Anne E. Storey

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.

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.

Male identity and enclosure size affect paternal attendance of meadow voles, Microtus pennsylvanicus

Paternal care in meadow voles, Microtus pennsylvanicus, was compared (1) for sires of the litter and non-sires, (2) in the presence and absence of a second male on the other side of a wire partition, and (3) for voles housed in laboratory cages or larger enclosures. Paternal attendance was assessed by the amount of time males spent with pups, and the effect of this care on pup survival and weight gain was observed. In both small cages and large enclosures, sires spent more time with pups than did non-sires, and the presence of a non-sire across the partition reduced the sires paternal attendance. In small cages fewer pups survived in the non-sire group than in the sire group, but in the enclosure pup survival was high for all groups. Males in all groups approached the nest equally often, but females attempted to prevent nest entry by nonsires. Pup weights were lower when a non-sire was on the other side of the partition. When a non-sire was present instead of, or in addition to the sire, the amount of male attendance was reduced. This is consistent with the pattern of pregnancy disruption for this species, suggesting that pregnancy disruptions may function to limit female investment in a litter when male investment is likely to be low. Since litters with sires gained more weight than litters housed only with females, and since paternal attendance by sires remained high when voles were housed in large enclosures, functional paternal care may contribute to the reproductive success of meadow voles.

Function of Manx Shearwater Calls in Mate Attraction

Playback experiments were used to study the role of vocalization in mate attraction by Manx shearwaters, a nocturnal seabird. Pre-breeding birds were exposed to test calls of male and female shearwaters calling from the range of normal locations: above the colony as in a flyover call, on the ground in the colony, or from within the nesting burrow. Both female and male test calls increased the frequency of male calling but only male calls increased the frequency of female calling. These findings suggest that male calls 1) facilitated competing responses from other males that are attempting to attract females to their burrows and 2) stimulated calling in available females that require more directional information to find the advertising male. Male calling location, inside or outside the burrow, probably reflected a compromise between being audible to females and being susceptible to predation. Because the call was more widely broadcast, male test calls played from outside the burrow caused more females to land in the colony than the same call played from inside the burrow. However in a simultaneous choice test between a burrow and an outside male test call, males calling from inside did not lose females to the adjacent outside male. Thus calling from inside the burrow in an area where another male is calling outside maximized female attraction while minimizing risk of predation. The male call played from inside the burrow attracted as many females as a pair call from inside but the response of females to the pair was less sustained, indicating that duetting pairs-inhibited the response of unpaired females. Male and female calls emanating from above the colony suppressed the rate of female flyover calls suggesting that during this test condition other birds stopped calling in an attempt to orient to the source of the test call.

Prolactin responses to infant cues in men and women: Effects of parental experience and recent infant contact

We used a longitudinal design to test whether parental experience differentially affects the development of prolactin responses to infant cues in men and women. Couples provided two blood samples at three tests, one test just before their babies were born, and two tests during the early postnatal period (n=21). Nine couples repeated the tests near the birth of their second babies. In the 30 min between the two samples, couples listened to recorded infant cries at the prenatal test and held their baby (fathers) or a doll (mothers) at the postnatal tests. Blood samples were analyzed for prolactin concentrations. Prolactin values were then related to sex and parity differences as well as to questionnaire data concerning emotional responses to infant cries and previous infant contact. We found that (1) prior to the birth of both the first and second babies, womens prolactin concentrations increased after exposure to infant stimuli, whereas mens prolactin concentrations decreased; postnatal sex differences varied with parity; (2) womens prolactin reactivity did not change significantly with parental experience; (3) the same mens prolactin concentrations decreased after holding their first newborns but increased after holding their second newborns; this change was not gradual or permanent; (4) men reporting concern after hearing recorded infant cries showed a different postnatal pattern of prolactin change after holding their babies than men not reporting concern; and (5) men who had little contact with their babies just prior to testing had a more positive prolactin response than men who had recently held their babies for longer periods. Although parental experience appears to affect mens prolactin responses, differences in reactivity were also related to patterns of recent infant contact and individual differences in responses to infant cues.

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.

