Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus)

Abstract.

• 1 To investigate the range of resource size that burying beetles (Nicrophorus) exploit, small (21–33 g), medium (50–90 g) and large (120–210g) carcasses, were placed in the field and then exhumed after 1, 4, 8, 12 or 18 days.
• 2 Nicrophorus attempts to utilize carcasses over this entire size range but has greater success on smaller carcasses.
• 3 Larger carcasses were more difficult to exploit because: (a) they took longer to conceal beneath the leaf litter; (b) they were less likely to be rounded into brood balls; (c) they were more likely to be utilized by dipterans; and (d) they were occupied by greater numbers of congeners.
• 4 Larger carcasses, however, did support greater numbers of larvae and contained broods of greater total mass than smaller carcasses.
• 5 Beetles sometimes bred communally on larger carcasses in the field and same-sex adults were observed to feed young.
• 6 Two follow-up experiments were conducted in the laboratory. On a large carcass N.defodiens, N.tomentosus or N.orbicollis can raise a maximum of 35–50 young. Nicrophorus pustulatus, in contrast, appears to be unique among Nicrophorus in that it can raise nearly 200 young on larger carcasses.
• 7 Nicrophorus orbicollis and Nicrophorus sayi are extremely dependent on parental regurgitations and young fail to survive to the second instar if parents are removed. Young of Nicrophorus defodiens, N.tomentosus and N.pustulatus can develop normally without parental regurgitations.
• 8 I discuss these results in the context of reproduction on carcasses of different size and hypothesize that this breeding system is facultatively quasisocial.

     

Seasonal variation in parental care, offspring development, and reproductive success in the burying beetle, Nicrophorus vespillo

1. Beetles of the genus Nicrophorus reproduce on small vertebrate carcasses that they bury in the soil to provide the larvae with food. Usually, both parents cooperate in brood care by feeding and guarding their progeny. 2. In pairs of the common European species N. vespillo, the duration of care depended on the time of year when the beetles reproduced. Both in 1990 and in 1991, male and female parents stayed longer with their broods when reproduction started in spring than when reproduction started in early or late summer. This was probably due to the longer development time of the larvae caused by lower temperatures in spring, because laboratory experiments suggested a strong influence of temperature on both the duration of brood care and offspring development. 3. The number of adult offspring produced by a beetle pair did not vary among different times of the year. 4. The median time required for offspring development, measured as time from burial of the carcass to emergence of young adults, was between 62 and 84 days. When the beetles reproduced in late summer, only about three-quarters of the offspring left the soil and hibernated as adults. The remaining offspring stayed underground and adults appeared on the soil surface the following spring. They still showed the flexible cuticle typical of newly-hatched beetles, suggesting that they may have overwintered in a pre-adult stage.     

Species packing and temperature dependent competition among burying beetles (Silphidae, Nicrophorus)

Abstract. 1. Burying beetles are carrion feeders that specialize on small carcasses. We investigated interactions among congeners at two sites in Michigan, U.S.A., that differ in both number and relative proportion of species.
2. Intra- and interspecific competition for carcasses is intense. The majority of carcasses are found within 24 h of their placement.
3. Competition between N.arbicollis and N.defodiens is temperature dependent. N.orbicollis can displace N.defodiens on single carcasses, but requires warm temperatures to find the carcasses. Cool weather therefore serves as a refuge for N.defadiens .
4. The southern edge of N.defodien's geographical range is probably determined by competition with N.orbicollis .
5. N.sayi and N.tomenrosus are spring and autumn breeders respectively, and rarely interact with each other or the other two species. Nevertheless, interspecific competition is the most likely evolutionary force leading to seasonal segregation.     

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.     

Regulation of brood size in a burying beetle,Nicrophorus tomentosus (Silphidae)

Regulation of brood size in a biparental burying beetle, Nicrophorus tomentosusWeber, was studied by providing pairs with one of two sizes of mouse carcasses in the laboratory. For a given carcass size, there was an inverse relationship between number and mass offspring in a brood. The requirement for regulation was that brood size was adjusted such that mean mass of individual larvae was constant for carcasses of different size. Brood size was regulated if parents were present but regulation did not occur if parents were removed prior to hatching of larvae. Pairs bred in quick succession on two carcasses raised fewer than the regulated number of young in the second reproductive attempt. Reasons for regulation of brood size in this genus are discussed.     

