Maternal allocation in eggs when counting on helpers in a cooperatively breeding bird

For cooperatively breeding birds, it has been proposed that breeders should reduce their investment in eggs when they count on helpers, because this can be compensated for by helpers provisioning of nestlings. Data from some species have supported this prediction, but this is not the case in others. It has also been proposed that mothers should not reduce but rather increase investment if the presence of helpers enhances the reproductive value of offspring, a pattern that might also influence egg production as long as helpers are predictable for laying females. Here, we studied maternal expenditure in eggs and clutches in the Iberian magpie, to see whether mothers reduce their expenditure at the egg stage in the presence of helpers. Our results show that investment in clutches varied depending on the year, date in the season and age of the mother, but there were no reductions in maternal expenditure per individual egg when they counted on helpers. On the contrary, a pattern emerged in the opposite direction of more investment in eggs associated with the future presence of helpers at the nestling stage. Our data suggest that the predictability of helpers, along with the type of benefits accrued from the contribution of helpers, may be crucial to understanding the reaction of mothers at egg production.     

Egg investment in response to helper presence in cooperatively breeding Tibetan ground tits

Life‐history theory predicts a trade‐off between current and future reproduction to maximize lifetime fitness. In cooperatively breeding species, where offspring care is shared between breeders and helpers, helper presence may influence the female breeders’ egg investment, and consequently, survival and future reproductive success. For example, female breeders may reduce egg investment in response to helper presence if this reduction is compensated by helpers during provisioning. Alternatively, female breeders may increase egg investment in response to helper presence if helpers allow the breeders to raise more or higher quality offspring successfully. In the facultatively cooperative‐breeding Tibetan ground tit Pseudopodoces humilis, previous studies found that helpers improve total nestling provisioning rates and fledgling recruitment, but have no apparent effects on the number and body mass of fledglings produced, while breeders with helpers show reduced provisioning rates and higher survival. Here, we investigated whether some of these effects may be explained by female breeders reducing their investment in eggs in response to helper presence. In addition, we investigated whether egg investment is associated with the female breeder's future fitness. Our results showed that helper presence had no effect on the female breeders’ egg investment, and that egg investment was not associated with breeder survival and reproductive success. Our findings suggest that the responses of breeders to helping should be investigated throughout the breeding cycle, because the conclusions regarding the breeders’ adjustment of reproductive investment in response to being helped may depend on which stage of the breeding cycle is considered.     

Mothers adjust egg size to helper number in a cooperatively breeding cichlid

Mothers should adjust the size of propagules to the selectiveforces to which these offspring will be exposed. Usually, alarger propagule size is favored when young are exposed to highmortality risk or conspecific competition. Here we test 2 predictionson how egg size should vary with these selective agents. Whenoffspring are cared for by parents and/or alloparents, protectionmay reduce the predation risk to young, which may allow mothersto invest less per single offspring. In the cooperatively breedingcichlid Neolamprologus pulcher, brood care helpers protect groupoffspring and reduce the latters' mortality rate. Therefore,females are expected to reduce their investment per egg whenmore helpers are present. In a first experiment, we tested thisprediction by manipulating the helper number. In N. pulcher,helpers compete for dispersal opportunities with similar-sizedindividuals of neighboring groups. If the expected future competitionpressure on young is high, females should increase their investmentper offspring to give them a head start. In a second experiment,we tested whether females produce larger eggs when perceivedneighbor density is high. Females indeed reduced egg size withincreasing helper number. However, we did not detect an effectof local density on egg size, although females took longer toproduce the next clutch when local density was high. We arguethat females can use the energy saved by adjusting egg sizeto reduced predation risk to enhance future reproductive output.Adaptive adjustment of offspring size to helper number may bean important, as yet unrecognized, strategy of cooperative breeders.     

Effects of maternal stress on egg characteristics in a cooperatively breeding fish

Elevated stress experienced by a mother can compromise both her own reproductive success and that of her offspring. In this study, we investigated whether chronically stressed mothers experienced such effects in cooperatively breeding species, in which helpers at the nest potentially compound the negative effects of maternal stress. Using Neolamprologus pulcher, a group-living cichlid fish from Lake Tanganyika, we observed the effects of experimentally increased stress on female reproductive success (measured as inter-spawn interval, and number of eggs) as well as egg characteristics including egg size and cortisol concentrations. Stress levels were manipulated by repeated exposure to the acute stresses of chasing and netting. Stressed females had longer inter-spawn intervals and laid fewer, smaller eggs. Although no significant differences in egg cortisol concentrations were detected between control and stressed females, egg cortisol concentration fell between spawns in control but not in stressed fish. No effect of helper number was detected for any parameter examined, except there appeared to be less change in egg cortisol content in groups with helpers present. Our results suggest that stress imposes fitness costs on breeding females, and social regulation of a dominance hierarchy does not appear to exacerbate or alleviate the negative effects of maternal stress.     

