Effects of carrion decomposition on litter arthropod assemblages

1. Many organisms contribute to the decomposition of carrion. For arthropods, many studies focus on the necrophagous community, those directly consuming carrion.
2. Necrophagous arthropods use carrion as a shelter or food source. Therefore, carrion generally increases the abundance and biodiversity of necrophagous species. However, it is unclear if carrion has similar effects on detrital communities.
3. This study examines changes in community structure and composition of necrophilous and detrital communities over the course of decomposition.
4. Five pig head carrion were placed at least 7 m apart under cages in temperate mixed forest. Leaf litter was sampled 0 m, 1.5 m, and 3 m from each carrion weekly during summer, and monthly during autumn, until the first frost. Arthropods were extracted from leaf litter by using Berlese funnels.
5. At the carrion site, necrophagous insects increased in abundance, species richness, and Shannon diversity during decomposition, and all decreased after dry decay.
6. Detritus arthropods displayed a sharp increase in abundance during advanced decay, decreasing during dry decay, and a general increase over time for species richness and diversity.
7. In conclusion, carrion can influence the surrounding, non-necrophagous arthropod community, highlighting the need to investigate carrion effects beyond typical necrophagous species to have a more holistic understanding of carrion ecology.

     

Vertebrate Decomposition Is Accelerated by Soil Microbes

Carrion decomposition is an ecologically important natural phenomenon influenced by a complex set of factors, including temperature, moisture, and the activity of microorganisms, invertebrates, and scavengers. The role of soil microbes as decomposers in this process is essential but not well understood and represents a knowledge gap in carrion ecology. To better define the role and sources of microbes in carrion decomposition, lab-reared mice were decomposed on either (i) soil with an intact microbial community or (ii) soil that was sterilized. We characterized the microbial community (16S rRNA gene for bacteria and archaea, and the 18S rRNA gene for fungi and microbial eukaryotes) for three body sites along with the underlying soil (i.e., gravesoils) at time intervals coinciding with visible changes in carrion morphology. Our results indicate that mice placed on soil with intact microbial communities reach advanced stages of decomposition 2 to 3 times faster than those placed on sterile soil. Microbial communities associated with skin and gravesoils of carrion in stages of active and advanced decay were significantly different between soil types (sterile versus untreated), suggesting that substrates on which carrion decompose may partially determine the microbial decomposer community. However, the source of the decomposer community (soil- versus carcass-associated microbes) was not clear in our data set, suggesting that greater sequencing depth needs to be employed to identify the origin of the decomposer communities in carrion decomposition. Overall, our data show that soil microbial communities have a significant impact on the rate at which carrion decomposes and have important implications for understanding carrion ecology.     

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.     

Abundance and reproductive strategy of the dung beetle Aphodius rufipes (L.) (Scarabaeidae)

Abstract. 1. Adult A.rufipes invade fresh dung pats (mainly in August) and stay for a few days in each pat to feed and oviposit; maximum abundances: 0–100 beetles per cattle dung pat. Larval growth is completed within 40–55 days.
2. The dispersion of beetles is contagious or seemingly random. In sunny weather, with rapid crust formation on the dung, pats deposited in the afternoon are invaded by more beetles than those deposited in the morning.
3. In the field, the total number of eggs per pat is significantly less variable than the number of adult beetles; this might indicate a density-dependent, regulatory, rate of oviposition. The subsequent larval mortality is probably density-independent.
4. Experiments confirmed that the number of eggs laid per female-day in the pats was density-dependent.
5. The non-opportunistic reproductive strategy of A.rufipes may have evolved as an adaptation to life in dung pats: at excessive population densities pats might disappear before completion of larval growth.
6. Finally, A.rufipes in dung pats is compared with blowflies breeding in carrion.     

