Wikipedia

Nicrophorus pustulatus

(Redirected from Pustulated carrion beetle)

Nicrophorus pustulatus, also known as the pustulated carrion beetle[1] or blistered burying beetle,[2] is a species of burying beetle that was described by Johann Karl Wilhelm Illiger in 1807.[3] This species is native to North America.[4] N. pustulatus exhibits unique habitat utilization and breeding behaviour relative to other members of the genus.[5][6] This species may be the only described example of a true parasitoid targeting a vertebrate host.[7][8][9]

Nicrophorus pustulatus
Right-lateral view of a medium-sized adult beetle. The beetle is shiny and black, with small, dark orange spots on the elytra. It has approximately 20 small, brown mites clinging to its head, thorax, and abdomen.
Adult Nicrophorus pustulatus beetle, with phoretic mites
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Coleoptera
Family: Silphidae
Genus: Nicrophorus
Species:
N. pustulatus
Binomial name
Nicrophorus pustulatus
Illiger in Herschel (1808)
Synonyms
  • Necrophorus [sic] pustulatus Illiger in Herschel, 1808
  • Necrophorus [sic] bicolon Newman, 1838
  • Necrophorus [sic] tardus Mannerheim, 1853
  • Necrophorus [sic] marginatus fasciatus Portevin, 1924
  • Necrophorus [sic] marginatus unicolor Portevin, 1924

Taxonomy

edit

Phylogeny

edit

N. pustulatus is one of over 60 extant species in the genus Nicrophorus.[7] This genus belongs to the subfamily Nicrophorinae (sexton beetles), which is one of two subfamilies in the family Silphidae (carrion beetles, large carrion beetles, or burying beetles).[10] The family Silphidae belongs to the superfamily Staphylinoidea, infraorder Staphyliniformia, suborder Polyphaga, and order Coleoptera.[11] The genus Nicrophorus is hypothesized to have evolved in the Cretaceous Period approximately 99-127 million years ago and then undergone most of its speciation in the period approximately 40-60 million years ago. This was the period when the small-bodied vertebrates that these beetles use for carrion were also radiating.[12]

One recent molecular phylogeny of the genus Nicrophorus placed N. pustulatus as the sister species to N. hispaniola. The clade containing N. pustulatus and N. hispaniola is hypothesized to be sister to the clade containing N. tomentosus, N. hybridus, N. semenowi, N. nigrita, N. mexicanus, N. interruptus, N. investigator, N. encaustus, N. argutor, and N. sepultor.[12] This placement was based on sequences from the mitochondrial COI (Cytochrome C Oxidase Subunit I) and COII (Cytochrome C Oxidase Subunit II) gene regions, and the nuclear D2 region of the 28S ribosomal RNA gene and protein coding CAD (carbamoylphosphate synthetase) gene.[12]

General phylogeny and evolutionary divergence timeline diagrams can be accessed via Timetree.[13]

Species description

edit

The species is sometimes referred to as N. pustulatus Herschel, after Johann Dietrich Herschel. Hershel published an article describing two Nicrophorus beetles, to which a footnote was added by Johann Karl Wilhelm Illiger naming one of the species N. pustulatus. The article lists 1807 on the title page, but may have been published in 1808. The scientific name is now attributed in some places to Illiger, 1808.[3] However, the valid name for this species registered with the Integrated Taxonomic Information System (ITIS) and the Catalogue Of Life (COL) is still Nicrophorus pustulatus Herschel, 1807.[11][14] The original publication describing this species is available via the Biodiversity Heritage Library, with the relevant footnote on page 271.[15] The presumed holotype specimen collected by Herschel was part of the Hellwig and Hoffmannsegg insect collection purchased by the Museum für Naturkunde Berlin in 1817, and is one of many historical type specimens housed in their Beetles and Strepsiptera collection.[3][16]

Physical description

edit
 
Adult Nicrophorus pustulatus beetle found in Maryland, United States

N. pustulatus is a medium-sized beetle, averaging 14.0-22.2 mm in length. Like other beetles in the family Silphidae, it has a semi-flattened body, noticeable tibial spurs, clubbed antennae, and a distinctive elytra shape that is broader at the posterior end.[10][17] This species can be identified as part of the Nicrophorinae subfamily because of its distinctly clubbed and apparently 10-segmented antennae, as well as the shortened elytra that exposes 3-4 posterior abdominal segments.[10]

The body of N. pustulatus is shiny and predominantly black in colour, with distinctive small, orange spots on the elytra. Each elytron has one spot midway down on the lateral edge, and two smaller spots on the posterior apex.[10] These bright spots act as aposematic signals.[10] The pronotum is oval shaped, relative to the more circular pronotum seen in other Nicrophorus species.[18] Each antenna ends in a lamellate club that is divided into one basal, black segment and three terminal, orange segments. Unlike other members of the genus, N. pustulatus does not have long setae on the dorsal surface of the elytra.[10] This species has sparse, yellow to brown pubescence (hairs) on the ventral surface of the metathorax, and is glabrous on the metepimeron on the side of the metathorax.[4] N. pustulatus beetles also have a straight hind tibia with a lobe on the apex of the mesotibia,[4][19] and an entirely black epipleuron with a long epipleural ridge on the elytron extending forwards towards the scutellum.[10]

More photos of this species are available via the Maryland Biodiversity Project and iNaturalist.[20][21]

Geographic range

edit

N. pustulatus is distributed in North America. It is present in southern Canada east of the Rocky Mountains, spanning Alberta, Saskatchewan, Manitoba, Ontario, Quebec, New Brunswick, Nova Scotia, and Prince Edward Island.[4][22][23] N. pustulatus has been found as far north as near Marten Falls in the Kenora District of Ontario and Akimiski Island of Nunavut in Hudson Bay.[24] One potential observation was submitted to iNaturalist from the Saint Piere and Miquelon island, off of Newfoundland, Canada, although the presence of an N. pustulatus population in this region needs to be confirmed.[25] The range extends south in the eastern United States, from North Dakota south to Florida and the eastern region of Texas.[10][22] N. pustulatus is not currently known to occur outside of North America.[4][10][22][23]

Maps of the current distribution of N. pustulatus observations are available via iNaturalist and the Global Biodiversity Information Facility (GBIF).[22][26] The Catalogue Of Life (COL) provides a list of Canadian provinces and American states where this species is present.[14]

Habitat

edit
 
Example underground pitfall trap; pitfall traps targeting Nicrophorus beetles are baited with decomposing carrion

N. pustulatus beetles were formerly considered to be rare across their range, with unknown habitat requirements. Ground pitfall traps baited with carrion (which are typically successful for other Nicrophorus species) are ineffective at capturing this species, with N. pustulatus representing approximately 0-6% of Nicrophorus specimens caught in the traps.[5] However, recent efforts with baited traps deployed above the ground in the canopy have been much more successful at capturing this species. N. pustulatus is now believed to be a common temperate forest canopy specialist, found in mature deciduous and mixed forests across its range.[6][27] This is consistent with previous anecdotal observations of adult N. pustulatus beetles being found primarily in forests.[4]

N. pustulatus has been detected using urban, suburban, and rural forests.[28]

Life history

edit

Reproduction

edit

The reproductive strategy of N. pustulatus remained unknown for many years, and still presents several knowledge gaps. Recent research and observations point to differences between N. pustulatus and other members of the genus.[5][7]

N. pustulatus reproduces sexually, and has a variable breeding system that can include monogamy, polygyny, polyandry, or polygynandry.[29][30] In Ontario, Canada, this species is reproductively active from late April until May or June.[4][31]

