Precocial Neonates Research Articles

Development of fetal Eurasian beavers (Castor fiber)

Mammals are categorized along an altricial-precocial spectrum based on degrees of neonatal development. Altricial neonates are immature at birth and dependent on care, whereas precocial neonates are relatively well developed and independent post-partum. The Eurasian beaver (Castor fiber) is a large, semiaquatic, relatively precocial mammal in the order Rodentia. However, the extended care of kits in burrows begs the question of why beavers have precocial characteristics. A study of fetal development might enable understanding of the traits that are significant for neonatal survival. The present study examined external morphological characteristics, external biometry and the development of internal organs in 80 Eurasian beaver fetuses (crown-rump length [CRL], 2.5–19.3 cm) derived from 33 wild pregnant females hunted in Norway (33 gestational age). We also created equations to predict fetal ages from biometric parameters based on a linear relationship between biometric parameters and fetal ages estimated from fetal weight. Fetal features appeared in the following chronological order; eyelid bulbs and tactile hairs (CRL ≥ 7.3 cm), outer ears, claws, skin differentiation (CRL ≥ 8.9 cm), and hair coverage and tooth eruption (CRL ≥ 9.4 cm). All biometric parameters increased linearly and positively as the CRL increased and did not tend to stabilize. Notably, slopes of hindfoot parameters were higher than those of forefeet, suggesting that the hindfeet of beavers grow faster than forefeet, as they do in other semi-aquatic mammals. Our calculations revealed that dorsal length, CRL, thoracic and abdominal circumferences were candidate predictors of fetal age due to a high coefficient of determination (≥ 0.95) and broad range (≥ 10 cm). Our findings revealed that beaver growth was precocial in terms of differentiated skin, hair coverage, and tooth eruption, but not fully completed, as none of the fetuses had open eyes. The rapid growth of the hindfoot and some precocial traits (skin and hair differentiation) may be involved with the ability of neonatal beavers to move in water.

Is a Little Enough? Paucity of Immune Proteins in Serum of Precocial Neonates of a Marine Carnivoran—the Atlantic Grey Seal

Mammalian mothers usually provide their offspring with large quantities of immunoglobulins (antibodies) for circulation in blood, either trans-placentally before birth, via colostrum briefly thereafter, or, less commonly, from milk. Neonates of true, phocid seals, however, are peculiarly impoverished in serum immunoglobulins, the levels of which slowly increase but do not reach adult levels by the time of weaning. We investigated whether grey seal (Halichoerus grypus) neonates compensate through an elevation or rapid maturation in levels of serum innate immune factors, namely acute phase and complement proteins. Instead, their sera contained remarkably low levels of acute phase proteins (including C-reactive protein, haptoglobin, hemopexin, ceruloplasmin, orosomucoid), compared to their mothers, that barely increased to adult levels by weaning. For complement, there was a strong demarcation between the early activation and amplification cascade components (present at normal adult levels in pups) and the late lytic membrane attack complex and regulatory proteins (consistently at low relative levels). Phocid neonates therefore differ dramatically from land Carnivorans, such as dogs and cats, in early life immune protection. That neonatal phocids survive this apparent vulnerability to infections between birth and weaning prompts questions as to what other mechanisms protect them, and the adaptive value of their seeming vulnerability.

Comparative skeletal anatomy of neonatal ursids and the extreme altriciality of the giant panda.

Mammalian neonates are born at a wide range of maturity levels. Altricial newborns are born with limited sensory agency and require extensive parental care. In contrast, precocial neonates are relatively mature physically and often capable of independent function shortly after birth. In extant mammals, placental newborns vary from altricial to precocial, while marsupials and monotremes are all extremely altricial at birth. Bears (family Ursidae) have one of the lowest neonatal-maternal mass ratios in placental mammals, and are thought to also have the most altricial placental newborns. In particular, giant pandas (Ailuropoda melanoleuca) are thought to be exceptionally altricial at birth, and possibly marsupial-like. Here we used micro-computer (micro-computed) tomography scanning to visualize the skeletal anatomy of ursid neonates and compare their skeletal maturity with the neonates of other caniform outgroups. Specifically, we asked whether ursid neonates have exceptionally altricial skeletons at birth compared with other caniform neonates. We found that most bear neonates are similar to outgroup neonates in levels of skeletal ossification, with little variation in degree of ossification between ursine bears neonates (i.e. bears of the subfamily Ursinae). Perinatal giant pandas, however, have skeletal maturity levels most similar to a 42-45-day-old beagle fetus (~70% of total beagle gestation period). No bear exhibits the skeletal heterochronies seen in marsupial development. With regards to skeletal development, ursine bears are not exceptionally altricial relative to other caniform outgroups, but characterized largely by the drastic difference between newborn and adult body sizes. A review on the existing hypotheses for ursids' unique reproductive strategy suggests that the extremely small neonatal-maternal mass ratio of ursids may be related to the recent evolution of large adult body size, while life history characteristics retained an ancestral condition. A relatively short post-implantation gestation time may be the proximal mechanism behind the giant panda neonates' small size relative to maternal size and altricial skeletal development at birth.

