The reproductive behaviors of the burying beetles, Nicrophorus spp.
(Coleoptera: Silphidae): A literature review
The evolution of the burying beetles, Nicrophorus spp. (Coleoptera: Silphidae) has produced a series of relatively complex behaviors related to reproduction. Successful reproduction depends upon adults locating, defending, burying, and processing mammal carcasses of the size and condition that will support complete larval development. Both the female and the male adults that often work together exhibit these behaviors. In some situations, these behaviors are done by more than two adults, resulting in "facultative" communal breeding. Parental- larval interactions include sound production, initial direct feeding of the larvae, and sometime filial cannibalism. This paper will explore the research that as been done on these behaviors and where research might go in the future.
A dead mouse. A dead vole. One might think that small vertebrate carcasses would not be difficult to find. However, what if one were in competition with vertebrate scavengers, with carrion flies that can lay over hundreds of eggs, or with microbes? To find and retain a carcass relatively free of competitors might be compared to attempting to fend the latest toy to become a popular at Christmas. Much like the parent shopper, adult burying beetles (Silphidae: Nicrophorus spp.) must secure a limited resource in order to ensure the well being of their offspring. However, for the burying beetle, the stakes are much higher.
Burying beetle behaviors have been observed by scientists for many years, spawning lively debates (Bell 1873, Morley 1902, Selous 1911, Fabre 1919). However, it was in 1933 that Pukowski published the first detailed investigation on the Nicrophorus of Europe. The following year Leech made the first thorough studies of species in North America. The general public has been introduced to these beetles via the publications such as those of Milne and Milne (1976, 1980). During the mid twentieth century, relatively little research was done on the burying beetles.
An overview: summary of Pukowski, Leech, Milne and Milne
An adult burying beetle locates the carcass of a small vertebrate. The female and/or male buries the carcass and in the process removes all hair or feathers. The flesh is formed into a sphere (brood-ball) onto which the beetle secretes oral or anal liquid which may act a preservatives. Both parents must defend the brood-ball from competitors. The female then lays eggs in a corridor leading away from the underground crypt in which the brood-ball sits. The larvae feed on carrion directly regurgitated from a parent and well as on the brood-ball itself. Depending on the species, the male will stay until the larvae emerge or until the larvae leave the brood-ball to pupate in the soil around the crypt. The female stays until the larvae have left.
While this overview lists complex behaviors, burying beetle reproduction has been found to also include intense competition, "facultative" communalism, and filial cannibalism. The past twenty years have seen a renewed interest in the burying beetles. The purpose of this paper is to review the research that is being done on the burying beetles unusual reproductive behaviors. Many of the researchers in this area are concluding that the evolution of these behaviors is due to a limiting resource, the carcass. Therefore, this paper will be "carcass focused," reviewing what is known about competitive, sexual, and parental interactions.
Securing a carcass
For almost all species of Nicrophorus, a small vertebrate carcass is necessary for reproduction. When an adult encounters a carcass, it first evaluates it with its mouth parts and then immediately begins to bury it (Pukowski 1933). In most species, it doesnt matter whether the carcass was a poikilotherm or a homoioterm (Shubeck1976). If the carcass is on unsuitable ground it will be moved to a location where it can be buried (Pukowski 1933, Muths 1991). Fabre (1919) conjectured that the burying behavior permits the beetle to remove the carcass before the numbers of competitors attracted to the carcass become to large. The burying beetles must contend with both interspecific and intraspecific competitors.
Interspecific competitors include carrion flies and ants which can colonize a carcass quickly (Wilson 1983, Scott et al. 1987, Trumbo 1990a). The extent to which microbial competition is important has not been evaluated. Another interspecific competition exists completely within the genus Nicrophorus. Trumbo (1990b) studied a physically smaller speices N. defodieins and found that larger beetles of other species took over the carcasses of N. defodiens, killing any offspring and laying new eggs.