Reproduction in Nicrophorus beetles centres around the use of small vertebrate carrion or other vertebrate-derived resources to raise broods of offspring. The typical reproduction process in this genus begins when adults emerge from overwintering in the spring and begin searching for suitable breeding resources via chemoreception (see Senses and communication: Chemoreception below). The beetles assess the suitability of carcasses they find by tasting and manipulating them, determining whether they are of appropriate size and freshness.[5] Nicrophorus beetles target small carcasses (such as mice or birds) that are very fresh, and have not yet been used by other insects, such as Dipterans (flies).[4] Males release pheromones to attract females. If the male has not located a carcass, the pair will mate and separate, allowing the female to use the sperm later on. If the male has found a suitable carcass, the pair may copulate repeatedly while preparing the carcass by removing hair or feathers, applying anti-microbial secretions, rounding it into a brood ball, and burying the ball underground by digging underneath it. The pair may encounter competition with conspecifics or heterospecifics during this time, along other potential mating opportunities. N. pustulatus beetles are oviparous, with the female depositing her clutch of eggs in the soil next to the carcass.[4][10]

This reproductive system describes N. pustulatus for the most part, with some unique exceptions. For example, N. pustulatus has not been known to utilize carrion or bury breeding resources underground in the wild (see Use of breeding resources below).[5][6]

Research on the related species N. vespilloides has indicated that mating pairs of beetles that are raising broods together can recognize each other using the pattern of hydrocarbons present in their cuticles.[32]

The size of the N. pustulatus brood and larvae are dependant on the size of the carcass, population density, and the age, size, and condition of the female.[30][33][34][35] N. pustulatus pairs have been known to be hyper-fecund compared to other members of the genus, raising broods of up to 187 offspring on larger carcasses in captivity.[30]

Use of breeding resources

edit

There is a remaining knowledge gap surrounding what set of breeding resources N. pustulatus uses in the wild. Unlike most Nicrophorus beetles that utilize and bury small carcasses underground, N. pustulatus appears to be capable of using a wider range of resources in unique ways. In the wild, N. pustulatus has only ever been observed successfully breeding on snake eggs (see Ecosystem roles and relationships: Parasitoidism below).[5] The species has not been observed reproducing on small carcasses in the wild (either naturally occurring or experimentally deployed); however, this may be due to experimental carcasses being placed on the ground and not in the canopy.[5][6] The forest canopy is rich in carrion resources that could potentially be used by this species, including Sciuridae (squirrel), Aves (bird), and Chiroptera (bat) sources.[6] Recent studies baiting traps with raw chicken and fish in the canopy have successfully captured N. pustulatus adults.[6] In laboratory settings, N. pustulatus buries small vertebrate carcasses (approximately mouse-sized), as is typical of the genus, but has also been found to utilize larger carcasses (approximately rat-sized).[8] In experiments offering mouse carcasses, snake eggs, and turtle eggs, N. pustulatus pairs raised broods successfully on all three and even combined resources - utilizing carrion and snake eggs at the same time.[5]

N. pustulatus beetles have also been found in association with bird nests. In one case, a Nicrophorus pustulatus beetle was observed burying live Tachycineta bicolor (tree swallow) nestlings under the substrate in a nest box at the Queen's University Biological Station (QUBS) outside Kingston, Ontario, Canada. The beetle may have initially been attracted by one dead nestling, and proceeded to bury the remaining live ones.[36] In another case, three adults were found in a failed Aegolius acadicus (northern saw-whet owl) nest.[37] As a canopy specialist, N. pustulatus may be utilizing bird nests as sources of food or sites for reproduction, and potentially even targeting fish-eating raptor nests as sources of fish carrion.[6]

Burying carrion in the canopy may not be possible, unless the beetles utilize bird nests. Further, N. pustulatus beetles do not appear to bury snake eggs when they utilize them, while they do bury small carcasses in laboratory settings. Thus, the burying behaviour that this genus and subfamily are known for may not be characteristic of N. pustulatus.[5][6]

Development

edit

N. pustulatus beetles are holometabolous and have six life stages, including the egg, first larval instar, second larval instar, third larval instar, pupal, and adult stages. The female oviposits approximately 36–72 hours after locating a suitable food source, depositing her eggs close to the carrion or reptile eggs. These eggs typically hatch within 3 days.[38] The first instar larvae crawl into the carrion or other food source after hatching and feed for approximately 12 hours, at which point they molt into the second instar through the process of ecdysis. The second larval stage lasts for approximately 24 hours, and the third for 5–15 days.[4] The third instar larvae disperse from the brooding area, wander for several days, and then and pupate for 3–4 weeks, eventually emerging as new adults after completing their metamorphosis. These adults will become sexually mature within 1 month.[38] It is thought that N. pustulatus overwinters in the adult stage, before resuming activity in the spring to reproducing.[4]

The phenology of development varies by location. In Ontario, Canada, the teneral adults emerge in late July or early August.[4]

Parental care

edit

N. pustulatus exhibits highly developed, yet partially facultative, bi-parental or uni-parental care. The parents provide obligate pre-hatching parental care by supplying food to the young; this involves procuring a suitable resource, preparing it (such as making a brood ball or opening up egg shells), pre-digesting material using oral secretions, and protecting the resource from both conspecifics and heterospecifics. Once the eggs hatch, N. pustulatus beetles provide post-hatching parental care by regurgitating food for the first instar larvae directly from their mandibles in response to larval begging, and then by preparing food for the later instars using their oral secretions. N. pustulatus parents manage the brood size to ensure the success of remaining larvae, either by controlling the number of eggs or culling the larvae according to resource availability.[10][30][39] This type of intentional cannibalism of offspring to manage for the carrying capacity on limited resources is relatively uncommon among insects.[10] Both the male and female will physically defend the young against intruders and predators, which may involve considerable risk to the parent.[39]

Post-hatching parental care is facultative in N. pustulatus because the brood can survive and develop successfully with uni-parental care, or even in the absence of post-hatching parental care. Uni-parental care can be provided by either the male or female parent, and both sexes will increase their parental investment to compensate for the loss of a mate.[10] However, the larvae of this species can successfully develop on their own after a food source has been provided and prepared by the parents.[32] N. pustulatus larvae are known to be more independent than the larvae of related species, and the larvae subsequently invest less energy in begging.[40] Because the parents and larvae must share the finite carrion or reptile eggs as a food source during the reproductive period, bi-parental care may even be costly under certain conditions. The contribution of the male to parental care is weighed against the amount of food he eats, and the female benefits energetically when the male deserts early.[41]

Lifespan

edit

The lifespan of N. pustulatus individuals in the wild has not yet been studied. Research on the related species N. orbicollis suggests that the beetles generally live for one year and reproduce only once, but may occasionally survive a second winter and reproductive season.[35]

Behaviour

edit

N. pustulatus adults are nocturnal. The adults are frequently observed around lights at night.[4]

Intraspecific competition

edit

Nicrophorus species generally compete intensely with conspecifics for access to scarce breeding resources, as carcasses are often only utilized by one pair in the wild. Breeding adults may attempt to take over the carcass of another pair, involving physical fights and infanticide. The intruders typically kill and consume most of the previous pair's larvae, but some may be raised along with the new brood.[10] Intruders may be pairs or single male or female beetles; successful single intruders typically mate with the remaining opposite-sex resident, producing their own brood. Intrusions and infanticide usually occur while the resident beetle's offspring are eggs or first instar larvae, and become less frequent when the larvae reach their second instar stage and the food source is more depleted.[39] Body size influences the outcome of competitive interactions.[42]