Social stimuli affect juvenile hormone during breeding in biparental burying beetles (Silphidae: Nicrophorus)

Extended biparental care is rare in insects but provides an excellent opportunity to investigate the interaction between the endocrine system and the physical and social environment in the regulation of this behavior. Burying beetles (Nicrophorus spp.) have facultative biparental care and depend on locating a small vertebrate carcass that they bury and prepare as food for their young. Commonly, both male and female Nicrophorus orbicollis remain in the burial chamber after eggs hatch to feed and guard the larvae. In both sexes, juvenile hormone (JH) rises rapidly in response to the discovery and assessment of the carcass; it returns to near baseline in 24 h; then in females it reaches very high titers at the onset of maternal care. In this paper, we investigate some social (presence of a mate, mating history, larval age) and environmental (carcass size) factors that may affect this endocrine profile. For females, neither the presence of a mate nor mating status (i.e., virginity) affected the initial rise of JH. However, the absence of a mate significantly depressed the JH rise in males. Eighty-seven percent of the single males buried the carcass like paired males but 87% also released pheromones to attract a mate. JH hemolymph titers in females whose broods were replaced every 24 h with newly hatch larvae were significantly higher than those of females rearing aging broods. Lastly, even though larger carcasses took longer to bury and prepare and oviposition was delayed, neither JH titers nor speed of ovarian development was affected by carcass size.     

Biparental care is predominant and beneficial to parents in the burying beetle Nicrophorus orbicollis (Coleoptera: Silphidae)

Parenting strategies can be flexible within a species and may have varying fitness effects. Understanding this flexibility and its fitness consequences is important for understanding why parenting strategies evolve. In the present study, we investigate the fitness consequences of flexible parenting in the burying beetle Nicrophorus orbicollis, a species known for its advanced provisioning behaviour of regurgitated vertebrate carrion to offspring by both sexes. We show that, even when a parent is freely allowed to abandon the carcass at any point in time, biparental post‐hatching care is the most common pattern of care adopted in N. orbicollis. Furthermore, two parents together raised more offspring than single parents of either sex, showing that the presence of the male can directly influence parental fitness even in the absence of competitors. This contrasts with studies in other species of burying beetle, where biparental families do not differ in offspring number. This may explain why biparental care is more common in N. orbicollis than in other burying beetles. We suggest how the fitness benefits of two parents may play a role in the evolution and maintenance of flexible biparental care in N. orbicollis.     

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.     

Burying beetles: intraspecific interactions and reproductive success in the field

Abstract. 1. The discovery and utilization of small carcasses by burying beetles (Silphidae, Nicrophorus ) was studied by placing dead mice at random points on large grids at two Iocations in Michigan, U.S.A.
2. The majority of mice are found within 24 h by more beetles than ultimately will utilize the carcass. If a carcass is likely to be usurped by a larger species of beetle or by a vertebrate, then intraspecific competition may be postponed until the carcass is concealed and buried.
3. Both males and females practice parental care. Maturing broods are tended by no adults, a single female, a single male, or a male—female pair. No differences in brood success were observed among these categories.
4. The female lays a larger clutch than ultimately will survive. Brood size is regulated after the egg stage, such that offspring number varies, but individual offspring size does not.
5. A large amount of unexplained variation exists in brood size, in both the laboratory and the field. This variation is probably caused by the environment, and not the reproductive physiology of the beetles. Competition with microbes is a likely candidate.
6. Differences exist not only between Nicrophorus species, but also between localities for a single species, suggesting adaptation to local environments.     

Adaptation to monogamy influences parental care but not mating behavior in the burying beetle,Nicrophorus vespilloides

The mating system is expected to have an important influence on the evolution of mating and parenting behaviors. Although many studies have used experimental evolution to examine how mating behaviors evolve under different mating systems, this approach has seldom been used to study the evolution of parental care. We used experimental evolution to test whether adaptation to different mating systems involves changes in mating and parenting behaviors in populations of the burying beetle, Nicrophorus vespilloides. We maintained populations under monogamy or promiscuity for six generations. This manipulation had an immediate impact on reproductive performance and adult survival. Compared to monogamy, promiscuity reduced brood size and adult (particularly male) survival during breeding. After six generations of experimental evolution, there was no divergence between monogamous and promiscuous populations in mating behaviors. Parents from the promiscuous populations (especially males) displayed less care than parents from the monogamous populations. Our results are consistent with the hypothesis that male care will increase with the certainty of paternity. However, it appears that this change is not associated with a concurrent change in mating behaviors.     

