Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses

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Abstract

Physiological mechanisms mediating carryover effects, wherein events or activities occurring in one season, habitat, or life-history stage affect important processes in subsequent life-history stages, are largely unknown. The mechanism most commonly invoked to explain carryover effects from migration centres on the acquisition and utilization of resources (e.g. body mass, or individual ‘condition’). However, other mechanisms are plausible, e.g. trade-offs reflecting conflict or incompatibility between physiological regulatory systems required for different activities or life-history stages (migration vs. reproduction). Here we show that in female black-browed albatrosses (Thalassarche melanophris) the decision to reproduce or to defer reproduction, made prior to their arrival at breeding colonies after long-distance migration, is associated with condition-related (body mass, hematocrit, hemoglobin concentrations) and hormonal (progesterone, testosterone, estrogen-dependent yolk precursors) traits. In contrast, reproductive success showed little association with condition but showed significant associations with the steroidogenic processes underlying follicle development. Specifically, success was determined by reproductive readiness via differences in steroid hormones and hormone-dependent traits. Successful albatrosses were characterized by high progesterone and high estradiol-dependent yolk precursor levels, whereas failed albatrosses had high testosterone and low yolk precursor levels. Results are discussed with reference to migratory carryover effects and how these can differentially affect the physiologies influencing reproductive decisions and reproductive success.

Highlights

► Breeding decisions and success are influenced by two different mechanisms in female albatrosses. ► Upon arrival at a breeding colony females had already decided whether or not to breed. ► Breeding deferral was condition and hormone dependent with low body mass, hematocrit, and P4. ► Breeding success however was not related to condition but to disruption of E2 vitellogenic pathways.

Introduction

An ever-increasing number of studies are documenting the existence of carryover effects in animal populations, wherein events or activities occurring in one season, habitat, or life-history stage affect important processes at subsequent stages (see reviews by [16], [25]). The majority of studies examining carryover effects have examined the influence of over-wintering and migratory experiences on aspects of reproduction including breeding decisions, timing of reproduction, reproductive output, and in some cases reproductive success [16]. However, despite the growing number of studies examining these phenomena, our understanding of the physiological and hormonal mechanisms driving carryover effects remains rudimentary.

In migratory animals, the mechanism most commonly invoked to explain carryover effects on reproduction centres on the acquisition and utilization of resources, i.e. differences in individual condition. Under such a model, the events and activities occurring at the transition from the migratory non-breeding period in winter to spring breeding can “carry over” to affect patterns of resource acquisition and utilization which directly determine reproductive success [2], [16], [20], [23], [24], [28]. Some studies show links between individual condition at arrival and aspects of reproduction (laying date and egg size), but individual variation in these traits tends to be high and their direct effects on reproductive success are currently largely speculative (but see [11]). As an alternative hypothesis, there is growing evidence that endocrine processes themselves might mediate carryover effects to influence reproductive decisions. For example, Goutte et al. [13] showed that in an annually-breeding seabird, elevated baseline corticosterone levels during the pre-laying period after migration were associated with a higher probability of deferred breeding, and speculated that elevated corticosterone might inhibit luteinizing hormone (LH) and the downstream secretion of sex-steroids necessary for reproduction. Other studies have shown that non-breeding or deferring birds are fully capable of elevating LH, when presented with a luteinizing hormone releasing hormone (LHRH) challenge, but they do not or cannot sustain gonadal steroid production [5], [14], [15]. These studies suggest that the metabolic demands of migration might down-regulate the reproductive axis in terms of gonadal steroid production, an effect that might be mediated by, or simply correlated with, elevated corticosterone levels and/or inhibition of LH. Few studies have considered individual variation in circulating gonadal steroids at arrival in migratory birds in relation to subsequent reproduction. Furthermore, the studies cited above only considered breeding decisions as breeding/not breeding (all-or-none decisions), and did not extend the analysis of hormonal patterns at arrival to consider the consequence of the decision to breed in terms of success or failure. Recently, Crossin et al. [8] showed that migratory carryover effects can place constraints on the estrogen-dependent production of yolk precursors by egg-producing females, with negative effects on egg sizes, and that these effects are unrelated to variation in individual condition. However, the functional significance of reduced or constrained sex-steroid production, during the migration-reproduction transition, to reproductive success remains largely unknown. Nevertheless, what is emerging is the recognition that condition (or resource state) at arrival need not be the only mechanism affecting reproductive success. The endocrine processes controlling female reproduction may be directly affected by migratory carryover effects, via constraints on, or incompatibilities between, competing physiological regulatory systems [8], [17], [37].

