A systematic review of animal predation creating pierced shells: implications for the archaeological record of the Old World

Human made holes in shells

Table 1 shows hole assessment in 49 taxa of Mollusca perforated by humans from archaeological sites. Anthropogenically modified shells come from 21 countries of the Old World, with most archaeological sites located in Spain and France (Table 3). Twenty-seven taxa exhibited more than one type of hole location in their shells, while shells from 22 taxa were classified as having only one type of hole (Fig. 2A). However, 15 taxa from the latter group were recovered at one archaeological site alone.

The number of hole location types was diverse amongst mollusc species (Fig. 2A). Bivalves were more diverse in terms of hole location than Scaphopoda with most species exhibiting more than one type of hole location (Table 3). Gastropoda was the most numerous and diverse class in terms of hole location. Nassarius gibbosulus was the most variable species in terms of hole location among all archaeological sites (1, 2, 3, 4, 6, 7, 8 and 11) (Table 1; Fig. 2A). Moreover, shells of Nassarius gibbosulus from Üçağızlı (Turkey) and Grotte des Pigeons (Morocco) had the most variable hole location from single archaeological site (Table 3). Compared to other mollusc species, which are more frequently found at archaeological sites, but are less variable in terms of types of hole location, high variation in hole location in Nassarius gibbosulus does not appear to be a consequence of the relative abundance of this species.

Bivalves were the least common taxa found in archaeological assemblages and are characterised by hole locations 4, 9 and 10 (Table 3). Scaphopoda were more common than Bivalvia, but much less diverse in terms of types of hole location. Shell beads belonging to Scaphopoda had two holes, one in the anterior and the second one in the posterior of the shell (type number 5, Fig. 2A). In turn, gastropod shell beads were recovered at almost all archaeological sites and mostly showed more than one type of hole location.

Fumane (Italy) was the most diverse in context of number of gastropod species (13 taxa, Table 3), while Üçağızlı (Turkey) was characterised by the greatest number of types of hole location in gastropod shells at single archaeological site. Across all species, the most variable placed holes in shells were found at the site of Riparo Mochi (Italy) dated to the earliest Aurignacian (Kuhn & Stiner, 1998; Stiner, 1999).

Predator made holes in shells

Table 2 shows that almost all mollusc taxa recovered from the analysed archaeological sites are preyed upon by hole-making predators (41 taxa). Among these taxa we were able to assess the hole location in the shells made by non-human animals in 30 mollusc species. Most of the assessed species exhibited two types of hole location in their shells, while only four species were classified as having three types of hole (Fig. 2B).

All species from the Bivalvia have predators that make holes in shells (Table 2). Species from this mollusc class are usually associated with more than one predator. Gastropoda is the class with the most numerous predators (nine species), then the Asteroidea (three species) and then Malacostraca with only one predator (Table 2). Almost all taxa from the Gastropoda have non-human predators that attack the prey by piercing holes in the mollusc’s shell.

Assessment of hole location types in shells made by predators was possible only for one Scaphopoda species (Dentalium sp., Table 2). Dentalium sp. can be attacked by five species of the Gastropoda and is pierced by gastropod predators in two places: in the middle or at the apex of the shell. Bivalvia is more diverse than Scaphopoda in terms of the placement of holes made by non-human predators. Gastropoda, Asteroidea and Malacostraca make holes in bivalves in the following locations: 1, 2, 3, 9 and 10 (Fig. 1). In turn, gastropods have predators that usually pierce holes in only one or two locations in particular species (Table 2, Fig. 2B).

Comparison of hole locations made by humans and predators

The number of hole location types per scaphopod and bivalve species were higher for hole-boring predators than for anthropogenically modified shells. In turn, holes in gastropod shells made by humans were characterised by slightly greater variation than holes in shells pierced by non-human predators (Table 4). However, the sign test revealed no significant difference in types of hole location between shells perforated by humans and non-human animals within mollusc species (Table 4, P = 0.398). The result of the sign test was supported by value of the Cohen-d index. For differences between human made and non-human made holes in shell, the Cohen’s d value was small (d = 0.14, Table 4).

Holes in the shells of Gastropoda

Among molluscs, species within the Gastropoda were found to be the most varied in terms of hole locations in shell beads made by humans (Fig. 2A, Table 4). This may be associated with natural morphological variation (shape, size and shell thickness) among species in this mollusc class (Stiner, 2014). Different styles of Palaeolithic bead adornments using ornate shells (Stiner, 2014) may also increase the variability of hole placements in the analysed shells.

