Animal Carrion Research Articles

First evidence and potential sources of novel brominated flame retardants and BDE 209 in the deepest ocean

Organic anthropogenic pollutants reach even the deepest parts of the oceans, i.e., the hadal trenches. We here presented the concentrations, influencing factors, and potential sources of polybrominated diphenyl ethers (PBDEs) and novel brominated flame retardants (NBFRs) in hadal sediments and amphipods from the Mariana, Mussau and New Britain trenches. Results showed that BDE 209 was the dominant PBDEs congener and DBDPE was the dominant NBFRs. No significant correlation was found between TOC contents and PBDEs or NBFRs levels in sediment. Lipid content and body length were the potential important factors affecting variation in pollutant concentrations in the carapace & muscle of amphipods, while the pollution levels of viscera were mainly affected by the sex and lipid content. PBDEs and NBFRs might reach trench surface seawater through long-range atmospheric transport and oceans currents but with little contribution from the Great Pacific Garbage Patch. Determination of carbon and nitrogen isotopes indicated that the pollutants were transported and accumulated in amphipods and sediment via different pathways. PBDEs and NBFRs in the hadal sediments were generally transported via the settling of sediment particles of either marine or terrigenous origin whereas in amphipods they accumulated via feeding on animal carrion through the food web. This is the first study reporting on BDE 209 and NBFR contaminations in hadal settings and provide new insight on influencing factors and sources of PBDEs and NBFRs in the deepest oceans.

The roles of plasma accessible and cytosolic carbonic anhydrases in bicarbonate (HCO3-) excretion in Pacific hagfish (Eptatretus stoutii).

Pacific hagfish (Eptatretus stoutii) are marine scavengers and feed on decaying animal carrion by burrowing their bodies inside rotten carcasses where they are exposed to several threatening environmental stressors, including hypercapnia (high partial pressures of CO2). Hagfish possess a remarkable capacity to tolerate hypercapnia, and their ability to recover from acid-base disturbances is well known. To deal with the metabolic acidosis resulting from exposure to high CO2, hagfish can mount a rapid elevation of plasma HCO3- concentration (hypercarbia). Once PCO2 is restored, hagfish quickly excrete their HCO3- load, a process that likely involves the enzyme carbonic anhydrase (CA), which catalyzes HCO3- dehydration into CO2 at the hagfish gills. We aimed to characterize the role of branchial CA in CO2/HCO3- clearance from the plasma at the gills of E. stoutii, under control and high PCO2 (hypercapnic) exposure conditions. We assessed the relative contributions of plasma accessible versus intracellular (cytosolic) CA to gill HCO3- excretion by measuring in situ [14C]-HCO3- fluxes. To accomplish this, we employed a novel surgical technique of individual gill pouch arterial perfusion combined with perifusion of the gill afferent to efferent water ducts. [14C]-HCO3- efflux was measured at the gills of fish exposed to control, hypercapnic (48h) and recovery from hypercapnia conditions (6h), in the presence of two well-known pharmacological inhibitors of CA, the membrane impermeant C18 (targets membrane bound, plasma accessible CA) and membrane-permeant acetazolamide, which targets all forms of CA, including extracellular and intracellular cytosolic CAs. C18 did not affect HCO3- flux in control fish, whereas acetazolamide resulted in a significant reduction of 72%. In hypercapnic fish, HCO3- fluxes were much higher and perfusion with acetazolamide caused a reduction of HCO3- flux by 38%. The same pattern was observed for fish in recovery, where in all three experimental conditions, there was no significant inhibition of plasma-accessible CA. We also observed no change in CA enzyme activity (measured in vitro) in any of the experimental PCO2 conditions. In summary, our data suggests that there are additional pathways for HCO3- excretion at the gills of hagfish that are independent of plasma-accessible CA.