Locally elevated cortisol in lymphoid organs of the developing zebra finch but not Japanese quail or chicken

Glucocorticoids are important for production of functional lymphocytes and immunity. In altricial neonates, adrenal glands are unresponsive and local glucocorticoid synthesis in lymphoid organs may be necessary to support lymphocyte development. Precocial neonates, in contrast, have fully responsive adrenal glucocorticoid production, and lymphoid glucocorticoid synthesis may not be necessary. Here, we found that in altricial zebra finch hatchlings, lymphoid organs had dramatically elevated endogenous glucocorticoid (and precursor) levels compared to levels in circulating blood. Furthermore, while avian adrenals produce corticosterone, finch lymphoid organs had much higher levels of cortisol, an unexpected glucocorticoid in birds. In contrast, precocial Japanese quail and chicken offspring did not have locally elevated lymphoid glucocorticoid levels, nor did their lymphoid organs contain high proportions of cortisol. These results show that lymphoid glucocorticoids differ in identity, concentration, and possibly source, in hatchlings of three different bird species. Locally-regulated glucocorticoids might have species-specific roles in immune development.

The placentation of eulipotyphla-reconstructing a morphotype of the Mammalian placenta.

Placentation determines the developmental status of the neonate, which can be considered as the most vulnerable stage in the mammalian life cycle. In this respect, the different evolutionary and ecological adaptations of marsupial and placental mammals have most likely been associated with the different reproductive strategies of the two therian clades. The morphotypes of marsupial and placental neonates, as well as the placental stem species pattern of Marsupialia, have already been reconstructed. To contribute to a better understanding of the evolution of Placentalia, a histological and ultrastructural investigation of the placenta in three representatives of Eulipotyphla, that is, core insectivores, has been carried out in this study. We studied the Musk shrew (Suncus murinus), the four-toed hedgehog (Atelerix albiventris), and the Iberian mole (Talpa occidentalis). As a result, a eulipotyphlan placental morphotype consisting of a compact and invasive placenta was reconstructed. This supports the widely accepted hypothesis that the stem lineage of Placentalia is characterized by an invasive, either endothelio- or hemochorial placenta. Evolutionary transformations toward a diffuse, noninvasive placenta occurred in the stem lineages of lower primates and cetartiodactyles and were associated with prolonged gestation and the production of few and highly precocial neonates. Compared to the choriovitelline placenta of Marsupialia, the chorioallantoic placenta of Placentalia allows for a more intimate contact and is associated with more advanced neonates.

Mother–young vocal communication and acoustic recognition promote preferential nursing in sheep

In mammals with precocial neonates, exclusive maternal care and investment depend on mutual mother-young recognition. In sheep, this is ensured by rapid olfactory recognition of the neonate by its mother. However, recent studies suggest that other processes may participate in preferential maternal care. We investigated the possibility that acoustic communication promotes preferential nursing of the lamb. In the first of two studies, we examined the association between nursing and vocal activity in ewes and their lambs during the first 2 weeks of lactation. As early as 3 and 6 h postpartum, vocal activity was preferentially concentrated before nursing and by day 15 all vocal activity occurred within 2.5 min before nursing. In the second study, we tested the responses of ewes and lambs at 15 days postpartum to the playback of recorded bleats of their partner or from unrelated ewes and lambs. When playback was performed 30 min after a nursing episode, both ewes and lambs responded to bleats of their partner but not to bleats from alien subjects. When playback was performed 5 min after nursing, ewes did not respond to any lamb's bleats, while lambs continued responding to the bleats of their mothers, but significantly less than 30 min after nursing. Nursing therefore appears to play an important role in structuring very early vocal communication between the mother and her neonate. In turn, if the motivational state of the members of the mother-young dyad is adequate, this ensures the display of mutual acoustic recognition and prepares them for preferential nursing before maternal olfactory recognition of the lamb comes into play.

