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Constitutive immune function in European starlings, Sturnus vulgaris, is decreased immediately after an endurance flight in a wind tunnel

Authors:
Silke Nebel at Birds Canada
Silke Nebel
  • Birds Canada
Ulf Bauchinger at Jagiellonian University
Ulf Bauchinger
Deborah M Buehler
Deborah M Buehler
Lillie Langlois at Clemson University
Lillie Langlois
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Abstract and Figures

Life-history theory predicts that animals face a trade-off in energy allocation between performing strenuous exercise, such as migratory flight, and mounting an immune response. We experimentally tested this prediction by studying immune function in European starlings, Sturnus vulgaris, flown in a wind tunnel. Specifically, we predicted that constitutive immune function decreases in response to training and, additionally, in response to immediate exercise. We compared constitutive immune function among three groups: (1) 'untrained' birds that were kept in cages and were not flown; (2) 'trained' birds that received flight training over a 15 day period and performed a 1-4 h continuous flight, after which they rested for 48 h before being sampled; and (3) 'post-flight' birds that differed from the 'trained' group only in being sampled immediately after the final flight. A bird in our trained group represents an individual during migration that has been resting between migratory flights for at least 2 days. A bird in our post-flight group represents an individual that has just completed a migratory flight and has not yet had time to recover. Three of our four indicators (haptoglobin, agglutination and lysis) showed the predicted decrease in immune function in the post-flight group, and two indicators (haptoglobin, agglutination) showed the predicted decreasing trend from the untrained to trained to post-flight group. Haptoglobin levels were negatively correlated with flight duration. No effect of training or flight was detected on leukocyte profiles. Our results suggest that in European starlings, constitutive immune function is decreased more as a result of immediate exercise than of exercise training. Because of the recent emergence of avian-borne diseases, understanding the trade-offs and challenges faced by long-distance migrants has gained a new level of relevance and urgency.
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Content may be subject to copyright.
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Haptoglobin (z-score)
–1
0
1
2
50
100
150
Agglutination
2.0
2.5
Lysis
Untrained Post-flight
A
B
C
A (45) A,B (25)
B (14)
A (56) A (29)
B (16)
A (56) A,B (29)
B (16)
Trained
0 100 200 300 400 500
Flight time (min)
–3
–2
–1
0
1
2
3
Plasma haptoglobin concentration (z-score)
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... In line with energetic trade-offs or immunopathology avoidance, several studies report lower immune indices during migration compared to those in other annual-cycle stages (Owen andMoore 2006, Eikenaar andHegemann 2016). While immune defences might vary seasonally (Owen and Moore 2008), experimental work suggests that immune functions may also be impacted by strenuous flight on a much finer temporal scale (Matson et al. 2012a, Nebel et al. 2012; but see Hasselquist et al. 2007). ...
... Although the relations to refuelling have not fully been elucidated (Eikenaar et al. 2020b), physiological recovery has been suggested to occur in the context of oxidative balance (Skrip et al. 2015, Eikenaar et al. 2020c, 2023c, Cooper-Mullin and McWilliams 2022 and may extend to the recovery of immune functions Hegemann 2016, Eikenaar et al. 2020a, b). Such a recovery may be needed after arrival on a stopover, as indices of immune function can be impacted by flight (Matson et al. 2012a, Nebel et al. 2012; but see Hasselquist et al. 2007), especially in birds that are mounting an acute phase response (Nebel et al. 2013). Indeed, immune indices have been found to increase over time since arrival on a stopover (Buehler et al. 2010a, Eikenaar et al. 2020a, 2023a, suggesting that this process takes time. ...
... β ± SE e β e β 95%CI (L-U) z p(>|z|) χ 2 (1) p(>χ) Page 8 of 14 been restoring their oxidative balance. However, how flight impacts haptoglobin levels is poorly understood (Nebel et al. 2012, Matson et al. 2012a, and although oxidative lipid damage was found to decrease during stopover (Skrip et al. 2015, Eikenaar et al. 2020c, 2023b, Cooper-Mullin and McWilliams 2022, the evidence linking it to stopover durations is mixed McWilliams 2022, Eikenaar et al. 2023b). Apart from the weak positive correlation involving haptoglobin, we found no other correlations between immune indices and minimum stopover duration. ...
