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.

     

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.     

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.     

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.     

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.     

Interference competition among burying beetles (Silphidae, Nicrophorus)

Abstract. 1. This study investigated the impact of intraspecific and interspecific competition on the reproductive success of a biparental burying beetle, Nicrophorus defodiens Mannerheim.
2. Marked pairs or single females were placed on small and large mouse carcasses in the field in 1985 and 1986. Carcasses were exhumed after 9–10 days to determine the identity of the resident adult(s) and the production of young.
3. Competition was assessed by the prevalence of takeovers by intruders (unmarked adults). For N.defodiens , after the initial colonization of the carcass, interspecific competition from larger N.orbicollis Say and N.sayi Laporte was substantial and more intense than intraspecific competition. Competition was also greater in the middle of the breeding season and on large as opposed to small carcasses.
4. Successful takeovers resulted in the expulsion of the prior resident(s), killing of any offspring present on the carcass, and oviposition of a new clutch by the intruder.
5. Females aided by males were more likely than single females to avoid takeovers but did not produce larger broods or larvae of larger mass.
6. An additional laboratory experiment in 1985 and a field experiment in 1986 suggest that N.defodiens is able to reproduce on very small carcasses despite intense heterospecific activity.     

Nestmate recognition in burying beetles: the "breeder's badge" as a cue used by females to distinguish their mates from male intruders

Burying beetles use small vertebrate carcasses as food for theirlarvae and defend these carcasses against intra- and interspecificcompetitors. Breeding associations on carcasses can consistof single females, heterosexual pairs, or various combinationsof males and females. When a heterosexual pair collaborate ina breeding attempt, they do not typically exhibit aggressivebehavior toward each other, but do attack newly arrived conspecificsthat attempt to usurp the carcass. We investigated the cuesinvolved in discrimination between breeding partners and intrudersby female burying beetles. We found that resident females toleratemales that have cared for a brood, as well as males that havenot cared for a brood but have been on a carcass for a day ortwo. Males that have had no prior contact with a carcass areattacked. Females appear to use a chemical cue, the "breeder'sbadge," an apolar substance on the male's cuticle that can beremoved by washing with pentane. This cue is reliably correlatedwith recent male experience with a carcass that is suitablefor reproduction. The breeder's badge develops as a result ofprolonged contact with such a carcass, and disappears on removalfrom the carcass; its presence does not require contact witha female or with larvae. Female recognition of their male partnersin burying beetles thus does not involve individual recognition,but rather recognition of reproductive condition.     

Use of infochemicals to attract carrion beetles into pitfall traps

When the bodies of small vertebrates start to decay shortly after death, a number of organosulfur compounds are produced, including methanethiol, dimethylsulfide (DMS), dimethyldisulfide (DMDS), dimethyltrisulfide (DMTS), and S-methyl thioacetate. These molecules appear to attract various necrophagous animals. We tested the roles of DMS, DMDS, and DMTS (in order of decreasing volatility) as attractants of carrion beetles (Coleoptera: Silphidae: Nicrophorinae) in a field experiment in an agricultural landscape in southern Bohemia, Czech Republic. We collected a total of 362 adult Nicrophorus vespillo (L.) that were attracted to 220 baited pitfall traps in a 3-day experiment. Sets of traps baited with DMTS were more successful in catching N. vespillo than sets baited with a blank. Traps containing DMDS had higher trapping success than traps containing DMS. In addition, trapping success strongly increased using DMTS in the presence of DMDS but not of DMS, suggesting a synergistic effect of DMDS and DMTS. We observed similar patterns between males and females in response to the infochemicals tested.     

Developmental stress increases reproductive success in male zebra finches

There is increasing evidence that exposure to stress during development can have sustained effects on animal phenotype and performance across life-history stages. For example, developmental stress has been shown to decrease the quality of sexually selected traits (e.g. bird song), and therefore is thought to decrease reproductive success. However, animals exposed to developmental stress may compensate for poor quality sexually selected traits by pursuing alternative reproductive tactics. Here, we examine the effects of developmental stress on adult male reproductive investment and success in the zebra finch (Taeniopygia guttata). We tested the hypothesis that males exposed to developmental stress sire fewer offspring through extra-pair copulations (EPCs), but invest more in parental care. To test this hypothesis, we fed nestlings corticosterone (CORT; the dominant avian stress hormone) during the nestling period and measured their adult reproductive success using common garden breeding experiments. We found that nestlings reared by CORT-fed fathers received more parental care compared with nestlings reared by control fathers. Consequently, males fed CORT during development reared nestlings in better condition compared with control males. Contrary to the prediction that developmental stress decreases male reproductive success, we found that CORT-fed males also sired more offspring and were less likely to rear non-genetic offspring compared with control males, and thus had greater overall reproductive success. These data are the first to demonstrate that developmental stress can have a positive effect on fitness via changes in reproductive success and provide support for an adaptive role of developmental stress in shaping animal phenotype.     

