Lactation performance of guinea pigs (Cavia porcellus) does not respond to experimental manipulation of pup demands

To ensure proper development of young, mothers should react to offspring signals of need. Studies of such parent-offspring interaction often manipulated litter size to measure effects of changed offspring food demand. We used the extreme precociality of guinea pig (Cavia porcellus) pups to increase offspring demand without changing any other litter characteristic. As pups contribute to their own energy demands from birth by independent feeding, their food demand can be increased by withholding solid food early in lactation. We studied whether mothers reacted to increased food demand of offspring by enhanced parental care, especially by changes in the pattern of milk production and nursing. Pups deprived of solid food early in lactation grew more slowly and were in poorer body condition than pups in control litters, even after the former had access to solid food in late lactation. Mothers of deprived young reacted to offspring long-term need by maintaining nursing behaviour for longer than control mothers. However, this change in behaviour did not occur early in lactation when pup short-term need was greatest nor did it result in increased milk transfer at any time. Energy allocation of mothers measured by changes in their food intake, maternal body reserves, and milk production stayed the same whether offspring had early access to solid food or not. Thus mothers did not increase energy allocation to pups even though they apparently had information about the pups' poor state.     

Sibling competition in guinea pigs (<Emphasis Type="Italic">Cavia aperea</Emphasis> f. <Emphasis Type="Italic">porcellus</Emphasis>): scrambling for mother’s teats is stressful

Lactation is the most energy-intense period in the life of a female mammal. This can cause severe conflict between mother and offspring over the duration of lactation but also between siblings over the amount of milk each pup gets from its mother. Thus, competitive interactions between siblings are expected, and competition is likely to increase with litter size, particularly in species where the number of offspring exceeds the number of teats. We studied sibling competition in the domestic guinea pig (Cavia aperea f. porcellus), which has two teats, but frequently bears litters of up to five pups. By cross-fostering we created non-competition (control) litters with two pups and competition litters with four pups and observed nursing behaviour on days 5, 10, 15 and 20 postpartum. Pups of larger litters had lower growth rates, indicating increased competition among siblings in these litters. Pups of larger litters had to wait longer for access to a teat and spent less time suckling than pups of smaller litters but ate more solid food instead. Additionally, we manipulated the individual short-term need of pups by separating half of the pups of each litter for 2 h from their mothers before observation. Within a litter, hungry pups achieved access to milk faster and spent more time suckling than non-hungry pups. Pups competed mostly by scramble competition. Aggressive interactions occurred only in large litters. Pups of large litters had higher cortisol levels than pups in small litters. These effects decreased with age as pups became increasingly independent of maternal milk. Pup behaviour appears to fit better with models of scramble competition than with those of honest signalling. This contribution is part of the special issue “Sibling competition and cooperation in mammals” (guest editors: Robyn Hudson and Fritz Trillmich).     

Costs and benefits of communal rearing to female prairie voles (<Emphasis Type="Italic">Microtus ochrogaster</Emphasis>)

Communal rearing of offspring may help mothers maximize their investment in offspring at a reduced cost to their own bodily condition, thus maximizing their potential for reproductive success. The objective of this study was to quantify the costs and benefits of communal rearing to prairie vole (Microtus ochrogaster) pups and mothers. Mothers were assigned to one of three social units: solitary mothers, singularly breeding groups (i.e. one mother and one non-reproductive sister) and plurally breeding groups (i.e. two lactating sisters). For each type of social unit, some replicates were provided with food ad libitum, while others were provided with limited food. The body mass of focal mothers (i.e. the first mother to produce a litter) was a significant predictor of pup growth. Regardless of food availability, litters of focal mothers in plurally breeding groups gained more weight than litters reared by solitary mothers. Pups reared in singularly breeding groups were intermediate in weight gain, but did not gain significantly more weight than solitary offspring. There was no difference in the body mass of focal mothers from each type of social unit, regardless of food availability. Within plurally breeding groups, the weight gain of the two litters and body mass of focal and second mothers did not differ. However, focal mothers from plurally breeding groups nursed fewer pups than solitary mothers and also fewer pups than their nestmates when food was limited. Our results suggest that plural breeding results in greater fitness to mothers than solitary and singular breeding.Communicated by E. Korpimäki     

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.     

