Abstract

Beetles in the family Silphidae are fairly complex in their reproductive and subsequent brood rearing behaviors. Generally they choose a carcass, attract a mate and, after burying it lay their eggs in the carcass, co-parenting during the early stages. A number of behavioral factors appear to affect their ultimate reproductive success. Males use two tactics in seeking a mate and significant differences occur between males in the amount of time spent using one versus the other. Carcass selection by adults appears to be another of the initial choices that plays into their success or failure. Interactions on a variety of levels appear to play significant roles as well. These include interactions with their associated mites and predators as well as with other members of the Silphidae family. The length of time a male chooses to stay in the crypt appears to vary greatly, at least in one species. This can have an effect on the success of the brood as the female may be left to defend intruders alone. Differences between species, as well as those within species, are explored. Possible environmental and genetic reasons for these differences are also examined.
 

Introduction

Beetles in the genus Nicrophorus (Family Silphidae Order: Coleoptera) are unique in that, although they are not true social insects, they engage in a number of behaviors that are social in nature including a high investment in their offspring. This group has been studied extensively due to this unique trait and a number of factors appear to have an effect on the eventual success or failure of each brood. These beetles make use of small vertebrate carcasses, burying them in the soil, laying eggs nearby and then rearing their young on the carcass. Mate finding tactics, carcass and substrate selection, encounters with con specifics as well as with predators, competitors, and phoretic mites and nematodes, all seem to play a role in their complex interactions. In addition to direct effects on the young, beetles seem to vary their parenting techniques according to cues from these outside influences. Studies reviewed in this paper deal primarily with the genus Nicrophorus and cover these potential influences on the beetle’s interactions and care of the brood. The potential tradeoffs for use of different tactics and approaches are presented where they have been considered. Ultimately these choices and their consequences determine the ability of an individual beetle to pass on its genetic material to the next generation.

Mate-finding Tactics

Both male and females search for suitable carcasses using odor cues emanating from the carcass itself. It was long thought that this was the only way in which the two sexes could meet. However, it has since been discovered that males also emit a pheromone to attract potential females both with and without a carcass present. A female who finds a carcass has the option of either waiting for a male to arrive or using sperm stored in her spermatheca in order to make use of the carcass. (Eggert 1992) In doing so she faces the prospect of rearing the young on her own without the help of a male to defend the nest. Males can also find a carcass and wait for a conspecific female to arrive but, unless one does, he can not make use of this valuable resource. In this case males use a pheromone as an extra attractant when they have found a suitable carcass and a female has not shown up within a certain amount of time. Carcasses are a limiting factor and therefore it benefits a male to have an additional way of locating a female. Males have also been observed to make use of the pheromone when no oviposition site has been found in the hopes of attracting a female and mating at least once before she leaves. In this case his overall reproductive success is determined by how many females he can mate with in a given amount of time and their chances of success after leaving. Females have been observed uniparenting successfully therefore validating the benefits for a male who is able to mate even without a carcass present. There are apparent reproductive benefits for a female in this scenario as well. Females responding to long distance male pheromone signaling is an unusual scenario in the insect world. However, due to the intense competition among females for resources in this situation, it would presumably benefit her to respond to all males even on the chance that he does not have a carcass available. In addition, multiple matings increase her chances of having viable sperm in her spermatheca, if and when she does come across a carcass and is unable to find a male at that time. (Eggert 1992).

Time of day seems to play a significant role in determining which method, or combination thereof, is utilized by a male. Early in the day males are primarily moving about in search of a carcass but by the end of the day the majority of the males in one study had assumed the characteristic pheromone emitting position, hind end in the air. During the last few hours of the normal active period males appeared to be using some combination with individuals varying in the amount of time used in each type of tactic and the time at which they switched methods. A study in heredity was able to show that these variations in use of the different techniques may be due at least in part to genetic differences. (Egget 1992) Presumably, both methods and their various combinations are still present in the behavioral gene pool due to the fact that they offer benefits depending upon the situation and time of day. Females are more active later in the day and therefore more likely to be moving about and responding to pheromone emission. In addition, the availability of carcasses has been observed to decrease over the day as they are discovered and utilized by other Nicrophorus beetles. Fewer females may be available later in the day as well as they find carcasses and mates. Flight and physical searching are generally thought of as a more costly activity metabolically than pheromone production. Therefore it becomes more energy efficient for a male to use pheromone emission at certain times and not spend precious resources searching for females and carcasses that are farther and fewer between. (Eggert 1992). Ideally, males and females are able to make contact on a carcass, mate, bury and defend this resource and their young together. However, it is apparent that both have adapted to less than ideal situations with alternative methods, ensuring the potential of a chance at reproductive success.
 

