| 1. |
- Aastrup, Christian, et al.
(author)
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Jackdaw nestlings rapidly increase innate immune function during the nestling phase but no evidence for a trade-off with growth
- 2021
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In: Developmental and Comparative Immunology. - : Elsevier BV. - 0145-305X. ; 117
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Journal article (peer-reviewed)abstract
- Although animals are born with a protective immune system, even the innate immune system is under development from birth to adulthood and this development may be affected by sex and growth. However, most knowledge comes from captive animals or long-lived slow growing species. Moreover, little is known about how innate immune function, the important first line of defence, develops during early life in fast-growing animals such as free-living passerines. We studied development of innate baseline immune function in nestlings of free-living jackdaws Corvus monedula. We measured four immune parameters (hemolysis, hemagglutination, bacterial-killing capacity, haptoglobin concentration) and structural body size (body mass, wing length, tarsus length) at day 12 and day 29 post-hatching. We found that three out of four immune parameters (hemolysis, hemagglutination, bacterial-killing capacity) substantially increased with nestling age and had roughly reached adult levels shortly prior to fledging. We found little differences in immune development between males and females despite them differing in structural development. We also found no evidence that the nestlings traded off immune development with growth. That nestlings rapidly increase innate baseline immune function during early life and similarly in males and females indicates the importance of a well-functioning immune system already during the nestling phase.
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| 2. |
- Aastrup, Christian, et al.
(author)
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Size and immune function as predictors of predation risk in nestling and newly fledged jackdaws
- 2023
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In: Animal Behaviour. - : Elsevier BV. - 0003-3472. ; 198, s. 73-84
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Journal article (peer-reviewed)abstract
- Prey choice by predators may be based on the potential prey's condition, for example resulting in substandard individuals running a higher risk of being predated. Over 5 years, we studied young jackdaws, Corvus monedula, to determine whether size and innate baseline immune function may predict predation risk by goshawks, Accipiter gentilis, during the nestling and early fledging phases. We measured body mass, wing length, tarsus length and four innate immune indices two to four times when nestlings were 12–29 days old. To determine which individuals had been predated during the nestling phase and shortly after fledging, we searched for metal rings of the jackdaws in the only goshawk territory close to the jackdaw colony. Nestling mortality before 12 days of age was entirely due to starvation, whereas between 12 days of age and fledging, mortality was mainly due to predation. Nestlings with smaller size (mass, wing, tarsus) and low lysis titre and haptoglobin concentrations were at a higher risk of being predated before fledging. Directly after fledging, individuals with short wings were preferentially predated, with no effects of body mass, tarsus length or any of the four immune indices measured at day 29 (i.e. shortly before fledging). That lower immune function and smaller size predict predation risk in nestlings may reflect that these individuals are of poor quality and/or lag behind in development. We hypothesize that hunger makes these nestlings sit closest to the entrance hole and hence become the first to be predated. For fledglings, our results suggest that poor flight ability makes individuals with short wings the easiest targets for avian predators.
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| 3. |
- Andreasson, Fredrik, et al.
(author)
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Experimental facilitation of heat loss affects work rate and innate immune function in a breeding passerine bird
- 2020
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In: Journal of Experimental Biology. - : The Company of Biologists. - 1477-9145 .- 0022-0949. ; 223:8
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Journal article (peer-reviewed)abstract
- The capacity to get rid of excess heat produced during hard work is a possible constraint on parental effort during reproduction [heat dissipation limit (HDL) theory]. We released hard-working blue tits (Cyanistes caeruleus) from this constraint by experimentally removing ventral plumage. We then assessed whether this changed their reproductive effort (feeding rate and nestling size) and levels of self-maintenance (change in body mass and innate immune function). Feather-clipped females reduced the number of feeding visits and increased levels of constitutive innate immunity compared with unclipped females but did not fledge smaller nestlings. Thus, they increased self-maintenance without compromising current reproductive output. In contrast, feather clipping did not affect the number of feeding visits or innate immune function in males, despite increased heat loss rate. Our results show that analyses of physiological parameters, such as constitutive innate immune function, can be important when trying to understand sources of variation in investment in self-maintenance versus reproductive effort and that risk of overheating can influence innate immune function during reproduction.
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| 4. |
- Eikenaar, Cas, et al.
(author)
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A hidden cost of migration? Innate immune function versus antioxidant defense
- 2018
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 8:5, s. 2721-2728
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Journal article (peer-reviewed)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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| 5. |
- Eikenaar, Cas, et al.
(author)
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Migrating birds rapidly increase constitutive immune function during stopover
- 2020
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In: Royal Society Open Science. - : The Royal Society. - 2054-5703. ; 7:2
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Journal article (peer-reviewed)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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| 6. |
- Eikenaar, Cas, et al.
(author)
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Migratory common blackbirds have lower innate immune function during autumn migration than resident conspecifics
- 2016
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In: Biology letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 12
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Journal article (peer-reviewed)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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| 7. |
- Eikenaar, Cas, et al.
(author)
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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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In: Current Zoology. - : Oxford University Press (OUP). - 1674-5507 .- 2396-9814.
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Journal article (peer-reviewed)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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| 8. |
- Eikenaar, Cas, et al.
