Obligate costs of parental care to offspring: egg brooding-induced hypoxia creates smaller, slower and weaker python offspring

Python egg brooding typifies parental care because it consists of multiple behaviours that provide for multiple developmental needs. For example, tightly coiling around the eggs benefits embryonic water balance, but periodic female postural adjustments improve embryonic gas exchange. Regardless of these postural adjustments, egg brooding creates a hypoxic intra-clutch environment that constrains embryonic metabolism. We further examined this novel and useful parental care model to determine: (1) any fitness-related costs of egg brooding to offspring; (2) whether any long-term costs are alleviated by postural adjustments. We artificially incubated Children's python ( Antaresia childreni ) clutches and modulated oxygen partial pressure ( P O₂) to create three treatments: normoxic (NRM, 20.3 kPa O₂), brooding [BRD, P O₂ profile typical of clutch P O₂ ( P O_2clutch) in maternally brooded clutches, 15.8–19.3 kPa O₂] and low (LOW, predicted P O₂ profile of maternally brooded P O_2clutch if females did not make postural adjustments, 14.4–18.6 kPa O₂). Using various metrics from ∼12 days pre-hatching to 14 days post-hatching, we demonstrated that NRM offspring were larger, faster and stronger than BRD offspring. As only hatchling heart mass differed between BRD and LOW treatments (LOW > BRD), postural adjustments may not alleviate hypoxia-related costs to embryos. Our results demonstrate that parental care may represent a compromise between competing developmental needs and thus entails obligate costs to the offspring.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 414–421.     

Do Brooding Pythons Recognize their Clutches? Investigating External Cues for Offspring Recognition in the Children's Python,Antaresia childreni

Parental care provides substantial benefits to offspring but exacts a high cost to parents, necessitating the evolution of offspring recognition systems when the risk of misdirected care is high. In species that nest, parents can use cues associated with the offspring (direct offspring recognition) or the nest (indirect offspring recognition) to reduce the risk of misdirected care. Pythons have complex parental care, but a low risk of misdirected care. Thus, we hypothesized that female Children's pythons (Antaresia childreni) use indirect cues to induce and maintain brooding behavior. To test this, we used a series of five clutch manipulations to test the importance of various external brooding cues. Contrary to our hypothesis, we found that female A. childreni are heavily internally motivated to brood, needing only minimal external cues to induce and maintain egg‐brooding behavior. Females were no more likely to brood their own clutch in the original nest as they were to brood a clutch from a conspecific, a pseudoclutch made from only the shells of a conspecific, or their clutch in a novel nest. The only scenario where brooding was reduced, but even then not eliminated, was when the natural clutch was replaced with similarly sized stones. These results suggest that egg recognition in pythons is similar to that of solitary‐nesting birds, which have similar nesting dynamics.     

Maternal brooding in the children’s python <Emphasis Type="Italic">(Antaresia childreni)</Emphasis> promotes egg water balance

Parental care provides considerable benefits to offspring and is widespread among animals, yet it is relatively uncommon among squamate reptiles (e.g., lizards and snakes). However, all pythonine snakes show extended maternal egg brooding with some species being facultatively endothermic. While facultative endothermy provides thermal benefits, the presence of brooding in non-endothermic species suggests other potential benefits of brooding. In this study we experimentally tested the functional significance of maternal brooding relative to water balance in the children’s python, Antaresia childreni, a small species that does not exhibit facultative endothermy. Clutch evaporative water loss (EWL) was positively correlated with clutch mass and was much lower than expected values based on individual eggs. The conglomerate clutch behaved as a single unit with a decreasing surface area to volume ratio as clutch size increased. Maternal brooding had a dramatic impact on evaporation from eggs, reducing and possibly eliminating clutch EWL. In a separate experiment, we found that viability of unattended eggs is highly affected by humidity level, even in the narrow range from 75 to 100% relative humidity at 30.5°C (20–33 mg m⁻³ absolute humidity). However, the presence of the brooding female ameliorated this sensitivity, as viability of brooded clutches at 75% relative humidity was higher than that of non-brooded eggs at either the same absolute humidity or at near-saturated conditions. Overall, these results demonstrate that brooding behavior strongly promotes egg water balance (and thus egg viability) in children’s pythons.     