Carcass Selection and Interspecies Competition

At least one species Nicrohorus investigator has been shown to select carcasses based on size. A minimum size has been correlated with important consequences for the fitness of the brood. Average brood size was larger for larger carcasses and even when smaller ones were buried larvae were not successfully reared on them. Carcasses above a certain weight were rejected as well, although groups of adults did utilize them as a food source for themselves. (Smith et al 1995) In this case rejection may be due to an inability to move the carcass easily to an ideal burial site, or to do so quickly enough to reduce competition with others. The acceptable size range appears to vary among species in the genus Nicrophorus. How the beetles are able to gage the size of a carcass is not known for certain. Observations of pre-burial behavior may offer some insight and possibilities for the mechanism. Adults crawl under the carcass and, laying on their backs, lift the carcass with their hind legs, possibly estimating the weight and thereby it’s potential for successful brood rearing. Brood mass has been shown to correlate to eventual adult size and therefore potentially the ability to successfully compete for resources as vicious fights are known to occur over carcasses with the larger beetle generally winning.

In addition to size of a carcass, location in the landscape appears to play a role in the final acceptance or rejection of it as an oviposition site. N. investigator was observed to reject carcasses, even those within the acceptable size range based on location. This high elevation, day-active species preferred sunny open meadow habitats to shadier forested habitats. Experiments conducted by Smith et al in 1995 showed that larvae in shady habitats had a slower growth rate then those in sunny locations. While this may not have a long-term effect on the larvae, slower development means more time on the part of the parents is required to rear the brood in a shady location. In the long run, this means more investment in one brood and decreased opportunities for subsequent matings. Lower elevation, nocturnal species do not show these same preferences for sunny locations and this may be due to the fact that the season is longer and daytime temperatures are warmer (Smith et al 1995).

When a number of species coexist in a given area a variety of interactions are observed. In a study conducted in two locations in Michigan, Wilson et al observed four species of Nicrophorus in 1984. Season and temperature seemed to play primary roles in allowing multiple Nicrophorus species to share the same habitat. Of the species observed one, N. sayi, is a spring breeder and N. tomentosus is an autumn breeder and therefore they rarely compete with each other or the other two mid summer breeders also present in the habitat. N. orbicollis and N. defendien are actively breeding during the same time of year and competition and temperature and relative size of the species apparently affected success. Two other species were also collected in the area but did not appear to interact or compete at all for similar resources and so were not considered in the final evaluation. Monitoring of daily activity and flight patterns showed significant differences between three of the four species. However, the authors are careful to point out that non-overlapping flight patterns do not necessarily mean that there is no competition for desirable carcasses. A period of time is required in order for a beetle to drag the carcass to a desirable site and accomplish complete burial, during which time it is susceptible to takeover from the other species. Observations in the field were made on which, and how many species were found on mouse carcasses placed in various locations. In this study two or more species were found in the area of a carcass 18% of the time, validating the assumption that competition between species is occurring despite differing habits. Size seemed to often be the determining factor in these cases with the larger of the beetles present maintaining a dominant position on the carcass and the smaller ones being observed a short distance away. In the specific interactions between the N.orbicollis and N. defodiens, the species with overlapping breeding seasons, the larger of the two, N.orbicollis, was able to lay claim to desirable mice most of the time. This was in spite of the fact that N.defodiens searches earlier in the day and may be the initial discoverer of a carcass. Even after burial and egg-laying N.defodiens was observed to lose possession of a carcass in competition with other species. This was especially prevalent during the midsummer season at the peak of their activity.