(author)
-
Recovery of constitutive immune function after migratory endurance flight in free-living birds
- 2023
-
In: Biology letters. - : The Royal Society. - 1744-9561 .- 1744-957X. ; 19:2
-
Journal article (peer-reviewed)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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| 9. |
- Eikenaar, Cas, et al.
(author)
-
Stopover departure decisions in autumn are not associated with constitutive immune function in Northern Wheatears Oenanthe oenanthe
- 2019
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In: Journal of Ornithology. - : Springer Science and Business Media LLC. - 2193-7192 .- 2193-7206. ; 160:3, s. 813-817
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Journal article (peer-reviewed)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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| 10. |
- Ellis, Vincenzo A., et al.
(author)
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Explaining prevalence, diversity and host specificity in a community of avian haemosporidian parasites
- 2020
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In: Oikos. - : Wiley. - 0030-1299 .- 1600-0706. ; 129:9, s. 1314-1329
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Journal article (peer-reviewed)abstract
- Many hypotheses attempt to explain parasite–host associations, but rarely are they examined together in a single community. For hosts, key traits are the proportion of infected individuals (prevalence) and the diversity of parasites infecting them. A key parasite trait is host specificity, ranging from specialists infecting one or a few closely related species to generalists infecting many species. We tested 10 hypotheses to explain host-parasite associations; five ‘host-centric’ (e.g. prevalence is related to host abundance) and five ‘parasite-centric’ (e.g. parasite abundance is related to host specificity). We analyzed a community of 67 locally transmitted avian haemosporidian parasite lineages (genera Plasmodium, Haemoproteus or Leucocytozoon), sampled from 2726 birds (64 species) in southern Sweden. Among host-centric hypotheses, Haemoproteus and Leucocytozoon prevalence and Haemoproteus diversity were related to host habitat preferences, whereas there were no relationships with host abundance or body mass. Haemoproteus and Leucocytozoon prevalences were more similar among closely related than among distantly related host species. Haemoproteus prevalence and diversity were lower in host species with few close relatives (‘evolutionarily distinct’ hosts). Among parasite-centric hypotheses, most lineages, even relative generalists, infected closely related host species more often than expected by chance. However, the host species of Haemoproteus and Leucocytozoon lineages overlapped less among lineages than expected by chance. Specialists did not reach higher prevalences than generalists on single host species. However, the abundance of Haemoproteus lineages was related to host specificity with generalists more common than specialists; this was driven by three closely related generalists. Host specificity of parasites was unrelated to the abundance or evolutionarily distinctiveness of their hosts. Parasite communities are likely structured by many factors and cannot be explained by hypotheses focusing solely on hosts or parasites. However, we found consistent effects of host phylogenetic relationships, plausibly a result of evolutionarily conserved host immune systems limiting parasite distributions.
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| 11. |
- Hegemann, Arne, et al.
(author)
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A mimicked bacterial infection prolongs stopover duration in songbirds—but more pronounced in short- than long-distance migrants
- 2018
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In: Journal of Animal Ecology. - : Wiley. - 0021-8790. ; 87:6, s. 1698-1708
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Journal article (peer-reviewed)abstract
- Migration usually consists of intermittent travel and stopovers, the latter being crucially important for individuals to recover and refuel to successfully complete migration. Quantifying how sickness behaviours influence stopovers is crucial for our understanding of migration ecology and how diseases spread. However, little is known about infections in songbirds, which constitute the majority of avian migrants. We experimentally immune-challenged autumn migrating passerines (both short- and long-distance migrating species) with a simulated bacterial infection. Using an automated radiotelemetry system in the stopover area, we subsequently quantified stopover duration, “bush-level” activity patterns (0.1–30 m) and landscape movements (30–6,000 m). We show that compared to controls, immune-challenged birds prolonged their stopover duration by on average 1.2 days in long-distance and 2.9 days in short-distance migrants, respectively (100%–126% longer than controls, respectively). During the prolonged stopover, the immune-challenged birds kept a high “bush-level” activity (which was unexpected) but reduced their local movements, independent of migration strategy. Baseline immune function, but not blood parasite infections prior to the immune challenge, had a prolonging effect on stopover duration, particularly in long-distance migrants. We conclude that a mimicked bacterial infection does not cause lethargy, per se, but restricts landscape movements and prolongs stopover duration, and that this behavioural response also depends on the status of baseline immune function and migration strategy. This adds a new level to the understanding of how acute inflammation affect migration behaviour and hence the ecology and evolution of migration. Accounting for these effects of bacterial infections will also enable us to fine-tune and apply optimal migration theory. Finally, it will help us predicting how migrating animals may respond to increased pathogen pressure caused by global change.
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| 12. |
- Hegemann, Arne, et al.