Food habits

edit

N. pustulatus adults and larvae are necrophagous.[10] Adult N. pustulatus beetles may consume Diptera (fly) larvae, the larvae of competitors, and carrion at carcasses, as well as other food resources such as dung and decaying fungi.[4] Carrion is consumed via extra oral digestion, by applying oral secretions containing proteinases and other enzymes and then consuming the resulting fluid.[43] Adults visit larger, more decomposed carcasses to feed before the breeding period, in contrast to the smaller, fresher food sources used for breeding.[5] N. pustulatus larvae specialize on the pre-digested carrion or other food provided by the parents.[10]

Ecosystem roles and relationships

edit

Brood parasitism

edit

N. pustulatus is known to be capable of facultative brood parasitism, targeting other Nicrophorus species. In laboratory experiments, N. pustulatus has been shown to parasitize broods of N. orbicollis, laying eggs amongst the N. orbicollis brood that are raised by the host parents.[44] Nicrophorus beetles appear to be able to detect brood parasites in some cases, but often only cull a portion of the introduced larvae and raise the others. The outcome of competition between Nicrophorus beetles over scarce carrion resources is typically determined by body size, so brood parasitism may allow N. pustulatus to benefit from carrion even when excluded by larger species (see Interspecific competition below).[45][44] This behaviour may also be adaptive because it allows N. pustulatus to benefit from the antimicrobial secretions of other Nicrophorus species (see Microbiome below).[44][46]

Parasitoidism

edit
 
Adult Pantherophis spiloides (gray ratsnake); eggs in the communal nests of these snakes are used by Nicrophorus pustulatus beetles to raise their broods

N. pustulatus is unique among beetles in the genus Nicrophorus as the only species that has been demonstrated to use the eggs of oviparous reptiles as a food source to raise larvae, in addition to carrion. This is an example of a host shift relative to the hypothesized ancestral life history of Nicrophorus beetles. N. pustulatus adults locate reptile eggs, oviposit next to the eggs, open holes in the shells, and then feed their broods from this resource - killing the eggs. The reptile eggs are otherwise alive and viable when the beetles attack them, making N. pustulatus a parasitoid.[5][8] The discovery of this host shift may have been the first scientifically published example of a true parasitoid using a vertebrate species as a host.[7][8]

 
Adult Diadophis punctatus edwardsii (northern ringneck snake); N. pustulatus beetles have been found using the eggs of this species
 
Adult Pantherophis vulpinus (foxsnake); N. pustulatus beetles have been found using the eggs of this species

In the wild, N. pustulatus has primarily been observed targeting Pantherophis spiloides (gray ratsnake) eggs.[5][8] N. pustulatus appears to target this species commonly, with the abundance of N. pustulatus individuals caught in baited traps being significantly higher close to P. spiloides hibernacula.[47] N. pustulatus has only been observed utilizing eggs in communal nests (where multiple snakes have oviposited) so far, which may be because communal nests are easier to locate or because they provide a larger amount of food.[8] There have also been individual observations of N. pustulatus beetles targeting Diadophis punctatus edwardsii (northern ringneck snake) and P. vulpinus (foxsnake) eggs.[5][8][48] In laboratory settings, N. pustulatus has successfully bred on Lamprophis fuliginosus (brown house snake) eggs. This suggests that N. pustulatus may be able to use a broad range of snake eggs, rather than behaving as a host-specific parasitoid.[5] N. pustulatus has also successfully raised broods on Chelydra serpentina (common snapping turtle) and Chrysemys picta (painted turtle) eggs in captivity, but the breeding responses to turtle eggs are less rapid and consistent than to snake eggs.[5]

It has been hypothesized that this parasitoid association evolved from brood parasitism behaviours, with adults digging into the soil to access failed reptile eggs instead of the brood ball of other species. From this point, the beetles may have evolved to utilize fresh, live eggs instead of just failed eggs.[8] Many of the same behaviours involved in breeding on carrion are applied to snake eggs, including ovipositing near the resource, regulating brood size based on resource size, and manipulating the resource (such as opening holes) to increase accessibility for larvae. At the same time, other behaviours required for carrion are no longer applied to snake eggs, such as the removal of hair, rounding into a brood ball, and burial in an underground crypt.[5] These differences suggest that the host shift to snake eggs may have adaptive benefits, given that the eggs require less energetic investment through preparation and burial and are found in large quantities in communal nests. Further, depositing beetle eggs near live snake eggs may be less risky, due to the absence of so-called "grave-soil microbes" found around decaying carcasses that can lead to beetle egg failure.[5][49] An analysis weighing the potential costs and benefits of the host shift is required.

It is unclear to what extend wild populations use reptile eggs versus carrion to breed. It is possible that N. pustulatus exhibits host shifts across its range, taking advantage of different species of reptile eggs or carrion depending on the local relative availability of these resources. For example, utilization of carrion or turtle eggs could increase in the northern part of the N. pustulatus range, where oviparous snakes are absent.[5][8]

In one experiment, N. orbicollis and N. defodiens did not respond to snake eggs with the same breeding behaviour as N. pustulatus, suggesting that the host shift may be unique to N. pustulatus.[5]

Decomposition

edit

Feeding and potentially breeding on vertebrate carrion makes N. pustulatus beetles important decomposers, contributing to nutrient cycling in the ecosystem and managing the buildup of carcasses. This may play a role in preventing the spread of diseases.[4][10]

Interspecific competition

edit

Other Nicrophorus species

edit

In regions where multiple Nicrophorus species overlap, they may be in competition with each other for limited carrion resources. In southeastern Ontario, Canada, there are seven sympatric Nicrophorus species, including N. pustulatus and N. orbicollis. These two species have overlapping habitats, breeding periods, and carrion size requirements. In laboratory experiments, N. orbicollis has been shown to be the behaviourally dominant species. N. orbicollis typically overcomes N. pustulatus in aggressive competitions for carrion resources, with its larger body size conferring an advantage in chasing, grappling, digging, and fighting.[42]

Interspecific competition for shared limiting resources is thought to have been a driving force influencing the natural histories of Nicrophorus beetles. The ecological divergence of N. pustulatus into a canopy specialist may represent spatial niche partitioning, which was selected for to reduce competition against larger and more dominant species.[6][42][31] Niche partitioning amongst Nicrophorus beetles is thought to occur via spatial partitioning in habitat specialists (such as N. pustulatus), and via temporal partitioning of breeding periods among habitat generalists.[31]

Other insects

edit

N. pustulatus can be in competition with other insects that reproduce in carrion, such as other Coleoptera (beetle) and Diptera (fly) species. Nicrophorus beetles are generally adapted to detect and monopolize breeding resources quickly before other species can get established, and to rely on mutualistic relationships with mites that eat other larvae (see Phoresy below).[10][50][51]

Vertebrates

edit

N. pustulatus is also in competition with vertebrate scavengers and predators for food resources, such as the species Corvus brachyrhynchos (American crow), Procyon lotor (raccoon), Didelphis virginiana (Virginia opossum), and Mephitis mephitis (striped skunk). Burying carrion or utilizing snake eggs pre-concealed by the ovipositing female likely helps protect the breeding resources from other species.[5][10]

Seasonal phenology

edit

As canopy specialists, N. pustulatus beetles have evolved to rely on small birds and mammals in the canopy as important sources of carrion.[31] One study in the Frontenac Arch region of Ontario, Canada found that the highest abundance of adult N. pustulatus beetles occurred during the period when most small birds and mammals species were breeding, which is when carrion would be most available due to offspring mortality. This suggests that the phenology of the life history and population dynamics in this species have evolved to coincide with the phenology of other canopy species that could provide carrion resources.[31]

