Maternal Body Size Research Articles

Patterns of Reproductive Allocation: Clutch and Egg Size Variation in Three Freshwater Turtles

Understanding the mechanisms and patterns of how energy is allocated into the reproductive components of offspring size and number is central to life-history theory. We used X-ray photographs from a long-term mark recapture study of Kinosternon subrubrum, Sternotherus odoratus, and Pseudemys floridana to investigate hypotheses concerning variation in reproductive allocation due to constraint on egg size, withinfemale variability (within and among clutches), interannual environmental variation, multiple annual clutches, allocation of continuous resources into small integer numbers of offspring (fractional offspring-size problem), and age. Patterns of reproductive allocation varied markedly within and among species. Overall, egg size varied as a function of maternal body size and age, intra-annual clutch frequency, the fractional offspring-size problem, and environmental variation. Clutch size varied with maternal body size, clutch frequency, and environmental variation. We examine how effectively the data support optimal-egg-size and phenotypic-plasticity models of reproductive allocation, and identify limitations of fundamental biological findings necessary to address the issues.

Intra‐individual variation in clutch and offspring size in an oviparous snake

AbstractIntra‐individual variation can be extremely informative in understanding the evolution of life‐history traits. In this study, we examined intra‐individual variation in clutch and offspring size for brown house snakes Lamprophis fuliginosus, a species that can lay up to six clutches in the laboratory within a 12‐month interval without a refractory period. The number of clutches produced per female during this interval ranged from two to six, and there was no significant relationship between the total number of clutches laid and maternal body size. Unlike results from lizards and turtles, house snakes showed no significant changes in clutch size or offspring size among successive clutches, and individual repeatability of both traits was moderate to high. House snakes in this study also showed a strong negative relationship between clutch size and offspring size for all clutches produced, as expected by life‐history theory. Our data indicate that house snakes show much less intra‐individual variation than most other reptile species examined. However, this high level of consistency may be due to regulation of food availability under laboratory conditions. This will be varied in future experiments to test the degree of plasticity exhibited by individual females for these traits.

Relationship between egg features and maternal body size in the simultaneous hermaphrodite Oxynoe olivacea (Mollusca, Opisthobranchia, Sacoglossa)

This paper provides information on spawn morphology and egg features of the stenophagous planktotrophic Mediterranean sacoglossan Oxynoe olivacea. Smith and Fretwell’s hypothesis, predicting that individuals of the same population growing in the same environmental conditions and varying in size should spawn eggs of a constant size, was tested in a population of O. olivacea living in the Straits of Messina. To determine whether (a) spawn mass size, (b) total egg number per spawn, and (c) egg size were related to parent size of O. olivacea, 21 egg masses (seven egg masses deposited by seven different 20 mm animals, seven egg masses deposited by seven different 25 mm animals and seven egg masses by seven different 30 mm animals) were randomly chosen and examined. Results showed that both spawn mass width and number of eggs per spawn mass increased across O. olivacea body size and apart from the significant variation of the short capsule diameter, there was no consistent variation of egg features in O. olivacea. In conclusion the species allocates constant amounts of energy to individual embryos and thus supports the prediction designed by Smith and Fretwell.

Oviposition vs. offspring fitness in Aphidius colemani parasitizing different aphid species

AbstractWe measured the acceptance and suitability of four aphid species [Aphis gossypii Glover, Myzus persicae (Sulzer), Rhopalosiphum padi (L.), and Schizaphis graminum (Rondani)] (Homoptera: Aphididae) for the parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Female parasitoids parasitized fewer R. padi than the other three aphid species, and fewer offspring successfully completed development in R. padi than in the other three host species. Sex ratios of emerging adults were more male‐biased from R. padi than from the other three aphid species, suggesting that R. padi is a poor quality host for this population of A. colemani. Ovipositing A. colemani encountered R. padi at a slower rate, spent more time handling R. padi, and parasitoid offspring died at a higher rate in R. padi compared to A. gossypii. Our results show that oviposition behavior and offspring performance are correlated. In each experiment, we tested the effect of the host species in which the parasitoids developed (parental host) on the number of hosts attacked, the proportion of each host species accepted for oviposition and the survival of progeny. Parental host affected maternal body size and, through its effect on body size, the rate of encounter with hosts. Other than this, parental host species did not affect parasitism.

