Differentiation in Searching Behavior for Carcasses Based on Flight Height Differences in Carrion Beetles (Coleoptera: Silphidae)

Flight ability allows insects to search for food and locate oviposition sites across a wide range of environments and, thus, allows insects to locate scarce and patchy resources such as carcasses. We examined differentiation in searching for carcasses, based on capture height differences in carrion beetles, and found that capture height differed among species. For Nicrophorus quadripunctatus and Oiceoptoma nigropunctatum, the height of abundance peaks differed among sites and was related to species composition at each site, indicating that shifts in flight height can occur plastically, whereas those for Nicrophorus maculifrons and Nicrophorus investigator did not differ among sites, indicating that the flight heights of these species are largely genetically determined. Thus, the present differentiation in capture height is primarily determined by current plastic shifts and on some genetic basis.     

The volatile organic compounds of introduced and native dung and carrion and their role in dung beetle foraging behaviour

1. The decomposition of biological material produces a plethora of volatile organic compounds (VOCs), which are implicated in the foraging behaviour of coprophagous and necrophagous insects. Dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) have an acute olfactory system used to locate food resources. Accordingly, identification of food resource VOCs potentially used in food location is integral to understanding dung beetle foraging ecology. 2. In this study, volatile emissions from dung and carrion of native and introduced animals in New Zealand were analysed using solid‐phase microextraction (SPME) and gas chromatography‐mass spectrometry (GC‐MS). Volatile profiles were compared via principal component analyses (PCAs) and cluster solutions based on attractiveness using canonical discriminant analysis (CDA). 3. A total of 115 compounds were detected from 21 food types. Statistical analyses showed that dung and carrion volatile profiles clustered according to attractiveness to the dung beetle Saphobius edwardsi, and that different dung types formed distinct clusters and grouped separately from carrion. 4. This study suggests that volatile profiles emitted by food resources used by dung beetles are complex, producing distinct odours, which potentially mediate foraging decisions.     

Not all dung beetles feed on dung: Scarabaeinae (Coleoptera: Scarabaeidae) attracted to different carrion types in contrasting habitats at Brazilian Amazon

By understanding how assemblages segregate according to food types, it is possible to depict and understand species distribution and exploitation of similar food resources. Although it is well known that dung beetles may feed on carrion, but the attractiveness of different carrion types for these beetles is still poorly understood. In this study, we compared the dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity attracted to two carrion types in different habitats in an Amazonian landscape. Dung beetles were captured by using pitfall traps baited with decaying cattle beef and cattle liver in native forest, peach palm plantation, teak plantation and exotic pasture. Overall, we captured 582 dung beetles of 43 species, where Canthidium aff. lentum was classified as a specialist of cattle beef, Deltochilum sp. One was considered specialist of liver carrion, 11 were considered generalists and for the 30 remaining species, it was not possible to determine their carrion preference due to the low number. Abundance, but not species richness, was affected by carrion type, and a higher number of beetles was recorded in beef-baited traps compared to liver-baited traps. According to functional groups, endocoprid beetles were more abundant in traps baited with decaying beef, while paracoprid and telecoprid beetles did not show preference for any carrion type. This study suggests a novel scenario of intra-resource segregation, where species vary their preferences depending to the part of the dead corpse being exploited. The amount of food resource, the maintenance of stable populations and trophic preference mediated by chemical cues are some mechanisms that may explain the segregation of dung beetles among carrion types.     

