Physiological costs and carry-over effects of avian interspecific brood parasitism influence reproductive tradeoffs

Although models of co-evolution between brood parasites and their hosts primarily focus upon the cost to hosts in the current reproductive bout, the impact of brood parasitism may carry over to future reproductive attempts by altering resource allocation. Glucocorticoid stress hormones help mediate resource allocation to reproduction, yet they have rarely been examined in brood parasitic systems. Here we determined if shifts in parental care and corticosterone had carry-over effects on future reproductive effort in the rufous-and-white wren (Thryophilus rufalbus), a host of the Central American striped cuckoo (Tapera naevia). We found that parasitized parents had significantly higher stress-induced, but not baseline, corticosterone than natural parents during the fledgling stage, which was associated with changes in parental care. The high investment in current reproduction while parasitized may be due to the value of fledged chicks in tropical systems. This maladaptive response by parasitized parents was associated with delayed re-nesting and a reduced likelihood of nesting in the subsequent breeding season. Although a reduction in future reproductive effort can result from a combination of factors, this work suggests that fitness costs of brood parasitism are mediated by changes in corticosterone and parental care behavior that carry over into subsequent breeding seasons.     

Timing of current reproduction directly affects future reproductive output in European coots

Life-history theory suggests that the variation in the seasonal timing of reproduction within populations may be explained on the basis of individual optimization. Optimal breeding times would vary between individuals as a result of trade-offs between fitness components. The existence of such trade-offs has seldom been tested empirically. We experimentally investigated the consequences of altered timing of current reproduction for future reproductive output in the European coot (Fulica atra). First clutches of different laying date were cross-fostered between nests, and parents thereby experienced a delay or an advance in the hatching date. The probability and success of a second brood, adult survival until and reproduction in the next season were then compared to the natural variation among control pairs. Among control pairs the probability of a second brood declined with the progress of season. Delayed pairs were less likely and advanced pairs were more likely to produce a second brood. These changes were quantitatively as predicted from the natural seasonal decline. The number of eggs in the second clutch was positively related to egg number in the first clutch and negatively related to laying date. Compared to the natural variation, delayed females had more and advanced females had fewer eggs in their second clutch. The size of the second brood declined with season, but there was no significant effect of delay or advance. Local adult survival was higher following a delay and reduced following an advance. The effect of the experiment on adult survival was independent of sex. Laying date and clutch size of females breeding in the next year were not affected by treatment. The study demonstrates the existence of a trade-off between increased probability of a second brood and decreased parental survival for early breeding. Timing-dependent effects of current reproduction on future reproductive output may thus play an important role in the evolution of the seasonal timing of reproduction.     

Trade-off between current reproductive effort and delay to next reproduction in the leatherback sea turtle

The trade-off between current and future reproduction plays an important role in demographic analyses. This can be revealed by the relationship between the number of years without reproduction and reproductive investment within a reproductive year. However, estimating both the duration between two successive breeding season and reproductive effort is often limited by variable recapture or resighting effort. Moreover, a supplementary difficulty is raised when nonbreeder individuals are not present sampling breeding grounds, and are therefore unobservable. We used capture–recapture (CR) models to investigate intermittent breeding and reproductive effort to test a putative physiological trade-off in a long-lived species with intermittent breeding, the leatherback sea turtle. We used CR data collected on breeding females on Awa:la-Ya:lima:po beach (French Guiana, South America) from 1995 to 2002. By adding specific constraints in multistate (MS) CR models incorporating several nonobservable states, we modelled the breeding cycle in leatherbacks and then estimated the reproductive effort according to the number of years elapsed since the last nesting season. Using this MS CR framework, the mean survival rate was estimated to 0.91 and the average resighting probability to 0.58 (ranged from 0.30 to 0.99). The breeding cycle was found to be limited to 3 years. These results therefore suggested that animals whose observed breeding intervals are greater than 3 years were most likely animals that escaped detection during their previous nesting season(s). CR data collected in 2001 and 2002 allowed us to compare the individual reproductive effort between females that skipped one breeding season and females that skipped two breeding seasons. These inferences led us to conclude that a trade-off between current and future reproduction exists in leatherbacks nesting in French Guiana, likely linked to the resource provisioning required to invest in reproduction.     

