Insights into the costs of complex maternal care behavior in the burrower bug (Sehirus cinctus)

The evolution of life history characters, including parental care behaviors, depends on costs and benefits. When offspring can influence parental behaviors, parent-offspring conflict over parental care can occur, but only if these parental behaviors are costly. Mother burrower bugs (Sehirus cinctus) exhibit extended and complex care of offspring. Mothers guard eggs until hatching and then attend and provision offspring for approximately 2 weeks after hatching. Using four experimental treatments, we attempted to identify the costs associated with specific components of these behaviors. Under laboratory conditions, egg guarding increases inter-clutch interval, but provisioning does not appear to be very costly. We discuss additional ecological factors that may be important in mediating provisioning costs under natural conditions. Through analysis of individual maternal performance, we find no evidence for trade-offs between successive clutches. These data suggest that variation in overall condition may obscure variation in allocation strategies.Communicated by F. Trillmich     

Embryonic and parental preferences for incubation temperature in herring gulls: implications for parent-offspring conflict

According to Trivers (1974), parent-offspring (P-O) conflict arises because offspring are selected to solicit more care than parents are selected to provide. However, should benefits fail to increase with increasing care, the offspring optimum can be reduced to the point where predicted P-O conflict vanishes. We examined offspring demand and parental care in such a benefit-limited system in herring gulls (Larus argentatus). In this species, parents typically neglect their lasthatched (C-) egg during the final hours of hatching (pipped-egg stage), allowing mean temperature to drop by about 4°C, to near 33°C. Other studies indicate that no increased offspring benefit arises from increasing pipped egg incubation temperature above that level, but embryo damage occurs if temperature drops lower. In such a system, P-O conflict over preferred incubation temperature is predicted to be minimal or absent. We assessed phenotypic manifestations of conflict by determining incubation temperature preferences of parent and offspring independently. Temperature provided solely by parental initiative was 33.9°C (artificial eggs, corrected for embryonic heat production). Preferred incubation temperature of pipped embryos was measured by exposing them to moderate chilling (20°C) punctuated by 4-min periods of rewarming when they called. Temperature of vocally thermoregulating embryos stabilized around a mean of 32.9–33.4°C, about 0.5–1.0°C below parental preference. Acting independently, parents and embryos each maintained egg temperature at or near minimum developmentally safe levels. Results provided no evidence for phenotypic conflict, as predicted by a benefit-limited version of Trivers' P-O conflict model. Benefit limitation may also be relevant to P-O conflict in other contexts such as feeding of newly-hatched young.     

Genetic relationship between offspring and guardian adults of a rhacophorid frog and its care effort in response to paternal share

The rhacophorid frog, Kurixalus eiffingeri, is one of only a few frog species that exhibits polyandry and paternal care of eggs. Previous studies predicted that multiple paternity within an egg clutch could influence the degree of paternal care and reproductive strategies. We used microsatellite DNA markers to assess the prevalence of multiple paternity within egg clutches and the relationship between male paternal care and the percent of male’s genetic contribution to the clutch, i.e., paternal share. We conducted field observations of paternal care and collected tissues from both male frogs and tadpoles for parentage analyses. Our results showed that at least five out of 31 egg clutches had multiple paternity. Attending males were always the genetic fathers of some, if not all of the eggs in the clutch they guarded. All egg clutches except one were attended by one male frog but the attending male did not necessarily sire the majority of offspring. Multiple paternity in all cases consisted of two fathers and one mother and most likely resulted from synchronous polyandry. Paternal care effort correlated significantly with the male’s genetic contribution to the clutch, suggesting that male frogs adjust the effort expended in care in response to paternal share. In addition, our results suggest that externally fertilizing species with parental care and multiple paternity may develop novel reproductive and behavioral strategies to safeguard their parental investment and overcome sperm competition.     

