Nicrophorus Species Research Articles

Competition among host-specific lineages of Poecilochirus carabi mites influences the extent of co-adaptation with their Nicrophorus vespilloides burying beetle hosts.

Reciprocal selection between symbiotic organisms and their hosts can generate variations in local adaptation between them. Symbionts often form species complexes with lineages partially adapted to various hosts. However, it is unclear how interactions among these lineages influences geographic variation in the extent of host-symbiont local adaptation. We addressed this shortcoming with experiments on burying beetles Nicrophorus vespilloides and their specialist phoretic mite Poecilochirus carabi in two adjacent woodlands. Burying beetles transport these mites to vertebrate carrion upon which they both reproduce. P. carabi appears to be a species complex, with distinct lineages that specialise on breeding alongside different Nicrophorus species. We found that in one wood (Gamlingay Woods), N. vespilloides carries a mixture of mite lineages, with each lineage corresponding to one of the four Nicrophorus species that inhabits this wood. However, two burying beetle species coexist in neighbouring Waresley Woods and here N. vespilloides predominantly carries the mite lineage that favours N. vespilloides. Mite lineage mixing alters the degree of local adaptation for both N. vespilloides and the P. carabi mites, affecting reproductive success variably across different woodlands. In Gamlingay, mite lineage mixing reduced N. vespilloides reproductive success, while experimentally purifying mites lineage enhanced it. The near pure lineage of vespilloides mites negligibly affected Waresley N. vespilloides. Mite reproductive success varied with host specificity: Gamlingay mites had greatest reproductive success on Gamlingay beetles, and performed less well with Waresley beetles. By contrast, Waresley mites had consistent reproductive success, regardless of beetle's woodland of origin. We conclude that there is some evidence that N. vespilloides and its specific mite lineage have coadapted. However, neither N. vespilloides nor its mite lineage adapted to breed alongside other mite lineages. This, we suggest, causes variation between Waresley and Gaminglay Woods in the extent of local adaptation between N. vespilloides beetles and their P. carabi mites.

Spatiotemporal variation in the competitive environment, with implications for how climate change may affect a species with parental care.

Burying beetles of the genus Nicrophorus havebecome a model for studying the evolution of complex parental care in laboratory studies. Nicrophorus species depend on small vertebrate carcasses to breed, which they process and provision to their begging offspring. However, vertebrate carcasses are highly sought after by a wide variety of species and so competition is expected to be critical to the evolution of parental care. Despite this, the competitive environment for Nicrophorus is rarely characterized in the wild and remains a missing factor in laboratory studies. Here, we performed a systematic sampling of Nicrophorus orbicollis living near the southern extent of their range at Whitehall Forest in Clarke County, Georgia, USA. We determined the density of N. orbicollis and other necrophilous species that may affect the availability of this breeding resource through interference or exploitation competition. In addition, we characterize body size, a key trait involved in competitive ability, for all Nicrophorus species at Whitehall Forest throughout the season. Finally, we compare our findings to other published natural history data for Nicrophorines. We document a significantly longer active season than was observed 20 years previously at Whitehall Forest for both N. orbicollis and Nicrophorus tomentosus, potentially due to climate change. As expected, the adult body size of N. orbicollis was larger than N. tomentosus, the only other Nicrophorus species that was captured in 2022 at Whitehall Forest. The other most prevalent insects captured included species in the families Staphylinidae, Histeridae, Scarabaeidae, and Elateridae, which may act as competitors or predators of Nicrophorus young. Together, our results indicate significant variation in intra- and interspecific competition relative to populations within the N. orbicollis range. These findings suggest that the competitive environment shows extensive spatiotemporal variation, providing the basis to make predictions for how ecology may influence parenting in this species.

Effect of food source availability in the salivary gland transcriptome of the unique burying beetle Nicrophorus pustulatus (Coleoptera: Silphidae).

