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.     

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.     

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.     

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.     

Nesting failure in burying beetles and the origin of communal associations

Summary Information on reproductive success and the probability of nest failure was gathered from 11 recent studies ofNicrophorus defodiens, which readily forms communal breeding associations andNicrophorus orbicollis, which rarely tolerates consexuals in the nest.Nicrophorus defodiens was subject to a high rate of nest failure on larger carcasses and consequently, is expected to achieve little reproductive benefit by excluding a rival during nest initiation.Nicrophorus orbicollis, on the other hand, was successful on a higher proportion of carcasses of all sizes and is predicted to gain substantial benefits by excluding a rival. These findings support the hypothesis that high rates of nest failure can promote the evolution of tolerance and incipient communality among unrelated adults, even in the absence of immediate reproductive gains.     

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.

     

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.     

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.     

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.     

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.     

Intended and unintended receivers of the male pheromones of the burying beetles Nicrophorus humator and Nicrophorus vespilloides

Male Nicrophorus beetles (Coleoptera: Silphidae) attract females through volatiles that are emitted at species‐specific times of day. Not only beetles of the opposite sex but also conspecific males are attracted. Another observation is the co‐attraction of congeners, a phenomenon that was shown in particular for Nicrophorus vespilloides Herbst, the smallest Nicrophorus species in Central Europe. In the current study, we identified the Nicrophorus humator Gleditsch male pheromone as methyl 4‐methyloctanoate through gas chromatography/mass spectrometry analysis. In field experiments, we tested and compared the attractiveness of synthetic analogs of the male pheromones of N. humator and N. vespilloides in baited pitfall traps. An asymmetric cross‐attraction to the synthetic male pheromones was observed, which is best explained by the skewed competitive relationship of the two species, with regard to the restricted availability of breeding resources. Nicrophorus humator is attracted by both its own male pheromone and by the pheromone of the smaller N. vespilloides, whereas N. vespilloides is almost exclusively attracted by its own male pheromone. The observed attraction of conspecific males of either species to male pheromone baits can be explained by both competition for females and competition for breeding resources.     

Number and size of clutch in Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae), with comparisons to Nicrophorus

Ptomascopus morio displays simpler parental care than Nicrophorus species. The effects of carcass size and clutch number on clutch size in P. morio were examined. Clutch size was related to carcass size. There was a negative correlation between number of clutch and clutch size for most sizes of carcass. Longevity of females was shorter when the carcass size was larger, such that total lifetime fecundity did not differ among carcasses of different sizes. The clutch size of P. morio was larger than that of Nicrophorus quadripunctatus. The clutch size of P. morio declined rapidly with repeated clutch production, but that of N. quadripunctatus was rather constant. This indicates that N. quadripunctatus maintains a more constant clutch size than P. morio over several reproductive attempts, although the former displays more complex parental care.     

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     

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.     

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.     

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.     

Evolutionary importance of parental care performance,food resources,and direct and indirect genetic effects in a burying beetle

Indirect genetic effects (IGE) of parental care performance and the direct–indirect covariance contribute substantially to total heritability in domesticated and laboratory mammals. For animals from natural populations empirical estimates of IGE are sparse. Thus, despite recent models relating IGE to evolution, evolutionary interpretations of IGE are limited. To address this deficit, we used a reciprocal cross‐fostering breeding design to estimate environmental influences, direct and indirect genetic effects, and direct–indirect genetic covariances in the burying beetle Nicrophorus pustulatus to determine the evolutionary importance of IGE arising from variation in parental care performance. Carrion size positively affected adult mass and time on carrion, but had no effect on total development time. Males were slightly larger than females. For both mass and development, independent of these environmental influences, direct and indirect genetic effects were of moderate magnitude. Total genetic effects explained 36–50% of the phenotypic variance in mass and size and 27–37% of phenotypic variance in development time. Direct–indirect genetic covariances were zero or close to zero. Thus, for both mass and development time, the response to natural selection arising from environmental variation may be accelerated by the presence of IGE in N. pustulatus. The generality of this pattern and the evolutionary significance of IGE arising from parental care awaits further study of natural populations.     

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.     

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.     

Are species differences in maternal effects arising from maternal care adaptive?

Parental care benefits offspring through maternal effects influencing their development, growth and survival. However, although parental care in general is likely the result of adaptive evolution, it does not follow that specific differences in the maternal effects that arise from care are also adaptive. Here, we used an interspecific cross‐fostering design in the burying beetle species Nicrophorus orbicollis and N. vespilloides, both of which have elaborate parental care involving direct feeding of regurgitated food to offspring, to test whether maternal effects are optimized within a species and therefore adaptive. Using a full‐factorial design, we first demonstrated that N. orbicollis care for offspring longer regardless of recipient species. We then examined offspring development and mass in offspring reared by hetero‐ or conspecific parents. As expected, there were species‐specific direct effects independent of the maternal effects, as N. orbicollis larvae were larger and took longer to develop than N. vespilloides regardless of caregiver. We also found significant differences in maternal effects: N. vespilloides maternal care caused more rapid development of offspring of either species. Contrary to expectations if maternal effects were species‐specific, there were no significant interactions between caretaker and recipient species for either development time or mass, suggesting that these maternal effects are general rather than optimized within species. We suggest that rather than coadaptation between parents and offspring performance, the species differences in maternal effects may be correlated with direct effects, and that their evolution is driven by selection on those direct effects.