Effects of experience and avpr1a microsatellite length on parental care in male prairie voles (Microtus ochrogaster)

Pair-bonded males often make substantial contributions to the care of their offspring. Male parental behavior may be affected by a range of factors, including previous experience (parental or alloparental), genetic influences, and contributions by the female partner. Previous studies have shown that a microsatellite polymorphism in the regulatory region of the avpr1a gene influences aspects of paternal behavior in male prairie voles (Microtus ochrogaster). Specifically, males with longer avpr1a microsatellites groomed offspring more than did males with shorter avpr1a microsatellites. Previous experience with alloparental care also appears to influence subsequent paternal care in prairie voles. We investigated the influence of avpr1a microsatellite length and previous parental experience on paternal behavior in prairie voles two generations from the field and specially bred to exaggerate differences in avpr1a microsatellite length. We found that avpr1a microsatellite length alone did not affect any of the paternal behaviors that we measured. In contrast, males differed in parental behavior between first and second litters. Regardless of avpr1a microsatellite length, males licked/groomed the second litter less, and retrieved pups more quickly during the second compared to the first litter. Our results show that previous paternal experience may play a more important role than the length of the microsatellite in the regulatory region of the avpr1a gene in influencing paternal care.     

Testosterone treatment suppresses paternal care in superb fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship

Courtship displays and paternal care in male birds are generally thought to be mutually exclusive, because testosterone, necessary for stimulation of sexual behaviours, suppresses paternal behaviours. Superb fairy-wrens, Malurus cyaneus, are unusual in that males concurrently engage in courtship and paternal care. Fairy-wrens live in stable socially monogamous pairs with 0-4 subordinate male helpers. Both helper and dominant males provide care whenever it is required but continue courtship throughout the period of care as most fertilisations are extra-group and females are multi-brooded. To examine the role of testosterone in this trade-off, we compared testosterone levels in males of different social status, while they had dependent nestlings, and determined the effect of testosterone treatment on provisioning rates of pairs. Testosterone levels were lower in subordinate helpers, although these do not provide more paternal care than dominant males. Conversely, testosterone levels were similar in dominant males with or without helpers, although as the number of helpers increases males invest substantially less in nestling care and more in extra-group courtship. Although testosterone levels are high, irrespective of paternal duties, experimental testosterone treatment of males resulted in a large (65%) reduction in nestling feeding rates. Surprisingly, there was no indication that females compensated for this reduction in provisioning, suggesting that females might assume a constant male contribution to offspring care. We conclude that during nestling provisioning, male fairy-wrens maintain testosterone at an individual level that does not interfere with parental duties, while allowing high investment in extra-group courtship.     

The presence of eggs in the nest and female choice in common freshwater gobies (Rhinogobius brunneus)

In many species of fishes with paternal care, females prefer to spawn with males who are already guarding eggs. We studied the effect of egg presence on female mate choice in common freshwater gobies, Rhinogobius brunneus sp. OR. In our tests, females did not prefer males with eggs, suggesting egg presence per se may not act as a cue to attract females. We also examined the effects of brood size on paternal care and offspring survival to look for possible benefits females could obtain when choosing males with eggs. Both fanning by egg-guarding males and egg survival increased with brood size. The presence of neighboring males did have a significantly negative effect on males' parental activity, which subsequently results in a lower level of egg survival than in solitary egg-guarding males. This result provides a partial explanation for the result of eggs not attracting females to mate.     

Nest-maintenance effort and health status in chinstrap penguins, Pygoscelis antarctica: the functional significance of stone-provisioning behaviour

