Interspecific associations between circulating antioxidant levels and life-history variation in birds

Antioxidants play an important role in protecting tissues against aging-associated oxidative damage and are thus prime candidates for relating physiological mechanisms to variation in life histories. We measured total antioxidant capacity, antioxidant response to stress, and levels of uric acid, vitamin E, and four carotenoids in 95 avian species, mostly passerines from Michigan or Panama. We compared antioxidant measures to seven variables related to life histories (clutch size, survival rate, incubation period, nestling period, basal metabolic rate, body mass, and whether the species lived in a tropical or temperate climate). Life-history-related traits varied over at least three statistically independent axes. Higher antioxidant levels were generally characteristic of more rapid development, lower survival rate, smaller body size, larger clutch size, and higher mass-adjusted metabolic rate, but the relationships of particular antioxidants with individual life-history traits showed considerable complexity. Antioxidant-life history associations differed between tropical and temperate species and varied with respect to taxonomic sampling. Vitamin E showed few relationships with life-history traits. Overall, our results partly support the hypothesis that antioxidant levels evolve to mirror free radical production. Clearly, however, the complex patterns of physiological diversification observed here result from the interplay of many factors, likely including not just investment in somatic maintenance but also phylogenetic constraint, diet, and other aspects of ecology.     

Oxidative damage and plasma antioxidant capacity in relation to body size,age, male sexual traits and female reproductive performance in the collared flycatcher (<Emphasis Type="Italic">Ficedula albicollis</Emphasis>)

The study of oxidative stress is a potential tool for studying the functional interactions among life history traits, sexual traits and physiological status in animals. In this study, we investigated relationships between measures of plasma oxidative status and male sexual traits, female reproductive investment and three other life history traits, in a wild population of collared flycatchers (Ficedula albicollis). Flycatcher males with a larger white forehead patch had higher level of plasma antioxidant capacity. For females, clutch size was not associated with plasma oxidative status, but egg size was positively correlated with antioxidant capacity. The relationship between age and levels of plasma oxidative damage remains controversial in this species: young female flycatchers showed higher levels of hydroperoxides compared to antioxidants, whereas age did not predict oxidative status of males. Males had higher levels of oxidative damage than females, although the concentration of antioxidant compounds was similar between the sexes. Females that mated with more ornamented males had higher plasma antioxidant capacity. Our results suggest that, for males and females, greater investment in sexual signal and reproduction, respectively, does not reduce the capacity for self-maintenance or avoidance of oxidative stress. Finally, our data support indirectly the occurrence of assortative mating in our species, since females with higher plasma antioxidant capacity mated with more ornamented males.     

Stress-Induced Tradeoffs in a Free-Living Lizard across a Variable Landscape: Consequences for Individuals and Populations

Current life history theory suggests that the allocation of energetic resources between competing physiological needs should be dictated by an individual’s longevity and pace of life. One key physiological pathway likely to contribute to the partitioning of resources is the vertebrate stress response. By increasing circulating glucocorticoids the stress response can exert a suite of physiological effects, such as altering immune function. We investigated the effects of stress physiology on individual immunity, reproduction and oxidative stress, across an urban landscape. We sampled populations in and around St. George, Utah, examining corticosterone in response to restraint stress, two innate immune measures, reproductive output, and the presence of both reactive oxygen metabolites and antioxidant binding capacity, in populations of common side-blotched lizards (Uta stansburiana) experiencing variable levels of environmental stress. Additionally, using capture-mark-recapture techniques, we examined the relationships between these physiological parameters and population-level differences. Our results reveal elevated physiological stress corresponds with suppressed immunity and increased oxidative stress. Interestingly, urban populations experiencing the most physiological stress also exhibited greater reproductive output and decreased survival relative to rural populations experiencing less physiological stress, demonstrating a tradeoff between reproduction and life maintenance processes. Our results suggest that environmental stress may augment life history strategy in this fast-paced species, and that shifts in life history strategy can in turn affect the population at large. Finally, the urban environment poses definite challenges for organisms, and while it appears that side-blotched lizards are adjusting physiologically, it is unknown what fitness costs these physiological adjustments accrue.     

