Josef K. Müller

Joint breeding in female burying beetles

SummaryBurying beetles (Nicrophorus) exhibit advanced parental care, by feeding and guarding their offspring on buried vertebrate carrion. Till now, interactions between two conspecific females on a carcass have been thought to be mostly competitive, and parental care was thought to be provided by single females or male-female pairs exclusively. Here we demonstrate that cooperative brood care occurs in this species, and that its incidence is contingent on carcass size. Small carcasses are usually monopolized by one female; typically the larger of two female combatants secures the carcass for her offspring (Figs. 1 and 2). On large carcasses fights still occur, but in most cases both females stay on the carcass long enough to provide care for the brood. The use of genetic markers revealed that the maternity of offspring is shared evenly among joint breeders (Figs. 3, 4). We hypothesize that cooperative breeding is an adaptive response to a situation that arises partly as a consequence of a physical constraint.

The Coolidge effect, individual recognition and selection for distinctive cuticular signatures in a burying beetle

The ability to recognize individuals is an important aspect of social interactions, but it can also be useful to avoid repeated matings with the same individual. The Coolidge effect is the progressive decline in a males propensity to mate with the same female combined with a heightened sexual interest in new females. Although males that recognize previous partners and show a preference for novel females should have a selective advantage as they can distribute sperm evenly among the females they encounter, there are few invertebrate examples of the Coolidge effect. Here we present evidence for this effect in the burying beetle Nicrophorus vespilloides and examine the mechanism underlying the discrimination between familiar and novel mates. Burying beetles feed and reproduce on vertebrate carcasses, where they regularly encounter conspecifics. Males showed greater sexual interest in novel females (virgin or mated) than in females they had inseminated before. The application of identical cuticular extracts allowed us to experimentally create females with similar odours, and male responses to such females demonstrated that they use female cuticular patterns for discrimination. The chemical analysis of the cuticular profile revealed greater inter-individual variation in female than in male cuticular patterns, which might be due to greater selection on females to signal their individual identity.

Carcass maintenance and biparental brood care in burying beetles: are males redundant?

1. Burying beetles inter small vertebrate carcasses that ultimately serve as a food source for their developing young. The male remains with the female on the carcass after the brood has been produced, purportedly to aid in the feeding and protection of larvae. However, numerous laboratory experiments have failed to demonstrate a beneficial effect of the male on the growth and survival of offspring.

Pheromone‐mediated attraction in burying beetles

In a recent paper Bartlett (1987) tried to obtain some evidence for a sex attractant in burying beetles. In laboratory and field experiments he found that male and female burying beetles are significantly more likely to go to a container with a mouse buried by a Necrophorus male than to one with a hand-buried mouse. From his experiments he deduced that males attract other beetles to the corpse. But it is not unlikely that hand-buried mice are less attractive for Necrophorus than mice buried by beetles. In a field study carried out by Wilson et al. (1984) mice buried by a pair of Necrophorus were frequently (more than 50%) taken over by other Necrophorrrr individuals the day after burial. These mice must have been attractive for Necrophorus though there was no luring male. So Bartlett’s experiments may be influenced by the odour of the carcass buried by the males. Pukowski (1933) was the first to report a conspicuous behaviour of Necrophorus males that have found a carcass on which no female is present. These males take a typical posture: the extended abdomen is pointing up, the head touching the ground, and from time to time the tip of the abdomen is moved slightly up and down in such a way that the intersegmental membranes can be seen. The term ‘sterzeln’ she used for this kind of behaviour is derived from apidology where it describes a similar posture taken by honey bee workers during the release of pheromones attractive to other workers.

Ethyl 4-Methyl Heptanoate: A Male-Produced Pheromone of Nicrophorus vespilloides

Sexually mature male beetles of the genus Nicrophorus (Coleoptera: Silphidae) exhibit a conspicuous behavior, recognized as pheromone-releasing activity. Laboratory and field studies demonstrated that females are attracted to males that exhibit this behavior, both on or off reproductive resources. Here, we report the results of a study in which volatile chemicals released by calling Nicrophorus vespilloides were collected by solid-phase microextraction and analyzed by using coupled gas chromatography–mass spectrometry. These analyses revealed that ethyl 4-methyl heptanoate and (E)-geranylacetone are emitted by males that engage in the behavior. In the field, traps baited with racemic ethyl 4-methyl heptanoate caught roughly equal numbers of male and female N. vespilloides. Some male and female Nicrophorus vespillo and male Nicrophorus humator were also caught in traps baited with this compound. Traps baited with (E)-geranylacetone did not catch significant numbers of beetles.

Correlated changes in breeding status and polyunsaturated cuticular hydrocarbons: the chemical basis of nestmate recognition in the burying beetle Nicrophorus vespilloides?