Predation

edit

Reports of predation on N. pustulatus are rare.[52] Insectivorous birds likely encounter adult N. pustulatus beetles frequently around carcasses, especially for bird species that scavenge on carrion themselves.[10] N. pustulatus has been reported in the stomach of the birds Corvus brachyrhynchos (American crow) and Anas platyrhynchos (Mallard).[52] However, an experimental trial offering insects to eight species of insectivorous birds determined that birds avoid N. pustulatus and other Nicrophorus beetles as food sources. This may be due to the aposematic colouration of these beetles, warning of noxious anal secretions. The orange and black aposematic colouration has been found to be highly visible to birds.[52][53][54]

The buried carrion crypts or snake nests provide protection to N. pustulatus eggs and larvae from most predators. However, the eggs and larvae may be predated upon by species of Staphylinidae (rove beetles) or Acari (mites).[10][52] The anti-predator defences exhibited by N. pustulatus parents - including fighting off other species and producing noxious anal secretions - suggest that past predation may have been a driving factor in the evolution of this species.[10][52]

Phoresy

edit
 
Adult mite in the genus Poechilochirus

N. pustulatus has coevolved with mites, which are phoretic on the beetle hosts. Mites in their final juvenile stage grab on to the legs of adult beetles and get transported back to the food that the beetle is preparing for its offspring.[50] The mites will use the food in the beetle's brood chamber as a resource to complete their final stages of development, feeding on carrion, other insect eggs and larvae, and microorganisms. The mites either complete their development into adults and breed, leaving new mite offspring to disperse on the beetle offspring, or disperse early on the adult beetles.[50][51][55] Reducing competition with fly larvae, nematodes, and other organisms on the carrion is beneficial for the burying beetles, making this aspect of the relationship mutualistic.[50][51] However, the mites can also potentially compete for food resources or even consume the Nicrophorus beetle larvae.[56][57][58] The balance between mutualism, commensalism, and exploitation depends on the density of mites, size of the beetle brood, and other environmental conditions, although mutualism and commensalism appear to be the predominant relationship types.[50][56][57][58] N. pustulatus is known to host several species of generalist mites that associate with multiple Nicrophorus beetle hosts, and some monospecific host specialists that only engage in phoresy with this species - including some mites in the genus Poecilochirus.[50][59]

Microbiome

edit

Like other carrion beetles in the family Silphidae, N. pustulatus beetles harbour characteristic communities of bacterial and fungal endosymbionts in their gut, as well as in their oral and anal secretions.[60][61][62] This microbiome facilitates the use of carrion or similar resources to feed larvae, by helping to preserve the food, prevent colonization by other microbes, detoxify compounds found in vertebrate tissue (such as urea), and digest nutrients that would otherwise be inaccessible to the beetles.[60][61][62] Endosymbionts known to associate with the subfamily Nicrophorinae include bacteria in the groups Xanthomonadaceae, Enterobacteriaceae, Burkholderiaceae, Bacillaceae, Clostridiaceae, Bacteroidaceae, Ruminococcaceae, Lachnospiraceae, Erysipelotrichaceae, Oceanospirillaceae, and Neisseriaceae, and yeast species related to Yarrowia lipolytica.[60] The species-level composition of the microbiome varies by location.[62] Unlike other Nicrophorus species, the secretions produced by N. pustulatus do not have antimicrobial properties, which may be due to the microbial or enzymatic composition.[44][46] The lack of antimicrobial secretions may be correlated with the evolution of brood parasitism in N. pustulatus.[46]

Senses and communication

edit

Stridulation

edit

Beetles in the genus Nicrophorus all stridulate, using a stridulatory ridge on the dorsal side of the abdomen at the posterior end of the elytra.[10] The stridulatory ridge consists of two striated files on the fifth abdominal tergite, which are rasped against the underside of the elytra; this produces a series of pulses, at a frequency of approximately 300-8000 hertz.[63] These vibrations have a low amplitude and travel a short distance.[64] The characteristics of the sound do not differ between sexes, but do differ significantly between species.[64] Stridulation is used by both males and females as a form of intraspecific communication during nest preparation, copulation, and interactions with the brood.[10] Stridulation may also be used as a form of aposematic signal to defend against predators, however further experimental research confirming this is still required.[64] In addition, some species in the genus Nicrophorus are Müllerian mimics that have evolved stridulatory patterns resembling the buzzing of bumblebees, although a mimicry relationship has not yet been described in N. pustulatus.[63][65][18]

While it is known that these beetles use stridulation to communicate, the anatomical structure they use to hear those vibrations has not yet been identified. It remains unknown whether they perceive airborne sound or substrate-born vibrations.[64]

Stridulation by Nicrophorus beetles was discussed by Charles Darwin in his book, "The Descent of Man and Selection in Relation to Sex," where he hypothesized that stridulation was a secondary sexual characteristic involved in mating interactions.[66]

Chemoreception

edit

The antennal clubs of Nicrophorus beetles have sensitive chemoreceptors that can detect volatile organic compounds released by fresh carcasses, such as sulphur-containing compounds.[67][68] The chemoreceptors are a type of olfactory sensilla called sensilla coelosphaerica, which have a sac-like structure.[4][69] This allows adults to detect carcasses within one day of death, and locate them via chemotaxis from up to several kilometres away.[67] Adults generally detect olfactory cues while flying and then land in the area of the carcass to perform more sensitive chemotaxis by walking and moving their antennae back and forth, narrowing in on the precise location of a food source.[5]

Chemical communication is used by males to attract females, either to mate and separate or to mate and raise a brood together. Males perform a "head-stand" movement to expose the last abdominal segment, where glandular cells produce sex pheromones. These pheromones are similarly received by females using the antennal chemoreceptors.[10]

Vision

edit

N. pustulatus has two large compound eyes, and two small, unpigmented ocelli on the lateral portions of the head.[4] Vision has been shown to be less important for locating carcasses and mates than olfactory cues in this genus.[4][10]

Genetics

edit

Genome

edit

The genome of N. pustulatus has not yet been studied. Previous research on the related species N. vespilloides determined that the species is diploid, with six autosomes and an XO sex-determination system.[70] N. sayi is also known to have this genome structure.[71] However, further research on N. pustulatus will be required to assess whether this karyotype is shared, given that beetles exhibit considerable diversity in chromosome number and sex determination system due to chromosomal fission and fusion.[citation needed]

Genetic data

edit

Several specimen records and associated sequences are available for N. pustulatus on the Barcode of Life Database (BOLD) System database, primarily from the Centre for Biodiversity Genomics at the University of Guelph in Ontario, Canada.[72] These records all provide DNA barcode sequences from the Cytochrome C Oxidase Subunit I 5' locus of the N. pustulatus mitochondrial genome, which fall into one genetic cluster with one Barcode Index Number (BIN).[73] The National Center for Biotechnology Information (NCBI) GenBank repository also has genetic records available for this species,[74] including sequences from the mitochondrial Cytochrome C Oxidase Subunit I, nuclear protein coding CAD (carbamoylphosphate synthetase) gene, and nuclear 28S ribosomal RNA gene.[75] No reference sequences for the whole genome or individual chromosomes are currently available.[74][76]

Reference genome sequences are available for other members of the genus, including reference genomes for N. vespilloides (195.3 megabases, Mb),[70][77] N. orbicollis (192.6 Mb),[78] and N. investigator (202.3 Mb)[79] as well as the complete mitochondrial genome for N. nepalensis (17,299 base pairs, bp).[80][81]