In light of these observations, the authors wondered how this smaller and less competitive species was able to exist at all in the same habitat with the larger and more effective N.orbicollis. After discarding the possibility that the bimodal distribution represented separate generations or single individuals who remain underground for the mid summer period, a third possible explanation was examined. Warmer nights seemed to allow N.orbicollis to aquire the majority of the carcasses and as colder nights are more prevalent during the early and late summer, this might account for the bimodal distribution of N.defodiens if it possessed a lower temperature tolerance. Over the two-year study, differences between the two seasons in terms of temperatures and subsequent distributions between these two species seem to support this hypothesis. Although both benefit from higher temperatures in their searching ability, N. orbicollis can outcompete the smaller beetle, thereby negating the benefits of the higher temperature for N. defodiens. This causes it to have a bimodal seasonal distribution as it is forced into niches with specific night temperature ranges, which it appears to tolerate better. With this kind of specific interspecies competition going on the authors suggest that other areas where numerous species occur, present their own interesting scenarios of adaptation to conditions and competition in order to coexist. Slight differences in temperature due to geographic differences could easily sway the balance in favor of different species according to individual life cycles, and tolerances as it affects ability to compete for resources. Nicrophorus pustulatus, is a species found with other burying beetles but does not compete for the small vertebrate carcasses that the four species included in the previous study do. In an attempt to understand what their potential competitive role may be, studies in both the lab and field were conducted to determine why they do not make use of these same resources. Results in the lab indicate that N. pustulatus are able to reproduce on smaller carcasses. However evidence also suggests that they are more adapted for use of the larger carcasses and produced larger broods without a reduction in size for individual larvae. This species is more rare in the field but seems to have adapted to a specific niche in terms of carcass size in order to avoid competition. (Robertson 1992). Other studies have indicated that resource partitioning and varying habitat utilization amongst Nicrophorus species does occur. Each seems to adjust to the presence of others and create specialized niches that improve chances of survival and reduce competition. (Beninger and Peck 1992)
 

Substrate Discrimination

Once a carcass has been found, the beetle may use nearby rodent burrows to hide it, bury it directly where they found it, or drag it to another location for preparation and burial. It has been suggested that soil factors may affect speed of concealment due to ease of excavation. In the study previously mentioned, (Smith et al 1995), beetles showed a preference for certain habitats for burial site, but actual soil types were not included in the analysis. Soil structure, humidity, and other properties may affect the stability of the chamber and eventual success and ability to rear a brood within it. In a laboratory study conducted at Kansas State University by Erin Muths, beetles where provided with a choice of substrates in which to bury a carcass. The three substrates were presented in one container separated by plywood that was flush with the soil surface. Field soil untreated, a 2:1, and a 5:1 mixture of soil: added bulk, were the choices presented to the beetles. Both pairs of beetles, and individual females, were observed. In both trials beetles preferred soil with added bulk over that without, indicating that they may be using soil bulk to discriminate, at least in part, in order to determine location of burial.
 

Nest Behaviors and Duration of Parental Care

Once a suitable carcass has been secured, it is stripped of fur, rolled into a ball, and buried. Discovery and preparation of the carcass causes rapid hormonal changes in the female that trigger egg maturation. (Scott 1996). Eggs are laid in the soil nearby and after hatching larvae are tended for approximately twelve days by the parents. (Ratcliffe 1996) Parents leave the chamber, with the male usually leaving prior to the female, sometimes substantially earlier. Investment in the care of the young has benefits as well as costs. In the case of the burying beetles, a male who stays longer and helps defend the nest from intrusions ensures success of that particular set of offspring. In doing so, however, he potentially forfeits the opportunity for other matings and subsequent broods. A balance between these two would seem to be ideal.

In a series of experiments conducted at the Queen’s University Biological Station in eastern Ontario, variations in parental care and the result of these variations were examined. In some cases intruders move in in the middle of brood development, destroy the clutch and mate with the remaining beetle and initiate their own clutch. These studies examined whether or not duration of male care decreased as the possibility of a takeover decreased, and whether the occurrence of takeovers changed over the course of brood development. Results from field trails on numbers of takeovers indicate that many nests are intruded upon. There is a rapid decrease in the number of takeovers after a period of five days. It is speculated that this may be due in part to changes in the carcass due to degradation, and so changes in the chemical cues emitting from it. Potential intruders may be less able to detect the carcass or realize it has a reduced value as a potential source for brood rearing. At this point it may not be worth the risks incurred by entering into battle with the resident beetles. A third influence may be that, over the course of the study, those susceptible to takeover have already been invaded within the first five days, leaving only those pairs who are fit enough to fight off intruders.