Intraspecific competition occurs when more than one conspecific female encounters a carcass they will fight for ownership (Pukowski 1933). The winner of the fight is usually the larger of the two beetles (Bartlett 1988). When more than one conspecific male encounters a carcass with no female present they do not fight. Instead, they will all work to bury the carcass until a female arrives, at which time they will fight for ownership of the carcass (Pukowski 1933, Bartlett 1988). Males will fight males; females will fight females. There is little courtship, rather the winning males mate with the winning female (Milne and Milne1976). However, the competition in not over. The winners must continually defend their carcass. After they bury the carcass, males and females appear to assist their mates in driving off intrasexual competitors (Scott 1990). The losers do not abandon the carcass immediately. Muller et al. (1990) found that female losers stayed to lay eggs of their own and in laboratory experiments found that in over half of the cases some of the losers larvae were cared for by the winner and survived to adulthood. Male losers also stay and mate with the winning female (Bartlett 1988, Robertson 1994).
Carcass as stimuli
Wilson and Knollenberg (1984) concluded that beetles with mature ovaries tend to favor mice carcasses while newly emerged adults with immature ovaries tend to feed at large carcasses. The final oocyte development only occurs after a small carcass is secured. Scott and Traniello (1987) found that the cue that triggers this development is the behavior of the female herself. Neither the behavior of the male nor the nutritional benefits of the carcass serve as cues. Trumbo et al. (1994), precisely measured the timing of the endocrine response to a carcass and found that juvenile hormone levels were significantly elevated in just 10 minutes of discovering a carcass. The behaviors observed during this short time period were palpating, lifting, walking around the carcass and making forays into the surrounding soil. They concluded that this surge in hormone is due to information obtained during behavioral assessment of the carcass.
A male burying beetle, upon arriving at a carcass where there is no female, will walk to a higher elevation near by and adopts a sterzeln position in which he circles the tip of his abdomen in the air intermittently for several hours (Pukowski 1933). It has been proven that the male is producing a female attracting pheromone (Bartlett 1987a, Eggert and Muller 1989). Males have also been found to sterelzn when there is no carcass, and will mate with females on very large carcasses, an adult feeding resource on which the female does not lay eggs (Muller and Eggert 1987).
A result of these copulations is that most females arriving at a small carcasses have stored sperm within their spermethecae (Muller and Eggert 1989). Since there does not appear to be any sperm precedence, males must compete with other male ejaculates for the fertilization of the females eggs (Muller and Eggert 1989). They can achieve high levels of paternity via repeated matings shortly before and during oviposition (Muller and Eggert 1989, Trumbo and Fiore 1991). In the species N. vespilloides studied by Muller and Eggert (1989), the pairs mated an average of seventy time in the first 24 h period.
After laying her eggs, the female guards the passage-way from the egg chamber to the crypt, perhaps keeping predators such as staphylinids from eating her offspring (Pukowski 1933). When the young hatch they crawl to the brood ball (Pukowski 1933 ) At this time the female begins to "chirp" via stridulating her elytra on her abdomen (Morley 1902, Pukowski 1933) The larvae crawl to up ontop of the brood-ball and gather where the female has opened up a depression. At this time the female directly feeds the larvae regurgitated flesh (Pukowski 1933). Pukowski (1933) reported that in some species the mother must feed her young after each molt, otherwise the young will die or if they do survive to pupate they never emerge as adults. However, Trumbo (1992) found some variation in species; N. orbicollis and N. sayi failed to survive to the second instar if the parents were removed but, N. defodiens and N. tomentosus developed normally.
Muller and Eggert (1990) determined that females response to larvae encounter was strongly time-dependent. Most females killed and ate larvae that could not have hatched from their own eggs. However, if all larvae appear within the right window of time the females would accept larvae even if not her own (Muller and Eggert 1990).
However, under certain circumstances, females will kill larvae that do arrive during the right time window. Wilson and Fudge (1984) found that some species of burying beetle could not adjust clutch size according to the carcass size and would lay more eggs that the carcass would support. Bartlett (1987a) found that females of N. vespilloides will intentionally kill some of their first instar offspring, an act called filial cannibalism. He concluded that this act occurred on carcass that were too small for all to develop and that the extra eggs were perhaps an insurance policy against high egg or first instar predation.