Load Lightening in Southern Lapwings: Group‐Living Mothers Lay Smaller Eggs than Pair‐Living Mothers

Females of some cooperative‐breeding species can decrease their egg investment without costs for their offspring because helpers‐at‐the‐nest compensate for this reduction either by feeding more or by better protecting offspring from predation. We used the southern lapwing (Vanellus chilensis) to evaluate the effects of the presence of helpers on maternal investment. Southern lapwings are cooperative (some breeding pairs are aided by helpers), chick development is precocial, thus adults do not feed the chicks, and adults offer protection from predators through mobbing behaviors. We tested whether southern lapwing females reduced their reproductive investment (i.e. load‐lightening [LL] hypothesis) or increased their investment (i.e. differential allocation hypothesis) when breeding in groups when compared with females that bred in pairs. We found that increased group size was associated with lower egg volume. A significant negative association between the combined egg nutritional investment (yolk, protein, and lipid mass) and group size was observed. Chicks that hatched from eggs laid in nests of groups were also smaller than chicks hatched in nests of pairs. However, there was no relationship between the body mass index of chicks, or clutch size and group size, which suggests that such eggs are, simply, proportionally smaller. Our results support the LL hypothesis even in a situation where adults do not feed the chicks, allowing females to reduce investment in eggs without incurring a cost to their offspring.     

The energetics of lactation in cooperatively breeding meerkats Suricata suricatta

Species may become obligate cooperative breeders when parents are unable to raise their offspring unassisted. We measured the daily energy expenditure of mothers, helpers and offspring during peak lactation in cooperatively breeding meerkats Suricata suricatta using the doubly labelled water technique. Lactating mothers expended more energy per day than allo-lactating subordinate females, non-lactating females or suckling offspring. Metabolizable energy intakes of lactating mothers were calculated from isotope-based estimates of offspring milk energy intake, and were not significantly different from the previously suggested maximal limit for mammals. Allo-lactating females were the only category of animals that lost weight during the period of study, probably because they spent more time babysitting than non-lactating females. Daily energy expenditure (DEE) of lactating mothers increased with litter size but decreased with the number of helpers. Calculations show that for every 10 helpers, even in the absence of allo-lactators, mothers are able to reduce their DEE during peak lactation by an amount equivalent to the energy cost of one pup. These results indicate that helpers have beneficial energetic consequences for lactating mothers in an obligate cooperatively breeding mammal.     

Testis size depends on social status and the presence of male helpers in the cooperatively breeding cichlid Julidochromis ornatus

Cooperatively breeding animals, in which helpers may participatein reproduction with dominant breeders, are ideal species forexamining intraspecific variation in testis size because theyoften exhibit both monogamous breeding (low risk of sperm competition)and polyandrous breeding (high risk) within a population. However,little is known about testis investment as a result of spermcompetition in these animals. The substrate-brooding cichlidfish Julidochromis ornatus has a cooperatively breeding system,in which some males mate monogamously and other males reproduceas dominant breeders or helpers within cooperatively breedinggroups, in which male helpers frequently sire young. We examinedthe relationship between testis investment and male social statusin relation to the risk of sperm competition. As predicted fromsperm competition models, in groups with male helpers, boththe male breeders and the male helpers invested more in testesmass, compared to breeding males without male helpers. We alsofound a positive relationship between the testes mass of malebreeders and their male helpers, suggesting that males increasetheir investment in reproductive capability under the risk ofsperm competition. Sperm competition models also predict thatlarger testes are associated with increased siring success.Our paternity analysis supported this prediction; we found apositive relationship between testis investment by male helpersand the number of offspring they sired.     

