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Gut Morphology and the Avoidance of Carrion among Chimpanzees, Baboons, and Early Hominids

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Meat-eating primates avoid scavenging for dietary protein and micronutrients even when carrion is relatively fresh. Chimpanzees, baboons, and modern hunter-gatherers supplement their diets of high-energy, low-protein fruit with protein obtained from leaves, insects, and animal prey. Most primates, especially leaf-eating primates, digest the cellulose cell walls of ingested plant material in a well developed caecum and/or large intestine through fermentation caused by enzymes released by their normal gut flora. The primate digestive strategy combines a rapid passage through the stomach and prolonged digestion in the ileum of the small intestine and caecum, and this combination increases the likelihood of colonization of the small intestine by ingested bacteria that are the cause of gastrointestinal disease. Carrion is very quickly contaminated with a high bacterial load because the process of dismemberment of a carcass exposes the meat to the bacteria from the saliva of the predator, from the digestive tracts of insects, and from the carcasses' own gut. Thus, the opportunistic eating of uncooked carrion or even unusually large quantities of fresh-killed meat by nonhuman primates or humans is likely to result in gastrointestinal illness. We propose that among meat-eating primates, carrion avoidance is a dietary strategy that develops during their lifetime as a response to the association of gastrointestinal illness with the ingestion of contaminated meat from scavenged carcasses. This has important implications for our understanding of early hominid behavior.
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Gut Morphology and the Avoidance of Carrion among Chimpanzees, Baboons, and Early
Hominids
Author(s): Sonia Ragir, Martin Rosenberg and Philip Tierno
Source:
Journal of Anthropological Research,
Vol. 56, No. 4 (Winter, 2000), pp. 477-512
Published by: The University of Chicago Press
Stable URL: https://www.jstor.org/stable/3630928
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GUT MORPHOLOGY AND THE AVOIDANCE OF
CARRION AMONG CHIMPANZEES, BABOONS,
AND EARLY HOMINIDS1
Sonia Ragir
Department of Sociology and Anthropology, College of Staten Island-City
University of New York, Staten Island, NY 10301
Martin Rosenberg
Department of Dermatology, New York University Medical Center,
New York, NY 10016
Philip Tierno
Department of Microbiology and Pathology, New York University
Medical Center, New York, NY 10016
Meat-eating primates avoid scavenging for dietary protein and micronutrients
even when carrion is relatively fresh. Chimpanzees, baboons, and modern hunter-
gatherers supplement their diets of high-energy, low-protein fruit with protein
obtained from leaves, insects, and animal prey. Most primates, especially leaf-
eating primates, digest the cellulose cell walls of ingested plant material in a well
developed caecum and/or large intestine through fermentation caused by enzymes
released by their normal gut flora. The primate digestive strategy combines a
rapid passage through the stomach and prolonged digestion in the ileum of the
small intestine and caecum, and this combination increases the likelihood of
colonization of the small intestine by ingested bacteria that are the cause of
gastrointestinal disease. Carrion is very quickly contaminated with a high
bacterial load because the process of dismemberment of a carcass exposes the
meat to the bacteria from the saliva of the predator, from the digestive tracts of
insects, and from the carcasses' own gut. Thus, the opportunistic eating of
uncooked carrion or even unusually large quantities of fresh-killed meat by
nonhuman primates or humans is likely to result in gastrointestinal illness. We
propose that among meat-eating primates, carrion avoidance is a dietary strategy
that develops during their lifetime as a response to the association of
gastrointestinal illness with the ingestion of contaminated meat from scavenged
carcasses. This has important implications for our understanding of early
hominid behavior.
THE OCCASIONAL SCAVENGING observed among modem hunter-gatherer
societies has led some anthropologists to assume that the kill of other carnivores
Journal of Anthropological Research, vol. 56, 2000
Copyright ? by The University of New Mexico
477
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478 JOURNAL OF ANTHROPOLOGICAL RESEARCH
could have been a regular source of dietary protein, fat, and micronutrients for early
hominids (Blumenschine 1987; Bunn and Kroll 1986; Bunn and Ezzo 1993; Isaac
and Crader 1981; O'Connell, Hawkes, and Blurton Jones 1988a; Shipman 1986).
Carrion,2 whose amino and fatty acid chains become partially decomposed by cell
lysosomes and bacteria, is probably as easy to digest as cooked meat; yet
nonhuman primates, even those that eat meat, avoid the kill of other hunting
species as a source of nutrients. We argue that gastrointestinal distress caused by
the high bacterial loads in carrion, which accumulate within hours of the kill,
generate carrion-avoidance behavior among nonhuman and human primates.
It is plausible, although not generally accepted, that driven by the increased
seasonality of fruit during the Plio-Pleistocene, late Australopithecines may well
have added plant underground storage organs (USOs) to their diet (Hatley and
Kappelman 1980; Kappelman 1997; Kay and Grine 1988, cf., note 3, this article;
contra O'Connell, Hawkes, and Blurton Jones 1999). Subsequently, early Homo
appear to have increased their consumption of animal protein and fats (Cachel and
Harris 1996; Milton 1999a; Potts 1988a, 1988b; contra O'Connell, Hawkes, and
Blurton Jones 1999; Wrangham et al. 1999). Prolonged in utero and postnatal
phases of growth resulting in a larger energy-expensive brain and body were likely
the source of the higher nutrient demands that were felt by early Homo and
probably motivated an increase in their consumption of meat to supplement fruit
and USOs (Clegg and Aiello 1999; Leonard and Robertson 1994, 1996; Milton
1999a, 1999b; Ragir 1986, 2000; Smith 1999; Speth and Davis 1976; Spielmann
1989). In as much as hominids were not equipped with hard claws for digging up
underground rootstocks or sharp teeth for killing game, the exploitation of both
rootstocks and meat necessitated the expansion of knowledge about hard-to-obtain
plants and animals and an extractive technology that included methods of
detoxification.
Selective and systemic processes that favored larger bodies and/or brains in
primates would have been limited by the lack of dietary protein, lipids, and
micronutrients (iron, zinc, and vitamin B'2) in a diet of fruit and rootstocks (Martin
1983; Milton 1999b). The human brain requires a larger proportion of higher
quality dietary protein and micronutrients during gestation and the early years of
growth than does those of other primates (Milton 1999a; Ulijaszek 1991, 1995).
Milton (1999a: 19) concluded that "given the postulated body and brain size of the
earliest humans and the anatomy and kinetic characteristics of the extant hominoid
gut, the most expedient dietary avenue open to protohumans seems to have been to
turn increasingly to the intentional consumption of animal matter on a routine
rather than a fortuitous basis." Multiple lines of evidence suggest that at least some
demes of early hominids ate the meat and bone marrow of small and medium-sized
herbivores; the association of stone tools with prey species, tool cut marks on
bones, and various stable-isotope analyses of hominid teeth and bones3 have most
often been interpreted as evidence for the eating of meat derived from scavenging
(cf., Potts 1988a; Potts and Shipman 1981; Dominguez-Rodrigo 1997, 1999; Isaac
and Crader 1981; Marean 1998; Monahan 1996). However, if carrion avoidance in
present-day human and nonhuman primates is determined by digestive strategies
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GUT MORPHOLOGY AND CARRION AVOIDANCE 479
that are not different from those of early hominids, then scavenging could not have
been a significant source of supplementary protein for our earliest ancestors.
THE SCAVENGING HYPOTHESIS
The idea that early hominids might have obtained meat by scavenging as a
transitional phase between foraging and hunting has been a topic of active debate
for at least thirty years (Blumenschine, Cavallo, and Capaldo 1994; Gordon 1987;
Potts 1983, 1984, 1988b; Read-Martin and Read 1975; Szalay 1975). In a widely
quoted paper by Schaller and Lowther (1969:326), the scavenging hypothesis was
proposed and rejected on the grounds that scavenging was not an evolutionary
stage or independent mode of subsistence activity among carnivorous mammals
but merely an adjunct to predatory adaptations. Teleki (1981) expressed
puzzlement about the persistence of the scavenging hypothesis in light of the
contradictory evidence, such as carrion avoidance and hunting activity observed
among baboons, capuchin monkeys, and chimpanzees.
Scavenging has been observed very infrequently among predatory primates
(Goodall 1986; Harding 1981; Hasegawa et al. 1983; Ihobe 1992; Nishida 1994;
Strum 1981; Stanford et al. 1993, 1994). Teleki (1973) described chimpanzees'
responses to the corpse of a commonly hunted monkey, maintaining that they
resembled reactions to dead conspecifics rather than to food. Both Goodall (1968)
and Strum (1981) offered carcasses of their usual prey to chimps and baboons and
failed to stimulate a meat-eating response. Goodall (1986; Morris and Goodall
1977) reported only ten instances of scavenging by Gombe chimpanzees in more
than twenty-five years in the field. Stanford (1995; Stanford et al. 1994) reported
that chimpanzees, although curious about the dead animals that they saw during
foraging, did not usually treat carrion as if it were food. He observed one instance
of scavenging by a female; however, it was not known whether or not a member of
the troop had been the primary predator (Stanford et al. 1993).
Strum (1981) described seven instances of scavenging among baboons in five
years, six occurring in 1976-1977. During 1973, an increase in successful hunts and
cooperative hunting among males appeared to be instigated by one highly
motivated individual. Apparently excited by this success, juveniles and even some
females engaged in predatory behavior. The disappearance of cooperative hunting
and the reduction of kills in 1976-1977-possibly a result of the abandonment of
the motivating male and/or of the increased wariness on the part of prey animals-
was followed by a brief rise in scavenging. Most of the scavenged carcasses were
still warm, and at times the baboons treated the carcasses as if they were their own
kill. Neither scavenging nor cooperative hunting was sustained or resumed after
this single season.