Temporal and spatial complexity of maternal thermoregulation in tropical pythons

Parental care is a widespread adaptation that evolved independently in a broad range of taxa. Although the dynamics by which two parents meet the developmental needs of offspring are well studied in birds, we lack understanding about the temporal and spatial complexity of parental care in taxa exhibiting female-only care, the predominant mode of parental care. Thus, we examined the behavioral and physiological mechanisms by which female water pythons Liasis fuscus meet a widespread developmental need (thermoregulation) in a natural setting. Although female L. fuscus were not facultatively thermogenic, they did use behaviors on multiple spatial scales (e.g., shifts in egg-brooding postures and surface activity patterns) to balance the thermal needs of their offspring throughout reproduction (gravidity and egg brooding). Maternal behaviors in L. fuscus varied by stage within reproduction and were mediated by interindividual variation in body size and fecundity. Female pythons with relatively larger clutch sizes were cooler during egg brooding, suggesting a trade-off between reproductive quantity (size of clutch) and quality (developmental temperature). In nature, caregiving parents of all taxa must navigate both extrinsic factors (temporal and spatial complexity) and intrinsic factors (body size and fecundity) to meet the needs of their offspring. Our study used a comprehensive approach that can be used as a general template for future research examining the dynamics by which parents meet other developmental needs (e.g., predation risk or energy balance).     

Thermal influences on foraging ability: body size, posture and cooling rate of an ambush predator, the python Morelia spilota

1. The interface between thermal biology and foraging mode has attracted little scientific attention, but may be crucially important to the biology of ectothermic predators. Slip & Shine (1988c) suggested that the ability of large heavy-bodied snakes to ambush nocturnally active mammals relied on the snakes' control of cooling rates through their thermal inertia (via body size and postural adjustments) and microhabitat selection.
2. We tested assumptions underlying this hypothesis, using Diamond Pythons ( Morelia s . spilota ) from southeastern New South Wales. Our laboratory studies confirmed that larger body sizes and coiled postures significantly retarded cooling rates, and that body temperature affected the snakes' ability to detect potential prey items.
3. The magnitude of these effects on cooling rates was great enough to extend the time period substantially over which an adult Diamond Python, lying in ambush in a suitable microhabitat, would be able to detect and capture nocturnally active prey. For example, the times taken for pythons to reach thermal equilibration under our experimental conditions (cooling from 33 to 12°C) were <1h for hatchling pythons regardless of posture, 1 h for outstretched juveniles, 2 h for coiled juveniles and outstretched adults, and almost 8 h for coiled adults.
4. The high rates of cooling of juvenile pythons, even when they are tightly coiled, may force them to rely upon diurnally active prey rather than crepuscular or nocturnal species.     

Respiratory morphology of the Abedus herberti Hidalgo egg chorion (Hemiptera: Belostomatidae)

Although giant water bugs (Hemiptera: Belostomatidae) are large, aquatic insects known for their obligate paternal egg brooding behaviors, little research has focused on the structure of their eggs. The respiratory requirements of developing embryos likely created selection for brooding, so a thorough understanding of the respiratory morphology of belostomatid eggs could help explain how brooding behaviors facilitate embryonic gas exchange. This study used scanning electron microscopy to document the respiratory microstructure of the eggs of Abedus herberti, a back brooding giant water bug. The exochorion is similar to that of other belostomatids in texture and organization except that the respiratory region is confined to the uppermost quarter of the egg. This is the area exposed to the atmosphere by encumbered males. A plastron network made up of densely packed vertical projections demarcates the boundary between the respiratory and nonrespiratory regions of the chorion. The internal chorion is composed of alternate air‐filled and denser layers that likely facilitate the movement of oxygen from the aeropyles at the top of the eggs to the developing embryonic tissues. J. Morphol., 2011. © 2011 Wiley‐Liss, Inc.     

The use of ultrasonography to assess reproductive investment and output in pythons

Reproductive investment and output are integral fitness components, often incorporated into life‐history trade‐off models and important to population dynamics. The trade‐offs associated with reproduction can be dramatic in species such as snakes that make especially large investments into reproduction. Unfortunately, traditional methods used to determine reproductive investment and output are effective in many (but not all) situations. Thus, we used portable ultrasonography to serially estimate reproductive investment and reproductive output in three python species that exhibit significant variation in phylogeny, geographic range, body size, egg size, and clutch size: ball pythons (Python regius), Children's pythons (Antaresia childreni), and water pythons (Liasis fuscus). At each time point of measurement (range: 1–49 days pre‐oviposition), ultrasound estimates of viable clutch size were highly accurate in all three species. However, ultrasound estimates of mean viable egg mass, and thus viable clutch mass, significantly differed from the actual values (range: 23–73% error). Interestingly, this error was considerably smaller as females approached oviposition, suggesting that female pythons transfer a significant amount of water into their eggs during the week before oviposition. Thus, water balance during late‐stage egg development may be an integral part of reproductive success. The results obtained in the present study form the foundation for future assessments of reproductive investment, and also provide insight into the use of ultrasound technology to assist such efforts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 772–778.     