Effects of immune status on stopover departure decisions are subordinate to those of condition, cloud cover and tailwind in autumn‐migrating common blackbirds Turdus merula
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Migratory birds encounter a large variety of parasites and pathogens en route and invest in immune defences to limit the risk and fitness costs of infection. Since both migration and immune defences carry costs, individuals on tight budgets may face trade‐offs between migratory progress and immune status. Many species alternate legs of strenuous migratory flight with stopovers during which birds refuel, rest, and recover physiologically. Despite this, most time and energy consumed during migration are actually spent on stopovers. As a result, identifying what determines stopover duration is key in understanding how migratory birds balance investments in immune defences and migration. Yet, it is unknown under what conditions an individual's immune status may affect migratory progress through the duration of stopovers. We explored whether immune status at arrival affects stopover duration by radio‐tagging and blood‐sampling common blackbirds Turdus merula during autumn stopovers on the Dutch island of Vlieland. To measure immune status, we quantified levels of bacterial killing ability, natural antibodies, complement, and haptoglobin, as well as heterophil–lymphocyte ratios. We show that stopover departures peaked during periods with low cloud cover and strong tailwinds. While lean birds prolonged stopovers, we only found a weak tendency of prolongation in birds with elevated haptoglobin levels. We conclude that effects of immune status on minimum stopover durations are subordinate to those of condition, cloud cover, and tailwinds in autumn‐migrating common blackbirds. Hence, future studies on the link between immune defences and stopover durations should take weather conditions into account.
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... Thus, they are an ideal natural system to study how the endogenous antioxidant system responds to flight training, dietary antioxidants, and dietary fat. We used European starlings Sturnus vulgaris as representative songbirds for this study because they are abundant in the New World and Old World, are omnivorous, acclimate well to captivity and new diets, and have been successfully trained and flown in wind tunnels in other studies (Nebel et al. 2012, Hall et al. 2014, Casagrande et al. 2020. Hatch year European starlings were caught at a dairy farm 20 km north of the Advanced Facility for Avian Research (AFAR), University of Western Ontario, London, Ontario, prior to fall migration in 2015 (19-23 August). ...
Flying stimulates the antioxidant system and protects against oxidative damage in a migratory songbird, yet diet quality has little effect
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Full-text available
Ecologically relevant factors such as exercise and diet quality can directly influence how multifaceted physiological systems work; however, little is known about how such factors directly and interactively affect key components of the antioxidant system in multiple tissues of migratory songbirds. We tested 3 main hypotheses across three tissues in European starlings fed diets with more or less antioxidants (anthocyanins) and long‐chain omega‐6 polyunsaturated fats (18:2n6) while being flight‐trained in a wind tunnel. Stimulatory effect of flight: flight‐training stimulated the antioxidant system in that 1) plasma oxidative damage (dROMs) was reduced during a given acute flight, and contrary to our predictions, 2) antioxidant capacity (OXY or ORAC) and oxidative damage in plasma (dROMs), flight‐muscle, and liver (LPO) of flight‐trained birds were similar to that of untrained birds (i.e. not flown in a wind tunnel). Flight‐trained birds that expended more energy per unit time (kJ min⁻¹) during their longest, final flight decreased antioxidant capacity (OXY) the most during the final flight. Dietary fat quality effect: contrary to our predictions, dietary 18:2n‐6 did not influence oxidative status even after flight training. Dietary antioxidant effect: flight‐trained birds supplemented with dietary anthocyanins did not have higher antioxidant capacity in plasma (OXY), or liver and flight‐muscle (ORAC) compared to untrained birds. Counterintuitively, oxidative damage (dROMs) was higher in flight‐trained supplemented birds compared to unsupplemented birds after an acute flight. In sum, the antioxidant system of songbirds flexibly responded to changes in availability of dietary antioxidants as well as increased flight time and effort, and such condition‐dependent, individual‐level, tissue‐specific responses to the oxidative costs of long‐duration flights apparently requires recovery periods for maintaining oxidative balance during migration.