Male Vs Female brood care?
When a male and a female are found in a crypt together, the females tends to brood provision more than male, while the male tends to brood guard more than the female, though both do both jobs (Fetherston et al 1994) . Experiments have been done to assess the effects of offspring having both the female and male present versus having either the male or the female removed. In the laboratory, the survival rates and larvae weights for each of these treatments were very similar (Bartlett 1988, Scott and Traniello 1990, Fetherston et al 1994). Both single males and single females increased their brood provisioning time and spent less time guarding the crypt (Fetherston et al.1994). Pairs do not bury the carcass faster than single beetles or increase parental reproductive success (Wilson and Fudge 1984, Scott 1989). In the field, however, two parents dramatically reduce the probability that conspecifics will usurp the resource, replace either the male or the female, kill brood, and produce a replacement clutch (Scott 1990).
Carcass size, monogamy, and survival
Small carcasses Reproductive competition between females can be severe. On small carcasses, there may not be enough food to support the eggs she laid, resulting in filial cannibalism described above. If there is not enough food the resulting offspring are smaller, and small larvae become small adults (Bartlett and Ashworth 1988). Small larvae can divert reserves to make adult structures, but this leaves them dependent on finding resources quickly after they emerge (Bartlett and Ashworth 1988). Work by Bartlett (1988) suggests that small carcass size can reduce the amount of time the male parent stays with the offspring. He concluded that because the male maintains its body weight during its time in the crypt, that it is eating some of the brood-ball. In some cases, if the male does not leave after the eggs hatch the female will run him off or kill him (Bartlett 1988).
Large carcasses The "sterzeln" behavior of males describe earlier has also been described on carcasses on which a female is already present. When a carcass is large a male will attempt to attract more females to it, a behavior he will not display when the carcass is small (Bartlett and Ashworth 1988, Trumbo and Eggert 1994). It has been found that male reproductive success on large carcasses increases with polygyndry (Scott and Williams 1993, Trumbo and Eggert 1994, Eggert and Sakuluk 1995). However, for females the opposite may be true; the mean number of offspring per female is reduced (Trumbo and Fiore 1994, Trumbo and Eggert 1994, Scott and Williams 1993). Eggert and Sakuluk (1995) observed that females will physically interfere with male polygynous signaling by mounting, pushing, undercutting or pinching the male.
When a second female beetle approaches a female on a large carcass a fight still occurs, but in most cases both females will stay on the carcass to breed and care for the offspring (Eggert and Muller 1992). Unrelated adults, females in particular, provide care to broods of mixed parentage (Scott 1996). In addition, polyandrous and polygynandrous situations have been observed (Scott 1994).
One may question why, with reduced maternity, do females allow this communal situation. Females of most species cant lay enough eggs to exploit all the available resources in a large carcass (Bartlett 1988). In addition, Scott (1994) determined that on medium and large carcases pairs rearing broods on carcasses with fly oviposition had fewer young than pares on clean carcasses or foursomes on carcasses with fly ovipostion. The result seems to be that on larger carcasses "facultative" communal situations occur (Eggert and Muller 1992).
The title of Trumbos 1992 paper, "Monogamy to communal breeding: exploitation of a broad resource base by burying beetles," perhaps sums up these behaviors. He concludes that while large carcass can yield more and heavier young there are some costs. Larger carcasses are harder round into brood-balls, take longer to bury and thus are exposed to competitors longer, are more likely to be used by dipeterans, and are occupied by greater numbers of congeners. Cooperative breeding helps to overcome some of these obstacles. Smaller carcasses may yield fewer and lighter offspring, but they are more manageable and most of the offspring will be of the two adults (Trumbo 1992).
An interesting new twist
In one of Scotts recent papers (1996), she has uncovered another interesting twist in the burying beetle world. On large carcasses, the proportion of eggs attributed to two communal females was random and not skewed towards one female. However, on medium sized carcasses the number of eggs attributed to one female was less often random and more often skewed. Upon further investigation she discovered the following.
