Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

In several cooperatively breeding species, reproductively suppressed, nonbreeding females are attracted to infants and routinely provide alloparental care, while breeding females may attack or kill other females' infants. The mechanisms underlying the transition from alloparental to infanticidal behavior are unknown. In this study, we tested the hypothesis that this transition is associated with cessation of reproductive suppression and onset of ovarian activity in the Mongolian gerbil (Meriones unguiculatus), a cooperatively breeding rodent. Young female gerbils were housed with their natal family (FH), with a female pairmate (PH) or singly (SH). When females were either 11-13 or 16-18 weeks of age, we characterized their behavioral responses to an unfamiliar pup, reproductive development, and plasma progesterone, cortisol, and prolactin concentrations. In both age groups, FH females were significantly less likely to attack pups than PH or SH females and in fact never did so. FH females also had smaller ovaries and uteri, less developed scent glands, and lower progesterone levels, and were more likely to be anovulatory than PH or SH females, especially in the 11- to 13-week-old age group. Prolactin concentrations did not differ with reproductive status but were significantly higher in females that did not attack pups than in those that did. We found no other significant associations, however, between reproductive or endocrine measures and behavioral responses to pups. These results suggest that cohabitation with the natal family inhibits both infanticidal behavior and reproductive maturation in young female gerbils but that these two effects may not be causally related.     

Improving the productivity of breeding colonies of Mongolian gerbils (Meriones unguiculatus)

The productivity of breeding colonies of Mongolian gerbils can be substantially enhanced by using as breeding stock only the 40% of females that exhibit vaginal opening before reaching 25 days of age. Early-maturing females are more likely to breed successfully on first pairing. The lifetime fecundity of early-maturing females is more than twice that of their late-maturing sisters. In those cases in which early-maturing females fail to breed with the first male with which they are paired, they (but not late-maturing females) can be mated with a second male with a high probability of success. Two-thirds of the early-maturing females that failed to reproduce following a first pairing became pregnant following a second. Only 11% of late-maturing females did so.     

Influence of reproductive success on breeding frequency in four southern petrels

Patterns of breeding frequency of White-headed Pterodroma lessoni, Great-winged Pterodroma macroptera, White-chinned Procellaria aequinoctialis and Grey Petrels Proceharia cinerea have been studied at Kerguelen and Crozet Islands. The White-headed Petrel (summer breeder) followed an essentially biennial cycle with only 13% of successful individuals breeding again the next year. On the other hand, the Great-winged Petrel (winter breeder) was mainly an annual breeder with 78% of successful birds breeding again the next year. Both White-chinned (summer breeder) and Grey Petrels (winter breeder) showed a higher breeding frequency than Pterodroma species, with 91% and 93%, respectively, of successful birds returning to breed the following season. These contrasting patterns may be related to the timing of energetic constraints encountered during the interbreeding period, principally the moult and the restoration of breeding condition. It is suggested that these post-breeding constraints are more marked in winter and in oceanic waters, leading to breeding frequencies being lower than in summer and in neritic waters. The intermediate patterns of breeding frequency found in the Great-winged Petrel (mainly annual) and the White-headed Petrel (mainly biennial) show that among Procellariiformes there is a continuum between annual and strictly biennial species.     

Effects of supplemental food on the social organization of Mongolian gerbils during the breeding season

Social groups occur in many rodents and vary in size and complexity under varying environments. Food availability is often limited in northern temperate regions and alters the life history and behavior of rodents. Increased food availability is hypothesized to increase the size and complexity of rodent social groups by enhancing individual survival and philopatry. We tested this hypothesis in Mongolian gerbils Meriones unguiculatus under semi-natural conditions in Inner Mongolia, China. The Mongolian gerbil is a cooperative breeder living in groups year-round. Gerbil colonies in 10 m × 10 m chambers were the experimental units, with four replicate chambers each for food supplementation and food unsupplemented controls in 2004 and six replicate chambers for each treatment in 2005. At 2-day intervals wheat grain supplemented the normal food in experimental chambers throughout the breeding season (May through August). We estimated founder mortality, cumulative recruitment, proportion of philopatric juveniles, ages at sexual maturity and social group size in each colony from May through August. Rates of change in group size were inversely related to social group size. The social organization of Mongolian gerbils did not differ in any of the measured parameters between food-supplemented and -unsupplemented chambers. Therefore, additional food does not influence the social organization of Mongolian gerbils during the breeding season.     