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... This explanation is supported by a number of studies that have shown that seasonal variation in immune parameters is attributed to increases in parasite prevalence over the breeding season (Merino et al. 2000, Arriero 2009, Emmenegger et al. 2018). The condition-dependent immunoglobulin levels found in our study, along with the fluctuation in energy stores (muscle and fat), seem to support the idea that the variation in immune parameters observed could result from trade-offs mediated by energetic constraints, given the tremendous energetic demands involved in migration (Piersma 2002, Nebel et al. 2012; but see Linek et al. 2024). Therefore, the variation observed may reflect individual flexibility in how animals cope with the environment and may be shaped by the combined effect of immunological responses linked to seasonal variation in infections, and the effect of immunological trade-offs mediated by nutrition and energy stores (Pedersen and Babayan 2011, Hegemann et al. 2012, Arriero et al. 2018, Ohmer et al. 2021. ...
Adaptive immunity modulation linked to migratory behaviour in two partially migratory hoopoe Upupa epops populations
Article
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Ecophysiology has enhanced our understanding of avian migration, yet many aspects of how these processes interrelate are still unclear. Partially migratory populations provide an ideal framework for its study in the wild, since resident and migratory individuals coexist temporarily in the same area and face similar selection pressures. We focused on two Iberian populations of Eurasian hoopoe Upupa epops, a trans‐Saharan long‐distance migrant, to explore the links between the immune system and migratory behaviour. We determined the migratory status of individual hoopoes using stable isotope analysis of deuterium (²H) and measured a number of immunological parameters, including estimates of innate and adaptive immunity, as well as body condition, and muscle and fat stores. Our results indicate that resident hoopoes had higher IgY levels and higher muscle and fat stores compared to migrants during the breeding season. Moreover, we found seasonal variation in leukocyte profiles of resident birds, with higher heterophil/lymphocyte (H/L) ratios in winter than during the breeding season. We observed significantly higher H/L ratios and complement activity in resident males than in resident females, but not within migratory birds. Overall, we show differences in immune response linked to migratory behaviour in partial migratory populations. This study contributes to unraveling the associations between physiological status and migratory behaviour and ultimately helps to understand how different migratory strategies are maintained in partially migratory populations.
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... Overcoming these challenges requires highly specialised physiological adaptations (Hederströn 2008, Piersma andvan Gils 2011), such as the ability to rapidly build up fat reserves adjusting to changes in nutritional landscapes (Lindström andPiersma 1993, Price 2010). Migrants also face considerable immunological challenges during migration, most notably being able to regulate the trade-off between pathogen defence and costly immune responses (Nebel et al. 2012, Eikenaar and Hegemann 2016, O'Connor et al. 2018 during increased exposure to novel pathogens (Figuerola and Green 2000, Leung and Koprivnikar 2016, Poulin and de Angeli Dutra 2021. Many of these physiological adaptions of migrants require extreme phenotypic flexibility as individuals switch between migratory stages, ecosystems, and latitudes. ...
Migratory microbiomes: the role of the gut microbiome in bird migration eco‐physiology
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Long‐distance bird migration is one of the most metabolically and immunologically challenging feats in the animal kingdom, with birds often needing to double their weight in a matter of days and facing increased exposure to novel pathogens. The physiological and behavioural adaptations required to survive such journeys may be facilitated by the gut microbiome, a diverse community of symbiotic microbes that produce rare nutrients, fatty acids, and immune compounds that can confer rapid physiological adaptations to changing environmental conditions. However, the causal role of the gut microbiome in regulating migration physiology remains a mystery. In this review, we synthesize current knowledge of gut microbiome composition and function during migration, outline possible mechanisms by which changes in the gut microbiome could benefit migrants, and identify future research priorities. We find that active migration is usually associated with reduced diversity of the gut microbiome and with the expansion of several study‐specific taxa. Additionally, some microbial traits have been found to correlate with host condition and fat deposits during migration. However, there remains little understanding of how changes in the gut microbiome during migration relate to most physiological parameters, the molecular mechanisms linking the gut microbiome to host physiology during migration, or the underlying ecological, dietary, and intrinsic drivers of gut microbiome changes across the migratory cycle. Our review draws from examples across non‐migratory systems to explore how gut microbiomes could adaptively regulate physiological traits relevant to migration. We highlight the need for studies that connect gut and circulating metabolites and for experimental studies that test the underlying drivers of gut microbial and metabolite dynamics in controlled settings. Given its diverse physiological demands and ubiquity, bird migration presents an excellent model system to investigate the adaptive potential of the gut microbiome in natural populations.