Extended Mother–Offspring Relationships in Crayfish: The Return Behaviour of Juvenile Procambarus Clarkii

Crayfish shows a relatively complex parental behaviour compared with other invertebrates, but the literature provides only anecdotal accounts of this phenomenon. In Procambarus clarkii, we described the ‘return’ behaviour of third‐stage juveniles when offered four types of adults: biological mothers, foster mothers, non‐brooding females and males. Then, we analysed the posture and behaviour of the adults to understand the role played by the putative mother in attracting the juveniles. Contrary to non‐brooding individuals, both biological and foster mothers displayed a relatively rare locomotion, executed few cleaning and feeding acts, and never attempted to prey on juveniles. They often assumed a ‘spoon‐like telson posture’ that seemed to facilitate offspring’s approaches. Juveniles increased the frequency of tail‐flips away in the presence of non‐brooding adults; conversely, they accepted foster mothers, along with biological mothers, but not as fast as the latter. Taken together, these results suggest that mother–offspring relationships in P. clarkii are more refined than previously thought, being possibly a key factor enabling this species to thrive in harsh environmental conditions.     

δ18O‐derived incubation temperatures of oviraptorosaur eggs

In order to determine the incubation temperature of eggs laid by non‐avian dinosaurs, we analysed the oxygen isotope compositions of both eggshell carbonate (δ¹⁸O_c) and embryo bone phosphate (δ¹⁸O_p) from seven oviraptorosaur eggs with preserved in ovo embryo bones. These eggs come from the Upper Cretaceous Nanxiong Formation of Jiangxi Province, China. Oviraptorosaur theropods were selected because of their known brooding behaviour as evidenced by preserved adult specimens fossilized in brooding posture on their clutch. Incubation temperature of these embryos was estimated based on the following considerations: eggshell δ¹⁸O_c value reflects the oxygen isotope composition of egg water fluid; embryo bones precipitate from the same egg fluid; and oxygen isotope fractionation between phosphate and water is controlled by the egg temperature. A time‐dependent model predicting the δ¹⁸O_p evolution of the embryo skeleton during incubation as a function of egg temperature was built, and measured δ¹⁸O_c and δ¹⁸O_p values used as boundary conditions. According to the model outputs, oviraptorosaurs incubated their eggs within a 35–40°C range, similar to extant birds and compatible with the known active brooding behaviour of these theropod dinosaurs. Provided that both eggshell and embryo bones preserved their original oxygen isotope compositions, this method could be extended to investigate some reproductive traits of other extinct groups of oviparous amniotes.     

Ecological and environmental factors related to variation in egg size of New World flycatchers

Geographical variation in egg size is well documented for several taxa, but remains insufficiently described for birds in spite of a well‐known latitudinal gradient in clutch size. Several hypotheses have been proposed to explain avian egg size variation; however, they were not tested on a continental scale. Egg size is a key component of reproductive investment that influences offspring fitness. It is thought to vary geographically as one of a set of correlated life‐history traits that are under selection from varying ecological conditions. We completed a comprehensive literature review and calculated egg sizes for the most widespread clade within tyrant flycatchers, describing for the first time the geographical variation in egg size on a continental scale. We examined the relative support for ecological and environmental variables in explaining egg size variation using multi‐model inference and linear mixed models controlled for phylogenetic autocorrelation among species. We tested five hypotheses and found that: larger eggs occur in colder sites, which is consistent with the embryonic temperature hypothesis; medium/long‐distance migrants had smaller eggs than resident species while short‐distance migrants had the largest eggs; neither species clutch size, nor species nest type, nor evapotranspiration seasonality influenced egg size. Avian egg size is larger in Austral and Neotropical America (ANA), where species are resident or short‐distance migrants, and smaller across the medium/long‐distance migrants of the Nearctic region. In addition, while clutch size increases towards higher northern latitudes and is almost invariable across ANA species, egg sizes vary largely across ANA sites, increasing with southern latitudes and higher elevations and being influenced by summer temperature. While the embryonic temperature hypothesis has been usually linked to parental nest attentiveness, we highlight that environmental temperatures also have strong effects in shaping investment in egg size.     

