AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 140:630–642 (2009) Shallow-Water Habitats as Sources of Fallback Foods for Hominins Richard Wrangham,1* Dorothy Cheney,2 Robert Seyfarth,3 and Esteban Sarmiento4 1Department of Human Evolutionary Biology, Harvard University, Cambridge, MA 02138 2Department of Biology, University of Pennsylvania, Philadelphia, PA 19104 3Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104 4Department of Mammalogy, Human Evolution Foundation, East Brunswick, NJ 08816 KEY WORDS wet savanna; delta; baboon; USOs; seasonality ABSTRACT Underground storage organs (USOs) high densities of plant-bearing USOs are likely to have have been proposed as critical fallback foods for early occurred. Given that early hominins in the tropics lived hominins in savanna, but there has been little discussion in relatively dry habitats, while others occupied temper- as to which habitats would have been important sources ate latitudes, ripe, fleshy fruits of the type preferred by of USOs. USOs consumed by hominins could have African apes would not normally have been available year included both underwater and underground storage round. We therefore suggest that water-associated USOs organs, i.e., from both aquatic and terrestrial habitats. were likely to have been key fallback foods, and that dry- Shallow aquatic habitats tend to offer high plant growth season access to aquatic habitats would have been an im- rates, high USO densities, and relatively continuous USO portant predictor of hominin home range quality. This availability throughout the year. Baboons in the Oka- study differs from traditional savanna chimpanzee models vango delta use aquatic USOs as a fallback food, and of hominin origins by proposing that access to aquatic aquatic or semiaquatic USOs support high-density human habitats was a necessary condition for adaptation to sa- populations in various parts of the world. As expected vanna habitats. It also raises the possibility that harvest- given fossilization requisites, the African early- to mid- ing efficiency in shallow water promoted adaptations for Pleistocene shows an association of Homo and Paranthro- habitual bipedality in early hominins. Am J Phys Anthro- pus fossils with shallow-water and flooded habitats where pol 140:630–642, 2009. VC 2009 Wiley-Liss, Inc. Inhabiting areas with low rainfall and temperate cli- growth seasons, features USOs owe to their primary mates, early- to mid-Pleistocene African hominins would function of storing nutrients and/or water (Andersen, have needed to find plant foods year-round but would 1987; Laden and Wrangham, 2005). USOs have therefore have found difficulty in obtaining them during periods of been proposed to be important components of the homi- low plant productivity. During some periods of the an- nin diet (Hatley and Kappelman, 1980; Brain and Ship- nual cycle, fruits tend to be unpredictable or scarce man, 1993; O’Connell et al., 1999; Wrangham et al., (Peters et al., 1984). Nuts and seeds are often then avail- 1999). An increase in USO consumption may have even able, but like fruits are too seasonal to be relied on facilitated the hypothesized hominin shift from forest to (Peters, 1987). In savanna,1 during periods of fruit scar- more open habitats (Laden and Wrangham, 2005). city, the herbaceous foliage that forest-living African Ecological, archaeological, dental, nutritional, and apes tend to eat as a fallback is also scarce (Remis, comparative data all support the proposed dietary impor- 1997; Tutin et al., 1997; Wrangham, 2005). Some prima- tance of USOs in hominin evolution (Hatley and Kappel- tes including orangutans Pongo pygmaeus utilize inner man, 1980; Laden and Wrangham, 2005). Edible USOs bark during periods of fruit shortage (Knott, 1998), and are much more abundant in savanna than rainforest bark-eating could in theory be important for savanna habitats and there is little competition among mammals chimpanzees (Pruetz, 2006). However, extensive bark- for USOs, since their underground location makes them eating has not yet been recorded by chimpanzees in sa- unavailable to most species. USOs are widely eaten by vanna: the density of suitable trees may be insufficient human hunter-gatherers, hominid fossil sites charac- outside rainforest. Meat has been proposed as a possible teristically sample habitats rich in USOs, and early fallback food, though Speth (1989) argued that during dry seasons the fat content of meat would have been so low that protein poisoning would have been induced by a Grant sponsor: NIH; Grant number: MH62249; Grant sponsors: NRSA, Leakey Foundation, University of Pennsylvania. diet of more than about 30% meat. By contrast, plant underground storage organs (USOs) tend to be nutrition- *Correspondence