Birth Synchrony Research Articles

When will the stork arrive? Patterns of birth seasonality in neotropical primates

We review and discuss the ultimate and proximate causes of birth seasonality in Neotropical primates and the seasonal patterns shown by each genus within this group. Our review of the literature shows that most New World monkey populations studied so far show some degree of birth seasonality. Photoperiod is the most important proximate cue used by populations living at relatively high latitudes to time their reproductive events, but almost nothing is known about the proximate factors used by those near the equator. The findings are consistent with the hypothesis that food availability is the most important ultimate cause of birth seasonality. Predation seems to promote birth synchrony in some species (e.g., squirrel monkeys). Multiple regression ANCOVA was used to estimate how the degree of birth seasonality is affected by ecological and life history variables. The ANCOVA model shows that three factors affect the degree of birth seasonality: diet, latitude, and body size. Folivores (howlers) are less seasonal than frugivores and insectivores. The degree of seasonality increases with latitude and shows a humped relationship with body size, peaking at 1.66 kg body mass. This last relationship was expected since small bodied species have to pay a cost (in terms of time lost) by being seasonal on a yearly basis, and large species are buffered against fluctuations in food availability due to their large body mass. To understand which of three alternative birth strategies is followed by each species (reduce energy stress during peak lactation, wean infants during peak food availability, or store reserves during peak energy availability), we compared the location of the birth peak in relation to the peak in food availability for those populations from which data were available. Most species conform to the typical pattern of births concentrated before the peak in food availability, allowing peak lactation (small-sized species) or weaning (capuchins) to take place before the start of the lean season. The pattern of births of the atelines is consistent with the weaning hypothesis. However, since they give birth during the lean season, this pattern is also consistent with an alternative strategy. Am. J. Primatol. 50:109–130, 2000. © 2000 Wiley-Liss, Inc.

When will the stork arrive? Patterns of birth seasonality in neotropical primates.

We review and discuss the ultimate and proximate causes of birth seasonality in Neotropical primates and the seasonal patterns shown by each genus within this group. Our review of the literature shows that most New World monkey populations studied so far show some degree of birth seasonality. Photoperiod is the most important proximate cue used by populations living at relatively high latitudes to time their reproductive events, but almost nothing is known about the proximate factors used by those near the equator. The findings are consistent with the hypothesis that food availability is the most important ultimate cause of birth seasonality. Predation seems to promote birth synchrony in some species (e.g., squirrel monkeys). Multiple regression ANCOVA was used to estimate how the degree of birth seasonality is affected by ecological and life history variables. The ANCOVA model shows that three factors affect the degree of birth seasonality: diet, latitude, and body size. Folivores (howlers) are less seasonal than frugivores and insectivores. The degree of seasonality increases with latitude and shows a humped relationship with body size, peaking at 1.66 kg body mass. This last relationship was expected since small bodied species have to pay a cost (in terms of time lost) by being seasonal on a yearly basis, and large species are buffered against fluctuations in food availability due to their large body mass. To understand which of three alternative birth strategies is followed by each species (reduce energy stress during peak lactation, wean infants during peak food availability, or store reserves during peak energy availability), we compared the location of the birth peak in relation to the peak in food-availability for those populations from which data were available. Most species conform to the typical pattern of births concentrated before the peak in food availability, allowing peak lactation (small-sized species) or weaning (capuchins) to take place before the start of the lean season. The pattern of births of the atelines is consistent with the weaning hypothesis. However, since they give birth during the lean season, this pattern is also consistent with an alternative strategy.

Reproductive Synchrony in Brucellosis-Exposed Bison in the Southern Greater Yellowstone Ecosystem and in Noninfected Populations

