The trade-offs of foraging at landfills: Landfill use enhances hatching success but decrease the juvenile survival of their offspring on white storks (Ciconia ciconia)

Highlights

• Landfill use by parentals improves hatching success.

• Landfill use by parentals has negative effects on juvenile survival.

• Landfill use implies benefits for current reproduction but costs for future offspring survival.

Abstract

During the last decades, landfills have become a valuable food source for wildlife, being in some cases determinants of large avian population increases. Superabundant food resources at landfills can increase reproductive and/or survival parameters; however, negative effects such as intoxication, plastic ingestion, skeletal deformities, unbalanced oxidative stress, and other health problems have also been reported. White stork (Ciconia ciconia) commonly benefits from landfill resources. Here, we evaluate potential landfill effects on demographic parameters (reproduction and offspring survival) at the individual level in a single population.

Our results show that a more intense use of landfills by breeders has a positive effect on hatching success but a negative effect on juvenile survival probability after emancipation, at least during the first year of life. High amount of food and proximity to landfill may explain their beneficial effect on reproductive parameters. On the other hand, poor quality food, pollutants, and pathogens acquired during early development from a diet based on refuse may be responsible for reduced future survival probability. Consequently, both positive and negative effects were detected, being foraging at landfills at low to medium levels the better strategy. Although our study shows that intense foraging on rubbish can imply both costs and benefits at an individual level, the benefits of superabundant food provisioning observed at population level by other studies cannot be ignored. Management actions should be designed to improve natural food resources, reduce non-natural mortality and/or human disturbances to guarantee the species viability under current European Union regulations designed to ban open-air landfills in a near future.

Introduction

Around one third of total worldwide food production is wasted or lost in supply chains (FAO, 2011). In the European Union, this translates to 88 million tonnes of food are wasted yearly and mainly end up in landfills (Stenmarck et al., 2016), transforming these facilities in a worldwide, predictable, abundant, and anthropogenic food resource for wildlife. Since feeding on landfill facilitates food accessibility, reduces energetic costs typically associated with food foraging on wilderness, and diminishes competition for feeding resources, it implies several benefits to landfill scavengers at both population and individual levels (Oro et al., 2013; Plaza and Lambertucci, 2017). As a consequence, a large diversity of animal species have changed their behaviour to take advantage of anthropogenic food refuse (Oro et al., 2013; Plaza and Lambertucci, 2017). The superabundant food provided by landfills can improve the body condition as well as the reproductive parameters of species exploiting these resources (Auman et al., 2008; Djerdali et al., 2016a; Eley et al., 1989; Steigerwald et al., 2015; Tortosa et al., 2003). Furthermore, easy food access and predictability associated with landfills imply an increase on individual survival (Eley et al., 1989; Rotics et al., 2017). Thus, for some species, landfill use promotes population growth and plays a key role for the recovery of vulnerable or endangered species (Tauler-Ametller et al., 2017).

Anthropogenic leftovers are, however, usually poor-quality food (Grémillet et al., 2008; Murray et al., 2018) and, in landfills, organic waste is mixed with other non-beneficial items (e.g., metals, plastics, glasses, wires, and different toxic products or pollutants) that may cause amputation, suffocation, and/or intoxication (Matejczyk et al., 2011). Nutrition is a key component of animal health, particularly on early development, with important consequences on future phenotypic traits (Lindström, 1999). Lack of essential micronutrients linked to low quality food available at dumps could modify morphological or behavioural traits and jeopardize future individual survival (Catoni et al., 2008; Noguera et al., 2015; Richardson et al., 2019). In the same vein, dense aggregations of individuals in predictable rubbish subsides may also involve a wide range of health issues on immune system including higher probabilities of pathogen transmission which potentially effects reproduction and/or survival (Becker et al., 2015; Plaza and Lambertucci, 2018). Finally, landfills favour aggregation of breeding individuals in their periphery (Bialas et al., 2020), reducing the time that breeders spend away from their breeding sites (Moritzi et al., 2001). These animals are attracted by food abundance, which would lead to an increase of competence (i.e. nesting places) (Djerdali et al., 2016a; Gilchrist and Otali, 2002). In summary, both positive and negative effects on life history traits that play a key role on population dynamics can occur as a consequence of landfill use by wildlife (Oro et al., 2013).

The white stork (Ciconia ciconia) is a good model species to study landfill use effects on wildlife. The white stork is a species for which numerous positive effects of increased food availability at landfills have been described (Cheng et al., 2019; Djerdali et al., 2016b; Rotics et al., 2017; Tortosa et al., 2002). European populations experienced dramatic declines and became endangered after the 50s, but most of them have evidenced dramatic population recoveries over the last 30 years associated to an increasing use of landfills, among other factors (Barlein, 1991; Blanco, 1996; Massemin-Challet et al., 2006; Schulz, 1999; Tortosa et al., 2002). Specifically, storks nesting near landfills show bigger clutch sizes, increased egg viability, nestling survival, and number of fledglings (Djerdali et al., 2008, Djerdali et al., 2016a, Djerdali et al., 2016b; Tortosa et al., 2002). Moreover, the appearance and increased availability of predictable feeding resources during the last decades across Europe resulted in shortened migration distances, new wintering areas closer to breeding areas, shifts on passage at Strait of Gibraltar, or complete migration suppression resulting in enhanced survival probabilities of juveniles and adults at a population level (Cheng et al., 2019; Ciach and Kruszyk, 2010; Rotics et al., 2016, Rotics et al., 2017; Sanz-Aguilar et al., 2015; Zurell et al., 2018). On the other hand, negative effects of anthropogenic food resources have also been shown for white storks such as plastic or rubber band ingestion, leg deformation by strings or wires (Kwieciński et al., 2006; Peris, 2003), accumulation of metals, metaloids, PCBs, brominated flame retardants, and a variety of pathologies linked to this pollutants (De la Casa-Resino et al., 2015a; Martín-Maldonado et al., 2020; Muñoz-Arnanz et al., 2011; Pérez-López et al., 2016; Saez et al., 2009; Smits et al., 2005, Smits et al., 2007).

Overall, despite the inconveniences of foraging at landfills, positive effects of landfill use on demographic parameters (i.e., reproduction and survival) at the population level are well known and have been documented for several stork populations. However, populations are typically composed of individuals with different behaviours (Araújo et al., 2011; Bolnick et al., 2003). Variability in individual experience, competitive abilities, optimization criteria, or physiological requirements could tip the scale to exploiting landfills instead of agricultural or other “natural” feeding areas (Sanz-Aguilar et al., 2015). Consequently, individuals within a single population could experience differential reproductive or survival prospects associated to their use of foraging resources available at landfills.

In this study, we evaluate the demographic effects of individual foraging on landfills on reproductive parameters and offspring survival. We expected that higher use of predictable and abundant food resources at landfills may positively associate to demographic parameters as a consequence of extra-food supply (Oro et al., 2013). However, foraging on junk food could also generate impacts on future survival of nestlings. The effects may be positive if the potential quantity of food is more important than the quality of food, or negative otherwise.