Breeding success in cooperative meerkats: effects of helper number and maternal state

Studies of cooperatively breeding birds and mammals generallyconcentrate on the effects that helpers have on the number ofreproductive attempts females have per year or on the numberand size of offspring that survive from hatching/weaning toindependence. However, helpers may also influence breeding successbefore hatching or weaning. In the present study, we used anultrasound imager to determine litter sizes close to birth,and multivariate statistics to investigate whether helpers influencefemale fecundity, offspring survival to weaning, and offspringsize at weaning in cooperative meerkats, Suricata suricatta.We found that the number of helpers in a group was correlatedwith the number of litters that females delivered each year,probably because females in large groups gave birth earlierand had shorter interbirth intervals. In addition, althoughpup survival between birth and weaning was primarily influencedby maternal dominance status, helper number may also have asignificant positive effect. By contrast, we found no evidenceto suggest that helpers have a direct effect on either littersizes at birth or pup weights at weaning, which were both significantlyinfluenced by maternal weight at conception. However, becausedifferences in maternal weight were associated with differencesin helper number, helpers have the potential to influence maternalfecundity and offspring size within reproductive attempts indirectly.These results suggest that future studies may need to considerdirect and indirect helper effects on female fecundity and investmentbefore assessing helper effects on reproductive success in societiesof cooperatively breeding vertebrates.     

Maternal investment tactics in superb fairy-wrens

In cooperatively breeding species, parents often use helper contributions to offspring care to cut their own costs of investment (i.e. load-lightening). Understanding the process of load-lightening is essential to understanding both the rules governing parental investment and the adaptive value of helping behaviour, but little experimental work has been conducted. Here we report the results of field experiments to determine maternal provisioning rules in cooperatively breeding superb fairy-wrens (Malurus cyaneus). By manipulating carer: offspring ratios, we demonstrate that helpers allow females to reduce the rate at which they provision their brood. Female reductions, however, were less than that provided by helpers, so that chicks still received food at a faster rate in the presence of helpers. Despite this, chicks fed by parents and helpers were not heavier than those provisioned by parents alone. This is because maternal load-lightening not only occurs during the chick provisioning stage, but also at the egg investment stage. Theoretically, complete load-lightening is predicted when parents value themselves more highly than their offspring. We tested this idea by 'presenting' mothers with a 'choice' between reducing their own levels of care and increasing investment in their offspring. We found that mothers preferred to cut their contributions to brood care, just as predicted. Our experiments help to explain why helper effects on offspring success have been difficult to detect in superb fairy-wrens, and suggest that the accuracy with which theoretical predictions of parental provisioning rules are matched in cooperative birds depends on measuring maternal responses to helper presence at both the egg and chick stages.     

Cooperative Breeding and Group Structure in the Lake Tanganyika Cichlid Neolamprologus savoryi

As yet, cooperative breeding has been described only for some fish species. However, evidence is accumulating that it is widespread among Lake Tanganyika cichlids. We studied the cooperative breeding system of the substrate breeding cichlid Neolamprologus savoryi. Breeding groups typically consisted of a large breeding male with one to four breeding females and three to 33 helpers (mean group size: 14.3 members). Group size was significantly related to breeding male and female body sizes, and larger males had more breeding females and larger sized male helpers. The size of the largest female in the group was positively related to the number and sizes of secondary breeding females and female helpers. In case of multiple breeding females, these females usually divided the group's territory into sub‐territories, each with its own helpers (subgroups). Interspersed between groups, independent fish were detected defending an individual shelter (4.4% of all fish). In 9% of the groups no breeding female was present. All group members participated in territory defence and maintenance, and showed submissive behaviours to larger group members. As expected, the level of between‐subgroup conflicts was high compared with the level of within‐subgroup conflicts. We compare these results with data available from other cooperatively breeding fishes.     

Maternal investment during pregnancy in wild meerkats

Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success.     

First field evidence for alloparental egg care in cooperatively breeding fish

Helping behaviour in cooperative breeders has been intensively studied in many animal taxa, including arthropods, birds and mammals. In these highly social systems, helpers typically engage in brood care and the protection of dependent young. Such helping systems also exist in cooperatively breeding cichlid species of Lake Tanganyika. However, breeding in these species happens in clefts, narrow holes or shelters underneath stones. Therefore, direct brood care by breeders and helpers has thus far only been observed under artificial laboratory conditions. Under natural conditions, brood care behaviour has been estimated indirectly by determining the time spent in the breeding chamber, or by the number of visits to the breeding chamber. The reliability of such substitutes needs to be validated, for instance, by demonstrating alloparental egg care of helpers through direct observations in nature. Here, we describe direct egg care by a male helper of the cooperatively breeding cichlid Neolamprologus savoryi in the field. The helper inspected and cleaned the eggs and defended them against predators. By reconstructing the genetic relatedness using microsatellite markers, we show that the helper was the son of the breeding male, but unrelated to the breeding female. The genetic mother of the helper was defending a different territory next to the one where the helper showed alloparental egg care. This indicates that the helper had dispersed inside the male territory to assist another female to care for his half‐siblings. These results demonstrate alloparental egg care without reproductive share in a fish species under natural conditions, underlining that helping behaviour in cooperatively breeding fish has a strong non‐self‐serving component.     

Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter

I studied the contributions of individuals to incubation and nestling feeding in a population of cooperatively breeding laughing kookaburras, Dacelo novaeguineae. In most cooperatively breeding birds where nest success is limited by nestling starvation, related helpers increase the overall level of provisioning to the nest, thus boosting the production of nondescendent kin. However, although partial brood loss is the largest cause of lost productivity in kookaburra nests, additional helpers failed to increase overall provisioning. Instead, all group members, but especially helpers, reduced their feeding contributions as group size increased. Breeders and helpers reduced the size of prey delivered, and helpers also reduced the number of feeding visits. An important benefit of helping in kookaburras may be to allow all group members to reduce their effort. Within groups, contributions to care depended on status, sex, group size and the brood size. Breeding males delivered the most food. Breeding females provisioned less than their partner, but their effort was comparable to that of male helpers. Female helpers contributed the least food. Incubation effort followed similar patterns. The relatedness of helpers to the brood had no impact on their provisioning. Across all group sizes, helpers generally brought larger items to the nest than breeders. Copyright 2000 The Association for the Study of Animal Behaviour.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.     

Sex-biased preferential care in the cooperatively breeding Arabian babbler

In many social birds there are sex differences in dispersal patterns, with males commonly remaining in their natal group whereas females typically disperse at adolescence. Group members may therefore increase their fitness by preferentially caring for offspring of a particular sex according to social circumstances. Although previous studies have focussed on intragroup social factors that may affect preferential care, we propose that the relative size of neighbouring groups is of primary importance. Here we show that in the cooperatively breeding Arabian babbler (Turdoides squamiceps), parents preferentially feed male offspring when relative group size is small, and female offspring when group size is large. Unlike parents, helpers consistently favour young of the opposite sex to themselves, suggesting the risk of competition with members of the same sex for future breeding opportunities may override other considerations. These results emphasize the complexity of investment strategies in relation to social circumstances and the variable benefits of raising males vs. females in a species with sex-biased philopatry.     

Group Structure,Nest Size and Reproductive Success in the Cooperatively Breeding Cichlid Julidochromis ornatus: A Correlation Study

The effect of group size on reproductive success has long been studied in cooperatively breeding species, as it might provide an adaptive explanation for group‐living in social species. Numerous studies have shown positive effects of subordinates on reproductive success (‘helper effect’), but these studies have also revealed the importance of controlling statistically, or experimentally, for the effect of other factors that might affect reproductive success. Here, we first examine the relationships between group size, body size of group members and nest size in the cooperatively breeding cichlid Julidochromis ornatus, in which unrelated helpers frequently participate in reproduction and their breeding nests inside rock crevices may be crucial for reproduction and survival of all group members. Then, we subsequently investigate the relationship between group size and reproductive success, while controlling for these factors. The results showed that group size was significantly related to body size of group members rather than nest size; and larger breeders had larger helpers. It was found that group size significantly increased group reproductive output. More importantly, reproductive success of male breeders did not depend on the presence of mature helpers, whereas female reproductive success increased when two males assisted her and tended to decrease when two females bred cooperatively. We conclude that breeding groups of J. ornatus have size hierarchical societies that relate to group size, and group composition of genetically unrelated and co‐breeding members affects their reproductive success.     

Strategic female reproductive investment in response to male attractiveness in birds

Life-history theory predicts that individuals should adjust their reproductive effort according to the expected fitness returns on investment. Because sexually selected male traits should provide honest information about male genetic or phenotypic quality, females may invest more when paired with attractive males. However, there is substantial disagreement in the literature whether such differential allocation is a general pattern. Using a comparative meta-regression approach, we show that female birds generally invest more into reproduction when paired with attractive males, both in terms of egg size and number as well as food provisioning. However, whereas females of species with bi-parental care tend to primarily increase the number of eggs when paired with attractive males, females of species with female-only care produce larger, but not more, eggs. These patterns may reflect adaptive differences in female allocation strategies arising from variation in the signal content of sexually selected male traits between systems of parental care. In contrast to reproductive effort, female allocation of immune-stimulants, anti-oxidants and androgens to the egg yolk was not consistently increased when mated to attractive males, which probably reflects the context-dependent costs and benefits of those yolk compounds to females and offspring.     