Nicrophorus is a genus of beetles that bury and transform small vertebrate carcasses into a brood ball coated with their oral and anal secretions to prevent decay and that will serve as a food source for their young. Nicrophorus pustulatus is an unusual species with the ability to overtake brood of other burying beetles and whose secretions, unlike other Nicrophorus species, has been reported not to exhibit antimicrobial properties. This work aims to better understand how the presence or absence of a food source influences the expression of genes involved in the feeding process of N. pustulatus. To achieve that, total RNA was extracted from pooled samples of salivary gland tissue from N. pustulatus and sequenced using an Illumina platform. The resulting reads were used to assemble a de novo transcriptome using Trinity. Duplicates with more than 95% similarity were removed to obtain a “unigene” set. Annotation of the unigene set was done using the Trinotate pipeline. Transcript abundance was determined using Kallisto and differential gene expression analysis was performed using edgeR. A total of 651 genes were found to be differentially expressed, including 390 upregulated and 261 downregulated genes in fed insects compared to starved. Several genes upregulated in fed beetles are associated with the insect immune response and detoxification processes with only one transcript encoding for the antimicrobial peptide (AMP) defensin. These results confirm that N. pustulatus does not upregulate the production of genes encoding AMPs during feeding. This study provides a snapshot of the changes in gene expression in the salivary glands of N. pustulatus following feeding while providing a well described transcriptome for the further analysis of this unique burying beetle.

Stridulation is unimportant for effective parental care in two species of burying beetle

1. Communication among family members is often essential for navigating the social and trophic interactions that arise during parental care. In insects, this communication is often accomplished via pheromonal signals. However, some insects also produce acoustic signals (stridulations) during parental care.2. Burying beetles (Nicrophorusspp) audibly stridulate during mating and parental care and several studies have suggested that stridulation is an important form of communication between family members. Experimental studies have generally supported a role of stridulation inNicrophorusparental care: preventing stridulation or changing the vibrational properties of stridulation generally reduces parental performance. However, some of these previous experiments are difficult to interpret and the importance of this form of communication in burying beetles is still unclear.3. Here we describe experiments involving twoNicrophorusspecies (N.vespilloidesandN.orbicollis) in which we used a minimally invasive phenotypic manipulation to test whether stridulation is necessary for effective parental care. Our phenotypic manipulation rendered the both species silent; however, it had no detectable impact on parental performance in either species.4. Our results suggest that stridulation does not play an important role in mating or the coordination of parental care in at least twoNicrophorusspecies, casting doubt upon a long‐assumed function of stridulation in the genus.

A case of a Pustulated Carrion Beetle (<i>Nicrophorus pustulatus</i>, Coleoptera: Silphidae) burying live Tree Swallow (<i>Tachycineta bicolor</i>, Passeriformes: Hirundinidae) nestlings under the nest

The ecology of Pustulated Burying Beetle (Nicrophorus pustulatus, Coleoptera: Silphidae) appears distinct among Nicrophorus species, with evidence of it parasitizing snake eggs and foraging primarily above the ground and into the forest canopy. Here we document an extension of its aberrant ecology and behaviour: a case of N. pustulatus burying 2-day-old live and dead nestlings of Tree Swallow (Tachycineta bicolor, Passeriformes: Hirundinidae) under the nest, behaviour consistent with the early stages of breeding in N. pustulatus. Based on different levels of decomposition, we suspect that N. pustulatus responded to one dead swallow nestling in the brood of five and went on to bury all of the nestlings at the bottom of the nest box. The observation provides the first evidence, to our knowledge, of Nicrophorus burying live vertebrates.

Habitat use of co-occurring burying beetles (genusNicrophorus) in southeastern Ontario, Canada

The coexistence of closely related species plays an important role in shaping local diversity. However, competition for shared resources can limit the ability of species to coexist. Many species avoid the costs of coexistence by diverging in habitat use, known as habitat partitioning. We examine patterns of habitat use in seven co-occurring species of burying beetles (genus Nicrophorus Fabricius, 1775), testing the hypothesis that Nicrophorus species partition resources by occupying distinct habitats. We surveyed Nicrophorus abundance and 54 habitat characteristics at 100 random sites spanning an environmentally diverse region of southeastern Ontario, Canada. We found that three species occupied distinct habitat types consistent with habitat partitioning. Specifically, Nicrophorus pustulatus Herschel, 1807, Nicrophorus hebes Kirby, 1837, and Nicrophorus marginatus Fabricius, 1801 appear to be specialists for forest canopy, wetlands, and open fields, respectively. In contrast, Nicrophorus orbicollis Say, 1825, Nicrophorus sayi Laporte, 1840, and Nicrophorus tomentosus Weber, 1801 appear to be generalists with wide breadths of habitat use. We were unable to identify the habitat associations of Nicrophorus defodiens Mannerheim, 1846. Our findings are consistent with habitat acting as an important resource axis along which some Nicrophorus species partition; however, divergence along other resource axes (e.g., temporal partitioning) also appears important for Nicrophorus coexistence.