Reproduction and modulation of the stress response: an experimental test in the house sparrow

The stress response is highly variable among individuals, but the causes of this variation remain largely unknown. In response to stressors, vertebrates secrete elevated levels of glucocorticoids which enhance survival, but concurrently interfere with reproduction. We tested the hypothesis that individuals flexibly modulate their stress response with respect to the reproductive value of their brood in free-living house sparrows (Passer domesticus). We experimentally increased or decreased clutch size during the nestling period and found that parents tending enlarged clutches responded less strongly to a stressor than those tending reduced clutches. In addition, we examined whether individuals responded less strongly to a stressor as the breeding season progressed and future reproductive opportunities declined. We found that the stress response decreased with breeding date during the birds' first breeding attempt, but it remained constant during their second breeding attempt. Within-individual variability in the stress response was related to the brood size manipulations the birds received in their two consecutive breeding attempts. These results provide the first experimental support for the hypothesis that individuals actively modulate their stress response with respect to the value of current reproduction.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

Experimentally delayed hatching triggers a magnified stress response in a long-lived bird

In birds, the timing of breeding is a key life-history trait with crucial fitness consequences. We predicted that parents may value a brood less if it hatched later than expected, thereby decreasing their parental effort. In addition, breeding effort would be further modulated by the age-specific decline of future breeding opportunities. We experimentally investigated whether snow petrels, Pagodroma nivea, were less committed to care for a chick that hatched later than expected. The timing of hatching was manipulated by swapping eggs between early and late known-age pairs (7-44 years old), and investigations on hormonal and behavioral adjustments were conducted. As a hormonal gauge of parental commitment to the brood, we measured the corticosterone stress response of guarding adults. Indeed, an acute stress response mediates energy allocation towards survival at the expense of current reproduction and is magnified when the current brood value is low, as it is expected to be in young and/or delayed parents. As predicted, egg desertion and the magnitude of the stress response was stronger in delayed pairs compared to control ones. However, the treatment did not decrease the length of the guarding period, chick condition and chick survival. In addition, old parents resisted stress better (lower stress-induced corticosterone levels) than young ones. Our study provides evidence that snow petrels, as prudent parents, may value a brood less if it hatched later than expected. Thus, in long-lived birds, the responsiveness to stressors appeared to be adjusted according to the individual prospect of future breeding opportunities (age) and to the current brood value (timing of breeding).     

Prolactin stress response does not predict brood desertion in a polyandrous shorebird

One of the fundamental principles of the life-history theory is that parents need to balance their resources between current and future offspring. Deserting the dependent young is a radical life-history decision that saves resources for future reproduction but that may cause the current brood to fail. Despite the importance of desertion for reproductive success, and thus fitness, the neuroendocrine mechanisms of brood desertion are largely unknown. We investigated two candidate hormones that may influence brood desertion in the Kentish plover Charadrius alexandrinus: prolactin ('parental hormone') and corticosterone ('stress hormone'). Kentish plovers exhibit an unusually diverse mating and parental care system: brood desertion occurs naturally since either parent (the male or the female) may desert the brood after the chicks hatch and mate with a new partner shortly after. We measured the hormone levels of parents at hatching using the standard capture and restraint protocol. We subsequently followed the broods to determine whether a parent deserted the chicks. We found no evidence that either baseline or stress-induced prolactin levels of male or female parents predicted brood desertion. Although stress-induced corticosterone levels were generally higher in females compared with males, individual corticosterone levels did not explain the probability of brood desertion. We suggest that, in this species, low prolactin levels do not trigger brood desertion. In general, we propose that the prolactin stress response does not reflect overall parental investment in a species where different parts of the breeding cycle are characterized by contrasting individual investment strategies.     

Baseline and stress-induced levels of corticosterone during different life cycle substages in a shorebird on the high arctic breeding grounds

After a migratory flight of several thousand kilometers to their high arctic breeding grounds, red knots (Calidris canutus islandica, Scolopacidae) showed high baseline concentrations of plasma corticosterone (58 ng/mL). Such high baseline corticosterone levels may be conditional for the right behavioral and metabolic adjustments to environmental and social stresses that shorebirds experience on arrival in an unpredictable tundra breeding environment. Despite the high baseline levels of corticosterone, red knots still showed a marked stress response during the postarrival period, with corticosterone concentrations increasing significantly during a 60-min period of confinement. Baseline levels of corticosterone declined as the breeding season progressed. Red knots with brood patches, that is, birds that had completed egg laying and commenced incubation, had a reduced adrenocortical response to the stress of confinement compared with red knots with no, or with half-developed, brood patches. This is consistent with the idea that birds breeding in extreme environments with short breeding seasons may exhibit a decreased adrenocortical response to stressful events to prevent high corticosterone concentrations from inducing interruptions of reproductive behavior.     