Nishida (1994) reported seven instances during which Mahale chimpanzees
may have fed on carcasses killed by other species. He described in detail an instance
that illustrates the paradox inherent in scavenging activity and carrion avoidance in
this species:
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480 JOURNAL OF ANTHROPOLOGICAL RESEARCH
At Mahale, about 10 chimpanzees including adult males were found sitting
about 10 meters from the carcass of a large bushpig that, from the evidence
of injuries on the throat and chest of the victim, had probably been killed by
a leopard. It was likely that the leopard fled upon hearing the approach of a
large party of chimpanzees. The body was fresh and still infested with many
ticks. The chimpanzees only gazed at the pig for a long time and departed
without eating it. (We, however, did partake of the meat, which was quite
palatable!) (Nishida 1994:375)
Among tropical and mid-latitude hunter-gatherer populations, the most
common and reliable feeding strategy included a high daily consumption of fruit,
cooked rootstocks, and occasional bulbs, shoots, and young leaves, which were
gathered primarily by women and children (Bailey 1993; Blurton Jones 1993;
Blurton Jones, Hawkes, and O'Connell 1989; Hawkes, O'Connell, and Blurton
Jones 1995, 1997; Sept 1994; Vincent 1985). Plant foods were supplemented by
protein from small slow-moving turtles, lizards, insects, and birds' eggs that
everyone collected and by the meat and fat from larger mammals that were hunted
and occasionally scavenged by men. Tanaka (1976, 1980; see also Lee 1969;
Silberbauer 1981) calculated that 96.4 percent of the bulk (67 percent of the total
calories) consumed by Kalahari B/wi San was plant storage organs and fruit, while
only 3.6 percent was animal prey. While animal prey constituted less than 15
percent of the bulk of an Australian Aborigine's diet, the Hadza diet included about
30 percent animal protein (Lee 1968; O'Connell, Hawkes, and Blurton Jones
1988a, 1988b; O'Dea 1991; Woodburn 1968; Yengoyan 1968). In higher altitudes
and latitudes, meat and fat constituted a larger proportion of the hunter-gatherer
diet-as much as 70 percent of the winter fare among subarctic and Arctic hunters
(Hayden 1981).
O'Connell, Hawkes, and Blurton Jones (1988a) described scavenging as a
standard part of Hadza foraging, especially in the late dry season. The Hadza
monitored the flight of vultures and the nighttime calls of lions and hyenas to locate
carcasses; during a fourteen-month study, the Hadza successfully killed fifty-four
medium/large animals and scavenged eleven partial carcasses-14 percent of the
total weight of the meat consumed. When the Hadza anticipated a scavenging
opportunity, men, boys, and in some cases women abandoned other activities and
ran quickly to the source, usually driving off predators with bows and arrows but
sometimes with only noise and digging sticks (O'Connell, Hawkes, and Blurton
Jones 1988a:357). The abandoned carcasses were usually fairly fresh; however, on
one occasion a carcass was badly decomposed (O'Connell, Hawkes, and Blurton
Jones 1988a:361). All of these carcasses were cooked before they were consumed
(O'Connell, personal communication). While the total caloric or protein yield from
scavenging was small, it may nevertheless have been important as a supplement to
an inadequate supply of essential amino acids and micronutrients obtained from
fruit and rootstocks.
Given the opportunity, indigenous peoples of the North Pacific Coast, the
Arctic, and the South African Cape ate beached sea mammals; in higher latitudes,
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GUT MORPHOLOGY AND CARRION AVOIDANCE 481
the fat and meat were frequently consumed uncooked. However, these beached
animals are not usually killed by predators, and the stomach and gut contents have
not been released prior to human butchering activity. When the air is cold and the
intestine of the animal stays intact, the meat, which is protected by hair, skin, and
a thick layer of fat, remains uncontaminated by fecal, insect, or airborne bacteria.
Proper butchering that keeps intestinal contents separate from the rest of the carcass
and the subsequent burial of uneaten meat and fat in the cold ground protects the
meat from bacterial contamination (Greenberg 1991; Shean, Messinger, and
Papworth 1993; Smith et al. 1992). Two or three weeks later the buried meat can
still be consumed; although partially decomposed by cell lysosomes rather than
bacteria, it is unlikely to harbor dangerous levels of bacterial toxin.
Blumenschine (1987) surveyed predation and carcass distribution on the
Serengeti Plains to determine what conditions presented the most favorable
scavenging opportunities. Subsequent studies have continued to support his
conclusion that scavenging need not have required intense competition with large
carnivores and primary predators and that Plio-Pleistocene hominids might have
occupied a "passive scavenging niche" in the East African riparian woodland
(Blumenschine 1987:394; Cavallo and Blumenschine 1989; Sikes 1994).
However, Potts's (1983) analysis of cut marks on prey species demonstrated that at
Zinji, the prey did not fit the age structure predicted by models of passive
scavenging, and many femora and humeri revealed cut marks on their shafts, thus
indicating early rather than late access to carcasses. Opportunistic confrontation
between primary predators and human hunters with respect to kill is observed more
frequently than passive scavenging among modern tropical hunter-gatherers; still,
scavenging accounts for only a minute proportion of the animal protein that is
consumed by these hunters (O'Connell, Hawkes, and Blurton Jones 1988a).
An absence of piercing implements for killing combined with the evidence of
confrontational scavenging among ethnographic hunters has led some scholars to
adopt a confrontational rather than a passive scavenging hypothesis to account for
meat eating through the Middle Pleistocene (Bunn and Ezzo 1993; Capaldo 1997;
Dominguez-Rodrigo 1997, 1999; Klein 1987; Marean 1989, 1997; Monahan
1996, 1999; O'Connell, Hawkes, and Blurton Jones 1988b). However, if small
groups of humans yelling and brandishing sticks can drive a partially satiated
leopard or lion from its kill (O'Connell, Hawkes, and Blurton Jones 1988a; Treves
and Naughton-Treves 1999), then there is little reason to believe that hungry
chimpanzees or baboons who shriek and wave their arms or sticks would be less
successful than humans at confrontational scavenging (see Nishida 1994:375,
quoted above). No attempt at confrontational scavenging by chimpanzees and
baboons has ever been observed.
O'Connell, Hawkes, and Blurton Jones (1999) doubted that either passive or
confrontational scavenging could have provided enough food to meet the energy
requirements of the large brain and body of Homo erectus juveniles (cf. Milton
1999a, 1999b; Rush 1989; Clegg and Aiello 1999). In fact, Blurton Jones, Hawkes,
and O'Connell (1989; Blurton Jones 1993; Hawkes, O'Connell, and Blurton Jones
1995, 1997) have argued that even among present-day tropical hunters such as the
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482 JOURNAL OF ANTHROPOLOGICAL RESEARCH
Ache, Hadza, !Kung, and Australian Aborigines, families are provisioned
primarily by the returns from female gathering rather than from male hunting.4 As
with chimpanzees, human hunting in the tropics appears largely motivated by male
affiliative and status concerns rather than by their energy requirements or those of
other members of their social group (Hawkes 1990, 1992; Mitani and Watts 1999;
Nishida et al. 1992; Stanford 1995). On the other hand, Milton (1999a) and Jones
(1998), among others (Spielmann 1989; Ulijaszek 1995:6-7), have argued that the
staple energy foods, seasonal fruit, and rootstocks cannot supply the large
quantities of amino acids and micronutrients that were required for the growth of
a relatively large-brained, large-bodied hominid juvenile. Even if USO's were a
staple of early Homo diet, they could not fulfill the need for larger quantities of
essential amino acids and micronutrients during fetal and juvenile growth and
development.
Ulijaszek (1995) concluded that without dietary supplements, present-day
cultivated rootstocks alone, such as yams, sweet potato, plantain, casava, and sago-
palm, would not supply a sufficient number of the amino acids and micronutrients
for normal growth in children or even a moderate level of activity in adults. Nor do
rootstocks have the complement of essential amino acids and micronutrients
necessary to sustain episodes of hominid encephalization and increases in body
mass without the consumption of a larger proportion of animal matter than that
observed in other large frugivorous primates (Leonard and Robertson 1994, 1996;
Milton 1999a, 1999b; Stini 1988).
Insects, birds' eggs, small lizards, and small mammals are an integral part of
chimpanzee, gorilla, and orangutan diets. While the Australopithecine body was
about two thirds the mass of that of a modem chimpanzee, its brain was comparable
in volume (Falk 1999; Hartwig-Schwerer 1993:32, fig. 6); one could expect such
encephalization to be accompanied by a moderate increase in the metabolic
demand for protein and micronutrients, at least among pregnant and nursing
females and their slowly developing, semidependent offspring. Furthermore, as the
brain of early Homo increased well beyond the volumes expected in modern apes,
their body mass remained equivalent to that of a modern chimpanzee. How much
more animal protein would have been necessary to support the small but significant
encephalization of the small-bodied Australopithecines (Falk 1999; Falk et al.
2000), much less that of the large-bodied early Homo, is still problematic.
GUT MORPHOLOGY AND DIET
Several indices of gut specialization seem to clearly differentiate the relatively
short, unspecialized gut of faunivores and the long, folded, villi-covered intestinal
walls of specialized caeco-colic fermenters such as folivores. The coefficient of gut
differentiation (CGD) (Chivers and Hladik 1980) that is characteristic of
frugivores falls in between and partially overlaps the ranges of specialized
folivores (CGD 1.5-6.0) and unspecialized faunivores (CDG 0.2-0.5) (Figure 1).
The gut proportions of larger frugivorous primates, who depend on secondary
animal or plant foods to supplement the low protein content of fruit, tend to overlap
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GUT MORPHOLOGY AND CARRION AVOIDANCE 483
* Capr- Mature (3.81)
Eqguus (3.4)
Sapra- Immtu (2.92)
* PrebSt s 9nex (2.61
* Hyloba es p leatul (2.55)
*r olobu npolmos) (2.23)
Presbytis tan.40)
* Paap gonaan ( 1.68
esby scura (1.)(1.29)
Cercopithecu nlectus (1.29)
SMacacanica 4)
SPresbyts melapo (1.17)
Pan troo e 6
* Ce Api s nt (sJ1. 10)
* Presi is rubicunda .0u)
* Nasa arvatus(1
? ..-'ongo pygmaeus (1.u4)
0 apio slnx (1.03.