Females increase the proportion of their offspring in the brood by committing differential ovicide. Secondly, burying and preparing a carcass cooperatively stimulates ovarian development of the larger female and slow it for the smaller female, reducing or delaying ovipostion by the subordinate. Thirdly, larger females are more likely to be dominant and are more fecund than smaller females. (Scott 1996)
Scott concludes that the subordinate females submit to reduced numbers of offspring because they benefit by at least rearing a few offspring on a carcass which is a rare and unpredictable resource.
A limiting resource in reproduction has perhaps played a pivotal role in the evolution of some very rare animal behaviors. In this review, I have not commented on the significance of understanding the burying beetle. While better understood, there is much in the from evolution/ecology to behavior to physiology to molecular, about which much is to be learned. It appears obvious that this could be an interesting model system, for scientists in many branches of biology, not just entomologists, in part because it is quite different from that of other beetles and many arthropods (not to mention vertebrates). In many of the papers cited, most often the burying beetle reproductive behaviors are compared to those of birds. There has been hypothesizing. The next step is to test some of these hypotheses. The direction of research by Scott, Trumbo, Eggert and Muller appears a continuation of exploring communal breeding dynamics.
I started this review with a silly Christmas shopping metaphor. Let me end with a wish-list for burying beetle research directions: ethograms of behavior (with an eye to behavior loops and probabilities), modeling of behavior in terms of resource availability, a look at the beetles nervous system, an investigation into whether there are any bacterial or fungal interactions, and a comparison of the genera as a whole versus individual species.
Bartlett, J. 1987a. Evidence for a sex attractant in burying beetles. Ecol. Entomol. 12:471-472.
Bartlett, J. 1987b. Filial cannibalism in burying beetles. Behav. Ecol. Sociobiol. 21: 179-183.
Bartlett, J. 1988. Male mating success and paternal care in Nicrophorus vespilloides (Coleoptera: Silphidae). Behav. Ecol. Sociobiol. 23: 297-303.
Bartlett, J. and Ashworth, C. M. 1988. Brood size and fitness in Nicrophorus vespilloides (Coleoptera: Silphidae). Behav. Ecol. Sociobiol. 22: 429-434.
Bell, Prof. 1873. A glimpse of insect life. Can. Ent. 5: 94-95.
Eggert, A-K. and Muller J.K. 1989. Pheromone-mediated attraction in burying beetles. Ecol. Entomol. 14: 2355-237.
Eggert, A-K. and Muller J.K. 1992. Joint breeding in female burying beetles. Behav. Ecol. Sociobiol. 31: 237-242.
Eggert, A. K. and Sakaluk. 1995. Female-coerced monogamy in burying beetles. Behav. Ecol. Sociobiol. 37: 147-153.
Fabre, J. H. 1919. The Glow-worm and Other Beetles. Hodder & Stoughton, London.
Fetherston, I. A., Scott, M. P., and Traniello, J. F. 1994. Behavioral compensation for mate loss in the burying beetle Nicrophorus orbicollis. 47: 777-785.
Leech, H. B. 1934. The Family History of Nicrophorus conversator Walker. Proc B. C. Ento Soc.
Milne, L. J. and Milne, M. 1976. The social behavior of the burying beetles. Scientific American. 235:84-89.
Milne, L. J. and Milne, M. 1980. Insect Worlds. Charles Scribners Sons, New York.
Morley, R. L. 1902. Notes on stridulation. Entomol. Mo. Mag. 38: 249-250.
Muller, J. K. and Eggert, A-K, 1989. Paternity assurance by "helpful" males: adaptation to sperm competition in burying beetles. Behav. Ecol. Sociobiol. 24: 245-249.
Muller, J. K. and Eggert, A-K. 1990. Time-dependent shifts between infanticidal and parental behavior in female burying beetles: a mechanism of indirect mother-offspring recognition. Behav. Ecol. Sociobiol. 27: 11-16.
Muller, J. K., Eggert, A-K. and Dressel, J. 1990. Intraspecific brood parasitism in the burying beetle, Necrophorus vespilloides (Coleoptera: Silphidae). Anim. Behav. 40:491-499.