Past studies have established that nests defended by single females, especially those in areas of high competition, are most susceptible to takeover. ( Trumbo 1991 as quoted in Robertson 1993) Results from this particular study did not seem to indicate that occurrence or lack of these intrusions influenced the duration of male care. In fact there was a great deal of variation in when a male left despite the fact that is well established that broods benefit with biparental care. Why this variation occurs is not exactly known. One suggestion by the author of this study is that condition of the carcass may play a role here as well. A male may be more inclined to leave as the value of the carcass to intruders decreases. He may also stay if it holds potential value as a substrate and attractant for subsequent matings with intruding females. Extra-pair copulations in certain species, but not in others, have been show to occur when a conspecific female intrudes a nest. Although both males and females can intrude, the overall cost to the resident pair is higher when a male intrudes. He will destroy the present brood and expel the residents. A female may intrude, threaten to destroy the present brood, but provide the male with extra mating opportunities that might be worth the risk to his current brood (Robertson et al 1994). The final possibility suggested is that the cost in overall fitness for the male is low in terms of duration of his care for an individual brood. (Robertson 1993)
 

Communal Breeding and Reproductive Cooperation

Having established that resources are scarce, valuable and hotly competed for, it makes sense that in some situations, reproductive cooperation may be worth the tradeoffs involved. In the case of Nicrophrus tomentosus, a medium-sized beetle, cooperation as been observed. This allows them to make use of larger carcasses that a single pair may not be able to handle alone. The size of the carcass appears to be the determining factor as no species has been observed to breed communally on a small carcass. This would be an obvious factor due the fact that a carcass can only support a limited number of larvae to full maturity. In the case of a larger carcass, both females gain in communal use. One would be unable to utilize the entire resource and she gains the assistance of the other in preparation and burial of it. In an evaluation of paternity in communal resource use it was discovered that maternity varied. However the larger of both the males and females present invariable produced the majority of the offspring and invested the most time in brood care, staying the longest. Size is important but other factors may be involved including rate of egg maturation after carcass discovery. A subordinate female may be able to produce some offspring of her own and she will remain and assist as long as the possibility that some of her offspring will survive exists. The dominant female can either drive off the other or limit their share of the resources as much as possible. The larger the carcass the less she has to lose and the benefits may outweigh the costs. Added help in defense from intrusions by other beetles did not appear to be a factor in determining communal use of resources. (Scott 1997) It appears that one of the primary benefits to this species is additional help in removing the eggs of flies. This particular species is active during the day when flies are also out in greater number. A carcass being infested with flies reduces the number of young a pair is able to rear on it. Therefore, an increase in assistance from other adults in their removal is a definite benefit to all. As the author points out this is a very fine balance and cooperation does not occur except when the situation is just right. (Scott 1997).
 

Role of Phoretic Associates

The Necrophorus beetles are know to support a number of mite species that are phoretic in their association. In a study conducted on Japan, 23 out of 33 beetle species examined had mites associated with them (Takaku et al 1994) In the case of the burying beetles it is a cyclical phoresy, indicating a high level of specificity, in which the mites inhabit the nests of their host and rely on them for dispersal (Athias-Binche et al 1993). Males and female adults carry the mites down into the burial chamber with them where they reproduce and the majority of the dueteronymphs then ride out of the crypt on the male. Behavioral cues seem to determine which beetle they congregate on (Schwarz et al 1992). Local specialization of specific species of mites to certain species of beetle hosts has been demonstrated (Brown et al 1992).

The benefits to the mite are obvious. They feed on the carcass, fly eggs, and in some cases, eggs of the beetle that carry it. They also benefit in dispersal. The benefits to the beetle may be less apparent initially and some costs are involved. In the presence of flies, reproduction of the beetle was shown to be dependent on the presence of certain mites, especially when repeated infestation by flies was a problem. Wilson and Knollenberg (1987 as quoted in Beninger et al 1993) observed a long-term beneficial effect for the beetle community in the presence of mites. This could possible be attributed to the fact that they decrease brood size and increase larval weight. The mites also reduce colonization of the carcass by soil microbes. It is unclear as to whether or not the increase in individual larval size is a true advantage over large brood size. However, larger individuals are more successful in competitive situations and therefore may have a long-term competitive edge. The author also makes the point that less individuals produced means less competition for available resources and therefore increases the overall chances for each individual (Beniger et al 1993).
 

Summary

Burying beetles have long fascinated scientists due to their semi-social behaviors, a phenomenon that is not known to occur in other groups in the order Coleoptera. Countless studies indicate that the beetles incorporate a complex series of cues and interactive behaviors in completing their lifecycle. All appear to be, not surprisingly, based on the ultimate benefits and tradeoffs for their long-term reproductive success. Males and females cooperate in the rearing of the brood but behaviors are modified along the way according to each individual’s drive to pass on their own genetic material. Climate, habitat, and presence or absence of other species and resources are all potential modifiers of behavior in the different species in the genus Nicrophorus.

References

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