Perinatal life history traits in New World monkeys

Gestation length, neonatal and maternal body weight, and neonatal and adult brain weight data were collected for New World monkeys in an attempt to establish typical patterns of perinatal life history. This study attempts to illuminate the most accurate values from the available data, which suggest that gestation length and prenatal growth rate are broadly conserved in relation to maternal size in New World monkeys. Exceptions to the patterns evident in the data point to derivations in life history strategies. In particular, this study suggests that the extended gestation length of callitrichines is a function of minimum viable neonate size and not exclusively energy minimization associated with simultaneous lactation. Cebus is shown to undergo more postnatal brain growth relative to other New World monkeys, but not as much as previously believed. Alouatta is shown to be relatively small brained at birth as well as in adulthood. Saimiri is shown to present the most unusual package of perinatal life history traits, in which precocial neonates are gestated for a relatively long time and at a slightly faster growth rate than is typical for New World monkeys. © 1996 Wiley-Liss, Inc.

Cellular Aspects of the Stress Response in Precocial Neonates

The extent to which control over adrenal steroidogenic function is established during embryogenesis, and therefore the ability of precocial neonates to withstand stress, is probably an important determinant of breeding success. Studies on the ontogeny of adrenal steroidogenic function in birds, however, have been limited to the chicken Gallus domesticus and the duckling Anas platyrhynchos. Up to the 21st day of embryogenesis, the temporal patterns of adrenal gland development in these species are similar. By the 15th day the adrenal anlage is encapsulated and consists of islands of chromaffin cells distributed throughout a mass of structurally typical steroidogenic cells; at this time the steroidogenic cells are responsive to 1-24 ACTH and they contain small quantities of corticosterone and aldosterone. During the next six days the corticotropic responsiveness increases although the inducible response of cells from the 21 day-old emerging chick embryo is less than that of cells from the 21 day-old duck embryo. In the duckling, corticotropic responsiveness increases further during the next week preceding emergence. Also the steroidogenic cells in the emerging duck embryo, but not those in the emerging chicken embryo, preferentially synthesize aldosterone in response to angiotensin II. Although catecholamines and acetylcholine each suppress basal unstimulated rates of corticosterone and aldosterone release from the steroidogenic tissue, none has an effect on 1-24 ACTHinducible corticosteroid release.

Comparative Reproductive Strategies of Altricial and Precocial Eutherian Mammals

Mammals produce neonates of varying degrees of development described by the terms altricial and precocial. I rank eutherian mammals by a comprehensive measure of development in which neonates are scored in four areas of independence: thermoregulatory, sensory, locomotory and nutritional. The association between neonatal development and nine life-history traits is examined in 239 species. The distribution of neonatal developmental rankings is associated with adult mass and is related to taxonomic level, with precocial neonates more common among orders, and altricial neonates more common among genera and species. When the effect of adult mass is controlled, precocial mammals produce heavier neonates and heavier litters, possess longer gestation periods, attain adult mass more slowly, and have smaller litter sizes. Mass at weaning, length of the total reproductive interval, and age at first parturition do not differ among developmental categories. Although the continuous nature of development is intuitively appealing, mammalian development patterns do not map onto predictable, continuous changes in life-history patterns. Length of the lactation period is extended in precocial primates but shortened in precocial rodents. Neonate mass varies continuously with stage of neonatal development, while litter size varies dichotomously, and age at first parturition and litter mass differ uniquely in only one developmental category. Thus, neonatal developmental patterns do not appear to result from one continuous axis of selection.