SCercopinhecus cepus(.00)
* Macaqa ascicuan s.96)
* Aotus tnriviraatus .870
* Macaca mulatta 7
* Cercopithecu? a ius (0.84)
* Alouata senicu)us ~.8)
* Flis (0.6)
* Vu vulpes (0.69)
us 2 (large (0.67)
*? .Atspaniscus (0.663
* Htman (0.62) <====
* Papio paplo (0. 58)
Nandinia binotata (0.57)
* us(small(0.53)
* Cani (0.52)
* Mustela einea (0.50)
* Panthera pardus (0.50)
* Genetta servalina (0.41
* Leontocebu midas (0.36)
: Mustel nivals (.32)
Funisciurus pyrrmo (0.31
* Funiscauru saneryts 0.2
* Ceus capucinus (0.18
* Tursiops truncatus (0.08)
I ' ' I I . . ..! .I I I I 'I I I I I I I I i ' I 1 ' I I I ItI'I ' 'I
0 1 2 3 4 5
Coefficient of Gut Differentiation
Figure 1. Coefficient of Gut Differentiation
The coefficient of gut differentiation clearly demonstrates the response of gut morphology
to dietary adaptations. Adapted by Ragir and Rosenberg for this article from Chivers and
Hladik (1980, 1984) and from Sussman (1987).
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484 JOURNAL OF ANTHROPOLOGICAL RESEARCH
the CGD of unspecialized faunivores or folivores (CGD .33-2.0) depending on the
primary sources of their dietary protein (cf. MacLarnon, Chivers, and Martin
1984). Baboons, humans, and pigs, whose coefficients of gut differentiation
(CGD) are 0.58, 0.62 and 0.67 (0.53 for small pigs), respectively, have similar diets
and food preferences, as already noted by fieldworkers (Hatley and Kappelman
1980). The coefficient of 1.16 found in chimpanzees is below that of most
folivores, but well above that of baboons and modem humans, and probably
reflects the higher proportion of leaves and stems in their diets. Using the same
methods as Chivers and Hladik, Sussman (1987:175) found a coefficient of gut
differentiation of 0.62 (N = 6, range 0.37-1.15) in six modem urban males. Thus,
in this measurement of proportionate lengths of gastrointestinal compartments, the
modem humans that were measured fell within the frugivorous range and close to
the upper range of nonspecialized faunivores (cf. Chivers and Hladik 1984:218,
fig. 9.2; MacLarnon, Chivers, and Martin 1984; Martin et al. 1985).
Species that supplement fruit with leaves, such as vervets and macaques,
require a longer ileum, a larger caecum, and longer colon than chimpanzees,
baboons, capuchin monkeys, and humans, who avoid mature leaves and
supplement fruit with animal and/or insect protein, rhizomes, forbs, oily nuts, or
seeds (Martin et al. 1985). The CGD does not provide a particularly good
indication of digestive strategy; for example, while pigs have a CDG comparable
to that of humans, their digestive kinetics differ significantly from that of humans
(see Figure 2, below). However, the CDG is consistently different between animal
species that come from lineages adapted to very high-fiber and very low-fiber diets.
This probably means that gut proportions per se constrain an animal's ability to
digest high-fiber foods but not low-fiber foods such as ripe fruit, fresh meat, or even
carrion (Martin et al. 1985; Sussman 1987).
Speth (1989, 1991; Speth and Spielmann 1983) presented evidence that
excessive amounts of animal protein were unhealthy and sometimes dangerous to
humans, especially during fetal growth (cf. Profet 1997; Flaxman and Sherman
n.d.). In addition, the metabolic costs of catabolizing protein greatly exceeded
those of converting carbohydrates and fat. Among circumpolar and perhaps
periglacial peoples, the consumption of large quantities of fat with meat increased
these people's ability to convert animal protein to energy and, as a result, to
substitute animal flesh for plants (Cachel 1997; Carpenter 1994). But tropical
mammals are relatively lean, and this makes meat an improbable replacement for
plant carbohydrates as an important energy source for growth or increased daily
activity in early Homo (Cachel 1997; Schaller 1972).
Milton (1999a: 18) concluded that meat eating "played an absolutely essential
role in human evolution," even though fruit and USOs remained the main source of
energy. Among other necessary nutrients, animal protein contributed sulfur-
containing amino acids that were essential for detoxification of the cyanogenic
fruit, nuts, and rootstocks in human diets (Jones 1998:157-58). However, Milton
appears to underestimate the difficulties involved in the supplementation or
replacement of fruit with USOs as a dietary staple (Johns 1996; Jones 1998;
O'Connell, Hawkes, and Blurton Jones 1999; Peters 1990; Peters, O'Brien, and
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GUT MORPHOLOGY AND CARRION AVOIDANCE 485
Box 1984).5 Wild tubers are more fibrous and more likely to be high in protease
inhibitors and cyanogenic glycosides than cultigens; thus, a seasonal staple of
rootstocks entails some form of preconsumptive preparation (Johns 1996; Hawkes,
O'Connell, and Blurton Jones 1999; Katz 1987; Peters and O'Brien 1981, 1994;
O'Brien and Peters 1991; O'Connell, Hawkes, and Blurton Jones 1999; Peters
1987, 1990; Peters and Maguire 1981; Stahl 1984; Wandsnider 1997).6 While
cyanogenesis is reported for both corn and many species of wild and domesticated
potatoes, domesticated varieties of grass seeds such as wheat are particularly high
in cyanoglycosides (Jones 1998). If the roots were not pounded, soaked, mixed
with clay, and/or eaten with a small meat supplement, the increased consumption
of rootstocks by early hominids would not have relieved malnutrition or increased
available energy. Furthermore, a diet consisting solely of unprocessed rootstocks,
fruit, and nuts could easily have resulted in the debilitating neurological
dysfunction that is symptomatic of chronic cyanide poisoning (Johns 1996:52).
Crushing, grating, mixing with clay, lime, or ash, soaking, or fire roasting largely
detoxifies wild tubers; without such preparation, a major portion of the
carbohydrates and protein in USOs is indigestible (Johns 1996; Milton 1999b).
Wrangham et al. (1999) and O'Connell, Hawkes, and Blurton Jones (1999)
have argued that rootstocks rather than meat were the new food source exploited by
early Homo; they have addressed the question of USO toxicity and indigestibility
by arguing that fire-burned patches in East African Homo erectus sites are evidence
for a controlled use of fire for warmth, protection, and cooking as early as 1.6 mya
(cf. Milton 1999b). If such an early use of fire could be substantiated, then
rootstocks and meat, scavenged or hunted, might have all been cooked, and Homo
erectus would have made the revolutionary discovery that probably underlay the
stable, year-round, high-nutrient diet necessary for modern human growth and
development. However, no fire alteration has been observed on bone or stone
debris in any of the intensively studied Bed I and II Olduvai Gorge hominid activity
areas, and the repeated volcanic eruptions that have left burned patches on the
floors of many East African hominid sites make the assumption of a controlled use
of fire problematic (Bunn 1994, 1999; contra Bellomo 1994; James 1989; Rowlett
1990, 1999; Hawkes, O'Connell, and Blurton Jones 1999).7 An additional
counterindication of the controlled use of fire for cooking comes from the
descriptions of !Kung San and Hadza cooking fires; these fires are used to roast
gathered roots and tubers but left no noticeable fire alteration on clay surfaces
(O'Connell, Hawkes, and Blurton Jones 1999). The bowl-like depressions with
baked clay sides in early Pleistocene sites were very unlike the negligible
alterations left by the cooking fires of mobile ethnographic gatherers. Instead, the
Koobi Fora "hearths" resembled Rowlett's (1990) experimental bonfires that
burned for more than four hours at temperatures much higher than those associated
with cooking (Rowlett 1999:585).
Substantial evidence for the widespread use of fire for cooking has been
associated with burned bone, fire-altered stone, and charcoal; such fire-altered
archaeological debris occurred less than three hundred thousand years ago, long
after the first appearance of Homo heidelbergensis in Europe (Balter 1995;
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486 JOURNAL OF ANTHROPOLOGICAL RESEARCH
Bermudez de Castro et al. 1997; Cachel and Harris 1996; Carbonell 1999; Clark
and Harris 1985; Gowlett et al. 1981; James 1989:2, table 1; McGrew 1999;
Monnier et al. 1994)-and thus it came too late to play any significant role in Homo
ergaster's preparation of rootstocks. Stiner (1994) has demonstrated through a
comparative study of faunal bone fragments in Middle Pleistocene cave deposits
that scavenged carcasses appeared in middle Mousterian sites two hundred
thousand years after we have abundant evidence of the use of fire for cooking.
On the other hand, there are less revolutionary methods of detoxifying USOs,
such as peeling, pounding, soaking, and the ingestion of roots mixed with clay, and
these techniques have been observed in use among numerous varieties of
nonhuman primates (Johns 1996; McGrew 1992). Hominids could have increased
nutrient availability by crushing and soaking tubers in the mineral-rich water of
shallow lakes or slow-moving streams and by mixing the pulp with absorbent clay
or lime to bind digestion-inhibiting compounds (Wing and Brown 1979:70). It is
hard to imagine what archaeological evidence for soaking would look like, but the
connection between hominid stone tools and stream or lake margins is common.