Weaning in the guinea pig (<Emphasis Type="Italic">Cavia aperea</Emphasis> f. <Emphasis Type="Italic">porcellus</Emphasis>): Who decides and by what measure?

Offspring should be selected to influence maternal effort to maximize their own fitness, whereas mothers are selected to limit investment in present progeny. In mammals, this leads to a conflict over the amount of milk provided and the timing of weaning. The intensity and time course of such conflict has so far mostly been investigated experimentally in altricial rodents. However, it is expected that offspring options for conflict will depend on developmental state. We therefore investigated in the highly precocial domestic guinea pig (Cavia aperea f. porcellus) who decides over nursing performance and weaning and how pup state influences these decisions. Specifically, we tested whether a threshold mass of pups predicts weaning time. By exchanging older litters against neonates and vice versa, we produced a situation in which females differed in lactational stage from the cross-fostered pups. Our results indicate that females decide about the timing of weaning, as cross-fostered younger pups were weaned at a much younger age than controls and older pups benefited from continuing lactation of foster mothers. Growth rates did not differ in the treatment groups, and different weaning ages resulted in differing weaning mass refuting the hypothesis that weaning is based on a threshold mass of offspring. This constitutes clear evidence that in a precocial rodent, the guinea pig, decisions about maternal care are primarily determined by maternal state and little influenced by pup state despite the extreme precociality of offspring. We suggest that precocial pups show little resistance to early weaning when food is abundant, as they reach sufficient nutritional independence by the middle of lactation to enable independent survival.     

Effectiveness of territorial polygyny and alternative mating strategies in northern fur seals, <Emphasis Type="Italic">Callorhinus ursinus</Emphasis>

We conducted a 6-year longitudinal behavioral and genetic investigation of a highly polygynous pinniped, the northern fur seal (Callorhinus ursinus), to determine the contribution of terrestrial polygyny to male fertilization success and to assess the occurrence of alternative mating strategies. Genetic samples from 37 adult males, 50 adult females, and 85 pups were collected and genotyped using five polymorphic microsatellite loci. Pup paternity was assigned using Cervus 2.0 at 99% confidence level. Paternity of 83 pups (98%) was assigned to terrestrial males who held territories or stayed temporarily in the study area during the breeding season when fertilization occurred. For 56 pups of which attendance records of their mothers were available, paternity of 45 pups (80%) was assigned to the associate males in whose territory their mothers stayed during the perioestrus period. In addition to defending breeding territories, territorial males have often been observed attempting to forcibly abduct adult females from adjacent territories (female stealing): We observed a total of 95 such cases, in which the stealers had significantly fewer females than the territorial males from whose territories they stole females. Our results indicate that terrestrial resource-defense polygyny is the major mating system in this species and that nonassociated paternity occurs mostly as a result of alternative mating strategies of less successful males. Male northern fur seals thus appear to adopt conditional alternative strategies that depend on their current social status to maximize their life-time reproductive success.     

Maternal state affects intestinal changes of rat pups at weaning

Two treatments of hooded rat (Rattus norvegicus) mothers after the birth of their pups affected the stage of development at which their pups started to take solid food and showed an increase in the expression of sucrase, an enzyme needed for digesting solid food. The pups of mothers that became pregnant in a post-partum oestrus showed the changes significantly earlier than those in the control group (Fig. 1A, B). The pups of mothers that had been mildly food-restricted after birth showed the changes significantly later than those in the control group. In brief, the pups of the pregnant mothers weaned first, the control pups next and those of food-restricted mothers weaned last. Differences in the timing of weaning between the three groups occurred in the absence of differences in pup body weight at the time of weaning. Within each experimental group, on the day in which sucrase expression showed the first detectable increase, sucrase activity was strongly predicted by the weight of the pups shortly after birth (Fig. 3). Pregnant mothers put on weight rapidly before implantation and their pups prepared for early weaning even though they did not differ in body weight from control pups (Fig. 4A, B). Food-restricted mothers were significantly lighter than control mothers and, with lighter pups before weaning started, settled for a longer period of suckling.     