(author)
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A physiological perspective on the ecology and evolution of partial migration
- 2019
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In: Journal of Ornithology. - : Springer Science and Business Media LLC. - 2193-7192 .- 2193-7206. ; 160:3, s. 893-905
-
Research review (peer-reviewed)abstract
- Billions of animals migrate between breeding and non-breeding areas worldwide. Partial migration, where both migrants and residents coexist within a population, occurs in most animal taxa, including fish, insects, birds and mammals. Partial migration has been hypothesised to be the most common form of migration and to be an evolutionary precursor to full migration. Despite extensive theoretical models about partial migration and its potential to provide insight into the ecology and evolution of migration, the physiological mechanisms that shape partial migration remain poorly understood. Here, we review current knowledge on how physiological processes mediate the causes and consequences of avian partial migration, and how they may help us understand why some individuals migrate and others remain resident. When information from birds is missing, we highlight examples from other taxa. In particular, we focus on temperature regulation, metabolic rate, immune function, oxidative stress, telomeres, and neuroendocrine and endocrine systems. We argue that these traits provide physiological pathways that regulate the ecological and behavioural causes and/or consequences of partial migration, and may provide insight into the mechanistic basis of wintering decisions. They may, thus, also help us to explain why individuals switch strategies among winters. We also highlight current gaps in our knowledge and suggest promising future research opportunities. A deeper understanding of the physiological mechanisms mediating the causes and consequences of partial migration will not only provide novel insights into the ecology and evolution of migration in general, but will also be vital to precisely modelling population trends and predicting range shifts under global change.
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| 13. |
- Hegemann, Arne, et al.
(author)
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Early and Late Migrating Avian Individuals Differ in Constitutive Immune Function and Blood Parasite Infections – But Patterns Depend on the Migratory Strategy
- 2022
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In: Frontiers in Ecology and Evolution. - : Frontiers Media SA. - 2296-701X. ; 10
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Journal article (peer-reviewed)abstract
- Billions of birds migrate every year. To conduct a successful migration, birds undergo a multitude of physiological adaptions. One such adaptation includes adjustments of immune function, however, little is known about intraspecies (between-individual) and interspecies (between-species) variation in immune modulations during migration. Here, we explore if early and late migrating individuals differ in their immune function, and if such patterns differ among species with short- vs. long-distance migration strategies. We quantified three parameters of baseline (constitutive) innate immune function and one parameter of baseline (constitutive) acquired immune function in 417 individuals of 10 species caught during autumn migration at Falsterbo (Sweden). Early and late migrating individuals differed in lysis and total immunoglobulins (IgY), but the patterns show different directions in long-distance migrants (LDMs) (wintering in Africa) as compared to short-distance migrants (SDMs) (wintering within Europe). Specifically, early migrating LDMs had lower lysis but higher immunoglobulin levels than late migrating individuals. In short distance migrants, there was no difference in lysis between early and late migrating individuals, but immunoglobulin levels were higher in late migrating individuals. We found no correlation between timing of migration and haptoglobin, but LDMs had lower levels of haptoglobin than SDMs. We also found that the prevalence of haemosporidian blood parasite infections decreased in LDMs, but increased in SDMs, as the autumn progressed. Taken together, our study suggests that the investment into immune function depends on the migratory strategy (short- vs. long-distance migrants), and that early and late migrating individuals of a migration strategy might invest differently in baseline immune function, potentially driven by differences in the trade-offs with timing and speed of migration. Our study highlights the potential adaptations of immune function that could help explain trade-offs with other physiological systems, and behavioural responses during migration.
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| 14. |
- Hegemann, Arne, et al.
(author)
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Immune function and blood parasite infections impact stopover ecology in passerine birds
- 2018
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In: Oecologia. - : Springer Science and Business Media LLC. - 0029-8549 .- 1432-1939. ; 188:4, s. 1011-1024
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Journal article (peer-reviewed)abstract
- Stopovers play a crucial role for the success of migrating animals and are key to optimal migration theory. Variation in refuelling rates, stopover duration and departure decisions among individuals has been related to several external factors. The physiological mechanisms shaping stopover ecology are, however, less well understood. Here, we explore how immune function and blood parasite infections relate to several aspects of stopover behaviour in autumn migrating short- and long-distance migrating songbirds. We blood sampled individuals of six species and used an automated radio-telemetry system in the stopover area to subsequently quantify stopover duration, ‘bush-level’ activity patterns (~ 0.1–30 m), landscape movements (~ 30–6000 m), departure direction and departure time. We show that complement activity, the acute phase protein haptoglobin and blood parasite infections were related to prolonged stopover duration. Complement activity (i.e., lysis) and total immunoglobulins were negatively correlated with bush-level activity patterns. The differences partly depended on whether birds were long-distance or short-distance migrants. Birds infected with avian malaria-like parasites showed longer landscape movements during the stopover than uninfected individuals, and birds with double blood parasite infections departed more than 2.5 h later after sunset/sunrise suggesting shorter flight bouts. We conclude that variation in baseline immune function and blood parasite infection status affects stopover ecology and helps explain individual variation in stopover behaviour. These differences affect overall migration speed, and thus can have significant impact on migration success and induce carry-over effects on other annual-cycle stages. Immune function and blood parasites should, therefore, be considered as important factors when applying optimal migration theory.
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| 15. |
- Hegemann, Arne, et al.