Eavesdropping on the dead: heterogeneity of tallgrass prairie soundscapes and their relationship with invertebrate necrophilous communities

ABSTRACT Tallgrass prairies are rapidly vanishing biodiversity hotspots for native species, yet little is known about the spatio-temporal variation of prairie soundscapes and how they relate to grassland biological communities. Using an ecoacoustic approach to examine the relationship between a southern tallgrass prairie soundscape and the spatial distributions of an ecologically important community of necrophilous invertebrates, we used pitfall traps and programmable passive acoustic recorders to conduct a Nicrophorus burying beetle field survey while simultaneously obtaining soundscape recordings across a 16,000 ha tallgrass prairie site. We quantified soundscape characteristics using six ecoacoustic indices and found that associations between Nicrophorus burying beetle abundances and acoustic index values were species-specific and unique to particular acoustic indices and times of day. Although Nicrophorine burying beetles share a dependence on vertebrate carcasses for reproduction, these distinctive relationships with the prairie soundscape likely reveal fine-scale temporal, spatial and carcass-size niche segregation that occurs between Nicrophorus species. Key policy insights Soundscape datasets analyzed using acoustic indices can produce useful time-series data that captures spatio-temporal trends associated with both biotic and abiotic ecosystem factors. Environmental acoustic data can be used to assess habitat quality for non-soniferous species of interest that depend on or interact closely with sound-producing species or acoustic communities. Broadly, acoustic indices may produce data that allows managers to rapidly assess critical habitats in the context of disturbance, restoration, or climate-mediated effects.

Disrupting information alters the behavioral response to a mutual signal trait in both sexes of Nicrophorus (Coleoptera: Silphidae) burying beetles

AbstractEffective signals transfer information in a way that enhances the fitness of the sender. Signal traits are often sexually dimorphic. However, in some species, males and females display similar signals, and these mutual signals are less often studied. Competition for resources occurs in both males and females, and mate choice is likely to occur whenever mates vary in quality and reproductive investment is high. Nicrophorus burying beetles compete intrasexually over the carrion resources on which they biparentally raise their young. Nicrophorus species also often have clypeal membranes which scale hyperallometrically with body size, exaggerating the apparent body size of larger individuals. To examine the potential signaling function of clypeal membranes, we examined the behavioral responses of male and female Nicrophorus orbicollis and Nicrophorus pustulatus burying beetles to same- and opposite-sex social partners which had their membranes painted black or clear. We found evidence that blocking the information in clypeal membranes affected intrasexual aggressive interactions for both sexes of both species. Blocking a female’s signal reduced the likelihood of mating attempts for male N. pustulatus, whereas blocking a male’s signal influenced female rejection behaviors in N. orbicollis. Our results show that males and females can experience similar selection pressures, and suggest that examining mutual signals in a broader range of systems will expand our understanding of evolutionary differences and similarities between the sexes.

The Type of Nicrophorus chryseus Mazokhin-Porshnyakov, 1953 (Coleoptera: Silphidae) Rediscovered and a Commentary on “Accidental Taxonomy”

Study of the previously lost type of Nicrophorus chryseusMazokhin-Porshnyakov, 1953 determined it to be a member of the polymorphic Holarctic species Nicrophorus investigatorZetterstedt, 1824, new synonymy. The unintentional but formal changing of a taxonomic classification, which we term “accidental taxonomy,” is discussed.

Volatiles Emitted by Calling Males of Burying Beetles and Ptomascopus morio (Coleoptera: Silphidae: Nicrophorinae) Are Biogenetically Related.