Complex sex allocation in the laughing kookaburra

In groups of the cooperatively breeding laughing kookaburra(Dacelo novaeguineae), offspring sex varied with the type ofsocial group and with hatch rank. Groups with female helpers,especially if all helpers were female, had male-biased clutchand fledging sex ratios. Groups without female helpers (unassistedpairs or male-only helpers) had female-biased clutch and fledgingsex ratios. Breeding females responded facultatively to increasesin the number of female helpers in their group by producingmore male eggs. These biases may occur if breeding femalestry to limit the number of daughters recruited into their groupbecause unlike male helpers, female helpers depress the breedingsuccess of their parents. Across all nests, two-thirds of first-hatchedyoung were male, two-thirds of second-hatched young were female, and the sex ratio of third-hatched young was even. Hatch ranksex ratios also varied dramatically between different typesof social groups, from 16.7% for second-hatched nestlings ofunassisted pairs to 100% for first-hatched nestlings of groupswith only female helpers. A corollary of the relationship betweenhatch rank and sex was that hatching sex sequences were distributed nonrandomly: all groups avoided hatching a daughter first followedby a son (FM). Sibling competition is aggressive and sometimesfatal. Since females grow to be 15% larger than males the hatchingsequence of sexes could affect nestling growth and mortality.However, an exhaustive analysis found little evidence thatgrowth or survival of males was compromised if hatched aftera sister. The small number of FM sequences may only have occurredin nests that were able to ameliorate any negative consequences.Alternatively, when clutch size is small and fledging successunpredictable because of brood reduction, the preferred broodsex ratio may be contingent on the number of fledged young,making it advantageous to order the sexes in the brood.     

Relationships between oviposition date, hatch date, and offspring size in the grasshopper Chorthippus brunneus

Abstract 1. The grasshopper Chorthippus brunneus has been shown to increase egg size with maternal age under constant laboratory conditions, such that late-laid eggs are larger than early laid eggs. In this study, an increase in the size of eggs (and hatchlings from those eggs) was recorded with date of oviposition in a field cage population. This suggests that the relationship between maternal age and egg size, observed previously in the laboratory, also occurs in the field. There was, however, some evidence that the behaviour of the maternal females in field cages was modified by the onset of autumnal weather at the end of the breeding season. Only a small number of eggs was laid in the last 3 weeks of the summer but these yielded relatively small hatchlings.
2. The date on which eggs were laid was correlated positively with their date of hatch in the following year. A consequence of this relationship, and that between oviposition date and egg size, was that size at hatch increased with date of hatch through most of the spring but then declined as the last few eggs hatched. Temporal variation in size at hatch parallelled temporal variation in the maternal females' investment in egg size in the previous year.
3. An undisturbed field population was monitored to assess whether the temporal variation in size at hatch resulted in size variation at eclosion in subsequent developmental stages. There were negative correlations between size at eclosion and date of eclosion at the third and fourth instars, suggesting that despite their smaller size at hatch, early hatchers experienced more favourable conditions for juvenile growth than late hatchers. The larger size at hatch of late hatchers may enhance their survival and compensate (albeit incompletely) for their reduced opportunity for growth. Female reproductive behaviour may represent an adaptive response to a predictable seasonal decline in offspring fitness at hatch.     

Sex-related effects of maternal egg investment on offspring in relation to carotenoid availability in the great tit

1. Maternal carotenoids in the egg yolk have been hypothesized to promote maturation of the immune system and protect against free radical damages. Depending on availability, mothers may thus influence offspring quality by depositing variable amounts of carotenoids into the eggs. Sex allocation theory predicts that in good quality environments, females should invest into offspring of the sex that will provide larger fitness return, generally males. 2. In a field experiment we tested whether female great tits bias their investment towards males when carotenoid availability is increased, and whether male offspring of carotenoid-supplemented mothers show higher body condition. We partially cross-fostered hatchlings to disentangle maternal effects from post-hatching effects, and manipulated hen flea Ceratophyllus gallinae infestation to investigate the relationship between carotenoid availability and resistance to ectoparasites. 3. As predicted, we found that carotenoid-supplemented mothers produced males that were heavier than their sisters at hatching, while the reverse was true for control mothers. This suggests that carotenoid availability during egg production affects male and female hatchlings differentially, possibly via a differential allocation to male and female eggs. 4. A main effect of maternal supplementation became visible 14 days after hatching when nestlings hatched from eggs laid by carotenoid-supplemented mothers had gained significantly more mass than control nestlings. Independently of the carotenoid treatment, fleas impaired mass gain of nestlings during the first 9 days in large broods only and reduced tarsus length of male nestlings at an age of 14 days, suggesting a cost to mount a defence against parasites. 5. Overall, our results suggest that pre-laying availability of carotenoids affects nestling condition in a sex-specific way with potentially longer-lasting effects on offspring fitness.