Conservation status

edit

Unlike the critically endangered species N. americanus (American burying beetle),[82] N. pustulatus does not currently have a conservation status on the IUCN Red List,[83] or on the national conservation status lists across its range in North America - including those managed by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC)[84] and the United States Fish and Wildlife Service.[85] NatureServe ranks the species as Secure globally and within Canada.[86] Recent efforts using canopy traps targeting N. pustulatus indicate that the species may be common across its range.[6][47]

N. pustulatus is not known to be a major invasive species outside of its native range.[87]

Currently, N. pustulatus is most relevant to conservation efforts in North America as a threat to Pantherophis spiloides (gray ratsnake) and other oviparous snake populations as an egg parasitoid, leading to reduced fecundity. The beetles may destroy up to 100% of the eggs in the nests they target.[8] P. spiloides populations are currently listed as Threatened (Great Lakes/St. Lawrence population) and Endangered (Carolinian population) in Canada by COSEWIC.[88] This species does not have a listed conservation status under the United States Fish and Wildlife Service.[85]

Economic and other human importance

edit

N. pustulatus has been the focus of laboratory and field-based research studies at many academic institutions, investigating the evolution, ecology, behaviour, and biology of the species.[5][6][42][27][39][43]

N. pustulatus is not known to be a major agricultural pest, biological control agent, pet species, or vector of human disease.[89][90][91][92]

Burying carrion makes it less available to other groups of insects that breed on vertebrate carcasses; thus, utilization of carrion by N. pustulatus could help reduce the populations of noxious fly species that would otherwise breed on the carrion.[4]

Some species of carrion beetles are useful in forensic applications, as the post-mortem interval can be estimated based on the type and developmental stage of the larvae on a body.[93] N. pustulatus may be an informative species for forensic entomology because it has been known to colonize large vertebrate carcasses. This species was observed on Sus scrofa L. (domestic pig) carcasses in a study by the Canadian Police Research Centre investigating potential arthropod succession on human bodies.[94]