Spatial movements and social networks in juvenile male song sparrows

The time between fledging and breeding is a critical period in songbird ontogeny, but the behavior of young songbirds in the wild is relatively unstudied. The types of social relationships juveniles form with other individuals can provide insight into the process through which they learn complex behaviors crucial for survival, territory establishment, and mate attraction. We used radio telemetry to observe social associations of young male song sparrows (Melospiza melodia) from May to November. Juvenile song sparrows were frequently observed in social flocks and generally associated with more birds in the summer than in the autumn months. Most juvenile subjects formed stable social relationships with other birds and were seen with the same individual on up to 60% of the days observed. The strongest associations occurred with other juvenile males, and these individuals were often seen <1 m from the subject, even when the subject moved large distances between tracking observations. Associations also had long-term behavioral consequences as subjects were more likely to establish territories near their associates and learn shared song types. Our results indicate that male song sparrows spend a large percentage of the juvenile life stage forming social relationships and suggest that these associations may be important for the ecology of young birds and the ontogeny of their behaviors.     

Investment in survival and reproduction along a semelparity–iteroparity gradient in the Beta species complex

The Beta species complex shows a gradient of life histories from pronounced semelparity (big‐bang reproduction) to pronounced iteroparity (repeated reproduction). Models assume a trade‐off between investment in reproduction and survival. Reproductive effort is thought to increase with decreasing life span, and to be invariable in semelparous plants and susceptible to environmental conditions in iteroparous plants. These assumptions and hypotheses were verified by a greenhouse experiment testing six different life cycles at three contrasting nutrient levels. This study suggests that reproductive effort is negatively correlated with mean life span along the life‐cycle gradient. Unlike semelparous beets, reproductive effort in iteroparous beets is extremely sensitive to nutrient level. Phenotypic correlation between allocation to reproduction and allocation to survival generally appeared significantly negative in the longest‐lived iteroparous beets, nonsignificant in intermediate life histories and obviously positive in semelparous beets (no trade‐off control).     

The influence of sex and body size on nestling survival and recruitment in the house sparrow

Differences in the survival rates of males and females over the period from hatching to recruitment can have important impacts on individual fitness and population demographics. However, whilst the influence of an individual's sex on nestling growth and survival has been well studied, less is known about sex‐specific survival over the period between fledging and recruitment. Here, we analyse nestling survival and recruitment in an isolated, island population of house sparrows (Passer domesticus), using data collected over a 4‐year period. Nestlings that had a greater mass at 1 day old were more likely to fledge. Recruitment was also positively associated with day 11 mass. The positive influence of nestling mass on survival to fledging also increased as brood size increased. There was no difference in the survival of male and female individuals prior to fledging. In contrast, over the period from fledging to recruitment, females had significantly less mortality than males. Recruitment was also positively associated with 11‐day‐old mass. Neither the nestling sex ratio nor the fledging sex ratio deviated from 0.5, but the sex ratio amongst recruits was female biased. Our study shows that sex can influence juvenile survival, but also shows that its effect varies between different life‐history stages; therefore, these stages should be considered separately if we want to understand at what point sex‐specific differences in juvenile survival occur. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 680–688.     

Large‐brained birds suffer less oxidative damage

Large brains (relative to body size) might confer fitness benefits to animals. Although the putative costs of well‐developed brains can constrain the majority of species to modest brain sizes, these costs are still poorly understood. Given that the neural tissue is energetically expensive and demands antioxidants, one potential cost of developing and maintaining large brains is increased oxidative stress (‘oxidation exposure’ hypothesis). Alternatively, because large‐brained species exhibit slow‐paced life histories, they are expected to invest more into self‐maintenance such as an efficacious antioxidative defence machinery (‘oxidation avoidance’ hypothesis). We predict decreased antioxidant levels and/or increased oxidative damage in large‐brained species in case of oxidation exposure, and the contrary in case of oxidation avoidance. We address these contrasting hypotheses for the first time by means of a phylogenetic comparative approach based on an unprecedented data set of four redox state markers from 85 European bird species. Large‐brained birds suffered less oxidative damage to lipids (measured as malondialdehyde levels) and exhibited higher total nonenzymatic antioxidant capacity than small‐brained birds, whereas uric acid and glutathione levels were independent of brain size. These results were not altered by potentially confounding variables and did not depend on how relative brain size was quantified. Our findings partially support the ‘oxidation avoidance’ hypothesis and provide a physiological explanation for the linkage of large brains with slow‐paced life histories: reduced oxidative stress of large‐brained birds can secure brain functionality and healthy life span, which are integral to their lifetime fitness and slow‐paced life history.     