Nesting strategies and disease risk in necrophagous beetles

While the effects of carcass decomposition on microorganisms have been demonstrated in recent years, little is known of how this impacts necrophagous insects. A common assumption is that insects that exploit carcasses are exposed to a high density of potentially harmful microorganisms, but no field data have so far validated this. Necrophagous beetles such as the Scarabaeinae have complex nesting behaviors with elaborate parental care. So here, we begin to explore whether this conjunction of life history and nesting behavior represents an adaptive response to the threat posed by microbes in these environments, mainly by entomopathogens. We evaluated the density and distribution of fungi and bacteria from soil near the carcasses, and their ability to infect and kill insects that are in contact with this soil during the decomposition process. Our data showed an increase in the density and activity of opportunistic or facultative pathogens during the apex of decomposition, when there is a predominance of necrophagous insects. Meanwhile, the survivorship of bait insects decreased when in contact with soil from this period of decomposition, indicating a potential risk of infection. However, the density and activity of these microorganisms decreased with distance from the carcass, mainly with depth, which would benefit tunneller beetles in particular. We have thus provided the first field data to show that necrophagous insects are indeed exposed to high densities of potentially harmful microorganisms. Furthermore, we propose that some parental care strategies may have arisen not only as a response to competition, but also as adaptations that reduce the risks of disease. Although we have focused on carrion feeders, we suggest that the same occurs with coprophagous beetles, as both carrion and dung are nutrient‐rich resources.     

Intrasexual Competition and Mating Behavior in <Emphasis Type="Italic">Ptomascopus morio</Emphasis> (Coleoptera: Silphidae Nicrophorinae)

In nicrophorine beetles, genus Nicrophorus care their larva using small vertebrate carrion, whereas genus Ptomaucopusreproduce with small vertebrate carrion but show no parental care. Aggression and sexual behavior were examined in Ptomascopus morio and Nicrophorus quadripunctatus. Nicrophorus quadripunctatus had intense female–female as well as male–male contests. In Ptomascopus morio, by contrast, female–female aggression was rarely observed. Male–male aggression (pushing, biting, male–male mounting) in Ptomascopus morio was observed when a resource for breeding was present, whether or not a female was present. The lack of female–female aggression, and male–male aggression when resources but not females are present, suggest that the mating system of Ptomascopus morio is resource defense polygyny. Large males of Ptomascopus morio were also found to exhibit mate choice, preferring large females over small females.     

Host shift by the burying beetle, Nicrophorus pustulatus, a parasitoid of snake eggs

Recent work [Ecoscience (2000) vol. 7, 395-397] suggests that the burying beetle Nicrophorus pustulatus may have undergone a remarkable host shift, exploiting snake eggs rather than carrion as resources for breeding. We conducted behavioural and physiological experiments to examine the hypothesis of a host shift and to formulate hypotheses on its origin. Two congeners of N. pustulatus, Nicrophorus orbicollis and Nicrophorus defodiens did not respond to snake eggs with typical breeding behaviour. When N. pustulatus male-female pairs (n = 14) were presented with clutches of snake eggs, the number of offspring but not the mean size of offspring varied with snake egg mass, indicating effective regulation of brood size. When breeding on turtle eggs, N. pustulatus had a more variable response than when exploiting snake eggs, suggesting that turtle eggs are not a primary resource for breeding. Nicrophorus pustulatus presented with both snake eggs and a mouse carcass combined and exploited the two resources within the same nest (10 of 12 trials). Mouse carcasses and snake eggs were treated differently. Carcasses were moved, buried and stripped of hair in a manner characteristic of burying beetles, whereas snake eggs were not moved or buried. Females that discovered a mouse carcass also had a significantly greater juvenile hormone increase than did females discovering snake eggs. Some responses to the two resources, however, were similar. Female N. pustulatus oviposited rapidly in response to either a mouse carcass or snake eggs, and males elevated sex pheromone emission in response to either resource. The efficient use of snake eggs, the ability to regulate brood size and the different responses to snake eggs and carrion suggest that N. pustulatus is well adapted to exploiting snake eggs for breeding. The use of snake eggs by N. pustulatus has potential implications for conservation of oviparous reptiles.     