Delayed breeding affects lifetime reproductive success differently in male and female green woodhoopoes

In cooperatively breeding species, many individuals only start breeding long after reaching physiological maturity [1], and this delay is expected to reduce lifetime reproductive success (LRS) [1-3]. Although many studies have investigated how nonbreeding helpers might mitigate the assumed cost of delayed breeding (reviewed in [3]), few have directly quantified the cost itself [4, 5] (but see [6, 7]). Moreover, although life-history tradeoffs frequently influence the sexes in profoundly different ways [8, 9], it has been generally assumed that males and females are similarly affected by a delayed start to breeding [7]. Here, we use 24 years of data to investigate the sex-specific cost of delayed breeding in the cooperatively breeding green woodhoopoe (Phoeniculus purpureus) and show that age at first breeding is related to LRS differently in males and females. As is traditionally expected, males that started to breed earlier in life had greater LRS than those that started later. However, females showed the opposite pattern: Those individuals that started to breed later in life actually had greater LRS than those that started earlier. In both sexes, the association between age at first breeding and LRS was driven by differences in breeding-career length, rather than per-season productivity. We hypothesize that the high mortality rate of young female breeders, and thus their short breeding careers, is related to a reduced ability to deal with the high physiological costs of reproduction in this species. These results demonstrate the importance of considering sex-specific reproductive costs when estimating the payoffs of life-history decisions and bring into question the long-held assumption that delayed breeding is necessarily costly.     

Resource availability, breeding site selection, and reproductive success of red-winged blackbirds

Red-winged blackbirds are polygynous and show strong breeding site preferences, but it is unclear which environmental factors regulate their reproductive success and are ultimately responsible for shaping their patterns of habitat selection and their mating system. We evaluated the effect of variation in insect emergence rates on the reproductive success of male and female redwings nesting on replicate ponds. The number of male and female redwings that settled on a pond varied two- to three-fold among ponds, but was not related to insect emergence rates. Insect emergence rates had a positive effect on the number of nestlings successfully fledged by females, the number of nestlings fledged from male territories, and on the mass of nestlings at fledging. Typha stem density also varied widely among ponds, and was positively related to male and female settling density and mass of nestlings at fledging, but not to the number of nestlings fledged by females or males. We conclude that alternative breeding sites differ in their ability to support redwing reproduction, and that the availability of emerging odonates is an important environmental factor influencing the reproductive success of both male and female red-winged blackbirds. Received: 31 March 1997 / Accepted: 3 July 1997     

Genetic consequences of group living in Mongolian gerbils

Social behavior can shape the local population genetic structure of mammals. Group living can increase pairwise genetic relatedness of mammals at a local level but differentiate the genetic structure at a population level through offspring philopatry and nonrandom mating. Our study aimed to test the hypothesis that social groups of Mongolian gerbils (Meriones unguiculatus) would consist of genetically related individuals due to offspring philopatry and would have distinct genetic structures because of restricted gene flow among social groups and nonrandom mating. We genotyped 327 wild gerbils, live captured from 28 social groups in Inner Mongolia, China, using nine microsatellite loci. The within-group pairwise genetic relatedness coefficient averaged 0.28 ± 0.14 (standard deviation), whereas the average pairwise genetic relatedness coefficient of the whole gerbil population was 0.0 ± 0.2. Additionally, the value of the global F statistic (F(st)) was 0.21, suggesting a substantial genetic differentiation among social groups of Mongolian gerbils. The Bayesian clustering divided the 327 gerbils into 23 distinct genetic clusters. Therefore, our results show that high within-group genetic relatedness and among-group genetic differentiation are the genetic consequences of group living in social mammals because of restricted gene flow, female philopatry, and nonrandom mating within social groups.     