Corticosterone manipulation reveals differences in hierarchical organization of multidimensional reproductive trade-offs in r-strategist and K-strategist females

Life history trade-offs are often hierarchical with decisions at one level affecting lower level trade-offs. We investigated trade-off structure in female side-blotched lizards (Uta stansburiana), which exhibit two evolved strategies: yellow-throated females are K-strategists and orange-throated are r-strategists. Corticosterone treatment was predicted to differentially organize these females' reproductive decisions. Corticosterone-treated yellow females suppressed reproduction but survived well, and augmented egg mass without decreasing clutch size. Conversely, corticosterone enhanced mortality and reproductive rates in orange females, and increased egg mass only after lengthy exposure. Corticosterone did not affect post-laying condition, suggesting that corticosterone increased egg mass through enhanced energy acquisition (income breeding). Corticosterone enhanced survival of lightweight females, but decreased survival of heavy females, introducing a foraging vs. predation trade-off. We conclude that rather than being a direct, functional relationship, observed trade-offs between offspring size and number represent evolved differences in hierarchical organization of multidimensional trade-offs, particularly in response to stress.     

Offspring pay sooner,parents pay later: experimental manipulation of body mass reveals trade-offs between immune function,reproduction and survival

Introduction

Life-history theory predicts that organisms trade off survival against reproduction. However, the time scales on which various consequences become evident and the physiology mediating the cost of reproduction remain poorly understood. Yet, explaining not only which mechanisms mediate this trade-off, but also how fast or slow the mechanisms act, is crucial for an improved understanding of life-history evolution. We investigated three time scales on which an experimental increase in body mass could affect this trade-off: within broods, within season and between years. We handicapped adult skylarks (Alauda arvensis) by attaching extra weight during first broods to both adults of a pair. We measured body mass, immune function and return rates in these birds. We also measured nest success, feeding rates, diet composition, nestling size, nestling immune function and recruitment rates.

Results

When nestlings of first broods fledged, parent body condition had not changed, but experimental birds experienced higher nest failure. Depending on the year, immune parameters of nestlings from experimental parents were either higher or lower than of control nestlings. Later, when parents were feeding their second brood, the balance between self-maintenance and nest success had shifted. Control and experimental adults differed in immune function, while mass and immune function of their nestlings did not differ. Although weights were removed after breeding, immune measurements during the second brood had the capacity to predict return rates to the next breeding season. Among birds that returned the next year, body condition and reproductive performance a year after the experiment did not differ between treatment groups.

Conclusions

We conclude that the balance between current reproduction and survival shifts from affecting nestlings to affecting parents as the reproductive season progresses. Furthermore, immune function is apparently one physiological mechanism involved in this trade-off. By unravelling a physiological mechanism underlying the trade-offs between current and future reproduction and by demonstrating the different time scales on which it acts, our study represents an important step in understanding a central theory of life-history evolution.

     

Constraints on, and determinants of, the annual number of breeding attempts in the multi-brooded Black Redstart Phoenicurus ochruros

With reference to models predicting patterns of reproduction in multi-brooded species, I analysed some of the factors potentially affecting the number of breeding attempts per season made by female Black Redstarts Phoenicurus ochruros in the central Swiss Alps. The maximum number of successful broods per female per season was three, the median two. The proportion of females initiating only a single clutch per season varied from 16 to 58% over 10 years. Variation in the frequency of single brooding between years was positively related to the date of the onset of breeding. Egg-laying started after a temperature-related threshold value was crossed in April. Females frequently re-nested before fledglings of the previous brood were independent. Short interbrood intervals were associated with triple brooding. The interbrood interval shortened during the breeding season. Intra-individual variation in the number of breeding attempts per season was partitioned according to female age, laying date of the season's first egg (standardized in relation to the median date of first laying within a year) and the occurrence of breeding failures before the ultimate nesting attempt. However, mortality during the season often terminated breeding early, in particular among novice breeder females. Seasonal reproductive success increased linearly with each additional breeding attempt. The productivity of a breeding attempt was independent of the time in the season. Increased reproductive effort affected neither current or future survival nor reproduction of females. The reproductive patterns and trade-offs in multi-brooded Black Redstarts contrast in many aspects with those found in single-brooded species. They are in accordance with models predicting that multi-brooded species are selected to start breeding as early as possible, continue breeding for as long as conditions are suitable, and save time by overlapping broods.     

