Benefits of communal breeding in burying beetles: a field experiment

1. The ultimate causes of communal breeding and joint parental care in various species of Nicrophorus burying beetles have not been resolved satisfactorily. One hypothesis suggests that females remain on the carcass for extended periods of time because joint defence affords them improved probabilities of retaining the carcass successfully in the face of intense competition from intra‐generic competitors. 2. In a field experiment designed to test this hypothesis in N. defodiens (Mannerheim), breeding associations of two females and a male were no more successful at retaining their carcass than were monogamous pairs, lending no support to the hypothesis. 3. Intra‐generic intruders that usurped already‐buried carcasses were typically much larger than the original residents. 4. The body size of original residents affected both the burial depth and the probability of a takeover. Larger beetles buried the carcass deeper and were more likely to retain possession of the carcass. Group composition also did not affect the depth at which carcasses were buried. 5. Severe and even fatal injuries incurred by some residents indicated the occurrence of violent and damaging fights between competitors over carcasses in the field.     

Timing of oviposition and reproductive skew in cobreeding female burying beetles (Nicrophorus vespilloides)

Burying beetles (genus Nicrophorus) are known for their elaborate parental care. Two or more conspecific females may reproduceon the same carcass, especially when the carcass is large.Here we present the results of experiments in which we observedpatterns of larval hatching and parental care in unmanipulatedcobreeders, manipulated hatching synchrony between cobreeders,and compared patterns of oviposition in cobreeding and single females. Our results show that in these cobreeding associations,one of the females may or may not monopolize the carcass duringthe period of larval hatching. We present evidence that ineither case, infanticide based on temporal cues constitutesan important proximate mechanism underlying the observed reductionin average reproductive success in cobreeding females. Femaleswith higher synchrony (i.e., greater overlap between their oviposition patterns) produce larger broods with lower reproductive skew.Cobreeding females oviposit later and less synchronously thansingle breeders. Such delayed oviposition may reduce the riskthat a female's larvae fall victim to cannibalistic acts committedby her cobreeder or maximize her own opportunity to selectivelykill her cobreeder's larvae.     

Factors affecting overwinter survival of the American burying beetle, <Emphasis Type="Italic">Nicrophorus americanus</Emphasis> (Coleoptera: Silphidae)

The endangered American burying beetle (Nicrophorus americanus) is relatively abundant at Fort Chaffee Maneuver Training Center in northwestern Arkansas. There is a paucity of basic life-history information available, particularly with respect to factors affecting overwintering success. In a field experiment we: (1) captured beetles at Fort Chaffee; (2) bred them in captivity; (3) in the fall on Fort Chaffee placed offspring individually in well-ventilated, lidded 21.1-l buckets containing original soil plugs in grassland or woodland, either provisioned or not with a rat carcass as potential food; (4) overwintered the beetles; (5) checked in the spring to determine survival; and (6) released surviving beetles. Overall, 59.6% of 104 beetles survived the winter, with 77.1% and 44.6% survival in provisioned and nonprovisioned buckets, respectively. No differences were evident between habitats. Beetle age was an important survival predictor, with older beetles having a higher survival probability, but only if nonprovisioned. Gender and body size were not predictive of survival. Many surviving beetles were at or near the surface; depth averaged 6.0 cm, with some as deep as 20 cm. Our findings suggest that American burying beetles will have a higher probability of overwinter survival if carcasses are readily available as winter approaches.     

Mechanisms and fitness effects of antibacterial defences in a carrion beetle

Parents of many species care for their offspring by protecting them from a wide range of environmental hazards, including desiccation, food shortages, predators, competitors, and parasites and pathogens. Currently, little is known about the mechanisms and fitness consequences of parental defences against bacterial pathogens and competitors. Here, we combine approaches from microbiology and behavioural ecology to investigate the role and mechanistic basis of antibacterial secretions applied to carcasses by parents of the burying beetle Nicrophorus vespilloides. This species rears its larvae on vertebrate carcasses, where larvae suffer significant fitness costs due to competition with bacterial decomposers. We first confirm that anal secretions produced by parents are potently bactericidal and that their effects are specific to gram-positive bacteria. Next, we identify the source of bacterial killing as a secreted lysozyme and show that its concentration changes throughout the breeding cycle. Finally, we show that secreted lysozyme is crucial for larval development, increasing survival by nearly two-fold compared to offspring reared in its absence. These results demonstrate for the first time that anal secretions applied to carrion is a form of parental care and expand the mechanistic repertoire of defences used by parent insects to protect dependent offspring from microbial threats.     

