Carolyn J. Walsh

Hormonal correlates of paternal responsiveness in new and expectant fathers

Little is known about the physiological and behavioral changes that expectant fathers undergo prior to the birth of their babies. We measured hormone concentrations and responses to infant stimuli in expectant and new fathers living with their partners to determine whether men can experience changes that parallel the dramatic shifts seen in pregnant women. We obtained two blood samples from couples at one of four times before or after the birth of their babies. After the first sample, the couples were exposed to auditory, visual, and olfactory cues from newborn infants (test of situational reactivity). Men and women had similar stage-specific differences in hormone levels, including higher concentrations of prolactin and cortisol in the period just before the births and lower postnatal concentrations of sex steroids (testosterone or estradiol). Men with more pregnancy (couvade) symptoms and men who were most affected by the infant reactivity test had higher prolactin levels and greater post-test reduction in testosterone. Hormone concentrations were correlated between partners. This pattern of hormonal change in men and other paternal mammals, and its absence in nonpaternal species, suggests that hormones may play a role in priming males to provide care for young.

Neuropsychology of maternal behavior in the rat : c-fos expression during mother-litter interactions

This series of studies used the pattern of nuclear Fos-like immunoreactivity (Fos-lir) to map the functional pathways in the brain that mediate the onset and retention of maternal behavior. In the first two experiments, parturient rat dams were exposed to either pups or to other stimuli on Day 1 postpartum. Dams interacting with pups were either intact or sustained ventral somatosensory, olfactory, or combined desensitizations. Results showed that 1) all intact pup-interacting dams showed elevated levels of Fos-lir in the medial preoptic area (MPOA) and the medial and cortical amygdala as compared to control groups, and 2) olfactory and ventral somatosensory desensitization, either alone or in combination, did not decrease Fos-lir in the MPOA. However, olfactory desensitizations did decrease Fos-lir in the medial amygdala and the combined desensitizations significantly reduced Fos-lir in both the basolateral and central amygdala. In the third study, dams were either exposed to pups or to other stimuli and were subsequently reexposed to pups or to pup cues. Regardless of prior maternal experience, females who were able to interact with pups upon reexposure showed increased Fos-lir in the MPOA, the basolateral and central nuclei of the amygdala, and the nucleus accumbens when compared to females which did not interact with pups. Taken together, these studies suggest that the neuroanatomy of maternal behavior is a complex one, involving multiple systems that interconnect with the MPOA and that mediate the many behavioral processes activated when an animal responds maternally.

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

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.

Divorce in common murres ( Uria aalge ): relationship to parental quality

Behavioral precursors of 12 divorces were examined in 30 color-banded pairs of common murres (Uria aalge) over six breeding seasons. Common murres are long-lived seabirds that typically return each year to the same mate and nest site in dense colonies. At least one parent is present continuously from egg lay to chick fledging. Murres, therefore, have considerable opportunities to compare their mates’ parental behavior with that of several familiar neighbors. Previous reproductive success was lower for divorcing birds than for reuniting pairs. As predicted by the better option hypothesis, there were clear ‘choosers’ (seven females and five males) that initiated divorce by moving to a new bird’s site or by courting a new partner at their current site. Choosers improved their reproductive success after the divorce, whereas their previous partners, the ‘victims’ did not. Yearly divorce rates (average 8.2% per year) were significantly correlated with yearly mortality rates. Divorces appear to be opportunistic: pairs divorced after varying numbers of reproductive failures with the immediate precursor usually being the disappearance (death) of a murre from a successful neighboring site. In contrast to the delays experienced by victims, choosers formed new pairs quickly and laid their eggs no later than reuniting pairs. Prior to the divorce, victims fed their chicks less often than choosers, and some engaged in other behaviors that compromised egg or chick survival. These observations suggest that deficiencies in parental behavior were precursors to the divorce. This report is one of the first cases where reproductive failure of divorcing pairs has been linked to deficits in the parental behavior of the subsequent divorce victim.

Hippocampal volume is related to complexity of nesting habitat in Leach's storm-petrel, a nocturnal procellariiform seabird.

The hippocampal and telencephalon volumes of the nocturnal Leach’s storm-petrel (Oceanodroma leucorhoa, n = 15) were compared with published data for food-storing and non-storing Passerines. The hippocampus to telencephalon ratio of Leach’s storm-petrels is intermediate between food-storing and non-storing birds. Leach’s storm-petrels taken from nesting burrows in wooded habitat had a larger relative hippocampal volume than those taken from burrows in an open meadow. Relative olfactory volume did not differ between woods and open-nesting storm-petrels. The larger relative hippocampal volume of storm-petrels may be associated with increased spatial demands of returning to their nests at night in the darker, more navigationally complex woods. It is not known whether the larger hippocampus in storm-petrels from the woods is due to selection on different subpopulations or whether experience in a more complex environment results in greater hippocampal volume. Hippocampal volume from the brain of one diurnal Procellariiforme, the northern fulmar (Fulmaris glacialis), fell within the range of non-storing species, which supports the view that hippocampal enlargement in the storm-petrel is related to the spatial demand of returning to the nest at night.