Pukowski, E. 1933. Okologische Untersuchungen and Necrophorus. F. Z. Morph Okol Tiere. 27: 518-596.
Robertson, I. C. 1994. Extra-pair copulations in burying beetles (Coleoptera: Silphidae). J. Kansas Entomol. Soc. 67(4): 418-420.
Scott, M. P. 1990. Brood guarding and the evolution of male parental care in burying beetles. Behav. Ecol. Sociobiol. 26: 31-39.
Scott, M. P. 1994. Competition with flies promotes communal breeding in the burying beetle, Nicrophorus tomentosus. Behav. Ecol. Sociobiol. 34:367-373.
Scott, M. P. and Traniello, J. F. A. 1987. Behavioral cues trigger ovarian developmetn int he burying beetel Nicrophorus tomentosus. J. Insect Physiol. 33 (10): 693-696.
Scott, M. P. and Traniello, J. F. A. 1990. Behavioral and ecological correlates of male and female parental care and reproductive success in the burying beetles (Nicrophorus spp.). Anim. Behav. 39:247-283.
Scott, M. P. and Williams, S. M. 1993. Comparative reproductive success of communally breeding burying beetles as assessed by PCR with randomly amplified polymorphic DNA. Proc. Nat. Acad. Sci. 90: 2242-2245.
Selous, C. F. 1911. A preliminary note on the so-called carrion-feeding Coleoptera. Entomol. Mo. Mag. 47: 36-38.
Shubeck, P.P. 1976. Carrion beetle responses to poikilotherm and homoiotherm carrion (Coleoptera: Silphidae). Entomol. News. 87: 265-269.
Trumbo, S. T. 1990a. Reproductive success, phenology, and biogeography of burying beetles (Silphidae, Nicrophorus). Am. Midl. Nat. 124: 1-11.
Trumbo, S. T. 1990b. Interference competition amoung burying beetles (Silphidae, Nicrophorus). Ecol. Entomol. 15:347-355.
Trumbo, S. T. 1992. Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus). Ecol, Entomol. 14: 289-298.
Trumbo, S. T., Borst, D. W., and Robinson, G. E. 1994. Rapid elevation of juvenile hormone titer during behavioral assessment of the breeding resource by the burying beetle, Nicrophorus orbicollis. J. Insect Physiol. 41(6): 535-543.
Trumbo, S. T. and Eggert, A-K. 1994. Beyond monogamy: territory quality influences sexual advertisement in male burying beetles. Anim. Behav. 48: 1043-1047.
Trumbo, S. T. and Fiore, A. J. 1991. A genetic marker foe investigating paternity and maternity in the burying beetle Nicrophorus orbicollis (Coleoptera: Silphidae). J. New York Entomol. Soc. 99(4): 637-642.
Trumbo, S. T. and Fiore, A. J. 1994. Interspecific competition and the evolution of communal breeding in burying beetles. Am. Midl. Nat. 131:169-174.
Wilson, D. S. 1983. The effect of population structure on the evolution of mutualism: a field test involving burying beetles and their phoretic mites. Amer. Nat. 121(6): 851-870.
Wilson. D. S. and Fudge, J. 1984. Burying beetles: intraspecific interactions and reproductive success in the field. Ecol. Entomol. 9: 195-203.
Wilson, D. S. and Knollenberg, W. G. 1984. Food discrimination and ovarian development in burying beetles (Coleoptera: Silphidae: Nicrophorus). Ann. Entomol. Soc. Am. 77: 165-170.
Readings on other Nicrophorus behaviors:
Shubeck or Abbott (finding carcasses)
Wilson (phoretic mites) Brown, J. M. and Wilson, D. S. 1994. Poecilocheirus carabi: Behavioral Life History. Mites: Ecological and Evolutionary Analyses of Life-History Patterns. Ed. Houck, M. A. Chapman and Hall, New York.
Thanks to Ilka Gilmer for translating Pukowski to me in exchange for fermented agave.