Introduction

The origin of small fish bone deposits in caves occupied by human populations during Palaeolithic times is a recurrent problem. There are multiple predators that can have frequented or occupied the cave, and the different types of alteration observed on bones can illustrate the action of either human or non-human predators, like carnivores or birds. It is important to document these agents as they can accumulate and/ or modify the deposit and potentially alter the surface structure of the bone. In the case of fish remains, very few studies have been done to identify the bone accumulator or verify the contribution of each predator, and further experimental work needs to be conducted.

The natural disintegration of pellets produced by raptors can be an important process of accumulation. Birds produce regurgitation pellets containing bones that display varying degrees of damage and digestion (Andrews 1990). One of them, the Eurasian eagle owl (Bubo bubo), is a nocturnal raptor of the Strigidae family that accumulates pellets under perching and nesting sites (Penteriani et al. 1999, Cochard 2008). Considered the largest nocturnal raptor in Europe, it lives mainly in rocky and mountain areas or on the escarpments bordering river valleys, alternating between wooded and open areas. It hunts preferentially in open spaces (Jürgen 1995). It is present from Europe to North Africa and East Asia. In France, it is found mainly in the southern regions. Bubo bubo is a dietary opportunist that feeds on carrion as part of a varied diet. Its diet consists mainly of medium mammals such as hedgehog, lagomorphs, and rodents, but also includes birds, reptiles and amphibians (Géroudet 1984, Cramp 1985). Several studies have mentioned fish consumption in its diet (Bocheński 1960, Hiraldo et al. 1975, Malafosse 1984, Bayle et al. 1987, Le Gall 1999, Penteriani et al. 2002).

Despite its behaviour and opportunistic subsistence, the Eurasian eagle owl has been considered a potential accumulator of fish remains in cave deposits (Nicholson 1991, Le Gall 1999, Laroulandie 2002, Rambaud et al. 2008, Russ 2010, Russ & Jones 2011), its presence is documented during the Palaeolithic (Mourer-Chauviré 1975, Louchart & Soave 2002).

The aim of this article is to present a taphonomic analysis of the diet and damage related to digestion in the Eurasian eagle owl in the south of France. This will constitute an aid for understanding archaeological fish accumulations and will provide supplementary data to previously existing taphonomic references.

Material and Methods

Samples were collected near the River Verdouble, close to Tautavel (42°48′55′′ N, 2°44′50′′ E, altitude 194 m, Pyrénées Orientales, France) between June and August 2016. This river has woody riparian vegetation and is classified as “2^nd category”. It is populated with cyprinids like the Mediterranean barbel (Barbus meridionalis), chub (Squalius cephalus), common carp (Cyprinus carpio) and carnivores such as northern pike (Esox lucius). Samples were collected from the inside of a small cavity (Fig. 1), a European eagle owl nesting place, and from the immediate area outside of the cavity (under the porch). This material was not exposed to the weather for a prolonged time, therefore, the remains did not display any sign of weathering or of having been disturbed by scavengers. The remains from these two zones are recognizable by the different colouration of the bone's surface.

