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.