Stone provisioning is a nest-maintenance activity accomplished by pygoscelid penguins after reliefs during the incubation/brooding period. The functional significance of this behaviour has been mainly explained as a parental strategy preventing nest flooding under detrimental weather conditions. In addition, and in the light of recent studies, this behaviour could also fit into the sexual selection process. In this study, we tested the first idea, that is, whether stone provisioning is a nest-maintenance behaviour to increase egg/nestling survival by lowering the risk of nest flooding, and can thus be considered a form of parental care. Additionally, we investigated if the effort invested by parents in nest maintenance is constrained by physiologically limiting resources. The effort of stone collection and the perceived risk of nest flooding were experimentally manipulated during the incubation and early brooding phases in a chinstrap penguin, Pygoscelis antarctica, colony. Three groups of nests were established. After weighing, control nests were left unmanipulated. In a second group of nests (reduced group), only one-half of the initial weight of stones was returned to the nests. In a third group of nests (snow-added group), we both reduced nest weight by a half and added snow outside the nest bowl over 6 consecutive days. Ten days after manipulation, the difference in nest weight between initial and final conditions was significantly related to treatment: penguins increased stone provisioning in the reduced group (44% of half-reduced nests), but drastically more in the reduced and snow-added group (123% of half-reduced nests), while the weight of control nests was unchanged compared to premanipulation conditions. The intensity of stone provisioning was affected by nest date, peaking about hatching time and shortly after, and declining with advancing chick age. These results suggest that stone provisioning is a mechanism that has evolved to prevent egg or chick mortality by nest flooding. The haematocrit, but not leukocyte numbers as expressed by the buffy coat layer, varied with the experimental conditions. Penguins investing more time in nest maintenance had a lower haematocrit, suggesting a physiological trade-off probably mediated by competition between the time devoted to nest maintenance versus foraging activities. The amount of stones collected and the haematocrit were positively related to the number of neighbour nests, so those individuals surrounded by more nests seemed to obtain benefits in the availability of nest material and energy savings. This study indicates that stone-provisioning behaviour is a nest-maintenance activity evolved to improve thermal nest characteristics potentially increasing offspring survival, and competing in time and energy with other reproductive activities. Stone provisioning in penguins should therefore be regarded as a form of parental care and an important part of individual reproductive effort in species breeding in harsh environments. Furthermore, nest size and nest-maintenance effort should be considered reproductive traits indicative of parental quality and thus could also be involved in the post-mating sexual selection process.     

Rising costs of care make spiny chromis discerning parents

When the costs of parental care do not scale with the number of offspring being cared for, inclusion of non-descendant young into broods can be advantageous, leading to systems of alloparental care. However, if the cost of care scales with the number of offspring, selection may act against misdirected parental care. The spiny chromis, Acanthochromis polyacanthus, is a marine fish with extended biparental care, and broods that increase in size over the care period strongly suggest that alloparental care occurs in this species. However, A. polyacanthus parents directly provision their offspring by producing ectodermal mucus for their fry to feed on. The costs of such provisioning may scale with brood size, potentially increasing the costs of parental care. Using wild A. polyacanthus pairs, we tested whether foreign offspring are accepted into established broods, and measured how brood defence effort and mucal feeding scale with brood size. We found that A. polyacanthus discriminate between their own and foreign young, vigorously expelling experimentally introduced foreign offspring. Although defensive effort did not scale with brood size, mucal feeding was strongly dependent on brood size, and this increasing cost of care likely acts as the primary selective force on parental discrimination and rejection of foreign fry in A. polyacanthus.     

Relationship between body size, provisioning rate, longevity and reproductive success in females of the solitary bee Osmia cornuta

Body size has often been related to reproductive success in bees and wasps. The objective of this 3-year study was to analyze the relationship between nesting female body size, provisioning rate and longevity and their effect on several traits related to parental investment and reproductive success in the solitary bee Osmia cornuta. Body size was not correlated to longevity, and it was only correlated to provisioning rate in the third year (with poor weather conditions during nesting). Variation in fecundity, offspring size and offspring mortality was not well explained by nesting female body size in any of the 3 years. However, in the third year, small females biased their investment toward males, the sex requiring smaller pollen–nectar provisions. Large females were more successful usurpers of other females' nests, but fecundity of usurpers was no higher than fecundity of nonusurpers. Large females were more likely to establish at the release site, probably in relation to size-dependent vigor at emergence. A review of the literature on parental investment in solitary aculeate Hymenoptera showed a stronger relationship between body size and reproductive success in wasps than in bees. In O. cornuta, fecundity was strongly related to longevity and provisioning rate in all 3 years. Offspring size was associated with provisioning rate in 1 year, when females with higher provisioning rates tended to produce larger sons and daughters. Both longevity and provisioning rate appeared to be strongly conditioned by stochastic events.     

Prelaying maternal condition modifies the association between egg mass and T cell-mediated immunity in kestrels

Theoretical models of parental care predict differential allocation in relation to the expected fitness of the offspring. As birds must allocate all the resources required for embryonic development in self-contained packages, maternal egg allocation takes a central role in avian life histories. It is predicted that mothers can influence offspring performance by varying the size or composition of their eggs. In this context, T cell-mediated immune response has been revealed as a valuable tool to evaluate fledgling fitness. However, little is known about its relationships to egg mass. I describe a negative association between egg mass and cellular immune response in Eurasian kestrel nestlings (Falco tinnunculus) throughout 3 years. To explore how environmental conditions could mediate this relationship, I experimentally supplied food to females before egg formation in the third study year. I found that this relationship turned to positive in food-supplied females without any effect on egg size. This result shows that environmental conditions before egg formation mediate the relationship between egg mass and future immune response of the nestlings. I suggest that females may be constrained in improving the future immune response of their offspring due to resource allocation trade-offs determined by their pre-laying condition.     