Changing dominant–subordinate relationships during carcass preparation between burying beetle species (Nicrophorus: Silphidae: Coleoptera)

I studied the influence of carrion burial on the interaction between Nicrophorus quadripunctatus and Nicrophorus vespilloides. In the preburial phase, N. quadripunctatus, the smaller species, occupied more carcasses than N. vespilloides, the larger species, when both species were allowed to compete for mouse carcasses. However, after carcasses were buried, N. vespilloides was more successful in protecting those it had buried, and more successful in intruding on carcasses buried by N. quadripunctatus. Direct observation supported these findings. These results may suggest that N. vespilloides is cleptoparasitic on N. quadripunctatus for carrion burial. Received: March 25, 1999 / Accepted: August 31, 1999     

Juvenile hormone-mediated reproduction in burying beetles: From behavior to physiology

The burying beetle, Nicrophorus orbicollis, is the first beetle exhibiting parental care for which endocrinological studies have been initiated. Burying beetles bury and prepare small vertebrate carcasses as a breeding resource for their offspring. After emergence as an adult, hemolymph titers of juvenile hormone and ovarian size increase in concert for 2–3 weeks, and both plateau until an appropriate resource is discovered. Upon finding a suitable carcass, titers of juvenile hormone increase extremely rapidly (<20 min), and within 18 h ovarian mass increases threefold and oviposition begins. This rapid reproductive development is hypothesized to be selected by the intense competition for these protein-rich but quickly deteriorating resources. Burying beetle females exhibit an additional juvenile hormone surge at the time young hatch. This peak in juvenile hormone is hypothesized to be associated with either the considerable behavioral demands which accompany care of young larvae or with a female's willingness to oviposit a replacement clutch should brood failure occur early in the care-giving phase. Parental care has evolved in at least 16 additional families within the Coleoptera. Comparative studies of nonparental and parental groups will be important for understanding how the physiology of ancestral groups affects the evolution of complex social behavior. Arch. Insect Biochem. Physiol. 35:479–490, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Post-hatching parental care masks the effects of egg size on offspring fitness: a removal experiment on burying beetles

Parents can increase the fitness of their offspring by allocating nutrients to eggs and/or providing care for eggs and offspring. Although we have a good understanding of the adaptive significance of both egg size and parental care, remarkably little is known about the co-evolution of these two mechanisms for increasing offspring fitness. Here, we report a parental removal experiment on the burying beetle Nicrophorus vespilloides in which we test whether post-hatching parental care masks the effect of egg size on offspring fitness. As predicted, we found that the parent's presence or absence had a strong main effect on larval body mass, whereas there was no detectable effect of egg size. Furthermore, egg size had a strong and positive effect on offspring body mass in the parent's absence, whereas it had no effect on offspring body mass in the parent's presence. These results support the suggestion that the stronger effect of post-hatching parental care on offspring growth masks the weaker effect of egg size. We found no correlation between the number and size of eggs. However, there was a negative correlation between larval body mass and brood size in the parent's presence, but not in its absence. These findings suggest that the trade-off between number and size of offspring is shifted from the egg stage towards the end of the parental care period and that post-hatching parental care somehow moderates this trade-off.     

Starving the competition: a proximate cause of reproductive skew in burying beetles (Nicrophorus vespilloides)

Proximate mechanisms underlying reproductive skew are obscure in many animals that breed communally. Here, we address causes of reproductive skew in brood-parasitic associations of burying beetles (Nicrophorus vespilloides). Male and female burying beetles feed and defend their larvae on buried carcasses. When several females locate the same small carcass, they engage in violent physical altercations. The subordinate then acts as an intraspecific brood parasite, laying eggs, but not providing care. The dominant female largely monopolizes access to the carcass; she alone provides parental care and her share of the brood is much larger than the subordinate's. On larger carcasses, subordinates have greater access to the carcass than on small ones, and reproductive skew is reduced. Differential fecundity, ovicide and larvicide have been suggested as causes of skew on small carcasses. Here, we report the results of the experiments pertaining to the first two of these potential mechanisms. Ovicide did not significantly contribute to reproductive skew on small carcasses, but differential fecundity did. Fecundity differences were due to dominance status, not body size per se. Fecundity differences disappeared when supplemental food was available, suggesting that reduced access to the carcass limits fecundity by causing nutritional deficiencies. Supplemental food prevented such nutritional deficiencies and allowed subordinates to produce as many eggs as dominants. Apparently, aggressive behaviour by dominants functions in the context of reproductive competition, limiting subordinate reproduction by preventing food intake on the carcass.     