Cascading costs of reproduction in female house wrens induced to lay larger clutches

In many species, females produce fewer offspring than they are capable of rearing, possibly because increases in current reproductive effort come at the expense of a female's own survival and future reproduction. To test this, we induced female house wrens (Troglodytes aedon) to lay more eggs than they normally would and assessed the potential costs of increasing cumulative investment in the three main components of the avian breeding cycle – egg laying, incubation and nestling provisioning. Females with increased clutch sizes reared more offspring in the first brood than controls, but fledged a lower proportion of nestlings. Moreover, nestlings of experimental females were lighter than those of control females as brood size and prefledging mass were negatively correlated. In second broods of the season, when females were not manipulated, experimental females laid the same number of eggs as controls, but experienced an intraseasonal cost through reduced hatchling survival and a lower number of young fledged. Offspring of control and experimental females were equally likely to recruit to the breeding population, although control females produced more recruits per egg laid. The reproductive success of recruits from broods of experimental and control females did not differ. The manipulation also induced interseasonal costs to future reproduction, as experimental females had lower fecundity than controls when breeding at least 2 years after having their reproductive effort experimentally increased. Finally, females producing the modal clutch size of seven eggs in their first broods had the highest lifetime number of fledglings.     

Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers.

Why do some parents care for their young whereas others divorce from their mate and abandon their offspring? This decision is governed by the trade-off between the value of the current breeding event and future breeding prospects. In the precocial Kentish plover Charadrius alexandrinus females frequently, but not always, abandon their broods to be cared for by their mate, and seek new breeding partners within the same season. We have shown previously that females'' remating opportunities decline with date in the season, so brood desertion should be particularly favourable for early breeding females. However, the benefits are tempered by the fact that single-parent families have lower survival expectancies than those where the female remains to help the male care for the young. We therefore tested the prediction that increasing the value of the current brood (by brood-size manipulation) should increase the duration of female care early in the season, but that in late breeders, with reduced remating opportunities, desertion and thus the duration of female care should be independent of current brood size. These predictions were fulfilled, indicating that seasonally modulated trade-offs between current brood value and remating opportunities can be important in the desertion decisions of species with flexible patterns of parental care.     

Reproduction in shark-attacked sea turtles is supported by stress-reduction mechanisms

Vertebrates exhibit varied behavioural and physiological tactics to promote reproductive success. We examined mechanisms that could enable female loggerhead turtles to undertake nesting activities and maintain seasonal reproduction despite recent shark injuries of varying severity. We proposed that endocrinal mechanisms that regulate both a turtle's stress response and reproductive ability are modified to promote successful and continued reproduction. Irrespective of the degree of injury, females did not exhibit increased levels of the stress hormone corticosterone, nor decreased levels of the reproductive steroid testosterone; hormone responses consistent with stress. When exposed to a capture stressor, females with shark injury did not exhibit any greater corticosterone response than controls. In addition, breeding females showed a reduced corticosterone stress response compared to non-breeding females. Reduced endocrinal responses following shark injury, and during breeding in general may, in part, enable females to maintain behavioural and physiological commitment to reproduction.     

Adverse foraging conditions may impact body mass and survival of a high Arctic seabird

Tradeoffs between current reproduction and future survival are widely recognized, but may only occur when food is limited: when foraging conditions are favorable, parents may be able to reproduce without compromising their own survival. We investigated these tradeoffs in the little auk (Alle alle), a small seabird with a single-egg clutch. During 2005-2007, we examined the relationship between body mass and survival of birds breeding under contrasting foraging conditions at two Arctic colonies. We used corticosterone levels of breeding adults as a physiological indicator of the foraging conditions they encountered during each reproductive season. We found that when foraging conditions were relatively poor (as reflected in elevated levels of corticosterone), parents ended the reproductive season with low body mass and suffered increased post-breeding mortality. A positive relationship between body mass and post-breeding survival was found in one study year; light birds incurred higher survival costs than heavy birds. The results of this study suggest that reproducing under poor foraging conditions may affect the post-breeding survival of long-lived little auks. They also have important demographic implications because even a small change in adult survival may have a large effect on populations of long-lived species.     