Corticosterone levels of Atlantic puffins vary with breeding stage and sex but are not elevated in poor foraging years

Corticosterone (CORT) levels in seabirds fluctuate across breeding stages and in different foraging conditions. Here we use a ten-year data set to examine whether CORT levels in Atlantic puffins differ in years with high or low availability of capelin, the preferred forage species. Female puffins had higher CORT levels than males, possibly related to cumulative costs of egg production and higher parental investment. Puffins had higher CORT levels and body mass during pre-breeding than during chick rearing. Yearly mean chick growth rates were higher in years when adults had higher body mass and in years where adults brought chicks a lower percentage of non-fish (invertebrates/larval fish) food. Unlike most results from seabird species with shorter chick-rearing periods, higher CORT levels in puffins were not associated with lower capelin abundance. Puffins may suppress CORT levels to conserve energy in case foraging conditions improve later in the prolonged chick-rearing period. Alternatively, CORT levels may be lowest both when food is very abundant (years not in our sample) or very scarce (e.g., 2009 in this study), and increase when extra foraging effort will increase foraging efficiency (most years in this study). If these data primarily represent years with medium to poor foraging, it is possible that CORT responses to variation in foraging conditions are similar for puffins and other seabirds.

ARE CHEMICAL CUES AS EFFECTIVE AS PUP CONTACT FOR INDUCING PATERNAL BEHAVIOUR IN MEADOW VOLES

We tested what social cues mediate the transition from non-parental to parental behavior in male meadow voles, based on our previous findings that postpartum interaction with mate and pups was the most effective social experience for making males paternal. Males housed with their mates and pups for a day were more paternal and less aggressive to unrelated pups than males removed from their mates before parturition. Males housed with their mates, but with the litter removed, interacted with pups but were initially as likely to be aggressive as males with no exposure to mates and pups. These results suggest that the mate facilitates interaction with pups, but exposure to pups accelerates the sensitization process. Twenty-four hours of exposure to chemical cues from the mate and pups (mother and litter in cage with wire mesh floor suspended above males cage) eliminated male aggression towards pups, but physical contact was necessary to enhance positive interactions with pups. Exposure to chemical cues from parturient mates reduced aggression, whereas cues from non-mates were not effective. These results may explain our previous findings that females keep sires removed during pregnancy out of the nest for about a day after reintroduction (while males become sensitized via chemosignals), and continue repelling unfamiliar males (that would not be sensitized by chemical cues from non-mates).

Why timing is everything: Energetic costs and reproductive consequences of resource mismatch for a chick‐rearing seabird

Timing reproduction to overlap with peak prey availability is vital to success for many species. This may be especially true for species that rely on one or a few prey species that exhibit strong seasonal peaks in abundance. Any mismatch must be mediated by parents that provision offspring through flexible behavioral changes within the bounds of their physiological tolerances. In Newfoundland, common murre Uria aalge breeding coincides with the inshore movement of capelin Mallotus villosus—their primary prey—such that peak prey availability overlaps with chick-rearing, the most energy demanding phase of breeding. We use colony-based observations and temperature-depth recorders to track the behavioral responses of murres to temporal match and mismatch with capelin availability. Activity budgets, daily energy expenditure (DEE) and chick-provisioning rates were constant across years when chick and capelin timing matched. However, when capelin were late, despite increasing diving effort and DEE, parents deliv...

Evaluation of seabirds in Newfoundland and Labrador, Canada, as hosts of influenza A viruses.

Abstract Influenza A viruses infect a wide range of hosts, including many species of birds. Avian influenza A virus (AIV) infection appears to be most common in Anseriformes (ducks, geese, and swans) and some Charadriiformes (shorebirds and gulls), but many other birds also serve as hosts of AIV. Here, we evaluated the role of seabirds as hosts for AIV. We tested 3,160 swab samples from 13 seabird species between May 2008 and December 2011 in Newfoundland and Labrador, Canada. We also tested 156 serum samples for evidence of previous infection of AIV in Common Murres (Uria aalge) and Atlantic Puffins (Fratercula arctica). Avian influenza A virus was detected in breeding Common Murres and nonbreeding Thick-billed Murres (Uria lomvia), and Common Murres also had high antibody prevalence (44%). From these findings, combined with other studies showing AIV infection in murres, we conclude that murres are important for the ecology of AIV. For other species (Razorbill, Alca torda; Leachs Storm-Petrel, Oceanodroma leucorhoa; Black-legged Kittiwake, Rissa tridactyla; Atlantic Puffin) with good coverage (>100 samples) we did not detect AIV. However, serology indicates infection does occur in Atlantic Puffins, with 22% antibody prevalence found. The possibility of virus spread through dense breeding colonies and the long distance movements of these hosts make a more thorough evaluation of the role for seabirds as hosts of AIV important.

Time Budgets of Common Murres Vary in Relation to Changes in Inshore Capelin Availability

Abstract Changes in capelin (Mallotus villosus) biology since the 1990s have directly or indirectly induced variable breeding conditions for many seabirds in the Northwest Atlantic. Time budgets of the same individual Common Murres (Uria aalge) were examined in relation to annual variations in the arrival of inshore spawning capelin during three consecutive chick-rearing periods (1998–2000) on Great Island in the Witless Bay Ecological Reserve, Newfoundland, Canada. Despite high foraging effort (longer provisioning trips, lower co-attendance time, and faster colony departure after a brooding bout), chick-feeding rates were low during early chick rearing in 2000 due to a mismatch between early egg hatching and the later inshore arrival of spawning capelin. Time budgets of murres breeding on Great Island were examined in relation to those of murres in other nearby colonies and to long-term changes in capelin spawning behavior across decades (1982–1985 versus 1998–2000). Recent overall provisioning rates on Great Island were comparable to those of other nearby colonies during the same time period (with the exception of Funk Island) and to those reported during the 1980s. However, murres breeding in recent years in the reserve exhibited higher foraging effort, which is likely linked to recent changes in the availability of capelin as a result of later spawning, changes in capelin distribution, and their overall smaller size. Murres currently may be constrained to timing their egg laying such that hatching coincides with the arrival of inshore capelin rather than peak capelin abundance and, thus, are vulnerable to sudden changes in the ecosystem.