In total, we studied 27 samples of undigested and regurgitated material (pellets – samples may contain one or more pellets, as some of them were disintegrated before collection). Several samples also contained the remains of birds (MNI = 106), lagomorphs (MNI = 82) and rodents (MNI = 132). First, the samples were dry-cleaned to separate the bones by taxon; then each category of bone was sent to the specific expert. However, this study only reports on the fish remains. Each bone was identified by anatomic and taxonomic comparison with the reference collection of freshwater fishes from the Muséum National d'Histoire Naturelle (MNHN, Paris) and the Institut Royal des Sciences Naturelles de Belgique (IRSNB, Bruxelles). We also used published keys (Lepiksaar 1994, Radu 2005). All the remains were examined both macroscopically and microscopically. A binocular microscope was used for the identification of small skeletal elements and for the observation of digestion marks. For the quantitative analysis, we used the number of identified specimens (NISP) and the minimum number of individuals (MNI). The MNI was estimated from the number of first vertebrae or paired bones and according to the differences in the size of the bones (Poplin 1976) by sample and by spatial localization (inside or outside the cavity). Prey sizes were estimated by direct comparison with specimens from the osteological reference collection of the MNHN. Following the methodology used in a previous study (Guillaud et al. 2017), surface modification was classified following Nicholson (1991). The percentage of visible surface was adapted from Villa & Mahieu (1991). The proportions of bone damage on bone surface were divided into five categories of digestion: null, light, moderate, heavy and extreme (Fernández-Jalvo & Andrews 2016). Damage to the bone surface caused by beak hit was noted and counted. Percentage of bone representation was calculated using the formula by Dodson & Wexlar (1979): PR = FO/FT × MNI, where FO is the number of elements in the sample and FT is the number of elements in the prey skeleton. This method was adapted for fish bones and gives an overview, since samples were studied together and not separately.

Fig. 1.

Small cavity used by a European eagle owl for nesting and from where samples were collected.

Fig. 2.

a) Beak marks on pharyngeal bone; b) fissure on the surface of an articular of cyprinid; c) beak marks on precaudal vertebra.

Table 1.

Family in order of importance in the assemblage with the number of identified specimens (NISP) and minimum number of individuals (MNI) by sample and spatial localization.

Results

Seven fish species were identified: allis shad (Alosa alosa), European eel (Anguilla anguilla), gudgeon (Gobio gobio), roach (Rutilus rutilus), Mediterranean barbel (Barbus meridionalis), chub (Squalius cephalus) and tench (Tinca tinca). The most frequently represented family was Cyprinidae, followed by Anguillidae, and Clupeidae (Table 1). Size estimations indicated that the fish eaten by the eagle owl had a fresh weight ranging between 25 and 1800g.

Anatomical representation

A total of 1812 skeletal remains were recovered from the 27 samples (Table 2). Only 46 % were identified anatomically and specifically. Among them, 36 % (300) belong to the cranial skeleton and 64 % (542) to the axial skeleton. Cranial and vertebral unidentified bone fragments, neural and haemal spines, and scales represented 54 % (970) of all fish remains.

Table 2.

Number of identified fish specimens per Eurasian eagle owl samples.

For cyprinids, the entire skeleton was represented and the caudal vertebrae (25 %) were the most numerous elements. For anguillids, we observed some lack of cranial elements, and precaudal vertebrae (3 %) were the most numerous elements. For clupeids, the only remain was an opercle.

Digestion

Damage to the bone surface was observed under a binocular microscope. Different categories of digestion damage were applied to bones and teeth (Fernández-Jalvo & Andrews 2016). Five categories of digestion were distinguished: null (0); light (1); moderate (2); heavy (3); and extreme (4–5). For fish bones, the digestion degrees have been illustrated in Guillaud et al. (2017).

Fig. 3.

Modification of a cyprinid basipterygium (scanning electron microscope, scale 500 μm); presence of holes and polished aspect of the spongious bone surfaces typically due to gastric juices.

Table 3.

Percentages and classes of digestion for fish taxa according to the spatial distribution (int: interior, ext: exterior of the cavity).

The action of gastric juices results in a smooth and polished surface (Andrews 1990); and although the prolonged transportation of bones in water can also produce this result, only digestion could have caused these effects in our study.

The rounding and polishing of articulation edges observed on the scanning electron microscope (SEM) picture indicate advanced degradation and the presence of digestion holes (Fig. 3); this was notable in 2 % of all the remains.