Small bone shafts worn at one end, stone flakes with wear similar to that made by
woodworking, and crushed pebbles and cores are widely encountered in sites
younger than two million years (Brain 1988; Harris 1983; Harris and Ross 1987;
Howell, Haesaerts, and de Heinzelin 1987; Keeley and Toth 1981); these have been
interpreted as tools for digging, for making wooden digging implements, and for
crushing bones, seeds, and nuts-so why not rootstocks as well? Fieldworkers
have occasionally observed geophagy and the pounding, peeling, or soaking of
food items among apes in the wild (Huffman and Wrangham 1994; McGrew 1992;
Nishida 1994). It might reasonably be assumed that early hominids with digging
implements were capable of peeling, crushing, soaking, and thus detoxifying and
breaking down the complex carbohydrates that are stored in USOs. However, such
a technology would not reduce bacterial contamination in meat, and without fire,
neither carrion nor very large quantities of fresh meat could be safely consumed by
pregnant females or juveniles.
Selection for changes in developmental timing that resulted in larger brains
and bodies appeared slightly prior to and semi-independent of the changes in local
ecology that led to new dietary opportunities and the exploitation of additional
food sources (Ragir 2000). As the metabolic demands of larger brains and bodies
had to be met, early Homo probably included both new staple plant and animal
foods. Prepared rootstocks and animal kill required some system of demand or
generalized sharing between group members-that is between hunters and
nonhunters, males and females, females and juveniles. Hunting was the only way
that hominids could obtain edible animal food before fire was employed to kill
bacterial growth (Asfaw et al. 1999; Culotta 1999; de Heinzelin et al. 1999).
BACTERIAL GASTROENTERITIS IN HUMANS
A heavy bacterial load develops in carcasses that are left in the open for even
a few hours, and this would have prevented the consumption of meat scavenged
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GUT MORPHOLOGY AND CARRION AVOIDANCE 487
from the kill of other predators prior to the use of fire for cooking. Acute enteritis
or colitis can result from infection by viruses, fungi, protozoa, helminths, or
bacteria. A number of bacterial pathogens of the intestine have been found
worldwide, and although it is difficult to observe their effect on wild primates,
there is little reason to believe that they are not as affected by these pathogens as
their captured conspecifics, which frequently serve as medical research models for
the study of gastrointestinal disease in humans (Macfarlane and Gibson 1995).
There are two broad categories of colonic microflora, each characterized by
their relationship to the host: (1) indigenous bacteria that at some stage have been
able to colonize the intestinal wall and (2) contaminant bacteria that reside
temporarily in gut contents and do not permanently establish themselves in the
host's ecosystem. The principal human intestinal bacterial pathogens are
characterized according to virulence factors that enable them to overcome the host
defense. Among others, Escherichia coli, Salmonellae, Shigellae, Clostridium,
and Camphylobacter have virulent strains. Insofar as Clostridium perfringens and
Campylobacters form the primary category of bacteria that are common in the
intestine of domestic animals and wild game and are harmful but not usually fatal
to humans, they seem to offer the best models for paleobacterial-host relationships
in the formation of food aversions.
The major nonimmunological host defense mechanisms against bacteria and
bacterial toxins are gastric acid secretion, bile, intestinal motility, the inhibitory
effect of the normal gut microflora,8 lysozyme activity, and those pancreatic
enzymes such as trypsin and chymotrypsin that are active in the digestion of
proteins-including bacteria. Nevertheless, the host's defenses can become
compromised or overwhelmed, and intestinal bacterial infection can occur. This
situation may arise as a result of toxins or toxic metabolites released into the host
by the pathogen, the ingestion of large bacterial loads, the digestion-inhibiting
activity of recently consumed roots or leaves (Cook 1979; Johns 1996; Lawrence
1992), poor protease production (see below), or an underlying illness in the host.
During butchering, the contents of the intestine are often spilled so that fecal
matter contaminates the meat; however, the resultant illnesses are not usually fatal
in adults. Enterotoxin-producing strains of C. perfringens that are found in the
intestinal tracts of wild and domestic herbivores are common causes of food
poisoning and diarrhea in the United States. The incubation period following
exposure to contaminated meat is brief (four to fourteen hours), and the symptoms
usually include diarrhea, abdominal cramps, nausea, and vomiting; fevers occur
infrequently. Nearly all patients experience a spontaneous resolution of symptoms
from six to twenty-four hours after the onset of the infection. Beta toxin-producing
strains of C. perfringens type C (CPC) can occasionally cause a severe infection of
the small bowel, sometimes fatal to children (Cook 1979; Lawrence 1992;
Macfarlane and Gibson 1995). Data from the Centers for Disease Control (1985)
indicate that C. perfringens accounts for more than 7 percent of reported food-
borne outbreaks of food poisoning (Macfarlane and Gibson 1995), and many cases
are probably not reported because of the relatively mild symptoms and the
sophisticated laboratory procedures that are needed to identity the bacteria.
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488 JOURNAL OF ANTHROPOLOGICAL RESEARCH
In adults, normal pancreatic enzymes-such as trypsin and chymotrypsin-
can reduce the C. perfringens toxin to harmless amino acids. Depressed enzyme
activity or low trypsin production means that the digestion of the C. perfringens
enterotoxin is incomplete, and this partial digestion results in enhanced toxicity.
Such modification occurs when digestive enzymes are partially deactivated by
protease inhibitors like those found in yams and sweet potatoes or the wild
savannah rootstocks that are consumed by modem foragers (Buonocore and Silano
1986; Lawrence 1992; Prathibha, Nambisan, and Leelamma 1995). In humans and
animals on low-protein diets, experimental evidence suggests that protease
production is also low and, thus, that sporadic gorging on uncontaminated meat
increases the risk of infection and intestinal illness. The organisms that cause the
disease in animals, the type C enterotoxemia of adult sheep and pigs, were probably
already present in the intestine; they multiplied transitorily in the changed
environment of a single high-protein or high-carbohydrate meal with disastrous
effect. High-protein meals among people with low-protein diets were a leading
cause of the epidemics of Enteritis necroticans (EN) in Germany and Norway after
World War II (Lawrence 1992:339). A reduction in the production of pancreatic
enzymes accompanying low-protein diets may also account for the intestinal
distress that is felt by vegetarians when they suddenly eat a substantial quantity of
meat at one meal.
Enteritis necroticans, such as "Pig Bel"-associated with pig feasts that
accompanied important occasions in the highlands of Papua New Guinea-
occurred when yams and sweet potatoes were consumed with great quantities of
roasted pig meat (Cook 1979; Lawrence 1992). Yams and sweet potatoes contain
substantial amounts of a heat-resistant trypsin inhibitor. Measurements made on
sweet potato cooked over a fire showed that the core temperature reached was quite
low, about 70'C (cf., Rowlett 1990), and not sufficient to deactivate the protease
inhibitor. CPC beta toxin is a protein that is ordinarily very rapidly deactivated by
proteolysis, but in the New Guinea highlands, very low protein consumption (4-7
percent of the diet) led to low levels of protease production. Suppressed protease
production combined with the presence of the trypsin inhibitor in the sweet potato
resulted in a partial decomposition of the CPC beta toxin into a more virulent
molecule that made whole villages ill and was often fatal to children between two
and four years of age (Cook 1979; de Garine 1997:230, table 1; Lawrence
1992:337). As in the enterotoxemia of pigs and sheep, Pig Bel gut damage
followed the growth of CPC after an unusually protein-rich meal consumed by
people who usually ate very little meat.
Because the bacteria that are present in the native intestinal flora of prey
species frequently contaminate carcasses during butchering, C. perfringens is the
kind of agent that might induce carrion avoidance and inhibit scavenging. If the
staple diets of Australopithecine or early Homo hunters consisted of fruit and
savannah rootstocks with even moderate levels of protease inhibitors (Buonocore
and Silano 1986; Johns 1996; Lawrence 1992; Prathibha, Nambisan, and
Leelamma 1995), we might expect frequent, severe, and sometimes fatal illnesses
to have been associated with opportunistic carrion eating and to have sometimes
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GUT MORPHOLOGY AND CARRION AVOIDANCE 489
accompanied sporadic gorging on large quantities of uncontaminated meat.9
Campylobacters, the second model for the bacterial infection of hominid
scavengers, are gram negative, nutritionally demanding organisms that are also
common in the intestinal tracts of food animals that are herded closely together.
The pathogenesis of Campylobacter in man and animals appears similar, involving
enterocolitis toxin as well as infection of the intestinal wall, and it is one of the most
frequent causes of bacterial diarrhea in humans (Macfarlane and Gibson
1995:213). The typical incubation period is roughly fourteen hours, and the illness
is characterized by fever, abdominal pain, and bloody diarrhea. If vomiting occurs,
it is usually mild, and dehydration is infrequent. Complications include
bacteremia, appendicitis, pseudo-membranous colitis, toxic megacolon, and
cholecystitis; however, Campylobacter infections are generally not fatal and are
usually self-resolved within a few days.
Campylobacterjejuni, the most common pathogenic species, is widespread in
the animal kingdom and has been isolated from the intestines of a variety of
domestic animals, including poultry, and every known wild bird species.
Campylobacters are also found in the small and large bowel of common wild
herbivore species-reservoirs for bacteria that assure the ubiquity of C. jejuni spp.
in nature.'1 Although human volunteer studies show that a mere five hundred C.
jejuni were sufficient to cause diarrhea, the infectious dose was extremely variable
(Macfarlane and Gibson 1995).
In the incidents of confrontational scavenging recorded by O'Connell,
Hawkes, and Blurton Jones (1988a:361-62), the carcasses were usually recovered
after the upper hindquarter and viscera had been completely consumed by the
primary predator. Wolves, lions, and wild dogs, but not cheetahs, open their kill
through the soft underbelly, thereby releasing the intestinal contents and
contaminating the meat (Estes and Goddard 1967; Marean 1989; Mech 1970;
Schaller 1972:269, cf., note 11). The primary predator's consumption of the
viscera practically guaranteed the contamination of the rest of the carcass (Schaller
1972:269); a brisk growth of contaminant bacteria begins within an hour after the
death of an animal during hot weather" (Shean, Messinger, and Papworth 1993).