Male eastern bluebirds trade future ornamentation for current reproductive investment

Life-history theory proposes that organisms must trade-off investment in current and future reproduction. Production of ornamental display is an important component of reproductive effort that has rarely been considered in tests of allocation trade-offs. Male eastern bluebirds (Sialia sialis) display brilliant ultraviolet-blue plumage that is correlated with mate acquisition and male competitive ability. To investigate trade-offs between current reproductive effort and the future expression of a sexually selected ornament, we manipulated the parental effort of males by changing their brood sizes. We found that parents provisioned experimentally enlarged broods more often than reduced broods. As predicted by life-history theory, the change in parental effort had a significant effect on the relative plumage ornamentation of males in the subsequent year: males with reduced broods significantly increased in plumage brightness. Moreover, this change in plumage coloration had a direct effect on the timing of breeding in the following season: males that displayed brighter plumage in the year following the manipulation mated with females that initiated egg laying earlier in the season. These data indicate that male bluebirds must trade-off conserving energy for production of future ornamentation versus expending energy for current reproduction.     

Brood size manipulations within the natural range did not reveal intragenerational cost of reproduction in the Willow Tit Parus montanus

To test for the existence of a reproductive cost, we manipulated brood sizes (-2 and +2 nestlings) over 6 years in a northern population of Willow Tits Parus montanus breeding in natural holes. Possible effects were sought in subsequent survival and fecundity of the parents. Parents given extra chicks made more feeding visits than did parents with reduced and control broods. However, this was not reflected in differences in parental body-weight between groups at the end of the nestling period. Brood size manipulation did not significantly affect female or male survival. In 4 out of 6 years, there was a weak and nonsignificant effect on male survival, consistent with a cost of reproduction. Female and male fecundity in the year following the experiment was not affected by the manipulations. Thus, the data do not give evidence of an intragenerational cost of reproduction in the Willow Tit. Parents appeared unwilling to increase their breeding effort to a level which jeopardized their own survival or future breeding success. It is possible that, because of the time constraints in northern latitudes, females work under their capacity and lay smaller clutches than would otherwise be most profitable. Thus, no costs to the parents would be expected as a consequence of manipulations. These results suggest that the current reproductive rate is not maintained by reproductive cost in the Willow Tit. However, the results do not rule out the possibility that selection has operated outside the current range of reproductive rates during evolutionary history of the species.     

Seasonal variation in hormonal responses of timber rattlesnakes (<Emphasis Type="Italic">Crotalus horridus</Emphasis>) to reproductive and environmental stressors

Data addressing adrenocortical modulation across taxonomic groups are limited, especially with regard to how female reproductive condition influences the sensitivity of the hypothalamus–pituitary–adrenal axis. We investigated seasonal and reproductive variation in basal and stress-induced hormone profiles in a population of free-ranging timber rattlesnakes (Crotalus horridus) in north-central Pennsylvania during spring (i.e., May), summer (i.e., July), and early fall (i.e., September). Baseline corticosterone concentrations varied seasonally and were significantly lower during the summer sampling period in July. We observed a significant negative relationship between baseline corticosterone and testosterone in male snakes, while baseline corticosterone and estradiol tended to be positively correlated in females. Treatment of snakes with 1 h of capture stress significantly increased corticosterone across all seasons. However, there was a significant interaction between corticosterone responses to capture stress and season, suggesting that adrenocortical function is modulated seasonally. Because elevated corticosterone may be associated with reproduction, we asked whether hormonal stress responses vary with female reproductive condition. Although sample sizes are low, reproductive snakes had significantly higher baseline and stress-induced corticosterone concentrations than non-reproductive or post-parturient females. Further, despite similar baseline corticosterone concentrations between non-reproductive and post-parturient rattlesnakes, post-parturient females responded to capture stress with a significantly higher increase in corticosterone. Collectively, these data suggest that the sensitivity of the hypothalamus–pituitary–adrenal axis varies both seasonally and with changing reproductive states.     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

THE EFFECT OF BIRTH DATE ON FITNESS OF FEMALE DWARF PERCH,MICROMETRUS MINIMUS (PERCIFORMES: EMBIOTOCIDAE)

Lifetime reproductive success may vary considerably with birth date. I measured phenotypic selection on female birth date in a viviparous teleost fish (Embiotocidae: Micrometrus minimus) by sampling birth-date cohorts over time in Tomales Bay, California. Four episodes of selection were measured: survival from birth to first reproduction, reproductive success in the first breeding season, survival to second reproduction, and reproductive success in the second season. Birth date had a significant impact on fitness in the first two episodes. Early born females were more successful in their first breeding season than late born females (directional selection on birth date), but early born females were less likely to survive the period between birth and first reproduction, relative to females born in the middle of the season (stabilizing selection on birth date). The final two episodes of selection had no detectable effect on birth date. Because of the relationship between birth date and survival in the first year, overall selection on female birth date was stabilizing.