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Necrophage
Organism that consumes dead animal matter From Wikipedia, the free encyclopedia
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Necrophages are organisms that obtain nutrients by consuming decomposing dead animal biomass, such as the muscle and soft tissue of carcasses and corpses (also known as carrion).[1][2] The term derives from Greek nekros, meaning 'dead', and phagein, meaning 'to eat'.[2] Many hundreds of necrophagous species have been identified including invertebrates in the insect,[3] malacostracan[4] and gastropod[5] classes and vertebrates such as vultures, hyenas, quolls and wolves.[4]
Necrophagous insects are important in forensic science[3] as the presence of some species (e.g. Calliphora vomitoria) in a body, coupled with information on their development stage (e.g. egg, larva, pupa), can yield information on time of death.[6][7] Information on the insect species present can also be used as evidence that a body has been moved,[6][8] and analysis of insect tissue can be used as evidence that drugs or other substances were in the body.[6][9]
Necrophages are useful for other purposes too. In healthcare, green bottle fly larvae are sometimes used to remove necrotic (dead) tissue from non-healing wounds,[10][11] and in waste management, black soldier fly larvae are used to convert decomposing organic waste into animal feed.[12][13] Biotechnological applications for necrophage-derived genes, molecules and microbes are also being explored.[4][14]
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Classification
Necrophages can be classified according to their nutritional reliance on carrion and also their level of adaptation to carrion feeding. Animals are described as 'obligate necrophages' if they use carrion as their sole or main food source and depend on carrion for survival or reproduction.[4] The term 'specialists' is also sometimes used in recognition that these animals have traits favoring necrophagy and making other feeding behaviors difficult.[17] For example, large wingspans facilitate the energy-efficient gliding vultures need to cover long distances in search of carrion,[15] but reduce the agility needed to kill prey.[16] Animals that eat carrion opportunistically and retain the traits needed to find and consume other food sources are described as 'facultative necrophages' and 'generalists'.[4][16]
Both obligate and facultative necrophages are sometimes sub-classified as 'wet' and 'dry' feeders.[18] These terms differentiate animals feeding on moist, putrefying tissue from animals feeding on desiccated and keratinized tissues.[18]
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Invertebrates
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Flies
The European bone skipper, Thyreophora cynophila, is an obligately necrophagous fly. It relies on carrion bone marrow in the first stage of its life cycle.[19] Many other types of fly are facultatively necrophagous. Examples commonly found on land include blow flies, flesh flies, muscid flies, black soldier flies, ensign flies and thread-horns. Other necrophagous flies, for example black flies and lake flies, are semi-aquatic.[3][20] Types of carrion fed upon include wildlife,[21][22][23] livestock and poultry carcasses, slaughterhouse and fishing discards, and human bodies.[4]
Necrophagous flies have several traits and adaptations that facilitate their feeding behavior. For example, blow flies and flesh flies have a well-developed sense of smell[25][26] and are highly mobile.[6][18] This enables them to rapidly detect and locate carrion.[6][24][25] Also, flesh flies and some blow flies lay larvae instead of eggs.[25][27] This gives these flies a competitive advantage over other slower-developing, egg-laying species.[27] In addition, blow flies, flesh flies, muscid flies and black soldier flies have many defenses against the pathogens and toxins found in carrion. These include a protective lining in their midgut, antibiotic-producing microbiota species, and a large number of pattern recognition receptors, lysozymes, antimicrobial peptides and detoxification enzymes.[4]
The diversity and abundance of necrophagous fly species vary geographically and seasonally.[6][19][26] For example, Chrysomya species are present in subtropical regions of the USA but are rare in most of Canada.[6] This geographic variation is attributable to factors such as soil type and meteorological conditions, and the effects these have on carrion decomposition.[6] Whether urbanization affects fly species richness is open to dispute.[26][28] Seasonally, many necrophagous fly species are observed in higher abundance in summer,[26] but Thyreophora cynophila is more active in winter.[19]
Flies play a critical role in forensic science as they are often the first insects to discover and colonize human remains.[6][20] Blow flies can arrive within minutes and begin laying eggs in the nose, mouth and other openings. Because adult flies very rarely deposit eggs in live hosts, the age of the developing fly larvae can be used to estimate time of death.[6] Fly larvae can also provide information regarding cause of death because necrophagous flies deposit their eggs in any open wounds.[6]
Bees
Vulture bees are a small group of obligately necrophagous bees in the Trigona genus.[29][30] Trigona worker bees play a similar role to worker bees in the Apis genus; however, along with collecting pollen, nectar, and plant resins, Trigona workers also collect carrion.[29][31] Although pollen is associated with higher energy value, carrion is preferred by Trigona bees because it is biochemically easier to extract energy from.[30] This dead animal tissue is used as a source of amino acids too.[32]
Cerumen pots are utilized by some Trigona species, such as T. necrophaga, as vesicles to store foodstuff.[33] The foodstuff of T. necrophaga consists of both honey and carrion from vertebrate carcasses.[29] Ultimately, the stored food is utilized by developing larvae and the worker bee itself as a source of nutrition and energy. Due to the rapid decomposition of carrion, especially in warm temperatures, the bees must efficiently metabolize the carrion to avoid rotten carrion in their cerumen pots.[29]
Trigona hypogea communicate the presence of a valuable carcass through olfactory signals.[29] The bees create an odour trail between their nest and the prospective animal carcass; thus, the bees recruit the other nest members to respond and exploit the corpse's resources rapidly. Additionally, interspecific competition is observed in Trigona hypogea bees. The bees are observed to defend their colonized food item, including but not limited to a monkey, lizard, fish, or snake carcass, from competing necrophages, such as flies.
