Sexual dimorphism in sea lion pups: differential maternal investment,or sex-specific differences in energy allocation?

Proximal mechanisms underlying a faster growth rate in male compared to female California sea lion pups were investigated. Males are significantly larger at birth than females. Specifically, we asked if differential maternal investment contributed to enhanced male growth via: (1) larger mothers having disproportionately more male pups, (2) more time and energy put into foraging by mothers of male pups, and (3) greater milk production in mothers of male pups. We also considered four aspects of differential energy utilization and acquisition by male and female pups: (1) male pups attempting to save energy for growth by changes in behavior, (2) longer suckling bouts with mother and more sneak suckling of non-filial females by male pups, (3) lower maintenance costs in males via a lowered resting metabolic rate, and (4) increased assimilation efficiency in males. Our study showed that there are no differences in the size of females or length of foraging trips for mothers of male and female pups. Male pups received more milk from their mothers, but the difference was no longer significant when the larger body size of males was considered. There were no differences in either the activity budgets or suckling behavior of male and female pups. Male pups, however, did have lower resting metabolic rates than females. We conclude that enhanced male perinatal growth is a consequence of a larger size at birth, proportionally more milk from mothers to support the greater demands of larger body size, and lower maintenance costs due to a lower resting metabolic rate. Received: 28 April 1995/Accepted after revision: 25 July 1995     

Philopatry,reproductive success of females,and maternal investment in the red-necked wallaby

Summary Female red-necked wallabies settle within their mothers' home ranges, apparently for life, while males disperse at about two years of age. However, sons spend much more time with their mothers before dispersing than do daughters of similar ages. Females who associate regularly with their subadult offspring are less likely to reproduce successfully at their next breeding attempt than are females who spend little time with their subadults, and sons therefore impose greater short-term reproductive costs on their mothers than do daughters. Females who are generally gregarious also suffer reduced reproductive success, even though reproductive success is independent of local density. It is suggested that the reproductive costs to females of associating with their subadult offspring, and other relatives, are incurred through tolerance of ecological competition from those kin, and therefore reflect a form of prolonged maternal investment, which is initially heaviest in sons but is sustained for longer periods in daughters. Females produce equal numbers of male and female offspring, and spend equal amounts of time suckling them in infancy.     

Variable within-brood maternal provisioning in newly extruded embryos of Homarus gammarus

Offspring quality of decapod crustaceans has been widely studied, with special emphasis on the sources of variability determining embryonic and larval quality. Nevertheless, maternal provisioning has commonly been overlooked as a potential source of offspring within-brood variability. In the present study, the existence of variable maternal provisioning was assessed through the analysis of the fatty acid (FA) profile of newly extruded embryos from different regions of the brooding chamber of Homarus gammarus. Significant differences in the FA profile of embryos sampled from different pleopods and sides of the brooding chamber were recorded. Significant deviations of the overall mean of each surveyed female were also observed for essential FA, particularly 20:4n-6, 20:5n-3 and 22:6n-3. Lipid energy available to fuel embryogenesis also varied among embryos sampled from different regions of the brooding chamber. Results suggest variable female investment at oocyte production, which may be amplified during the incubation period of developing embryos by differential lipid catabolism. For the first time, maternal provisioning is evidenced as an additional source for within-brood variability in the FA profile of embryos.     

