Adaptability of large carnivores to changing anthropogenic food sources: diet change of spotted hyena (Crocuta crocuta) during Christian fasting period in northern Ethiopia

Authors

  • Gidey Yirga,

    Corresponding author
    1. Department of Biology, Mekelle University, P.O. Box 3072, Mekelle, Ethiopia
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  • Hans H. De Iongh,

    1. Institute of Environmental Sciences, Leiden University, P.O. Box 9518, Leiden, The Netherlands
    2. Evolutionary Ecology Group, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerpen, Belgium
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  • Herwig Leirs,

    1. Evolutionary Ecology Group, University of Antwerp, Groenenborgerlaan 171, 2020 Antwerpen, Belgium
    2. Department of Agro-Ecology, Aarhus University, Forsøgsvej 1, 4200 Slagelse, Denmark
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  • Kindeya Gebrihiwot,

    1. Department of Land Resource Management and Environmental Protection, Mekelle University, P.O. Box 231, Mekelle, Ethiopia
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  • Jozef Deckers,

    1. Department of Earth and Environmental Sciences, Catholic University of Leuven, Celestijnenlaan 200E, B-3001 Heverlee, Belgium
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  • Hans Bauer

    1. Department of Earth and Environmental Sciences, Catholic University of Leuven, Celestijnenlaan 200E, B-3001 Heverlee, Belgium
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Correspondence author. E-mail: gidey1998ec@yahoo.com

Abstract

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Introduction

Across the globe, maintaining viable populations of large carnivores in several ecosystems requires that they coexist in a landscape with people that bring anthropogenic resources such as livestock, garbage and pet food (Linnell, Swenson & Andersen 2001; Conover 2002; Woodroffe, Thirgood & Rabinowitz 2005). Many large carnivores readily use anthropogenic food sources, which often leads to conflict (Woodroffe & Ginsberg 1998; Beckmann & Berger 2003; Packer et al. 2005). Understanding details of the foraging behaviour of carnivores in an anthropogenic environment can help reveal specific causes of conflict, leading to better strategies for reducing availability of anthropogenic food and preventing conflict (Breck, Lance & Seher 2009). Urban ecosystems are typically characterized by reduced species diversity but increased abundance of a few species able to exploit anthropogenic food sources (Newsome et al. 2010).

Spotted hyenas (Crocuta crocuta), hereafter referred to as hyenas, show evidence of many particular behaviour that set them apart from other mammals, making them a fascinating model organism for the study of animal behaviour (Smith & Holekamp 2010). They can adapt to habitats with dense human population (Woodroffe 2001) eating almost any organic matter, even putrid carrion and anthrax-infected carcasses (Johnson 2006). Hyenas have been recorded to eat almost any mammal, bird, fish or reptile but they also feed on garbage, cooked porridge and dung (Mills & Hofer 1998). Although hyenas do scavenge opportunistically, they are efficient hunters and directly kill 60–95% of the food they eat in natural habitats of the Maasai Mara ecosystem, Kenya (Smith & Holekamp 2010). They are capable of eating and digesting all parts of their prey except hair and hooves (Smith & Holekamp 2010). Bones are digested so completely that only the inorganic components are excreted in the hyena’s droppings (Smith & Holekamp 2010).

An analysis of 15 studies throughout its range in Africa showed that hyena are both scavengers and active hunters and show a preference for prey in the range of 56–182 kg but no clear preference for any particular species (Hayward 2006). Hyenas hunt alone or in group, an adult hyena is capable of bringing down a prey animal weighing up to four times its own body mass (Mills & Hofer 1998). They depend primarily on wild prey in East Africa but have long been known to depend more on anthropogenic food sources in the Horn of Africa (Gade 2006). We have previously demonstrated that hyenas in northern Ethiopia depend exclusively on anthropogenic food sources; mostly scavenged livestock remains (Abay et al. 2011).