Paternal expenditure is related to brood sex ratio in polygynous great reed warblers

In many polygynous animals, parents invest more heavily in individual sons than in daughters. However, it is unclear if these differences in investment are a consequence of sex differences in the demand of offspring related to sexual size dimorphism or a consequence of parental manipulation. Here, we report on parental food delivery frequency in relation to brood size and brood sex ratio in a wild population of polygynous great reed warblers Acrocephalus arundinaceus. We used the polymorphic microsatellite loci on the Z chromosome to sex chicks. We found that paternal feeding frequency (times/h per nest) increased not with brood size, but with the proportion of males in the brood, although the demand per nest was more closely related to brood size than to brood sex ratio. Additionally, the increase in rate of paternal feeding frequency in relation to the brood sex ratio was much higher than the increase in rate of nestling food demands. Maternal feeding frequency was independent of both brood size and brood sex ratio. These results strongly suggest that fathers preferentially invest in their sons. We propose that parents can afford sex-biased parental care in animals in which food provisioning is enough for all offspring to survive. Received: 22 January 1996/Accepted after revision: 30 June 1996     

Experimental increase in food supply influences the outcome of within-family conflicts in Tengmalm’s owl

Within a family there are conflicts of interest between parents and offspring, and between male and female parents, over the supply of parental care. The observed pattern of parental care is the outcome of negotiations within the family, and may be influenced by environmental factors such as food abundance. We experimentally increased food supply to ten Tengmalm’s owl (Aegolius funereus) nests from hatching to fledging, mimicking natural cached prey. Ten un-supplemented nests served as controls. Parents and offspring were fitted with radio-tags. Food provisioning by parents was measured both in the (1) mid- and (2) late nestling stage and in the (3) early and (4) late post-fledging stage. In response to food supplementation, both males and females reduced food provisioning, but the effect was more pronounced in females. Females generally contributed much less to food provisioning than males, and food supplementation increased the difference between the sexes. Mass loss during the brooding stage was substantially lower for supplemented than for control females. Food supplementation did not improve offspring survival, and had no effect on body measurements of nestlings. In conclusion, parents of both sexes used the increased food supply to reduce the costs of caring for their current offspring, but females responded more strongly than males.     

On the coadaptation of offspring begging and parental supply—a within-individual approach across life stages

Parental care is often characterized by complex behavioral interactions between offspring soliciting for food and parents providing food. During this interplay both behaviors, offspring begging and parental provisioning, can exert a selective pressure on the expression of the other. It has, therefore, been predicted that traits involved in this interplay may coevolve and ultimately become (genetically) correlated. Such covariation has—at least at the phenotypic level—been found in a number of cross-fostering studies, including evidence from the canary (Serinus canaria), our model species. However, a common challenge for these studies has been to establish a genetic covariation given the difficulty to disentangle the relative contribution of genetic and maternal effects, as the latter may act already before cross-fostering. We addressed this problem by studying within-individual covariation between begging (expressed at the nestling stage) and provisioning (expressed at the adult stage). In addition, we estimated the degree of heritability of these behaviors using parent-offspring regressions, as inheritance forms a prerequisite for any genetic correlation. Both traits showed a low to moderate non-significant heritability, similar to those previously reported in other bird species. However, offspring begging and parental provisioning did not covary at the intra-individual level. Thus, individuals begging intensively as nestlings were not necessarily individuals that provided more food as adults or vice versa. These findings provide important insights for our understanding of coadaptation, suggesting that factors other than genes such as maternal effects may play a role in adjusting offspring begging to the levels of parental provisioning.     

