Pre- and Postnatal Predator Cues Shape Offspring Anti-predatory Behavior Similarly in the Bank Vole

Prey animals can assess the risks predators present in different ways. For example, direct cues produced by predators can be used, but also signals produced by prey conspecifics that have engaged in non-lethal predator-prey interactions. These non-lethal interactions can thereby affect the physiology, behavior, and survival of prey individuals, and may affect offspring performance through maternal effects. We investigated how timing of exposure to predation-related cues during early development affects offspring behavior after weaning. Females in the laboratory were exposed during pregnancy or lactation to one of three odor treatments: (1) predator odor (PO) originating from their most common predator, the least weasel, (2) odor produced by predator-exposed conspecifics, which we call conspecific alarm cue (CAC), or (3) control odor (C). We monitored postnatal pup growth, and we quantified foraging and exploratory behaviors of 4-week-old pups following exposure of their mothers to each of the three odour treatments. Exposure to odors associated with predation risk during development affected the offspring behavior, but the timing of exposure, i.e., pre- vs. postnatally, had only a weak effect. The two non-control odors led to different behavioral changes: an attraction to CAC and an avoidance of PO. Additionally, pup growth was affected by an interaction between litter size and maternal treatment, again regardless of timing. Pups from the CAC maternal treatment grew faster in larger litters; pups from the PO maternal treatment tended to grow faster in smaller litters. Thus, in rodents, offspring growth and behavior are seemingly influenced differently by the type of predation risk perceived by their mothers.

Relationship between the female attendance pattern and pup growth rate in the South American sea lion (Carnivora)

Changes in the duration and frequency of foraging trips by female otariids may result in changes in the duration and frequency of lactation bouts and hence influence pup growth rate, unless females modify milk energy density and/or the total amount of milk delivered depending on the trip duration. To test this hypothesis on South American sea lions, we measured two attendance pattern components (foraging trip and haul-out duration) and three diving behaviour components of nursing females (dive time, bottom time and number of dives per h) at two different rookeries in Uruguay and Argentina, the composition and energy density of their milk, and the growth rate of their pups. Female foraging trip and haul-out durations depended on pup sex and weight, whereas milk energy density depended on female body mass and foraging trip durations. By contrast, the three dive variables were independent of female body mass or pup sex. Pup growth was also independent of the foraging trip and haul-out duration, with pup sex as the only significant variable. This suggests that individual differences in female foraging behaviour play a minor role in determining pup growth rates during the first three weeks after birth.

Deficiency of the paternally inherited gene Magel2 alters the development of separation induced vocalization in mice

Offspring behavior results from the combined expression of maternal and paternal genes. Genomic imprinting, however, silences some genes in a parent-of-origin specific manner, a process that, among all animals, occurs only in mammals. How genomic imprinting affects the behavior of mammalian offspring remains poorly understood. Here we studied the effects of the loss of the paternally inherited gene Magel2 on the emission of separation-induced ultrasonic vocalization (USV) by mouse pups. Using quantitative analysis of more than one hundred thousand USVs, we characterized the rate of vocalizations as well as their spectral features from postnatal days 6 to 12 (P6-P12), a critical phase during mouse development when pups fully depend on the mother for survival. Our analyses show that Magel2 deficient offspring emit separation-induced vocalizations at lower rates and with altered spectral features. Using methods for a holistic analysis of the entire vocal repertoire of pups, we found that Magel2 deficient mice at postnatal day 8 (P8) emit USVs that resemble the vocal repertoire of wildtype mice at older ages (P10-12). These results suggest that the deficiency of this paternally inherited gene impairs the expression of separation-induced vocalization in pups, a behavior that supports pup growth and development.

Practical Application of a Bioenergetic Model to Inform Management of a Declining Fur Seal Population and Their Commercially Important Prey

Food availability is a key concern for the conservation of marine top predators, particularly during a time when they face a rapidly changing environment and continued pressure from commercial fishing activities. Northern fur seals (Callorhinus ursinus) breeding on the Pribilof Islands in the eastern Bering Sea have experienced an unexplained population decline since the late-1990s. Dietary overlap with a large U.S. fishery for walleye pollock (Gadus chalcogrammus) in combination with changes in maternal foraging behavior and pup growth has led to the hypothesis that food limitation may be contributing to the population decline. We developed age- and sex-specific bioenergetic models to estimate fur seal energy intake from May–December in six target years, which were combined with diet data to quantify prey consumption. There was considerable sex- and age-specific variation in energy intake because of differences in body size, energetic costs, and behavior; net energy intake was lowest for juveniles (18.9 MJ sea-day–1, 1,409.4 MJ season–1) and highest for adult males (66.0 MJ sea-day–1, 7,651.7 MJ season–1). Population-level prey consumption ranged from 255,232 t (222,159 – 350,755 t, 95% CI) in 2006 to 500,039 t (453,720 – 555,205 t) in 1996, with pollock comprising between 41.4 and 76.5% of this biomass. Interannual variation in size-specific pollock consumption appeared largely driven by the availability of juvenile fish, with up to 81.6% of pollock biomass coming from mature pollock in years of poor age-1 recruitment. Relationships among metabolic rates, trip durations, pup growth rates, and energy intake of lactating females suggest the most feasible mechanism to increase pup growth rates is by increasing foraging efficiency through reductions in maternal foraging effort, which is unlikely to occur without increases in localized prey density. By quantifying year-specific fur seal consumption of pollock, our study provides a pathway to incorporate fur seals into multispecies pollock stock assessment models, which is critical for fur seal and fishery management given they were a significant source of mortality for both juvenile and mature pollock.