Influence of maternal food availability on offspring dispersal

Prenatal effects caused by the maternal environment during gestation are known to contribute to the phenotype of the offspring. Whether they have some adaptive value is currently under debate. We experimentally tested the existence of such a maternal effect (food availability during gestation) on dispersal of offspring in the common lizard (Lacerta vivipara). Pregnant females were captured and kept in the laboratory until parturition. During this period, females were offered two rates of food delivery. After parturition, we released mothers and offspring at the mother's capture point. Dispersal of young was significantly affected by the mother's nutrition. To our knowledge, this is the first evidence of a prenatal effect on dispersal. Offspring of well fed mothers dispersed at a higher rate than those of less well fed mothers. As current hypotheses clearly predict the opposite result, our evidence calls for their reassessment. Dispersers are not always the least fit individuals or those coming from the poorest environments.     

A field test of the effects of familiarity and relatedness on social associations and reproduction in prairie voles

Inbreeding depression is a well-documented phenomenon. In animals, one means of avoiding the costs of inbreeding is through the recognition and avoidance of kin as mates. Prairie voles (Microtus ochrogaster) are short-lived, socially monogamous rodents that demonstrate inbreeding depression in the laboratory. Field data indicate that pair formation in nature is opportunistic but pairing among close relatives seems uncommon. We examined the role of relatedness and familiarity on prairie vole social associations and reproduction by placing adult voles into 0.1-ha enclosures with familiar siblings, unfamiliar siblings, and unrelated, unfamiliar conspecifics. Live-trapping data indicated that indices of social pair bonding were random with respect to relatedness and familiarity. Among females whose litters were sired by a single male, litters were significantly more likely to be sired by unfamiliar than familiar males, but the number of litters sired by males that were unrelated to their partner was not different from the number of litters sired by males that were related to their partner. Additionally, females that produced offspring with familiar siblings were significantly more likely to have litters with multiple paternity than females not producing offspring with familiar siblings. However, multiple paternity was not influenced by relatedness of sires. Finally, older individuals were more likely to produce offspring with each other than with younger individuals. Our findings suggest that prior association is a more important mechanism of inbreeding avoidance than phenotype matching for prairie voles mating under ecologically relevant conditions.     

Sex ratio shifts within litters of meadow voles (Microtus pennsylvanicus)

Summary Changes in the sex ratio of juvenile recruits into a population of meadow voles (Microtus pennsylvanicus) were correlated with shifts in the weight and mortality of pups within the population. The biased recruitment of female juveniles in the spring was reflected in differential allocation of energy within the litters, as measured by female pups being heavier than male pups (n=245). In the fall, the shift in recruitment to male juveniles was reflected within litters by male pups being heavier than female pups (n=139). Nestling mortality showed a similar gender bias. Skewed sex ratios were most evident within the litters of larger mothers, indicating the gender bias was not trigered by energy limitations. We postulate that gender differences in social spacing and behavior result in spring/fall fluctuations in the reproductive success of offspring, based on their gender.     

Development of food preferences: social learning by Belding's ground squirrels Spermophilus beldingi

Summary The mechanisms by which food selection behavior develops may constrain the evolution of optimal foraging, yet these mechanisms have received relatively little attention in recent optimal foraging studies. We used cafeteria-style feeding trials to examine the role of social learning in the development of food preferences by a generalist mammalian herbivore, Spermophilus beldingi. Naive young spent relatively little time feeding and showed no preferences among five plant species offered in their feeding trials. This random pattern persisted for one set of young during two subsequent trials in the absence of their mother. A second group of young squirrels was tested initially alone, once with their mothers, and then once more alone. These squirrels fed more than those in the control group during their final trials, and showed significant preferences among plant species. These paralleled the preferences of their mothers. These results suggest that social learning may be important in the development of feeding behavior in ground squirrels, and provide a possible mechanism for cultural differences in food preferences among populations.     