Shooting of bison (Bison bison) in the Greater Yellowstone Ecosystem is a highly polarized, emo- tional issue because native ungulates exposed to brucellosis (Brucella abortus) may infect cattle when they dis- perse or migrate beyond protected reserves. Both bison and elk (Cervus elaphus) carry brucellosis, a disease that causes abortion in livestock and is often transmitted through contact with expelled fetuses or birth mem- branes andfluids. If Brucella-infected bison experience a prolongedperiod of birth, cattle in areas of sympatry will have increased susceptibility to disease. We tested the hypothesis that reproductive synchrony differs be- tween Brucella-free and Brucella-infected bison by contrasting patterns between the Brucella-exposed bison population (in Jackson Hole, Wyoming) within the southern Greater Yellowstone Ecosystem with three non- exposed populations (National Bison Range in Montana, and Wind Cave and Badlands National Parks in South Dakota) that inhabit prairies. Populations averaged 42 births per site per year. Fifty percent of all the births occurred within 1 month, and 95% within 61 days at three sites. It took 89 days for 95% of the births to occur at the noninfected Badlands site. Multiple comparison of regression slopes of the relationship between birth synchrony and the cumulative proportion of total births revealed interpopulation differences (p < 0.01), but the brucellosis-exposed population did not exhibit a parturition period different from that of the nondiseased populations. These among-population similarities suggest that reproductive synchrony is not protracted in Brucella-infected bison. Although Brucella transmission from bison to cattle occurs experimen- tally, captive densities during testing exceeded the mean for the Greater Yellowstone Ecosystem by about 1500 times, and that in 10 noninfected populations by more than 100 times. Although mean density can be mis- leading as a surrogate for the potential transmission of disease from bison to cattle, bison densities have not approached those reportedfor disease transmission. Among the ecologicalfactors that may affect the spread of brucellosisfrom bison to cattle in the southern Yellowstone region, two stand out: (1) access to high-quality food, perhaps because animals in superior physiological condition tend to exhibit tighter reproductive syn- chrony and (2) incidence of disease in elk. The timing of parturition in bison is neither a simnple process nor is it likely to be based on responses to a single variable. A potentially fertile area for future investigation will concern relationships among food, reproductive synchrony, and spatial-temporal components of bison, elk, and cattle distribution.

Timing and Synchrony of Parturition in Alaskan Moose: Long-Term Versus Proximal Effects of Climate

We studied timing and synchrony of parturition in Alaskan moose ( Alces alces ) in Denali National Park and Preserve, Alaska, from 1990 to 1994. Mean date of birth was 25 May ( SD = 5.7 days) and did not differ significantly among years. Although moose did not congregate to give birth, parturition was highly synchronized (95% of births occurred in 16 days) with no significant differences among years. Most young moose were killed by predators, especially grizzly bears ( Ursus arctos ), but timing of reproduction had no effect on survivorship of young, which was low (ca. 0.2 by 16 June). We reject the hypothesis that moose timed births to avoid predation. We also measured depth of snow in winter, and precipitation, cloud cover, and temperature in spring; none of these variables was related to timing or synchrony of births. Likewise, quality of willow ( Salix pulchra ) in 3 springs in which percent nitrogen and in vitro dry-matter digestibility of this important forage varied markedly was unrelated to timing of births. We reject the hypothesis that moose timed parturition in response to proximal changes in their environment. We hypothesize that both timing and synchrony of parturition in moose are adaptations to long-term patterns of climate that provide the most hospitable conditions to bear and rear young. Consequently, moose may be more susceptible to climatic change than other ungulates that are more adapted to climatic variability.

Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus

AbstractTiming of birth was determined for 292 roe deer (Capreolus capreolus) fawns belonging to 146 litters on an island in central Norway between 1991 and 1994, and for 33 fawns belonging to 19 litters from an inland site from 1995 to 1997. On the island site there was no significant variation between years in the mean date of birth, 22 May, nor was there any significant effect of dam age, fawn sex, or litter size. Individual does tended to give birth close to the same date in consecutive years. Mean birth date at the inland site was 5 June. The births showed a relatively high degree of synchrony with 80% occurring within 26 days and 24 days at the island and inland sites, respectively. Copulation dates were much more synchronized than birth dates on the island site. Gestation length averaged 301 days, although individuals varied by up to 26 days. When comparing published data from European populations, there appears to be extensive variation in timing of birth, while birth synchrony is very conservative. There appears to be little possible anti‐predator benefit for roe deer in any pattern of birth synchrony. Because of their high post‐natal investment and large litter size, we hypothesize that roe deer are constrained to give birth close to the peak of forage productivity.