Larval morphology and temperature-dependent development models of Fannia pusio (Wiedemann): A forensic indicator with expanding distribution

Fannia pusio (Wiedemann) is originally from tropical and subtropical regions of the Americas, where it has repeatedly been collected from both animal carrion and human cadavers. This species is expanding its distributional range, and it has been introduced to Africa, Asia, Australia, Oceania, and Europe. Newly introduced species may be confused with native species of local arthropod necrophagous assemblages, which from a forensic entomology perspective may impact the accuracy of post-mortem interval (PMI) estimations based on insect evidence. In this work we aim to raise awareness among forensic entomologists of the potential benefits and risks associated with the expanding range of F. pusio. Morphology of all larval instars is documented with a combination of light, confocal laser scanning and scanning electron microscopy. Characters allowing identification from other forensically important Fanniidae are listed. Thermal requirements for the development of immature stages of F. pusio were examined under nine ambient temperatures. Models describing changes in larval body length over time were produced for eight different temperatures. The thermal summation constant (k) and developmental zero (Tmin) were calculated for six developmental events: hatching, first ecdysis, second ecdysis, wandering, pupariation, and eclosion.

Grey seal Halichoerus grypus breeding sites contribute substantial carrion biomass to the Firth of Forth

Decomposing organic matter is central to the recycling of energy and nutrients in all ecosystems. Few studies have investigated the role of animal carrion biomass in ecosystem functioning, and quantitative data on carrion biomass are lacking. The role of carrion inputs in the marine environment specifically is poorly understood. The grey seal Halichoerus grypus breeding colony on the Isle of May in the Firth of Forth, Scotland, provides insight into the contribution of regular carrion pulses to the surrounding marine ecosystem. This study analysed 3 breeding locations with a range of topographies, elevations and tidal influences. Carcasses were mapped from aerial images and ground visual surveys in the 2008 and 2012 breeding seasons. Generalised linear mixed models were used to explore the degree to which breeding location and the position of a carcass influenced its availability to marine scavengers. Carcasses closer to shore were more likely to be completely displaced to the marine environment, and this effect varied with breeding location. An approximate 0.9 to 1.3 t of biomass per hectare of breeding site per year were released into the marine system. For carcasses that were below the high-water spring tide range but remained on shore, we quantified the typical duration of submersion to range from 5% to 44% of the time carcasses were ashore. Additionally, up to 808 kg of carrion was accessible to marine scavengers while washed by tides. Our results suggest breeding colonies of grey seals may contribute significantly to the carrion biomass available in local marine systems.

Chrysomya albicepsWiedemann (Diptera: Calliphoridae) colonising poisoned rabbit carcasses

AbstractChrysomia albicepsWiedemann (Diptera: Calliphoridae) is one of the first insects to colonise human and animal carrion and thus one of the most important insects in forensic entomology. Since the presence of these blow flies have been reported in most of the provinces in Saudi Arabia, we analyse the succession patterns ofC. albicepson decomposing rabbit carcasses injected with heroin or administered orally with alcoholic beverages. Samples of flies from the carcasses of heroin or alcohol‐treated and untreated rabbits were obtained for 15 days post mortem. A total of 1,297 and 1,426 flies were attracted to rabbit carcasses during the heroin and alcohol tests, respectively. The blow flies appeared in different developmental instars (larvae, pupae and adults), and at all stages of decomposition. Administration of higher concentrations of heroin or higher amounts of alcohol were generally associated with an increase in the number of blow flies drawn to rabbit carcasses (P < 0.05). The highest number of blow flies were attracted during the decay stage of decomposition, and the lowest during the fresh stage. In the case of medicolegal investigation, whenC. albicepsused as a forensic indicator, it is recommended that the impact of heroin or alcoholic beverages on the succession patterns be considered.

Description of the puparium and other notes on the morphological and molecular identification of Phthitia empirica (Diptera, Sphaeroceridae) collected from animal carcasses

BackgroundA correct identification of species is fundamental in order to derive all the biological, ecological, and behavioral information useful to reconstruct previous events when insects are used in forensic and funerary archaeological contexts. Little attention was paid in the past to the description of the immature stages of flies, especially of species belonging to family found only occasionally on human cadavers and animal carrion. Sphaeroceridae species belong to this category.ResultsIn this work, adult and puparia of Phthitia empirica (Hutton, 1901) are illustrated and described. In addition, some observations about the molecular identification of this species are presented and discussed.ConclusionsThis work will allow the identification of puparia of this species providing additional tools in forensic entomological investigation. More in general, the effort of producing morphological descriptions and molecular information of species of potential forensic interest clearly implements the possibility to provide a deeper understanding of the peri- and post-mortem events in violent crimes.