Procellariiforme seabirds (the albatrosses and petrels) are pelagic species which also make good models for exploring the effects of migratory activity on the hormonal processes underlying reproduction. Like many seabirds, the Procellariiformes have a slow life-history characterized by delayed age of reproduction, a single-egg clutch, prolonged parental care, and longevity, and they make very long, pelagic migrations during a non-breeding period which lasts 6–16 months in Thalassarche spp. [9], [26]. Among breeding-age albatrosses and petrels, there is typically a high proportion of non-breeding individuals, and among even the most experienced breeders, breeding deferral for one or more years is a common tactic underlying lifetime fitness [27], [36]. The annual breeding pattern of black-browed albatrosses (Thalassarche melanophris) make this species a particularly tractable model for the study of carryover effects. Each year, black-browed albatrosses return to breeding colonies from distant foraging areas occupied during the non-breeding period [26], and in the weeks preceding arrival, birds are presumably balancing their own physiological requirements against those needed for the initiation of reproduction. Upon arrival at breeding colonies, they then experience one of three inevitable outcomes: they will defer reproduction entirely until the next season, or they will lay and then either fail or succeed at fledging a chick [26].

In this study, we investigate the physiological mechanisms that mediate reproductive decisions (breeding or deferral) and reproductive outcomes (success or failure) in female black-browed albatrosses during the transition between winter migration and spring breeding. Specifically we consider condition or resource-related traits (mass, hematology), as well as the steroidogenic hormones and estrogen-dependent yolk precursor pathways underlying reproductive readiness (sensu [8]), in mediating decisions and outcomes. We predicted that the decision to lay or to defer would be condition-dependent, and that females deferring reproduction would be in poorer condition (low body mass, low hematocrit [Hct] and hemoglobin [Hb] concentrations) relative to breeding females. However, we also predicted that reproductive success (e.g. fledging of chicks) might reflect differences in “reproductive readiness” upon arrival at the colony, as indicated by the estrogen-dependent production of the yolk precursors vitellogenin [VTG] and yolk-targeted very low density lipoprotein [VLDLy], as well as by patterns of production of the reproductive steroid hormones progesterone [P4] and testosterone [T].

Section snippets

Study site and field sampling protocol

Fieldwork was conducted during the austral summer beginning in September 2008 at a large long-term demographic study-colony of black-browed albatrosses (Colony J) breeding on Bird Island, South Georgia (54°01′S, 38°02′W). Research was conducted through permits issued by the British Antarctic Survey, and conformed to guidelines established by the Canadian Council on Animal Care (Simon Fraser University Animal Care Permit # 897B-8).

Beginning in late September when black-browed albatrosses return

Results

Female black-browed albatrosses in this study returned to the breeding colony on 10–17 October 2008, which is consistent with data from previous years (e.g. [26]). Of the 33 females that we sampled, 8 deferred reproduction entirely, 8 laid eggs which either failed to hatch (N = 5), or hatched but failed shortly thereafter (N = 3), and 17 fledged chicks successfully. Mean dates of egg-laying occurred approximately 15 days after arrival (range 8–18 days), with a median lay-date of 26 October. Based on

Discussion

In this study we show that after long-distance migrations to a breeding colony, reproductive decisions (breeding or deferring) and reproductive outcome (successful or failed) in female black-browed albatrosses are associated with marked differences in patterns of circulating gonadal steroids (P4, T) and steroid-dependent traits (yolk precursors). Previous studies of black-browed albatrosses have shown that all breeding-age females generally return to colonies at the start of the breeding

Conclusion

We present data which suggest that migratory carryover effects can impact two very different aspects of reproductive effort. In the short term, carryover effects constraining the acquisition of resources and body condition during the pre-breeding period mediated the trade-off between current and future reproductive investment (e.g. breeding decision), via hormonal mediators. However, for females deciding to initiate reproduction, the steroidogenic processes underlying yolk precursor production

Acknowledgments

We extend thanks to Fabrice Le Bouard for logistical support, Stacey Adlard, Ewan Edwards, and Jaume Forcada for field support, to Lea Bond for laboratory support, and to Andy Wood for data support. Financial support was provided by the British Antarctic Survey through an Antarctic Funding Initiative Collaborative Gearing Scheme awarded to AD, PNT, and RAP. Additional support was provided through a National Science and Engineering Research Council of Canada (NSERC) Post-doctoral Fellowship, and

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