Wilson's Storm Petrels Oceanites oceanicus Recognise the Olfactory Signature of Their Mate

Chemical signals in birds have rarely been considered as recognition cues. Nevertheless, recent experiments showed that several petrel species are able to recognize their nest by smell, and in at least one species even their mate. But the use of smell may be different across the petrel species and olfactory nest recognition appears to be dependent on species’ breeding biology. To increase our knowledge of individual olfactory recognition in petrels and the relationships between breeding biology and use of smell, we tested Wilson’s storm petrels Oceanites oceanicus in Antarctica. In previous experiments, these birds failed to home if rendered anosmic, but the method employed to obtain anosmia (potentially stressing birds) and the fact that they breed in 24‐h daylight suggest that they might use visual, rather than olfactory, cues to recognize their nest. Our birds were tested in T‐maze experiments where nest odours or partner odours were presented. Wilson’s storm petrels preferred odours of their own nest and mate. Results on olfactory nest recognition confirm and complete previous results, viz. anosmic Wilson’s storm petrels do not home. Storm petrels olfactory mate recognition suggests that this ability may be widespread in burrowing petrels and implements olfactory nest recognition.     

Antioxidant status in relation to age,condition, reproductive performance and pollution in three passerine species

Oxidative stress has been suggested as a mediator in life‐history trade‐off. By spending more resources on for example reproduction an organism might sacrifice its antioxidant defence. So far, most conclusions on trade‐offs between life‐history traits and oxidative stress have been drawn from laboratory studies using a few model species and there is a need for studies conducted in natural settings. We investigated associations between markers for antioxidant status (antioxidant enzyme activities and antioxidant levels), body condition, age and reproduction in three species of wild‐living passerines. The impact from an anthropogenic stressor (metal pollution) was also assessed. The three bird species showed interspecific variation in their SOD and CAT activities, indicating different pathways to eliminate radicals. The age of females affected both antioxidant status and the breeding performance, indicating the importance of age as a factor in life‐history studies. Old birds had lower levels of antioxidants/antioxidant enzyme activities and they produced larger broods/more successful broods, though the latter might be confounded by surviving females having increased fitness. Metal exposure had a negative impact on breeding, and improved breeding outcome was also associated with increased antioxidant defence, but metal exposure was not directly related to the oxidative status of birds, emphasizing that additional stressors might independently affect the same traits. Our results highlight that caution has to be taken when generalizing and extrapolating results to even closely related species. The results support the idea that there is a cost of reproduction, in terms of increased resources spent on antioxidant defence, though this should be confirmed with experimental studies.     

The relationship between uric acid and its oxidative product allantoin: a potential indicator for the evaluation of oxidative stress in birds

Uric acid is the main nitrogenous waste product in birds but it is also known to be a potent antioxidant. Hominoid primates and birds lack the enzyme urate oxidase, which oxidizes uric acid to allantoin. Consequently, the presence of allantoin in their plasma results from non-enzymatic oxidation. In humans, the allantoin to uric acid ratio in plasma increases during oxidative stress, thus this ratio has been suggested to be an in vivo marker for oxidative stress in humans. We measured the concentrations of uric acid and allantoin in the plasma and ureteral urine of white-crowned sparrows (Zonotrichia leucophrys gambelii) at rest, immediately after 30 min of exercise in a hop/hover wheel, and after 1 h of recovery. The plasma allantoin concentration and the allantoin to uric acid ratio did not increase during exercise but we found a positive relationship between the concentrations of uric acid and allantoin in the plasma and in the ureteral urine in the three activity phases. In the plasma, the slope of the regression describing the above positive relationships was significantly higher immediately after activity. We suggest that the slope indicates the rate of uric acid oxidation and that during activity this rate increases as a result of higher production of free radicals. The present study demonstrates that allantoin is present in the plasma and in the ureteral urine of white-crowned sparrows and therefore might be useful as an indicator of oxidative stress in birds.     