(author)
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Indices of immune function used by ecologists are mostly unaffected by repeated freeze-thaw cycles and methodological deviations
- 2017
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In: Frontiers in Zoology. - : Springer Science and Business Media LLC. - 1742-9994. ; 14:1
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Journal article (peer-reviewed)abstract
- Background: Over the past couple of decades, measuring immunological parameters has become widespread in studies of ecology and evolution. A combination of different immunological indices is useful for quantifying different parts of the immune system and comprehensively assessing immune function. Running multiple immune assays usually requires samples to be repeatedly thawed and re-frozen. There is some evidence that repeated freezing and thawing can affect assay results, but this has never been comprehensively studied in some common ecological immunology assays. We tested the effect of multiple (1, 2, 3, 4, 5, 10) freeze-thaw cycles on the results of four commonly used immunological assays: haemolysis-haemagglutination titres, haptoglobin concentration, bacterial killing capacity and total immunoglobulins (IgY). We tested five different bird species from four different bird orders (Passeriformes, Columbiformes, Charadriiformes and Galliformes), and we included both captive and free-living individuals. In addition, we tested for haptoglobin concentrations and the haemolysis-haemagglutination assay if re-analysing samples 1 year apart led to different results. For the haemolysis-haemagglutination assay we also tested two different sources of rabbit blood, and we compared untreated microtitre plates with plates that were "blocked" to prevent nonspecific interactions between the plate and assay reagents. Results: Repeated freezing and thawing of plasma had no effect on lysis titres, haptoglobin concentrations, bacterial killing capacity, or total immunoglobulin levels. Agglutination titres were unaffected by up to five cycles but were lower after ten freeze-thaw cycles. For the haemolysis-haemagglutination assay and haptoglobin concentrations, re-analysing samples 1 year apart yielded highly correlated data. For the haemolysis-haemagglutination assay, the source of rabbit blood did not influence the results, and the untreated vs. blocked plates differed slightly overall, but at the individual level assay results were highly correlated. Using different rabbit blood sources or different types of microtitre plates yielded highly correlated data. Conclusions: Our data suggest that repeated freeze-thaw cycles do not impair assay results to the point of influencing ecological or evolutionary conclusions. Plasma samples can be safely stored in one tube and thawed repeatedly for different assays. Nevertheless, we recommend consistent treatment of samples in terms of freeze-thaw cycles or other laboratory treatments to minimize the potential for introducing a systematic bias.
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| 16. |
- Hicks, Olivia, et al.
(author)
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Holding time has limited impact on constitutive innate immune function in a long-lived Antarctic seabird, the Adélie penguin : implications for field studies
- 2023
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In: Biology Open. - : The Company of Biologists. - 2046-6390. ; 12:2
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Journal article (peer-reviewed)abstract
- There is great interest in measuring immune function in wild animals. Yet, field conditions often have methodological challenges related to handling stress, which can alter physiology. Despite general consensus that immune function is influenced by handling stress, previous studies have provided equivocal results. Furthermore, few studies have focused on long-lived species, which may have different stress-immune trade-offs compared to short-lived species that have primarily been tested. Here, we investigate whether capture and handling duration impacts innate immune function in a long-lived seabird, the Adélie penguin (Pygoscelis adeliae). We found no evidence for changes in three commonly used parameters of innate immune function upon holding time of up to 2 h, suggesting that immune function in this species is more robust against handling than in other species. This opens up exciting possibilities for measuring immune function in species with similar life-histories even if samples cannot be taken directly after capture.
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| 17. |
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| 18. |
- Nebel, Carina, et al.
(author)
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Parental morph combination does not influence innate immune function in nestlings of a colour-polymorphic African raptor
- 2021
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In: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 11:1
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Journal article (peer-reviewed)abstract
- Conditions experienced during early life can have long-term individual consequences by influencing dispersal, survival, recruitment and productivity. Resource allocation during development can have strong carry-over effects onto these key parameters and is directly determined by the quality of parental care. In the black sparrowhawk (Accipiter melanoleucus), a colour-polymorphic raptor, parental morphs influence nestling somatic growth and survival, with pairs consisting of different colour morphs (‘mixed-morph pairs’) producing offspring with lower body mass indices, but higher local apparent survival rates. Resource allocation theory could explain this relationship, with nestlings of mixed-morph pairs trading off a more effective innate immune system against somatic growth. We quantified several innate immune parameters of nestlings (hemagglutination, hemolysis, bacteria-killing capacity and haptoglobin concentration) and triggered an immune response by injecting lipopolysaccharides. Although we found that nestlings with lower body mass index had higher local survival rates, we found no support for the proposed hypothesis: neither baseline immune function nor the induced immune response of nestlings was associated with parental morph combination. Our results suggest that these immune parameters are unlikely to be involved in providing a selective advantage for the different colour morphs’ offspring, and thus innate immunity does not appear to be traded off against a greater allocation of resources to somatic growth. Alternative hypotheses explaining the mechanism of a low nestling body mass index leading to subsequent higher local survival could be related to the post-fledgling dependency period or differences in dispersal patterns for the offspring from different morph combinations.
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| 19. |
- Nicholas P.C., Horrocks, et al.