O'Connell, Hawkes, and Blurton Jones (1988a) and Treves (Treves and Naughton-
Treves 1999) estimated that confrontational scavenging took place between four
and twelve hours after a kill had been made-in other words, long after the meat
had been contaminated by intestinal contents, feces, bacteria from the mouths of
primary and secondary predators, and insects. Even relatively fresh carrion
harbored huge numbers of these gram-negative bacteria.12
Ortiz and Smith (1994) showed carrion to be a major source of botulinal toxins
for animals. Their study indicated that carrion-transmitted botulism is usually type
C or type D and that ingesting contaminated meat is very dangerous, if not fatal, to
scavenging animals. Hubalek and Halouzka (1991) detected Clostridium
botulinum type C toxin in high concentrations in mute swan (Cygnus olor)
carcasses, in lower concentrations in invertebrates such as ptychopterid fly larvae,
leeches, and sow bugs that were associated with these carcasses, and occasionally
in water samples close to the carrion. Toxin-bearing maggots were exposed in the
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490 JOURNAL OF ANTHROPOLOGICAL RESEARCH
mud at the study site for 131 days from November to March. Although the toxin
activity decreased twenty-five fold and forty fold in the samples during this period,
it remained very high, and birds ingesting even a relatively low number of these
toxic larvae in the spring received a lethal dose. With bacterial toxins that kill the
host, such as those produced by variants of Salmonella, Clostridium botulinum,
and Esherichia coli, avoidance behavior cannot develop because the host dies.
Avoidance behavior can develop because of the transitory and self-limiting
qualities of C. perfringens, Campylobactor, and other microbial infections of
moderate toxicity.
THE "GARCIA EFFECT": THE RAPID CONDITIONING OF FOOD
AVOIDANCE IN RATS, MONKEYS, AND HUMANS
Garcia, Hankins, and Rusiniak (1974) clearly describe the mechanisms by
which reptiles, birds, and mammals, including humans, acquire strong food
aversions in response to gastrointestinal illness, including vomiting, cramping,
and diarrhea. "The only requirement for an enduring aversion is stimulation of the
gustatory receptors followed, even hours after the consumption of the food, by a
visceral illness" (Garcia, Hankins, and Rusiniak 1974:826, emphasis added;
Garcia et al. 1968). There is both experimental and neuro-anatomical evidence that
taste, not olfaction, is the sufficient and primary modality for the acquisition of
food aversions in mammals (Garcia, Hankins, and Rusiniak 1974:826; Garcia et al.
1968). A brainstem relay has been found in mammals between the viscera and the
feeding areas of the pons, the hypothalamus, and the cortex; this relay governs the
palatability of food and appears directly involved in an almost instantaneous
manifestation of food avoidance behavior in mammals (Garcia, Hankins, and
Rusiniak 1974:831; Rolls 1997; Schiefenhovel 1997).
Although the avoidance of bitter or acidic tastes may be conditioned in the
infant before weaning by preferences for sweet foods in the maternal primate diet,
this is an unlikely mechanism to establish carrion avoidance. Hladik (1981),
Milton (1987), and Rozin (1987), among others (Rozin and Kalat 1971; Rozin and
Fallon 1981; Rozin, Fallon, and Augustoni-Ziskind 1986; Rozin et al. 1993;
Fallon, Rosen, and Pliner 1984), claimed that taste discrimination of toxins and of
digestibility-reducing compounds in plants is an active component of food choice
in all mammals. And Milton (1991) found that a nutrient-availability/digestion-
inhibitor ratio predicted food selection in many frugivorous primates.
Gastrointestinal distress has been experimentally manipulated in all kinds of
animals to enhance taste discrimination at progressively smaller levels of toxic
compounds and among previously ignored differences in taste (Garcia, Hankins,
and Rusiniak 1974; Milton 1984; Simmens 1994; Wilkerson and Rumbaugh
1978). Several principles have been unequivocally established. First, everything
else being equal, the stronger the taste of the food or drink, the greater the aversion
that is induced by illness. Second, the more severe the illness, the stronger the
aversion for the taste. Third, if neither the taste nor the severity of the illness vary,
the strength of the aversion is inversely related to the span of time between
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GUT MORPHOLOGY AND CARRION AVOIDANCE 491
consumption and illness (Garcia, Hankins, and Rusiniak 1974:825). Unlike
classical conditioning, where an animal acts as if it had acquired information about
a negative stimulus in some spatial-temporal context, aversion conditioning
changed the hedonic value of the substance; the animal acts as if the substance were
unpleasant--e.g., a rat will rub its chin on the floor in a sign of disgust and groom
itself vigorously. Many animals make involuntary disgust gestures and in extreme
cases retch (Garcia, Hankins, and Rusiniak 1974:831). An aversion remains strong
even when the taste is encountered in a new place and mixed with favorite foods
that are not associated with digestive illness (Garcia, Hankins, and Rusiniak
1974:828).
Experimentally inducedfood aversions do not require the temporal contiguity
of cue and consequence. A rat will avoid a food even when the illness occurs hours
after it is consumed or the illness is experimentally induced in an unconscious
animal sometime after eating (Garcia, Hankins, and Rusiniak 1974:825).
Moreover, the rat will not necessarily avoid the food that is consumed immediately
before becoming ill; if that food is bland and familiar, the rat is more apt to avoid
a distinctively flavored, novel food that was eaten hours before any symptoms
occur (Garcia, Hankins, and Rusiniak 1974; Rozin and Kalat 1971). Conditioning
to food-induced illness can occur in a single trial and rarely requires more than
three to five trials, even though the negative effects of the meal are delayed for
hours (Garcia, Hankins, and Rusiniak 1974:831; Rozin 1987; Rozin and Fallon
1981; Rozin, Fallon, and Augustoni-Ziskind 1986). Conversely, research shows
that if recuperation from internal distress follows the ingestion of a substance, the
taste of that item is enhanced (Garcia, Hankins, and Rusiniak 1974:831; Rolls
1997; Schiefenhovel 1997).
Parenthetically, the positive enhancement of the tastes of substances that are
associated with recuperation has tantalizing implications for our understanding of
the use of rarely eaten plants for medicinal purposes by primates and other animals
in the wild (Huffman and Wrangham 1994:141). The same mechanism that
operates in food aversions could also act to establish internal cues for medicinal
plant or mineral choices. Such rapid conditioning to the homeostatic effects of
ingested substances through a hedonic adjustment of palatability would make the
process of trial and error discovery quick and reliable and would minimize the risk
of accidentally losing esoteric knowledge about medicinal plants and minerals.
The existence of gustatory conditioning through the relief of symptoms would
explain how widely separated primate populations have so often achieved the same
phytochemical solutions to particular kinds of internal distress. Geographically
separated populations of monkeys and apes could be expected to consume rarely
eaten leaves, bark, roots, and clay in response to particular symptoms of visceral
distress because substances in those items have relieved their symptoms-if only
once before. "Not only does visceral illness condition a strong aversion to an
ingested substance after one trial, but relief of symptoms of parasite infestation,
and plant, bacterial, or insect toxin might just as effectively condition the
consumption of unpalatable, fruit, leaves, bark, roots, gravel, and clay through the
same pathway" (Garcia, Hankins, and Rusiniak 1974:831).
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492 JOURNAL OF ANTHROPOLOGICAL RESEARCH
Even carnivores, including eagles and wild cats, can be conditioned to avoid
particular kinds of foods:
the coyote, a specialized carnivore, was not subjected to the same
evolutionary pressures as herbivores. After all, most natural toxins exist in
plants, while toxic animals are distinctive and rare. In addition, the coyote
was described a natural killer who killed animals even without a need for
food. However, after coyotes had consumed one or two meals consisting of
minced lamb flesh, skin, and wool infused with lithium chloride, and had
consequently experienced lithium illness, they refused to attack lambs. In
fact, these "killers" ran away from the lambs and retched. The same coyotes
continued to attack rabbits, indicating that the aversion was specific for
lamb flesh-that is lamb was no longer an incentive for the coyotes. (Garcia,
Hankins, and Rusiniak 1974:830; emphasis added)
This kind of conditioned gustatory response could just as easily result in carrion
avoidance in animals that hunt occasionally and have a relatively small proportion
of animal protein in their diet.
Milton (1991), Rozin, and others (Fallon, Rozin, and Pliner 1984; Heligman
and Hager 1972) showed a sensitive period for juvenile mammals and birds during
which food preferences and aversions are readily acquired. The diet of the
mammalian mother imparts characteristic tastes to her milk, setting a high hedonic
value on these tastes for her nursing offspring; this establishes some basis for later
food avoidances before weaning. Birds and mammals continue to feed their young
until the young learn to forage or hunt; during parental feeding, offspring continue
to acquire tastes for specific foods brought to the nest or den (Galef 1990; Garcia,
Hankins, and Rusiniak 1974:830). Thus, in both humans and animals, many
avoidance behaviors are conditioned during early feeding, and the young never
actually taste the offending foods or experience a specific food-related illness
(Bailey 1993; Barton et al. 1992; Fallon, Rozin, and Pliner 1984; Gordon 1987;
Hohmann and Fruth 1997; see also Wilkerson and Rumbaugh 1978). 3
"Easy food contamination, a low-protein/high-carbohydrate diet, sporadic
gorging on meat, and the presence of digestion-inhibitors in the staple foods
provided ideal conditions for the maintenance of bacterial infection and
poisoning" (Lawrence 1992:341, emphasis added). These conditions probably
prevailed among hominids until the use of fire for cooking meat and would have led
to carrion avoidance among hominids and other meat-eating primates.
