Supplementary feeding and endoparasites in threatened avian scavengers: Coprologic evidence from red kites in their wintering stronghold

Highlights

• Red kites feeding on livestock carcass show higher helminth infections than those feeding on wild prey.

• Overcrowding of kites foraging on livestock carcasses can increase the acquisition and transmission of parasites.

• Supplementary feeding stations can promote the spread of parasites to wintering individuals.

Abstract

Many obligate and facultative avian scavengers are increasingly dependent on food provided in supplementary feeding stations (SFS), which are managed for the conservation of these species. Deliberate feeding can influence disease-related host demography and population dynamics through physiological changes and density-dependent parasite acquisition and transmission, but information on this threat to avian scavengers is scarce. Due to their effects on host aggregation and density, we hypothesised that the predictability and concentration of food in SFS can exacerbate parasite infection. This hypothesis was tested by comparing the prevalence, richness, abundance and mixed infection of endoparasites (coccidia and helminths) in red kites Milvus milvus foraging on livestock carcasses (mostly of pigs and poultry) in overcrowded and confined conditions at SFS, relative to those foraging alone or in small groups on wild prey unevenly randomly distributed within large areas during winter, mostly wild rabbits (Oryctolagus cuniculus). No clear differences were found between areas with and without SFS in the prevalence and abundance of oocyst of Eimeria. This coccidian genus appears to include parasites of the prey rather than the raptors, thus representing parasite transport or pseudo-parasitism rather than actual parasitism in the kites. A higher prevalence and richness of helminths, as well as mixed infections with several phyla, was found in kites exploiting SFS than in those feeding on wild prey in the area without SFS. The unsanitary conditions derived from the stack of livestock carcasses and the contamination of carrion with the faeces of multiple scavenger hosts can increase the accumulation and persistence of helminths eggs and intermediate hosts. The regular use and frequent confinement of large numbers of red kites at SFS can promote the spread of parasites to a large proportion of the European breeding population distributed across Spain during the winter. We encourage that carcasses of free roaming livestock can be left in the countryside, as well as the conservation management of wildlife exploited as food by red kites (especially wild rabbits), to attempt avoiding overcrowded and confined conditions at SFS. Further research is required to assess the impact of deliberate feeding on the spread of parasites and other disease agents in the threatened species SFS are intended to favour.

Introduction

The influence of human activities on the disease dynamics of wildlife populations is gaining increasing attention for its implications on biodiversity conservation and environmental health (Daszak et al., 2000, Aguirre and Tabor, 2008, Keesing et al., 2010, Gottdenker et al., 2014). In particular, human activities are increasingly altering food and foraging conditions of many wildlife species worldwide (Fischer and Lindenmayer, 2007, Sih et al., 2011, Oro et al., 2013). By providing food in predictable foraging sites, humans can intentionally or unintentionally modify the behaviour, distribution, and density of wildlife populations (Robb et al., 2008, Oro et al., 2013, Kubasiewicz et al., 2016). This can influence disease-related host demographics and population dynamics through physiological changes and density-dependent processes such as parasite acquisition and transmission (Arnsberg et al., 1998, Lebarbenchon et al., 2006, Becker et al., 2015). Therefore, evaluating whether the prevalence of particular parasites and concurrent infections are due to the hosts’ habits and environmental features which are influenced by anthropogenic effects is fundamental to understanding the health and dynamics of wildlife populations.