(author)
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Environmental proxies of antigen exposure explain variation in immune investment better than indices of pace of life
- 2015
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In: Oecologia. - : Springer Science and Business Media LLC. - 1432-1939 .- 0029-8549. ; 177:1, s. 281-290
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Journal article (peer-reviewed)abstract
- Investment in immune defences is predicted to covary with a variety of ecologically and evolutionarily relevant axes, with pace of life and environmental antigen exposure being two examples. These axes may themselves covary directly or inversely, and such relationships can lead to conflicting predictions regarding immune investment. If pace of life shapes immune investment then, following life history theory, slow-living, arid zone and tropical species should invest more in immunity than fast-living temperate species. Alternatively, if antigen exposure drives immune investment, then species in antigen-rich tropical and temperate environments are predicted to exhibit higher immune indices than species from antigen-poor arid locations. To test these contrasting predictions we investigated how variation in pace of life and antigen exposure influence immune investment in related lark species (Alaudidae) with differing life histories and predicted risks of exposure to environmental microbes and parasites. We used clutch size and total number of eggs laid per year as indicators of pace of life, and aridity, and the climatic variables that influence aridity, as correlates of antigen abundance. We quantified immune investment by measuring four indices of innate immunity. Pace of life explained little of the variation in immune investment, and only one immune measure correlated significantly with pace of life, but not in the predicted direction. Conversely, aridity, our proxy for environmental antigen exposure, was predictive of immune investment, and larks in more mesic environments had higher immune indices than those living in arid, low-risk locations. Our study suggests that abiotic environmental variables with strong ties to environmental antigen exposure can be important correlates of immunological variation.
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| 20. |
- Nord, Andreas, et al.
(author)
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Reduced immune responsiveness contributes to winter energy conservation in an Arctic bird
- 2020
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In: Journal of Experimental Biology. - : The Company of Biologists. - 1477-9145 .- 0022-0949. ; 223:8
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Journal article (peer-reviewed)abstract
- Animals in seasonal environments must prudently manage energyexpenditure to survive the winter. This may be achieved throughreductions in the allocation of energy for various purposes (e.g.thermoregulation, locomotion, etc.). We studied whether such tradeoffsalso include suppression of the innate immune response, bysubjecting captive male Svalbard ptarmigan (Lagopus mutahyperborea) to bacterial lipopolysaccharide (LPS) during exposureto either mild temperature (0°C) or cold snaps (acute exposure to−20°C), in constant winter darkness when birds were in energyconservingmode, and in constant daylight in spring. The innateimmune response was mostly unaffected by temperature. However,energy expenditure was below baseline when birds were immunechallenged in winter, but significantly above baseline in spring. Thissuggests that the energetic component of the innate immuneresponse was reduced in winter, possibly contributing to energyconservation. Immunological parameters decreased (agglutination,lysis, bacteriostatic capacity) or did not change (haptoglobin/PIT54)after the challenge, and behavioural modifications (anorexia, massloss) were lengthy (9 days). While we did not study the mechanismsexplaining these weak, or slow, responses, it is tempting to speculatethey may reflect the consequences of having evolved in anenvironment where pathogen transmission rate is presumably lowfor most of the year. This is an important consideration if climatechange and increased exploitation of the Arctic would alter pathogencommunities at a pace outwith counter-adaption in wildlife.
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| 21. |
- Nwaogu, Chima Josiah, et al.
(author)
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Innate immune function and antioxidant capacity of nestlings of an African raptor covary with the level of urbanisation around breeding territories
- 2023
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In: Journal of Animal Ecology. - : Wiley. - 0021-8790 .- 1365-2656. ; 92:1, s. 124-141
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Journal article (peer-reviewed)abstract
- Urban areas provide breeding habitats for many species. However, animals raised in urban environments face challenges such as altered food availability and quality, pollution and pathogen assemblages. These challenges can affect physiological processes such as immune function and antioxidant defences which are important for fitness. Here, we explore how levels of urbanisation influence innate immune function, immune response to a mimicked bacterial infection and antioxidant capacity of nestling Black Sparrowhawks Accipiter melanoleucus in South Africa. We also explore the effect of timing of breeding and rainfall on physiology since both can influence the environmental condition under which nestlings are raised. Finally, because urbanisation can influence immune function indirectly, we use path analyses to explore direct and indirect associations between urbanisation, immune function and oxidative stress. We obtained measures of innate immunity (haptoglobin, lysis, agglutination, bactericidal capacity), indices of antioxidant capacity (total non-enzymatic antioxidant capacity (tAOX) and total glutathione from nestlings from 2015 to 2019. In addition, in 2018 and 2019, we mimicked a bacterial infection by injecting nestlings with lipopolysaccharide and quantified their immune response. Increased urban cover was associated with an increase in lysis and a decrease in tAOX, but not with any of the other physiological parameters. Furthermore, except for agglutination, no physiological parameters were associated with the timing of breeding. Lysis and bactericidal capacity, however, varied consistently with the annual rainfall pattern. Immune response to a mimicked a bacterial infection decreased with urban cover but not with the timing of breeding nor rainfall. Our path analyses suggested indirect associations between urban cover and some immune indices via tAOX but not via the timing of breeding. Our results show that early-life development in an urban environment is associated with variation in immune and antioxidant functions. The direct association between urbanisation and antioxidant capacity and their impact on immune function is likely an important factor mediating the impact of urbanisation on urban-dwelling animals. Future studies should explore how these results are linked to fitness and whether the responses are adaptive for urban-dwelling species.
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| 22. |
- Sumasgutner, Petra, et al.