PASSAGE KINETICS AND DIGESTIVE STRATEGY: NATURAL
DEFENSES AGAINST HEAVY LOADS OF INGESTED BACTERIA
AMONG HUNTING AND SCAVENGING ANIMALS
If eating scavenged animal matter created a high risk of intestinal illness and,
as a result, led to avoidance behavior toward carrion, how would scavenging
animals manage to avoid illness? The animal's best defense against a bacterial
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GUT MORPHOLOGY AND CARRION AVOIDANCE 493
invasion of the gut consists in a prolonged exposure of the food bolus to stomach
acid and then the rapid passage of potentially contaminated items through the
vulnerable intestine. Hoelzel (1930), Stevens (1977, 1988; Stevens and Hume 1995),
and Milton (1984, 1999a) found a rough correlation between body size, food
choice, and food transit time (Clemens and Phillips 1980; Sibly 1981) (Table 1).
TABLE 1
Transit Times Cited in the Text
Time of First Appearance Mean Transit Time
15-20% of Markers 50-60% of Markers
Animal Species N (hours) (hours)
Chimpanzee 6
Low-fiber diet 27.4 48.0
High-fiber diet 23.3 37.7
Orangutan 3 24.2 73.7
Gorilla 4 23.4 57.2
Vervet monkey 24.0
Macaca mulata 17-28
Domestic dog 4-6 8-10
Domestic cat 11-24
Mink 2.4 (1.03-3.6)
Polar bear (814 Ibs.) 17-18 23-26 (bimodal defecation)
Human 24 26.0
Low-fiber diet 62.4
High-fiber diet 40.9
Sources: Chimpanzee, orangutan, gorilla, polar bear, and human data from Milton (1999a: 14, table 1).
Vervet monkey and domestic dog data from Stevens (1977:109-14). Macaca mulata data from Hoelzel
1930:476-78. Human data also from Sussman (1987).
Stomach acid either kills bacteria or stimulates them to produce toxins that
cause regurgitation. The storage of meat in the acid bath of the carnivorans'
stomach may eliminate most ingested bacteria. The extremely rapid passage
through the intestine prevents bacterial spores that remain in the food bolus from
colonizing either the small or large intestine. If the food bolus passes quickly into
the neutral pH environment of the intestine, contaminant bacteria move with it.
Stomach acid will kill ingested bacteria but not necessarily bacterial spores, and a
partial buffering of stomach acidity by ingested food may last up to two hours after
eating. Many of the bacteria that cause intestinal disease produce toxins when they
contact gastric acid; vomiting ensues, and the stomach is emptied, incidentally
protecting both bacteria and the host. Vomiting may not eliminate all the
bacterially contaminated food and, thus, protracted diarrhea, cramping, fever, and
pain due to bacterial toxins in the intestine often follow, which can affect kidney,
liver, and pancreatic function.
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494 JOURNAL OF ANTHROPOLOGICAL RESEARCH
The rapid movement of digestia through the intestine can limit bacterial
reproduction in the gut. A successful colonizing effort depends on the number and
virulence of the contaminant ingested, the condition of the host, and the
effectiveness of vomiting and diarrhea in the evacuation of the stomach and gut.
Holding the food bolus in the stomach for several hours after gorging and
extremely rapid digestive kinetics-the speed with which the bolus passes through
the small and large intestine-underlie the ability of carnivores to eat carrion
without getting sick. The contents of the human gastrointestinal tract have a
residence time of 48 hours and the GI tract has a working volume of eight liters-
any ingested microorganism that doubles less than two times a day will wash out.
In a dog, where the residence time is less than 12 hours, any ingested organism that
doubles less than four or five times a day will wash out (Tierno, personal
communication).
In Stevens and Hume's (1995:127-28) study of the digestive kinetics of
mammals (Figure 2), the dog did not release particulate markers from its stomach
for almost 4 hours after ingestion. Subsequent to the markers' release, they passed
quickly through the intestine and appeared in the feces in 5 to 8 hours; it took less
than 12 hours for all of the markers to appear in the dog's feces. Wolves, dogs, and
cats gorge and can store the food bolus in the stomach for up to 12 hours, while
releasing small portions into the intestine for digestion and quick absorption
(Mech 1975). Carnivores have relatively short intestines, smooth intestinal walls,
and lack a caecum; as a result, the digestive tract has a low absorption potential and
a rapid transit time (Mech 1975; Schaller 1972:270; Thompson 1952). The very
rapid breakdown of animal protein by digestive enzymes into amino acids insures
that despite the rapid passage of the food bolus through the small intestine and
colon, wolves, lions and other carnivores are capable of absorbing close to 95
percent of the amino acids in ingested protein (Mech 1970). According to Stevens
and Hume (1995), all the major scavengers, such as wolves, hyenas, jackals, wild
dogs, lions, and even scavenging birds and reptiles, follow this pattern of gorging,
storing food in the stomach, and releasing small portions of meat into the small
intestine where they are quickly digested or eliminated (Gittleman 1989; Glickman
1995; Mech 1970, 1975).
Milton (1999a) reported the transit time for a small pure carnivore such as a
mink as 2.4 hours (range 1.03 to 3.6 hours) and a remarkably rapid, bimodal pattern
of defecation for a polar bear (see Table 1). In contrast, the characteristic gut
anatomy and digestive kinetics of extant apes result in the rapid release of the food
bolus into a moderately long small intestine and its slow passage through it, the
small caecum, and into a capacious, markedly sacculated colon. Human gut
anatomy is quite similar to that of apes, although the caecum is poorly developed
or absent and the walls of the small intestine are more or less smooth rather than
heavily villiform (Snipes 1994). Despite differences in adult body weight and
preferred foods, solid indigestible food markers first appeared in the feces of
various apes and humans in approximately 24-26 hours after being ingested and
continued to appear for three to six days (Milton 1999a:14, table 1). Captive
chimpanzees that were fed on a diet low in fiber yielded mean transit times (MTT)
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GUT MORPHOLOGY AND CARRION AVOIDANCE 495
PIG
10 Liquid
75 2mm
50. 0 2 HR
754 HR
4HR
50
25
75-r8HR
50
25 - L,
DOG 75 12 HR
50
8011)25 -6,_
2HR 751HR
40- 50-
75220 HR
80 75450
8 HR 75 38 HR
40 50
25
12 HR 25- n n
S1 S2 SI1 SI2 SI3 C C1 C2 Sl S2S1SIS2SI3CesPCC2C3C4CS TC
Section of Tract Section of Tract
VERVET MONKEY
sok 2HR
40
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Section of Tract Section of Tract
Figure 2. Percentage of Digesta Fluid and Particulate Markers Recovered from the
Gastrointestinal Tracts of the Dog, Pig, Raccoon, and Vervet Monkey at Various Times
Following Oral Administration at the Time of Feeding.
Raccoons were fed a commercially prepared, pelleted, low-concentrate, high-fiber diet.
Dogs were fed a meat diet. Animals were fed at twelve-hour intervals for at least two weeks
before the study. Fluid markers consisted of PEG or "5Cr-EDTA. Plastic particulate markers
consisted of polyethylene tubing with an outside diameter of 2 mm, cut into lengths of
2 mm. Animals were sacrificed in groups of three at the times designated following the meal,
and sections of the gut were immediately separated by ligatures for recovery markers. Solid
bars = fluid markers; open bars = particulate markers; S = stomach; SI = small intestine;
Ce = cecum; C = colon; F = feces. Modified from Stevens and Hume (1995:127-28).
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496 JOURNAL OF ANTHROPOLOGICAL RESEARCH
of 48.0 hours, while those fed high fiber meals yielded MTTs of 37.7 hours. The
MTTs in orangutan and gorillas were 73.7 and 57.2 hours, respectively. The MTTs
in humans were 62.4 hours on low-fiber meals and 40.9 hours on meals with high
fiber contents (Milton 1999a: 14, table 1).
In many primates, including humans, the food bolus containing enteric
infective organisms may pass through the stomach in as little as 30 minutes, and
because food and saliva buffer the effect of stomach acid, some contaminant
bacteria and spores are likely to enter the more hospitable environment of the
intestine. A vervet monkey passed the first particulate markers from its stomach
into the small intestine in less than 2 hours, and the markers were seen
accumulating in the caecum 4 hours after ingestion; markers remained in the
caecum and passed slowly into the colon over the next 12 to 60 hours (see Figure
2). The pig's digestive strategy differed from those of primates in that pellets
remained in its stomach for 8-24 hours, moved quickly through the small intestine,
and accumulated in an enlarged caecum for 4 to 8 hours; the bulk of the pellets were
eliminated in 50 hours. The pattern of pig digestive kinetics demonstrates that similar
overall transit times can be found in animals that differ in digestive strategy.
In non-Colobine primates, food is released from the stomach into the small
intestine relatively quickly (Stevens and Hume 1995). Because feeding may go on
for several hours and the gastric acids are continuously buffered by saliva and
ingested food particles, ingested bacteria and bacterial spores are likely to be
released into the small intestine with food during these prolonged periods of low
acidity. While bacterial toxins can be produced in the stomach and illness can
develop within half an hour, visceral response may be delayed by as much as 24 to
48 hours. The digesta transit from ingestion to defecation takes five times longer in
humans and seven to eight times longer in chimpanzees than in dogs and wolves.
Contaminant bacteria and spores that are ingested by chimpanzees and humans can
remain in the intestine for days rather than hours, which gives the bacteria ample
time to colonize and produce gastrointestinal distress.
Both the Hominoidea and the Carnivora appear to have retained their ancestral
patterns of gut anatomy and digestive kinetics. Gut morphology is
phylogenetically conservative; wolves, dogs, foxes, bears, raccoons, and pandas
include various amounts of fruit, leaves, and shoots in their diets, but their use of
plant foods is not reflected in significant changes in gut anatomy or digestive
kinetics (Milton 1999a: 14). Hundreds of thousands of years of digestible, calorie-
rich, cooked, and refined diets have not changed the pattern of kinetics or the rate
of transit through the human digestive tract (Milton 1999a: 14, table 1). Thus, the
pattern of passage kinetics within lineages appears conservative, and despite a
considerable degree of gut plasticity in individuals and populations, it is unlikely
that the digestive strategy of fossil hominids differed significantly from the one
observed in modern apes and humans (Milton 1999a:12-15). The initially low
protein diet of early hominids coupled with the high bacterial load of raw meat,
especially carrion, would have made either passive or confrontational scavenging
extremely dangerous and, therefore, an unlikely source of protein for them before
the use of fire for cooking.