Fuels for development: evolution of maternal provisioning in asterinid sea stars

For marine invertebrates, larval developmental mode is inseparably linked to the nutritional content of the egg. Within the asterinid family of sea stars there have been multiple, independent, evolutionary transitions to lecithotrophic development from the ancestral, planktotrophic state. To investigate the evolution of maternal investment and development within the Asterinidae, we quantified individual lipid classes and total protein for eggs and larval stages of closely related species representing three developmental modes (planktotrophy, planktonic lecithotrophy and benthic lecithotrophy). Within species, maternal provisioning differed between females indicating that egg quality varied with parentage. Maternal investment was related to egg size but, after correcting for egg volume, we identified two major oogenic modifications associated with the evolution of lecithotrophic development: (1) a reduction in protein deposition that probably reflects the reduced structural requirements of nonfeeding larvae, (2) an increase in deposition of a single class of energetic lipid, triglyceride (TG). The exception was Parvulastra exigua, which has benthic, lecithotrophic development and lays eggs with a lipid to protein ratio close to that of planktotrophs. This oogenic strategy may provide P. exigua larvae with a protein “weight-belt” that assists in maintaining a benthic existence. Asterinids with planktotrophic development used a significant portion of egg TG to build a feeding bipinnaria larva. For Meridiastra mortenseni, female-specific differences in egg TG were still evident at the bipinnaria stage indicating that egg quality has flow-on effects for larval fitness. In lecithotrophic asterinids, TG reserves were not depleted in development to the larval stage whereas protein stores may help fuel early larval development. Available data indicate that there may be two evolutionarily stable egg lipid profiles for free-spawning, temperate echinoderms.     

Influence of social factors on sex ratio at birth,maternal investment and young survival in a prosimian primate

Summary In order to determine whether social factors influence sex ratio at birth in lesser mouse lemurs, experiments were conducted during 5 successive breeding periods on 51 females. At the beginning of the breeding season, females were either isolated (I) or grouped (G) in heterosexual groups with an increasing number of females (2, 3 or 4). To ensure mating, I females were introduced in a group only during the oestrous period. After mating, both I and G females were isolated during pregnancy and lactation. Reproductive capacities of females in terms of oestrus occurrences (n = 324), impregnations (n–210), pregnancies (n = 136) or abortions (n = 38) or litter sizes (1–3 young) were affected neither by age and parity of females nor by group housing prior to conception. G females produced significantly more sons than daughters (67% males for 189 newborn) while females living alone except during the mating period demonstrated a significant inverse tendency (39.6% males for 96 newborn). Distribution of sexes in litters was statistically different from random and varied according to the shift of sex ratio at birth. In G females, the shift in the sex ratio towards males was consistent across the different groups, independent of the number of females living together, suggesting that the presence of only 1 female is sufficient to induce a bias in the sex ratio. No correlation was found between infant survival at weaning and age, parity or group housing of the mother. The maternal investment allocated to male or female newborn was similar provided the litter contained at least 1 male. In litters without males, growth and survival of female infants were significantly less. These results on sex ratio bias in captive female mouse lemurs agree with directions of bias predicted by the local resource competition model for facultative sex ratio adjustment (Clark 1978). Nevertheless, the pattern observed in mouse lemurs appears to be independent of the nutritional state of the female and of differential maternal investment.     

The effect of a natural environmental disturbance on maternal investment and pup behavior in the California sea lion

Summary Observed changes in maternal investment due to an environmentally induced decrease in food supply (the 1983 El Ni?o-Southern Oscillation) are compared witha priori predictions for the California sea lion (Zalophus californianus). Changes in behavior, growth and mortality of off-spring were also examined. Data collected in the first two months postpartum for the years before (PRE), during (EN), and the two years after (POST1 and POST2) the 1983 El Ni?o indicate that females initiated postpartum feeding trips earlier during the food shortage, and spent more time away on individual feeding trips in both the El Ni?o year and the year after. Perinatal sex ratios (♀:♂) in the years PRE, EN, POST1 and POST2 were 1:1, 1.4:1, 1.1:1 and 1:1.4, respectively. Fewer copulations were observed during the El Ni?o year, but this difference was not statistically significant. Pups spent less time suckling in the food shortage year and the year following, but attempted to sneak suckle more. Pups were less active and played on land less in the El Ni?o and following year. Finally, maternal investment as measured by milk intake of offspring was decreased, pups grew more slowly, and suffered increased mortality during the food shortage year. Despite expected sex differences in maternal investment and pup behavior in response to food shortage, there were no sex-biased differences in response in either females or pups. As expected, the food shortage did not affect adult males since they migrate north during the non-breeding season where the environmental perturbation was less severe.     