Stress, metabolism, and antioxidants in two wild passerine bird species

Antioxidants protect against free-radical damage, and free radicals, in turn, are thought to underlie aging. Thus, measuring antioxidants may aid field ecologists in understanding the physiological mechanisms that underlie life-history trade-offs. Antioxidant levels are known to vary markedly in response to the stress of capture in many birds. These changes in antioxidants could result from regulation (e.g., by stress-related hormones) or consumption (e.g., by an increase in free radicals due to increased metabolic rate). Here we experimentally test the effect of increased metabolic rate on circulating antioxidant and corticosterone concentrations in two wild passerine bird species, house sparrows (Passer domesticus) and gray catbirds (Dumetella carolinensis). We increased metabolic rate via exposure to low ambient temperatures overnight in captivity and measured circulating antioxidant capacity, uric acid, corticosterone, and oxygen consumption in cold-exposed and control individuals. Both species showed increases rather than decreases in all antioxidant parameters overnight, contradicting a consumption-by-energy-expenditure hypothesis. Both positive and negative correlations between antioxidant response and corticosterone response were occasionally but not consistently present, refuting a generalized regulation-by-corticosterone hypothesis. High baseline uric acid predicted diminished response of corticosterone and all antioxidants. Thus, high uric acid may reflect recent stress, poor condition, or a compensatory response. Relationships among metabolic rate, antioxidants, and corticosterone differed qualitatively between the species.     

The post‐fledging period in a tropical bird: patterns of parental care and survival

How environmental conditions affect the timing and extent of parental care is a fundamental question in comparative studies of life histories. The post‐fledging period is deemed critical for offspring fitness, yet few studies have examined this period, particularly in tropical birds. Tropical birds are predicted to have extended parental care during the post‐fledging period and this period may be key to understanding geographic variation in avian reproductive strategies. We studied a neotropical passerine, the western slaty‐antshrike Thamnophilus atrinucha, and predicted greater care and higher survival during the post‐fledging period compared to earlier stages. Furthermore, we predicted that duration of post‐fledging parental care and survival would be at the upper end of the distribution for Northern Hemisphere passerines. Correspondingly, we observed that provisioning continued for 6–12 weeks after fledging. In addition, provisioning rate was greater after fledging and offspring survival from fledging to independence was 75%, greater than all estimates from north‐temperate passerines. Intervals between nesting attempts were longer when the first brood produced successful fledglings compared to nests where offspring died either in the nest or upon fledging. Parents delayed initiating second nests after the first successful brood until fledglings were near independence. Our results indicate that parents provide greater care after fledging and this extended care likely increased offspring survival. Moreover, our findings of extended post‐fledging parental care and higher post‐fledging survival compared to Northern Hemisphere species have implications for understanding latitudinal variation in reproductive effort and parental investment strategies.     

Attraction of petrels to artificial lights in the Canary Islands: effects of the moon phase and age class

The extent and intensity of artificial night lighting has increased with urban development worldwide. The resulting light pollution is responsible for mortality among many Procellariiformes species which show nocturnal activity on their breeding grounds. Here, we report light‐induced mortality of Procellariiformes during a 9‐year study (1998–2006) on Tenerife, the largest island of the Canary archipelago. A total of 9880 birds from nine species were found grounded, the majority being Cory’s Shearwaters Calonectris diomedea (93.4%). For this species the majority of grounded birds were fledglings (96.4%), which fall apparently while leaving their nesting colony for the first time; for the smaller species (storm‐petrels) adult birds were more often grounded than fledglings. For almost all species, grounding showed a seasonal pattern linked with their breeding cycle. Certain phases of the moon influenced grounding of Cory’s Shearwater, with the extent of grounding being reduced during phases of full moon. The percentage of fledglings attracted to lights in relation to the fledglings produced annually varied between species and years (0–1.3% for the Madeiran Storm‐petrel Oceanodroma castro; 41–71% for Cory’s Shearwater). Mean adult mortality rates also varied between species (from 0.4% for the European Storm‐petrel Hydrobates pelagicus and the Cory’s Shearwater, to 2.3% for the Manx Shearwater Puffinus puffinus). Here we show that light‐induced mortality rates are of concern, at least for petrels and small shearwaters. Thanks to efforts involving civil cooperation, 95% of grounded birds have been returned to the wild. To minimize the impact of artificial lights on petrels we recommend several conservation measures: continuing rescue campaigns, alteration of light signatures and reduction of light emissions during the fledging peaks. Furthermore, we recommend that a monitoring program for petrel populations be implemented, as well as further studies to assess the fate of released fledglings and continued research to address why petrels are attracted to lights.     