Vertebrate Carrion in Land Snail Diets: First Observation of Amphibian (Plethodontid Salamander) Consumption by a Terrestrial Snail in Southern Appalachia

The diet of land snails that are detritivores usually consists of decaying plant material and fungi. Animal carrion is also consumed, and is usually composed of invertebrates like earthworms and other snails. However, while working at the Coweeta Hydrologic Laboratory in southwestern North Carolina in 2017, I observed a land snail (most likely Cepaea nemoralis [Grove Snail]) feeding on the carcass of a Desmognathus aeneus (Seepage Salamander), a vertebrate. This is the first report of a land snail feeding on an amphibian carcass in the United States. The Erratum for this article can be found in Southeastern Naturalist 19(3).

Trophic ecology of ghost crabs with diverse tastes: Unwilling vegetarians

Food webs on ocean-exposed sandy beaches are almost entirely underpinned by trophic subsidies from the sea. Ghost crabs (Ocypode spp.), which are highly mobile invertebrate consumers that display a diversity of feeding modes, form an important consumer on numerous beaches around the world. However, little is known of their trophic structure and the role they play as vectors for spatial subsidies through movement of marine derived nutrients inland. The aim of this study was to determine the trophic ecology of the Golden ghost crab (Ocypode convexa) and understand what its role is in terms of marine connectivity along the mid-west coastline of Australia. Based on stomach content (percentage frequency (%F) and percentage volume (%V)) and stable isotope analyses (mixing models using ẟ13C and ẟ15N), the dietary composition of O. convexa was typically dominated by brown algae, and complemented by marine and terrestrial vascular plants and arthropods (various insects and amphipods). However, feeding assays revealed that the species had a clear preference for fish and invertebrate carcasses when the choice was offered, indicating a proclivity for the more nutritionally valuable animal flesh when available. Thus, ghost crabs are likely to be unenthusiastic consumers of vegetables, and are likely to feed on algae and macrophyte matter only when animal carrion or live animal prey is sparse. Consistent intake and assimilation of marine matter by ghost crabs, and their likely predation by higher level consumers, such as foxes (e.g. Vulpes vulpes) and birds (e.g. Corvus coronoides), support the concept that they form a vector for cross-boundary fluxes of marine carbon to inland ecosystems, although it needs to be recognized that ghost crabs also derive part of their nutritional requirements from terrestrial sources.

Insect succession on carrion in Fars Province, southwestern Iran

BackgroundThe entomofauna found on animal carrion, which is used as vertebrate model, can help in the estimation of postmortem interval (PMI). The aim of this study was to determine the succession pattern of insects on carrion in outdoor and indoor habitats in Fars Province, southwestern Iran.ResultsA total of 19 species from nine families were collected. Chrysomya albiceps and Musca domestica were the first species to visit the outdoor carrion while only Musca domestica was seen on the indoor carrion. Sarcophaga crassipalpis, Lucillia sericata, and Histeridae species were observed exclusively on the indoor carrion while Dermestes maculatus, Piophila casei, and some hymenopteran species were the most dominant species seen on the outdoor carrion. Vespula germanica and Vespa orientalis fed on both outdoor and indoor habitats.ConclusionInsects’ succession pattern was found to differ between the two respective habitats. This is really important and could be used in medicolegal cases to estimate the PMI.

Defensive (anti-herbivory) Batesian mimicry in plants

Several types of defensive Batesian mimicry seem to be much more common in plants than was historically and is currently considered. It is based either on visual aspects (shape, coloration, and even movement), on odors, and on combinations of both these sensing modalities. Various characters that seem to function as defensive Batesian mimicry, may also simultaneously take part in pollination, physiological functions, or in other defensive mechanisms. The defended models for the visual Batesian mimics in plants belong to several categories: (1) spiny, thorny and prickly plant species, (2) mechanically or chemically defended parts of the same individual plant, or other members of the same species (auto mimicry), (3) colorful and chemically defended plants, (4) dangerous animals (aggressive, toxic), (5) fungal attacks, (6) animal action and animal damage cues, and (7) oozing defensive white latex. Olfactory defended models include: (1) toxic plants, (2) animal alarm pheromones, and (3) animal carrion and feces odors. Many more descriptive, genetic, phylogenetic and experimental studies have to be done in order to better understand the role of defensive Batesian mimicry in plant biology.