to: Richard Wrangham, Peabody Museum, ally adequate and predictably available during low- 11 Divinity Avenue, Cambridge, MA 02138, USA. E-mail: [email protected] 1Following Laden and Wrangham (2005), we use ‘‘savanna’’ to Received 30 September 2008; accepted 18 May 2009 mean all habitats other than rainforest. Savanna thus includes not only closed canopy woodlands, bush, grassland, etc., but also shal- DOI 10.1002/ajpa.21122 low-water habitats such as lake shores, deltas, and the outside Published online in Wiley InterScience bends of slow-moving rivers. (www.interscience.wiley.com). VC 2009 WILEY-LISS, INC. HOMININ FALLBACK FOODS IN SHALLOW-WATER HABITATS 631 hominin remains exhibit stable isotope signals with val- range use and population distribution. Our food-derived ues similar to those of the USO-eating mole-rats (Bathy- hypothesis thus conforms to prior suggestions that ergidae) (Yeakel et al., 2007). Humans and early homi- aquatic habitats have been important in hominin ecology nins all have jaws and teeth that appear well adapted (e.g., Jolly, 1970; Ellis, 1993; Verhaegen et al., 2002). for eating USOs (Hatley and Kappelman, 1980; Ungar We first examine whether plants growing in aquatic et al., 2006). Notably, Ungar et al. (2006) found that habitats tend to be especially productive of USOs. We habiline teeth are adapted to crushing hard and brittle then present data on baboon (Papio cynocephalus ursi- objects. These properties together with low toughness nus) diet in the Okavango Delta (Botswana) in order to are characteristic of USO’s such as corms (Dominy et al., test the hypothesis that a catarrhine with access to shal- 2006). Hominin dental adaptations for processing USOs low-water habitats surrounded by relatively arid land are consistent with the strong selective pressures that uses aquatic USOs as fallback foods. The Okavango ba- fallback foods are expected to place on an organism’s boon data together with data on USO ingestion in mod- food-processing structures (Marshall and Wrangham, ern human populations is further used to assess the hy- 2007). USOs are a valuable human staple because they pothesis that USOs would have been a likely fallback have a low concentration of fiber (Schoeninger et al., food for hominins living in shallow-water habitats. 2001; Conklin- Brittain et al., 2002) and may have suffi- Although baboon diets are not appropriate analogs for cient nutritional quality to be significant dietary compo- the specific composition of hominin diets (Codron et al., nents for most human populations (Laden and Wrang- 2008), the fact that baboons and modern humans con- ham, 2005; Peters and Vogel, 2005). Finally, chimpan- sume USOs suggests that early hominins might also do zees have the cognitive ability to find and extract tubers so. Finally, we review the depositional habitats of early using tools (Hernandez-Aguilar et al., 2007) or with their fossil hominins (i.e., Paranthropus and Homo), to test if bare hands (Lanjouw, 2002), indicating that the last the hominin fossil record is in accord with the use of common ancestor of chimpanzees and humans (LCA) shallow-water USOs as fallback foods. and early hominins probably also shared these abilities. USOs are thus well-supported candidates as fallback Are aquatic habitats especially foods for early hominins. However, their proposed impor- productive of USOs? tance in hominin evolution has been challenged. For instance, some USOs need to be cooked by humans to be Because light and water are principal factors limiting edible, and there is little direct evidence for control of plant growth, tropical and subtropical shallow-water fire in the Lower Paleolithic (e.g., Plummer, 2004). Fur- habitats tend to produce a high biomass of plant mate- thermore, the caloric value of some wild tubers is so low rial compared to terrestrial habitats (Westlake, 1982). that their nutritional significance is questionable Aquatic habitats might therefore be unusually produc- (Schoeninger et al., 2001). In addition, microwear studies tive of USOs. Accordingly, we consider USO productivity of early Homo reveal fewer pits than expected for a in the three main macrophyte types known to grow in hard-object specialist, and early Homo is argued to have shallow water: 1) fully aquatic macrophytes with floating had too much occlusal relief to be well adapted to eating leaves; 2) semiaquatic or emergent macrophytes, i.e., USOs (Ungar et al., 2006). Moreover, African hunter- plants with roots anchored below water but leaves and gatherer populations where USOs are reported to be stems largely above water; and 3) floodplain herbs, most important in the diet (Hadza and San) are believed which have roots submerged in water only seasonally. to be ‘‘demographic sinks.’’ Living