Nicrophorus pustulatus

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Nicrophorus pustulatus
Nicrophorus pustulatus (1 of 1).jpg
Adult Nicrophorus pustulatus beetle, with phoretic mites
Scientific classification OOjs UI icon edit-ltr.svg
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] pustulatusIlliger in Herschel, 1808
  • Necrophorus [sic] bicolonNewman, 1838
  • Necrophorus [sic] tardusMannerheim, 1853
  • Necrophorus [sic] marginatus fasciatusPortevin, 1924
  • Necrophorus [sic] marginatus unicolorPortevin, 1924

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]

Contents

Taxonomy

Phylogeny

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

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

Adult Nicrophorus pustulatus beetle found in Maryland, United States Nicrophorus pustulatus SERC 06-06-15 0094 (18242687514).jpg
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

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

Example underground pitfall trap; pitfall traps targeting Nicrophorus beetles are baited with decomposing carrion Beetle pitfall trap with stones.png
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

Reproduction

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

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

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

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

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

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

Intraspecific competition

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

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

Brood parasitism

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

Adult Pantherophis spiloides (gray ratsnake); eggs in the communal nests of these snakes are used by Nicrophorus pustulatus beetles to raise their broods Gray Ratsnake (Pantherophis spiloides) (43567652625).jpg
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 Diadophis punctatus edwardsii crop.jpg
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 Western Fox Snake 04.jpg
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

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

Other Nicrophorus species

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

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

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

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

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. [53] [54] [55]

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

Adult mite in the genus Poechilochirus Poecilochirus sp. 01.JPG
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] [56] 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. [57] [58] [59] 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] [57] [58] [59] 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] [60]

Microbiome

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. [61] [62] [63] 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. [61] [62] [63] 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. [61] The species-level composition of the microbiome varies by location. [63] 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

Stridulation

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. [64] These vibrations have a low amplitude and travel a short distance. [65] The characteristics of the sound do not differ between sexes, but do differ significantly between species. [65] 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. [65] 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. [64] [66] [67]

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. [65]

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. [68]

Chemoreception

The antennal clubs of Nicrophorus beetles have sensitive chemoreceptors that can detect volatile organic compounds released by fresh carcasses, such as sulphur-containing compounds. [69] [70] The chemoreceptors are a type of olfactory sensilla called sensilla coelosphaerica, which have a sac-like structure. [4] [71] This allows adults to detect carcasses within one day of death, and locate them via chemotaxis from up to several kilometres away. [69] 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

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

Genome

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. [72] [73] N. sayi is also known to have this genome structure. [74] 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. [72]

Genetic data

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. [75] 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). [76] The National Center for Biotechnology Information (NCBI) GenBank repository also has genetic records available for this species, [77] including sequences from the mitochondrial Cytochrome C Oxidase Subunit I, nuclear protein coding CAD (carbamoylphosphate synthetase) gene, and nuclear 28S ribosomal RNA gene. [78] No reference sequences for the whole genome or individual chromosomes are currently available. [77] [79]

Reference genome sequences are available for other members of the genus, including reference genomes for N. vespilloides (195.3 megabases, Mb), [73] [80] N. orbicollis (192.6 Mb), [81] and N. investigator (202.3 Mb) [82] as well as the complete mitochondrial genome for N. nepalensis (17,299 base pairs, bp). [83] [84]

Conservation status

Unlike the critically endangered species N. americanus (American burying beetle), [85] N. pustulatus does not currently have a conservation status on the IUCN Red List, [86] 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) [87] and the United States Fish and Wildlife Service. [88] NatureServe ranks the species as Secure globally and within Canada. [89] 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. [90]

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. [91] This species does not have a listed conservation status under the United States Fish and Wildlife Service. [88]

Economic and other human importance

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. [92] [93] [94] [95]

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. [96] 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. [97]

See also

Related Research Articles

<span class="mw-page-title-main">Forensic entomology</span> Application of insect and other arthropod biology to forensics

Forensic entomology is an science study of colonization of a dead body by arthropods. This includes the study of insect types commonly associated with cadavers, their respective life cycles, their ecological presences in a given environment, as well as the changes in insect assemblage with the progression of decomposition. Insect succession patterns are identified based on the time a given species of insect spends in a given developmental stage, and how many generations have been produced since the insects introduction to a given food source. Insect development alongside environmental data such as temperature and vapor density, can be used to estimate the time since death, due to the fact that flying insects are attracted to a body immediately after death. The identification of postmortem interval to aid in death investigations is the primary scope of this scientific field. However, forensic entomology is not limited to homicides, it has also been used in cases of neglect and abuse, in toxicology contexts to detect the presence of drugs, and in dry shelf food contamination incidents. Equally, insect assemblages present on a body, can be used to approximate a given location, as certain insects may be unique to certain areas. Therefore, forensic entomology can be divided into three subfields: urban, stored-product and medico-legal/medico-criminal entomology.

