Brood discrimination, nest mate discrimination, and determinants of social behavior in facultatively quasisocial beetles (Nicrophorus spp.)

In this study we investigated ecological determinants of socialityin burying beetles (Nicrophorus spp.), potential conflicts ofinterest among reproductive females, and the effects of nestingfailure and costs of fighting on cooperation. Burying beetlesare known to form monogamous pairs when exploiting small vertebratecarcasses. More complex social behavior in this group is poorlyunderstood. We conducted experiments in which one or two females(N. defodiens, N. orbicollis) were provided small or large carcasseson which to breed. On large but not on small carcasses, twofemales often formed cooperative breeding associations (jointlyprepared a carcass and fed young). In N. defodiens, but notN. orbicollis, two females produced a larger brood than singlefemales on large carcasses. In both species, the reproductiveoutput per female was less for two than for one female. Thepresence of a second female did not decrease the preparationtime of a carcass (discovery of resource to egg hatch). Conflictwas evident between females. Trials employing females of similarsize were more likely to result in injury than trials usingfemales of dissimilar size (N. tomentosus, N. defodiens, N.orbicollis). In N. tomentosus, those associations that persistedthe longest resulted in the fewest injuries. After care of youngwas initiated, conflict among familiar nest mates was not observed.There was no evidence that breeding females could discriminatebetween brood; use of a genetic marker (N. orbicollis) demonstratedthat females fed related and unrelated young alike. Femalesof similar size (high potential cost of fighting for the dominantindividual) were not more likely to form cooperative breedingassociations than females of dissimilar size (low cost of fightingfor dominant). Females of a species subject to a high rate ofnest failure (N. defodiens) were more likely to cooperate thanfemales of a species with a low rate of nest failure (N. orbicollis).It is argued that limited reproductive opportunities, difficultyin controlling rivals' access to a large carcass, and the superabundantlarval food supply represented by a large carcass, but not kinselection, have contributed to the evolution of cooperativebehavior in this group. In addition, we hypothesize that beetlesmight initially tolerate consexual rivals on large carcasseswhen there is a high likelihood of nesting failure, therebyavoiding potentially costly conflicts.     

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.

     

Habitat Fragmentation and Burying Beetle Abundance and Success

Four species of burying beetle (Nicrophorus marginatus F., N. tomentosus Weber, N. orbicollis Say and N. defodiens Mannerheim) are attracted to small, fresh mouse carcasses in northern Michigan. The number of burying beetles and their success (burial of a carcass) were greater in woodlands than in edge or field habitats. Species diversity was least in open fields as assessed by two different indices of diversity. Nicrophorus marginatus was the only species captured in large fields (<25ha). This species was never trapped in small fields (>5ha) suggesting that a minimum habitat size might be necessary to maintain local populations. In contrast to previous studies which employed pitfall traps baited with a large quantity of carrion, N. tomentosus was caught exclusively in woodlands at single mouse carcasses. In Connecticut woodlands, burying beetle success, assayed as the proportion of carcasses buried and held for 7 days, was significantly greater in larger as compared to smaller woodlands. The limited success of burying beetles in smaller woodlands was due, in part, to a higher rate of scavenging by vertebrates.     

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     

Calculating males? An empirical and theoretical examination of the duration of paternal care in burying beetles

Summary Male and female burying beetles (Nicrophorus orbicollis) bury and preserve small carcasses which become food for their young. Typically, females remain with the brood until after larval development is complete, but males leave about 3 days after larvae hatch. In the absence of competitors, the effect of male presence throughout larval development is to reduce the size and weight of the brood on small carcasses, but not on larger ones. However, male assistance greatly reduces the probability that a conspecific competitor will usurp the carcass and kill the brood. A dynamic optimization model of the duration of paternal care is developed and the daily probabilities of discovery by conspecific competitors and of finding a new reproductive opportunity are varied. The model predicts that the duration of care should not be very sensitive to either the intensity of competition or the probability of finding another carcass. For a given probability of discovery by an intruder, the probability of finding a new carcass affects the duration of care in a stepwise fashion such that males should either provide no care or remain 10 days on large carcasses and 9 days on small ones (3 days after larvae hatch, in each case). The model also suggests that by providing an average of 9.5 days of care in nature, males act as if there is a negligible chance of having another brood, i.e. they are maximizing their reproductive success with their current brood.     

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.     