The structure of carrion fly communities: the size and the type of carrion

Species composition and abundance relations of flies attracted to and bred from different sizes (20-100 g) and types of carrion (small mammal, cow liver, bird, and fish) were studied experimentally in natural breeding conditions in South Finland. Large pieces of carrion did not attract significantly more individuals or species than did small ones, but there was a positive correlation between size of carrion and numbers of flies bred, apparently because of competition. Altogether 10 species emerged from 50 cultures, and on average 2.78 ± 1.22 (SD) species emerged from one culture. The number of co-occurrences among the emerging flies indicated random colonization. Variation in species composition between like pieces of carrion was not less than variation between carcasses of different size or type; hence, size and type of carrion are not important determinants of community structure within the size and type ranges used.
Lucilia illustris (Meig.) was the predominant species, comprising 50% of flies trapped and 85% of flies bred. The difference indicates changing species composition in the community. Two sets of cultures were left open for egg-laying for 2 and 7 d. Competition was less Intensive in the former cultures, which produced 4.0 individuals per gram of carrion, contrasting with only 1.4 individuals per gram in the latter cultures. Competition delayed development in all species, but least in L. illustris , which suggests that fast developing species are at a competitive advantage. In agreement with this, abundance was positively correlated with the rate of development.     

Seasonality of insect succession on exposed rabbit carrion in Guangzhou, China

Abstract  Succession patterns for insect fauna, spanning four seasons, on rabbit carcasses were studied in Guangzhou China from 2006 to 2008. A total of 49 taxa belonging to three orders and 15 families were collected and identified. Four decomposition stages were recognized: fresh, bloated, decay and dry stage. Taxa diversity was higher in bloated and decay stages than fresh and dry stages. Internal and ambient temperatures were measured. Maximum internal temperature arrived earlier in warmer seasons. The sequence of insect succession in this study follows the same general patterns: the Diptera peaked initially, and the Coleoptera peaked later. Chrysomya megacephala was the dominant species in four seasons. Its time point of different development stages on carrion could be the most important indicators for PMI (postmortem interval) estimation in Guangzhou. Yearly and seasonal differences in activities of insects were compared. Alpha diversity indices were calculated. There were no significant differences in Shannon-Wiener index, evenness ( J ) and dominance ( C ) between seasons and years. From the Jaccard similarity index, the highest similarity was between winter and spring, while the lowest was between summer and winter. Some species occurring exclusively in one season may be important to characterize different seasons. A list of the insect taxa associated with above-ground rabbit carrion during the four seasons was compiled, which can be used for estimating time since death in similar bio-climate areas.     

Species packing and temperature dependent competition among burying beetles (Silphidae, Nicrophorus)

Abstract. 1. Burying beetles are carrion feeders that specialize on small carcasses. We investigated interactions among congeners at two sites in Michigan, U.S.A., that differ in both number and relative proportion of species.
2. Intra- and interspecific competition for carcasses is intense. The majority of carcasses are found within 24 h of their placement.
3. Competition between N.arbicollis and N.defodiens is temperature dependent. N.orbicollis can displace N.defodiens on single carcasses, but requires warm temperatures to find the carcasses. Cool weather therefore serves as a refuge for N.defadiens .
4. The southern edge of N.defodien's geographical range is probably determined by competition with N.orbicollis .
5. N.sayi and N.tomenrosus are spring and autumn breeders respectively, and rarely interact with each other or the other two species. Nevertheless, interspecific competition is the most likely evolutionary force leading to seasonal segregation.     