Biparental investment and reproductive success in a subsocial desert beetle: the role of maternal effort

Parastizopus armaticeps is a nocturnal subsocial detritivorous desert tenebrionid that produces very few offspring per brood. The two environmental factors that constrain reproduction, rapid sand desiccation rate and food scarcity, are countered by biparental effort. Males dig and extend breeding burrows, maintaining their moisture level; females forage on the surface at night for high-quality detritus, the larval food. This was shown to be a scarce and unpredictable resource for which there is high competition. When food was supplemented in a field experiment, offspring number and survivorship doubled and burrow failure due to desiccation dropped from approximately half, the typical failure rate for unsupplemented burrows, to zero. Food supplementation did not, however, increase larval foodstore size and there was no difference in the size of the offspring produced. Supplemented females reallocated their time, foraging less and digging more with the male. This change in maternal behaviour patterns resulted in deeper burrows which remained moist longer, thus extending the larval production period. Female foraging efficiency, particularly food retrieval speed, determined how much time females could allocate to digging, consequently increasing the reproductive success of the pair. Burrow depth and sand moisture level at the burrow base were the major correlates of reproductive success, but the scarcity and unpredictability of high-quality food on the surface and the competition for this resource influenced the number of offspring indirectly through their effect on female behaviour. Received: 29 November 1996 / Accepted after revision: 7 December 1997     

Early maternal investment in male and female African elephant calves

Summary The suckling behaviour of 130 freeranging elephant calves aged between birth and 4.5 years old was examined in Amboseli National Park, Kenya. Analyses of frequencies of suckling and durations of suckling bouts showed that males attempted to suckle more often, were more successful at their attempts, and as a result were estimated to have a higher milk intake than did female calves. Mothers were equally tolerant of their sons' and daughters' demands to suckle at young ages, but were less tolerant of their older sons' demands. The growth rates of males based on hind footprint length were faster than those of females from birth onwards. During drought years with low food availability, male calf survivorship in the first year was lower than that of female calves. During wet years, there was little difference between sexes in survivorship. It appeared that during dry years mothers were unable to sustain milk production at a level that met the metabolic requirements of their sons, and as result male calves were more likely to die. Females with a surviving son tended to have a longer interbirth interval than did females with a surviving daughter. We suggest that greater early maternal investment in male calves occurs because, in the highly-competitive polygynous mating system of elephants, size in adult male elephants is an important factor in mating success.     

The influence of maternal rank and infant sex on maternal investment trends in rhesus macaques: birth sex ratios,inter-birth intervals and suckling patterns

Summary In the new colony of rhesus macaques at Madingley, no overall difference was found in the length of the inter-birth intervals following the birth of male and female infants. The lack of overall differences in the reproductive costs of raising sons and daughters, was associated with an absence of differences in suckling patterns between male and female infants. It is argued that similar pre-weaning investment in sons and daughters may be related to the presence of similar growth rates for male and female infants during the first year of life. Most high ranking mothers reproduced in consecutive years, while low ranking mothers were more likely to experience two year long inter-birth intervals. Further analyses revealed that this difference was mainly due to the fact that low ranking mothers always failed to reproduce the year after raising a daughter. Thus, no difference was found in the length of inter-birth intervals between high ranking mothers with infants of either sex and low ranking mothers with sons. The daughters of low ranking females suckled more frequently and making more nipple contacts per bout, and such high nipple stimulation was responsible for the reproductive inhibition experienced by their mothers. It is suggested that the high degrees of nipple stimulation may have been a consequence of the high levels of aggression that low ranking females with daughters have been shown to receive, since their mothers could have allowed frequent ventro-ventral contact in order to protect them. Given that low ranking mothers find daughters reproductively costly to raise, it is possible that such high reproductive costs have played a significant role in the evolution of sex ratio biases at birth. As in other primate populations, in this colony low ranking females produced a greater proportion of sons than daughters, and high ranking mothers showed the opposite trend.     

