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