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... For example, an experimental captive group of Swainson's trushes Catharus ustulatus exhibiting migratory activity had lower induced immune responses compared to control non-migratory birds (Owen and Moore 2008a). Also, the concentration of haptoglobin, an acute phase protein, decreased with experimental flight duration in the common starling Sturnus vulgaris (Nebel et al. 2012). A comparison between migratory and resident Eurasian blackbirds Turdus merula captured during the autumn migration on the Helgoland island (North Sea) revealed significant differences in microbial killing capacity and haptoglobin-like activity, both of which serve as indices of innate immune function (Eikenaar and Hegemann 2016). ...
Condition‐dependent immune response in a migrating shorebird, the common snipe Gallinago gallinago
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Full-text available
Bird migration, as an energy‐demanding activity, is expected to generate allocation trade‐offs between important biological processes. For example, long‐distance migratory flights may require redirection of resources from immune response and promote temporal immunosuppression. Individuals in high body condition may have the capacity to cope with the costs of migration while maintaining adequate levels of immune activity. Here, we investigated the covariation of immune response and two measures of condition in a short‐distance migratory shorebird, the common snipe Gallinago gallinago. We captured and experimentally induced immune response using phytohaemagglutinin (PHA) in 148 snipes during the autumn migration. We found a positive relationship of PHA‐induced immune response with indices of body condition reflecting aerobic capacity (total blood haemoglobin concentration) and the level of accumulated energy reserves (size‐corrected body mass). The results provided evidence for a condition‐dependent immune response in migrating snipes, indicating that high‐quality individuals are capable of sustaining immune response during migration. We suggest that abundant food resources at high‐quality stopover sites may help individuals rapidly replenish body reserves essential for the effective functioning of the immune system. It also seems likely that the maintenance of adequate immune function or its upregulation may confer significant adaptive advantages under ecological conditions of increased pathogenic exposure during migration.
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... This could be because infection with haemosporidian parasites is influenced by biological and ecological factors. Migration is an energy demanding process that could weaken the hosts' immune system (Nebel et al., 2012), making them more susceptible to parasites. Infection with haemosporidian parasites in migratory birds or those already in wintering areas is increased by the fact that they usually stay in flocks (Agostini et al., 2004), which can attract more vectors and facilitate parasite transmission. ...
Prevalence and local transmission of haemosporidian (Haemosporida) parasites in nestlings of birds of prey (Aves, Accipitriformes) in the temperate forests in Lithuania
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Full-text available
  • Oct 2024
Wild birds of prey (Accipitriformes) are infected with haemosporidian (Haemosporida) parasites worldwide, and it is known that these parasites can negatively affect their health. These birds are less studied due to their low densities in ecosystems, conservation status, and difficulty of accessing them in the wild. Therefore, in this study, we focused on nestlings of birds of prey that are accessible in their nests during late breeding stages in temperate forests in Lithuania. Investigating haemosporidian parasites in nestlings is crucial for understanding local parasite transmission. To identify the haemosporidian parasite species transmitted in Lithuania, we sampled nestlings of the white-tailed eagles (Haliaeetus albicilla), lesser spotted eagles (Clanga pomarina), and common buzzards (Buteo buteo) in 2019–2022. Blood samples were collected from the nestlings, and molecular methods were employed to sequence a fragment of the parasite's cytochrome b (cyt b) gene using specific primers (Plas1F/HaemNR3 and 3760F/HaemJR4). In addition to molecular techniques, microscopy was used to examine blood smears for the presence of parasites. Our results revealed that nestlings of birds of prey were infected only with Leucocytozoon spp., with an overall prevalence of 30.5%. The prevalence was similar between years, but it was significantly species-dependent. The common buzzard nestlings had the highest prevalence (80%), followed by the lesser spotted eagle (29.2%) and the white-tailed eagle (13.2%). A total of nine genetic lineages were identified, with five of them being novel. Our study demonstrates that Leucocytozoon parasites are actively transmitted to nestlings of birds of prey in Lithuania, with a high prevalence.