Difference in parenting in two species of burying beetle, <Emphasis Type="Italic">Nicrophorus orbicollis</Emphasis> and <Emphasis Type="Italic">Nicrophorus vespilloides</Emphasis>

Burying beetles (Nicrophorus) are model parents among insects, with all studied species known to regurgitate flesh from vertebrate carcasses to their offspring. However, most studies focus on a very few species, yet the interpretation of the function and importance of care is typically generalized to all burying beetles. Here we characterize subtle variation within and between individuals and sexes, and how this variation differs between two species of burying beetle. We find that Nicrophorus orbicollis exhibits low variance, with a normal distribution of parental care provided during peak care periods. In N. vespilloides, however, the distribution is more uniform as values of care are spread across the possible phenotypic spectrum. This suggests that there is stabilizing selection on care in N. orbicollis, but relaxed or disruptive selection in N. vespilloides. Although repeatability was similar between both species, transitions from other care behaviors into feeding were more common in N. orbicollis than N. vespilloides. Thus, while parenting is coarsely similar across the genus, variation in its expression should not be extrapolated to all Nicrophorus. We suggest that subtle variation both within and among species merits greater attention, and could inform us about the factors that lead to different distributions of care.     

A test of the competitive ability–cold tolerance trade-off hypothesis in seasonally breeding beetles

1. Closely related species that use similar resources often differ in their seasonal patterns of activity, but the factors that limit their distributions across seasons are unknown for most species. One hypothesis to explain seasonal variation in the distributions of species involves a trade-off between competitive ability and cold tolerance, where tolerance to the cold compromises competitive ability in warmer (benign) temperatures, either at the level of the individual or population.
2. We tested both individual-level and population-level mechanisms of this hypothesis in two co-occurring species of temperate burying beetles (Silphidae: Nicrophorus sayi, N. orbicollis) that differ in their seasonal patterns of activity.
3. We measured cold tolerance, breeding activity as a function of temperature, and competitive ability as a function of temperature and season.
4. Consistent with our hypothesis, the mid-season N. orbicollis was less able to function at the cold temperatures that characterise early spring, when the early-season N. sayi is most active. The larger beetle, however, always won one-on-one competitive trials at warm temperatures, regardless of species, inconsistent with an individual-level trade-off. N. orbicollis was usually larger and successful when competing for the same carrion later in the season, mostly because of its larger population size, consistent with a trade-off between competitive ability, and cold tolerance acting at the population level.
5. Our findings suggest that cold temperatures limit the mid-season N. orbicollis from earlier spring emergence, while competitive pressure from the more abundant, larger N. orbicollis constrains the early-season N. sayi from remaining active through the summer.

     

Behavioral constraints on local adaptation and counter‐gradient variation: Implications for climate change

Resource allocation to growth, reproduction, and body maintenance varies within species along latitudinal gradients. Two hypotheses explaining this variation are local adaptation and counter‐gradient variation. The local adaptation hypothesis proposes that populations are adapted to local environmental conditions and are therefore less adapted to environmental conditions at other locations. The counter‐gradient variation hypothesis proposes that one population out performs others across an environmental gradient because its source location has greater selective pressure than other locations. Our study had two goals. First, we tested the local adaptation and counter‐gradient variation hypotheses by measuring effects of environmental temperature on phenotypic expression of reproductive traits in the burying beetle, Nicrophorus orbicollis Say, from three populations along a latitudinal gradient in a common garden experimental design. Second, we compared patterns of variation to evaluate whether traits covary or whether local adaptation of traits precludes adaptive responses by others. Across a latitudinal range, N. orbicollis exhibits variation in initiating reproduction and brood sizes. Consistent with local adaptation: (a) beetles were less likely to initiate breeding at extreme temperatures, especially when that temperature represents their source range; (b) once beetles initiate reproduction, source populations produce relatively larger broods at temperatures consistent with their local environment. Consistent with counter‐gradient variation, lower latitude populations were more successful at producing offspring at lower temperatures. We found no evidence for adaptive variation in other adult or offspring performance traits. This suite of traits does not appear to coevolve along the latitudinal gradient. Rather, response to selection to breed within a narrow temperature range may preclude selection on other traits. Our study highlights that N. orbicollis uses temperature as an environmental cue to determine whether to initiate reproduction, providing insight into how behavior is modified to avoid costly reproductive attempts. Furthermore, our results suggest a temperature constraint that shapes reproductive behavior.     

Differentiation in Searching Behavior for Carcasses Based on Flight Height Differences in Carrion Beetles (Coleoptera: Silphidae)

Flight ability allows insects to search for food and locate oviposition sites across a wide range of environments and, thus, allows insects to locate scarce and patchy resources such as carcasses. We examined differentiation in searching for carcasses, based on capture height differences in carrion beetles, and found that capture height differed among species. For Nicrophorus quadripunctatus and Oiceoptoma nigropunctatum, the height of abundance peaks differed among sites and was related to species composition at each site, indicating that shifts in flight height can occur plastically, whereas those for Nicrophorus maculifrons and Nicrophorus investigator did not differ among sites, indicating that the flight heights of these species are largely genetically determined. Thus, the present differentiation in capture height is primarily determined by current plastic shifts and on some genetic basis.     