Effects of abiotic environmental factors and land use on the diversity of carrion-visiting silphid beetles (Coleoptera: Silphidae): A large scale carrion study.

Anthropogenic land use causes global declines in biodiversity. Despite the knowledge that animal carrion is the most nutrient-rich form of dead organic matter, studies on landscape and local scales determining whether and the means by which land use intensity influences the diversity of the carrion-associated insect fauna are globally scarce. We investigated the effects of land use intensity and abiotic and biotic environmental factors on the abundance, species richness, and diversity of the important ecosystem-service-providing silphid beetle taxon (carrion beetles) in three regions of Germany. In 61 forest stands distributed over three geographically distinct regions in Central Europe, we trapped silphid beetles on exposed piglet cadavers during late summer. In all three regions, higher ambient temperatures and higher fine sand contents were associated with the abundance of the silphid beetle taxa. The carrion community silphid diversity was negatively affected by an increase in mean ambient temperature in all three regions. Although management intensity in forests did not affect the overall abundance of Silphidae, the abundance of Nicrophorus humator decreased significantly with higher forest management intensity across all three regions. Unmanaged and age-class forests showed a higher abundance of N. humator compared with extensively managed forest stands. These findings indicate that N. humator has potential as an indicator species for anthropogenic disturbances in forests. Overall, the direct responses of the silphid beetle community to diverse soil characteristics underline soil as an important factor determining the abundance and diversity of necrophagous carrion beetles in Central Europe. To protect these valuable ecosystem-service providers, forest-management-induced soil modifications need to be paid close attention.

DNA barcoding allows identification of European Fanniidae (Diptera) of forensic interest

In forensic entomology practice, species identification is a prerequisite for any further analysis of collected material. Although morphology-based taxonomy may be hindered by a range of factors, these are not obstacles for a molecular identification approach, so-called DNA barcoding. The Fanniidae are a dipteran family that is attracted to and breeds in decomposing animal carrion and dead human bodies. However, morphological identification of fanniids, both at adult and immature stages, is considered to be difficult, particularly for non-experts. We investigated the usefulness of molecular taxonomy methods as an alternative/supplement for morphology-based identification in European Fanniidae of forensic interest. The material used in this study was collected from various regions in Asia, Europe and North America. We sequenced a barcode region of the mitochondrial cytochrome c oxidase subunit I (COI) in 27 species. For 13 species, including some taxa breeding in dead bodies, this study describes COI sequences for the first time. Our analysis revealed that both mini-barcode and full-length COI barcode sequences give very high specimen identification success. Despite the large number of COI barcode sequences referring to Fanniidae in the BOLD and GenBank databases, previous identification of forensically relevant Fanniidae was hindered by uneven taxonomic sampling. The majority of available sequences refer to species that are not of medico-legal interest, and many species of forensic interest are unrepresented or represented only by a single sequence. Because of erroneous data that are present in depository databases, DNA barcoding must be used with caution and cannot be considered to be the sole alternative to other identification methods. Wolbachia infections in the examined material did not disrupt specimen identification. The obtained results will facilitate precise identification of European Fanniidae of forensic interest, badly preserved material with degraded DNA, as well as matching of unidentified females and immature stages to already described specimens.