Carer provisioning rules in an obligate cooperative breeder: prey type, size and delivery rate

Providing food to developing offspring is beneficial for offspring but costly for carers. Understanding patterns of provisioning thus yields important insights into how selection shapes (allo-) parental care strategies. Broadly, offspring development will be influenced by three components of provisioning (prey type, size and delivery rate). However, all three variables are rarely considered simultaneously, leading to suggestions that the results of many studies are misleading. Additionally, few studies have examined the provisioning strategies of breeders and non-breeding helpers in obligate cooperative breeders, wherein reproduction without help is typically unsuccessful. We investigated these components of provisioning in obligately cooperative chestnut-crowned babblers (Pomatostomus ruficeps). Prey type was associated with size, and delivery rate was the best predictor of the overall amount of food provided by carers. As broods aged, breeders and helpers similarly modified the relative proportion of different prey provided and increased both prey size and delivery rate. Breeding females contributed less prey than male breeders and adult helpers, and were the only carers to load-lighten by reducing their provisioning rates in the presence of additional carers. While our results suggest that breeders and helpers follow broadly comparable provisioning rules, they are also consistent with the idea that, in obligately cooperative species, breeding females benefit more from conserving resources for future reproduction than do helpers which have a low probability of breeding independently.     

Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations.

When breeding diet is restricted, domesticated zebra finches,Taeniopygia guttata, produce male-biased primary and secondary sex ratios, but unexpectedly produce unbiased ratios when food is unrestricted. We investigated the primary sex ratios (at laying) of wild zebra finches in southeastern Australia in response to food supplementation and environmental factors predicted to enhance female breeding condition and to bias the primary sex ratio towards daughters. Molecular sexing of all nestlings in 54 complete broods where every egg hatched, failed to show any significant biases from random. Time of egg laying (month, season) and environmental conditions (rainfall, temperature) did not significantly predict variation in the primary sex ratio, but time of breeding did affect clutch size. Wild zebra finches at our colony did not bias their sex allocation as there were no differences in the primary sex ratio and no differences in the numbers and mass of sons and daughters at the end of parental care (day 35–40 post-hatch). Biases in primary sex ratio of our wild population are probably weak or non-existent possibly due to the unpredictable environment and/or multiple contrary selective forces acting on sex ratios. We also investigated the effects of photoperiod, biases in the adult sex ratio, and parental attractiveness on primary sex ratios of semi-domesticated, laboratory zebra finches. Molecular sexing of three-day old embryos from complete clutches, failed to reveal significant biases from random. In contrast to previous studies, sex of eggs did not correlate with laying order and egg mass declined with order, rather than increased. Domestication may be responsible for these differences.     

Linking male qualities to multiple display traits: an example in a fish with exclusive male care

Recent theoretical models predict that the relative allocation to advertisement and parental care depends on whether paternal care is necessary for offspring survival: In species with exclusive male care, male investment in attraction is expected to reliably indicate paternal care effort and male phenotypic quality. Previous research, yielding contrasting results, has considered how one trait involved in mate attraction interacts with parental care or a specific aspect of male quality. In the blenny Salaria pavo, we perform a comprehensive analysis of the interplay between overall male attractiveness and male quality, the latter in terms of fertility, condition, and parental care. In this fish, males are larger than females, exhibit two sexually dimorphic traits (head crest and anal glands), and solely care for eggs. We generated a male attractiveness index through principal component analyses of morphological traits and quantified parental effort as the total time spent in egg care. In addition, we analyzed the relationships between specific components of attractiveness and male qualities. In agreement with theory predictions, we found that male overall attractiveness is a reliable indicator of fertility, in terms of sperm number, but is unrelated to body condition and parental care effort, with males able to perform high levels of care regardless of their level of advertisement. However, the relative expression of head crest area appears positively related to sperm number but is traded-off with parental care effort. These findings underline the need, in addressing real patterns, to consider interactions between multiple aspects of male display and quality.     