Sibling competition does not exacerbate inbreeding depression in the burying beetle Nicrophorus vespilloides

Inbreeding results from matings between relatives and can cause a reduction in offspring fitness, known as inbreeding depression. Previous work has shown that a wide range of environmental stresses, such as extreme temperatures, starvation and parasitism, can exacerbate inbreeding depression. It has recently been argued that stresses due to intraspecific competition should have a stronger effect on the severity of inbreeding depression than stresses due to harsh physical conditions. Here, we tested whether an increase in the intensity of sibling competition can exacerbate inbreeding depression in the burying beetle Nicrophorus vespilloides. We used a 2 × 3 factorial design with offspring inbreeding status (outbred or inbred) and brood size (5, 20, or 40 larvae) as the two factors. We found a main effect of inbreeding status, as inbred larvae had lower survival than outbred larvae, and a main effect of brood size, as larvae in large broods had lower survival and mass than larvae in medium‐sized broods. However, there was no effect of the interaction between inbreeding status and brood size, suggesting that sibling competition did not influence the severity of inbreeding depression. Since we focused on sibling competition within homogeneous broods of either inbred or outbred larvae, we cannot rule out possible effects of sibling competition on inbreeding depression in mixed paternity broods comprising of both inbred and outbred offspring. More information on whether and when sibling competition might influence inbreeding depression can help advance our understanding of the causes underlying variation in the severity of inbreeding depression.     

Population density, body size, and phenotypic plasticity of brood size in a burying beetle

Theory predicts that organisms living in heterogeneous environmentswill exhibit phenotypic plasticity. One trait that may be particularlyimportant in this context is the clutch or brood size becauseit is simultaneously a maternal and offspring characteristic.In this paper, I test the hypothesis that the burying beetle,Nicrophorus orbicollis, adjusts brood size, in part, in anticipationof the reproductive environment of its adult offspring. N. orbicollisuse a small vertebrate carcass as a food resource for theiryoung. Both parents provide parental care and actively regulatebrood size through filial cannibalism. The result is a positivecorrelation between brood size and carcass size. Adult bodysize is an important determinant of reproductive success forboth sexes, but only at higher population densities. I testthree predictions generated by the hypothesis that beetles adjustbrood size in response to population density. First, averageadult body size should vary positively with population density.Second, brood size on a given-sized carcass should be larger(producing more but smaller young) in low-density populationsthan in high-density populations. Third, females should respondadaptively to changes in local population density by producinglarger broods when population density is low and small broodswhen population density is high. All three predictions weresupported using a combination of field and laboratory experiments.These results (1) show that brood size is a phenotypically plastictrait and (2) support the idea that brood size decisions arean intergenerational phenomenon that varies with the anticipatedcompetitive environment of the offspring.     

Why are males more attractive after brood care? Proximate causes of enhanced sex pheromone emission in a burying beetle

Recent studies demonstrate that pheromones can be costly to produce and emit and, therefore, the types and quantities that they express are likely to covary with individual condition. Previous experiments reveal that, when given the opportunity to breed and care for young, male burying beetles Nicrophorus vespilloides go on to produce a higher amount of their sex pheromone and attract more females than control males that do not exhibit parental care. This finding is surprising because parental care is usually assumed to be energetically costly, reducing the future capacity to invest in sexual signalling. However, burying beetles reproduce on dead vertebrates and the carrion meal might enable males to acquire resources that can subsequently be allocated to pheromone signalling. Alternatively, males might accumulate pheromone precursors because they do not emit their sex pheromone during brood care. To shed light on the mechanisms of enhanced pheromone emission after brood care, in the present study, we test the effect of diet quality, social condition during care (biparental versus uniparental care) and an experimentally enforced calling pause on subsequent male pheromone emission, body weight and energy storage components. The experimentally enforced calling pause and social condition during brood care demonstrate no impact on pheromone quantity. However, the results of the present study suggest that the vertebrate carrion meal during brood care partly explains enhanced pheromone release after care. Unravelling the biosynthetic pathways of the pheromone components and analyzing the impact of potential microbial symbionts on pheromone production represents a fruitful avenue for future research.     