Almost all gastropod taxa reported from archaeological sites are also vulnerable to hole-boring predators (e.g., Fig. 2B). In most cases, the predators belong to the class Gastropoda or Malacostraca (Table 2). The rest belong to Aves, Asteroidea, Cephalopoda and Polychaeta (Table 2). Despite the numerous predators, gastropod taxa had lower variation in the types of hole location per species made by non-human species than by humans (Table 4). These findings are supported by other research which shows that anatomical locations selected by predators of gastropods are not randomly selected, but are strategically located (Arpad, 1993; Zagyvai & Demeter, 2008). For example, in Neritina picta, access to the apex of the shell is preferred as a strategic location by predators belonging to Asteroidea, Muricidae, or Polychaeta (Zagyvai & Demeter, 2008). In turn, Theodoxus sp. usually exhibit a muricid (predatory sea snail) borehole that is often located close to the umbilicus (Arpad, 1993).

Holes in the shells of Scaphopoda

Scaphopoda was the least diverse mollusc class in terms of variation in hole location in shell beads made by humans (Table 4), which is probably a consequence of their characteristic anatomy (tusk shaped). All shell beads belonging to this class have two anatomical holes, one in the anterior (allowing the burrowing foot and captacula to protrude) and a second one in the posterior part of the shell (responsible for respiration; Reynolds, 2002). As such, these shells can be threaded onto a cord without being pierced.

Mean variation of hole location in shells pierced by predators of scaphopods was greater than in shells modified by humans (Table 4). Klompmaker (2011) found that predators pierced holes in the shells of Miocene scaphopods in the middle section of the shell, which is the thickest part. Whereas we found that Dentalium sp. was pierced in two places: in the middle or at the posterior part of the shell. However, we were only able to assess predator made holes in one species of Scaphopoda (Dentalium sp.), therefore results for this class should be interpreted with caution.

Holes in the shells of Bivalvia

Holes pierced by humans in bivalves were slightly more diverse than in scaphopods, but were less variable than in gastropods (Table 4). According to Carter (2008) bivalves in South America were rarely used as beads or pendants due to their size and weight and it is possible that most perforations could be attributed to predation or taphonomic processes. Other evidence, based upon context and use-wear analysis of shells from Palaeolithic sites, suggests the presence of bivalves can often be attributed to utilitarian purposes (e.g., food, receptacles for pigments) rather than use as body adornments (Harper, 2005; Bar-Yosef-Mayer, 2007; Rogalla & Amler, 2007; Douka et al., 2014). Zilhão et al. (2010) suggest that for most species of bivalves recovered from archaeological sites, anthropogenic modifications can be confirmed when (i) the weathering stage and perforation patterns do not agree with those seen in natural death assemblages; (ii) a tool was involved in the perforation, or (iii) the hole is associated with artificial modification of the shell’s geometry.

Predators of bivalves are also diverse and belong to Asteroidea, Gastropoda or Malacostraca. This variation in predators might be associated with higher variations in types of hole placement per species, which is slightly greater than reported in anthropogenically modified shells (Table 4). For example, variation in hole location is very low in Chlamys sp., with naticid and muricid predators usually choosing the region near the adductor muscle (corresponding to number 2 in Fig. 1), which may facilitate access to the viscera (Chattopadhyay & Dutta, 2013). Similar behaviour to non-human predators has been noted in the fossil bivalve Pseudodon in which 33% of holes were made near the anterior adductor muscle by Homo erectus at Trinil (Joordens et al., 2015). In this mollusc species, the adductor muscles are placed near the 1 and 6 of the hole location types (Fig. 1). Location of the holes made by H. erectus may vary from the data presented in our study because Pseudodon shells at Trinil, although engraved, appear to have been perforated in order to open the shells to access the meat rather than to be used as body adornments.

Evidence from the study of bivalve species from the early and middle Pleistocene, indicate that shells were most often pierced by non-human predators close to the umbo or near the centre (Amano, 2006). Only few examples of piercings near the adductor muscle have been described, and these could have been caused by the incomplete drill holes in prey which continue to grow after the attack changing the relative position of the incomplete hole (Chattopadhyay & Dutta, 2013).

Pierced shells; factors to consider

Our results show that within the analysed sample, there were no significant differences between the placement of holes made by non-human animals and those made by humans; both pierce shells in the same locations in most classes of molluscs (Table 4; Fig. 3). For example in Euthria cornea, Gibbula sp. and Mitra corniculata we observed that humans and non-human predators made holes in the same location (type number 4). Similarly, in Glycymeris sp. humans and predators pierced the same part of the shell (types number 4 and 9; Tables 1 and 2). However, for some mollusc species selection of hole location was only partial. For example in Littorina sp. we observed that humans and non-human animals made holes in the centre of shell (type number 4) and near apex (type number 8), but this species is also perforated by humans near the outer lip (type number 1; Tables 1 and 2).