In burying beetles, Nicrophorus spp. (Coleoptera: Silphidae: Nicrophorinae) mate finding is mediated by male produced volatile compounds. To date, pheromone components of only two species have been identified. In an attempt to better understand the evolution of male pheromone signaling in burying beetles, we investigated the male released volatiles of ten Nicrophorus species and one closely related nicrophorine species, Ptomascopus mori. Volatiles emitted by calling males were collected in the laboratory by means of solid phase micro extraction and analyzed using gas chromatography coupled with mass spectrometry. Identified volatiles included short chain esters of 4-methylcarboxylic acids, terpenoids, and some other aliphatic compounds. The long-range volatile signals of the burying beetle species included in this study are blends of two to seven components. We found that methyl or ethyl esters of 4-methylheptanoic acid and 4-methyloctanoic acid are produced by eight of the ten investigated Nicrophorus species. These esters may play a key role in chemical communication. Their widespread occurrence suggests that these compounds did not evolve recently, but appeared relatively early in the phylogeny of the genus. Although Ptomascopus is considered the sister genus of Nicrophorus, P. morio males do not produce any of the Nicrophorus compounds, but release 3-methylalkan-2-ones, which are absent in Nicrophorus. A better understanding of the evolution of burying beetle pheromones, however, will only be possible once more species have been studied.

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.

Dynamic changes in volatile emissions of breeding burying beetles

AbstractBurying beetles reproduce on small vertebrate carcasses by exhibiting elaborate biparental brood care. Partner recognition in breeding Nicrophorus species (Coleoptera: Silphidae) relies substantially on information encoded in cuticular hydrocarbon profiles. Until recently, it was unknown whether breeding burying beetles also produce volatile low molecular weight substances and, if so, which functions can be attributed to such volatiles. The present study reports a survey of the volatiles released by males and females of Nicrophorus vespilloides Herbst in nonbreeding status and at different stages of breeding. Headspace analyses are performed by using solid phase micro‐extraction fibres and gas chromatography–mass spectrometry. The volatiles released by nonbreeding males and females include phenolic compounds, alcohols, aldehydes and ketones and are quite similar in both sexes. With the onset of breeding, the volatile profiles of males and females become distinct, with a number of female‐specific compounds occurring. An analysis of the anal secretions reveals the presence of some of the compounds previously detected in the headspace analysis. The specific chemical properties suggest that some of the volatiles may function against competitors and parasites, such as bacteria, fungi, nematodes and arthropods at the carcass breeding resource. By contrast, the emission of 4‐methyl branched esters by the females closely parallels the emission of the terpenoid methyl geranate and they may function together as a complex signal by the females. Signalling traits associated with biparental care and specific constraints associated with the ephemeral nature of the breeding resource may explain the occurrence of both groups of compounds in the volatile profiles.

Isolation of nine polymorphic microsatellite loci from the burying beetle, Nicrophorus quadripunctatus (Coleoptera: Silphidae)

The burying beetle, Nicrophorus quadripunctatus Kraatz, is a common species in Japan, and its biparental care has been well studied. It exploits small vertebrate carrion as food for its young. Therefore, its reproductive success is restricted to large habitats in which carrion is abundant and available. Hence, the abundance of Nicrophorus species can be used as an indicator of forest fragmentation. Forests have recently become fragmented due to anthropogenic activities, and thus the population sizes of Nicrophorus species have decreased. To investigate the population genetic structure of N. quadripunctatus, we developed polymorphic microsatellite markers using magnetic particles. Nine microsatellites were polymorphic, with two to 12 alleles observed in the samples collected from our study sites, Matsunoyama and Nagaoka A and B. Deviation from the Hardy–Weinberg equilibrium was detected at five to seven loci in each population examined, which is indicative of significant heterozygous deficiencies. Higher genetic diversity was found in the Matsunoyama and Nagaoka B populations, the collection plots of which were covered by continuous woodlands, compared to Nagaoka A. The isolated microsatellite markers will be used to determine the genetic structures of the fragmented populations of N. quadripunctatus.

Description of Nicrophorus efferens, new species, from Bougainville Island (Coleoptera, Silphidae, Nicrophorinae).

A new species of Nicrophorus in the nepalensis species-group, Nicrophorus efferens Sikes and Mousseau, is described from Bougainville Island in the Solomon Islands archipelago. It is distinguished from the known species of the genus Nicrophorus and its likely closest relative, Nicrophorus reticulatus Sikes and Madge, based on external morphology. A comparison among the four Nicrophorus species known from the Solomon Island archipelago and Papua New Guinea is presented.