In the calendar of the Ethiopian Orthodox Tewahedo Church, there are various fasting periods in a year but the longest (55 days) is ‘Abye Tsome’ or ‘Hudade’ (Lent), before Easter. During this period, a vast majority of people in northern Ethiopia do not consume animal products leading to a sharp decline in demand for meat. The aim of our study was to investigate possible changes in the diet of hyenas before, during and after the fasting period. We hypothesize that reduced availability of waste from slaughtering forces hyenas to supplement their diet with alternative food sources during this period.

Study area

The research was conducted in three study sites bordering the regional capital of Mekelle (200 000 inhabitants). The first is 12 km to the West and is called Debri, with a total human and livestock population of approximately 7000 and 12 000, respectively. The second, Aynalem, is 5 km to the South, with a total human and livestock population of approximately 6000 and 12 000, respectively. The third site is Arid, the main campus of Mekelle University and an adjacent army camp, three km East of the town with a resident population of approximately 20 000 people. All sites are severely degraded highland of 2200–2300 m.a.s.l.

In all areas, the majority of the populations are Orthodox Christians. Despite the rampant poverty and scarce resources, people strictly follow religious restrictions on animal parts that can be eaten. The remains of slaughtered animals and all redundant pack animals are always left at the nearest convenient site, usually simply just outside the people’s compounds.

Materials and methods

In March–May 2010, permanent plots were established in each study site by describing natural landscape elements as virtual borders around areas of approximately one hectare containing hyena scats as identified using Stuart & Stuart (2000). The plots were demarcated with sticks on each corner. Firstly, all droppings in the plots were collected on the first day of fasting, representing hyena diet before fasting. Secondly, all droppings were collected from the same plots on the last day of the fasting; these droppings had accumulated during the fasting period. Finally, we collected all droppings 55 days later, representing the diet after fasting. Scat samples were put in plastic bags while avoiding cross-sample contamination. Following the method of Ramakrishnan, Coss & Pelkey (1999), hair was extracted from scat and compared with hair in our reference collection to establish prey species composition. Our reference collection contains hair of all domestic and wild species in the study area and includes human hair. We tested for differences in species composition between collection periods with a nonparametric Wilcoxon test using JMP-5 Software, SAS Institute Inc., Cary, North Carolina, USA. We conducted a randomization nonparametric vander Waerden test to examine whether the differences between the time periods are significant by taking the total number of samples for each species, and randomly assign each sample to each period.

Results

A total of 553 hyena scats were analysed (Fig. 1); the number of scats collected after fasting was low because the Arid and Aynalem plots had been plowed by farmers (Dryad Repository: doi:10.5061/dryad.pq050620). There was a statistically significant difference in hair composition between scat collected before and during fasting (P < 0·05) and between scat collected during and after fasting (P < 0·005). There was no significant difference between scat collected before and after the fasting. These results were further corroborated by the randomization tests using nonparametric vander Waerden test, with observed differences falling outside the distribution of randomized samples (P < 0·01, χ2 = 21, d.f. = 8).

Figure 1.

 Percentage of hair in scat before, during and after the fasting period in 2010. Error flags on the different columns indicate variations.

Discussion

Our study shows a remarkable change in diet of hyena during the fasting period, from predominantly scavenging on waste to active predation on donkeys. In northern Ethiopia, the natural prey base is highly depleted and hyenas are highly dependent on human-related resources (Gade 2006; Abay et al. 2011). The rural and urban populations of the district are predominantly Orthodox Tewahedo Christians, their vegan diet during fasting leads to a sharp reduction in available animal waste. This is apparently compensated by increased donkey depredation.

We previously reported that hyenas get most food from scavenging on urban and rural waste; depredation accounted for <20% of food intake in Debri and Aynalem (Abay et al. 2011). We infer that hyenas scavenge less and hunt more during fasting, selecting opportunistically for donkeys. Donkeys are in the preferred prey body mass range suggested by Hayward (2006), and in northern Ethiopia, they are extremely abundant (Ghebreab et al. 1999). In contrast to other livestock species, donkeys are kept outside the compound at night, and weak donkeys are abandoned altogether, which makes them a relatively easy food source.

