The effects of variable foraging conditions on common murre (Uria aalge) corticosterone concentrations and parental provisioning
Introduction
In many seabird species, biparental care is necessary for the successful rearing of offspring (Jones et al., 2002). When parental workload is shared, both pair members must balance required investments against energetic costs so that neither partner’s body condition declines to the point that either has to abandon the breeding attempt to preserve itself (Jones et al., 2002). An optimal investment balance between the requirements for parent and offspring maintenance may be particularly difficult to achieve when foraging conditions are poor, as parental strategies may have to be modified to suit the changing environment (Cairns, 1987, Monaghan et al., 1994, Wilhelm et al., submitted for publication). Previous studies indicate that stress hormone levels rise when food availability decreases (Harvey et al., 1984, Scott et al., 1983, Clinchy et al., 2004, Kitaysky et al., 1999) and elevated corticosterone levels are associated with higher frequencies of provisioning young (Carlson et al., 2006). Adult black-legged kittiwakes (Rissa trydactyla) with corticosterone implants increased their chick-provisioning rates and corticosterone-implanted chicks begged more often than controls (Kitaysky et al., 2001). It remains unclear, however, exactly how diffferent concentrations of these hormones mediate the effects of prey availability on parental workload. Common murres are an excellent study species for testing hypotheses about the costs of biparental care decisions in a changing environment as this species exhibits high levels of biparental investment, multi-year pair bonds with little nest site movement, and they are subject to prey base fluctuations within and across breeding seasons.
Common murres are monogamous alcid seabirds that nest in dense colonies on open cliff ledges. Group defense resulting from continuous attendance by at least one parent at each nest site reduces egg and chick predation (Ainley et al., 2002, Wilhelm and Storey, 2002). Male and female murres take turns brooding and provisioning (bringing one fish per trip) the single chick produced each season (Ainley et al., 2002). Capelin (Mallotus villosus) is the major forage species for common murres in Newfoundland colonies (Burger and Piatt, 1999, Davoren and Montevecchi, 2003, Wilhelm and Storey, 2004), and murres appear to synchronize their breeding in relation to the date of the capelin’s inshore arrival from the previous year (Regular et al., in preparation). When the inshore arrival of spawning capelin coincides with the chick-hatching period (prey match year), murres are able to find enough food to provision themselves and their chicks. In these years, parental co-attendance at the nest site is high (Cairns, 1987, Uttley et al., 1994, Zador and Piatt, 1999).
When prey availability decreases, or the capelin’s inshore arrival occurs after the onset of chick hatching (prey mismatch year), parental time budgets change (Cairns, 1987, Monaghan et al., 1994, Uttley et al., 1994, Bryant et al., 1999, Zador and Piatt, 1999, Gill et al., 2002, Wilhelm et al., submitted for publication). Adults increase their foraging effort (Bryant et al., 1999, Davoren and Montevecchi, 2003, Wilhelm et al., submitted for publication) and spend less time together at the nest site (Cairns, 1987, Uttley et al., 1994). Murres also suffer greater body mass loss compared to prey match years (Wilhelm, 2004), likely due to the high energetic demands of increased diving (Croll and McLaren, 1993) and flight, another energetically costly activity for these high wing-loaded seabirds (Greenwalt, 1962, Gabrielsen, 1996).
In prey mismatch years, some murres may be more able than others to increase their parental effort. In this species, where care by both parents is essential, these higher quality individuals should compensate for their mates when possible, allowing their lower quality partners to bring fewer fish to the young (as suggested in Jones et al., 2002). If high-quality birds are forced to compensate for their mates over too long a period, however, they may desert or divorce their long-term partners and re-pair with higher quality widowed neighbors. The lower quality, divorced birds subsequently have severely reduced re-pairing and reproductive success (Moody et al., 2005). Thus, the parental responsibilities of each bird to feed and brood the chick, to maintain its own and its mate’s body condition, and to work hard enough to uphold its long-term pair bond combine to make the chick-rearing period highly energetically demanding for common murres.
Reduced food availability (Harvey et al., 1984, Scott et al., 1983, Vleck et al., 2000, Clinchy et al., 2004), unstable or unfavorable breeding conditions (Kitaysky et al., 1999, Kitaysky et al., 2001, Bears et al., 2003), certain breeding stages (depending on species, Lormee et al., 2003, Adams et al., 2005), and increases in adult workload (Kitaysky et al., 1999, Kitaysky et al., 2001, Reneerkens et al., 2002) are all associated with increased serum corticosterone concentrations or differences in corticosterone responsiveness. Corticosterone, an adrenal hormone synthesized from cholesterol, is the primary glucocorticoid in birds (Holmes and Phillips, 1976). It is secreted in response to various physiological and psychological stressors (Harvey et al., 1984). In the short-term, corticosterone stimulates increased foraging behavior and locomotor activity, helps to mobilize stored lipids and proteins, and affects behavioral and physiological responses to challenges to an individual’s energy demands (Sapolsky, 1987, Astheimer et al., 1992, Wingfield, 1994, Wingfield et al., 1997, Belthoff and Dufty, 1998, Marra and Holberton, 1998). In addition, serum concentrations of corticosterone often correlate with behaviors associated with the care of offspring, such as feeding and nest-site attendance (Kitaysky et al., 2001, Bears et al., 2003, Carlson et al., 2006), suggesting that corticosterone may mediate these behaviors. It should be noted, however, that these short-term elevations differ significantly from chronically increased levels, which are typically detrimental to an organism’s physical condition (Harvey et al., 1984, Sapolsky, 1987, Wingfield, 1994) and reproductive output (Silverin, 1986, Wingfield, 1994).