Mechanisms and fitness effects of antibacterial defences in a carrion beetle

Parents of many species care for their offspring by protecting them from a wide range of environmental hazards, including desiccation, food shortages, predators, competitors, and parasites and pathogens. Currently, little is known about the mechanisms and fitness consequences of parental defences against bacterial pathogens and competitors. Here, we combine approaches from microbiology and behavioural ecology to investigate the role and mechanistic basis of antibacterial secretions applied to carcasses by parents of the burying beetle Nicrophorus vespilloides. This species rears its larvae on vertebrate carcasses, where larvae suffer significant fitness costs due to competition with bacterial decomposers. We first confirm that anal secretions produced by parents are potently bactericidal and that their effects are specific to gram-positive bacteria. Next, we identify the source of bacterial killing as a secreted lysozyme and show that its concentration changes throughout the breeding cycle. Finally, we show that secreted lysozyme is crucial for larval development, increasing survival by nearly two-fold compared to offspring reared in its absence. These results demonstrate for the first time that anal secretions applied to carrion is a form of parental care and expand the mechanistic repertoire of defences used by parent insects to protect dependent offspring from microbial threats.     

Experimental evidence that the mite Poecilochirus davydovae (Mesostigmata: Parasitidae) eats the eggs of its beetle host

The relationship between the mite Poecilochirus davydovae Hyatt and its burying beetle carrier ( Nicrophorus vespilloides ) was investigated. Beetles experimentally stripped of deuteronymphs of Poecilochirus had larger apparent clutch sizes than beetles carrying mites. Furthermore, apparent clutch sizes were not affected by the presence or absence of carrion flies (Diptera: Calliphoridae). These results support the hypothesis that P. davydovae is a specialist predator feeding on the eggs of N. vespiloides.     

Gray wolves as climate change buffers in Yellowstone

Understanding the mechanisms by which climate and predation patterns by top predators co-vary to affect community structure accrues added importance as humans exert growing influence over both climate and regional predator assemblages. In Yellowstone National Park, winter conditions and reintroduced gray wolves (Canis lupus) together determine the availability of winter carrion on which numerous scavenger species depend for survival and reproduction. As climate changes in Yellowstone, therefore, scavenger species may experience a dramatic reshuffling of food resources. As such, we analyzed 55 y of weather data from Yellowstone in order to determine trends in winter conditions. We found that winters are getting shorter, as measured by the number of days with snow on the ground, due to decreased snowfall and increased number of days with temperatures above freezing. To investigate synergistic effects of human and climatic alterations of species interactions, we used an empirically derived model to show that in the absence of wolves, early snow thaw leads to a substantial reduction in late-winter carrion, causing potential food bottlenecks for scavengers. In addition, by narrowing the window of time over which carrion is available and thereby creating a resource pulse, climate change likely favors scavengers that can quickly track food sources over great distances. Wolves, however, largely mitigate late-winter reduction in carrion due to earlier snow thaws. By buffering the effects of climate change on carrion availability, wolves allow scavengers to adapt to a changing environment over a longer time scale more commensurate with natural processes. This study illustrates the importance of restoring and maintaining intact food chains in the face of large-scale environmental perturbations such as climate change.     

Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems

Carrion use by terrestrial vertebrates is much more prevalent than conventional theory implies, and, rather than a curiosity of animal behavior, is a key ecological process that must be accounted for. Human aversion to rotted substances and difficulties associated with identifying scavenged material in studies of food habits have contributed to the relative lack of information concerning scavenging behavior in vertebrates. Several lines of evidence, however, suggest that carrion resources are more extensively used by vertebrates than has been widely assumed: 1) a substantial number of animals die from causes other than predation and become available to scavengers, 2) a wide variety of vertebrate scavengers, rather than microbes or arthropods, consume most available carcasses, and 3) intense competition exists between vertebrate scavengers and decomposers, especially in warm climates. Although vultures are best adapted to use carrion, nearly all vertebrate predators are also scavengers to some extent. The costs and benefits associated with carrion use influences the evolution of scavenging behavior in vertebrates, resulting in a continuum of facultative scavengers that use carrion to varying degrees. The realized usage of carrion by a vertebrate species is influenced by the speed and efficiency with which it forages, its visual and olfactory abilities, and its capacity for detoxifying products of decomposition. A deeper understanding of carrion use by facultative scavengers will improve our knowledge of community and ecosystem processes, especially the flow of energy through food webs.     