Timing and Synchrony of Parturition in Alaskan Caribou

Timing of parturition of caribou ( Rangifer tarandus ) varies within populations, but the relative influences of nutritional condition of females during the autumn breeding season and during gestation on that variation is not known. We determined timing of parturition of caribou in Denali National Park, Alaska, during 1984–1995, which had wide variation in snowfall that influenced nutritional condition and productivity of females. The first young were observed each year between 4 and 15 May. Annual median dates of parturition for radiocollared females during 1987–1995 varied from 13 to 21 May. Synchrony of births (i.e., proportion of births during 7 days centered on the median date) did not vary significantly among years ( P > 0.05). Females ≤4 years old were more likely to give birth after the annual median date than older females ( P = 0.005). Dates of parturition were significantly correlated with masses of females in the previous autumn ( P = 0.034) but not in late winter ( P = 0.155). Births tended to be earlier for parous females that were not lactating during the previous breeding season compared to those that were lactating ( P = 0.030). Annual onsets of parturition varied significantly with snowfall in late winter prior to conception ( P = 0.012) but not with snowfall during gestation. Timing of parturition in our study appeared to be a function of physical condition of breeding females in autumn.

Seasonality of Reproduction in Bottlenose Dolphins, Tursiops truncatus

We examined the seasonality of reproduction in captive and wild bottlenose dolphins, Tursiops truncatus . Stranding records of neonatal dolphins and observed births from a long-term field study were used to estimate peak periods of birth for wild populations, and information from captive-breeding colonies was used to assess the effects of latitude and origin of breeding females on timing of birth for dolphins in captivity. Bottlenose dolphins showed diffuse peaks and considerable flexibility in their seasonality of reproduction. There was no relationship between latitude and seasonality of reproduction or synchrony of births. However, there was a correlation between origin of population and seasonality of reproduction in both wild and captive dolphins. We suggest that adaptations to local environmental conditions have the strongest influence on seasonality of reproduction in these populations of bottlenose dolphins.

Communal suckling in the cavy Galea musteloides

We quantified the extent of communal suckling in the cavy Galea musteloides. Six groups of animals were held in large indoor enclosures and suckling behavior was recorded over 113 h of observation. The groups contained 2–6 lactating females and 3–14 sucking pups. Due to the relative synchronization of births, 73% of the pups present in each group during lactation were non-offspring. Each of the 22 lactating females in the six groups suckled non-offspring in addition to her own offspring. On average, females suckled 86% of non-offspring present in their groups. Thus, 98% of all pups (n = 47) received milk from non-mothers. Although suckling frequencies were significantly higher for mothers with their own individual offspring than with non-offspring individuals, females invested more total time suckling all non-offspring than did suckling just their own; this was possible because for each mother many more non-offspring than offspring pups were present during lactation. Suckling bouts were significantly longer for mothers with their own individual offspring than with non-offspring individuals. The proportion of non-offspring suckling of mothers correlated negatively with the proportion of own young among the pups of a group. Non-offspring suckling did not affect future reproduction of females. Our observations demonstrate extensive practice of communal suckling in G. musteloides under laboratory conditions. Probably because all mothers of a group participated more or less equally in communal suckling behavior, the obvious cost of giving energetically expensive milk to non-offspring did not result in reduced (future) reproductive success. Potential benefits directly involved with communal suckling are unclear. More indirectly, communal suckling as well as birth synchrony might contribute to the formation of advantageous multi-litter kindergardens.

Flehmen and birth synchrony among female sable antelope,Hippotragus niger

The role of female flehmen behaviour in maintaining reproductive synchrony was investigated in 11 adult female sable antelope and their associated offspring maintained on a 13·2-ha pasture at the National Zoological Park's Conservation and Research Center near Front Royal, Virginia. All occurrences of aggression and flehmen by adult females were recorded during 274h of observation over a 10-month period (1987), and the timing of births was recorded for four birth seasons (1986-1989). In each year, dominant females tended to give birth in temporal proximity to other females (birth clustering), while subordinates gave birth asynchronously. Flehmen frequency fluctuated seasonally, reaching highest levels just prior to the approximated time of conception. Adult, multiparous females were the primary targets of flehmen. There was positive assortment by reproductive state: pregnant females attended to urinations by other pregnant females and postpartum females responded to other postpartum females. Prepartum flehmen rates reliably predicted subsequent birth synchrony, and the degree of synchrony between a given pair of females was directly proportional to the frequency with which they sampled each other's urine in the preceding year. These results indicate that flehmen is a potential mechanism by which female sable antelope can manipulate the timing of both conception and parturition.