The non-random piercing of holes by the mollusc predators is widely reported (e.g., Johannesson & Ekendahl, 2002; Kingsley-Smith, Richardson c A & Seed, 2003; Dietl & Kelley, 2006; Gorzelak et al., 2013) and it can be associated with shell thickness of prey which varies across the body, probably due to differential age of the shell whorls and predatory pressure on snails (Rosin et al., 2013). In molluscs with ornamental shells, up to five times more force can be required to make a hole (Dalziel & Boulding, 2005). Predatory gastropods can spend between three to twenty minutes locating a piercing site on their prey’s shell surface and, once the location is fixed, it may take from several hours to several days to pierce the shell, depending on the thickness (Hagadorn & Boyajian, 1997). The variation in shell thickness within and between mollusc species may be linked to why holes in shells most often occur near the lip and in the centre (e.g., types number 1, 2, 3 and 4; Fig. 1) and why humans and non-human predators choose similar locations to pierce shells of Bivalvia and Gastropoda (Fig. 3) However, results for scaphopods deviated from this pattern, with humans and non-human predators piercing holes in different locations (type 8 and 4 versus type 5, respectively; Fig. 1). Similarity in the choice of hole location made by humans and non-human predators in most species of mollusc could cause researchers to wrongly assign shell perforations as anthropogenically manipulated because they believe predator made holes are less likely to be pierced in suitable locations for threading (D’Errico et al., 2005; Bouzouggar et al., 2007).

Bicho & Haws (2008) have suggested that the larger biomass of molluscs in the Palaeolithic likely meant that mollusc gathering formed part of hunter-gatherers’ regular foraging behaviour in Portugal. Furthermore, predator drill frequency in gastropods and bivalves has been estimated to range between 2.8%–50.0% and 8.6%–34.1%, respectively. In contrast, scaphopods were pierced at a much lower rates (0.9% in Dentalium sp.; Taraschewski & Paperna, 1982; Yochelson, Dockery & Wolf, 1983; Hagadorn & Boyajian, 1997; Zagyvai & Demeter, 2008; Sawyer, 2010). It is possible that prehistoric people that regularly foraged for molluscs, were more likely exposed to a greater numbers of naturally perforated shells than we might expect. As such, the likelihood of finding shells with predator-made holes in locations suitable for threading could be higher than researchers believe.

Beads made from shells with holes made by natural processes have been identified at archaeological sites, for example, the perforated bead of Antalis sp. from the Early Upper Paleolithic site in El Cuco (Spain; Gutiérrez-Zugasti & Cuenca-Solana, 2013). Some researchers claim that shell beads from the Middle and Lower Palaeolithic could have been perforated by natural processes. For example, Bednarik (2015) proposed that predators and parasitic organisms commonly perforate mollusc shells and that it should be expected that naturally perforated shells were used as beads and pendants. Hahn (1972) emphasized that the signs of human manipulation in shells from Aurignacian sites such as Krems-Hundssteig, Willendorf, Kostienki 1 and Sjuren, are not always present and that some holes could have been made by predators. It is possible that before tools were used to bore holes, finding shells with holes in favourable positions for threading into ornate jewellery may have increased their importance or value. Similarly the natural apertures in fish vertebrae or crinoid discs may have made them attractive as items for threading (e.g., see Mussi, 2002).

Finally we would like to draw attention to the common assumption that predator-made holes are mostly made by chemical processes and tend to be round in outline, while shells pierced by humans have elliptical or irregular outlines (Stiner, 1999; Komšo & Vukosavljević, 2011). We would argue, however, that this statement is probably an overgeneralisation because many predators form holes in their prey which range in shape from nearly perfect circles to ellipsoids (Zagyvai & Demeter, 2008). For example, muricids, naticids and cephalopods use their radula to bore into mollusc shells and they can adapt the size and shape of the pierced hole to the morphology of their prey, as a result, bore holes can differ in shape (Walker & Brett, 2002). Bird beaks can also cause cracks and chips to the shells that imitate stone tool use (Ingolfsson & Estrella, 1978; Harper, 2005; Shumaker, Walkup & Beck, 2011). Thus, detailed analytical methods remain critical to identifying the tell-tale signs of anthropogenic manipulation of shells recovered from archaeological sites.