Different degrees of digestion (Table 3) were observed on the surface of the skeletal remains; specifically, 5 % of the elements were altered to a light degree, 6 % to a moderate degree, and 3 % of bones suffered from moderate to heavy modification. We observed that Anguillidae and Cyprinidae remains displayed minimal digestion traces. Moderate digestion was observed on the only preserved remain attributed to Clupeidae (100 %), followed by Anguillidae (15 %) and Cyprinidae (13 %). Cyprinids were the most affected by heavy digestion (7 %). The localization of the remains seems to have had no impact on bone preservation.

Fig. 4.

Skeletal elements before and after digestion in eagle owl samples (common carp skeleton, modified from Coutureau (2005); for abbreviations see Table 4).

Table 4.

Number of remains by bone and fish family in the 27 Eurasian eagle owl samples.

Discussion

To summarize, 27 samples produced by Eurasian eagle owls were analysed. All of them contained fish bones. Among the total remains, 46 % were identified, and the rest were unidentifiable. All skeletal elements are represented in the sample. The breakage degree of skeletal elements was very low. The degree of digestion showed that more than 86 % of bones did not suffer any modification.

The eagle owl diet has been studied in various countries such as France (Bayle 1994, Cochard 2008), Greece (Papageorgiou et al. 1993, Alivizatos et al. 2005), Italy (Marchesi et al. 2002), Slovakia (Obuch & Karaska 2010) and Spain (Cramp 1985, Lloveras et al. 2009). This nocturnal predator has a generalist diet, locally specialized in medium-sized birds and mammals but is most often opportunistic (Hiraldo et al. 1975, Donázar et al. 1989). It consumes medium mammals such as hedgehog and lagomorph but also voles, field mice, rats and other small rodents. Birds may be consumed, mostly ducks, coots or diurnal and nocturnal raptors. Consumption of frogs is rarely mentioned (Géroudet 1978, 1984, Morel & Birchker 1990).

The abundance of fish remains in our sample is consistent with the data provided by Bayle (1992), Le Gall (1999) and Riols (2009). Likewise, the species we identified were among the most frequently recorded by these authors: chub (Squalius cephalus) dace (Leuciscus leuciscus), roach (Rutilus rutilus), brown trout (Salmo trutta), followed by pike (Esox lucius), common carp (Cyprinus carpio), common nase (Chondrostoma nasus), burbot (Lota lota), perch (Perca fluviatilis) and barbel (Barbus barbus). Some studies indicate that fish have not been always eaten by the eagle owl (e.g. Bustos & Muñoz 1973, Balluet & Faure 2006, De Cupere et al. 2009, Lloveras et al. 2009); this could be the result of seasonal variation in the diet or absence of a river near the nest. Le Gall (1999) indicates that the fish eaten by eagle owls measure between a few centimetres up to 40 cm. However, the remains belonging to fishes around 200–300 g (40–80 cm depending on the species) were frequent in our sample. The presence of different body mass classes indicates a non-selectivity of prey among the fish river community. The body weight of individuals, in our sample, ranged from 25 g to 1800 g, with the largest species being the eel. It cannot be excluded that small fish have been underestimated in this study, either because they are more sensitive to digestion or because their tiny bones were just not collected during pellet separation. Difficulties in identifying cyprinids can also cause biases. All species present in our study are coherent with the general diet of an eagle owl and with the fish fauna currently living in the River Verdouble. Our results confirm that eagle owl predation is dependent on the availability of fish population communities.

The eagle owl consumes whole fish, starting from the head. However, if the prey is too large, it may scavenge on it. These practices suggest that there is a selection of ingested body parts. Cramp (1985) noticed that the female eagle owl can dismember a prey and feed it in small pieces to their chicks. The eagle owl tends to deposit pellets at their roosts, which would suggest that any fish remains would be concentrated in the areas beneath and around the nest. The bleaching of bones also provides clear evidence of bioturbation at the cave's entrance (sun impact). For the purpose of this archaeological investigation, it was necessary to compare the spatial distribution of small mammals, birds and fish, which allowed us to make assumptions about the origin of the material deposited: anthropic vs. non-anthropic predator.