Timing and Synchrony of Births in Roe Deer

We examined timing and synchrony of births in a highly productive population of roe deer ( Capreolus capreolus ) during 5 consecutive years. Neither among-year differences in average date of fawning nor among-year differences in the dispersion of births occurred. Births were synchronized in all years; 80% of births took place in <30 days. Moreover, the sex-ratio of fawns was not related to timing or synchrony of births. We postulate that highly synchronous births are a consequence of selection against late fawning because of the short time separating fawning and rut in roe deer.

Effects of cohort, sex, and birth date on body development of roe deer (Capreolus capreolus) fawns.

We investigated the effects of the year of birth (cohort effect), sex and birth date on the variations observed in birth weight and postnatal growth rate in 209 newborn fawns marked during eight consecutive fawning seasons from a highly productive roe deer population under good nutritional conditions. Roe deer exhibited a fast body development with a birth weight of 1628 g and a postnatal growth rate of 139 g/day constant over the first 20 days of their life. As previously reported for dimorphic and polygynous ungulates, there was a marked cohort effect on the rate of body development. This variability was partly explained by climatic conditions during late gestation. When fewer than 5 days with rainfall over 5 mm occurred in April, fawns were heavier. High temperatures during April and during the winter could also be involved in fast body development of roe deer fawns. Sex of fawn did not affect roe deer growth pattern. This was expected on the basis of low sexual dimorphism in size and low polygyny level characteristic of roe deer. Lastly, the date of birth did not affect the body development of roe deer fawns. High constancy of mean birth dates and high synchrony of births observed in this population could account for this result.

Inter-litter competition and communal nursing among Norway rats: advantages of birth synchrony

The effect of inter-litter competition on pup survival was investigated in pairs of female rats (Rattus norvegicus) living and breeding in the same environment. If a female gave birth when a 0- to 14-day-old litter was already present in the environment, her pups had a very high chance of surviving, similar to the situation in which no other litter was present. Moreover, the mother was likely to nurse communally with the mother of the 0- to 14-day-old litter. This communal nursing benefitted the newborn pups as evidenced by their being heavier at weaning than litters that were not nursed communally. In contrast, if a female gave birth when a 15-to 28-day-old litter was already present in the environment, her newborn pups were likely to die within 3 days postpartum, owing to the fact that they were often prevented from suckling at their mother's teats, resulting in milk deprivation, and were often beneath the older pups, resulting in physical trauma. These findings suggest that inter-litter competition is an important source of pup mortality when litters are born 15-28 days apart. The data are discussed in terms of the advantages of birth synchrony.

Birth synchrony in squirrel monkeys (Saimiri oerstedi)

The vigilance behaviors and association patterns of adult female squirrel monkeys (Saimiri oerstedi) in Parque Nacional Corcovado, Costa Rica were studied over the annual reproductive cycle to identify a possible adaptive function associated with the unusually close within-group birth synchrony prevalent in Saimiri populations. Raptor association with the troops, predation attempts, and monthly changes in food abundance were also documented. Seasonal fluctuations in food abundance probably constrained the timing of births among three contiguous troops to a two month period. The close within-troop birth synchrony (majority of births occurring within a week) is suggested to be advantageous because of intense predation pressure on neonate squirrel monkeys. Adult females with neonates cooperate in anti-predator vigilance and defense of neonates. Participation in these maternal associations may increase the probability of neonate survivorship. Variable gestation length in squirrel monkeys may reflect a lability in the duration of gestation to allow coordination of the timing of births among females in a troop.

Adaptive Hypotheses of Birth Synchrony in Ruminants: An Interspecific Test

The ecological causes of birth synchrony in ruminants are examined. Measures of seasonality, including latitude and seasonal distribution of evapotranspiration, correlate well with birth-season length, explaining about half the variance of a 27-species sample. With one exception, the African buffalo, species with precocious "following" young display short birth seasons in all climates. It is inferred that predation on newborns plays an important role in imposing tight birth synchrony on following species, especially those occupying tropical and subtropical climates. A crude classification of species by diet (browsers vs. grazers) did not significantly improve predictions of birth-season length among sample species. I argue that, as a consequence of the diverse and complex mechanisms used to control the onset of breeding, birth-season lengths are extremely variable both between and within species. The onset of reproduction in species whose birth-season lengths are adapted to seasonal fluctuations in food supply and weather should be governed by reliable predictors of these conditions, such as photoperiod and nutritional status. However, species specially adapted to synchronize births in order to reduce predation on newborns may also respond to lunar cycles, social signals, and other cues that do not predict environmental conditions.