See also

edit

References

edit
  1. ^ DeMarco, Kestrel V.B.; Martin, Paul R. (28 November 2020). "A case of a Pustulated Carrion Beetle (Nicrophorus pustulatus, Coleoptera: Silphidae) burying live Tree Swallow (Tachycineta bicolor, Passeriformes: Hirundinidae) nestlings under the nest". The Canadian Field-Naturalist. 134 (3): 217–221. doi:10.22621/cfn.v134i3.2369.
  2. ^ "Common Names - Wild Species: The General Status of Species in Canada". www.wildspecies.ca. Retrieved 2024-02-03.
  3. ^ a b c Prena, Jens (2023). "Nomenclatural notes on two species of Nicrophorus FABRICIUS (Coleoptera, Staphylinidae, Silphinae, Nicrophorini) named in a publication authored by Johann Dietrich Herschel". Linzer biologische Beiträge. 54 (2022): 621–624. doi:10.35011/LBB.54.2-42.
  4. ^ a b c d e f g h i j k l m n o p q r s Agriculture Canada, Public Services and Procurement Canada; Anderson, Robert S.; Peck, Stewart B. (1985). "The Insects and Arachnids of Canada - Part 13 - The Carrion Beetles of Canada and Alaska" (PDF). publications.gc.ca. Retrieved 2024-03-28.
  5. ^ a b c d e f g h i j k l m n o p q r s t u v Smith, G.; Trumbo, S. T.; Sikes, D. S.; Scott, M. P.; Smith, R. L. (November 2007). "Host shift by the burying beetle, Nicrophorus pustulatus , a parasitoid of snake eggs". Journal of Evolutionary Biology. 20 (6): 2389–2399. doi:10.1111/j.1420-9101.2007.01404.x. PMID 17956400.
  6. ^ a b c d e f g h i j k Wettlaufer, Jillian D.; Burke, Kevin W.; Schizkoske, Adam; Beresford, David V.; Martin, Paul R. (15 November 2018). "Ecological divergence of burying beetles into the forest canopy". PeerJ. 6: e5829. doi:10.7717/peerj.5829. PMC 6240436. PMID 30479886.
  7. ^ a b c d Sikes, Derek S.; Madge, Ronald B.; Newton, Alfred F. (29 August 2002). "A catalog of the Nicrophorinae (Coleoptera: Silphidae) of the world". Zootaxa. 65 (1): 1. doi:10.11646/zootaxa.65.1.1.
  8. ^ a b c d e f g h i j Blouin-Demers, Gabriel; Weatherhead, Patrick J. (2000). "A novel association between a beetle and a snake: Parasitism of Elaphe obsoleta by Nicrophorus pustulatus". Écoscience. 7 (4): 395–397. Bibcode:2000Ecosc...7..395B. doi:10.1080/11956860.2000.11682609. ISSN 1195-6860.
  9. ^ Eggleton, Paul; Belshaw, Robert (1992). "Insect Parasitoids: An Evolutionary Overview". Philosophical Transactions: Biological Sciences. 337 (1279): 1–20. doi:10.1098/rstb.1992.0079. ISSN 0962-8436. JSTOR 57087.
  10. ^ a b c d e f g h i j k l m n o p q r s t u v w x y z LaBonte, James R. (1997-05-01). "The Carrion Beetles (Coleoptera: Silphidae) of Nebraska". Annals of the Entomological Society of America. 90 (3): 399. doi:10.1093/aesa/90.3.399. ISSN 1938-2901.
  11. ^ a b "ITIS - Report: Nicrophorus pustulatus". www.itis.gov. Retrieved 2024-03-28.
  12. ^ a b c Sikes, Derek S.; Venables, Chandra (2013). "Molecular phylogeny of the burying beetles (Coleoptera: Silphidae: Nicrophorinae)". Molecular Phylogenetics and Evolution. 69 (3): 552–565. doi:10.1016/j.ympev.2013.07.022. ISSN 1055-7903. PMID 23911726.
  13. ^ "TimeTree :: The Timescale of Life". timetree.org. Retrieved 2024-04-11.
  14. ^ a b "Nicrophorus (Nicrophorus) pustulatus (Herschel, 1807) | COL". www.catalogueoflife.org. Retrieved 2024-04-11.
  15. ^ Illiger, Johann Karl Wilhelm (1807). Magazin für Insektenkunde. Vol. Bd.6 (1807) [1856 reprint]. Braunschweig: Karl Reichard.
  16. ^ Museum für Naturkunde Berlin. "Beetles and Strepsiptera". Museum für Naturkunde - Our Science. Retrieved 2024-03-28.
  17. ^ McCain, Christy M.; Monk, Emily; Hinson, Kevin; Szewczyk, Tim; D'Oench, Holly (2021). "Key to the carrion beetles (Silphidae) of Colorado & neighboring states" (PDF). University of Colorado Boulder Department of Ecology & Evolutionary Biology. Retrieved 2024-03-29.
  18. ^ a b Milne, Lorus J.; Milne, Margery J. (1944). "Notes on the Behavior of Burying Beetles (Nicrophorus spp.)". Journal of the New York Entomological Society. 52 (4): 311–327. ISSN 0028-7199. JSTOR 25005075.
  19. ^ Sikes, Derek S.; Peck, Stewart B. (2000-05-01). "Description of Nicrophorus hispaniola, New Species, from Hispaniola (Coleoptera: Silphidae) and a Key to the Species of Nicrophorus of the New World". Annals of the Entomological Society of America. 93 (3): 391–397. doi:10.1603/0013-8746(2000)093[0391:DONHNS]2.0.CO;2.
  20. ^ "Maryland Biodiversity Project - Nicrophorus pustulatus". www.marylandbiodiversity.com. Retrieved 2024-03-31.
  21. ^ "Photos of Pustulated Carrion Beetle (Nicrophorus pustulatus) · iNaturalist Canada". iNaturalist Canada. Retrieved 2024-04-02.
  22. ^ a b c d Global Biodiversity Information Facility (GBIF). "Nicrophorus pustulatus (Herschel, 1807)". www.gbif.org. Retrieved 2024-03-28.
  23. ^ a b Agriculture Canada; Bousquet, Yves (1991). "Checklist of Beetles of Canada and Alaska" (PDF). publications.gc.ca. Retrieved 2024-03-28.
  24. ^ Ringrose, J. L.; Langer, Sarah Victoria Louise; Fleming, Kaitlyn Julia; Burt, Trevor O.; Bourne, D. R.; Brand, R.; Beresford, David V. (2019). "Burying Beetles of the Genus Nicrophorus Fabricius (Coleoptera: Silphidae) from Northern Ontario and Akimiski Island, Nunavut". Journal of the Entomological Society of Ontario. 150: 1–10 – via ResearchGate.
  25. ^ Gaspard, Mylène (2018-09-03). "Pustulated Carrion Beetle (Nicrophorus pustulatus)". iNaturalist Canada. Retrieved 2024-03-31.
  26. ^ "Pustulated Carrion Beetle (Nicrophorus pustulatus)". iNaturalist Canada. Retrieved 2024-04-02.
  27. ^ a b Ulyshen, Michael D.; Hanula, James L.; Horn, Scott (March 2007). "Burying beetles (Coleoptera: Silphidae) in the forest canopy: The unusual case of Nicrophorus pustulatus Herschel". The Coleopterists Bulletin. 61 (1): 121–123. doi:10.1649/924.1. S2CID 84153329.
  28. ^ Fusco, Nicole A.; Zhao, Anthony; Munshi-South, Jason (2017-03-15). "Urban forests sustain diverse carrion beetle assemblages in the New York City metropolitan area". PeerJ. 5: e3088. doi:10.7717/peerj.3088. ISSN 2167-8359. PMC 5356479. PMID 28316891.
  29. ^ Trumbo, Stephen T.; Eggert, Anne-Katrin (1994-11-01). "Beyond monogamy: territory quality influences sexual advertisement in male burying beetles". Animal Behaviour. 48 (5): 1043–1047. doi:10.1006/anbe.1994.1337. ISSN 0003-3472.
  30. ^ a b c d Trumbo, Stephen T. (1992). "Monogamy to communal breeding: exploitation of a broad resource base by burying beetles (Nicrophorus)". Ecological Entomology. 17 (3): 289–298. Bibcode:1992EcoEn..17..289T. doi:10.1111/j.1365-2311.1992.tb01060.x. ISSN 0307-6946.
  31. ^ a b c d e Wettlaufer, J.D.; Burke, K.W.; Beresford, D.V.; Martin, P.R. (2021). "Partitioning resources through the seasons: abundance and phenology of carrion beetles (Silphidae) in southeastern Ontario, Canada". Canadian Journal of Zoology. 99 (11): 961–973. doi:10.1139/cjz-2021-0081. hdl:1807/107765. ISSN 0008-4301.
  32. ^ a b Rauter, Claudia M.; Moore, Allen J. (2007). "Quantitative genetics of growth and development time in the burying beetle Nicrophorus pustulatus in the presence and absence of post-hatching parental care". Evolution: International Journal of Organic Evolution. 56 (1): 96–110. doi:10.1111/j.0014-3820.2002.tb00852.x. PMID 11913669 – via WILEY Online Library.
  33. ^ Rauter, Claudia M.; Mcguire, Michael J.; Gwartney, Melissa M.; Space, Jason E. (2010). "Effect of Population Density and Female Body Size on Number and Size of Offspring in a Species with Size-Dependent Contests over Resources". Ethology. 116 (2): 120–128. Bibcode:2010Ethol.116..120R. doi:10.1111/j.1439-0310.2009.01720.x. ISSN 0179-1613.