Seal carrion is a predictable resource for coastal ecosystems

The timing, magnitude, and spatial distribution of resource inputs can have large effects on dependent organisms. Few studies have examined the predictability of such resources and no standard ecological measure of predictability exists. We examined the potential predictability of carrion resources provided by one of the UK's largest grey seal (Halichoerus grypus) colonies, on the Isle of May, Scotland. We used aerial (11 years) and ground surveys (3 years) to quantify the variability in time, space, quantity (kg), and quality (MJ) of seal carrion during the seal pupping season. We then compared the potential predictability of seal carrion to other periodic changes in food availability in nature. An average of 6893 kg of carrion ∙yr⁻¹ corresponding to 110.5 × 10³ MJ yr⁻¹ was released for potential scavengers as placentae and dead animals. A fifth of the total biomass from dead seals was consumed by the end of the pupping season, mostly by avian scavengers. The spatial distribution of carcasses was similar across years, and 28% of the area containing >10 carcasses ha⁻¹ was shared among all years. Relative standard errors (RSE) in space, time, quantity, and quality of carrion were all below 34%. This is similar to other allochthonous-dependent ecosystems, such as those affected by migratory salmon, and indicates high predictability of seal carrion as a resource. Our study illustrates how to quantify predictability in carrion, which is of general relevance to ecosystems that are dependent on this resource. We also highlight the importance of carrion to marine coastal ecosystems, where it sustains avian scavengers thus affecting ecosystem structure and function.     

Parental care influences social immunity in burying beetle larvae

相似文献   

The underestimated role of carrion in vertebrates' diet studies

Aim

Despite the increasing scientific evidence on the importance of carrion in the ecology and evolution of many vertebrates, scavenging is still barely considered in diet studies. Here, we draw attention to how scientific literature has underestimated the role of vertebrates as scavengers, identifying the ecological traits that characterize those species whose role as scavengers could have gone especially unnoticed.

Location

Global.

Time Period

1938–2022.

Major Taxa Studied

Terrestrial vertebrate scavengers.

Methods

We analysed and compared (a) the largest database available on scavenging patterns by carrion-consuming vertebrates, (b) 908 diet studies about 156 scavenger species and (c) one of the most complete databases on bird and mammal diets (Elton Traits database). For each of these 156 species, we calculated their scavenging degree (i.e. proportion of carcases where the species is detected consuming carrion) as a proxy for carrion consumption, and related their ecological traits with the probability of being identified as scavengers in diet studies and in the Elton Traits database.

Results

More than half of the species identified as scavengers at monitored carcasses were not assigned carrion as food source in their diet studies nor in the Elton Traits database. Using a subset of study sites, we found a direct relationship between a species' scavenging degree and its rate of carrion biomass removal. In addition, scavenger species, which were classified as non-predators and mammals had a lower probability of being identified as scavengers in diet studies and in the Elton Traits database, respectively.

Main Conclusions

Our results clearly indicate an underestimation of the role of scavenging in vertebrate food webs. Given that detritus recycling is fundamental to ecosystem functioning, we encourage further recognition and investigation of the role of carrion as a food resource for vertebrates, especially for non-predator species and mammals with higher scavenging degree.     

Impacts of dietary amino acid composition and microbial presence on preference and performance of immature Lucilia sericata (Diptera: Calliphoridae)

1. As primary colonisers of ephemeral resources, the common green bottle fly, Lucilia sericata, must exercise efficient resource exploitation strategies to maximise fitness. Foraging incurs costs, so the efficient evaluation of resources is essential for individuals relying on fragmented patches whose dissimilarity may result in fitness consequences for offspring. Thus, selective pressures between carrion‐using insects and carrion‐associated microbes are expected to occur. 2. Microbes play a pivotal role in adult fly assessment of resources via production of volatile organic compounds (VOCs) resulting from the breakdown of essential amino acids. If one assumes that chemoreception of these VOCs provides public information regarding the corresponding essential amino acids, the resulting effects on maternal decision‐making could impact larval resource exploitation. 3. The essential amino acids phenylalanine, methionine, valine, and tryptophan, the corresponding VOCs of which are known fly attractants, were used to construct imbalanced diets with and without antimicrobial treatment to investigate the impact of suboptimal food sources on larval L. sericata. 4. The results of this study demonstrate that both amino acid composition and microbial presence influence behaviour, with larvae displaying a preference for untreated diets lacking methionine and a complete reversal in preference for antimicrobial‐treated diets. This interaction between diet and antimicrobial treatment indicates that the presence of microbes that produce essential amino acids may impact larval resource utilisation strategies. This investigation into larval performance on diets deficient in amino acids that provide important VOC cues to maternal flies provides a stepping stone for dissecting larval behavioural strategies on ephemeral resources when faced with limited choices.     