(author)
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Interactive effects of rising temperatures and urbanisation on birds across different climate zones : A mechanistic perspective
- 2023
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In: Global Change Biology. - : Wiley. - 1354-1013 .- 1365-2486. ; 29:9, s. 2399-2420
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Research review (peer-reviewed)abstract
- Climate change and urbanisation are among the most pervasive and rapidly growing threats to biodiversity worldwide. However, their impacts are usually considered in isolation, and interactions are rarely examined. Predicting species' responses to the combined effects of climate change and urbanisation, therefore, represents a pressing challenge in global change biology. Birds are important model taxa for exploring the impacts of both climate change and urbanisation, and their behaviour and physiology have been well studied in urban and non-urban systems. This understanding should allow interactive effects of rising temperatures and urbanisation to be inferred, yet considerations of these interactions are almost entirely lacking from empirical research. Here, we synthesise our current understanding of the potential mechanisms that could affect how species respond to the combined effects of rising temperatures and urbanisation, with a focus on avian taxa. We discuss potential interactive effects to motivate future in-depth research on this critically important, yet overlooked, aspect of global change biology. Increased temperatures are a pronounced consequence of both urbanisation (through the urban heat island effect) and climate change. The biological impact of this warming in urban and non-urban systems will likely differ in magnitude and direction when interacting with other factors that typically vary between these habitats, such as resource availability (e.g. water, food and microsites) and pollution levels. Furthermore, the nature of such interactions may differ for cities situated in different climate types, for example, tropical, arid, temperate, continental and polar. Within this article, we highlight the potential for interactive effects of climate and urban drivers on the mechanistic responses of birds, identify knowledge gaps and propose promising future research avenues. A deeper understanding of the behavioural and physiological mechanisms mediating species' responses to urbanisation and rising temperatures will provide novel insights into ecology and evolution under global change and may help better predict future population responses.
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| 23. |
- Tanneberger, Franziska, et al.
(author)
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Diet Analysis of Wetland Passerine Nestlings Using Neck Collars or Faecal Sampling Produces Similar Results
- 2017
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In: Ardea. - : Netherlands Ornithologists' Union. - 0373-2266. ; 105:2, s. 145-152
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Journal article (peer-reviewed)abstract
- Two methods are commonly used to study the diet of nestling passerines: the neck collar method and faecal sampling. Most studies apply either method, however, few methodological studies comparing both methods exist and are mainly limited to farmland birds. Furthermore, existing methodological studies only include high-level taxonomic diet categories. Here, we compared both methods using two wetland species, the Reed Bunting Emberiza schoeniclus and the Sedge Warbler Acrocephalus schoenobaenus, and included family level as a lower taxonomic prey level. We found no differences between the two methods in the dietary composition of high-level taxonomic categories (mainly orders) and only small differences in some orders at the family level. Hence, we recommend using the less invasive and easily accessible faecal sampling method rather than the use of neck collars in diet composition studies.
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| 24. |
- Tobler, Michael, et al.
(author)
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Telomeres in ecology and evolution : A review and classification of hypotheses
- 2022
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In: Molecular Ecology. - : Wiley. - 0962-1083 .- 1365-294X. ; 31:23, s. 5946-5965
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Research review (peer-reviewed)abstract
- Research on telomeres in the fields of ecology and evolution has been rapidly expanding over the last two decades. This has resulted in the formulation of a multitude of, often name-given, hypotheses related to the associations between telomeres and life-history traits or fitness-facilitating processes (and the mechanisms underlying them). However, the differences (or similarities) between the various hypotheses, which can originate from different research fields, are often not obvious. Our aim here is therefore to give an overview of the hypotheses that are of interest in ecology and evolution and to provide two frameworks that help discriminate among them. We group the hypotheses (i) based on their association with different research questions, and (ii) using a hierarchical approach that builds on the assumptions they make, such as about causality of telomere length/shortening and/or the proposed functional consequences of telomere shortening on organism performance. Both our frameworks show that there exist parallel lines of thoughts in different research fields. Moreover, they also clearly illustrate that there are in many cases competing hypotheses within clusters, and that some of these even have contradictory assumptions and/or predictions. We also touch upon two topics in telomere research that would benefit from further conceptualization. This review should help researchers, both those familiar with and those new to the subject, to identify future avenues of research.
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| 25. |
- van Dijk, Jacintha G. B., et al.
(author)
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A Comparative Study of the Innate Humoral Immune Response to Avian Influenza Virus in Wild and Domestic Mallards
- 2020
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In: Frontiers in Microbiology. - : Frontiers Media S.A.. - 1664-302X. ; 11, s. 1-13
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Journal article (peer-reviewed)abstract
- Domestic mallards (Anas platyrhynchos domesticus) are traditionally used as a model to investigate infection dynamics and immune responses to low pathogenic avian influenza viruses (LPAIVs) in free-living mallards. However, it is unclear whether the immune response of domestic birds reflects the response of their free-living counterparts naturally exposed to these viruses. We investigated the extent to which the innate humoral immune response was similar among (i) wild-type domestic mallards in primary and secondary infection with LPAIV H4N6 in a laboratory setting (laboratory mallards), (ii) wild-type domestic mallards naturally exposed to LPAIVs in a semi-natural setting (sentinel mallards), and (iii) free-living mallards naturally exposed to LPAIVs. We quantified innate humoral immune function by measuring non-specific natural antibodies (agglutination), complement activity (lysis), and the acute phase protein haptoglobin. We demonstrate that complement activity in the first 3 days after LPAIV exposure was higher in primary-exposed laboratory mallards than in sentinel and free-living mallards. LPAIV H4N6 likely activated the complement system and the acute phase response in primary-exposed laboratory mallards, as lysis was higher and haptoglobin lower at day 3 and 7 post-exposure compared to baseline immune function measured prior to exposure. There were no differences observed in natural antibody and haptoglobin concentrations among laboratory, sentinel, and free-living mallards in the first 3 days after LPAIV exposure. Our study demonstrates that, based on the three innate humoral immune parameters measured, domestic mallards seem an appropriate model to investigate innate immunology of their free-living counterparts, albeit the innate immune response of secondary-LPAIV exposed mallards is a better proxy for the innate immune response in pre-exposed free-living mallards than that of immunologically naive mallards.