The effects of mating on infanticide and pup discrimination in white-footed mice

Summary A laboratory study was conducted with white-footed mice (Peromyscus leucopus) to determine (1) if cohabitation and/or successful mating inhibits infanticide, and if so for how long, and (2) if males and females can discriminate between their own (familiar) and strange (unfamiliar) pups. Infanticidal males and females that were paired for 15 days and did not reproduce were not inhibited from killing pups, whereas infanticidal males and females that were paired until they reproduced were inhibited from committing infanticide at 4 days postpartum. Neither males nor females discriminated between familiar and unfamiliar pups with regard to engaging in infanticide. Approximately 50% of wild-caught males and females killed pups in the laboratory. Infanticidal pairs bred significantly sooner than did noninfanticidal pairs. The results are consistent with the promiscuous nature of P. leucopus males and territoriality of P. leucopus females. Offprint requests to: Donna M. Cicirello, Kellogg Biological Station, 3700 E. Gull Lake Drive, Hickory Corners, MI 49060, USA     

Variation in offspring sex ratio among individual Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>) females of different quality

The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Hunger and food allocation among nestlings of facultatively siblicidal ospreys

Summary Previous studies of food allocation among nestlings of siblicidal birds have focussed on the proximate link between food and aggression. However, food sharing among sibs (and brood reduction) need not involve aggression. Here I examine the role of hunger (defined operationally in terms of the amount of food eaten recently) within the broader framework of passive and aggressive food-sharing among nestlings of facultatively siblicidal ospreys (Pandion haliaetus). Feeding among brood members was hierarchical; senior, dominant sibs ate more when hungry, leaving a smaller residual share of food for junior sibs. Senior sibs did not become more generous at large meals (i.e., the prospect of a large meal did not quell the selfish tendencies of senior sibs). That individuals ate more when hungry indicates a proximate link between food and the allocation of resources among siblings. Overall, aggression was infrequent and seemed to be used when junior sibs contested food allocation at meals. Aggression was diminished and food allocation was skewed toward the junior sib in broods with artificially exaggerated hatching intervals, suggesting that senior sibs were more generous when their dominant status was not threatened.Offprint requests to the present address     

Inbreeding-based bias in parental responsiveness to litters of oldfield mice

This study investigated variation in parental behavior in oldfield mice (Peromyscus polionotus). Specifically, I examined the possibility that parental behavior and probability of litter loss may differ depending on whether parents are related to one another and, therefore, whether offspring are inbred. When parents are related, they share more genes with their offspring and so may be predicted to invest more in inbred offspring if these offspring do not inherently have a greater risk of juvenile mortality. Survival of inbred pups did not differ from survival of outbred pups, and females tended to exhibit a preference, in the form of enhanced parental care, for inbred litters. Males did not display any consistent preferences. Inbred litters were left unattended more often during the immediate post-partum period than were outbred litters, but this inconsistent finding appeared to have a smaller effect than the overall improved maternal care provided to inbred litters. Females thus appeared to modulate their behavior to a greater degree than did males depending on characteristics of the litter. Patterns of litter loss indicated that complete death of litters was independent of litter inbreeding, whereas loss of selected pups in a litter occurred significantly more often when litters were inbred. Complete and partial loss of litters may be functionally different behaviors that are triggered by different cues. Received: 20 September 1996 / Accepted after revision: 28 April 1997     

Food access, brood size and filial cannibalism in the fantail darter, Etheostoma flabellare

We compared the occurrence of filial cannibalism in fed and starved male fantail darters (Etheostoma flabellare). All males in the experiment consumed eggs, and 56% ate all of their eggs. A male's initial body condition did not explain the number of eggs that he ate. Neither did non-fed males eat more eggs than fed males. Fed males were able to maintain better body condition during the experiment, but the change in body condition also depended on the number of eggs eaten. Thus, males who ate more eggs were able to maintain better body condition.The most important determinant of whether or not a male ate all of his eggs was his initial egg number. Males with small egg masses ate all of their eggs whereas males with large egg masses were only partial cannibals. There was, however, no difference in the total number of eggs eaten by total and partial cannibals. We conclude that eggs are only partially eaten for energetic reasons. We also suggest that small egg masses are completely consumed because the costs of caring for a small egg mass may exceed the expected reproductive benefits of a small egg mass. Received: 26 January 1996 / Accepted after revision: 2 November 1996     