Burying beetle Nicrophorus investigator reproduction on Pacific salmon carcasses

Abstract.  1. In many undisturbed watersheds along the Pacific Rim, anadromous salmon ( Oncorhynchus spp.) provide a predictable source of carrion to the riparian zone, largely due to horizontal transfer of salmon carcasses by bears ( Ursus spp.) and other vertebrates.
2. Burying beetles are important members of the north-temperate carrion fauna, and may utilise salmon carcasses and remnants for breeding. In this study, isotopic and observational data are reported that demonstrate previously unrecognised Nicrophorus investigator (Zetterstedt) reproduction on large salmon carcasses from five watersheds in coastal British Columbia.
3. Stable isotope signatures (δ¹⁵N and δ¹³C) of adult beetles collected in autumn indicate a diet of salmon origin in all but one individual from all watersheds, suggesting that this beetle–salmon association is widespread. Comparison of autumn isotope signatures to individuals collected randomly in summer suggests that isotope signatures represent the larval carrion source from the previous autumn rather than immediate adult diet.
4. In a survey of N. investigator use of salmon carcasses from two watersheds, 35 broods were observed on chum and pink salmon carcasses, including 16 natural brood complexes containing over 100 larvae, and five ranging from 250 to 750 larvae.
5. Overall, north-coastal populations of N. investigator breed on the rich and reliable salmon resource and may exhibit a system of communal breeding on these carcasses. This is most relevant when the dramatic reduction in salmon spawning biomass over the last century is considered.     

The role of juvenile hormone in competition and cooperation by burying beetles

Few studies have addressed the physiological mechanisms that modulate aggression in insects. In some social insects, there is a correlation of JH and aggression in colony defense and in the establishment of dominance, but only a few studies demonstrate a causal relationship. Burying beetles aggressively defend a breeding resource, a carcass, and juvenile hormone (JH) hemolymph titers increase rapidly upon the discovery of a carcass. In this study, I show that treatment with the JH analog, methoprene, in the absence of a carcass increases the probability of injuries from aggressive interactions, but treatment to one member of a pair of competing Nicrophorus orbicollis females does not increase the probability that she will win control of the resource. In addition, higher JH levels are not associated with greater competitive ability in communally breeding Nicrophorus tomentosus females. Treatment of one female N. tomentosus does not increase her share of the communal brood. Methoprene seems to make a less competitive female more persistent and less willing to concede, which, although maintaining her share of reproduction, results in her exclusion from the brood chamber.     

Resolving phylogeny at the family level by mitochondrial cytochrome oxidase sequences: phylogeny of carrion beetles (Coleoptera, Silphidae)

We investigated the phylogenetic relationships of carrion beetles (Coleoptera, Silphidae) using 2094 bp of their mitochondrial cytochrome oxidase subunit I and II and tRNA leucine gene sequences. Shorter fragments of this gene region previously have been used to establish generic relationships in insects. In this study, they provided more than sufficient resolution, although the third positions of the protein-coding sequences reached saturation for the deeper divergences. This first published phylogeny for the Silphidae comprises 23 species from 13 genera sampled across the geographic range of the family. In addition, we included species from three related families as outgroups. One of these families, the Agyrtidae, was, until recently, included in the Silphidae, but its resolution here justifies its current position as a separate family. The silphid subfamilies Nicrophorinae and Silphinae are monophyletic in all analyses. All genera for which several species were sampled are supported as monophyletic groups, with the exception of the genus Silpha. European and North American representatives of two Nicrophorus species described from both continents are supported as each others' closest relatives. The lineage that colonized Gondwanaland and that most likely originated in the Palearctic is the most basal within the Silphinae.     