Are Density-dependent Effects on Elasmobranch Maturity Possible?

Fecundity and size at first maturity of elasmobranchs are believed to be limited by body size, making density-dependent effects on these life history traits unlikely. To examine the potential for density-dependent effects on size at first maturity, female spiny dogfish (Squalus acanthias) off the northeast coast of the United States were examined to determine both the presence of free embryos, fertilized eggs, or ovarian eggs, and the number of free embryos in each female in relation to maternal body size during 1998–2002. Severe biomass declines of the adult female portion of the population preceded and continued throughout the study period. Since the period of high abundance in the late1980s, size at first maturity has declined from 75 cm to 66 cm and the median size at maturity (L50) has declined from 85 cm to 79 cm; however, the relationship between number of free embryos and maternal length has not changed.

THE EVOLUTION OF LACTATION STRATEGIES IN PINNIPEDS: A PHYLOGENETIC ANALYSIS

Pinnipeds are a diverse group of aquatic carnivores that exhibit wide variation in body size, milk composition, lactation strategies, and the length of maternal care. We used 12 pinniped life‐history and ecological traits to test hypotheses concerning the influence of phylogeny, maternal body size, breeding substrate, and other factors on the evolution of lactation strategies. We used independent contrasts to account for phylogenetic effects on correlations between traits. Our findings indicate that the negative relationships between maternal mass and lactation length and between maternal mass and the percentage of time spent at sea by females during lactation are not recent adaptations, but likely a result of phylogenetic history and an evolutionary grade shift in lactation length, which occurred when the phocids diverged from the otariids. Differences in body size between the ancestral phocid and otariid impacted their foraging strategies and metabolic rates, which subsequently influenced lactation strategies. The fat‐storage abilities of large phocids may have allowed them to exploit remote and patchy prey resources and thereby reduce time spent feeding during lactation. We also suggest that an early divergence in the mammary gland structure of phocids and otariids is a fundamental influence on pinniped lactation strategies. Although estimates are lacking for several key species, body size appears to have little adaptive influence on the lactation length of extant species. Instead, an abbreviated lactation period seems to be adaptive in minimizing the relative milk energy expended over lactation, although it may have initially evolved to reduce maternal overhead, especially in ancestral fasting phocids. Subsequently, a brief lactation in phocids was also selected through the effects of terrestrial predation, the instability of breeding on pack‐ice, and the energy benefits of increasing milk energy output.

POPULATION CYCLES IN THE PINE LOOPER MOTH: DYNAMICAL TESTS OF MECHANISTIC HYPOTHESES

The forest insect pest Bupalus piniarius (pine looper moth) is a classic example of a natural population cycle. As is typical for populations that exhibit regular oscillations in density, there are several biological mechanisms that are hypothesized to be responsible for the cycles; but despite several decades of detailed study there has been no definite conclusion as to which mechanism is most important. We evaluated three hypotheses for which there was direct experimental evidence: (1) food quality (nutritional value of pine needles affected by defoliation); (2) parasitoids (trophic interactions with specialist parasitoids); and (3) maternal effects (maternal body size affects the performance of offspring). We reviewed the empirical evidence for each of these hypotheses and expressed each hypothesis in the form of a mechanistic dynamic model. We used a nonlinear forecasting approach to fit each model to three long‐term population time series in Britain that exhibit some degree of regular cycling, and we used parametric bootstrap to evaluate the significance of differences between models in their goodness of fit to the data. The results differed among the three forests: at Culbin, the parasitoid and maternal effects models fit equally well; at Roseisle, the food quality and maternal effects models fit equally well; and at Tentsmuir, the parasitoid model fit best. However, the best‐fit parasitism models required that the parasitism rate vary between nearly 0 and nearly 1 during a cycle, greatly exceeding the range of parasitism rates that have been observed in the field. In contrast, the required variation in the observable maternal quality variable (pupal mass) was within the range of empirical observations. Under mild constraints on the parasitism rate (though allowing a much wider range than has been measured in B. piniarius at any location), the fit of the parasitism model fell off dramatically. The maternal effects model then had uniformly strong support, outperforming the constrained parasitism model at all three sites and the food quality model at two; it performed slightly better than the food quality model at the remaining site. This represents the first system in which the maternal effects hypothesis for population cycles has been supported by both strong biological and dynamical evidence.