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... Hence, a well-functioning immune system during migration is important to minimize diseaserelated mortality. However, it has been shown that endurance flight may negatively impact constitutive immune parameters in European Starlings, Sturnus vulgaris (Nebel et al., 2012), as well as in Red knots, Calidris canutus (Buehler et al., 2010), suggesting lower immunocompetence in birds after a migratory flight. To (partly) compensate for this, migrants are able to boost immune function during stopover (Owen & Moore, 2008), within days of arrival at a stopover site (Eikenaar et al., 2023;Eikenaar, Hessler, & Hegemann, 2020). ...
Constitutive immune function is not associated with fuel stores in spring migrating passerine birds
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Full-text available
  • Jun 2024
Migratory birds may either upregulate their immune system during migration as they might encounter novel pathogens or downregulate their immune system as a consequence of trade‐offs with the resource costs of migration. Support for the latter comes not least from a study that reports a positive correlation in autumn migrating birds between fuel stores and parameters of innate and acquired immune function, that is, energy‐exhausted migrants appear to have lowered immune function. However, to our knowledge, no study has tested whether this pattern exists in spring migrating birds, which may face other trade‐offs than autumn migrants. Here, we investigate if in spring there is a relationship between fuel stores and microbial‐killing ability, a measure of innate immune function, and total immunoglobulin (IgY), a measure of acquired immune function, in four migrating bird species: chaffinches (Fringilla coelebs), dunnocks (Prunella modularis), song thrushes (Turdus philomelos) and northern wheatears (Oenanthe oenanthe). Our findings indicate no significant correlation between fuel stores and either microbial killing ability or IgY levels when considering all species collectively. When analysing species separately, we found a significant negative correlation between fuel stores and microbial‐killing ability in chaffinches and a positive correlation between fuel stores and IgY levels in wheatears. In song thrushes, but not in any of the other species, there was a significant negative correlation between relative arrival date and microbial‐killing ability and between arrival date and IgY levels. Sex did not affect immune function in any of the species. Our study suggests that the relationship between immune function and fuel stores may be different during spring migration compared to autumn migration. Differences in the speed of migration or pathogen pressure may result in different outcomes of the resource trade‐off between investment in immune function and migration among the seasons.
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... Several studies in birds suggested that migrants temporarily suppress immunity and re-allocate energy to endurance flights (Altizer et al., 2011;Eikenaar and Hegemann, 2016;Eikenaar et al., 2018;Møller et al., 2004;Nebel et al., 2012Nebel et al., , 2013Moore, 2006, 2008a,b). However, it is still unclear whether and how immunity might be optimally modulated during pre-migratory fuelling and to what extent individual variation of innate immunity is related to the rapid accumulation of energy stores during this specific life cycle stage. ...
Controlled expression of avian pre-migratory fattening influences indices of innate immunity
Article
Full-text available
  • Jan 2024
  • Biol Open
While immunity is frequently dampened when birds engage in strenuous migratory flights, whether and how immunity changes during the rapid accumulation of energy stores in preparation for migration remains largely unknown. Here we induced pre-migratory fattening through controlled changes of daylight in common quails (Coturnix coturnix) and regularly assessed changes in three markers of constitutive innate immunity (leukocyte coping capacity or LCC, hemagglutination and hemolysis titres) and measures of body composition (lean and fat mass). All the three markers showed similar changes over the pre-migratory fattening process. LCC responses, hemagglutination titres, and hemolysis titres, were on average higher in the mid-fattening phase compared to the peak-fattening phase, when values were similar to those observed prior the start of pre-migratory fattening. At mid-fattening, we found that the birds that showed a larger accumulation of fat mass (as % of body mass) had lower LCC peak responses and hemolysis titres. Reversibly, at mid-fattening, we also found that the birds that kept a higher proportion of lean mass (as % of body mass) had the highest LCC peaks. Our results indicate that migratory birds undergo changes in immune indices (over 8 weeks) as they accumulate energy stores for migration and propose that this could be due to competing or trade-off processes between metabolic remodelling and innate immune system function.