Phoretic mites associated with animal and human decomposition

Phoretic mites are likely the most abundant arthropods found on carcases and corpses. They outnumber their scavenger carriers in both number and diversity. Many phoretic mites travel on scavenger insects and are highly specific; they will arrive on a particular species of host and no other. Because of this, they may be useful as trace indicators of their carriers even when their carriers are absent. Phoretic mites can be valuable markers of time. They are usually found in a specialised transitional transport or dispersal stage, often moulting and transforming to adults shortly after arrival on a carcase or corpse. Many are characterised by faster development and generation cycles than their carriers. Humans are normally unaware, but we too carry mites; they are skin mites that are present in our clothes. More than 212 phoretic mite species associated with carcases have been reported in the literature. Among these, mites belonging to the Mesostigmata form the dominant group, represented by 127 species with 25 phoretic mite species belonging to the family Parasitidae and 48 to the Macrochelidae. Most of these mesostigmatids are associated with particular species of flies or carrion beetles, though some are associated with small mammals arriving during the early stages of decomposition. During dry decay, members of the Astigmata are more frequently found; 52 species are phoretic on scavengers, and the majority of these travel on late-arriving scavengers such as hide beetles, skin beetles and moths. Several species of carrion beetles can visit a corpse simultaneously, and each may carry 1–10 species of phoretic mites. An informative diversity of phoretic mites may be found on a decaying carcass at any given time. The composition of the phoretic mite assemblage on a carcass might provide valuable information about the conditions of and time elapsed since death.     

Dung beetles in an avian-dominated island ecosystem: feeding and trophic ecology

Globally, dung beetles (Scarabaeidae: Scarabaeinae) are linked to many critical ecosystem processes involving the consumption and breakdown of mammal dung. Endemic New Zealand dung beetles (Canthonini) are an anomaly, occurring at high abundance and low diversity on an island archipelago historically lacking terrestrial mammals, except bats, and instead dominated by birds. Have New Zealand’s dung beetles evolved to specialise on bird dung or carrion, or have they become broad generalist feeders? We test dietary preferences by analysing nitrogen isotope ratios of wild dung beetles and by performing feeding behaviour observations of captive specimens. We also use nitrogen and carbon stable isotopes to determine if the dung beetle Saphobius edwardsi will consume marine-derived carrion. Nitrogen isotope ratios indicated trophic generalism in Saphobius dung beetles and this was supported by behavioural observations where a broad range of food resources were utilised. Alternative food resource use was further illustrated experimentally by nitrogen and carbon stable isotope signatures of S. edwardsi, where individuals provided with decomposed squid had δ¹⁵N and δ¹³C values that had shifted toward values associated with marine diet. Our findings suggest that, in the absence of native mammal dung resources, New Zealand dung beetles have evolved a generalist diet of dung and carrion. This may include marine-derived resources, as provided by the seabird colonies present in New Zealand forests before the arrival of humans. This has probably enabled New Zealand dung beetles to persist in indigenous ecosystems despite the decline of native birds and the introduction of many mammal species.     

Measuring success of a reintroduced population of the American burying beetle (<Emphasis Type="Italic">Nicrophorus americanus</Emphasis> Olivier) to Nantucket Island,MA

The American burying beetle (Nicrophorus americanus) is a federally listed endangered beetle and since 1993 multiple organizations have collaborated to reintroduce this species to Nantucket Island, Massachusetts, USA. We present evidence that despite very successful reintroduction methods, the reintroduced population is not self-sustaining and requires human assistance for long term maintenance. Beetles were reintroduced from captive stock and each year we augmented the population by trapping wild beetles, pairing males and females, and supplying the pairs with carrion. Long term monitoring of this population has shown that, when provided with carrion, N. americanus on Nantucket have an over winter survival rate of 15?% and a reproductive success rate of 54?%. After seeing the number of beetles captured between 2007 and 2011 double, we modified protocols to determine if the established population would be self-sustaining and we have seen a drastic decline. We suggest that a lack of natural carrion is the main reason for this decline.