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| 26. |
- van Veelen, H. Pieter J., et al.
(author)
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Cloacal microbiota are biogeographically structured in larks from desert, tropical and temperate areas
- 2023
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In: BMC Microbiology. - : Springer Science and Business Media LLC. - 1471-2180. ; 23
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Journal article (peer-reviewed)abstract
- BACKGROUND: In contrast with macroorganisms, that show well-documented biogeographical patterns in distribution associated with local adaptation of physiology, behavior and life history, strong biogeographical patterns have not been found for microorganisms, raising questions about what determines their biogeography. Thus far, large-scale biogeographical studies have focused on free-living microbes, paying little attention to host-associated microbes, which play essential roles in physiology, behavior and life history of their hosts. Investigating cloacal gut microbiota of closely-related, ecologically similar free-living songbird species (Alaudidae, larks) inhabiting desert, temperate and tropical regions, we explored influences of geographical location and host species on α-diversity, co-occurrence of amplicon sequence variants (ASVs) and genera, differentially abundant and dominant bacterial taxa, and community composition. We also investigated how geographical distance explained differences in gut microbial community composition among larks. RESULTS: Geographic location did not explain variation in richness and Shannon diversity of cloacal microbiota in larks. Out of 3798 ASVs and 799 bacterial genera identified, 17 ASVs (< 0.5%) and 43 genera (5%) were shared by larks from all locations. Desert larks held fewer unique ASVs (25%) than temperate zone (31%) and tropical larks (34%). Five out of 33 detected bacterial phyla dominated lark cloacal gut microbiomes. In tropical larks three bacterial classes were overrepresented. Highlighting the distinctiveness of desert lark microbiota, the relative abundances of 52 ASVs differed among locations, which classified within three dominant and 11 low-abundance phyla. Clear and significant phylogenetic clustering in cloacal microbiota community composition (unweighted UniFrac) showed segregation with geography and host species, where microbiota of desert larks were distinct from those of tropical and temperate regions. Geographic distance was nonlinearly associated with pairwise unweighted UniFrac distances. CONCLUSIONS: We conclude that host-associated microbiota are geographically structured in a group of widespread but closely-related bird species, following large-scale macro-ecological patterns and contrasting with previous findings for free-living microbes. Future work should further explore if and to what extent geographic variation in host-associated microbiota can be explained as result of co-evolution between gut microbes and host adaptive traits, and if and how acquisition from the environmental pool of bacteria contributes to explaining host-associated communities.
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| 27. |
- Vinterstare, Jerker, et al.
(author)
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Defence versus defence : Are crucian carp trading off immune function against predator-induced morphology?
- 2019
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In: Journal of Animal Ecology. - : John Wiley & Sons. - 0021-8790 .- 1365-2656. ; 88:10, s. 1510-1521
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Journal article (peer-reviewed)abstract
- Numerous species adopt inducible defence strategies; that is, they have phenotypically plastic traits that decrease the risk of capture and consumption by potential predators. The benefits of expressing alternative phenotypes in high- vs. low-risk environments are well documented. However, inducible anti-predator traits are also expected to incur costs, as they are not expressed when predators are absent, yet empirical evidence of such costs remains scarce. Virtually, all animals in nature are simultaneously under strong selection to evade both capture by predators and infection by parasites or pathogens and, hence, display a diverse arsenal of defences to combat these threats, raising the possibility of trade-offs between defences. A classic example of a predator-induced morphological defence is the deep-bodied shape of crucian carp that reduces risk of predation from gape-size-limited predators. The goal of this study was to examine whether predator exposure affects also immune function in crucian carp, and whether the degree of expressed morphological defence is traded off against immune function in individuals. Following exposure to manipulations of perceived risk (predator presence/absence) in a long-term experiment (8 months), key aspects of innate immune function and individual differences in the expression of inducible morphological defence were quantified. Predator-exposed individuals showed lower haptoglobin levels and complement activity, but higher natural antibody titres than fish from predator-free conditions. When experimentally challenged with a mimicked bacterial infection (LPS injection), fish reared in the presence of a natural predator showed a weaker immune response. Moreover, among predator-exposed individuals, the magnitude of morphological defence expression correlated with both baseline immune function and the ability to mount an immune response. However, these relationships were not consistently supportive of a general trade-off among defences. Our results suggest that fish exposed to predators on average reduce investment in immune function, and, further, the observed relationships among defences in predator-exposed individuals can best be explained from individual fitness and pace-of-life perspectives.
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| 28. |
- Wemer, Laura, et al.