Egg size and offspring quality: a meta‐analysis in birds

Parents affect offspring fitness by propagule size and quality, selection of oviposition site, quality of incubation, feeding of dependent young, and their defence against predators and parasites. Despite many case studies on each of these topics, this knowledge has not been rigorously integrated into individual parental care traits for any taxon. Consequently, we lack a comprehensive, quantitative assessment of how parental care modifies offspring phenotypes. This meta‐analysis of 283 studies with 1805 correlations between egg size and offspring quality in birds is intended to fill this gap. The large sample size enabled testing of how the magnitude of the relationship between egg size and offspring quality depends on a number of variables. Egg size was positively related to nearly all studied offspring traits across all stages of the offspring life cycle. Not surprisingly, the relationship was strongest at hatching but persisted until the post‐fledging stage. Morphological traits were the most closely related to egg size but significant relationships were also found with hatching success, chick survival, and growth rate. Non‐significant effect sizes were found for egg fertility, chick immunity, behaviour, and life‐history or sexual traits. Effect size did not depend on whether chicks were raised by their natural parents or were cross‐fostered to other territories. Effect size did not depend on species‐specific traits such as developmental mode, clutch size, and relative size of the egg, but was larger if tested in captive compared to wild populations and between rather than within broods. In sum, published studies support the view that egg size affects juvenile survival. There are very few studies that tested the relationship between egg size and the fecundity component of offspring fitness, and no studies on offspring survival as adults or on global fitness. More data are also needed for the relationships between egg size and offspring behavioural and physiological traits. It remains to be established whether the relationship between egg size and offspring performance depends on the quality of the offspring environment. Positive effect sizes found in this study are likely to be driven by a causal effect of egg size on offspring quality. However, more studies that control for potential confounding effects of parental post‐hatching care, genes, and egg composition are needed to establish firmly this causal link.     

Parent–offspring conflict and selection on egg size in turtles

The trade‐off between offspring size and number can present a conflict between parents and their offspring. Because egg size is constrained by clutch size, the optimal egg size for offspring fitness may not always be equivalent to that which maximizes parental fitness. We evaluated selection on egg size in three turtle species (Apalone mutica, Chelydra serpentina and Chrysemys picta) to determine if optimal egg sizes differ between offspring and their mothers. Although hatching success was generally greater for larger eggs, the strength and form of selection varied. In most cases, the egg size that maximized offspring fitness was greater than that which maximized maternal fitness. Consistent with optimality theory, mean egg sizes in the populations were more similar to the egg sizes that maximized maternal fitness, rather than offspring fitness. These results provide evidence that selection has maximized maternal fitness to achieve an optimal balance between egg size and number.     

Male parental care and its adaptive significance in a neotropical frog

In the Puerto Rican frog Eleutherodactylus coqui, parental care is performed exclusively by males, and consists of attending the eggs and hatchlings at a terrestrial oviposition site. The two major behavioural components of parental care are egg brooding and nest defence against conspecific egg cannibals. Defence behaviour includes aggressive calling, biting, sustained biting, wrestling, and blocking directed against nest intruders. Parental care lasts from oviposition to hatching (17–26 days) and often for several days after hatching. During pre-hatching development, males are present in their nests 97.4% of the time during the day and 75.8% of the time at night. A large portion of this time is spent brooding eggs. In a field experiment, males were removed from their nests and the fate of clutches was monitored. Compared to control clutches (males not removed), experimental clutches had significantly lower hatching success and suffered significantly greater mortality from desiccation and cannibalism. Hence, parental care yields significant benefits to male fitness via increased offspring survival.     

Avian Incubation Patterns Reflect Temporal Changes in Developing Clutches

Incubation conditions for eggs influence offspring quality and reproductive success. One way in which parents regulate brooding conditions is by balancing the thermal requirements of embryos with time spent away from the nest for self-maintenance. Age related changes in embryo thermal tolerance would thus be expected to shape parental incubation behavior. We use data from unmanipulated Black-capped Chickadee (Poecile atricapillus) nests to examine the temporal dynamics of incubation, testing the prediction that increased heat flux from eggs as embryos age influences female incubation behavior and/or physiology to minimize temperature fluctuations. We found that the rate of heat loss from eggs increased with embryo age. Females responded to increased egg cooling rates by altering incubation rhythms (more frequent, shorter on- and off- bouts), but not brood patch temperature. Consequently, as embryos aged, females were able to increase mean egg temperature and decrease variation in temperature. Our findings highlight the need to view full incubation as more than a static rhythm; rather, it is a temporally dynamic and finely adjustable parental behavior. Furthermore, from a methodological perspective, intra- and inter-specific comparisons of incubation rhythms and average egg temperatures should control for the stage of incubation.     