Beetles
Numerous beetles in the Nicrophorus genus are obligately necrophagous, for example Nicrophorus americanus and N. vespilloides.[4] Many other beetles are facultative necrophages including checkered beetles,[21] dermestid beetles,[6] diving beetles,[20][34] scarab beetles,[35] silphine beetles[6] and water scavenger beetles.[34] Types of carrion fed upon include wildlife, livestock and poultry carcasses, livestock viscera and human bodies.[4]
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Necrophagous beetles have evolved many diet-related adaptations. For example, Nicrophorus species have specialized olfactory sensors on their antennae to help them detect carrion.[36][37] These sensors are sensitive to dimethyl sulphide and other sulfur-containing compounds emitted by bodies after death.[38] Also, Nicrophorus, Necrodes and other necrophagous silphine beetle species are flight-capable, making it easier for them to reach carrion.[39][40][41] Nicrophorus and Dermestes species have many defenses against dietary pathogens and toxins too. These include physical traits such as protective gut linings, antibacterial lectins and lysozymes, mutualistic relationships with microbiota bacteria, and behavioral traits such as preferentially selecting fresh carcasses and smearing carcasses with antibacterial and toxin-degrading exudates.[4] Given the often-limited availability of carrion, the ability of these beetles to share this resource with other beetles[36][37] and defend it against flies and ants[42][43] is also an advantage.
Regarding food preferences and the logistics of carrion use, N. vespilloides and other burying beetles favor small carcasses (e.g. rodents and small birds)[38] as these are easier to transport, clean and conceal from competitors.[37][44] Diving beetles, scarab beetles and water scavenger beetles have all been observed feeding on amphibian carrion (e.g. granular toads and tree frogs).[34][35] The scarab beetle Scybalocanthon nigriceps uses its front legs and clypeus to shape frog carrion into pellets for eventual consumption.[35] Other scarab beetles, for example, Coprophanaeus ensifer, build their burrows near carcasses for easier transportation of carrion pieces to offspring.[45]
Beetles that feed on human remains are important in forensic science. Terrestrial beetles such as checkered beetles and dermestid beetles colonize bodies in a predictable sequence and have well-characterized life cycles, so they can sometimes be used to estimate time of death.[6][46] Aquatic beetles are less useful for estimating time of death[6] but can cause physical damage to submerged bodies that must be distinguished from inflicted injuries when determining cause of death.[20] For example, the facultatively necrophagous diving beetle Meridiorhantus validus creates postmortem channels and chambers in human bodies that must be differentiated from antemortem piercing injuries.[20]
Marine snails
Nassa mud snails such as Nassarius festivus and Nassarius clarus scavenge on dead and decaying animal matter in the intertidal zone of eulittoral soft shores.[5][47] At Shark Bay in Australia, Nassarius clarus feeds on the carrion of fishes and bivalves.[47] In the presence of carrion, the animal's proboscis performs a search reaction followed by a quick onset of feeding.[47] When faced with a competitor, such as a hermit crab, at the site of the carrion, the Nassarius clarus attack the competition to defend their meal.[47] Nassarius clarus are attracted to fish and bivalve carrion to a distance of 26 meters and have a heightened interest in areas where the sand has been disturbed; thus, indicating the potential presence of organic detritus or damaged fauna.[47]
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Vertebrates
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Vultures
Many vulture species are obligately necrophagous including the bearded vulture, black vulture, cinereous vulture, Eurasian griffon, Himalayan vulture, king vulture and turkey vulture.[4][15] Types of carrion fed upon include dead wildlife, livestock, poultry and companion animals, human remains (sky burial), hunting discards, slaughterhouse offal and roadkill.[4] Typically, muscle tissue is consumed,[48] but bearded vultures feed on bones and bone marrow.[49] In addition to eating carrion, Egyptian vultures feed on small live animals such as turtles, eggs and rotting fruit.[50][51][52]
Vultures have many adaptations that help them detect, locate and consume carrion. For example, all vultures have keen eyesight,[15] and New World vultures have a highly developed sense of smell.[15][16] Hooded vultures also have excellent auditory perception, enabling them to hear distant predation-related noises and the distress calls of dying animals.[53] In addition, gliding flight enables vultures to cover long distances to reach carrion,[15][16] strong beaks allow vultures to cut through thick animal skin,[54] and strong immune defenses protect vultures from pathogens in carrion.[4] Given the inherently unpredictable and ephemeral nature of carrion as a food source, the ability of vultures to survive long periods between meals is also advantageous.[55][56]
Some human activities have had an adverse impact on vultures in Sicily,[50] the Azerbaijan Republic[57] and other countries.[58] For example, changes in farming practices such as the indoor raising of cattle and incineration or burial of cattle carcasses have reduced food availability for Eurasian griffon vultures.[50][57] Shootings of birds, removal of nestlings from nests,[57] and drug pollution[58] have also contributed to declines in vulture populations.