Nestmate recognition in eusocial insects has received a lot of attention in the last decades. Recognition in subsocial species, in contrast, has been ignored almost completely and consequently, and little is known about proximate mechanisms of recognition in subsocial systems. We studied one subsocial species, the biparental brood caring burying beetle Nicrophorus vespilloides, an interesting model organism for studies of recognition because of its ability to discriminate between breeding partners and conspecific competitors. Recognition appears to be based on a chemical cue closely linked to the breeding status of individuals. Breeding and non-breeding beetles consistently differ in their relative proportions of polyunsaturated cuticular hydrocarbons. To investigate the function of these polyenes in the burying beetles’ recognition system, we quantified their concentration on the cuticle during the early state of a breeding attempt and tested the response of breeding beetles in corresponding behavioural experiments. We observed a rapid increase in the proportion of polyunsaturated hydrocarbons of both males and females after they were provided with a carcass suitable for reproduction. Furthermore, we found that the relative amount of polyenes on an individual’s surface was closely correlated with its chance of being accepted as breeding partner. Our results support the idea that polyunsaturated hydrocarbons are involved in breeding partner recognition in N. vespilloides, functioning as a signal that conveys information about the individual’s breeding status. Breeding females have greater amount of polyenes than breeding males, and females ingest more carrion during the first days on the carcass, which supports our hypothesis that precursors for the respective polyenes are derived from ingested carrion.

(E)-Methylgeranate, a chemical signal of juvenile hormone titre and its role in the partner recognition system of burying beetles

In recent years, studies have shown that animals can communicate their physiological state or condition by means of chemical signals. However, as the chemicals involved in the condition-dependent signals have rarely been identified, evolutionary mechanisms that ensure their reliability are not well understood. We identified a volatile chemical signal that may serve as a reliable indicator of hormonal state in burying beetles, and is involved in their partner recognition system. Burying beetles reproducing on carcasses are able to distinguish between their breeding partners and infanticidal conspecifics. This discrimination depends on breeding status, which is positively linked to juvenile hormone III (JH III) titre. Breeding Nicrophorus vespilloides beetles, in contrast to nonbreeding ones, emitted considerable amounts of (E)-methylgeranate. The amount of emitted (E)-methylgeranate was positively correlated with juvenile hormone titres known from other burying beetle studies. Moreover, our behavioural experiments showed that dummies treated with methylgeranate induced tolerant behaviour, whereas control dummies were treated aggressively. The fact that (E)-methylgeranate and JH III share a conspicuous structural similarity and the same biosynthetic pathway may explain how the reliability of the signal for JH titre is ensured. We discuss the implications of our results in the light of theoretical work on the evolution of chemical communication, particularly on the origin of chemical signals.

‘True’ and ‘untrue’ individual recognition: suggestion of a less restrictive definition

We welcome the recent review of Tibbetts and Dale [1] on individual recognition (IR). In particular, we are pleased about their emphasis on the oft-neglected idea that selection for traits that reveal individual identity might have an important impact on the evolution and maintenance of phenotypic diversity.

Risk of Sperm Competition Mediates Copulation Duration, but not Paternity, of Male Burying Beetles

Males should increase their investment in ejaculates whenever they are faced with an increased risk of sperm competition. Burying beetles (Nicrophorus vespilloides), insects that breed on small vertebrate carcasses, offer an ideal model with which to examine sperm allocation tactics because females typically mate with many males prior to laying eggs. Males compete directly for control of carcasses, and males losing such contests often become satellites, lurking in the vicinity of the carcass and attempting surreptitious copulations with the resident female. We predicted that both the dominant resident male and the satellite male would increase their sperm allocation in the presence of the other, but that relative to dominant males, satellite males would allocate a greater number of sperm per ejaculate. We employed a repeated-measures design in which two full-sib rival males, differing only in their dominance status, were each mated a single time to a previously-inseminated female under two conditions, once in the absence of their rival and once in the presence of their rival. Satellite males exhibited longer copulation durations than dominant resident males when both males were present on a carcass. Copulation durations of dominant males did not differ in the presence or absence of satellite males. Contrary to expectation, the increased copulation durations of satellite males did not result in a greater share of paternity relative to dominant males. The absence of any discernible effect of increased copulation durations on paternity in satellite males could be due to post-copulatory preferences of females or, alternatively, satellite males may require longer durations of copulation to transfer the same amount of sperm as dominant males.

Too Fresh Is Unattractive! The Attraction of Newly Emerged Nicrophorus vespilloides Females to Odour Bouquets of Large Cadavers at Various Stages of Decomposition

The necrophagous burying beetle Nicrophorus vespilloides reproduces on small carcasses that are buried underground to serve as food for their offspring. Cadavers that are too large to bury have previously been postulated to be important food sources for newly emerged beetles; however, the attractiveness of distinct successive stages of decomposition were not further specified. Therefore, we investigated the potential preference of newly emerged N. vespilloides females for odour bouquets of piglet cadavers at specific stages of decomposition. Analyses of walking tracks on a Kramer sphere revealed a significantly higher mean walking speed and, consequently, a higher mean total track length when beetles were confronted with odour plumes of the decomposition stages ‘post-bloating’, ‘advanced decay’ or ‘dry remains’ in comparison with the solvent control. Such a change of the walking speed of newly emerged N. vespilloides females indicates a higher motivation to locate such food sources. In contrast to less discriminating individuals this behaviour provides the advantage of not wasting time at unsuitable food sources. Furthermore, in the advanced decay stage, we registered a significantly higher preference of beetles for upwind directions to its specific odour plume when compared with the solvent control. Such a change to upwind walking behaviour increases the likelihood that a large cadaver will be quickly located. Our findings are of general importance for applied forensic entomology: newly emerged N. vespilloides females on large cadavers can and should be regarded as potential indicators of prolonged post mortem intervals as our results clearly show that they prefer emitted odour bouquets of later decomposition stages.