Indirect effects and traditional trophic cascades: a test involving wolves, coyotes, and pronghorn

The traditional trophic cascades model is based on consumer resource interactions at each link in a food chain. However, trophic-level interactions, such as mesocarnivore release resulting from intraguild predation, may also be important mediators of cascades. From September 2001 to August 2004, we used spatial and seasonal heterogeneity in wolf distribution and abundance in the southern Greater Yellowstone Ecosystem to evaluate whether mesopredator release of coyotes (Canis latrans), resulting from the extirpation of wolves (Canis lupus), accounts for high rates of coyote predation on pronghorn (Antilocapra americana) fawns observed in some areas. Results of this ecological perturbation in wolf densities, coyote densities, and pronghorn neonatal survival at wolf-free and wolf-abundant sites support the existence of a species-level trophic cascade. That wolves precipitated a trophic cascade was evidenced by fawn survival rates that were four-fold higher at sites used by wolves. A negative correlation between coyote and wolf densities supports the hypothesis that interspecific interactions between the two species facilitated the difference in fawn survival. Whereas densities of resident coyotes were similar between wolf-free and wolf-abundant sites, the abundance of transient coyotes was significantly lower in areas used by wolves. Thus, differential effects of wolves on solitary coyotes may be an important mechanism by which wolves limit coyote densities. Our results support the hypothesis that mesopredator release of coyotes contributes to high rates of coyote predation on pronghorn fawns, and demonstrate the importance of alternative food web pathways in structuring the dynamics of terrestrial systems.     

Changes in maternal investment with climate moderate social behaviour in a facultatively social bee

Behavioral Ecology and Sociobiology - Scents play an important role in the life of most terrestrial mammals and may transmit valuable information about conspecifics. Olfaction was long considered...     

Effects of organic additions to sediment,and maternal age and size,on patterns of offspring investment and performance in two opportunistic deposit-feeding polychaetes

The investment made by a reproducing organism in its offspring can be affected by both extrinsic (environmental) and intrinsic (female condition) factors. The purpose of this study, conducted between December 1990 and June 1992, was to examine the influence of organic additions to sediment, and female age and size, on patterns of offspring investment and performance in the opportunistic polychaete Capitella sp. I (cf. Capitella capitata Farbricius). Sediment treatments were composed of marsh mud enriched with sewage or algae, or spiked with #2 fuel oil. All three of these additions are associated with opportunistic responses in Capitella sp. I populations in the laboratory and field. As a means of comparison,effects of sewage additions were also examined on the spionid Streblospio benedicti Webster. Organic additions to mud had no detectable effect on the C or N content of embryos in either species. However, sewage had a positive effect on juvenile performance in Capitella sp. I. Juveniles produced by adult Capitella sp. I in the sewage treatment grew 2 times larger (in 2 wk) than juveniles produced by adults in the mud treatment when these juveniles were raised in the same sediment type (mud). Such effects may facilitate opportunistic responses in Capitella sp. I offspring by reducing time to first reproduction. In addition to treatment sediment effects, maternal age and size had a strong influence on patterns of offspring investment in Capitella sp. I. The material investiment measured in collected embryos declined with maternal age in the oil and sewage treatments. The C:N ratio of embryos increased with maternal age for Capitella sp. I except in the algae treatment, which showed no effect of maternal age. Juvenile growth decreased with maternal age in the sewage treatment for Capitella sp. I. Maternal size appeared to have a positive effect on embryo investment in the mud and oil treatments, where reproducing worms were smallest. Previous studies of Capitella sp. I have documented a broad range of environmentally induced responses in growth and fecundity.The results of this study emphasize the importance of maternal environment, age, and size effects on the relationship between offspring investment and performance.Such effects may have profound consequences for the dynamics of populations and the fitness of individuals. Present address: WES-ES-F, USAE Waterways Experiment Station, 3909 Halls Ferry Rd., Vicksburg, Mississippi 39180-6199, USA     