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... According to the trade-off hypothesis, we predicted that species with more copies of MHC genes would show lower concentrations of natural antibodies and complement. While the costs of development, maintenance, and use of natural antibodies and complement are thought to be relatively low [11], downregulation of these defences has been documented during or after some energetically-demanding periods (e.g., endurance flight [38]), indicating that there is evolutionary potential for innate immunity to have been suppressed among species under limited resources. Also, individuals or species with more diverse MHC repertoires (i.e., larger numbers of gene copies) are thought to suffer greater physiological costs [39], which can promote fitness trade-offs between innate and acquired immunity. ...
Evolutionary trade-off between innate and acquired immune defences in birds
Article
Full-text available
  • Sep 2023
  • Front Zool
Background The development, maintenance, and use of immune defences are costly. Therefore, animals face trade-offs in terms of resource allocation within their immune system and between their immune system and other physiological processes. To maximize fitness, evolution may favour investment in one immunological defence or subsystem over another in a way that matches a species broader life history strategy. Here, we used phylogenetically-informed comparative analyses to test for relationships between two immunological components. Natural antibodies and complement were used as proxies for the innate branch; structural complexity of the major histocompatibility complex (MHC) region was used for the acquired branch. Results We found a negative association between the levels of natural antibodies (i.e., haemagglutination titre) and the total MHC gene copy number across the avian phylogeny, both at the species and family level. The family-level analysis indicated that this association was apparent for both MHC-I and MHC-II, when copy numbers within these two MHC regions were analysed separately. The association remained significant after controlling for basic life history components and for ecological traits commonly linked to pathogen exposure. Conclusion Our results provide the first phylogenetically robust evidence for an evolutionary trade-off within the avian immune system, with a more developed acquired immune system (i.e., more complex MHC architecture) in more derived bird lineages (e.g., passerines) being accompanied by an apparent downregulation of the innate immune system.
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Rising to The Challenge: Mounting An Acute Phase Immune Response Has No Long-Term Negative Effects on Captive Sparrow Migratory Body Composition Or Migratory Restlessness
Article
  • Aug 2023
  • INTEGR COMP BIOL
Synopsis Migratory animals may trade-off between investing energy in immune defense versus investing in energy reserves needed for seasonal migration. However, these trade-offs are often masked by other sources of variation and may not be detected through observational field studies of free-living animals. Moreover, observational studies can rarely distinguish the costs of pathogenic infection from those of mounting an immune response. To disentangle such effects, we conducted an immune challenge experiment. We captured song sparrows (Melospiza melodia) and white-throated sparrows (Zonotrichia albicollis) in autumn migratory condition, challenged the sparrows with non-infectious antigens that induce an acute-phase immune response, then monitored body composition and migratory restlessness behavior. For both species, body mass was higher the day after exposure to keyhole limpet hemocyanin (KLH) compared to controls. White-throated sparrows, but not song sparrows, increased lean mass 1 week after exposure to lipopolysaccharide (LPS), suggesting that effects of immune upregulation on body composition may be long-lasting and specific to certain combinations of hosts and antigens. White-throated sparrows exposed to KLH increased nocturnal migratory restlessness (Zugunruhe) for the week following exposure. These findings suggest that short-term activation of the acute immune response does not constrain migratory physiology in these songbirds.
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Parasite avoidance: The cause of post-calving migrations in Rangifer?
Article
Full-text available
Intensities of warble fly larvae, Hypoderma tarandi (L.), were examined in slaughtered reindeer (Rangifer tarandus tarandus L.) from different summer grazing areas of Finnmark County, northern Norway. To test the hypothesis-that larval abundance decreases with increase in post-calving migration distance (i.e., distance from calving grounds), herds with differing migration distances were sampled. The prevalence of infection in the total sample of 1168 animals was 99.9%. The study revealed significant differences in larval abundance among herds from different summer grazing areas. Herds with post-calving migrations have significantly lower larval abundances than herds remaining on or near the calving grounds for the whole summer. Between-herds variation in abundance of H. tarandi larvae is assumed to reflect differing densities of the infective stage (adult flies) on the herds' summer ranges. Larval abundance in a herd is in turn negatively correlated with the distance between the main larval shedding areas (i.e., calving grounds) and the areas of greatest transmission (i.e., summer pastures). These results are discussed in relation to transmission of other parasites common to Rangifer and suggest that this host's post-calving migration may be a behavioural adaptation that reduces levels of parasitic infections.