Cryptic species of mites (Uropodoidea: Uroobovella spp.) associated with burying beetles (Silphidae: Nicrophorus): The collapse of a host generalist revealed by molecular and morphological analyses

Uroobovella (Mesostigmata: Uropodoidea: Urodinychidae) species are among the most common mites associated with carrion-feeding Nicrophorus (Silphidae) beetles. Previous taxonomic understanding suggests that a single host generalist, U. nova, disperses and lives with Nicrophorus species worldwide (reported from at least seven host species). Using morphometrics and morphological characteristics, as well as partial cytochrome oxidase I (COI) and the entire internal transcribed spacer 2 (ITS2) markers, we tested whether this apparent generalist is truly a generalist or rather a complex of cryptic species with narrower host ranges. Based on deutonymph mites collected from 14 host species across six countries and 17 provinces or states, we show that U. nova represents at least five morphologically similar species with relatively restricted host ranges. Except for one species which yielded no molecular data (but did exhibit morphological differences), both molecular and morphological datasets were congruent in delimiting species boundaries. Moreover, comparing the mite phylogeny with the known ecology and phylogenetic relationships of their host species suggests that these mites are coevolving with their silphid hosts rather than tracking ecologically similar species.

Beetles and flies collected on pig carrion in an experimental setting in Thuringia and their forensic implications

Decomposition processes and insect succession were analysed on a total of eight pig (Sus scrofa) carcasses. The survey was carried out in four different periods between November 2007 and August 2008 and on two different substrates (meadow, concrete floor close to a building). The experiments were placed in a rural site in the surroundings of Jena, Thuringia. The duration and specificity of the different decomposition stages were dependent on season, weather and quality and quantity of insect colonization. Whereas the carrion maintained a bloated appearance even after 133 days in winter, it reached the dry stage within 8 days in the summer months. The type of substrate had few effects on the decaying process, but the insects were generally more abundant on the meadow. In total, more than 57 species of Diptera belonging to 17 families and 48 species of Coleoptera belonging to 14 families were identified. Dominant species belonged to the families of Calliphoridae (n = 11 spp.), Sarcophagidae (n = 8), Muscidae (n = 9), Piophilidae (n = 3), Silphidae (n = 6), Dermestidae (n = 3), Nitidulidae (n = 4), Cleridae (n = 3) and Histeridae (n = 2). Remarkably, the rather common Nicrophorus species were completely absent, whereas the usually rare Necrodes littoralis (L.) was present in larger numbers. No distinct coincidence between the occurrence of a single species and a certain decomposition stage could be confirmed. A main objective of the study is the establishment of a forensic entomological database for Central Europe, especially Thuringia.

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

Abstract 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.

Niche differentiation of burying beetles (Coleoptera: Silphidae: Nicrophorinae) in carcass use in relation to body size: Estimation from stable isotope analysis

Adult burying beetles use the carcasses of small vertebrates for food and breeding their young. Some species are known to have optimum carcass sizes related to their body sizes, but their carcass use is difficult to observe in situ. We explored their size-related niche differentiation in carcass resource using stable isotope analysis. The largest Nicrophorus species in Japan (N. concolor) showed the highest δ15N, and the smallest Nicrophorus species in Japan (N. montivagus) showed the lowest δ13C and δ15N among all Nicrophorus species, suggesting that their niches are differentiated from those of other species in carcass resource. We also revealed a positive correlation between δ15N and body size. Ptomascopus morio showed significantly higher δ15N than all studied Nicrophorus species. This species does not show parental care behavior and the adults may feed on quite different resources from Nicrophorus species.

Host defense inNicrophorus quadripunctatusagainst brood parasitism byPtomascopus morio(Coleoptera: Silphidae: Nicrophorinae)

AbstractFew studies have been conducted on the host defenses of insects against brood parasitism. We investigated whether the silphid beetlePtomascopus morio, a brood parasite of related silphid speciesNicrophorus concolor, can also parasitize another silphid speciesNicrophorus quadripunctatusand the manner in whichN. quadripunctatusdefends itself against parasitism. Successful brood parasitism under natural conditions was not observed at the time of year whenP. morioandN. quadripunctatusare both reproductively active. Follow‐up experiments revealed thatP. morioattempts to oviposit nearN. quadripunctatusnests, but is rarely successful if adult hosts are present. WhenP. moriolarvae were experimentally introduced toN. quadripunctatusbroods, someP. moriolarvae survived when the host and parasite larvae were at the same stage. We concluded thatN. quadripunctatusdefends itself against brood parasitism in two ways: (1) potential brood parasites are repelled, thus limiting their access to the resource; and (2) the young of the parasitic species are killed.