Sex bias or equal opportunity? Patterns of maternal investment in bison

Summary In polygynous mammals, it may be adaptive for mothers to invest more in sons and/or to adjust the sex ratio of offspring in relation to body condition. Calving patterns were examined over an 8-year period (1982–1989) for a population of Bison bison in which barren females are not selectively culled. From these data, we tested predictions of the sex ratio adjustment hypothesis as well as two assumptions: (1) that offspring weight at the end of the period of parental investment (PI) is correlated with later condition, and (2) that maternal and offspring condition during the period of PI are correlated. In contrast to predictions, there was little evidence that mothers in better condition bear more sons. Short- and long-term measures of maternal condition (previous reproductive status, age, dominance status, pre-pubertal body weight, age at first reproduction, birth date, and the duration of the mother's own suckling period) were little related to offspring sex ratio, although the last calves of old females were nearly always female. Similarly, there was little evidence for sex-biased PI. Weights at about 7 months of age were greater for males than females; males also had somewhat later birth dates, suggesting either longer gestation or later conception. However, maternal reproductive costs, as measured by subsequent fecundity, weight loss, and interbirth intervals, did not vary with calf sex. Both assumptions of the model received some support. However, while maternal condition was correlated with offspring condition, there may be sex differences in investment patterns. Mothers appear better able to influence the condition of daughters than of sons. This sex difference may negate any benefit from male-biased investment.     

Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata

The vertebrate brain is a remarkably plastic organ, which responds quickly to environmental changes. However, to date, studies investigating plasticity in brain morphology have focused mostly on the physical properties of the surrounding environment, and little is known about brain plasticity in response to the social environment. Moreover, sex differences in brain plasticity remain virtually unexplored. Here, we tested how the social environment influenced brain morphology in adult males and females using experimental manipulation of the sex composition of social pairs (same sex vs. mixed sex) in the guppy (Poecilia reticulata). We detected substantial sex-specific plasticity in both the overall brain size (controlling for body size) and separate brain structures. The brain size was larger in males that interacted with females, and female optic tectum was larger in female-only groups. Overall, females had larger olfactory bulbs and cerebellum in comparison to males. While net sexual dimorphism in the brain structure can be explained in light of the known differences in boldness and foraging behaviour between the sexes, our results also support that cognitive demands associated with courtship behaviour can lead to plastic changes in the brain size. Our findings demonstrate that not only social environment can generate rapid, plastic responses in the vertebrate brain but also that such responses can depend strongly on sex.     

Geographic variation in maternal investment: acidity affects egg size and fecundity in Rana arvalis

Environmental-stress-mediated geographic variation in reproductive parameters has been little studied in natural vertebrate populations outside the context of climatic variation. Based on life-history theory, an increase in the degree of environmental stress experienced by a population should lead to (1) a shift in reproductive allocation from fecundity to offspring quality, (2) stronger trade-offs between reproductive parameters, and (3) changes in the relationship between female phenotype and maternal investment. To test these predictions, we investigated geographic variation in maternal investment of moor frogs (Rana arvalis) in relation to breeding site acidity (pH 4-8). We found that mean egg size increased and clutch size and total reproductive output (TRO) decreased with increasing acidity among 19 Swedish moor frog populations. Tests for variation and co-variation in maternal investment and female size and age in 233 females from a subset of four acid origin (AO) and four neutral origin (NO) populations revealed that clutch size and TRO increased with female size in both acid and neutral environments. However, in AO populations, egg size also increased with female size, and clutch size and TRO with female age, whereas in NO populations, egg size increased with female age. The strength of the egg-size-clutch-size tradeoff tended to be stronger in AO than in NO females as expected if the former experience stronger environmental constraints. All in all, these results suggest that environmental acidification selects for investment in larger eggs at a cost to fecundity, imposes negative effects on reproductive output, and alters the relationship between female phenotype and maternal investment.     