Population density, body size, and phenotypic plasticity of brood size in a burying beetle

Theory predicts that organisms living in heterogeneous environmentswill exhibit phenotypic plasticity. One trait that may be particularlyimportant in this context is the clutch or brood size becauseit is simultaneously a maternal and offspring characteristic.In this paper, I test the hypothesis that the burying beetle,Nicrophorus orbicollis, adjusts brood size, in part, in anticipationof the reproductive environment of its adult offspring. N. orbicollisuse a small vertebrate carcass as a food resource for theiryoung. Both parents provide parental care and actively regulatebrood size through filial cannibalism. The result is a positivecorrelation between brood size and carcass size. Adult bodysize is an important determinant of reproductive success forboth sexes, but only at higher population densities. I testthree predictions generated by the hypothesis that beetles adjustbrood size in response to population density. First, averageadult body size should vary positively with population density.Second, brood size on a given-sized carcass should be larger(producing more but smaller young) in low-density populationsthan in high-density populations. Third, females should respondadaptively to changes in local population density by producinglarger broods when population density is low and small broodswhen population density is high. All three predictions weresupported using a combination of field and laboratory experiments.These results (1) show that brood size is a phenotypically plastictrait and (2) support the idea that brood size decisions arean intergenerational phenomenon that varies with the anticipatedcompetitive environment of the offspring.     

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.     

Molecular systematics and biogeography of Nicrophorus in part--the investigator species group (Coleoptera: Silphidae) using mixture model MCMC

Burying beetles (Silphidae: Nicrophorus) are well-known for their biparental care and monopolization of small vertebrate carcasses in subterranean crypts. They have been the focus of intense behavioral ecological research since the 1980s yet no thorough phylogenetic estimate for the group exists. The relationships among the species, and the validity of some species, are poorly understood. Here, we infer the relationships and examine species boundaries among 50 individuals representing 15 species, primarily of the investigator species group, using a mixture-model Bayesian analysis. Two mitochondrial genes, COI and COII, were used, providing 2129 aligned nucleotides (567 parsimony-informative). The Akaike Information Criterion and Bayes Factors were used to select the best fitting model, in addition to Reversible Jump MCMC, which accommodated model uncertainty. A 21 parameter, three-partition GTR + G was the final model chosen. Despite a presumed Old World origin for the genus itself, the basal lineages and immediate outgroups of the investigator species group are New World species. Bayesian methods reconstruct the common ancestor of the investigator species group as New World and imply one later transition to the Old World with two return transitions to the New World. Prior hypotheses concerning the questionable validity of four species names, Nicrophorus praedator, Nicrophorus confusus, Nicrophorus encaustus and Nicrophorus mexicanus were tested. No evidence was found for the validity of the Nicrophorus investigator synonym N. praedator. We found evidence rejecting the species status of N. confusus (NEW SYNONYM of Nicrophorus sepultor). Weak evidence was found for the species status of N. encaustus and N. mexicanus, which are tentatively retained as valid. Our results strongly reject a recently published hypothesis that Nicrophorus interruptus (NEW STATUS as valid species) is a subspecies of N. investigator.     

Study of community assembly patterns and interspecific interactions involved in insect succession on rat carcasses

Although many forensic entomological studies have described patterns of carrion insect succession and theoretical studies have explained interspecific interactions that drive succession, empirical studies on the quantitative and ecological aspects of carrion insect succession, such as the degree of historical contingency in community assembly and interspecific interactions during succession, are limited. In this study, I investigated variability in the successional pathways of carrion insect communities in rat carcasses and their decomposition processes, and examined the interspecific interactions involved in succession, such as the effects of carcass utilization by early‐arriving species on late‐arriving species. Members of the families Calliphoridae and Formicidae and the species Eusilpha japonica (Motschulsky) and Nicrophorus concolor Kraatz were chiefly observed. In almost all carcasses, formicid species arrived first, and calliphorid species and E. japonica arrived simultaneously or immediately after. Nicrophorus concolor arrived last, with its time of colonization occurring earlier in carcasses with greater E. japonica abundance. Meanwhile, the early‐arriving species decreased when N. concolor arrived. Nicrophorus concolor tended to reproduce on carcasses with lower cumulative abundance of early‐arriving species and tended to feed on carcasses with greater cumulative abundance of early‐arriving species. These results show that the successional pathways of the chief carrion insect species are highly consistent among carcasses. In contrast, early‐arriving species seem to influence the utilization patterns of carcasses by late‐arriving species, and therefore produce variability in the decomposition process. These results also show that succession could be driven by facilitation and interspecific competition between early‐arriving and late‐arriving species.     