The relationship between female brooding and male nestling provisioning: does climate underlie geographic variation in sex roles?

Comparative studies of populations occupying different environments can provide insights into the ecological conditions affecting differences in parental strategies, including the relative contributions of males and females. Male and female parental strategies reflect the interplay between ecological conditions, the contributions of the social mate, and the needs of offspring. Climate is expected to underlie geographic variation in incubation and brooding behavior, and can thereby affect both the absolute and relative contributions of each sex to other aspects of parental care such as offspring provisioning. However, geographic variation in brooding behavior has received much less attention than variation in incubation attentiveness or provisioning rates. We compared parental behavior during the nestling period in populations of orange‐crowned warblers Oreothlypis celata near the northern (64°N) and southern (33°N) boundaries of the breeding range. In Alaska, we found that males were responsible for the majority of food delivery whereas the sexes contributed equally to provisioning in California. Higher male provisioning in Alaska appeared to facilitate a higher proportion of time females spent brooding the nestlings. Surprisingly, differences in brooding between populations could not be explained by variation in ambient temperature, which was similar between populations during the nestling period. While these results represent a single population contrast, they suggest additional hypotheses for the ecological correlates and evolutionary drivers of geographic variation in brooding behavior, and the factors that shape the contributions of each sex.     

Double brooding and offspring desertion in the barn owl Tyto alba

Many bird species produce two annual broods during a single breeding season. However, not all individuals reproduce twice in the same year suggesting that double brooding is condition‐dependent. In contrast to most raptors and owls, the barn owl Tyto alba produces two annual clutches in most worldwide distributed populations. Nevertheless, the determinants of double brooding are still poorly studied. We performed such a study in a Swiss barn owl population monitored between 1990 and 2014. The annual frequency of double brooding varied from 0 to 14% for males and 0 to 59% for females. The likelihood of double brooding was higher when individuals initiated their first clutch early rather than late in the season and when males had few rather than many offspring at the first nest. Despite the reproductive benefits of double brooding (single‐ and double‐brooded individuals produced 3.97 ± 0.11 and 7.07 ± 0.24 fledglings, respectively), double brooding appears to be traded off against offspring quality because at the first nest double‐brooded males produced poorer quality offspring than single‐brooded males. This might explain why females desert their first mate to produce a second brood with another male without jeopardizing reproductive success at the first nest. Furthermore, the reproductive cycle being very long in the barn owl (120 d from start of laying to offspring independence), selection may have favoured behaviours that accelerate the initiation of a second annual brood. Accordingly, half of the double‐brooded females abandoned their young offspring to look for a new partner in order to initiate the second breeding attempt, 9.48 d earlier than when producing the second brood with the same partner. We conclude that male and female barn owls adopt different reproductive strategies. Females have more opportunities to reproduce twice in a single season than males because mothers are not strictly required during the entire rearing period in contrast to fathers. A high proportion of male floaters may also encourage females to desert their first brood to re‐nest with a new male who is free of parental care duties.     

Lesser double‐collared sunbirds Nectarinia chalybea do not compensate for hatching asynchrony by adjusting egg mass or yolk androgens

Substantial amounts of maternal androgens are found in birds’ eggs and have been shown to benefit offspring development. Within‐clutch patterns of increasing androgen concentrations over the laying sequence are often hypothesized to compensate for the negative effects of hatching asynchrony. However, detrimental effects to offspring fitness of exposure to high yolk androgen levels have also been demonstrated. This suggests that mothers should forego these costs to their offspring when the need for compensation for hatching asynchrony is low or when alternative compensatory strategies, e.g. in terms of increasing egg mass, are available. Here we show that in the south‐temperate lesser double‐collared sunbird Nectarinia chalybea, a species with hatching asynchrony but also with high survival of last‐hatched chicks, mothers do not deposit resources differentially in terms of either yolk androgen concentration or egg mass across the laying sequence. We discuss to what extend this challenges the original explanation of within‐clutch variation in these egg parameters and offer some explanation for their between‐clutch variation which was related to female body mass.     