Predator avoidance, breeding experience and reproductive success in endangered cheetahs, Acinonyx jubatus

I examine three hypotheses about predator avoidance behaviour: (1) avoidance increases an individual's reproductive success; (2) avoidance changes with breeding experience according to one of three described models; and (3) any reproductive or experience benefits accrued to individuals by avoidance are reflected in their spatial distribution. These hypotheses were tested on cheetahs which incur substantial juvenile mortality from predation by two larger competitors: spotted hyaenas, Crocuta crocuta, and lions, Panthera leo. To examine avoidance tactics, I played lion and hyaena vocalizations to individual female cheetahs. Lion avoidance increased with the statistical interaction between age and reproductive success, suggesting that it may be a learned behaviour, reinforced by successful reproductive events. This behaviour translated into a nonrandom spatial distribution of cheetahs with the most reproductively successful females found near lower lion densities than less successful females. Hyaena avoidance decreased with the interaction between age and reproductive success, suggesting that it is diminished by successful reproductive events, perhaps because a female cheetah switches from avoidance to using antipredator behaviours as she gets older. Hyaena avoidance behaviour translated into a spatial distribution with the most reproductively successful females found near lower hyaena densities than less successful females; however, younger females were found near lower hyaena densities than older females. Copyright 2000 The Association for the Study of Animal Behaviour.     

Polaprezinc attenuates Helicobacter pylori-associated gastritis in Mongolian gerbils

Background. The ammonia‐monochloramine system plays an important role in Helicobacter pylori‐associated gastric mucosal injury. Polaprezinc, a new antiulcer agent, has a scavenging action against monochloramine. The aim of the experiment was to investigate the inhibitory effects of polaprezinc on the H. pylori‐induced gastritis in Mongolian gerbils. Materials and Methods. Mongolian gerbils fasting for 24 hours were orally given culture broth containing 2–4 × 10⁸ colony‐forming units of H. pylori ATCC 43054 per milliliter. From 4 hours after inoculation until the end of the experiment, gerbils were given chow pellets with or without 0.02% polaprezinc. All gerbils were killed 12 weeks later. The grades of H. pylori density and histologic features of gastritis were evaluated in accordance with the Updated Sydney System. The scavenging effect of polaprezinc on monochloramine was investigated spectrophotometrically. Results. Polaprezinc had little or no influence on the H. pylori density in both pyloric and fundic mucosae. However, it significantly attenuated the development of polymorphonuclear neutrophil activity, mononuclear infiltration, and surface epithelial erosion in both pyloric and fundic mucosae compared with those of the control group. H. pylori inoculation significantly increased the heights of both pyloric and fundic mucosae (mainly due to the increased height of foveolar hyperplasia), but polaprezinc inhibited the increase of mucosal thickness in both pyloric and fundic mucasae. No intestinal metaplasia was detected in this study. Spectrophotometric examination revealed that polaprezinc scavenged monochloramine. Conclusions. Polaprezinc inhibited the development of H. pylori‐induced gastritis through its scavenging action against monochloramine.     

Climatic effects on the breeding phenology and reproductive success of an arctic-nesting goose species

Climate warming is pronounced in the Arctic and migratory birds are expected to be among the most affected species. We examined the effects of local and regional climatic variations on the breeding phenology and reproductive success of greater snow geese ( Chen caerulescens atlantica ), a migratory species nesting in the Canadian Arctic. We used a long-term dataset based on the monitoring of 5447 nests and the measurements of 19 234 goslings over 16 years (1989–2004) on Bylot Island. About 50% of variation in the reproductive phenology of individuals was explained by spring climatic factors. High mean temperatures and, to a lesser extent, low snow cover in spring were associated with an increase in nest density and early egg-laying and hatching dates. High temperature in spring and high early summer rainfall were positively related to nesting success. These effects may result from a reduction in egg predation rate when the density of nesting geese is high and when increased water availability allows females to stay close to their nest during incubation recesses. Summer brood loss and production of young at the end of the summer increased when values of the summer Arctic Oscillation (AO) index were either very positive (low temperatures) or very negative (high temperatures), indicating that these components of the breeding success were most influenced by the regional summer climate. Gosling mass and size near fledging were reduced in years with high spring temperatures. This effect is likely due to a reduced availability of high quality food in years with early spring, either due to food depletion resulting from high brood density or a mismatch between hatching date of goslings and the timing of the peak of plant quality. Our analysis suggests that climate warming should advance the reproductive phenology of geese, but that high spring temperatures and extreme values of the summer AO index may decrease their reproductive success up to fledging.     