The number of prey bird deposit studies is expanding, and the Eurasian eagle owl has been identified as a possible accumulation agent on several archaeological sites (e.g. Andrews 1990, Sanchis Serra 2000, Laroulandie 2002, De Cupere et al. 2009). Russ (2010) studied the traces left by eagle owls during a feeding experiment at the Chestnut Centre Conservation and Wildlife Park (England). The skeletal elements recovered from pellets containing fish remains represented almost complete fish. The digestion of fish remains was minimal as they were protected: the fish being camouflaged in rats because the captive birds did not want to eat them. Broughton et al. (2006) studied 14 pellets from the modern barn owl (Tyto alba), and gave a general overview of the traces left on fish bones. Most of the remains (3294 remains) belonged to small sized cyprinids (< 500 g). These pellet remains were characterised by a high level of bone preservation. Digestion processes and bone modifications were characterised by a low degree of damage: rounding (16.3 %), pitting (6.9 %) and deformation (5.7 %). Following Andrews's (1990) method, the results of these two Strigiformes samples have no significant difference. Conversely, pellets coming from diurnal raptors (Falconiformes) contained less bone with a high percentage of fragmentation and a higher digestion of the bone surface than nocturnal raptors (Mayhew 1977, Bocheński et al. 1998). Our study confirms observations made on Strigiformes: low fragmentation, beak marks on pharyngeal bones or cracking of the bone surface. Fish remains also showed signs of digestion like rounding.

The impact of digestion on vertebrate skeleton (small mammal) varies according to the enzymes and acidity of the digestive system of the predator (Denys et al. 1995, Fernández-Jalvo et al. 2016). We must not forget that the impact of digestion on the fish skeleton can also vary. The conservation of the fish bone is also correlated with its histological structure (Butler 1996, Fernández-Jalvo et al. 2002). In our study, there does not appear to be any difference in the bone conservation depending on the fish size or species. However, we did observe that the majority of the preserved bones were vertebrae; cranial bones are less compact and can be more fragmented and more rapidly digested. Andrews (1990) included eagle owl in moderate or heavy digesting concerning the tooth enamel of small mammals. According to the whole variables studied in this paper, Bubo bubo may be considered as an intermediate category (2) of predator modification (Andrews 1990).

Erlandson & Moss (2001) identified a large number of predator species that could potentially deposit fish remains in caves located close to the coastline: canids, bears and birds. The bone assemblages produced by raptors are characterised by their degree of digestion. Fragmentation is secondary in comparison to mammals. Some pitting was observed, and broken edges were rounded. Some of the remains showed characteristic signs of biochemical modifications like rounding and polishing.

Conclusion

The study of modern predator behaviour offers hypotheses regarding the potential accumulator in archaeological sites. During the Palaeolithic period, when caves were unoccupied by human groups, other species may have settled there and created fish bone deposits. The analysis of eagle owl pellets indicates that this owl has a diversified diet including fish when close to a river. This study of 27 pellets allowed us to characterize the damage caused to fish bones during digestion. Focusing on the taphonomic point of view, we need to take into account this species in future studies. Present work proposes a criteria for analyzing and interpreting Eurasian eagle owl pellet remains, a potential fish bone accumulator. However, because eagle owl digestion is less destructive than that of carnivores, damage produced on bone may partly or completely disappear due to the post-depositional process. Therefore, interpreting that data just on digestion is not enough; we need to combine this analysis with other criteria such as bone representation, surface modification, fractioning, fragmentation, size of fish specimens or spatial distribution. It is important to analyse the fish remains combined with other faunal and lithic remains and not separately, as it is currently the case. Although, eagle owls could have contributed to the accumulation of archaeological fish, according to the present results, it is particularly important to be prudent in the analyses of accumulations that can be created by more than one predator. The ability to determine the depositional origin of fish remains recovered from archaeological caves is crucial for the correct interpretation of deposits, but it remains challenging.