Latitudinal patterns in the diet of Andean condor (Vultur gryphus) in Chile: Contrasting environments influencing feeding behavior

Highlights

• Anthropized environments alter availability of resources for Andean condors.

• Little evidence as to how condor's diet vary along their large latitudinal range

• Introduced domestic and exotic species are common Andean condor prey across Chile.

• Condors in anthropized areas use C₄-based food from landfills/corn-fed livestock.

• Anthropic subsidies may help stabilize populations, also enhance mortality risks.

Abstract

Human-dominated environments alter the availability and quality of resources for many species, especially for scavengers that have large home ranges and plastic foraging behaviors that enable them to exploit novel resources. Along the western slope of the Andes, the modification of natural landscapes have resulted in significant declines in native prey, the introduction of non-native species, and an increase in the availability of anthropogenic resources. These factors have likely influenced the resources available to Andean condors (Vultur gryphus), however, data are lacking as to how condor's diet vary along their large latitudinal range. We evaluated differences in Andean condor diet along a ~2500 km latitudinal gradient in Chile from the heavily modified Central zone (32–34°S) to the more pristine Austral zone (44–56°S). We assessed diet composition through the identification of prey remains in condor pellets, and carbon and nitrogen isotope analysis of condor feathers and their primary prey identified from pellet analysis. Our results identified medium- and large-bodied domesticated mammals (ungulates) and introduced exotic species (lagomorphs) as common prey across the study area. Condors from the Central zone had the largest isotopic niche width, probably related to consumption of anthropogenic resources with distinctly high carbon isotope values indicative of C₄-based foods likely acquired from landfills or corn-fed livestock. Isotopic niches for condors from the Southern and Austral zones almost completely overlapped. Andean condor diet is strongly influenced by local conditions determining differential access to prey sources. The high dependence of Andean condors on livestock across a large geographical area, and landfills in more (sub)urban areas, may help stabilize their populations via anthropogenic resources subsidies. Long-term dependence on such resources, however, may have health costs including contaminant exposure and greater mortality risk. These data will help identify potential threats related to resource availability and use, and better inform management and conservation decisions.

Introduction

Land-use activities have transformed >50% of the Earth's surface to provide humans access to critical natural resources and ecosystem services. The clearing of natural forest and grassland ecosystems for forestry, agricultural, and livestock production, and more recently for (sub)urban and industrial expansion (Ellis et al., 2010), has influenced the availability and quality of resources on which many species rely (Barbar et al., 2015). In particular, predators (Newsome et al., 2015) and scavengers (Cortés-Avizanda et al., 2016) have been disproportionately impacted by both direct (e.g., overhunting) and indirect (e.g., habitat loss) anthropogenic influences. Vulture populations in particular have been severely affected as a result of negative interactions with humans (Ogada et al., 2012) and currently 52% of vulture species are threatened with extinction worldwide (IUCN, 2020).

Large-bodied soaring scavengers such as vultures have extensive home ranges and can efficiently search large areas to locate patchily distributed prey (Barbar et al., 2015). In natural environments, seasonal variation in mortality and movement of potential prey strongly influences the territory and movement of scavengers (Kendall et al., 2014; Newsome et al., 2015; Lambertucci et al., 2018; García-Jiménez et al., 2018). In anthropized environments, domestic herbivores as well as introduced wild herbivores change the species composition and abundance of prey for scavengers (Jaksic et al., 2002; Vázquez, 2002), which results in close and in some cases obligatory ecological relationships between introduced herbivores and scavengers (Barbar et al., 2016). Population declines of natural prey, the presence of veterinary drugs in carcasses, sanitary regulations, and livestock management strategies can alter prey availability, and may have contributed to large-scale declines in Old World vultures (Donázar et al., 2009; Margalida et al., 2014, Margalida et al., 2017; Buechley and Şekercioğlu, 2016; Arrondo et al., 2018). While livestock may benefit scavengers by providing resource subsidies (Jaksic et al., 2002; Vázquez, 2002), these sources of prey have also been identified as high-risk resources that may impact scavenger health and by extension lead to increased mortality risk (Blanco et al., 2017). Although livestock carcass dumps, landfills, and even fisheries bycatch have become a novel and relatively predictable food source for scavengers (Cortés-Avizanda et al., 2016; Tauler-Ametller et al., 2017), the use of these resources may be associated with either beneficial and detrimental health effects (Plaza and Lambertucci, 2017).