The use of conspecific reproductive success for breeding patch selection in terrestrial migratory species

Classical models of breeding habitat selection rarely deal with the question of information gathering for patch quality assessment. In this paper, we present two models comparing the fitness outcomes of behavioural strategies based on conspecific reproductive success as a cue to assess local environmental quality before selecting a new breeding habitat. The models deal with two phases of the life-cycle of a territorial migratory species: recruitment to a breeding population (model 1) and breeding site fidelity of subsequent breeding attempts (model 2). The first model shows that prospecting breeding patches before recruiting is the best strategy if the environment is predictable and contains a low proportion of good patches, even if it implies losing a breeding opportunity. The second model shows that dispersing after a breeding attempt according to the patch's breeding success rather than the individual's own success is the bests own success is the best strategy if the environment is patchy. These results underline the importance of studying the spatio-temporal variations of factors affecting reproductive success when considering the importance of habitat selection strategies based on conspecifics. Moreover, they allow the understanding of individual behaviour patterns observed in natural populations and their potential consequences at the metapopulation level.     

Patterns of synchrony in natterjack toad breeding activity and reproductive success at local and regional scales

Empirical studies of the spatiotemporal dynamics of populations are required to better understand natural fluctuations in abundance and reproductive success, and to better target conservation and monitoring programmes. In particular, spatial synchrony in amphibian populations remains little studied. We used data from a comprehensive three year study of natterjack toad Bufo calamita populations breeding at 36 ponds to assess whether there was spatial synchrony in the toad breeding activity (start and length of breeding season, total number of egg strings) and reproductive success (premetamorphic survival and production of metamorphs). We defined a novel approach to assess the importance of short‐term synchrony at both local and regional scales. The approach employs similarity indices and quantifies the interaction between the temporal and spatial components of populations using mixed effects models. There was no synchrony in the toad breeding activity and reproductive success at the local scale, suggesting that populations function as individual clusters independent of each other. Regional synchrony was apparent in the commencement and duration of the breeding season and in the number of egg strings laid (indicative of female population size). Regional synchrony in both rainfall and temperature are likely to explain the patterns observed (e.g. Moran effect). There was no evidence supporting regional synchrony in reproductive success, most likely due to spatial variability in the environmental conditions at the breeding ponds, and to differences in local population fitness (e.g. fecundity). The small scale asynchronous dynamics and regional synchronous dynamics in the number of breeding females indicate that it is best to monitor several populations within a subset of regions. Importantly, variations in the toad breeding activity and reproductive success are not synchronous, and it is thus important to consider them both when assessing the conservation status of pond‐breeding amphibians.     

Multiple paternity in an aggregate breeding amphibian: the effect of reproductive skew on estimates of male reproductive success

Aggregate, or explosive, breeding is widespread among vertebrates and likely increases the probability of multiple paternity. We assessed paternity in seven field-collected clutches of the explosively breeding spotted salamander (Ambystoma maculatum) using 10 microsatellite loci to determine the frequency of multiple paternity and the number of males contributing to a female's clutch. Using the Minimum Method of allele counts, multiple paternity was evident in 70% of these egg masses. Simple allele counts underestimate the number of contributing males because this method cannot distinguish multiple fathers with common or similar alleles. Therefore, we used computer simulations to estimate from the offspring genotypes the most likely number of contributing fathers given the distributions of allele frequencies in this population. We determined that two to eight males may contribute to A. maculatum clutches; therefore, multiple paternity is a common strategy in this aggregate breeding species. In aggregate mating systems competition for mates can be intense, thus differential reproductive success (reproductive skew) among males contributing to a female's clutch could be a probable outcome. We use our data to evaluate the potential effect of reproductive skew on estimates of the number of contributing males. We simulated varying scenarios of differential male reproductive success, ranging from equal contribution to high reproductive skew among contributing sires in multiply sired clutches. Our data suggest that even intermediate levels of reproductive skew decrease confidence substantially in estimates of the number of contributing sires when parental genotypes are unknown.     