A wide array of parasites exploit the limited resources of their avian hosts, which promote diverse immune responses mediated through nutritional condition, and eventually can cause disease and death (Clayton and Moore, 1997, Ardia and Schat, 2008). Condition-dependent investment in immunity against parasites can be shaped by food availability and different diet compositions that influence nutritional status, which is a main component of individual quality determining individual fitness (Nelson, 2002). In addition, diet can determine the acquisition of food-borne parasites and pathogens (Friend and Franson, 1999, Mor-Mur and Yuste, 2010; Wiethoelter al, 2015). Other factors, such as foraging grounds, sociality, density and food searching strategies can also influence parasite acquisition and transmission (Arnsberg et al., 1998, Lebarbenchon et al., 2006, Becker et al., 2015). Knowledge on how these factors influence the prevalence and effects of parasites on raptors (Falconiformes and Accipitriformes) come from surveys of dead individuals with and without disease signs in recovery centres, or by examination of patent effects of disease during outbreaks (Friend and Franson, 1999, Lumeij et al., 2000). Comparatively less information has been obtained from apparently healthy individuals in wild populations (e.g. Coulson et al., 2010). Depending on virulence, the prevalence of parasites evaluated by random sampling in the wild can be influenced by the fact that infected individuals may be lost at variable rates due to associated mortality (Wobeser, 2013). Experiments relating infection and increasing parasite burdens with poor health and mortality can shed light on the role of parasites in population regulation (Pedersen and Fenton, 2015). In practice, experimental approaches involving threatened species are challenging, and it requires previous baseline information of the wide array of pathogens and parasites generally infecting the wild threatened populations (Wobeser, 2013). In addition, knowledge is very limited for wild birds on how environmental and population conditions and associated related habits, such as diet and overcrowding influence infection and transmission of parasites (Friend et al., 2001, Lebarbenchon et al., 2006, Ardia and Schat, 2008). Obtaining this kind of baseline information can be especially relevant for conservation purposes of threatened species (Cleaveland et al., 2002, Smith et al., 2006, Thompson et al., 2010).

Obligate and facultative avian scavengers are among the most threatened vertebrates (Ogada et al., 2012, Buechley and Şekercioğlu, 2016). Due to environmental degradation and intensification of agriculture affecting wild food sources, many scavenger species are increasingly dependent on carcasses of domestic livestock in supplementary feeding stations (SFS), which are managed for the conservation of these species (Cortés-Avizanda et al., 2016). The predictability and availability of food can determine the degree of the host's infection of particular parasites and pathogens (Lebarbenchon et al., 2006, Becker et al., 2015). Despite satisfying these conditions, few data are available on the role of SFS on scavengers’ nutritional condition and disease. This role can be amplified based on the dynamics and demographics of scavengers’ populations through several processes. First, food abundance and predictability can attract multiple conspecific and heterospecific scavengers, thus artificially increasing the host spatial concentration, overcrowding, intra- and inter-specific agonistic interactions, and spread of parasites in a particular location and its effects on stress and density-dependent host to host infection probability (Wright and Gompper, 2005, Lebarbenchon et al., 2006, Becker et al., 2015). Second, livestock carcasses from different farming operations, especially confined farming versus free-ranging farming operations, can vary in the probability of transmission of food-borne parasites and pathogens to scavengers, and it can differ from those acquired from wild animals exploited as food of the host (Cortés-Avizanda et al., 2016). Third, diet can have an indirect effect on parasite acquisition and infection intensity through the scavengers exposure to livestock pharmaceuticals which predispose opportunistic infections, especially broad-spectrum antibiotics disrupting normal flora and then allowing infection by bacterial and fungal pathogens (Keeney et al., 2014, Blanco, 2015, Blanco et al., 2017). These factors can also have variable impacts on host nutritional condition which can directly and indirectly influence the host's immunological state, pathogen acquisition, and overall health (Ardia and Schat, 2008, Becker et al., 2015, López-Rull et al., 2015). However, all these factors remain poorly understood in regards to their implications in the management and conservation of avian scavengers.