Reproduction and feeding of the colubrid snake Tomodon dorsatus from south-eastern Brazil

AbstractBody size, sexual dimorphism, reproductive cycles, fecundity, diet and feeding behaviour of the colubrid snake Tomodon dorsatus from south-eastern Brazil were studied. Females of this viviparous species attained larger body sizes than males, the latter maturing with smaller body size than the former. Vitellogenesis occurred at the onset of rainy season, ovulation by mid rainy season, and parturition from late dry to early rainy season. Reproductive cycle was extended, maybe as a consequence of the low metabolism and food intake. Litter size ranged 4-26 offspring and was correlated with maternal body size. Relative clutch mass ranged 0.48-0.82, and neonates ranged 12-17 cm in snout-vent length. Tomodon dorsatus was shown to feed exclusively on veronicellid slugs quickly swallowed by long excursions of the specialized upper jaw units.

An alternative hypothesis to the obesity epidemic: Obesity is due to increased maternal body size, birth size, growth rate, and height

A new hypothesis for dealing with the obesity epidemic is based on changing several factors normally considered desirable by the medical community. These factors include reductions in pre-pregnancy maternal weight, modest reduction of infant birthweight, slower childhood and adolescent growth and reduced caloric intake from infancy through adulthood. The underlining roots for the obesity epidemic involve raised levels of insulin, insulin-like growth factor-1 and cell proliferation which are subject to human control. The implication of this hypothesis is that current measures are inadequate unless a much more comprehensive response is implemented to deal with the obesity epidemic.

Separating within and between effects in family studies: an application to the study of blood pressure in children.

In epidemiology the analyses of family or twin studies do not always fully exploit the data, as information on differences between siblings is often used while between-families effect are not considered. We show how cross-sectional time-series linear regression analysis can be easily implemented to estimate within- and between-families effects simultaneously and how these effects can then be compared using the Hausman test. We illustrate this approach with data from the Uppsala family study on blood pressure in children with age ranging from 5.5 to 12.3 years for the younger and from 7.5 to 13.8 years for the older siblings. Comparing the effect of differences in birth weight on blood pressure within-family (in full siblings) and between-families (in unrelated children) allows us to study the contributions of fixed and pregnancy-specific maternal effects on birth weight and consequently on blood pressure. Our data showed a 0.88 mmHg decrease (95 per cent confidence interval: -1.7 to -0.03 mmHg) in systolic blood pressure for one standard deviation increase in birth weight between siblings within a family and 0.88 mmHg (95 per cent confidence interval: -1.6 to -0.2 mmHg) decrease in systolic blood pressure for one standard deviation increase in birth weight between unrelated children. These estimates were controlled for sex, age, pubertal stage, body size and pulse rate of the children at examination and for maternal body size and systolic blood pressure. The within- and between-families effects were not significantly different, p = 0.19, suggesting that fixed and pregnancy-specific factors have similar effects on childhood systolic blood pressure.

Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae)

AbstractDissection of 286 specimens of the Bothrops neuwiedi pubescens, combined with data on captive individuals, provided information on the reproductive biology of this viperid snake from southern Brazil. Females attained larger body sizes than males, and reproduction was seasonal with mating taking place in autumn when males were more frequently encountered. Vitellogenesis occurred from summer to spring (January-September), sperm storage during autumn and winter (May-September), ovulation and fertilization in early spring (September), embryonic development during middle spring and summer (October-March), and parturition in the summer (January-March). Embryonic development was estimated to last from three to five months, a shorter time than was previously reported. The number of offspring of Bothrops neuwiedi pubescens born in one litter can vary from four to 25 (x = 11). Fecundity is correlated with maternal body size. Neonates measure 17-25 cm SVL. Inferred growth rate of juveniles was low (10 mm/month in first year), with males attaining sexual maturity at about 16 months, but maturity is delayed in females for at least two additional years.

Reproductive biology of the invasive Asian freshwater leech Barbronia weberi (Blanchard, 1897)

Barbronia weberi were collected from Hydrilla verticillata purchased from aquarium suppliers in Melbourne, Australia and additional B. weberi were obtained from aquatic plants in Canberra, ACT, Australia. Adult leeches fed Tubifex sp. ad libitum successfully reproduced under laboratory conditions (21 ± 5 °C ). Reproductively mature B. weberi produced cocoons every week for up to three months at which time the adults began to senesce. Cocoons contained one to five (barx=2.41±0.78 SD, N=58) eggs with juveniles leaving the cocoon within 27 ± 3.4 SD days (N=13) of cocoon production. Juvenile B. weberi reached reproductive maturity within four months (N=7) of hatching and had a maximum growth rate of 1.10 mm2 d−1 once they left the cocoon at around 30 days. Individual egg volume (r=0.63, scaling exponent = 1.21) and cocoon volume (r=0.65, scaling exponent = 1.24) showed a significant (P<0.001) and nearly isometric relationship when scaled with maternal body size. Because this species can grow rapidly and produce a large number of eggs over a short period of time and can piggyback with plant species and travel through the aquarium trade, there is potential for B. weberi to rapidly invade new localities.

Mothers influence offspring body size through post-oviposition maternal effects in the redbacked salamander, Plethodon cinereus.

In the terrestrial salamander (Plethodon cinereus), previous work has shown that mother's body size is positively correlated to offspring size at the time of hatching even after controlling for the effects of egg size. This study was designed to determine whether maternal body size affects offspring size via pre-oviposition factors (e.g., yolk quality, jelly coat composition, or maternal genes) or post-oviposition factors (e.g., parental care behaviors, parental modification of environment). Gravid females were captured and induced to lay eggs in experimental chambers in which the environment was standardized. Fifteen clutches were exchanged, or cross-fostered, between female pairs differing in body size. Ten females whose eggs were taken away and then returned served as controls for the crossing treatment. Foster mothers did not significantly differ from control mothers in the time spent with eggs, body position, or number of egg movements during brooding. Average egg mass measured midway through development was not significantly correlated to the body size of either the genetic or foster mother, but was correlated to pre-oviposition oocyte size. At hatching, offspring body length was positively correlated to egg size and the foster mother's body size. This correlation suggests that in P. cinereus post-oviposition maternal effects have a greater impact on offspring size than other maternal factors incorporated into the egg prior to oviposition. While our study showed that larger mothers moved their eggs less often and tended to spend more time in contact with their eggs, further work needs to be done to identify the specific mechanisms through which larger mothers influence the body size of their offspring. This is the first experimental demonstration of post-oviposition maternal effects for any amphibian with parental care.

Reproductive Biology, Mating Aggregations, and Sexual Dimorphism of the Argentine Boa Constrictor (Boa constrictor occidentalis)

We provide data on sexual dimorphism, reproductive biology, and mating aggregations of the Argentine Boa Constrictor (Boa constrictor occidentalis), a poorly known, threatened species. Snakes were examined by ultrasound scanning between 1998 and 2001. Adult females were 14% longer and 51% more massive than adult males. Litter size averaged 25.05 and increased significantly with maternal body size. Reproductive activity was seasonal and associated, with vitellogenesis and spermatogenesis occurring during the dry season (April to September). The ratio of reproductive to nonreproductive females was 1:1, suggesting females do not reproduce annually in this population. Reproductive females were in better body condition (mass relative to body length) than nonreproductive females, indicating that a female's initial “decision” to reproduce in any given year may be driven by her body condition (storing enough energy for a long period before expending it on reproduction: “capital breeder”). Aggregated boas were found only during the dry season. The high proportion of solitary reproductive males and the operational sex ratio (male:female, 1.53:1) suggests a system of “prolonged mate-searching polygyny.”