Propagation of nephropathia epidemica virus in Mongolian gerbils.

Nephropathia epidemica virus, the etiological agent of hemorrhagic fever with renal syndrome in Scandinavia, was serially propagated in Mongolian gerbils (Meriones unguiculatus). Intracerebrally inoculated suckling gerbils developed subclinical infections, with viral antigen found in lung, brain, liver and spleen. The distribution of viral antigen was similar to that seen in experimentally infected bank voles (Clethrionomys glareolus), the principal wild rodent reservoir of nephropathia epidemica virus. This model provides a readily available animal host for the study of experimental nephropathia epidemica virus infection.     

Height and reproductive success

In Western societies, height is positively correlated with reproductive success (RS) for men but negatively correlated with RS for women. These relationships have been attributed to sexual selection: women prefer tall men, and men prefer short women. It is this success in the marriage market which leads to higher RS for tall men and short women. We have already shown that the relationship between height and RS for women is quite different in a non-Western context. In a subsistence farming community in rural Gambia, height is positively correlated with reproductive success for women, largely owing to the higher survival of the children of tall women. Here, the relationship between height and reproductive success is analyzed for men in the same community. For these Gambian men, there is no significant relationship between height and the number of children they produce, although tall men do contract more marriages than shorter men. We conclude that environmental context needs to be taken into account when analyzing human reproductive behavior.     

Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum)

Female greater horseshoe bats form maternity colonies each summer in order to give birth and raise young. During the mating period, females visit males occupying territorial sites, copulation takes place and sperm are stored until ovulation occurs, normally in April. Using microsatellite markers and a likelihood method of parentage analysis, we studied breeding behaviour and male reproductive success over a five-year period in a population of bats in south-west Britain. Paternity was assigned with 80% confidence to 44% of young born in five successive cohorts. While a small annual skew in male reproductive success was detected, the variance increased over five years due to the repeated success of a few individuals. Mating was polygynous, although some females gave birth to offspring sired by the same male in separate years. Such repeated partnerships probably result from fidelity for either mating sites or individuals or from sperm competition. Females mated with males born both within and outside their own natal colony; however, relatedness between parents was no less than the average recorded for male female pairs. Gene flow between colonies is likely to be primarily mediated by both female and male dispersal during the mating period rather than more permanent movements.     

Male heterozygosity predicts territory size, song structure and reproductive success in a cooperatively breeding bird

Recent studies of non-social animals have shown that sexually selected traits signal at least one measure of genetic quality: heterozygosity. To determine whether similar cues reveal group quality in more complex social systems, we examined the relationship between territory size, song structure and heterozygosity in the subdesert mesite (Monias benschi), a group-living bird endemic to Madagascar. Using nine polymorphic microsatellite loci, we found that heterozygosity predicted both the size of territories and the structure of songs used to defend them: more heterozygous groups had larger territories, and more heterozygous males used longer, lower-pitched trills in their songs. Heterozygosity was linked to territory size and song structure in males, but not in females, implying that these traits are sexually selected by female choice and/or male-male competition. To our knowledge, this study provides the first direct evidence in any animal that territory size is related to genetic diversity. We also found a positive association between seasonal reproductive success and heterozygosity, suggesting that this heritable characteristic is a reliable indicator of group quality and fitness. Given that heterozygosity predicts song structure in males, and can therefore be determined by listening to acoustic cues, we identify a mechanism by which social animals may assess rival groups, prospective partners and group mates, information of potential importance in guiding decisions related to conflict, breeding and dispersal.