Dynamic changes in volatile emissions of breeding burying beetles

Burying beetles reproduce on small vertebrate carcasses by exhibiting elaborate biparental brood care. Partner recognition in breeding Nicrophorus species (Coleoptera: Silphidae) relies substantially on information encoded in cuticular hydrocarbon profiles. Until recently, it was unknown whether breeding burying beetles also produce volatile low molecular weight substances and, if so, which functions can be attributed to such volatiles. The present study reports a survey of the volatiles released by males and females of Nicrophorus vespilloides Herbst in nonbreeding status and at different stages of breeding. Headspace analyses are performed by using solid phase micro‐extraction fibres and gas chromatography–mass spectrometry. The volatiles released by nonbreeding males and females include phenolic compounds, alcohols, aldehydes and ketones and are quite similar in both sexes. With the onset of breeding, the volatile profiles of males and females become distinct, with a number of female‐specific compounds occurring. An analysis of the anal secretions reveals the presence of some of the compounds previously detected in the headspace analysis. The specific chemical properties suggest that some of the volatiles may function against competitors and parasites, such as bacteria, fungi, nematodes and arthropods at the carcass breeding resource. By contrast, the emission of 4‐methyl branched esters by the females closely parallels the emission of the terpenoid methyl geranate and they may function together as a complex signal by the females. Signalling traits associated with biparental care and specific constraints associated with the ephemeral nature of the breeding resource may explain the occurrence of both groups of compounds in the volatile profiles.     

A test of the competitive ability–cold tolerance trade-off hypothesis in seasonally breeding beetles

1. Closely related species that use similar resources often differ in their seasonal patterns of activity, but the factors that limit their distributions across seasons are unknown for most species. One hypothesis to explain seasonal variation in the distributions of species involves a trade-off between competitive ability and cold tolerance, where tolerance to the cold compromises competitive ability in warmer (benign) temperatures, either at the level of the individual or population.
2. We tested both individual-level and population-level mechanisms of this hypothesis in two co-occurring species of temperate burying beetles (Silphidae: Nicrophorus sayi, N. orbicollis) that differ in their seasonal patterns of activity.
3. We measured cold tolerance, breeding activity as a function of temperature, and competitive ability as a function of temperature and season.
4. Consistent with our hypothesis, the mid-season N. orbicollis was less able to function at the cold temperatures that characterise early spring, when the early-season N. sayi is most active. The larger beetle, however, always won one-on-one competitive trials at warm temperatures, regardless of species, inconsistent with an individual-level trade-off. N. orbicollis was usually larger and successful when competing for the same carrion later in the season, mostly because of its larger population size, consistent with a trade-off between competitive ability, and cold tolerance acting at the population level.
5. Our findings suggest that cold temperatures limit the mid-season N. orbicollis from earlier spring emergence, while competitive pressure from the more abundant, larger N. orbicollis constrains the early-season N. sayi from remaining active through the summer.

     

Staying with the young enhances the fathers’ attractiveness in burying beetles

Studying the relationship between parental and mating effort helps us to understand the evolution of parental care and, consequently, has been the subject of many theoretical and empirical investigations. Using burying beetles as a model, we found no correlation between the intensity of a sexual signal (sex pheromone quantity) and the amount of care provided by males. However, males that were given the opportunity to breed and care for young went on to produce a higher amount of their sexual signal and attracted three times more females in the field than control males that were not given the opportunity to breed. The likely explanation for our finding is that specific aspects of care in burying beetles, that is the defense and preservation of a nutrient rich breeding resource, a small vertebrate cadaver, is not only beneficial for the offspring but also for the adults themselves. Obtaining a good carrion meal possibly enables males to store resources that they can subsequently allocate toward sexual signaling. Collectively, our results highlight that conditions can exist where male participation in brood care has a positive effect on its sexual attractiveness. This in turn might have facilitated the evolution of male assistance in parental care.