Muscidae (Diptera) of forensic importance\u2014an identification key to third instar larvae of the western Palaearctic region and a catalogue of the muscid carrion community

The Muscidae is one of the main dipteran families recognized as important for medico-legal purposes. Although an association of adult flies with decomposing human and animal bodies is documented for about 200 taxa worldwide, cadavers and carrion represents a breeding habitat for considerably fewer species. Species that do colonize dead human bodies can do so under diverse environmental conditions and, under certain circumstances, Muscidae may be the only colonizers of a body. Because of difficulties in identification, many studies have identified immature and/or adult muscids only to the genus or family level. This lack of detailed species-level identifications hinders detailed investigation of their medico-legal usefulness in carrion succession-oriented experiments. Identification to species level of third instars of Muscidae of forensic importance and the utility of larval morphological characters for taxonomic purposes were subjected to an in-depth revision. A combination of characters allowing for the discrimination of third instar muscids from other forensically important dipterans is proposed. An identification key for third instar larvae, which covers the full set of cadaver-colonising species of Muscidae from the western Palaearctic (Europe, North Africa, Middle East), is provided. This key will facilitate more detailed and species-specific knowledge of the occurrence of Muscidae in forensic entomology experiments and real cases. The carrion-visiting Muscidae worldwide are catalogued, and those species breeding in animal carrion and dead human bodies are briefly discussed with regard to their forensic importance.

The Use of Forensic Entomology in Legal Veterinary Medicine: A Case Study in the North of Italy

During winter 2010 a forensic entomological study was undertaken in San Bartolomeo in Bosco (FE) Emilia-Romagna Region (North of Italy) on different animal carrion found in a farm several days after they died. The entomological evidence collected at the scene consisted of Calliphoridae (larvae of Calliphora vicina), Stratiomydae (larvae of Hermetia illucens), Dermestidae (larval exuviae of Dermestes maculatus). During diagnostic investigation the Diptera Larvae were taken from the carrion and were reared in the laboratory under constant temperature, humidity and fotoperiod. The minimum Post Mortem Interval (mPMI) was calculated using the quantity of thermal energy necessary for a given species to complete its life cycle from eggs to imago (accumulated degree-days-method). The results of the calculations were consistent with what the judicial investigation later showed. This case report illustrated the importance of using insects in legal veterinary medicine for define the time and circumstances of the death of an animal.

Chemical mimicry of insect oviposition sites: a global analysis of convergence in angiosperms

Floral mimicry of decaying plant or animal material has evolved in many plant lineages and exploits, for the purpose of pollination, insects seeking oviposition sites. Existing studies suggest that volatile signals play a particularly important role in these mimicry systems. Here, we present the first large-scale phylogenetically informed study of patterns of evolution in the volatile emissions of plants that mimic insect oviposition sites. Multivariate analyses showed strong convergent evolution, represented by distinct clusters in chemical phenotype space of plants that mimic animal carrion, decaying plant material, herbivore dung and omnivore/carnivore faeces respectively. These plants deploy universal infochemicals that serve as indicators for the main nutrients utilised by saprophagous, coprophagous and necrophagous insects. The emission of oligosulphide-dominated volatile blends very similar to those emitted by carrion has evolved independently in at least five plant families (Annonaceae, Apocynaceae, Araceae, Orchidaceae and Rafflesiaceae) and characterises plants associated mainly with pollination by necrophagous flies and beetles.

Convergent evolution of carrion and faecal scent mimicry in fly-pollinated angiosperm flowers and a stinkhorn fungus

Flowers of many angiosperms attract fly pollinators through mimicry of animal carrion and faeces. This phenomenon of “sapromyiophily” is also evident in the sporophytes of some mosses and fruiting bodies of “stinkhorn” fungi, both of which use flies as agents of spore dispersal. We studied the scent chemistry of a stinkhorn fungus ( Clathrus archeri) and seven fly-pollinated plant species with foetid odours to determine the degree to which these organisms mimic the scent of carrion and faeces (reference scent samples were collected from rotting meat, a rat carcass and horse and dog faeces), as well as the degree of convergent evolution between the fungus and angiosperm flowers. We found that scents of both the fungus and angiosperms tended to contain compounds typical of carrion, such as oligosulphides, and of faeces, such as phenol, indole and p-cresol. This study provides compelling new evidence for mimicry of carrion and faeces, as well as a striking pattern of convergence in the putrid scents of the fungus and the angiosperms, relative to those of confamilial species. The syndrome of sapromyiophily thus encompasses at least two kingdoms (Plantae and Fungi) and provides an effective means of exploiting flies as agents of pollen and spore dispersal.