<span class="mw-page-title-main">Silphidae</span> Family of beetles

Silphidae is a family of beetles that are known commonly as large carrion beetles, carrion beetles or burying beetles. There are two subfamilies: Silphinae and Nicrophorinae. Members of Nicrophorinae are sometimes known as burying beetles or sexton beetles. The number of species is relatively small, at around two hundred. They are more diverse in the temperate region although a few tropical endemics are known. Both subfamilies feed on decaying organic matter such as dead animals. The subfamilies differ in which uses parental care and which types of carcasses they prefer. Silphidae are considered to be of importance to forensic entomologists because when they are found on a decaying body they are used to help estimate a post-mortem interval.

<span class="mw-page-title-main">Burying beetle</span> Genus of beetles

Burying beetles or sexton beetles, genus Nicrophorus, are the best-known members of the family Silphidae. Most of these beetles are black with red markings on the elytra (forewings). Burying beetles are true to their name—they bury the carcasses of small vertebrates such as birds and rodents as a food source for their larvae, this makes them carnivorous. They are unusual among insects in that both the male and female parents take care of the brood.

<span class="mw-page-title-main">Trogidae</span> Family of beetles

Trogidae, sometimes called hide beetles, is a family of beetles with a distinctive warty or bumpy appearance. Found worldwide, the family includes about 300 species contained in four or five genera.

<i>Nicrophorus americanus</i> Species of beetle

Nicrophorus americanus, also known as the American burying beetle or giant carrion beetle, is a critically endangered species of beetle endemic to North America. It belongs to the order Coleoptera and the family Silphidae. The carrion beetle in North America is carnivorous, feeds on carrion and requires carrion to breed. It is also a member of one of the few genera of beetle to exhibit parental care. The decline of the American burying beetle has been attributed to habitat loss, alteration, and degradation, and they now occur in less than 10% of their historic range.

Forensic entomological decomposition is how insects decompose and what that means for timing and information in criminal investigations. Medicolegal entomology is a branch of forensic entomology that applies the study of insects to criminal investigations, and is commonly used in death investigations for estimating the post-mortem interval (PMI). One method of obtaining this estimate uses the time and pattern of arthropod colonization. This method will provide an estimation of the period of insect activity, which may or may not correlate exactly with the time of death. While insect successional data may not provide as accurate an estimate during the early stages of decomposition as developmental data, it is applicable for later decompositional stages and can be accurate for periods up to a few years.

<i>Nicrophorus vespilloides</i>

Nicrophorus vespilloides is a burying beetle described by Johann Friedrich Wilhelm Herbst in 1783. The beetles vary widely in size and can present with a range of anywhere from 12 mm to 20 mm in size. They have two conspicuous orange-yellow bands on the elytra. The color of the antennae are an important distinguishing feature, being totally black. The color of their orange and black markings is multifunctional, as they are conspicuous to avian predators. In general, they present a unique ecological niche, which is their evolution of aposematism, or the strategy they use to warn predators through their conspicuous signals. The wing cases of these beetles possess a squarish shape and are notably shorter in length than their abdomens, indicating a distinct physical characteristic of the species.

<i>Nicrophorus tomentosus</i> Species of beetle

Nicrophorus tomentosus is a species of burying beetle that was described by Friedrich Weber in 1801. The beetle belongs to the family Silphidae which are carrion beetles. The beetles have sensitive antennae that contain olfactory organs. Thus, the beetle can locate dead animals (carcass), and then as the name suggests, can bury them. However, unlike other burying beetles, N. tomentosus does not completely bury these brood carcasses. They instead dig a shallow hole under the carcass and cover it with leaf litter. Recognition of these beetles can be distinguished by its black color with orange markings on the wing covers (elytra).