Contrasting heterozygosity‐fitness correlations across life in a long‐lived seabird

Selection is a central force underlying evolutionary change and can vary in strength and direction, for example across time and space. The fitness consequences of individual genetic diversity have often been investigated by testing for multilocus heterozygosity‐fitness correlations (HFCs), but few studies have been able to assess HFCs across life stages and in both sexes. Here, we test for HFCs using a 26‐year longitudinal individual‐based data set from a large population of a long‐lived seabird (the common tern, Sterna hirundo), where 7,974 chicks and breeders of known age were genotyped at 15 microsatellite loci and sampled for life‐history traits over the complete life cycle. Heterozygosity was not correlated with fledging or post‐fledging prospecting probabilities, but was positively correlated with recruitment probability. For breeders, annual survival was not correlated with heterozygosity, but annual fledgling production was negatively correlated with heterozygosity in males and highest in intermediately heterozygous females. The contrasting HFCs among life stages and sexes indicate differential selective processes and emphasize the importance of assessing fitness consequences of traits over complete life histories.     

The evolution of life-history traits in parasitic and free-living platyhelminthes: a new perspective

Parasite life histories have been assumed to be shaped by their particular mode of existence. To test this hypothesis, we investigate the relationships between life-history traits of free-living and parasitic platyhelminthes. Using phylogenetically independent contrasts we examine patterns of interspecific covariation in adult size, progeny volume, daily fecundity, total reproductive capacity, age at first reproduction and longevity. The correlations obtained indicate a similar causal chain of life history variations for free-living and parasitic platyhelminthes. These results suggest that increased longevity favours delayed reproduction. Furthermore, growth pattern determines adult body size and age at maturity. For platyhelminthes, whether free-living or parasitic, the total reproductive capacity is found to be directly determined by the size of the worm. Within this group the parasitic way of life does not seem to influence the basic patterns of life history evolution. Received: 20 September 1997 / Accepted: 1 March 1998     

OXIDATIVE DAMAGE INCREASES WITH REPRODUCTIVE ENERGY EXPENDITURE AND IS REDUCED BY FOOD‐SUPPLEMENTATION

A central principle in life‐history theory is that reproductive effort negatively affects survival. Costs of reproduction are thought to be physiologically based, but the underlying mechanisms remain poorly understood. Using female North American red squirrels (Tamiasciurus hudsonicus), we test the hypothesis that energetic investment in reproduction overwhelms investment in antioxidant protection, leading to oxidative damage. In support of this hypothesis we found that the highest levels of plasma protein oxidative damage in squirrels occurred during the energetically demanding period of lactation. Moreover, plasma protein oxidative damage was also elevated in squirrels that expended the most energy and had the lowest antioxidant protection. Finally, we found that squirrels that were food‐supplemented during lactation and winter had increased antioxidant protection and reduced plasma protein oxidative damage providing the first experimental evidence in the wild that access to abundant resources can reduce this physiological cost.     

Do parasites and antioxidant availability affect begging behaviour,growth rate and resistance to oxidative stress?

Early‐life trade‐offs faced by developing offspring can have long‐term consequences for their future fitness. Young offspring use begging displays to solicit resources from their parents and have been selected to grow fast to maximize survival. However, growth and begging behaviour are generally traded off against self‐maintenance. Oxidative stress, a physiological mediator of life‐history trade‐offs, may play a major role in this trade‐off by constraining, or being costly to, growth and begging behaviour. Yet, despite implications for the evolution of life‐history strategies and parent–offspring conflicts, the interplay between growth, begging behaviour and resistance to oxidative stress remains to be investigated. We experimentally challenged wild great tit (Parus major) offspring by infesting nests with a common ectoparasite, the hen flea (Ceratophyllus gallinae), and simultaneously tested for compensating effects of increased vitamin E availability, a common dietary antioxidant. We further quantified the experimental treatment effects on offspring growth, begging intensity and oxidative stress. Flea‐infested nestlings of both sexes showed reduced body mass during the first half of the nestling phase, but this effect vanished short before fledging. Begging intensity and oxidative stress of both sexes were unaffected by both experimental treatments. Feeding rates were not affected by the experimental treatments, but parents of flea‐infested nests fed nestlings with a higher proportion of caterpillars, the main source of antioxidants. Additionally, female nestlings begged significantly less than males in control nests, whereas both sexes begged at similar rates in vitamin E‐supplemented nests. Our study shows that a parasite exposure does not necessarily affect oxidative stress levels or begging intensity, but suggests that parents can compensate for negative effects of parasitism by modifying food composition. Furthermore, our results indicate that the begging capacity of the less competitive sex is constrained by antioxidant availability.     