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GUT MORPHOLOGY AND CARRION AVOIDANCE 497
EVIDENCE OF DIETARY STRATEGIES IN EARLY HOMINIDS
The distinctive patterns of dental development and eruption in
Australopithecines and early Homo are the result of developmental and dietary
changes that are difficult to disentangle (van der Merwe, Cushing, and
Blumenschine 1999; Smith 1991; Thomson 1986; Turner and Wood 1993).
Pounding roots would leave dirt and stone grit, but the pulp would require less
mastication than unprepared USOs, and if the pulp were soaked or cooked before
consumption, the amount of chewing and thus surface pitting and abrasion on
posterior tooth surfaces ought to have decreased noticeably. The heavily stress-
cracked, pitted molar surfaces of Australopithecus species suggest tough, fibrous,
gritty food that is incompatible with a very high proportion of meat or cooked
rootstocks in the diet; on the other hand, the pattern of edge damage on stone cores
suggests that hominids could have been digging, crushing, and pounding fibrous
USOs, as well as extracting marrow from bones (Brain 1988; Hatley and
Kappelman 1980; Kay and Grine 1988; Leakey 1971, 1980; Puech 1984; Puech,
Albertini, and Serratrice 1983; Ryan and Johanson 1989; Tattersall 1993).
No archaeological evidence suggests that the Australopithecine demes ate any
more meat than present-day chimpanzees.14 Rootstocks or the more easily gathered
rhizomes of marshland sedges could have provided the additional energy necessary
for hominid adults to range over larger areas than modern apes and to feed
semidependent juveniles hard-to-obtain foods (Wrangham et al. 1992).
Australopithecus robustus, Homo habilis, and early Homo erectus/ergaster were
more likely to differ in the proportion of animal food that supplemented their usual
fare of fruit and rootstocks (Milton 1999a, 1999b) rather than in the proportion of
rootstocks that supplemented fruit and tender greens (see note 3, this article;
O'Connell, Hawkes, and Blurton Jones 1999; Wrangham et al. 1999).
The only reliable sources of animal foods that were available to our earliest
encephalized ancestors may have been the small mammals, reptiles, and insects
caught by hand and larger prey hunted with clubs and sticks. However, early
Homo's sharp-edged stone flakes, handaxes, and cut-marked large prey animals are
evidence for butchering meat and extracting marrow. Pointed wooden shafts that
are associated with the dismembered skeletons of mammoths and other very large
animals have been found at the Middle Pleistocene sites of Kalambo Falls,
Torralba, Clacton, and Lehringen, as well as at Schoeningen. It is likely that
sharpened wooden spears were the most effective weapon for hunting bison, deer,
mammoth, and horse until the Middle Paleolithic, when stone projectile points
appeared and some evidence for hafting points begins. Sharpened wooden spears
continued to be effective killing implements among subsistence hunters into
historic times, however.
Lacking hafted stone points or long-range weapons, early men could not have
been very efficient hunters; on the other hand, scavenged meat had a high bacterial
load and would have caused frequent illness. Aversion behavior toward scavenged
meat was likely to have been conditioned in a single trial. This "Garcia effect,"
which would prevent the consumption of the bacterially contaminated prey of other
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498 JOURNAL OF ANTHROPOLOGICAL RESEARCH
carnivores, has profound implications for hominid dietary choices and food
preparation behavior.
CONCLUSION
The evidence for physiological constraints that inhibit scavenging in
nonhuman primates and humans is strong, albeit indirect. Since the funnel-shaped
thoracic cavity of early hominids suggests that their intestinal morphology was
similar to that found in chimpanzees (Aiello and Wheeler 1995; Hladik, Chivers,
and Pasquet 1999; Milton 1995) and their enormous low-cusped molars were
cracked and pitted, it is likely that Australopithecines and early Homo consumed
mostly high-fiber fruit, nuts, and gritty rootstocks. Daily protein consumption was
likely to have been low among these hominids-perhaps slightly higher than that
of woodland chimpanzees. Animal protein would be only sporadically available
and protease production relatively low, and early hominids would have been as
prone to gastrointestinal illness as modem apes and human populations with low-
protein diets (Milton 1999a, 1999b; Powell 1985; Sept 1992a, 1992b; Speth 1987,
1989). Uncooked, bacterially contaminated meat would have caused intestinal
disease and conditioned adult hominids to avoid carrion. Carrion avoidance would
spread quickly through the entire group because of the habituation of adult feeding
choices among juveniles.
Because primate food avoidances are conditioned rather than innate,
scavenging will occasionally emerge under conditions of social and/or nutritional
stress and then quickly disappear (Nishida 1994; Strum 1981). Scavenged
carcasses came to be included in modern human diets only with the advent of
cooking and storage techniques that control bacterial growth. Finally, since the
demand for essential amino acids and micronutrients would have increased in
proportion to the overall changes in body and brain size, it seems reasonable to
assume that these additional nutrients necessary for Homo ergaster/erectus growth
and development would have had to be satisfied by hunting, rather than
scavenging.
NOTES
1. We gratefully acknowledge the suggestions and encouragement of the late
Professor Gordon Hewes (University of Colorado, Boulder) and Professor Nancy Bogen
(Department of English, College of Staten Island-City University of New York).
2. The authors use the word "carrion" to indicate the flesh scavenged from the kills of
primary predators or from an abandoned carcass. Animals killed and immediately
consumed by the hunters and/or comembers of a primate or hominid group are not
considered carrion. Beached sea mammals and terrestrial animals that did not die from
predation are carrion. Sea mammals whose skin and intestines are still intact so that the flesh
is uncontaminated by intestinal and fecal material may be butchered and subsequently
buried, refrigerated, or dried. Such meat, which is protected from bacterial infestation from
flies or other insect scavengers, may undergo partial digestion (putrefaction) by its own cell
lysosomes and yet remains safe to eat even after several weeks.
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GUT MORPHOLOGY AND CARRION AVOIDANCE 499
3. The stable-isotope ratios of 13C/12C, which are determined by CO2 photosynthetic
pathways, reflect dietary sources of carbons. These stable-isotope analyses not only
distinguish between different types of herbivorous diets but also make quantitative
estimates about the contribution of various foodstuffs to the diet. The most recent studies on
the structural carbonate in tooth enamel have confirmed that all early hominids, including
Australopithecus robustus, show a mixed diet with the 20-30 percent C4 contribution
probably derived from eating the flesh of grazing animals. African savanna grasses,
rhizomes, and seeds are almost exclusively C4; the fruit of trees and shrubs and rootstocks
are dietary sources of C3 (Lee-Thorp, van der Merwe, and Brain 1994; Sillen and Lee-
Thorpe 1993). Sillen (1992) has proposed that the different concentrations of skeletal
strontium relative to calcium may differentiate low-fiber diets from high-fiber diets.
Because dietary fiber binds calcium more effectively than strontium, foods high in fiber,
such as tubers and leaves, ought to leave higher skeletal Sr/Ca ratios than low-fiber foods
such as fruit and meat. An omnivorous diet that contained fruit, tubers, and meat in
proportions that vary seasonally and food preparation, such as cooking, that released bound
nutrients such as calcium from fibrous tubers and leaves may pose problems in
interpretation. See also, Ambrose and DeNiro 1986; Fitzer, Schoeninger, and Sept 1993;
Schoeninger 1989, 1996; Schoeninger, DeNiro, and Tauber 1983; Schwartz 1991;
Schwartz and Schoeninger 1991; Lee-Thorp, van der Merwe, and Brain 1994.
4. The importance of female gathering is noted among bonobos: "food sharing among
adults is most common among females, who share with unrelated individuals as well as with
their own infants" (Nishida and Hiraiwa-Hasegawa 1986:172). Bonobo females apparently
share food with the juveniles in the troop, both their own offspring and the offspring of
others (Kuroda 1984; Tuttle 1986).
5. Compare Milton's discussion of Langworthy and Deuel (1920) in her Evolutionary
Anthropology article (Milton 1999a) to her comments to the Wrangham et al. (1999) article
(Milton 1999b); in the latter, she notes that grating and soaking probably increased the
digestibility of the carbohydrates in the Langworthy and Deuel study.
6. Recent work on a variety of underground cultigens and wild rootstocks has
emphasized the complexity of starch and sugar digestion and the presence of protease and
amylase inhibitors in rootstocks that would require preconsumption preparation (Altman,
Post, and Klein 1987; Johns 1996; Johns and Kubo 1988; Katz 1987; Lawrence 1992;
Prathibha, Nambisan, and Leelamma 1995; Wanasundera and Ravindran 1994; Waterman
1984). Some simpler types of starches and sugars are water soluble and are easily digested
by humans. More complex forms of carbohydrates, such as soy beans, sago palm, casava,
and domesticated seeds, definitely require complex preparation and cooking (Johns and
Kubo 1988; O'Connell, Hawkes, and Blurton Jones 1999; Stahl 1984; Wandsnider 1997).
7. Only four instances of fire-altered debris and clay have been found between 1.6 and
1.0 mya: at Swartkrans (member 3), at Koobi Fora (FxJj 20), at Chesowanja, and at Gadeb
associated with very early Acheulian stone debris. James (1989:4; Clark and Harris 1985)
concluded that there was reason to believe that "the reddened patches, burned clay, and
burned lithics at the East African sites . . . were produced by natural fires or volcanic
activity." The Swartkrans fire-altered bone fragments have been redeposited into the
crevasse from the surface, and the exact relationship between the fire damage and the
hominid activity is very unclear (Brain 1993; Brain and Sillen 1998; Bunn 1999).