(author)
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Reduced ectoparasite load, body mass and blood haemolysis in Eurasian kestrels (Falco tinnunculus) along an urban–rural gradient
- 2021
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In: Science of Nature. - : Springer Science and Business Media LLC. - 0028-1042 .- 1432-1904. ; 108:5
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Journal article (peer-reviewed)abstract
- Urbanisation is proceeding at an alarming rate which forces wildlife to either retreat from urban areas or cope with novel stressors linked to human presence and activities. For example, urban stressors like anthropogenic noise, artificial light at night and chemical pollution can have severe impacts on the physiology of wildlife (and humans), in particular the immune system and antioxidant defences. These physiological systems are important to combat and reduce the severity of parasitic infections, which are common among wild animals. One question that then arises is whether urban-dwelling animals, whose immune and antioxidant system are already challenged by the urban stressors, are more susceptible to parasitic infections. To assess this, we studied nestlings of Eurasian kestrels (Falco tinnunculus) in Vienna, Austria, during 2015 and 2017. We measured biomarkers of innate immune function, oxidative stress and body mass index and ectoparasite infection intensity in 143 nestlings (from 56 nests) along an urban gradient. Nestlings in more urbanised areas had overall fewer ectoparasites, lower haemolysis (complement activity) and lower body mass index compared to nestlings in less urbanised areas. None of the other immune or oxidative stress markers were associated with the urban gradient. Despite some non-significant results, our data still suggest that kestrel nestlings experience some level of reduced physiological health, perhaps as a consequence of exposure to more urban stressors or altered prey availability in inner-city districts even though they had an overall lower ectoparasite burden in these heavily urbanised areas.
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| 29. |
- Zehtindjiev, Pavel, et al.
(author)
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Haemosporidian infections in skylarks (Alauda arvensis): a comparative PCR-based and microscopy study on the parasite diversity and prevalence in southern Italy and the Netherlands
- 2012
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In: European Journal of Wildlife Research. - : Springer Science and Business Media LLC. - 1612-4642 .- 1439-0574. ; 58:1, s. 335-344
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Journal article (peer-reviewed)abstract
- Changes in agricultural management have been identified as the most probable cause for the decline of Skylark (Alauda arvensis) populations in Europe. However, parasitic infections have not been considered as a possible factor influencing this process. Four hundred and thirty-four Skylarks from the Southern Italy and the Netherlands were screened for haemosporidian parasites (Haemosporida) using the microscopy and polymerase chain reaction (PCR)-based methods. The overall prevalence of infection was 19.5%; it was 41.8% in Italian birds and 8.3% in Dutch birds. The prevalence of Plasmodium spp. was 34.1% and 6.5% in Skylarks from Italy and Netherlands, respectively. Approximately 15% of all recorded haemosporidian infections were simultaneous infections both in Italian and Dutch populations. Six different mitochondrial cytochrome b (cyt b) lineages of Plasmodium spp. and three lineages of Haemoproteus tartakovskyi were found. The lineage SGS1 of Plasmodium relictum was the most prevalent at both study sites; it was recorded in 24.7% of birds in Italy and 5.5% in the Netherlands. The lineages SYAT05 of Plasmodium vaughani and GRW11 of P. relictum were also identified with a prevalence of <2% at both study sites. Two Plasmodium spp. lineages (SW2 and DELURB4) and three H. tartakovskyi lineages have been found only in Skylarks from Italy. Mitochondrial cyt b lineages SYAT05 are suggested for molecular identification of P. vaughani, a cosmopolitan malaria parasite of birds. This study reports the greatest overall prevalence of malaria infection in Skylarks during the last 100 years and shows that both Plasmodium and Haemoproteus spp. haemosporidian infections are expanding in Skylarks so it might contribute to a decrease of these bird populations in Europe.
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| 30. |
- Ziegler, Ann-Kathrin, et al.
(author)
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Exposure to artificial light at night alters innate immune response in wild great tit nestlings
- 2021
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In: Journal of Experimental Biology. - : The Company of Biologists. - 1477-9145 .- 0022-0949. ; 224:10
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Journal article (peer-reviewed)abstract
- The large-scale impact of urbanization on wildlife is rather well documented; however, the mechanisms underlying the effects of urban environments on animal physiology and behaviour are still poorly understood. Here, we focused on one major urban pollutant – artificial light at night (ALAN) – and its effects on the capacity to mount an innate immune response in wild great tit (Parus major) nestlings. Exposure to ALAN alters circadian rhythms of physiological processes, by disrupting the nocturnal production of the hormone melatonin. Nestlings were exposed to a light source emitting 3 lx for seven consecutive nights. Subsequently, nestlings were immune challenged with a lipopolysaccharide injection, and we measured haptoglobin and nitric oxide levels pre- and post-injection. Both haptoglobin and nitric oxide are important markers for innate immune function. We found that ALAN exposure altered the innate immune response, with nestlings exposed to ALAN having lower haptoglobin and higher nitric oxide levels after the immune challenge compared with dark-night nestlings. Unexpectedly, nitric oxide levels were overall lower after the immune challenge than before. These effects were probably mediated by melatonin, as ALAN-treated birds had on average 49% lower melatonin levels than the dark-night birds. ALAN exposure did not have any clear effects on nestling growth. This study provides a potential physiological mechanism underlying the documented differences in immune function between urban and rural birds observed in other studies. Moreover, it gives evidence that ALAN exposure affects nestling physiology, potentially causing long-term effects on physiology and behaviour, which ultimately can affect their fitness.
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