Insects Associated with Pig Carrion in Two Environments of the Brazilian Savanna

Studies of carrion fauna have increased in Brazil and have contributed to the knowledge of this fauna in the national territory. Brazil has continental dimensions and presents various biomes in its territorial area. Most of the carrion fauna have seldom been studied, and this is especially true for the Savanna or “Cerrado.” The present research examined the fauna visiting carrion in two environments and two seasons in a rural area situated in a region of Cerrado in southeastern Brazil. The two environments studied were a pasture and a fragment of semi-deciduous forest. Samples were collected during the dry and humid seasons of the year. The study identified the diversity and relative abundance of species attracted to pig carcasses (Sus scrofa L.) exposed in each environment and season. Eight pig carcasses (10 ± 1 kg) were placed in traps, and adult insects attracted to the traps were collected during the decay of the carcasses. A total of 92,489 insects were collected during the experiments. The Diptera was the most frequent order (92.2%) represented by 27 families and at least 124 species. This was followed by Coleoptera (4.4%) represented by 14 families and at least 65 species. Sarcophagidae had the greatest diversity of species, followed by Muscidae and Calliphoridae. Several species were collected only during a specific period of the year or in a single environment. The results are important from an ecological point of view and for Medico-Legal Forensic Entomology.     

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.     

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.     

Inhibition of microorganisms on a carrion breeding resource: the antimicrobial peptide activity of burying beetle (Coleoptera: Silphidae) oral and anal secretions

Competition between scavengers and microorganisms for the nutrients within carrion is well documented. As a significant contributor to food web energetics, carrion serves not only as a food source for scavengers, but also as a reproductive resource for many insects. One example are the burying beetles of the Nicrophorus genus (Coleoptera: Silphidae) whose reproduction is dependent on locating and successfully sequestering vertebrate carrion. Throughout the cooperative preparation of carrion and feeding of the larval offspring, parental beetles coat the carrion with oral and anal secretions known to attenuate the growth of molds and bacteria in the laboratory. We test the hypotheses that Nicrophorus secretions attenuate the growth of naturally occurring microorganisms likely to be found colonizing the carrion resource, and that the active antimicrobial components of the secretions are small antimicrobial peptides (AMPs) similar to those produced by other insects.     

Effects of vulture exclusion on carrion consumption by facultative scavengers

Vultures provide an essential ecosystem service through removal of carrion, but globally, many populations are collapsing and several species are threatened with extinction. Widespread declines in vulture populations could increase the availability of carrion to other organisms, but the ways facultative scavengers might respond to this increase have not been thoroughly explored. We aimed to determine whether facultative scavengers increase carrion consumption in the absence of vulture competition and whether they are capable of functionally replacing vultures in the removal of carrion biomass from the landscape. We experimentally excluded 65 rabbit carcasses from vultures during daylight hours and placed an additional 65 carcasses that were accessible to vultures in forested habitat in South Carolina, USA during summer (June–August). We used motion‐activated cameras to compare carrion use by facultative scavenging species between the experimental and control carcasses. Scavenging by facultative scavengers did not increase in the absence of competition with vultures. We found no difference in scavenger presence between control carcasses and those from which vultures were excluded. Eighty percent of carcasses from which vultures were excluded were not scavenged by vertebrates, compared to 5% of carcasses that were accessible to vultures. At the end of the 7‐day trials, there was a 10.1‐fold increase in the number of experimental carcasses that were not fully scavenged compared to controls. Facultative scavengers did not functionally replace vultures during summer in our study. This finding may have been influenced by the time of the year in which the study took place, the duration of the trials, and the spacing of carcass sites. Our results suggest that under the warm and humid conditions of our study, facultative scavengers would not compensate for loss of vultures. Carcasses would persist longer in the environment and consumption of carrion would likely shift from vertebrates to decomposers. Such changes could have substantial implications for disease transmission, nutrient cycling, and ecosystem functioning.     