The Andean condor (Vultur gryphus) is the largest avian scavenger in South America and occurs along the Andes mountain range from ~5°N to 55°S latitude (Del Hoyo et al., 1994). In most areas in this distribution, condor populations have declined due to poisoning, hunting, and decreases in resource availability. Only in the southernmost margin of its range does condor population size appear to be more dense (Lambertucci, 2010; Pavez, 2012) and stable (Jaksic et al., 2001). Like other scavengers, the Andean condor has had to adapt to a changing environment and to modify its foraging behavior and diet (Lambertucci et al., 2009, Lambertucci et al., 2018). Historically, Andean condors consumed a combination of marine resources sourced from the productive Humboldt Current (Lambertucci et al., 2018) and native terrestrial resources such as guanacos (Lama guanicoe) and lesser rheas (Rhea pennata) (Lambertucci et al., 2009). In addition to dramatic declines in native fauna (Ceballos, 2002), a suite of terrestrial mammals (e.g., red and fallow deer, wild boar) were introduced to Chile and Argentina more than a century ago (Jaksic et al., 2002) and are considered to be an ecological plague that have negative impacts on agriculture, livestock, and native vegetation and fauna (Vázquez, 2002). Some introduced species such as the lagomorphs like European hares (Lepus europaeus) and rabbits (Oryctolagus cuniculus) may also provide an indirect ecological benefit by serving as an alternate source of prey to large native predators and by extension decreasing predation pressure on native herbivores (Jaksic et al., 2002). These two lagomorph species, along with the introduced red deer (Cervus elaphus) and wild boar (Sus scrofa) are important dietary components of Andean condors inhabiting some regions of Chile and Argentina (Lambertucci et al., 2009; Perrig et al., 2016; Ballejo et al., 2017; Pavez et al., 2019). At present, Andean condors feed primarily on introduced terrestrial mammals (e.g., ungulates and lagomorphs) that are the most abundant sources of carrion in rural environments (Lambertucci et al., 2009; Ballejo et al., 2017; Pavez et al., 2019). Nevertheless, livestock production over the past 50 years in Chile has declined up to 40%, and along with the intensification and technological advances of livestock production strategies has led to a decrease in the availability of carrion to Andean condor populations, especially in the central area of the country (INE, 2018). While Andean condors have historically avoided habitats extensively modified by human activities (Wallace and Temple, 1988), the recent decline in ranching activities and the scarcity of native prey in central Chile (Pavez, 2012) have changed their feeding behavior to include more reliable sources of anthropogenic foods in landfills and (sub)urban areas (Pavez et al., 2019).

Although the diet of Andean condors has been studied previously (Wallace and Temple, 1987; Lambertucci et al., 2009; Perrig et al., 2016; Pavez et al., 2019), all of these efforts focused on a single population in a relatively small area of the species large latitudinal range. The objective of our study was to characterize Andean condor diet across a wide latitudinal range of >2500 km (from ~32 to 56°S) along the western slope of the Andes to assess spatial variation in prey composition that may relate to varying levels of anthropogenic influence. We use faunal analysis of condor pellets collected from 20 roosting sites coupled with carbon (δ¹³C) and nitrogen (δ¹⁵N) isotope analysis of condor feathers and potential prey sources. This work provides a better understanding of the role that different sources of prey are playing in maintaining condor populations across Chile, which currently hosts ~70% of the global populations of this iconic species. These data may also help identify potential threats related to local resource availability and used to guide management decisions for Andean condor conservation strategies.