Late lactation in small mammals is a critically sensitive window of vulnerability to elevated ambient temperature

Predicted increases in global average temperature are physiologically trivial for most endotherms. However, heat waves will also increase in both frequency and severity, and these will be physiologically more important. Lactating small mammals are hypothesized to be limited by heat dissipation capacity, suggesting high temperatures may adversely impact lactation performance. We measured reproductive performance of mice and striped hamsters (Cricetulus barabensis), including milk energy output (MEO), at temperatures between 21 and 36 °C. In both species, there was a decline in MEO between 21 and 33 °C. In mice, milk production at 33 °C was only 18% of that at 21 °C. This led to reductions in pup growth by 20% but limited pup mortality (0.8%), because of a threefold increase in growth efficiency. In contrast, in hamsters, MEO at 33 °C was reduced to 78.1% of that at 21 °C, yet this led to significant pup mortality (possibly infanticide) and reduced pup growth by 12.7%. Hamster females were more able to sustain milk production as ambient temperature increased, but they and their pups were less capable of adjusting to the lower supply. In both species, exposure to 36 °C resulted in rapid catastrophic lactation failure and maternal mortality. Upper lethal temperature was lowered by 3 to 6 °C in late lactation, making it a critically sensitive window to high ambient temperatures. Our data suggest future heat wave events will impact breeding success of small rodents, but this is based on animals with a long history in captivity. More work should be performed on wild rodents to confirm these impacts.

Maternal Microdeletion at the H19/Igf2 ICR in Mice Increases Offspring Susceptibility to In Utero Environmental Perturbation

Deficiency of methyl donor nutrients folate, choline, and methionine (methyl deficiency) during gestation can impair fetal development and perturb DNA methylation. Here, we assessed genetic susceptibility to methyl deficiency by comparing effects in wildtype C57BL/6J (B6) mice to mutant mice carrying a 1.3 kb deletion at the H19/Igf2 Imprinting Control Region (ICR) ( H19ICRΔ2,3). The H19ICRΔ2,3 mutation mimics microdeletions observed in Beckwith-Wiedemann syndrome (BWS) patients, who exhibit epimutations in cis that cause loss of imprinting and fetal overgrowth. Dams were treated during pregnancy with 1 of 4 methyl sufficient (MS) or methyl deficient (MD) diets, with or without the antibiotic commonly used to deplete folate producing gut microbes. As expected, after ~9 weeks of treatment, dams in MD and MD + antibiotic groups exhibited substantially reduced plasma folate concentrations. H19ICRΔ2,3 mutant lines were more susceptible to adverse pregnancy outcomes caused by methyl deficiency (reduced birth rate and increased pup lethality) and antibiotic (decreased litter size and litter survival). Surprisingly, pup growth/development was only minimally affected by methyl deficiency, while antibiotic treatment caused inverse effects on B6 and H19ICRΔ2,3 lines. B6 pups treated with antibiotic exhibited increased neonatal and weanling bodyweight, while both wildtype and mutant pups of heterozygous H19ICRΔ2,3/+ dams exhibited decreased neonatal bodyweight that persisted into adulthood. Interestingly, only antibiotic-treated pups carrying the H19ICRΔ2,3 mutation exhibited altered DNA methylation at the H19/Igf2 ICR, suggesting ICR epimutation was not sufficient to explain the altered phenotypes. These findings demonstrate that genetic mutation of the H19/Igf2 ICR increases offspring susceptibility to developmental perturbation in the methyl deficiency model, maternal and pup genotype play an essential role, and antibiotic treatment in the model also plays a key independent role.

Effects of Nutrient Intake during Pregnancy and Lactation on the Endocrine Pancreas of the Offspring

The pancreas has an essential role in the regulation of glucose homeostasis by secreting insulin, the only hormone with a blood glucose lowering effect in mammals. Several circulating molecules are able to positively or negatively influence insulin secretion. Among them, nutrients such as fatty acids or amino acids can directly act on specific receptors present on pancreatic beta cells. Dietary intake, especially excessive nutrient intake, is known to modify energy balance in adults, resulting in pancreatic dysfunction. However, gestation and lactation are critical periods for fetal development and pup growth and specific dietary nutrients are required for optimal growth. Feeding alterations during these periods will impact offspring development and increase the risk of developing metabolic disorders in adulthood, leading to metabolic programming. This review will focus on the influence of nutrient intake during gestation and lactation periods on pancreas development and function in offspring, highlighting the molecular mechanism of imprinting on this organ.

Impact of Fenugreek on Milk Production in Rodent Models of Lactation Challenge

Fenugreek, a herbal remedy, has long been used as galactologue to help mothers likely to stop breastfeeding because of perceived insufficient milk production. However, few studies highlight the efficacy of fenugreek in enhancing milk production. The aims of our study were to determine whether fenugreek increased milk yield in rodent models of lactation challenge and if so, to verify the lack of adverse effects on dam and offspring metabolism. Two lactation challenges were tested: increased litter size to 12 pups in dams fed a 20% protein diet and perinatal restriction to an 8% protein diet with eight pups’ litter, with or without 1 g.kg-1.day-1 dietary supplementation of fenugreek, compared to control dams fed 20% protein diet with eight pups’ litters. Milk flow was measured by the deuterium oxide enrichment method, and milk composition was assessed. Lipid and glucose metabolism parameters were assessed in dam and offspring plasmas. Fenugreek increased milk production by 16% in the litter size increase challenge, resulting in an 11% increase in pup growth without deleterious effect on dam-litter metabolism. Fenugreek had no effect in the maternal protein restriction challenge. These results suggest a galactologue effect of fenugreek when mothers have no physiological difficulties in producing milk.