Food storage and carrion feeding in the fiddler crab Uca lactea

Food hoarding is an adaptive strategy that enhances survival and reproductive success in food-scarce environments. It has been assumed that food hoarders, especially vertebrates, have the ability to cache food based on their current requirements and expected reproductive success. The present study provides empirical evidence that food storage in aquatic invertebrates is dependent on the availability of food and semilunar intertidal rhythms. The white-clawed fiddler crab Uca lactea, which inhabits food-scarce sandy mudflats, usually feeds on organic materials in sediment and occa- sionally on animal carrion, including conspecifics. This food is brought by the fiddler crabs into their burrows, presumably to be consumed during flood tides or heavy rains when the crabs cannot emerge to feed at the surface. When food was supplemented in the sediment every other day, females tended to store food-enriched sediment into their burrows. This behavior peaked around spring tides, when females were reproductively most active (i.e. mate-searching and mating). These results suggest that females may increase their reproductive effort by storing food.

Tachinids Associated with Carrion in the Centre of the Iberian Peninsula (Diptera: Tachinidae)

Tachinidae is a very large dipteran family, endoparasitism of insects being its primary biological characteristic. Despite the common feeding habit of the adults on flowers or honey dew, findings of tachinids on carrion are reported in several forensic entomology works. The present paper reports about new records of tachinid captures both on animal carrion and in carrion-baited traps, based on intensive studies in central Spain during 2004-2008. It is probable that Tachinidae are attracted by the odour of the carrion.

Deep-sea macrourid fishes scavenge on plant material: Evidence from in situ observations

Deep-sea benthic communities primarily rely on an allochthonous food source. This may be in the form of phytodetritus or as food falls e.g. sinking carcasses of nekton or debris of marine macrophyte algae. Deep-sea macrourids are the most abundant demersal fish in the deep ocean. Macrourids are generally considered to be the apex predators/scavengers in deep-sea communities. Baited camera experiments and stable isotope analyses have demonstrated that animal carrion derived from the surface waters is an important component in the diets of macrourids; some macrourid stomachs also contained vegetable/plant material e.g. onion peels, oranges, algae. The latter observations led us to the question: is plant material an attractive food source for deep-sea scavenging fish? We simulated a plant food fall using in situ benthic lander systems equipped with a baited time-lapse camera. Abyssal macrourids and cusk-eels were attracted to the bait, both feeding vigorously on the bait, and the majority of the bait was consumed in <30 h. These observations indicate (1) plant material can produce an odour plume similar to that of animal carrion and attracts deep-sea fish, and (2) deep-sea fish readily eat plant material. This represents to our knowledge the first in situ documentation of deep-sea fish ingesting plant material and highlights the variability in the scavenging nature of deep-sea fishes. This may have implications for food webs in areas where macrophyte/seagrass detritus is abundant at the seafloor e.g. canyon systems and continental shelves close to seagrass meadows (Bahamas and Mediterranean).

Diet of free-ranging domestic dogs (Canis familiaris) in rural Zimbabwe: implications for wild scavengers on the periphery of wildlife reserves

Numbers of free-ranging dogs (Canis familiaris) have reached unprecedented levels in Zimbabwean communal lands (agropastoralist rural areas). This study examined the potential competitive interactions between dogs and wild scavengers on the boundary of Gokwe Communal Land (GCL) and the Sengwa Wildlife Research Area (SWRA) in 1995–96. Dietary studies showed that dogs were primarily scavengers of human waste and animal carcasses. Twelve experimental carcasses indicated that dogs were the most successful species in the vertebrate scavenger guild, consuming 60% of available biomass and finding 66.7% of carcasses. Dogs monopolized the supply of domestic animal carrion within GCL, but also consumed wild carrion up to 1 km within the SWRA, and were seen 3 km inside the reserve. Their principal competitors for carcasses were vultures, and to a lesser degree lions (Panthera leo), leopards (P. pardus) and spotted hyaenas (Crocuta crocuta). Dogs outcompete vultures on wildlife reserve boundaries owing to their high densities, nocturnal and diurnal activity, physical dominance and greater tolerance of human disturbance. With a population growth rate of 6.5% per annum the influence of dogs will intensify on the peripheries of reserves, exacerbating their existing threat to wild scavengers. This scenario is probably occurring in many other African countries.