  34. ^ Steiger, Sandra; Richter, Katja; Müller, Josef K.; Eggert, Anne-Katrin (2007). "Maternal nutritional condition and genetic differentiation affect brood size and offspring body size in Nicrophorus". Zoology. 110 (5): 360–368. doi:10.1016/j.zool.2007.06.001. ISSN 0944-2006. PMID 17702555.
  35. ^ a b Trumbo, Stephen T. (2009). "Age-related reproductive performance in the parental burying beetle, Nicrophorus orbicollis". Behavioral Ecology. 20 (5): 951–956. doi:10.1093/beheco/arp082. ISSN 1465-7279.
  36. ^ DeMarco, Kestrel V.B.; Martin, Paul R. (2020-11-28). "A case of a Pustulated Carrion Beetle (Nicrophorus pustulatus, Coleoptera: Silphidae) burying live Tree Swallow (Tachycineta bicolor, Passeriformes: Hirundinidae) nestlings under the nest". The Canadian Field-Naturalist. 134 (3): 217–221. doi:10.22621/cfn.v134i3.2369. ISSN 0008-3550.
  37. ^ Academy of Natural Sciences of Philadelphia.; Philadelphia, Academy of Natural Sciences of; Society, American Entomological (1983). Entomological news. Vol. v.94-95 (1983-1984). [Philadelphia]: American Entomological Society. pp. 60–64.
  38. ^ a b Rauter, C. M.; Moore, A. J. (2002-05-01). "Evolutionary importance of parental care performance, food resources, and direct and indirect genetic effects in a burying beetle". Journal of Evolutionary Biology. 15 (3): 407–417. doi:10.1046/j.1420-9101.2002.00412.x. ISSN 1010-061X.
  39. ^ a b c d Trumbo, Stephen T. (6 August 2007). "Defending young biparentally: female risk-taking with and without a male in the burying beetle, Nicrophorus pustulatus". Behavioral Ecology and Sociobiology. 61 (11): 1717–1723. doi:10.1007/s00265-007-0403-5. S2CID 26073189.
  40. ^ Capodeanu-Nägler, Alexandra; Eggert, Anne-Katrin; Vogel, Heiko; Sakaluk, Scott K.; Steiger, Sandra (2018). "Species divergence in offspring begging and parental provisioning is linked to nutritional dependency". Behavioral Ecology. 29 (1): 42–50. doi:10.1093/beheco/arx117 – via Oxford Academic.
  41. ^ Keppner, Eva M.; Ayasse, Manfred; Steiger, Sandra (2020). "Contribution of males to brood care can compensate for their food consumption from a shared resource". Ecology and Evolution. 10 (7): 3535–3543. Bibcode:2020EcoEv..10.3535K. doi:10.1002/ece3.6150. ISSN 2045-7758. PMC 7141021. PMID 32274007.
  42. ^ a b c d Vangenne, Yohanna D.; Sheppard, Brendan; Martin, Paul R. (23 November 2023). "Behavioral dominance interactions between two species of burying beetles (Nicrophorus orbicollis and Nicrophorus pustulatus)". PeerJ. 11: e16090. doi:10.7717/peerj.16090. PMC 10676716. PMID 38025751.
  43. ^ a b Ayala-Ortiz, Christian O.; Farriester, Jacob W.; Pratt, Carrie J.; Goldkamp, Anna K.; Matts, Jessica; Hoback, W. Wyatt; Gustafson, John E.; Hagen, Darren E. (23 September 2021). "Effect of food source availability in the salivary gland transcriptome of the unique burying beetle Nicrophorus pustulatus (Coleoptera: Silphidae)". PLOS ONE. 16 (9): e0255660. Bibcode:2021PLoSO..1655660A. doi:10.1371/journal.pone.0255660. PMC 8460033. PMID 34555059.
  44. ^ a b c d Trumbo, Stephen T. (1994). "Interspecific Competition, Brood Parasitism, and the Evolution of Biparental Cooperation in Burying Beetles". Oikos. 69 (2): 241–249. Bibcode:1994Oikos..69..241T. doi:10.2307/3546144. JSTOR 3546144.
  45. ^ Smith, Ashlee N.; Belk, Mark C. (2018-03-05). "Evidence for Interspecific Brood Parasite Detection and Removal in Burying Beetles". Psyche: A Journal of Entomology. 2018: e2712945. doi:10.1155/2018/2712945. ISSN 0033-2615.
  46. ^ a b c Hoback, W. Wyatt; Bishop, Andrew A.; Kroemer, Jeremy; Scalzitti, Joanne; Shaffer, Julie J. (April 2004). "Differences Among Antimicrobial Properties of Carrion Beetle Secretions Reflect Phylogeny and Ecology". Journal of Chemical Ecology. 30 (4): 719–729. Bibcode:2004JCEco..30..719H. doi:10.1023/B:JOEC.0000028427.53141.41. PMID 15260219. S2CID 23754749.
  47. ^ a b Brown, Michael G. C.; Beresford, D. V. (2016). "Unusually High Trap Catches of a Snake Egg Parasitoid, Nicrophorus pustulatus (Coleoptera: Silphidae) in the Frontenac Axis Population of Gray Ratsnake Pantherophis spiloides". Canadian Wildlife Biology & Management. 5 (2): 25–31.
  48. ^ LeGros, David L.; Pratt, Shane; Beresford, David V. (2010). "Burying Beetles as Parasitoids of Northern Ringneck Snakes". IRCF Reptiles & Amphibians. 17 (4).
  49. ^ Jacobs, Chris G C; Wang, Yin; Vogel, Heiko; Vilcinskas, Andreas; van der Zee, Maurijn; Rozen, Daniel E (2014). "Egg survival is reduced by grave-soil microbes in the carrion beetle, Nicrophorus vespilloides". BMC Evolutionary Biology. 14 (1): 208. Bibcode:2014BMCEE..14..208J. doi:10.1186/s12862-014-0208-x. ISSN 1471-2148. PMC 4189599. PMID 25260512.
  50. ^ a b c d e f Canitz, Julia; Sikes, Derek S.; Knee, Wayne; Baumann, Julia; Haftaro, Petra; Steinmetz, Nadine; Nave, Martin; Eggert, Anne-Katrin; Hwang, Wenbe; Nehring, Volker (January 2022). "Cryptic diversity within the Poecilochirus carabi mite species complex phoretic on Nicrophorus burying beetles: Phylogeny, biogeography, and host specificity". Molecular Ecology. 31 (2): 658–674. Bibcode:2022MolEc..31..658C. doi:10.1111/mec.16248. ISSN 0962-1083. PMID 34704311.
  51. ^ a b c Wilson, David Sloan; Knollenberg, W. G. (April 1987). "Adaptive indirect effects: the fitness of burying beetles with and without their phoretic mites". Evolutionary Ecology. 1 (2): 139–159. Bibcode:1987EvEco...1..139W. doi:10.1007/BF02067397. ISSN 1573-8477.
  52. ^ a b c d e Young, Orrey P. (2014). "Vertebrate Predation on Silphidae (Coleoptera): A Literature Review". The Coleopterists Bulletin. 68 (2): 221–234. doi:10.1649/0010-065X-68.2.221. ISSN 0010-065X. JSTOR 24773351.
  53. ^ Jones, Frank Morton (1934). "Further Experiments on Colouration and Relative Acceptability of Insects to Birds". Transactions of the Royal Entomological Society of London. 82 (2): 443–453. doi:10.1111/j.1365-2311.1934.tb00039.x. ISSN 0035-8894.
  54. ^ Lindstedt, Carita; Boncoraglio, Giuseppe; Cotter, Sheena; Gilbert, James; Kilner, Rebecca M (2017-08-22). "Aposematism in the burying beetle? Dual function of anal fluid in parental care and chemical defense". Behavioral Ecology. 28 (6): 1414–1422. doi:10.1093/beheco/arx100. ISSN 1045-2249.
  55. ^ Schwarz, Horst H.; Koulianos, Stella (August 1998). "Review. When to leave the brood chamber? Routes of dispersal in mites associated with burying beetles". Experimental & Applied Acarology. 22 (11): 621–631. doi:10.1023/A:1006054604520. ISSN 1572-9702.
  56. ^ a b De Gasperin, Ornela; Kilner, Rebecca M. (23 September 2015). "Friend or foe: inter-specific interactions and conflicts of interest within the family". Ecological Entomology. 40 (6): 787–795. Bibcode:2015EcoEn..40..787D. doi:10.1111/een.12259. ISSN 0307-6946. PMC 4678582. PMID 26681822.
  57. ^ a b Nehring, Volker; Teubner, Heide; König, Sandra (September 2019). "Dose-independent virulence in phoretic mites that parasitize burying beetles". International Journal for Parasitology. 49 (10): 759–767. doi:10.1016/j.ijpara.2019.05.011. ISSN 0020-7519. PMID 31401062.
  58. ^ a b Schedwill, Petra; Paschkewitz, Sophia; Teubner, Heide; Steinmetz, Nadine; Nehring, Volker (21 January 2020). "From the host's point of view: Effects of variation in burying beetle brood care and brood size on the interaction with parasitic mites". PLOS ONE. 15 (1): e0228047. Bibcode:2020PLoSO..1528047S. doi:10.1371/journal.pone.0228047. ISSN 1932-6203. PMC 6974135. PMID 31961905.
