Discussion

There is little information on carrion removal rates by various carrion feeders in tropical forests. Although limited by sample size, our experiments allowed direct comparison of carrion removal rates between vertebrates, invertebrates, and microbes. After adjusting for carrion losses to other treatments, vertebrate scavengers removed carrion much faster than did invertebrates and microbes (figure 4). However, the daily removal of 83% of biomass by vertebrates was for carcass less than 2 kg, and removal rates would likely decrease with larger carcasses, as scavengers could potentially reach satiation. Nonetheless, the study showed drastic differences in carrion removal rates between taxa, and indicated the irreplaceable role of vertebrates in the scavenging community of tropical forests, without whom carcasses persisted over prolonged time periods. Thus, our results support earlier studies that found overwhelming influence of vertebrate scavengers on carrion removal compared to other scavenging / decomposing guilds (Devault, Brisbin and Rhodes, 2004; Cunningham et al. , 2018).
With vertebrates removing a majority of carcass biomass in a short time, most of the nutrients were retained and recycled in the biosphere. Vertebrate scavengers consumed chicken carcasses completely, down to the bones and skin. Invertebrates removed only the soft tissue, leaving the bones, skin and feathers behind. This would need to be mineralised by microbes or consumed by vertebrates to re-enter the biotic sphere. Vertebrate consumption ensures that these minerals – particularly calcium from bones – is at least partly retained in the biotic sphere, instead of its slow loss into abiotic environment, thereby playing an important ecosystem function. Quantitative studies on nutrient cycling through scavenging are rare (Barton et al. , 2013; Macdonaldet al. , 2014), and little is known about the proportions of nutrients absorbed into scavengers from carrion and thereby retained within the biosphere. We can assume that nutrient retention from carrion to scavengers would follow Lindeman’s ‘Ten Percent Law’ of energy transfer between trophic levels (Lindeman, 1942; Brown and Gillooly, 2003). This would likely differ between tropical and temperate regions, with nutrient cycling likely much faster in tropical regions than in temperate regions where cold climate may inhibit microbial action. Very few studies have examined the bioenergetics of carrion so far, with some exceptions (Putman, 1978).
Although invertebrates remove carrion at a slower rate than vertebrates, they do play an important role in decomposition of carcasses and nutrient cycling (Coleman and Hendrix, 2000). Exclusion of invertebrates from a carcass for the initial days decelerated carcass decomposition by several days (Pechal et al. , 2013). Thus, even in the paucity of vertebrate scavengers, nutrient recycling will be continued by invertebrate scavengers, but at a slower rate in a tropical dry deciduous forest system. Little is known about invertebrate scavenging, as a process. Future studies are required on succession in invertebrate community as the carrion decomposes, interactions with microbes during carrion decomposition, and if carrion removal rates are influenced by the diversity of invertebrate scavengers. Putman (1978) found that most of the carrion in the form of mouse carcasses was removed by blowfly larvae, among invertebrates. Another study found that carcass size and type of carrion influenced the dipteran community (Kneidel, 1984). Only two dipteran species which were more specialised with respect to season were found on mouse carrion, while a greater number of dipteran species which were less season-specific consumed other types of carrion.
Besides the quantification of carrion removal rate by different groups, our study yielded many qualitative observations which can contribute to the understanding of carrion natural history. When invertebrates were not excluded from carcasses, flies discovered carrion within a few hours and laid eggs. Maggots hatched after two to three days and consumed most of the carrion over a period of several days if vertebrates were excluded. Some beetles were also observed on/around carcasses but in less numbers than flies and their larvae. Feathers and skin slowed down their consumption; most of the consumption took place where the skin or flesh was exposed to invertebrates. When vertebrates were not excluded, several species visited carcasses such as the Red-Headed Vulture, Egyptian Vulture, Striped Hyena, and Leopard (Figure 3). These species were amongst the first to discover and consume carcasses. Other species which visited the carcass, but subsequently, were Wild Pigs, Ruddy Mongoose, Golden Jackal and Indian Fox. Most scavenging by mammals took place after sunset, while scavenging by vultures was entirely during the day.
Among obligate scavengers, the critically endangered Red-headed Vultures were the most photocaptured at the experimental carcasses followed by Egyptian Vultures. Considering their size, chickens might be predicted to be too small for these vultures. However, as many as five red-headed vultures – normally found in pairs or solitarily – were captured feeding on a single chicken carcass (Figure 3). Three of these appeared to be juveniles. Interestingly, a goat carcass placed nearby – although not at the same time – was not visited by any vultures at all. This could be due to random chance, or because of some difference in detectability. For example, the bright white feathers of the chicken might be more noticeable for a gliding vulture than a dark-coloured goat. An experiment to control for these factors with respect to detection of carcasses may reveal more. Among the species that were not captured at carcasses in the experiment, but were present at other carcasses or sighted in the area include Tiger, Cinereous Vulture, Jungle Cat, and Common Palm Civet.