Premature visual stimulation accelerates intersenory functioning in bobwhite quail neonates

Recent evidence from both altricial and precocial neonates suggests that premature stimulation of a later developing sensory system may alter the functioning of earlier developing sensory systems. The present study examined the influence of prenatal visual stimulation on postnatal auditory functioning in precocial bobwhite quail chicks. Hatchlings that experienced patterned light during the 24-36 hr prior to hatching did not exhibit a naive auditory preference for their species-specific maternal call at 24 hr or 48 hr following hatching, a reliable phenomenon in chicks not receiving embryonic visual stimulation. To examine whether this lack of responsiveness resulted from enhanced intersensory functioning, hatchlings were tested for preference for both auditory and visual features of the bobwhite hen. Results indicate that prematurely stimulated chicks require species-typical auditory and visual stimulation earlier in postnatal development than do normally reared chicks to direct their filial behavior. These findings point to the importance of normally occurring developmental limitation of sensory input to early species-typical sensory/perceptual organization.

The allometric approach to species differences in brain size

Allometric methods can be used to test quantitative theories of the relationship between brain size and body size across species, and to search for ecological, behavioural, life history, and ontogenetic correlates of brain size. Brain size scales with an allometric exponent of around 0.75 against body size across mammals, but is closer to 0.56 for birds and for reptiles. The slope of the allometric line often varies depending upon the taxonomic level of analysis. However, this phenomenon, at least in mammals, may be a statistical artifact. Brain size for a given body size (relative brain size) varies among orders in birds and mammals, and some dietary associations with relative brain size have been found in particular taxa. Developmental status at birth is the most consistent correlate of relative brain size: precocial neonates have larger brains for a given maternal size than altricial neonates in both birds and mammals. Altricial neonates, however, have more brain growth following birth, and in birds also have larger relative adult brain sizes. Energetic explanations for differences in neonatal brain growth, although attractive on theoretical grounds, have largely failed to stand up to empirical tests.

Reproductive Biology of Ototylomys (Cricetidae)

Reproductive biology of the Neotropical climbing-rat, Ototy- lomys, is described, based on the examination of 86 offspring of animals live- trapped from Campeche, Mexico. Animals were maintained in the Michigan State University Live Animal Colony. Vaginal smears were collected from Ototylomys kept in 14 hours of light and 10 hours of darkness. The average interval between comified cell periods was 8.8 ? 0.5 days. A postpartum estrous was observed for all littering females, as evidenced by the presence of sperm in vaginal smears taken within 24 hours after the discovery of new litters. Females mated as early as 29 days and males as early as 175 days. Gestation period was 52.8 ? 2.1 days. No statistical difference was found between the mean gestation lengths of lactating and nonlactating females. Both minimum and maximum extremes in gestation lengths were observed in lactating females. Embryos were first detected by palpation on day 14 of gestation. The fetal head was initially distinguishable at 28 days. Average litter size of 2.4 young consisted of 46 males and 40 females. The standard measurements, in millimeters, on day one were as follows: total length, 119.5 - 0.9; tail length, 47.1 - 0.8; hind foot, 16.4 ? 0.2; ear, 9.4 ? 0.2; weight, 10.2 ? 0.3 grams. The least variance over time was observed in the length of head and body. At birth, head and body length was 46.4 percent of adult body length. No statistical differences were found between males and females. For approximately 30 days after birth, the very precocial neonates adhere tenaciously to their mother's inguinal teats. The largest number of individuals initially responded to loud noises by day two and had opened their eyes by day six. Hearing preceded eye opening in all but four cases. Ototylomys reach 50 percent of adult body length by day two and 90 percent by 58 days of age. The reproductive biology of Ototylomys was judged to be primitive in form and best adapted for scansorial living. Early efforts to evaluate the possible evolutionary significance of reproduc- tive biology were made by Mossman (1953) and Keys (1958). They proposed that the internal mechanisms of implantation and subsequent development of placental membranes occurred under uniform internal conditions and with little influence from external environment. These characteristics would be more conservative than the usual morphological criteria in current use and therefore may be more evolutionarily significant. Within the cricetid genus, Peromyscus, Layne (1968) found that body size and environment were the most influential factors governing gestation length and postnatal development. To further elucidate evolutionary and reproductive relationships found in rodents, I have examined the reproductive biology of Ototylomnys. The re- sults are described herein and compared to the reproductive biology of other cricetid rodents as reported in the literature. Ototylomys belongs to an assemblage of Neotropical cricetine rodents of obscure ancestry. Ototylomys has been placed in the subfamily Neotominae