<i>Nicrophorus nepalensis</i> Species of beetle

Nicrophorus nepalensis, commonly known as a burying beetle, is widespread across tropical and subtropical countries in Asia. It belongs to the order Coleoptera and the family Silphidae, and is part of the nepalensis species-group, which is the second largest species group within the genus Nicrophorus. N. nepalensis differs from some other beetles in that it exhibits biparental care. Its role as a decomposer is crucial in the energy cycle and energy transformation in the ecosystem.

<i>Nicrophorus vespillo</i> Species of beetle

Nicrophorus vespillo is a burying beetle described by Carl Linnaeus in his landmark 1758 10th edition of Systema Naturae. It has a paleartic distribution and is commonly found across Europe and Asia, extending from Western Europe to Mongolia.

<i>Nicrophorus interruptus</i> Species of beetle

Nicrophorus interruptus is a species of burying beetle or sexton beetle belonging to the family Silphidae subfamily Nicrophorinae.

<i>Nicrophorus defodiens</i> Species of beetle

Nicrophorus defodiens is a burying beetle described by Mannerheim in 1846.

<i>Nicrophorus quadripunctatus</i> Species of beetle

Nicrophorus quadripunctatus is a species of burying beetle that predominates in East Asia. First described by German entomologist Ernst Kraatz in 1877, this beetle has since been the subject of much scientific inquiry—particularly concerning its parental care. Like other burying beetles, N. quadripunctatus inhabit small, vertebrate animal carcasses. This environment provides the beetles with the requisite nutrients for themselves and their offspring. To limit resource theft and predation, the carcass is buried underground. For additional protection, a single, dominant male-female pair guards the carcass cooperatively.

<i>Nicrophorus orbicollis</i> Species of beetle

Nicrophorus orbicollis is a nearctic burying beetle first described by Thomas Say in 1825. It is a member of the genus Nicrophorus or sexton beetles, comprising the most common beetles in the family Silphidae. This species is a decomposer feeding on carcasses of small dead animals. N. orbicollis can be used for scientific research both medically and forensically.

<span class="mw-page-title-main">American carrion beetle</span> Species of beetle

The American carrion beetle is a North American beetle of the family Silphidae. It lays its eggs in, and its larvae consume, raw flesh and fungi. The larvae and adults also consume fly larvae and the larvae of other carrion beetles that compete for the same food sources as its larvae.

<i>Poecilochirus</i> Genus of mites

Poecilochirus is a Holarctic genus of mites in the family Parasitidae. They are relatively large and often found on rotting corpses, where they are transported by beetles. Deuteronymphs are characterized by two orange dorsal shields and in many species a transverse band on the sternal shield. The juvenile development consists of a larval stage, protonymph, and deuteronymph, but no tritonymph. Females are smaller than males. Males guard female deuteronymphs shortly before these mate, and pairs mate venter-to-venter.

<i>Oiceoptoma noveboracense</i> Species of beetle

Oiceoptoma noveboracense is a member of the family Silphidae, or carrion beetles, which feed on decaying organic matter such as dead animals. Its common name is the margined carrion beetle, from the orange-red margins on the pronotum, which are helpful when identifying this species. The larva is typically light brown to red and also has vertical ridges on its thorax like the adult. This diurnal beetle can be found mainly in the spring into the fall, and it has a strong preference towards a deciduous forest habitat. The primary forensic importance of this beetle is its ability to use the succession of insect fauna to provide confirmation of postmortem intervals.

<span class="mw-page-title-main">Necrophage</span> Organism that consumes dead animal matter

Necrophages are organisms that obtain nutrients by consuming decomposing dead animal biomass, such as the muscle and soft tissue of carcasses and corpses. The term derives from Greek nekros, meaning 'dead', and phagein, meaning 'to eat.' Mainly, necrophages are species within the phylum Arthropoda; however, other animals, such as gastropods and Accipitrimorphae birds have been noted to engage in necrophagy.

<i>Diamesus osculans</i> Species of beetle

Diamesus osculans, is a species of carrion beetle found in Sri Lanka, Indonesia, Philippines, Laos, China, Australia.

<i>Necrodes littoralis</i> Species of beetle

Necrodes littoralis, also known as the short sexton beetle, is a species of carrion beetle of the genus Necrodes, found in countries across Europe. As a carrion beetle, it feeds on decaying vertebrate remains and maggots. This species' feeding behaviors make it an important asset to forensic entomology.

References

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