Coccidia and helminths are among the most common endoparasites in raptors. Both groups of parasites can cause malnutrition in their hosts because they provoke malabsorption, digestive problems and competition for resources. Often these parasites promote anaemia, weakness and are carriers for other parasites. In addition, immunosuppression due to infection by particular parasites may enhance host susceptibility to a concurrent infecting organism (Norris and Evans, 2000). These consequences are most common in young and debilitated individuals during stressful conditions (Friend and Franson, 1999, Lumeij et al., 2000, Klaphake and Clancy, 2005, Cooper, 2008). Infected animals spread helminths eggs and coccidian oocysts in faeces, so that other individuals can become infected when frequenting places where faeces accumulated due to stacked food and the habitual presence and overcrowding of foraging individuals (Wright and Gompper, 2005, Lebarbenchon et al., 2006, Becker et al., 2015). Helminths often occur in mixed infections involving several phyla (Sánchez-Andrade et al., 2002, Santoro et al., 2012) in combination with coccidian infections (Lumeij et al., 2000, Klaphake and Clancy, 2005, Cooper, 2008). Some coccidian species may cause disease (coccidiosis) producing diarrhoea and other detrimental effects that can lead to death in young of weak individuals. Other species can be transiently present without causing pathological effects due to the consumption of infected prey (Upton et al., 1990, Redig et al., 1993, Forbes and Fox, 2000).

In this study we investigated whether feeding habits associated with food availability and predictability at SFS were related to differences in the prevalence of endoparasites in a threatened generalist predator and facultative scavenger, the red kite Milvus milvus. Specifically, we compared diet and endoparasite prevalence and intensity in red kites foraging in areas with and without SFS. Previous studies have recorded through necropsy the presence of Capillaria sp. and other nematodes, as well as cestodes, trematodes and acanthocephalans in facultative and obligate scavenger species admitted in recovery centres (Sánchez-Andrade et al., 2002, Ferrer et al., 2004, Sanmartín et al., 2004, Santoro et al., 2010, Santoro et al., 2012), but little information is available for red kites (Krone, 2000, Sánchez-Andrade et al., 2002, Komorová et al., 2015), and no study cited the prevalence of coccidia in this species (see review by Duszynski et al. (1999)).

The red kite is listed as globally threatened because of steep population declines (BirdLife International, 2016), particularly in the Spanish breeding and wintering grounds (Viñuela et al., 1999, Mougeot et al., 2011). Despite these concerns, no study has evaluated the prevalence and intensity of parasitism and disease in this species or the environmental factors that can influence these traits in the wild. Previous studies have shown differences in diet composition of wintering populations, especially regarding the consumption of livestock carcasses depending on the farming and livestock residue elimination operations (Blanco, 2014a). The high predictability and abundance of food at SFS promote the repeated use of these places, a high abundance, density, and gregariousness of foraging red kites (Serrano, 1999, Viñuela et al., 1999, Contreras, 2001) and other scavenger species (Blanco, 1994, Blanco, 1996, Cortés-Avizanda et al., 2010). Deliberate feeding at SFS provides excellent opportunities to explore the consequences of overcrowding on parasite acquisition and transmission, as well as the related impact of food features (e.g. the content of pathogens and pharmaceuticals) and foraging grounds on infection and disease. Due to their effects on host aggregation and density (Arnsberg et al., 1998, McCallum et al., 2001), the predictability and concentration of food can exacerbate parasite infection (Lebarbenchon et al., 2006, Becker et al., 2015). This hypothesis predicts an increased kite exposure to endoparasite propagules from accumulated and concentrated faeces from overcrowded conspecifics and other scavengers foraging in the small specific locations of SFS (Cortés-Avizanda et al., 2010, Cortés-Avizanda et al., 2016) relative to those foraging alone or in small groups on prey randomly distributed within large areas (Heredia et al., 1991, Hiraldo et al., 1991, Viñuela et al., 1999). This is based on the fact that propagules of helminths and coccidia, as well as other disease agents, can remain viable for long periods in faeces and sludge while also fostering intermediate hosts and vectors (Anderson, 2000, World Health Organization, 2004, Botzler and Brown, 2014), thus contributing to increased host infection and re-infection in overcrowded conditions at SFS.