Sources of variation in larval quality for free-spawning marine invertebrates: Egg size and the local sperm environment

Summary There has been growing interest in the effects of variation in larval quality on the post-larval performance of adult marine invertebrates. Variation in egg/larval size is an obvious source of variation in larval quality but sources of variation have received little attention. For broadcast spawners, larval size may vary according to the local sperm environment but the generality of this result is unclear. Here, we show that, for a solitary ascidian, a polychaete and an echinoid, larval size is affected by the concentration of sperm present during fertilization. Larvae that are produced at high sperm concentrations are smaller than larvae that are produced from eggs exposed to low sperm concentrations. We also show that for three ascidians and an asteroid, egg size increases with maternal body size. These differences in larval size are likely to affect larval and subsequent adult performance in the field. Given that sperm concentrations in the field can fluctuate widely, it is likely that larval quality in free-spawning marine invertebrates will also vary widely.

Nicotine consumption before and during pregnancy affects not only newborn size but also birth modus.

The associations between cigarette smoking before and during pregnancy and maternal body size (pre-pregnancy weight status, end of pregnancy weight status, weight gain during pregnancy) and newborn size (birth weight, length, head circumference, arcomial circumference), as well as birth modus, were tested in 7803 single full-term births in Vienna. Nicotine consumption before and during pregnancy was found to be associated with smaller and lighter newborns, although maternal weight status and weight gain during pregnancy was significantly higher in smokers. Furthermore, a higher incidence of Caesarean sections was found in smokers. A reduction in the number of daily smoked cigarettes was associated with a lower percentage of low weight newborns (<2500 g).

Sequential deposition of yolk components during oogenesis in an insect, Aedes aegypti (Diptera: Culicidae)

Vitellogenesis in Aedes aegypti of uniform body size was followed at 27 °C in narrow time intervals throughout their first reproductive cycle by measuring the length, diameter, and volume of follicles and oocytes, the latter as an expression of the yolk mass (vitellus). Independent of all experimental conditions, a two-step process of elongation was recognized for both follicle length and yolk length, so that growth curves were consistently composed of two linear regressions with different slopes against time. Follicle lengths started to increase immediately after the blood meal, while oocytes took up to 6 h to show a measurable increase in yolk length. The first linear phase continued until 30 h, when yolk length reached 268±22 μm. At this point, a transition occurred where the linearity shifted sharply for the next 6 h to 2–4-times higher slopes for both regressions. This second growth phase represented a 40% elongation of oocytes and follicles. Then, both curves leveled off at their final size, characteristic of mature ovaries: 462±10 μm for oocytes, 489±11 μm for follicles. These values remained constant until oviposition. The first linear growth phase was associated with an equicaloric and synchronous protein and lipid incorporation into the oocytes; levels of these substances reached their maximum by the end of this first phase and remained constant until oviposition. The second linear growth phase was characterized by rapid glycogen incorporation into oocytes from 20 to 100% of the maximum. Subsequently, the surface pattern of the exochorion became visible, marking the end of yolk incorporation. Since eggs are always laid on moist substrates, within 2–3 h of oviposition they double in volume and fresh weight, driven by more than tripling of their water content. When blood-fed females were exposed to five different temperatures between 17 and 37 °C, the distinction between the two linear growth phases persisted, but the slopes of the respective regressions, and therefore their durations, were affected. Eggs still matured at 37 °C but never hatched and at 12 °C only 18% hatched, whereas at all the intermittent temperatures hatching was 80–90%. Oogenesis appears to be limited to the range between 12 and about 32 °C. The effects of age, maternal body size and the source of the blood on vitellogenesis were also examined. These parameters affected the onset and/or extent of oogenesis in various ways.