House sparrow Passer domesticus survival is not associated with MHC‐I diversity,but possibly with specific MHC‐I alleles

The MHC (Major Histocompatibility Complex) plays an important role in the immune system of vertebrates. MHC genes are extremely polymorphic and this variation is considered to be maintained by selection from pathogens. We investigate whether MHC diversity (number of different alleles per individual) affects the survival and recruitment of nestling house sparrows. We hypothesize that individuals with higher MHC diversity can recognize and combat a wider range of pathogens, and therefore are more likely to survive and recruit into the breeding population. Additionally, we hypothesize that specific MHC class I alleles (MHC‐I) could be associated with survival and recruitment. We screened MHC‐I genotypes in 518 house sparrow chicks hatched on Lundy Island but we found no evidence for a relationship between nestling survival, post‐fledging survival or recruitment success with MHC diversity. Then we investigated effects of specific MHC‐I alleles in 195 individuals from a single cohort. Twenty‐one MHC‐I alleles were tested for relationships with nestling survival, post‐fledging survival and recruitment, and we detected associations with survival for three different alleles. This pattern was, however, not different to what would be expected from random, so we could not conclude that particular MHC‐I alleles are associated with survival in house sparrows on Lundy Island. Nonetheless, one of these alleles (1105) showed both a tendency for a higher probability of surviving in nestlings, and a significant association with survival in fledglings. We envision that allele 1105 could be an interesting candidate gene for testing associations with survival in house sparrows in the future.     

Elevational trends in life histories: revising the pace‐of‐life framework

Life‐history traits in birds, such as lifespan, age at maturity, and rate of reproduction, vary across environments and in combinations imposed by trade‐offs and limitations of physiological mechanisms. A plethora of studies have described the diversity of traits and hypothesized selection pressures shaping components of the survival–reproduction trade‐off. Life‐history variation appears to fall along a slow–fast continuum, with slow pace characterized by higher investment in survival over reproduction and fast pace characterized by higher investment in reproduction over survival. The Pace‐of‐Life Syndrome (POLS) is a framework to describe the slow–fast axis of variation in life‐history traits and physiological traits. The POLS corresponds to latitudinal gradients, with tropical birds exhibiting a slow pace of life. We examined four possible ways that the traits of high‐elevation birds might correspond to the POLS continuum: (i) rapid pace, (ii) tropical slow pace, (iii) novel elevational pace, or (iv) constrained pace. Recent studies reveal that birds breeding at high elevations in temperate zones exhibit a combination of traits creating a unique elevational pace of life with a central trade‐off similar to a slow pace but physiological trade‐offs more similar to a fast pace. A paucity of studies prevents consideration of the possibility of a constrained pace of life. We propose extending the POLS framework to include trait variation of elevational clines to help to investigate complexity in global geographic patterns.     

Relationships among oxidative status,breeding conditions and life‐history traits in free‐living Great Tits Parus major and Common Starlings Sturnus vulgaris

The interest shown by ecologists in antioxidants and oxidative stress as potential modulators of life‐history trade‐offs has expanded greatly in recent years. However, we still know very little about natural variation in oxidative damage and antioxidant capacity in free‐living animals. In this study, we describe the natural variation in three components of oxidative balance in nestlings and breeding females in free‐living Great Tits Parus major and Common Starlings Sturnus vulgaris in central Italy, and relate these to breeding conditions and life‐history traits. Our results suggest that there are associations among oxidative physiology, reproductive activity, growth pattern and season in wild birds, but that the nature of these associations might be species‐specific rather than general across species.