Traits reveal ecological strategies driving carrion insect community assembly

1. The succession of carrion-associated (necrophilous) insects on decomposing carrion is well documented. To exploit the changing nutritious and dynamic resources available throughout the carrion decomposition process, different species colonise and consume carrion in a predictable temporal sequence. The traits of these necrophilous insects should reflect their ecological strategies. Morphological traits of these insects, such as body size and wing size, however, have not previously been examined during active and advanced decomposition. 2. We used fourth-corner multivariate generalised linear models to identify insect community morphological trait patterns and to quantify their change through time on decomposing rabbit carcasses in grassland and woodland environments. 3. We found that larger-bodied species of flies and carrion-specialist beetles were associated with the early stages of decomposition. The morphological traits of ants, in contrast, showed no changes at carcasses through time and instead showed body size differences between grassland and woodland environments. 4. Our findings indicate that specialist flies and beetles that arrive early in the decomposition process possess traits that enable rapid discovery of carrion at a large scale. Generalist beetles and ants do not share this same trait and are instead adapted to locate and consume a wider variety of resources in their preferred habitat type at their local scale. 5. Our results provide insights into the morphological adaptations linked to the ecological strategies of distinct components of carrion insect communities. Further, our results offer insights into the community assembly dynamics that structure the communities of necrophilous insect species.     

Carrion mimicry in a South African orchid: flowers attract a narrow subset of the fly assemblage on animal carcasses

BACKGROUND AND AIMS: Although pollination of plants that attract flies by resembling their carrion brood and food sites has been reported in several angiosperm families, there has been very little work done on the level of specificity in carrion mimicry systems and the importance of plant cues in mediating such specialization. Specificity may be expected, as carrion-frequenting flies often exploit different niches, which has been interpreted as avoidance of interspecific competition. Interactions between the orchid Satyrium pumilum and a local assemblage of carrion flies were investigated, and the functional significance of floral traits, especially scent, tested. Pollination success and the incidence of pollinator-mediated self-pollination were measured and these were compared with values for orchids with sexual- and food-deceptive pollination systems. METHODS AND KEY RESULTS: Observations of insect visitation to animal carcasses and to flowers showed that the local assemblage of carrion flies was dominated by blow flies (Calliphoridae), house flies (Muscidae) and flesh flies (Sarcophagidae), but flowers of the orchid were pollinated exclusively by flesh flies, with a strong bias towards females that sometimes deposited live larvae on flowers. A trend towards similar partitioning of fly taxa was found in an experiment that tested the effect of large versus small carrion quantities on fly attraction. GC-MS analysis showed that floral scent is dominated by oligosulfides, 2-heptanone, p-cresol and indole, compounds that also dominate carrion scent. Flesh flies did not distinguish between floral and carrion scent in a choice experiment using olfactory cues only, which also showed that scent alone is responsible for fly attraction. Pollination success was relatively high (31·5 % of flowers), but tracking of stained pollinia also revealed that a relatively high percentage (46 %) of pollen deposited on stigmas originates from the same plant. CONCLUSIONS: Satyrium pumilum selectively attracts flesh flies, probably because its relatively weak scent resembles that of the small carrion on which these flies predominate. In this way, the plants exploit a specific subset of the insect assemblage associated with carrion. Pollination rates and levels of self-pollination were high compared with those in other deceptive orchids and it is therefore unlikely that this mimicry system evolved to promote outcrossing.     

Macroconsumer effects on insect detritivores and detritus processing in a tropical stream

1. Few studies have assessed the effects of macroconsumers, such as fishes and shrimps, on detritus and detritivores.
2. We used an underwater electric field to prevent macroconsumers from feeding in and on leaf packs in a lowland stream in Costa Rica and thus to determine their effects on the density of insect detritivores and decay rates of leaves.
3. Exclusion of macroconsumers resulted in significantly higher densities of small invertebrates inhabiting leaf packs. Most of these were collector–gatherers, none were shredders.
4. Despite the increase in invertebrate density, decay rates of leaves were not statistically different. These findings contrast with results from temperate streams showing that increases in the density of invertebrates in leaf packs typically result in an increased rate of decay.
5. Leaf decay rates and invertebrate densities were also compared between leaf packs placed in electric exclusion treatments and those placed in coarse (2 cm) plastic net bags (as used in many previous studies). Our results suggest that using such netting in tropical streams may deter macroconsumers, which can affect insect density and, potentially, decay rates of organic matter.     