Alternative tactics and individual reproductive success in natural associations of the burying beetle, Nicrophorus vespilloides

Alternative reproductive tactics can be maintained through differentevolutionary avenues. They can be genetically or stochasticallydetermined, in which case they must yield equal fitness, ortheir use can be conditional, in which case the fitness payoffof alternatives may differ. We attempted to assess the reproductivesuccess of alternative reproductive tactics employed by wildmale and female burying beetles in natural associations on carcassesplaced in the field. A beetle's reproductive tactic was definedby its potential involvement in care of larvae, and parentagewas assessed using oligolocus DNA fingerprinting of offspringand potential parents. Both in males and in females, alternativetactics yielded significantly different reproductive benefits:subordinate females (brood parasites) and males (satellite males)had considerably lower reproductive success than dominant oruncontested individuals. Joint breeding was too infrequent forstatistical inferences, generating intermediate offspring numbers.About 15% of offspring were sired by males not present on thecarcass, suggesting that mating away from reproductive resourcescan produce reproductive benefits to males. Our results, inconcert with the observation that beetles using one tactic canbe manipulated into employing the alternative, support the notionthat Nicrophorus vespilloides uses alternatives conditionally,opportunistically employing lower-benefit tactics when moreprofitable tactics are not available, or as additional "on-the-side"tactics to bolster reproductive success.     

Sexual conflict over care: antagonistic effects of clutch desertion on reproductive success of male and female penduline tits

A fundamental tenet of sexual conflict theory is that one sex may increase its reproductive success (RS) even if this harms the other sex. Several studies supported this principle by showing that males benefit from reduced paternal care whereas females suffer from it. By investigating penduline tits Remiz pendulinus in nature, we show that parental conflict may be symmetric between sexes. In this small passerine a single female (or male) cares for the offspring, whereas about 30% of clutches are deserted by both parents. Deserting parents enhance their RS by obtaining multiple mates, and they reduce the RS of their mates due to increased nest failure. Unlike most other species, however, the antagonistic interests are symmetric in penduline tits, because both sexes enhance their own RS by deserting, whilst harming the RS of their mates. We argue that the strong antagonistic interests of sexes explain the high frequency of biparental desertion.     

Interaction between parental care and sibling competition: parents enhance offspring growth and exacerbate sibling competition

Species with elaborate parental care often also show intense sibling competition over resources provided by parents, suggesting joint evolution of these two traits. Despite this, the evolution of elaborate parental care and the evolution of intense sibling competition are often studied separately. Here, we examine the interaction between parental food provisioning and sibling competition for resources through the joint manipulation of the presence or absence of parents and brood size in a species with facultative parental care: the burying beetle Nicrophorus vespilloides. The effect of the interaction between the presence or absence of parents and brood size was strong; brood size had a strong effect on growth when parents provided care, but no effect when parents were absent. As in previous studies, offspring grew faster when parents were present than when parents were absent, and offspring grew faster in smaller broods than in larger broods. Our behavioral observations showed that brood size had a negative effect on both the amount of time parents spent providing resources to individual offspring and the offspring's effectiveness of begging, confirming that the level of sibling competition increased with brood size. Furthermore, offspring in larger broods shifted more from begging toward self-feeding as they grew older compared to offspring in small broods. Our study provides novel insights into the joint evolution of parental care and sibling competition, and the evolution of offspring begging signals. We discuss the implications of our results in light of recent theoretical work on the evolution of parental care, sibling competition, and offspring begging signals.     

Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae)

To investigate the function of maternal care and determinantsof reproductive success in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae), I used two different approaches,the measurement of phenotypic selection and female-removalexperiments under conditions differing in biotic-environmentalpressure. For two field populations, unattended eggs and youngernymphs consistently suffered severe predation pressure andattendance by parent females greatly enhanced their survival.In contrast, under enemy-excluded conditions, offspring performance was not reduced in broods without parent females, indicatingthat maternal care functions as a physical defense againstpredators. However, the determinant of female reproductivesuccess in E. putoni in the field was not the care behavioralone. Selection gradient analysis showed that early seasonoviposition and larger clutch size, as well as a longer durationof care by a female, was favored during the breeding episode.This study is the first to evaluate phenotypic selection onparental care and other reproductive traits in arthropods.     

A Review of Hypotheses of Decline of the Endangered American Burying Beetle (Silphidae: Nicrophorus americanus Olivier)

The largest species of North American Nicrophorus (Coleoptera: Silphidae), N. americanus, was placed on the US federal list of endangered species in 1989. This paper reviews literature bearing on eight hypotheses that attempt to explain the dramatic decline of this species over 90% of its former range. What is known regarding each hypothesis is separated from what remains to be investigated. We find that although progress has been made during the past 12 years, even the most well supported hypothesis requires a number of important studies to be completed or extended before we can confidently explain the decline of this species and predict the success of conservation efforts.     

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.     

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.     

State‐dependent cooperation in burying beetles: parents adjust their contribution towards care based on both their own and their partner's size

Handicapping experiments on species with biparental care show that a focal parent increases its contribution when its partner is handicapped. Such results are interpreted as evidence for negotiation, whereby each parent adjusts its amount of care to that of its partner. However, it is currently unclear whether the focal parent responds to a change in its handicapped partner's behaviour or state. To address this gap, we conducted an experiment on the burying beetle Nicrophorus vespilloides where we first generated different‐sized males and females by varying the duration of larval development. We then used a 2 × 2 factorial design in which a small or large male was paired with a small or large female. Small females provided less direct care (food provisioning and interactions with larvae) than large females, and both males and females provided less direct care when paired with a small partner. Thus, the focal parent adjusted its contribution towards care based on both its own state and that of its partner. There was also evidence for negotiation between the two parents as the focal parent adjusted its contribution based on the amount of care by its partner. However, there was no evidence that negotiation accounted for how the focal parent responded to its partner's size. Our results have important implications for our understanding of biparental cooperation as they show that each parent adjusts its contribution not only based on the amount of care provided by its partner but also based on its own state and its partner's state.