Pup contact promotes paternal responsiveness in male meadow voles

Male meadow voles, Microtus pennsylvanicus, were tested with unrelated pups to determine the social factors that affect the initiation of paternal responsiveness and the inhibition of infanticide. Adult males were initially more responsive to pups if they had been reared as neonates with their fathers rather than with unfamiliar males. Decreased aggression and facilitation of paternal responsiveness occurred most reliably after extensive exposure to pups, even if exposure had occurred more than 2 months before testing. Unlike house mice, neither copulation nor exposure to females enhanced male responsiveness to pups. Given that male meadow voles only nest with females and young during the colder parts of the breeding season, it may be adaptive for paternal responsiveness to be triggered by pup exposure, rather than by some aspect of earlier contact with the female.

Postimplantation pregnancy disruptions in meadow voles: Relationship to variation in male sexual and aggressive behavior

Previous research on Microtines indicates that the presence of new males may more effectively produce pregnancy disruptions than do pheromones alone. If the males presence is important, behavioral differences among males may be related to the occurrence of disruptions. We observed female meadow voles (Microtus pennsylvanicus) interacting with new males twelve days after they had been paired with stud males. Behavioral interactions were recorded for one hour on each of Days 12-14. Timing of parturition and weight gain by Day 12 were used to assess whether a disruption had occurred. Females with disrupted pregnancies were frequently observed mating within an hour of being placed with the new male, whereas females that retained their original pregnancies rarely copulated with the new male. When pregnancies were disrupted, female-new male pairs fought more, but also engaged in more nonaggressive contact than when pregnancies were retained. Pup survival and male attendance of pups were lower when females retained litters, suggesting that females could successfully rear more pups if the original pregnancy was reabsorbed. However, relatively aggressive females paired with nonaggressive new males protected retained litters from new males. New males were tested for aggressive and pup care responses to an unrelated pup on the day before they were placed with the females. Males aggressive to unrelated pups in these tests were also more aggressive to females on Day 12. These data suggest that male aggressiveness may signal females when it would be advantageous to disrupt pregnancy.

EGG COMPOSITION IN RELATION TO FEMALE AGE AND RELAYING: CONSTRAINTS ON EGG PRODUCTION IN THICK-BILLED MURRES (URIA LOMVIA)

Abstract There is growing awareness that costs associated with egg production play a significant role in shaping avian life histories. The life-history strategy of the Thick-billed Murre (Uria lomvia), a colonial, cliff-breeding seabird of Arctic waters, is characterized by a high annual adult survival rate, deferred breeding, and laying of a single-egg clutch. The single-egg clutch is a widespread phenomenon among seabirds and is generally thought to reflect demands of chick provisioning, rather than egg production. We compared composition of eggs laid by Thick-billed Murres most likely to be physiologically constrained in their capacity to produce eggs (young females with no prior experience, and females forming replacement eggs) to that of first eggs laid by early laying females (typically older, more experienced members of the population). Young, inexperienced females laid 4–18 days past the populationwide median laying date, and their eggs averaged 13% lighter in mass than those laid by early layers. Compared to early laid eggs, shell mass on young females’ eggs was similar to that predicted from egg mass, but their eggs had a lower yolk-to-albumen ratio. There was little difference between the two groups in relative protein content of albumen, relative protein or lipid content of yolk, or amino acid makeup of protein in yolk or albumen. Replacement eggs averaged 6% lighter in mass than first eggs laid by the same females earlier that season. As with young females’ eggs, replacement eggs had shells similar in mass to that predicted from egg mass, but lower yolk-to-albumen ratios, when compared to early laid eggs. Both protein and lipid concentrations in yolk were similar in first and replacement eggs, but replacements were deficient in albumen protein. Amino acid makeup of protein in yolk and albumen was similar in the two groups. Those results suggest that any limitations on egg production acting on young, inexperienced females are manifested in delayed laying and reductions in overall egg mass and proportional yolk content, but not in variation in biochemical composition of their eggs. Limitations on females forming replacement eggs are manifested not only in reduced egg mass and yolk content (as with young females), but also in changes in the biochemical composition of eggs; in particular, evidence suggests that relaying females may face a deficit of endogenous protein. The existence of such limitations suggests that demands of egg production can be significant even in a species that lays a single-egg clutch.

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.