Our findings, especially the estimates of carrion removal rates, could have been influenced by several ecological factors that were beyond the control of this experiment. Relative abundance of vertebrate scavenger species would influence carrion removal rates; e.g., carrion removal rates might differ between the study area and a different forest with fewer vultures but higher numbers of top and meso- mammalian predators. Carcass size is another important factor. Removal rates would have slowed down if larger carcasses such as goats or cattle were used, as individual scavengers that discovered the carcass became satiated. Further, invertebrate scavengers might take advantage of such larger resources and respond numerically due to their shorter generation times and thereby contribute more to carcass removal than currently estimated. We account for moisture loss by desiccation under natural conditions, and as seen in Fig. 2, moisture loss was a function of ambient humidity and temperature, on day five of the treatment there was mild rain and the carcasses gained weight. Whilst there was a non-significant difference in removal rates between microbes and control (evaporative moisture loss) (Table 2), this could imply that either microbes contributed negligibly to the removal of carrion, or the anti-microbial treatment in our control samples was not effective in reducing microbial activity and our estimates of moisture loss was compounded by some microbial losses. However, this issue does not affect the comparison of carrion removal rates between vertebrates and invertebrates. Our experiment spanned a single season (early summer) and did not capture seasonal variations in environmental conditions that could influence relative contribution of scavenger groups, and the absolute removal rates. Our sample size was also small that might have resulted in large variability in proportional weight of carcasses over time (Figure 2).
Whilst our field experiment provided some insights, many questions remain to be answered to further our understanding of carrion ecology in tropical forests. a) Effects of relative abundance of different species in the scavenging assemblage on carrion utilization (Huijbers et al. , 2016; Morales-Reyes et al. , 2017; Naves-Alegre et al. , 2021), b) succession of scavenging groups on carrion, c) influence of carrion size on the richness, abundance, composition and succession of scavenger community are some of these questions. Our experimental approach and inferences can form the foundation on which studies investigating the above questions can be developed.
Figure Legends
Figure 1: Experimental setup for observing carrion biomass loss due to different treatments (Clockwise from Top Left): 1. A chicken carcass being weighed after exposure to invertebrate scavenging; 2. vertebrate scavenging – carcasses were placed in the open and monitored through infrared camera traps; 3. invertebrate scavenging – carcasses were placed in a wire cage to exclude vertebrate scavenger; 4. microbial activity – carcasses were placed in cloth bags and hung in a wire cage to exclude invertebrates and vertebrate scavengers. Control carcasses were also placed similarly after treatment with an antimicrobial agent.
Figure 2: Boxplot showing distribution of proportional carcass biomass remaining over days for each treatment.
Figure 3: Some vertebrate scavenger species captured at experimental carcasses. Clockwise from top left - Red-headed Vulture (Sarcogyps calvus ), Egyptian Vulture (Neophron percnopterus ), Golden Jackal (Canis aureus ), Leopard (Panthera pardus ), Indian Fox (Vulpes bengalensis ), Striped Hyena (Hyaena hyanea ). Bottom: A group of Red-Headed Vulture and an Egyptian Vulture feeding on an experimental chicken carcass.
Acknowledgements
We would like to thank the Chief Wildlife Warden, and Chief Conservator Forests of the Madhya Pradesh Forest Department for granting permissions to carry out the field work. We thank the L. Krishnamurthy, Field Director Kanha Tiger Reserve, K.S. Bhadoria, Field Director of Panna Tiger Reserve, and the Madhya Pradesh Forest Department Staff , for all their support and facilitation. We thank the Director, Dean, Course Director and Assistant Course Director of XVI MSc Course, and faculty at WII. The field work was funded by a grant from Raptor Research and Conservation Foundation (RRCF) and facilitated by Kiran Srivastava. Bruce Marcot is thanked for useful comments on the study proposal. BI gratefully acknowledges the following field assistants and forest department staff for their assistance: Kanhaiya, Nirottam, Sampat, Suraj, and Manjula in Kanha, and Lal Singh and the tiger tracking teams of Panna. BI thanks XVI MSc students, and Shravana, Jayant, Anjali, Manish, Pratik, Ujjwal and Neha, K Ramesh and his team, particularly Deepti, Kamna, Supratim and Darshan for assistance and facilitation.
Author Contributions
BI – Study design, funding acquisition, data collection, analysis, Writing—Original Draft. YVJ – Study design, methodology, review and editing, supervision, funding acquisition. SD - Study design, methodology, review and editing, supervision. QQ - Study design, methodology, supervision.
Data Accessibility
The authors confirm that the data supporting the findings of this study are available in the appendix and on FigShare.
Funding
This work was conducted by BI as part of a dissertation for the award of a Master’s degree in Wildlife Science from Saurashtra University, through the Wildlife Institute of India. It was funded by the Wildlife Institute of India and the Raptor Research and Conservation Foundation (RRCF).
Competing Interests
The authors declare no competing interests.