Life-history and ecological correlates of geographic variation in egg and clutch mass among passerine species

Broad geographic patterns in egg and clutch mass are poorly described, and potential causes of variation remain largely unexamined. We describe interspecific variation in avian egg and clutch mass within and among diverse geographic regions and explore hypotheses related to allometry, clutch size, nest predation, adult mortality, and parental care as correlates and possible explanations of variation. We studied 74 species of Passeriformes at four latitudes on three continents: the north temperate United States, tropical Venezuela, subtropical Argentina, and south temperate South Africa. Egg and clutch mass increased with adult body mass in all locations, but differed among locations for the same body mass, demonstrating that egg and clutch mass have evolved to some extent independent of body mass among regions. A major portion of egg mass variation was explained by an inverse relationship with clutch size within and among regions, as predicted by life-history theory. However, clutch size did not explain all geographic differences in egg mass; eggs were smallest in South Africa despite small clutch sizes. These small eggs might be explained by high nest predation rates in South Africa; life-history theory predicts reduced reproductive effort under high risk of offspring mortality. This prediction was supported for clutch mass, which was inversely related to nest predation but not for egg mass. Nevertheless, clutch mass variation was not fully explained by nest predation, possibly reflecting interacting effects of adult mortality. Tests of the possible effects of nest predation on egg mass were compromised by limited power and by counterposing direct and indirect effects. Finally, components of parental investment, defined as effort per offspring, might be expected to positively coevolve. Indeed, egg mass, but not clutch mass, was greater in species that shared incubation by males and females compared with species in which only females incubate eggs. However, egg and clutch mass were not related to effort of parental care as measured by incubation attentiveness. Ecological and life-history correlates of egg and clutch mass variation found here follow from theory, but possible evolutionary causes deserve further study.     

Parental care trade‐offs in the inter‐brood phase in Barn Swallows Hirundo rustica

In seasonal environments with limited time and energy resources, double‐brooded birds face trade‐offs in the timing of their two reproductive attempts and in the effort allocated to the first and the second broods. In the Barn Swallow Hirundo rustica a long care period for the first brood enhances the survival of first‐brood chicks, but also delays the start of the second brood, which in turn reduces the survival prospects of second‐brood chicks. Probably as a response to this trade‐off, double‐brooded Barn Swallows reduce the period of post‐fledging care for first‐brood fledglings. By radiotracking whole families, we investigated the determinants of this behaviour and its consequences for the survival of the first‐brood fledglings. The end of the females’ investment in post‐fledging care of the first brood was related to the beginning of egg synthesis for the second clutch. With the start of egg synthesis, females significantly reduced provisioning rates to the first‐brood fledglings to less than one‐fifth of the previous rates, while the proportion of time they spent foraging remained high. Assuming that the females’ foraging success was constant, we conclude that their energy income was allocated to egg production rather than fledgling provision. Males did not compensate for the females’ reduced feeding rates. Thus the start of egg production for the second clutch had a marked effect on the quantity of food received by first‐brood fledglings. In parallel with the changes in parental behaviour and provisioning rates, we observed a marked drop in the daily survival rate of first‐brood chicks. These results support the hypothesis that females face a strong trade‐off in the allocation of energy to subsequent broods. Energy allocation to a second clutch involves a cost in terms of reduced provisioning, and as a result the survival of first‐brood chicks is compromised. This is probably outweighed by the improved success of an early second brood.     

Adjustment of parental expenditure in sympatric <Emphasis Type="Italic">Onthophagus</Emphasis> beetles (Coleoptera: Scarabaeidae)

Many organisms adjust their parental expenditure to offspring in response to resource quality. However, the mechanisms underlying the adjustment in parental expenditure are not well understood. We examined the adjustments in parental expenditure and subsequent offspring performance in two sympatric, closely related dung beetles, Onthophagus ater and O. fodiens, that were provided either monkey, deer, horse, or cow dung. The egg contained within each dung brood mass provisioned by the parent beetles develops to adulthood underground. Thus, the size of the brood mass roughly represents the amount of parental expenditure. The brood mass size differed between the two species and among the four dung types. Results of offspring performance suggested that O. ater parents optimally adjusted the brood mass size in response to dung quality, whereas O. fodiens parents did not. We hypothesized that brood mass size in O. ater may increase with prolonged egg maturation caused by the lower nutrition level of cow dung. In addition, our complex results may be explained in part by the specific threshold concept of dung quality (i.e., water content and nutritional level).