  59. ^ Knee, Wayne (2017-12-12). "New Macrocheles species (Acari, Mesostigmata, Macrochelidae) associated with burying beetles (Silphidae, Nicrophorus) in North America". ZooKeys (721): 1–32. Bibcode:2017ZooK..721....1K. doi:10.3897/zookeys.721.21747. ISSN 1313-2970. PMC 5740451. PMID 29308022.
  60. ^ a b c Kaltenpoth, Martin; Steiger, Sandra (March 2014). "Unearthing carrion beetles' microbiome: characterization of bacterial and fungal hindgut communities across the Silphidae". Molecular Ecology. 23 (6): 1251–1267. Bibcode:2014MolEc..23.1251K. doi:10.1111/mec.12469. PMID 24102980. S2CID 20734302.
  61. ^ a b Pratt, Carrie J. (May 2021). Bacterial communities in carrion and burying beetle (Silphidae) secretions (Thesis). hdl:11244/330942.[page needed]
  62. ^ a b c Pratt, Carrie J.; Meili, Casey H.; Youssef, Noha H.; Hoback, W. Wyatt (12 December 2023). "Culture-independent analyses of carrion beetle (Coleoptera: Silphidae) secretion bacterial communities". Microbiology Spectrum. 11 (6): e0169423. doi:10.1128/spectrum.01694-23. PMC 10714842. PMID 37874151.
  63. ^ a b Lane, Charles; Rothschild, Miriam (1965). "A case of Müllerian mimicry of sound". Proceedings of the Royal Entomological Society of London. Series A, General Entomology. 40 (10–12): 156–158. doi:10.1111/j.1365-3032.1965.tb00305.x. ISSN 0375-0418.
  64. ^ a b c d Hall, Carrie L.; Mason, Andrew C.; Howard, Daniel R.; Padhi, Abinash; Smith, Rosemary J. (2013-09-01). "Description of Acoustic Characters and Stridulatory Pars Stridens of Nicrophorus (Coleoptera: Silphidae): A Comparison of Eight North American Species". Annals of the Entomological Society of America. 106 (5): 661–669. doi:10.1603/AN13001 – via Oxford Academic.
  65. ^ Fisher, Richard M.; Tuckerman, Robert D. (1986). "Mimicry of Bumble Bees and Cuckoo Bumble Bees by Carrion Beetles (Coleoptera: Silphidae)". Journal of the Kansas Entomological Society. 59 (1): 20–25. ISSN 0022-8567. JSTOR 25084730.
  66. ^ Darwin, Charles, ed. (2009), "Secondary Sexual Characters of Insects", The Descent of Man and Selection in Relation to Sex, Cambridge Library Collection - Darwin, Evolution and Genetics, vol. 1, Cambridge: Cambridge University Press, pp. 341–385, doi:10.1017/cbo9780511703829.011, ISBN 978-1-108-00509-8, retrieved 2024-03-29
  67. ^ a b Degenkolb, Thomas; Düring, Rolf-Alexander; Vilcinskas, Andreas (2011-07-01). "Secondary Metabolites Released by The Burying Beetle Nicrophorus vespilloides: Chemical Analyses and Possible Ecological Functions". Journal of Chemical Ecology. 37 (7): 724–735. Bibcode:2011JCEco..37..724D. doi:10.1007/s10886-011-9978-4. ISSN 1573-1561. PMID 21667150.
  68. ^ Kalinová, B.; Podskalská, H.; Růžička, J.; Hoskovec, M. (2009). "Irresistible bouquet of death—how are burying beetles (Coleoptera: Silphidae: Nicrophorus) attracted by carcasses". Naturwissenschaften. 96 (8): 889–899. Bibcode:2009NW.....96..889K. doi:10.1007/s00114-009-0545-6. ISSN 0028-1042. PMID 19404598.
  69. ^ Ernst, Klaus-Dieter (1972-03-01). "Sensillum coelosphaericum, die Feinstruktur eines neuen olfaktorischen Sensillentyps". Zeitschrift für Zellforschung und Mikroskopische Anatomie (in German). 132 (1): 95–106. doi:10.1007/BF00310299. ISSN 1432-0878.
  70. ^ a b Cunningham, Christopher B.; Ji, Lexiang; Wiberg, R. Axel W.; Shelton, Jennifer; McKinney, Elizabeth C.; Parker, Darren J.; Meagher, Richard B.; Benowitz, Kyle M.; Roy-Zokan, Eileen M.; Ritchie, Michael G.; Brown, Susan J.; Schmitz, Robert J.; Moore, Allen J. (2015). "The Genome and Methylome of a Beetle with Complex Social Behavior, Nicrophorus vespilloides (Coleoptera: Silphidae)". Genome Biology and Evolution. 7 (12): 3383–3396. doi:10.1093/gbe/evv194. ISSN 1759-6653. PMC 4700941. PMID 26454014.
  71. ^ Vorontsov, N. N.; Yadav, J. S.; Lyapunova, E. A.; Korablev, V. P.; Yanina, I. Yu. (1984-01-01). "Comparative karyology of seven species of staphylinoid beetles (Polyphaga: Coleoptera)". Genetica. 63 (2): 153–159. doi:10.1007/BF00605900. ISSN 1573-6857.
  72. ^ Barcode of Life Database (BOLD). "Taxonomy Browser: Nicrophorus pustulatus". BOLDSYSTEMS. Retrieved 2024-03-28.
  73. ^ Barcode of Life Database (BOLD). "Public Data Portal - Record List: Nicrophorus pustulatus". BOLDSYSTEMS. Retrieved 2024-03-28.
  74. ^ a b National Center for Biotechnology Information. "Nicrophorus pustulatus". NCBI Taxonomy. Retrieved 2024-03-28.
  75. ^ National Center for Biotechnology Information. "Nicrophorus pustulatus - txid483347[organism:exp]". NCBI Nucleotide. Retrieved 2024-03-28.
  76. ^ National Center for Biotechnology Information (NCBI). "Genome - Nicrophorus". NCBI Genome. Retrieved 2024-03-28.
  77. ^ National Center for Biotechnology Information (NCBI). "Nicrophorus vespilloides genome assembly Nicve_v1.0". NCBI Genome. Retrieved 2024-03-28.
  78. ^ National Center for Biotechnology Information (NCBI). "Nicrophorus orbicollis genome assembly ASM1884563v1". NCBI Genome. Retrieved 2024-03-28.
  79. ^ National Center for Biotechnology Information (NCBI). "Nicrophorus investigator genome assembly icNicInve2.1". NCBI Genome. Retrieved 2024-03-28.
  80. ^ National Center for Biotechnology Information (NCBI) (30 March 2021). "Nicrophorus nepalensis voucher GZUTCM:003 mitochondrion, complete genome". NCBI Nucleotide. Retrieved 2024-03-28.
  81. ^ Cai, Yanpeng; Li, Xiaoyan (2021-06-03). "The complete mitochondrial genome of a burying beetle, Nicrophorus nepalensis Hope, 1831 (Coleoptera: Silphidae)". Mitochondrial DNA Part B. 6 (6): 1727–1728. doi:10.1080/23802359.2021.1930220. ISSN 2380-2359. PMC 8158231. PMID 34104752.
  82. ^ International Union for Conservation of Nature. "American Burying Beetle (Nicrophorus americanus)". The IUCN Red List of Threatened Species. Retrieved 2024-03-28.
  83. ^ International Union for Conservation of Nature (2023). "Search - Nicrophorus". The IUCN Red List of Threatened Species. Retrieved 2024-03-28.
  84. ^ "Species at risk registry". species-registry.canada.ca. Retrieved 2024-03-28.
  85. ^ a b "Listed Animals". ecos.fws.gov. Retrieved 2024-03-28.
  86. ^ NatureServe. "NatureServe Explorer 2.0 - Nicrophorus pustulatus - Blistered Burying Beetle". NatureServe Explorer. Retrieved 2024-03-28.
  87. ^ Invasive Species Specialist Group (ISSG) (2011-11-20). "Global Invasive Species Database (GISD)". Global Biodiversity Information Facility: Checklist Dataset. doi:10.15468/aaobov. Retrieved 2024-03-28.
  88. ^ Canada, Environment and Climate Change (2018-12-13). "Gray Ratsnake (Pantherophis spiloides): COSEWIC assessment and status report 2018". www.canada.ca. Retrieved 2024-03-28.
  89. ^ "List of pests regulated by Canada". Canadian Food Inspection Agency. 14 March 2013.
  90. ^ United States Department of Agriculture. "Pests and Diseases". Animal and Plant Health Inspection Service. Retrieved 2024-02-26.
  91. ^ "Import and release of biological control agents into Canada". Canadian Food Inspection Agency. 5 January 2018.
  92. ^ Oregon Department of Agriculture (2017). "Oregon Approved Invertebrate List" (PDF). Retrieved 2024-02-26.
  93. ^ Byrd, Jason H.; Castner, James L., eds. (2009). Forensic Entomology. doi:10.1201/noe0849392153. ISBN 978-0-367-80569-2.
  94. ^ Canadian Police Research Centre; Gill, Ginger Julie (2005). "Technical Report TR-06-2005 - Decomposition and Arthropod Succession on Above Ground Pig Carrion in Rural Manitoba" (PDF). publications.gc.ca. Retrieved 2024-02-26.
Retrieved from "https://en.wikipedia.org/w/index.php?title=Nicrophorus_pustulatus&oldid=1256842513"