Current roles and uses
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Maggot therapy
In maggot debridement therapy, sterile, medical-grade larvae of the necrophagous fly Lucilia sericata are used to eliminate necrotic (dead) tissue from non-healing skin and soft-tissue wounds.[60][61][62] This is important as dead tissue can facilitate bacterial growth, impede wound healing, and reduce the effectiveness of topical medications.[63] Physicians may administer the fly larvae directly to skin and soft tissue wounds[64] or indirectly within a sealed mesh bag.[59][65] Larvae then debride the wound by digesting, liquefying and consuming the dead tissue.[60][61] The US Food and Drug Administration (FDA) have cleared Lucilia sericata larvae for use as a "medical device" in the US to debride several types of wound including pressure ulcers, neuropathic foot ulcers, and nonhealing surgical wounds.[64][65]
Forensic entomology
Necrophagous flies and beetles play an important role in forensic entomology due to their postmortem colonization of human remains.[6][20] For example, in homicide cases, forensic medical examiners can sometimes determine the minimum post-mortem interval based on the fly and beetle species present in the body and their development stage.[6][66] This is because these insects rarely deposit eggs in live hosts, they colonize bodies in a predictable sequence following death, and information is available on how long it takes different species to reach different stages of development.[6] Because insect arrival and departure time and larval development time are affected by seasonal changes,[67] temperature,[68] moisture levels,[69] air exposure,[70] geographical region,[71] and other factors, these must all be carefully considered when estimating minimum post-mortem interval.[72]
Waste management
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In some countries, the black soldier fly, Hermetia illucens, is used to process food industry by-products and food waste. Hermetia illucens is a facultative necrophage and can grow on a wide range of decomposing organic substrates including those of animal origin (e.g. abattoir waste),[73] plant origin (e.g. almond hulls),[74] and a mix of both (e.g. meat, fish and vegetable food waste).[75] Fly larvae are grown on this organic waste and then used as livestock feed or fish feed. The frass generated by the larvae can be used as soil fertilizer too. This waste conversion process, known as bioconversion, has several advantages. It reduces the greenhouse gas emissions caused by microbial decomposition of food waste in landfills (e.g. methane), it generates high-quality protein for feeding livestock, and it generates low-cost fertilizer for crop cultivation.[76][77]
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Other possible uses
Drug and biomaterial development
Necrophages and their microbiotas ("friendly bacteria") produce several molecules of medical interest. These include molecules that can bind to bacterial pathogens (e.g. lectins), inhibit pathogen growth (e.g. chitin, cyclic lipopeptides), and kill pathogens (e.g. antimicrobial peptides, lysozymes). In nature, these molecules are thought to block pathogen entry into the integuments (e.g. skin, cuticle) and circulatory systems (e.g. blood, hemolymph) of necrophages, and enable the immune systems of necrophages to detect, inhibit and kill any pathogens that breach these barriers.[4][14] Research is underway in Germany,[78] China,[79] the USA[80] and other countries[81][82] to develop these molecules for use in medicine. Possible applications include antimicrobial wound dressings, antibacterial drugs, and drug delivery systems for bacterial infections.[4][80][83]
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Image and video gallery
The American burying beetle, Nicrophorus americanus, about to take flight.- The American carrion beetle, Necrophila americana, feeding on vole carrion.
Necrophagous snails feeding on starfish carrion.
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External links
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