Introduction
Vertebrate scavengers consume an estimated 75% of carrion around the
world (Devault et al. , 2003). Yet, scavenging by vertebrates, as
a process had gained recognition only recently. Vertebrate scavengers
play important ecosystem functions such as nutrient cycling (Cederholmet al. , 1999; Danell, Berteaux and Bråthen, 2002) sanitation and
disease moderation (Markandya et al. , 2008), and competitive
interactions (Kaczensky, Hayes and Promberger, 2005; Materassi et
al. , 2017). Scavenging retains nutrients from carrion and recycles them
in the biotic component of the ecosystem that would otherwise get
released into the physical environment through decomposition, thereby
playing a regulatory role in biogeochemical cycles (Danell, Berteaux and
Bråthen, 2002). Instead of allowing carcasses to decompose completely at
a site, leading to a large ‘island’ of nutrients which may persist over
years (Danell, Berteaux and Bråthen, 2002; Benninger, Carter and Forbes,
2008; Parmenter and Macmahon, 2009) vertebrate scavengers, in
particular, assist in dispersing these nutrients over a larger
landscape. This reduces the excessive concentration of nutrients such as
Phosphorus, Sodium and Potassium around carrion (Benninger, Carter and
Forbes, 2008; Parmenter and Macmahon, 2009) which would inhibit
vegetation growth (Towne, 2000). Obligate vertebrate scavengers remove
carrion more efficiently and rapidly than facultative scavengers or
decomposers (Ogada et al. , 2012). The highly acidic digestive
tract and gut microbiome of specialized scavengers such as vultures
reduces the transmission of pathogens and consequently the risk of
disease spread from decomposing carcass (Houston and Cooper, 1975;
Roggenbuck et al. , 2014; Graves, 2017; Zepeda Mendoza et
al. , 2018). In the absence of obligate vertebrate scavengers,
accumulation of carrion over longer durations, competitive release of
facultative scavengers, and disease transmission through facultative
scavengers can have serious ecological ramifications that are poorly
understood. In light of the global declines of vertebrate populations,
understanding these aspects of carrion ecology becomes vital. Such
insights can bolster the scientific rationale and global efforts for
conservation of vertebrate populations.
Quantifying the relative contribution of vertebrate scavengers to
carrion removal in comparison with invertebrate scavengers and microbial
decomposition allows us to better understand the role of different
scavenging communities, which in turn can inform conservation policy.
Conserving the diversity of scavenger assemblages is important in the
light of biodiversity loss (Cardinale et al. , 2012), as this
enhances functional redundancy, thereby stabilizing scavenging systems.
Previous studies have shown that manipulative reduction of a dominant
scavenger (raccoons Procyon lotor ) in an agricultural landscape
reduced system efficiency and left more carcasses un-scavenged (Olsonet al. , 2012). Exclusion of vultures from carcasses did not
increase carcass visitation or utilization by facultative scavengers and
resulted in 10-fold greater un-scavenged carcasses, indicating that
facultative scavengers cannot replace obligate vertebrate scavengers
completely (Hill et al. , 2018). Yet, in other ecoregions, the
decline of top predator and scavenger (Tasmanian devil Sarcophilus
harrisii ) or exclusion of dominant scavengers resulted in higher
detection and utilization of carcasses by meso-predators,
notwithstanding increased persistence time and availability of carrion
to decomposers (Cunningham et al. , 2018; Tobajas et al. ,
2021). Thus, the loss of apex vertebrate scavengers may elicit
differential responses in scavenging communities and carrion persistence
between eco-regions. Although rapid removal of carrion by vertebrates
was a consistent finding of the above studies, they became less
efficient in handling carrion at high carrion densities mimicking Mass
Mortality Event (>350kg/20 m2) that led
to reduced nutrient cycling, die-offs of vegetation and trees due to
nutrient overload, and subsequent introduction of new plants in the area
(Tomberlin et al. , 2017). As scavengers and decomposers compete
for carcasses, Devault et al. (2004) found that contribution of
vertebrates in removing carrion reduced and that of decomposers
increased with increasing ambient temperature, indicating an
environment-dependent outcome of such competition. However, studies that
compare carrion removal rates between scavenger types and decomposers
are lacking.
Our experimental study attempts to understand carrion removal in a
forested landscape of Central India, by estimating the utilization of
carrion by vertebrate scavengers compared to invertebrates, microbes
(decomposers), and moisture loss (control). We addressed this question
by placing chicken carcasses under uniform environmental conditions in
four experimental set-ups that excluded either or all of the scavenging
guilds (i.e. vertebrates, invertebrates, microbes and control). We
measured daily carcass biomass to compare removal rates between
scavenging guilds using linear mixed effect models. Our study showed
that vertebrate scavengers contributed to maximum carrion removal per
day, followed by invertebrate scavengers, and microbial decomposition.
Methods