This study examines the relationships between parental provisioning and serum corticosterone concentrations in the same individually color-banded common murres observed during years with considerable variation in prey availability. In examining the behavioral and physiological responses of common murres to changes in the prey resource base, we predict that corticosterone levels will be higher in the year of prey scarcity than in either of the years when prey was more abundant. Further, we predict that birds who feed chicks at higher rates when food is scarce will have elevated corticosterone levels compared to those individuals who provide fewer chick feeds.
Section snippets
Study animals and site
Blood samples and behavioral and mass data were collected from June 1998 to August 2000 from a high-density nesting group of the same individually color-banded breeding common murres (Uria aalge). The focal group of 30 pairs nested on a broad ledge (1.6 m × 2.5 m) located on Great Island, in the Witless Bay Ecological Reserve, Newfoundland and Labrador, Canada (47° 11′N, 52° 49′W). Continuous observations, beginning at dawn and ending at dusk, were made through a one-way glass window in a wooden
Sampling time and corticosterone concentrations
Blood spot corticosterone concentrations were not related to sampling time when sampling occurred within 3 min (r = 0.122, P = 0.736, regression F = 0.122, P = 0.736, intercept, 80.295, slope, − 0.025, Fig. 1a). The relationship was still not significant for birds sampled within approximately 6 min (r = 0.110, P = 0.698, regression F = 0.158, P = 0.698, intercept, 76.713, slope, 0.010, Fig. 1b). Blood spot corticosterone concentrations were significantly affected by sampling time when the regression also
Sampling time and corticosterone concentrations
We found no significant relationship between sampling time and corticosterone concentration for samples taken within 3 min, suggesting that these are baseline levels. These results agree with previous findings (Wingfield et al., 1982, Wingfield et al., 1992, Kitaysky et al., 1999). Corticosterone concentrations of murres sampled at approximately 2 and 6 min after capture were also not significantly related to sampling time. Similarly, corticosterone concentrations of red-footed boobies were not
Acknowledgments
We thank all field and laboratory assistants for their excellent technical support. Thank you to Dr. Greg Robertson, Dr. Ian Jones, Dr. A.S. Kitaysky, and Dr. John Piatt for their comments on the theses on which this manuscript is based (L.M.D. and S.I.W.). Thanks to Dr. Brian Nakashima for supplying the capelin diaries and to Dr. Ian Jones for advising us on scale design. This work was supported by funding from Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant
References (59)
- et al.
Corticosterone, body condition and locomotor activity: a model for dispersal in screech-owls
Anim. Behav.
(1998) - et al.
Prolactin responses to infant cues in men and women: effects of parental experience and recent infant contact
Horm. Behav.
(2007) - et al.
Testosterone, corticosterone, and photoperiod interact to regulate plasma levels of binding globulin and free steroid hormone in dark-eyed juncos, Junco hyemalis
Gen. Comp. Endocrinol.
(2001) - et al.
Testosterone and prolactin are associated with emotional responses to infant cries in new fathers
Horm. Behav.
(2002) - et al.
Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird
Horm. Behav.
(2003) - et al.
Effects of weather on corticosterone responses in wild free-living passerine birds
Gen. Comp. Endocrinol.
(2000) - et al.
Circulating corticosterone responses of feed- and water-deprived broilers and Japanese quail
Poult. Sci.
(1983) - et al.
Measurement of gonadal hormones in dried blood spots versus serum: verification of menstrual cycle phase
Horm. Behav.
(2001) Corticosterone-binding proteins and behavioral effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher
Gen. Comp. Endocrinol.
(1986)- et al.
Corticosterone responses of grey-faced petrels (Pterodroma macroptera gouldi) are higher during incubation than during other breeding stages
Physiol. Biochem. Zool.
(2005)
Common murres (Uria aalge)
Interactions of corticosterone with feeding, activity and metabolism in passerine birds
Ornis Scand.
Adrenocortical sensitivity to stress in dark-eyed juncos (Junco hyemalis oregonus) breeding in low and high elevation habitat
Ecoscience
Responses to changes in prey availability by common murres and thick-billed murres at the Gannet Islands, Labrador
Can. J. Zool.
Flexible time budgets in breeding common murres: buffers against variable prey abundance
Stud. Avian Biol.
Seabirds as indicators of marine food supplies
Biol. Oceanogr.
Cortisol levels are positively associated with pup-feeding rates in male meerkats
Proc. R. Soc. B.
Trophic relationships among capelin (Mallotus villosus) and marine birds in a changing ecosystem
ICES J. Mar. Sci.
Balancing food and predator pressure induces chronic stress in songbirds
Proc. R. Soc. Lond., B Biol. Sci.
Diving metabolism and thermoregulation in common and thick-billed murres
J. Comp. Physiol., B.
Consequences of foraging trip duration on provisioning behaviour and fledging of common murres Uria aalge
J. Avian Biol.
Search strategies of a pursuit-diving marine bird and the persistence of prey patches
Ecol. Monogr.
Capelin in Subarea2 + Div. 3KL
DFO Science Stock Status Report B2-02
Capelin in Subarea2 + Div. 3KL Update
DFO Science Stock Status Report B2-02
Energy expenditure of breeding common murres
Sensitivity of breeding parameters to food supply in black-legged kittiwakes
Ibis
Dimensional relationships for flying animals
Stress and adrenal function
J. Exp. Zool.
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