The influence of parental age and weather on testosterone concentration and offspring survival in broods of tawny owl Strix aluco

Previous research has suggested that parental condition may affect offspring mortality patterns by affecting offspring testosterone levels. Accordingly, we hypothesized that there is a relationship between offspring testosterone concentration and survival during the early nestling period, and that both are influenced by parent age/experience and by prey availability. We tested our hypothesis on tawny owls Strix aluco in their first and third known breeding seasons, when they bred either in adverse or mild weather conditions, in Duna-Ipoly National Park, Hungary. Plasma testosterone concentrations of the nestlings were analyzed and related to parental condition, hatching order and nestling mortality. Inexperienced parents breeding in all weather conditions and experienced parents breeding in adverse conditions were both in poor condition compared to experienced parents breeding in mild conditions. Parents in poor condition produced broods with large between-sibling differences in testosterone concentrations and their later-hatched nestlings (which had low testosterone levels) died during the early nestling period, whereas parents in good condition produced broods with lower variation in offspring testosterone concentrations and all offspring survived the early nestling period. We discuss environmental influences on the amount of testosterone deposited in eggs, and also how maternal testosterone might induce those mechanisms producing testosterone in the nestlings.Communicated by M. Webster, T. Czeschlik     

Resources and offspring provisioning: a test of the Trexler-DeAngelis model for matrotrophy evolution

Theoretical models of the evolution of matrotrophy from a lecithotrophic ancestor suggest that resource availability plays a major role in selective scenarios favoring a change in offspring provisioning. We examined effects of feeding level on embryo provisioning in the livebearing fish Gambusia geiseri, a species with dual provisioning of embryos via both yolk sequestered in large eggs and post-fertilization mother-to-embryo nutrient transfer. Females were fed either once per day or once every three days for three months. Females fed daily had marginally larger brood size, significantly larger embryos, and a higher rate of nutrient transfer (assayed directly by injection of radiolabeled nutrients) than females fed every third day. There was no difference in the size of unfertilized eggs between the feeding treatments. Resource effects on matrotrophic provisioning in G. geiseri suggest that matrotrophy plays an important role in provisioning and allows females to adjust offspring size in response to resource availability.     

Robin’s egg blue: does egg color influence male parental care?

A recent hypothesis suggests that birds’ blue-green egg colors may be a sexually selected signal of female (and potentially nestling) quality that males use to make parental investment decisions. While there is some empirical support for this idea, both theory and observations question its validity. To test this hypothesis experimentally, we examined the influence of egg color on male American robin Turdus migratorius behavior by replacing natural clutches with four artificial eggs that were all either pale or vividly colored, close to the extremes in natural egg coloration. At the end of the incubation period, three unrelated nestlings were fostered into each experimental nest, and parental provisioning behavior was monitored when nestlings were 3, 6, and 9 days old. Male provisioning rate for 3-day-old nestlings was significantly higher in the vivid egg treatment compared to both the pale egg treatment and untreated controls, but there was no effect of egg color on paternal behavior at the older nestling stages. Male feeding rate at unmanipulated nests was only weakly positively related to natural egg color (chroma) when nestlings were 3 days old. These results suggest that blue-green egg color may act as a post-mating signal of female quality or investment in this species, but our findings do not exclude the possibility that egg color pigmentation also serves other adaptive functions.     

Elaborately ornamented males avoid costly parental care in the house finch (<Emphasis Type="Italic">Carpodacus mexicanus</Emphasis>): a proximate perspective

Selection should favor flexibility in reproductive tactics when the combination of sexual traits and reproductive behaviors that achieve the highest fitness differs between males within a population. Understanding the functional significance of variation in male reproductive tactics can provide insight into their evolution. Male house finches (Carpodacus mexicanus) in a Montana population display continuous variation in parental tactics: males with more elaborated (redder) plumage color provide little or no parental care compared to less elaborated (dull) males. Here, we first determined whether elevation of prolactin (a pituitary hormone) was related to variation in male parental tactics and, second, we used the relationship between prolactin levels and parental behavior to investigate why redder males avoid a high investment in parental care. We found that prolactin elevation was closely associated with paternal care. In addition, males with redder plumage color had low prolactin levels, whereas dull males, which provision twice as frequently, had high levels of prolactin. We also found that male condition was unrelated to plumage color but negatively related to prolactin levels. These results suggest that the low provisioning of redder males was not due to physiological constraints, but instead reflected a tactic to avoid the costs associated with parental care. The condition benefits accrued by redder males may explain their higher post-breeding survival compared to dull males. Moreover, dull males were previously shown to have higher pairing success than redder males, suggesting that the relationship between male plumage color and parental care may reflect individually optimized parental tactics.Communicated by H. Kokko