Red howler monkey birth data I: Seasonal variation.

A large set of birth data from a population of red howler monkeys (Alouatta seniculus) in two habitats found a consistent birth "dip," with births occurring less frequently in early wet season (May-July) than during the remaining months. In one of two habitats, births were negatively correlated with rainfall, and viable conceptions were positively correlated with rainfall. The observed degree of within-troop birth synchrony appeared to reflect populational synchrony with environmental factors. Correlations between births and the phenology of plant foods were not striking, but there was weak support for the hypothesis that births are timed to maximize the availability of weaning foods. Reduced births in early wet season also minimize the number of Infants who would experience the transition to independent locomotion and feeding during the peak of the dry season when probable low moisture content of foods and high daytime temperatures might be disadvantageous. However, there was no relationship between season of birth and infant mortality.

Mating System and Reproductive Success in a Spring Population of the Red-Backed Vole, Clethrionomys Rufocanus Bedfordiae

The mating system of the red-backed vole, Clethrionomys rufocanus bedfordiae (Thomas), was examined in a wind shelter-belt and in the laboratory by using markrecapture and electrophoretic techniques. (1) Most of the adult females copulated at post-partum estrus. Birth synchrony was observed in both the field and laboratory. (2) The females occupied exclusive home ranges, while the males usually had overlapping home ranges that often enclosed those of several females. (3) The estimation of frequency of multiple paternity indicated that multiple paternity was rare in this population. (4) The paternity of twelve litters were determined. No male whose home range did not overlap with a female's range sired any of her offspring. However, the degree of the overlap did not always affect copulatory success. No male successfully copulated with two females who had synchronized their parturitions (4 cases). (5) The body weight, testis weight, seminal vesicle weight, adrenal gland weight, flank gland size, and root ratio (age) of 10 successful males were compared with those of all captured adult males. Strong evidence for mate selection in these six male traits could not be found, although some differences in the means of flank gland size and seminal vesicle weight between 10 successful males and the population were observed.

Birth Synchrony in American Bison (Bison bison): Response to Predation or Season?

Calving of American bison was observed at the National Bison Range, Montana, in 1982. Approximately 80% of the calves were born in the last week of April and first 2 weeks of May. During calving, cow-calf pairs grouped preferentially with other cow-calf pairs rather than with cows without calves. Because of their open-country habit and lack of group defense, bison are well-suited for application of Estes (1976) predator confusion and saturation hypothesis of reproductive synchrony. However, comparison shows that the length of bison calving seasons is fairly typical for temperate zone ungulates. Although bison calves are highly precocious, bison do not show the calving aggregations predicted by the anti-predator hypothesis. Thus, climatic factors appear to be the best explanation of breeding synchrony in bison.

The annual reproductive cycle of captive Macaca sylvana.

The annual reproductive cycle of a captive colony of Barbary apes, Macaca sylvana, was examined for the 26-year period from 1950 to 1976 and then compared with the annual reproductive cycle of semifree ranging M.sylvania in Gibraltar. Mating and birthing seasons for the two populations were similar although birth synchrony was more pronounced in the Gibraltar colony. The environmental factors influencing the maintenance of the annual cycles in both localities are examined.

Social factors influencing reproduction in wild lions

The paper summarizes seven years of records of the reproductive history of two wild prides of lions (Panthera leo L.) in the Serengeti National Park, Tanzania. These records are analyzed to demonstrate ways in which lion reproduction is influenced by their social group and by changes in that group.Females gave birth at any time of year; they did so sooner if their previous litter died. Females synchronized births with other pride members. Takeover of the pride by new males resulted in a drop in the birth rate. Most cubs died, before two years old. Birth synchrony resulted in better cub survival. The arrival of new males resulted in an increase in cub mortality. Females came into oestrus synchronously with other pride members. Males had a much longer effective reproductive life if they had male companions.The proximate causes of these features of lion reproduction are considered, and the evolution of aspects of the organization of reproduction in lions is discussed.