Differential effects of offspring condition-dependent signals on maternal care regulation in the European earwig

Parent–offspring conflict theory predicts the evolution of offspring solicitation signals that can influence the amount and/or the duration of parental investment. Short-term effects of offspring solicitation signals on parental food provisioning have been widely demonstrated, but persistent effects of offspring signals on the maintenance of parental care have been rarely studied. Also, the relation between the amount of care provided to the brood and how it is distributed among individual offspring within a brood is not well enough understood. Here, we investigated in the European earwig (Forficula auricularia) the effects of offspring condition-dependent chemical signals on the maintenance of maternal care among broods and the distribution of maternal food within broods. Mothers were isolated from their brood for 3 days and continuously exposed to chemical signals extracted from broods of experimentally manipulated nutritional state. After re-introducing mothers to their brood, a range of maternal behaviours were quantified. We found that earwig mothers groomed their offspring significantly more after exposure to chemical extract from high-food brood in comparison with mothers exposed to extract from low-food brood, which in turn displayed significantly more aggressive behaviour. Furthermore, we manipulated offspring individual nutritional condition within the brood to evaluate the effect of offspring state on the within-brood food distribution. Within broods, poorly fed individuals received significantly more food than well-fed individuals, probably due to scramble competition. These results show that earwig nymphs express multi-component condition-dependent signals and behaviours differentially affecting maternal care provisioned to the brood and the distribution of care within broods.     

Offspring sex ratio in relation to female size in southern elephant seals,Mirounga leonina

Southern elephant seals Mirounga leonina display extreme sexual dimorphism. In addition females show great variation in size and stored resources at parturition. Therefore they present an excellent opportunity for examination of responses of sex ratio to resource availability. We studied the relationships between the size of southern elephant seal females at parturition and the size and sex of their pups at South Georgia over four breeding seasons. We found a large individual variation in maternal post-partum mass (range 296–977 kg, n=151). Larger mothers gave birth to larger pups, irrespective of the sex of their pup. Male pups were on average 14% larger than females at birth and consequently more costly to bring to parturition. Our results suggest that female southern elephant seals must weigh more than 300 kg if they are to breed at all, and more than 380 kg if they are to give birth to a male pup. Above this threshold the proportion of males among offspring rapidly increases with maternal mass, and stabilizes at a level not significantly different from parity. These results show that smaller females of southern elephant seals vary offspring sex ratio in a way that is consistent with theories on adaptive offspring sex ratio. A smaller mother with a male foetus may benefit from terminating her pregnancy and allocating the resources she saves to her own growth. She could then give birth to and raise a larger pup in the subsequent season.     

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.     

Mixed sex allocation strategies in a polytocous mammal,the house mouse (<Emphasis Type="Italic">Mus musculus</Emphasis>)

The issue of adaptive adjustment of offspring sex ratio (proportion of male births) in polytocous mammals, producing several offspring per litter, is controversial because females of these species can maximize their fitness mainly by adjusting offspring number. To address this issue, we examined the effect of maternal condition at mating, experimentally decreased by pre-mating food restriction, on the sex ratio variation in 137 female mice. We tested two basic sex allocation hypotheses plausible for polytocous mammals: (1) the Myers hypothesis, predicting that cheaper sex should be favored in poor environmental conditions to maximize offspring number; and (2) the Williams hypothesis, predicting maximum fitness returns by adjusting size- and sex-specific composition of the litter according to the maternal condition. The food-restricted mothers produced larger litters with a higher proportion of cheaper daughters than the control mothers. By contrast, the control mothers optimized size and sex composition of the litter according to their weight at mating. In addition, the offspring of the food-restricted mothers suffered less from pre-weaning mortality than those of the control mothers. Therefore, when comparing the groups, the Myers hypothesis had a general significance while the Williams hypothesis was plausible only for the control mothers. Furthermore, some of the food-restricted mothers partly coped with the pre-mating food restriction and increased the proportion of sons in the litter with the increasing maternal weight loss (during the period of food restriction). The sex ratio variation was thus a result of three sex allocation strategies depending on the maternal condition at mating.