Despite the overall statistically significant diet change, cattle hair remained prevalent in hyena scat from Arid also during fasting. This may have two reasons. First, the 35th anniversary of Tigray People’s Liberation Front (TPLF) was celebrated by the soldiers during the fasting which included some slaughtering. Secondly, the College of Veterinary Science continued its activities and continued dumping some carcasses. In Arid and Mekelle, hyenas clean up the organic waste; they are the most efficient means of maintaining sanitation of the campus.

Despite events of depredation, hyenas are tolerated as efficient sanitation units. People are aware of the presence of hyenas; they can easily be observed and heard almost every night. Hyenas almost never attack people; people are afraid of them but accept their presence. They have removed waste of butchers and households from the city and are traditionally known as ‘municipal workers’. This is in fact opposite findings of Croes et al. (2011) who found that hyenas avoid villages in Cameron, because of persecution. This indicates that hyenas are highly adaptable to human behaviour.

We contributed further evidence that wildlife species can modify behaviour to successfully survive in their environment. This might have an implication for urban carnivore management, which may differ considerably from rural habitats. Certain animal species have adapted to human-dominated habitats well and benefit directly or indirectly from human activities including food (Shochat et al. 2004; Faeth et al. 2005; Adams, Lindsey & Ash 2006). Diet supplementation with anthropogenic food augmented predator’s densities and altered their diets in the Santa Monica Mountains, California (Fedriani, Fuller & Sauvajot 2001). It has been suggested that refuse and livestock carcasses at pastoral villages may influence the frequency of hyena visits to these areas (Mills & Hofer 1998; Kolowski & Holekamp 2007).

Seasonal variation in the use of refuse sites has been documented in a number of carnivores and is often associated with variation in prey availability (Craighead & Craighead 1971; Salvador & Abad 1987). Kolowski & Holekamp (2007) reported that hyenas were more likely to be found near open refuse pit during times of relative prey scarcity, indicating the potential impact of human refuse at pastoral villages to increase livestock losses to hyenas. They also found that livestock depredation was higher where hyenas were more abundant because of attraction from waste. In our case, the scarcity is not owing to natural prey fluctuations but to religiously inspired changes in human behaviour; the result is the same, however. In addition to the abundant literature on improved livestock management to mitigate depredation (Ogada et al. 2003; : Bauer, De Iongh & Sogbohossou 2010), these observations suggest mitigation by improved waste management.

In the context of prey-depleted northern Ethiopia, waste management would immediately impact hyena abundance, with possible impacts on their viability and subsequently on the ecology of the region. In our case, carrying capacity and hyena survival are dependent on anthropogenic food. Less extreme but still with a substantial impact on population viability, Bauer (2003) included livestock in his assessment of carrying capacity because livestock effectively constituted a large share of lion (Panthera leo) diet. In contrast, tolerance for lion depredation is very low in Nechisar National Park, southern Ethiopia; reportedly any lion that ventures anywhere near herds of livestock are pre-emptively shot (Y. Yirga, F. Gebresenbet, J. Deckers & H. Bauer, unpublished data). Advanced substitution of ungulates by cattle there has meant a reduction in carrying capacity leading to very low lion population viability. These cases confirm that changes in the availability of anthropogenic food may affect carnivore population density (Borokowski, Zalewski & Manor 2011).

In conclusion, in our study, hyenas mainly scavenge waste of butchers and households, but during fasting, donkeys provided an alternative food source. We conclude that hyenas are highly adaptable and opportunistic scavengers and hunters. Frequencies with which particular prey species occur among collections of scats are easily compiled to describe the diet and can be used to compare diets between periods.

Acknowledgements

We are grateful to VLIR-UOS (Flemish Interuniversity Council) for financial assistance. We thank Meheret Hadu and Solomon Amare for their respective contributions. We acknowledge statistical advice from Said Musa. We are grateful to Mekelle University for providing laboratory, space and materials.

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