Paternal care in the European starling,Sturnus vulgaris: nestling provisioning

The extent to which male birds in polygynous species with biparental care assist in nestling feeding often varies considerably between nests of different mating status. Both how much polygynous males assist and how they divide their effort between nests may have a profound effect on the evolution of mating systems. In this study we investigated how males in the facultatively polygynous European starling Sturnus vulgaris invested in their different nests. The amount of male assistance affected the quality of the offspring. Polygynous males invested as much as monogamous males, but divided their effort asymmetrically between nests, predominantly feeding nestlings of first-mated (primary) females. Although females partly compensated for loss of male assistance, total feeding frequency was lower at primary females’ nests than at monogamous females nests. Secondary females received even less assistance with nestling rearing, and the extent to which males assisted decreased with the length of the interval between the hatching of the primary and secondary clutches. These results are contrasted with those from a Belgian populations of starlings with a much more protracted breeding season and thus greater opportunities for males to attract additional mates during the nestling rearing period. The results show that both the “defence of male parental investment model” and the “asynchronous settlement model” have explanatory power, but that their validity depends on the potential length of the breeding season. Received: 21 July 1995/Accepted after revision: 13 July 1996     

Evidence of equal maternal investment in the sexes in the polygynous and sexually dimorphic grey seal (Halichoerus grypus)

In polygynous and sexually dimorphic mammals, parents may be expected to bias their investment towards sons because variation in reproductive success is usually higher among males than among females. Moreover, male reproductive success often depends on adult body size, which, in turn, may depend on the level of parental investment. We therefore predicted that in the grey seal (Halichoerus grypus), a polygynous and sexually dimorphic phocid seal, females should invest more in individual sons than in individual daughters. We found that male pups were born heavier than female pups, but that the growth rates and suckling behaviour were similar for the two sexes. The growth rates and the birth weights were not correlated for the pups of either sex. Mothers did not behave differentially towards offspring of the two sexes, except that mothers of male pups spent more time in visual contact with their pups. Male and female pups had similar activity levels and begged at similar rates. We argue that reports of equal expenditure on the two sexes can be accepted as evidence of equal investment, provided that three assumptions are fulfilled. First, parental care must be costly to the parent. Second, energy expenditure must be the most important component of parental investment. Third, there must be no negative correlation between maternal body condition and the ratio of sons to daughters produced. We argue that these assumptions are met in our study, and that our results provide evidence of equal maternal investment in the sexes in grey seals.     

Recolonizing wolves and mesopredator suppression of coyotes: impacts on pronghorn population dynamics.

Food web theory predicts that the loss of large carnivores may contribute to elevated predation rates and, hence, declining prey populations, through the process of mesopredator release. However, opportunities to test predictions of the mesopredator release hypothesis are rare, and the extent to which changes in predation rates influence prey population dynamics may not be clear due to a lack of demographic information on the prey population of interest. We utilized spatial and seasonal heterogeneity in wolf distribution and abundance to evaluate whether mesopredator release of coyotes (Canis latrans), resulting from the extirpation of wolves (Canis lupus) throughout much of the United States, contributes to high rates of neonatal mortality in ungulates. To test this hypothesis, we contrasted causes of mortality and survival rates of pronghorn (Antilocapra americana) neonates captured at wolf-free and wolf-abundant sites in western Wyoming, USA, between 2002 and 2004. We then used these data to parameterize stochastic population models to heuristically assess the impact of wolves on pronghorn population dynamics due to changes in neonatal survival. Coyote predation was the primary cause of mortality at all sites, but mortality due to coyotes was 34% lower in areas utilized by wolves (P < 0.001). Based on simulation modeling, the realized population growth rate was 0.92 based on fawn survival in the absence of wolves, and 1.06 at sites utilized by wolves. Thus, wolf restoration is predicted to shift the trajectory of the pronghorn population from a declining to an increasing trend. Our results suggest that reintroductions of large carnivores may influence biodiversity through effects on prey populations mediated by mesopredator suppression. In addition, our approach, which combines empirical data on the population of interest with information from other data sources, demonstrates the utility of using simulation modeling to more fully evaluate ecological theories by moving beyond estimating changes in vital rates to analyses of population-level impacts.