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.     

Species Traits Predict Assemblage Dynamics at Ephemeral Resource Patches Created by Carrion

Carrion is an ephemeral and spatially patchy resource that supports a diverse subset of species linked to nutrient cycling and the decomposition process. A number of studies have separately documented changes in the diversity of plants, arthropods and vertebrates at individual carcasses, but there are few studies that have examined how functional traits of different groups of organisms underpin their responses to carrion patches. We used a carrion addition experiment to compare changes in composition and functional traits of insect and plant assemblages at carcasses compared with control sites. We found that significant changes in insect assemblage evenness and heterogeneity was associated with species’ dispersal traits, and that plant assemblage responses to subsequent soil nitrogen changes was most apparent among graminoids and exotic species. Beetles at carcasses were twice as large as their counterparts at control sites during the first week of carrion decomposition, and also had higher wing loadings. Plants with high specific leaf area responded faster to the carcass addition, and twice as many species recolonised the centre of carcasses in exotic-dominated grassland compared with carcasses in native-dominated grassland. These results provide an example of how traits of opportunist species enable them to exploit patchy and dynamic resources. This increases our understanding of how carcasses can drive biodiversity dynamics, and has implications for the way carrion might be managed in ecosystems, such as appropriate consideration of spatial and temporal continuity in carrion resources to promote heterogeneity in nutrient cycling and species diversity within landscapes.     

White‐headed Vulture Trigonoceps occipitalis shows visual field characteristics of hunting raptors

The visual fields of the Aegypiinae vultures have been shown to be adapted primarily to meet two key perceptual challenges of their obligate carrion‐feeding behaviour: scanning the ground and preventing the sun's image falling upon the retina. However, field observations have shown that foraging White‐headed Vultures Trigonoceps occipitalis are not exclusively carrion‐feeders; they are also facultative predators of live prey. Such feeding is likely to present perceptual challenges that are additional to those posed by carrion‐feeding. Binocularity is the key component of all visual fields and in birds it is thought to function primarily in the accurate placement and time of contact of the talons and bill, especially in the location and seizure of food items. We determined visual fields in White‐headed Vultures and compared them with those of two species of carrion‐eating Gyps vultures. The visual field of White‐headed Vultures has more similarities with those of predatory raptors (e.g. accipitrid hawks) than with the taxonomically more closely related Gyps vultures. Maximum binocular field width in White‐headed Vultures (30°) is significantly wider than that in Gyps vultures (20°). The broader binocular fields in White‐headed Vultures probably facilitate accurate placement and timing of the talons when capturing evasive live prey.     

Insect biodiversity meets ecosystem function: differential effects of habitat and insects on carrion decomposition

1. Ecological processes are maintained in different environments by different species performing similar functional roles. Yet, little is known about the role of the environment in shaping insect biodiversity associated with a process that is ephemeral and patchy. 2. In this study, the mass loss of carrion in response to contrasting habitat types (grassland or tree) was quantified experimentally, as well as the presence, diversity and composition of insect assemblages. Differences in insect assemblages between these two habitats were also examined. 3. It was found that the presence of insects led to a doubling in mass loss, but that grassland or tree habitat type had no effect on this process. By contrast, habitat type had a significant effect on the composition of generalist ant and beetle assemblages, but not on specialist fly assemblages. Given the colonisation of insects, carrion mass loss was negatively associated with increasing evenness of fly assemblages and increasing ant abundance. Variation in fly assemblage composition was also found to correlate with variation in carrion mass loss. 4. This study highlights the major role of habitat type in shaping the composition of generalist insects at carrion, but the minor role in affecting specialist and highly vagile insects. This complements the authors' findings that insect colonisation of carrion was critical to accelerated mass loss, and that fly assemblages were responsible for variation in this process, regardless of habitat. The present study sheds new light on the contribution of insect biodiversity to decomposition in variable environments, with consequences for carrion food webs and nutrient cycling.