Elsevier

Hormones and Behavior

Volume 53, Issue 1, January 2008, Pages 140-148
Hormones and Behavior

The effects of variable foraging conditions on common murre (Uria aalge) corticosterone concentrations and parental provisioning

https://doi.org/10.1016/j.yhbeh.2007.09.009Get rights and content

Abstract

This study investigated how total corticosterone concentrations, chick-feeding rates, and adult body mass changed with food availability from 1998 to 2000 in the same individually marked common murres (Uria aalge). Capelin, the main prey species, arrived inshore by the onset of murre chick hatching in 1998 and 1999 (prey match years); whereas in 2000, hatching began approximately 1 week before the capelin arrived inshore to spawn (prey mismatch year). Serum corticosterone concentrations were higher in the same individuals in the prey mismatch year than they were in either of the match years. Birds sampled before peak capelin spawning in the mismatch year had higher corticosterone levels than murres sampled after peak spawning. Murres with higher corticosterone levels had higher chick-feeding rates and less mass loss in the mismatch year (compared to the match year 1999) than birds with lower levels. Corticosterone levels did not differ between birds that had not foraged for at least 12 h (brooded chick overnight) and those that had, suggesting that short-term food deprivation did not affect corticosterone concentrations. Taken together, these findings suggest that the difference between years reflects a baseline shift in corticosterone levels, particularly in the high-quality birds that were able to increase both corticosterone concentrations and foraging effort.

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

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