Measures of reproductive allometry are sensitive to sampling bias

SummaryIn both interspecific and intraspecific comparisons, maternal body size is the strongest predictor of fecundity for many kinds of animals. However, it has not been widely appreciated that the usual empirical descriptors of this relationship (correlation coefficient, slope andP‐value of the linear regression between maternal body size and offspring number) are sensitive to a factor that is very labile and subject to methodological bias: the degree of maternal investment, specifically the ratio of litter mass to maternal body mass (relative clutch mass, RCM).Samples of females used to assess reproductive allometry may often be biased with respect to RCM. For example, RCMs may vary through time within a single population as a consequence of prey availability, or may vary geographically among populations. Also, females with low RCMs may be more difficult to capture, or may be discarded by researchers who do not realize that they are reproductive.Our analyses on 173 litters of aspic vipers (Vipera aspisLinné) from central western France show that estimates of reproductive allometry are very sensitive to RCM: samples composed of high‐RCM females show a positive and highly significant reproductive allometry, whereas samples composed of low RCM females do not. Conclusions also depend on the method of regression analysis used. This result has strong implications for methodology (i.e. selection of samples, choice of analytical methods and timescales of study) in this field of research.

Capital‐breeding and reproductive effort in a variable environment: a longitudinal study of a viviparous snake

1 The ways that fluctuations in prey abundance and weather conditions can affect reproductive output in a ‘capital breeding’ ectotherm, the aspic viper (Vipera aspis) were examined. 2 Our longitudinal study confirms that female aspic vipers adjust reproductive investment by integrating allocations of energy from stores (‘capital’) and facultative feeding (‘income’). Thus, long-term energy storage enabled females to reproduce successfully even in years when prey were scarce. 3 Not surprisingly, temporal changes in body reserves of female vipers preparing for reproduction depended upon current feeding rates. However, the mean environmental temperature during the active season also affected mass gain. 4 Allometric patterns suggest that reproductive output was limited by energy availability in 8 out of the 9 years of our study. In the other year, high prey availability in the preceding season meant that reproductive output was maximized within the constraints set by maternal body size (and thus, abdominal volume). 5 High summer temperatures increased basking opportunities of gravid vipers and thus accelerated gestation. However, maternal metabolic costs also increased in such situations, resulting in low postpartum body condition.

HIV status and sociodemographic correlates of maternal body size and wasting during pregnancy.

To examine HIV status and sociodemographic variables as correlates of body size (height, body mass index (BMI), and mid-upper-arm circumference (MUAC)) and wasting (MUAC <22 cm) in pregnant women. Cross-sectional study. Four antenatal clinics in Dar es Salaam, Tanzania. Women presenting for first prenatal visit before the 23rd week of gestation, between April 1995 and July 1997 (n=13 760). Mean MUAC, BMI and height were 25.5 cm, 23.5 kg/m(2) and 155.1 cm, respectively. The prevalence of HIV infection was 13.1% and the overall prevalence of wasting was 4.7%. Wasting was 34% (95% CI=3%, 73%) more prevalent among HIV-infected than in uninfected mothers, after adjusting for week of gestation, height and sociodemographic indicators. The risk of wasting associated with HIV infection was highest among women with low level of education or unable to contribute to the household income. From a multiple linear regression model, BMI was positively associated with mother's age, level of education and money spent on food, but not with HIV infection, after adjusting for week of gestation. In multivariate analysis, height increased monotonically by categories of maternal age and level of education, and was also positively correlated with the ability to contribute to household income, the amount of money spent on food per person per day, and having a professional partner. HIV infection is a significant risk factor for wasting among pregnant women, particularly in groups of low socioeconomic status (SES). SES indicators are strongly correlated with maternal height and with BMI during the first and second trimesters of pregnancy independently of HIV status. The National Institute of Child Health and Human Development (NICHD R01 32257), and the Fogarty International Center (NIH D43 TW00004).