Resource availability and population dynamics of Nicrophorus investigator, an obligate carrion breeder

1. Food resources for rearing young may influence insect populations. This is particularly true for insects that breed obligately on rare, ephemeral resources such as dung, fungi, or carrion. 2. Beetles in the genus Nicrophorus bury small vertebrate carcasses for rearing their young. Studies reviewed by Scott (1998) have found a positive relationship between carcass mass and total brood size. It is likely that access to carcasses suitable for breeding, and not food or mates, limits reproduction in both male and female Nicrophorus. Thus, small mammal densities could determine Nicrophorus population sizes. 3. The work reported here examined the relationship between Nicrophorus investigator (Coleoptera: Silphidae) population size and small mammal abundance at two sites over a 4‐year period. 4. Nicrophorus investigator buried and reared young on all the native small rodent species trapped at two sites in south‐western Colorado, U.S.A. (Peromyscus maniculatus, Microtus montanus, Zapus princeps, Tamias minimus, Thomomys talpoides). They preferred to bury and reproduce on rodent carcasses weighing between 16 and 48 g; rodents of this size represented 82% of captures. 5. Population sizes of N. investigator and small rodents were estimated simultaneously using mark‐recapture censuses over a 4‐year period. Considering only rodents within the size range used by N. investigator, the estimated small mammal biomass per hectare in one year and the beetle population size in the following year were correlated significantly.     

Brood size reduction in Nicrophorus vespilloides after usurpation of carrion from Nicrophorus quadripunctatus (Coleoptera: Silphidae)

Burying beetles bury small vertebrate carcasses, which become food for their larvae. They sometimes usurp carcasses occupied and buried by other beetles. Brood sizes of intraspecific and interspecific intruders were examined using Nicrophorus quadripunctatus as the resident. The brood sizes of usurpers were not reduced relative to control brood sizes when the usurper was conspecific, but were reduced when the usurper was heterospecific (N. vespilloides).     

Residency Time as an Indicator of Reproductive Restraint in Male Burying Beetles

The cost of reproduction theory posits that there are trade-offs between current and future reproduction because resources that are allocated to current offspring cannot be used for future reproductive opportunities. Two adaptive reproductive strategies have been hypothesized to offset the costs of reproduction and maximize lifetime fitness. The terminal investment hypothesis predicts that as individuals age they will allocate more resources to current reproduction as a response to decreasing residual reproductive value. The reproductive restraint hypotheses predicts that as individuals age they will allocate fewer resources to current reproduction to increase the chance of surviving for an additional reproductive opportunity. In this study, we test for adaptive responses to advancing age in male burying beetles, Nicrophorus orbicollis. Burying beetles use facultative biparental care, but the male typically abandons the brood before the female. Previous work in male burying beetles has suggested several factors to explain variation in male residency time, but no study has observed male behavior throughout their entire reproductive lifetimes to determine whether males change residency time in an adaptive way with age. We compared residency time of males that reproduced biparentally, uniparentally, and on different-sized carcasses to determine if they used an adaptive reproductive strategy. Males did not increase residency time as they aged when reproducing biparentally, but decreased residency time with age when reproducing uniparentally. A decrease in parental care with age is consistent with a reproductive restraint strategy. When female age increased over time, males did not increase their residency time to compensate for deteriorating female condition. To our knowledge, this is the first test of adaptive reproductive allocation strategies in male burying beetles.     

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.     

Effect of Population Density and Female Body Size on Number and Size of Offspring in a Species with Size‐Dependent Contests over Resources

When size‐dependent contests over resources influence reproductive success, the trade‐off between number and size of offspring depends on the frequency of contests. Under these circumstances, clutch size should decrease and offspring size should increase as contests become more frequent. We tested these predictions with the burying beetle Nicrophorus pustulatus through manipulation of rearing densities. Burying beetles reproduce on small vertebrate carcasses, a rare but high quality food source for the larvae. Large beetles are more likely to win contests over carcasses and gain exclusive access to a carcass. The winner of a contest kills eggs and larvae already present on a carcass. As a result of the rarity of carcasses, burying beetles are unlikely to breed more than once. As predicted, brood size of N. pustulatus decreased with increasing rearing density. Despite a negative correlation between brood size and larval mass, larval mass did not increase with increasing rearing density. This may be due to the special biology of N. pustulatus which can use snake eggs for reproduction. Potentially larger supply of resources and generally small population densities of N. pustulatus may weaken selection on body size and thus the correlation between brood size and larval mass. As size‐dependent constraints can limit reproductive phenotypes, we examined whether female size influenced reproductive phenotype. Small females produced larger broods with smaller, but more variable, offspring than large females. Mechanical constraints of egg size seem an unlikely explanation for the differences because burying beetles can compensate for small egg size through parental care. Energetic constraints may impact small females because body mass and brood size of small females decreased with increasing density. Yet, at all density levels small females produced larger, not smaller, broods than large females. The larger and more variable broods of small females seem to be in agreement with a bet‐hedging strategy.