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Indices of Immune Function are Lower in Red Knots ( Calidris canutus ) Recovering Protein Than in Those Storing Fat during Stopover in Delaware Bay
Article
Full-text available
  • Apr 2010
Each year, hundreds of thousands of shorebirds use Delaware Bay, on the northeast coast of the United States, as a final stopover before migration to breeding areas. The bay provides them with abundant Horseshoe Crab (Limulus polyphemus) eggs, which they use to gain the fat stores necessary for continued migration and subsequent survival on the breeding grounds. However, abundant food attracts dense mixed-species flocks, which may facilitate pathogen transmission, and migration itself may suppress immune defense. Despite the potential importance of disease risk and immune function during migration, little is known about how immune function changes during stopover in migratory shorebirds. To examine this, we measured constitutive immune function in Red Knots (Calidris canutus aura) during stopover in Delaware Bay. We found lower total leukocyte, lymphocyte, and monocyte concentrations, complement-mediated lysis, and haptoglobin activity in birds recovering protein after migration than in birds storing fat to fuel subsequent flight. We discuss two possible reasons for this result. First, fueling birds may have an increased rate of infection or may be bolstering immune defense in response to high antigen exposure. Second, recovering birds may be immuno-compromised because of the physical strain of migratory flight or as a result of adaptive tradeoffs between immune function and migration. Received IS January 2009, accepted 26 August 2009.
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Stress and immune defense
Article
  • Jan 1998
  • ADV STUD BEHAV
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The costs of immunity
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  • Jan 2004
  • Acta Zoolog Sin
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Exercise and Immune Function
Article
  • Feb 1999
Comparison of immune function in athletes and nonathletes reveals that the adaptive immune system is largely unaffected by athletic endeavour. The innate immune system appears to respond differentially to the chronic stress of intensive exercise, with natural killer cell activity tending to be enhanced while neutrophil function is suppressed. However, even when significant changes in the level and functional activity of immune parameters have been observed in athletes, investigators have had little success in linking these to a higher incidence of infection and illness. Many components of the immune system exhibit change after prolonged heavy exertion. During this ‘open window’ of altered immunity (which may last between 3 and 72 hours, depending on the parameter measured), viruses and bacteria may gain a foothold, increasing the risk of subclinical and clinical infection. However, no serious attempt has been made by investigators to demonstrate that athletes showing the most extreme post-exercise immunosuppression are those that contract an infection during the ensuing 1 to 2 weeks. This link must be established before the ‘open window’ theory can be wholly accepted. The influence of nutritional supplements, primarily zinc, vitamin C, glutamine and carbohydrate, on the acute immune response to prolonged exercise has been measured in endurance athletes. Vitamin C and glutamine have received much attention, but the data thus far are inconclusive. The most impressive results have been reported in the carbohydrate supplementation studies. Carbohydrate beverage ingestion has been associated with higher plasma glucose levels, an attenuated cortisol and growth hormone response, fewer perturbations in blood immune cell counts, lower granulocyte and monocyte phagocytosis and oxidative burst activity, and a diminished pro- and anti-inflammatory cytokine response. It remains to be shown whether carbohydrate supplementation diminishes the frequency of infections in the recovery period after strenuous exercise. Studies on the influence of moderate exercise training on host protection and immune function have shown that near-daily brisk walking compared with inactivity reduced the number of sickness days by half over a 12- to 15-week period without change in resting immune function. Positive effects on immunosurveillance and host protection that come with moderate exercise training are probably related to a summation effect from acute positive changes that occur during each exercise bout. No convincing data exist that moderate exercise training is linked with improved T helper cell counts in patients with HIV, or enhanced immunity in elderly participants.
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