Dormancy and the influence of photoperiod and temperature on sexual maturity in Nicrophorus nepalensis (Coleoptera: Silphidae)

Abstract Carrion beetles (Nicrophorus spp.) use small vertebrate carcasses for food and reproduction. Their ecology and behaviors are highly affected by the availability of carcasses and the surrounding environmental conditions. Our results revealed that in subtropical Fushan, northern Taiwan, N. nepalensis was mainly active in spring (February to May), and could also be found in autumn (October and November); but there was no capture record in summer (June to September) and winter (December and January). A laboratory temperature tolerance study indicated that N. nepalensis adults become inactive at temperatures above 26°C, and had the highest mortality when the temperature was raised from 27°C to 28°C. Furthermore, N. nepalensis became sexually mature at 20°C, depending on the photoperiod: the longer the day, the lower the percentage of sexually mature 2‐week‐old females after emergence. In another experiment, N. nepalensis virgins were paired under three possible conditions at Fushan. At 15°C and 20°C, if carcasses were presented to the pairs within 3 days after emergence, all laid eggs in the second week after emergence. If carcasses were presented 1 week after emergence, most began to reproduce at 20°C with 12.5 h of daylight. However, at 15°C with 11 h of daylight, the carrion beetles hibernated first, and reproduced in the ninth week after emergence. At 25°C with 14 h of daylight, carrion beetles did not bury the mouse carcasses, the females did not lay eggs, and the adult lifespan was only one‐third of that at 20°C. This study revealed that both photoperiod and temperature influence the time needed to reach the sexual maturity of N. nepalensis; and also implied that the narrow temperature tolerance range and dormancy behavior of carrion beetles are highly regulated by those environmental factors.     

Late‐life and intergenerational effects of larval exposure to microbial competitors in the burying beetle Nicrophorus vespilloides

Intergenerational effects can have either adaptive or nonadaptive impacts on offspring performance. Such effects are likely to be of ecological and evolutionary importance in animals with extended parental care, such as birds, mammals and some insects. Here, we studied the effects of exposure to microbial competition during early development on subsequent reproductive success in the burying beetle Nicrophorus vespilloides, an insect with elaborate parental care. We found that exposure to high levels of microbial competition both during a female's larval development and during her subsequent reproduction resulted in females rearing smaller broods than those exposed to lower levels of microbial competition. To determine whether these differences arose before or after offspring hatching, a cross‐fostering experiment was conducted. Our results demonstrate that the impact of larval competition with microbes for resources extends into adult life and can negatively affect subsequent generations via impacts on the quality of parental care provided after hatching. However, we also find evidence for some positive effects of previous microbial exposure on prehatch investment, suggesting that the long‐term results of competition with microbes may include altering the balance of parental investment between prehatch and post‐hatch care.     

The frequency and fitness consequences of communal breeding in a natural population of burying beetles: a test of reproductive skew

Abstract.  1. Reproductive cooperation occurs in diverse taxa and a defining characteristic of these social systems is how reproduction is shared. Both male and female burying beetles ( Nicrophorus spp.) facultatively form associations to bury a carcass and rear a single brood, making burying beetles a model system for testing skew theory.
2. In this study, 50% of 40–45 g carcasses and 75% of 55–60 g ones were buried by more than one male and/or female Nicrophorus tomentosus .
3. Females were significantly more likely to cooperate on 55–60 g carcasses than on 40–45 g ones.
4. Analysis of parentage of 13 broods using microsatellite loci as genetic markers showed that maternity analysis of only 2% of the young excluded all females captured leaving the brood chamber after burial. Males previously mated with resident females or displaced by resident males fathered 7% of the young.
5. The male and female remaining the longest were usually the parents of the most offspring, and reproductively dominant individuals also tended to be the largest.
6. Although all but two or three individuals that helped to bury the carcass produced some offspring, reproduction was often not shared equitably. Reproduction of females was significantly skewed on six of nine 40–45 g carcasses but shared fairly equitably on all three 55–60 g ones. Reproduction was skewed among males on 7 of 10 broods.
7. Both males and females relinquished a greater proportion of the brood as the days of assistance from all consexuals increased.     

Effect of forest removal on the abundance of the endangered American burying beetle, Nicrophorus americanus (Coleoptera: Silphidae)

We test the hypothesis that the decline of the endangered American burying beetle (Nicrophorus americanus) from over 90% of its original range is the result of habitat loss and fragmentation of eastern North America. Forest removal at a site in southeastern Oklahoma known to have a significant population of N. americanus gave us a unique opportunity to test this hypothesis. At the local scale of this experiment, N. americanus declined significantly after forest removal while beetle numbers at adjacent forested plots did not change. Our results indicate that local disturbances such as forest removal, if occurring across relatively broad spatial scales, can cause wholesale geographic range collapse in this species.