, such as food limitation/ composition and locomotor activity. In the robins, there was a near significant decrease in MDA concentration in relation to how long the birds were already at stopover, suggesting that this species also physiologically recovers during stopover. AOX did not change during stopover in either of the wheatear studies. For the robins, however, uric acid–corrected AOX declined during stopover. Our results show that during stopover, migrating birds rapidly reduce oxidative lipid damage, thereby likely recovering their physiological state. In addition to the commonly accepted function of refueling, stopovers thus probably serve physiological recovery.
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| 12. |
- Eikenaar, Cas, et al.
(författare)
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The oxidative balance and stopover departure decisions in a medium- and a long-distance migrant
- 2023
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Ingår i: Movement Ecology. - : Springer Science and Business Media LLC. - 2051-3933. ; 11
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Tidskriftsartikel (refereegranskat)abstract
- Background: Birds have extremely elevated metabolic rates during migratory endurance flight and consequently can become physiologically exhausted. One feature of exhaustion is oxidative damage, which occurs when the antioxidant defense system is overwhelmed by the production of damaging reactive oxygen species (ROS). Migrating birds have been shown to decrease the amount of oxidative lipid damage during stopovers, relatively stationary periods in between migratory flights. It has therefore been argued that, in addition to accumulating fuel, one of the functions of stopover is to restore the oxidative balance. If this is so, we would expect that migrating birds are unlikely to resume migration from stopover when they still have high amounts of lipid damage. Methods: To test this hypothesis, we measured parameters of the oxidative balance and related these to stopover departure decisions of song thrushes (Turdus philomelos) and northern wheatears (Oenanthe oenanthe), a medium- and long-distance songbird migrant, respectively. We measured malondialdehyde (MDA) concentration, a biomarker for oxidative lipid damage, and total non-enzymatic antioxidant capacity (AOX), an overall biomarker of protection against ROS. Stopover departure decisions were determined using a fully automated telemetry system set-up on our small island study site. Results: The decision to resume migration was not related with MDA concentration in either study species, also not when this was corrected for circulating fatty acid concentrations. Similarly, AOX did not affect this decision, also not when corrected for uric-acid concentration. The time within the night when birds departed also was not affected by MDA concentration or AOX. However, confirming earlier observations, we found that in both species, fat individuals were more likely to depart than lean individuals, and fat northern wheatears departed earlier within the night than lean conspecifics. Northern wheatears additionally departed earlier in spring with more southerly winds. Conclusions: We found no support for the idea that stopovers departure decisions are influenced by parameters of the oxidative balance. We discuss possible reasons for this unexpected finding.
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| 13. |
- Jensen, Johan Kjellberg, et al.
(författare)
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Migrant blackbirds, Turdus merula, have higher plasma levels of polyunsaturated fatty acids compared to residents, but not enhanced fatty acid unsaturation index
- 2020
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Ingår i: Ecology and Evolution. - : Wiley. - 2045-7758. ; 10:18, s. 10196-10206
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Tidskriftsartikel (refereegranskat)abstract
- Birds have been observed to have dietary preferences for unsaturated fatty acids during migration. Polyunsaturated fatty acids (PUFAs) may increase the exercise performance of migrant birds; however, PUFAs are also peroxidation prone and might therefore incur increased costs in terms of enhanced oxidative damage in migratory individuals. To shed light on this potential constraint, we analyzed plasma fatty acid (FA) composition and estimated the unsaturation index as a proxy for susceptibility to lipid peroxidation of migrants and residents of the partially migratory common blackbird (Turdus merula) at a stopover site during autumn migration. As predicted, migrant birds had higher relative and absolute levels of PUFAs compared to resident birds. This included the strictly dietary ?-3 PUFA a-linolenic acid, suggesting a dietary and/or storage preference for these FAs in migrants. Interestingly, the FA unsaturation index did not differ between migrants and residents. These findings suggest a mechanism where birds alter their levels of metabolic substrate without simultaneously increasing the susceptibility of the substrate to lipid peroxidation. In summary, our results are in line with the hypothesis that increased exercise performance during migration might be constrained by oxidative stress, which is manifested in changes in the composition of key FAs to retain the unsaturation index constant despite the increased levels of peroxidizable PUFAs.
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