Chesowanja and Koobi Foora have literally dozens of patches of fire-reddened earth, only
two of which were associated with hominid activity; the association of a couple of the
largest, longest-burning fire features with stone-working debris suggests an opportunistic
use of a natural fire for warmth or protection (Bunn 1999:579).
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500 JOURNAL OF ANTHROPOLOGICAL RESEARCH
8. One cannot discount the small intestine as a microbially significant entity. In the
upper small intestines, Lactobacilli and Enterococci are predominant, but in the lower
ileum of the small intestines and the cecum, the flora is mostly fecal. Intestinal bacteria (1)
synthesize vitamin K, (2) convert bile pigments and bile acids, (3) allow absorption of
nutrients and breakdown products, and (4) act as antagonists to potential microbial
pathogens. Lactobacilli act as prohibitors-they prevent establishment of, or compete with,
potential pathogens by producing bacteriocins. For example, lactic acid bacteria prevent
diarrhea when taking antibiotics, decrease serum cholesterol in vitro in lab media via
oxidation or assimilation, and ameliorate lactose intolerance. Shigellae infects the terminal
ileum and large intestine, Salmonellae make lesions in the small and large intestine,
Campylobacter multiply in the small intestine, and Vibrio (cholera) colonize the microvilli,
or brush border, of epithelial cells.
9. Milton (1999a:18) suggested that there are no significant amylase inhibitors or
difficulties in digesting the carbohydrates of cultivated rootstocks; this has been
contradicted by much recent research on nutrition (Carpenter 1994; Cook 1979; Katz 1987;
Hawkes, O'Connell, and Blurton Jones 1999; O'Connell, Hawkes, and Blurton Jones
1999; Ulijaszek 1995; Wanasundera and Ravindran 1994; Waterman 1984). Furthermore,
in the Langworthy and Deuel study (1920), raw potato, corn, and wheat were grated and
starches were extracted from the roots and kernels and mixed into some kind of pudding.
The grating and extraction processes have a leaching and deactivating effect on the
digestive-inhibiting compounds and starch composition that was not controlled (cf., Milton
1999b:584; Johns and Kubo 1988).
10. The rise of such infections in industrialized countries is apparently the result of
unsanitary conditions in slaughterhouses, where fecal and intestinal contents frequently
come into contact with the meat, thereby contaminating it. Further opportunity for
contamination occurs in the precooked and packaged meats that sit on the open shelves of
butcher shops and supermarkets (Macfarlane and Gibson 1995).
11. Synanthropic flies, particularly Calliphorids, are initiators of carrion
decomposition and, as such, are actually the primary and most accurate forensic indicators
of time of death of an animal (Greenberg 1991). According to Shean, Messinger, and
Papworth (1993), rates of decomposition are significantly more rapid in the open than in
shaded woodland. An exposed pig carcass reached a stable minimal weight two weeks
before a shaded carcass did; maggot development appeared to be a major factor in
determining the overall rate of decomposition and was affected primarily by different
temperature patterns at the two sites.
12. "At times lions use a special technique to remove vegetable matter from intestines
before eating them: one end of the intestine is placed on the rough tongue and drawn in
slowly with a light lapping movement past the incisors which serve to squeeze the material
out of the other end. Some of it may also be shaken out" (Schaller 1972:269). Leopards, too,
often eat the viscera first, but tigers tend to consume the meat from the rump and thighs
before the intestines (Schaller 1972:269). Cheetahs, on the other hand, leave the digestive
tracts of their prey intact; large, Plio-Pleistocene "sabertooth cats," similar to cheetahs in
locomotor morphology and habitat, may have also devoured their prey without
disemboweling it; such kill would have had a relatively small initial bacterial load. If
hominids limited confrontational scavenging to "sabertooth cat" kills prior to the bursting
of the intestine, then they might have avoided meat heavily contaminated by fecal bacteria
(cf., Blumenschine 1991; Cavallo and Blumenschine 1989; Bunn and Ezzo 1993; Marean
1989).
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GUT MORPHOLOGY AND CARRION AVOIDANCE 501
13. Food preferences and avoidance behavior have been manipulated among primates
and other small mammals in laboratories, and food avoidance was quickly and easily
induced (cf., Rozin 1987; Rozin et al. 1993; Waterman 1984).
14. Root or cereal crops have supported some modem peoples on very small (4-7
percent) daily amounts of protein (de Garine 1997:230).
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... Moving onto gastrointestinal barriers, some necrophages hold food in their stomachs for an extended period (e.g. ∼4-12 hours for wolves and dogs versus ∼0.5-2 hours in primates) [57]. Inter-study comparisons of animal stomach acidity are challenging because of the many variables affecting measurements [58], but very low pH values have been documented in necrophages such as the white-backed vulture (pH 1.2) [59]. ...
... Some necrophages also have shorter intestinal tracts, so subsequent transit and excretion of the food bolus and any surviving bacteria is more rapid (e.g. 5-8 hours in dogs versus ≥12-60 hours in primates) [57]. ...
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... Even based on a small sample of modern humans, we are able to show much more variation in gut morphology than heretofore noticed. Where previous studies have compared the relative size of large intestines to small intestines in humans and extant ape species (as a measure of the degree of specialization on gut-fermented foods), those studies have included data from just six humans, described as ''urban males'', all from a single population (Ragir, Rosenberg & Tierno, 2000). Those six human males from a single, urban population were then compared to data from a single chimpanzee (Chivers & Hladik, 1980). ...
... Most catarrhine primate digestive systems are characterized by a simple stomach, a C-shaped duodenum, and a more globular and reduced cecum with increased emphasis on microbial fermentation in the colon (Stevens & Hume, 1998;Lambert, 2002). This is due, in large part, to a primarily herbivorous diet, which is quickly passed through the stomach and duodenum before slowing in the ileum and cecum (Ragir, Rosenberg & Tierno, 2000). By comparison, humans consume a greater diversity of food items comprising less fiber and more protein and fat; yet the only substantive morphological difference is a longer small intestine in humans (Carmody & Wrangham, 2009;Watkins et al., 2010). ...
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... Jim Peaco / Wikimedia Commons [24] The physiological defences scavengers have evolved are even more interesting. For example, wolves [25] hold food in their stomachs for up to 12 hours, twice as long as humans [26]. This gives their stomach acid longer to kill bacteria before they reach the gut. ...
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... Gut passage time varies between taxa, potentially contributing to the variation in seed viability and germination results of ingested seeds across taxa (Traveset 1998). Carnivores and omnivores have relatively fast gut passage rates (Ragir et al. 2000), whilst herbivores have longer retention times. For example, elephant Loxodonta africana retention times range from 21.4 to 46 h, blue wildebeest Connochaetes taurinus ranged between 45 and 75 h and white rhinoceros Ceratotherium simum retention times were estimated at 47 h (Rees 1982;Karasov et al. 1986;Manzano et al. 2005;Steuer et al. 2011). ...
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... The benefit of a diet high in meat is that it provided a concentrated source of protein to meet the high energy requirements of the large human body size and brain, reducing the time required foraging [62]. In terms of disgust, the consumption of meat, especially scavenging decaying meat, was also accompanied by a greater risk of gastrointestinal illness [63]. Thus, the emergence of heightened disgust towards signs of contaminated meat would have been beneficial in an omnivore that has increased its dependence on meat but does not have the evolved meat-borne pathogen protections possessed by carnivorous scavengers [44,64]. ...
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... The ethnohistorical account of an Inuit group that relied in part on "restes de phoques abandonnés sur la glace par les ours'' (seal remains abandoned by bears on the ice) during their long march between Baffin Land and NW Greenland is notable (21, p. 44). These examples show the relative importance of acquiring food from animals found dead as a complement to resources acquired by hunting (22). As explained by O'Connell et al. (19, p. 361), the "amount of scavenged animal tissue available to the Hadza would have been small indeed," but it was dependable. ...
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... An interesting question then is how far back in time does it actually go? If one assumes, as many do, that cooking is necessary in order to kill or inhibit the growth of pathogens such as C. botulinum, L. monocytogenes, and Salmonella, or to deactivate their toxic metabolites (e.g., Ragir et al. 2000;Smith et al. 2015), then the potential time-depth is dependent on when humans gained regular control of fire. This is an issue that has received a great deal of attention, yet one that remains far from resolved and quite contentious. ...
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It is widely known that traditional northern hunter-gatherers such as the Inuit included putrid meat, fish, and fat in their diet, although the ubiquity and dietary importance of decomposing animal foods seem often to have been underappreciated. There is no evidence that these arctic and subarctic foragers suffered from major outbreaks of botulism (Clostridium botulinum), or from the toxic metabolites of other pathogens such as Listeria monocytogenes or Salmonella spp., until the 1970s and 1980s when Euroamericans introduced more "sanitary" methods for putrefy-ing Native foods. While many scholars are at least generally aware of the importance of putrefied foods among such peoples, most would not expect similar practices to have been commonplace in the tropics, especially in hot, humid environments like the Congo Basin. And yet a deep dive into the ethnohistoric literature of sub-Saharan Africa, and elsewhere in the tropics and sub-tropics, shows that both hunter-gatherers and traditional small-scale rural farmers commonly ate putrefied animal foods, consuming some of it raw, frequently cooking it, but often barely so. Moreover, these ethnohistoric accounts make it clear that Indigenous peoples often preferred it that way. Equally surprising, this preference for putrid meat remained widespread in the tropics well into the first quarter of the 20th century. Combining the insights gained by looking at the consumption of putrid meat in both northern and tropical environments, several interesting implications become evident. First, it is clear that the disgust response with regard to the taste, smell, and sight of rotten meat is not a hardwired human universal, but more likely a learned cultural response, one that is closely linked to European colonization, Westernization, urbanization , and industrialization. Second, the capacity for both northern and tropical peoples to consume putrid meat suggests that their ability to resist the toxic effects of C. botulinum and other pathogens most likely stems in large part from the environmental priming of their gut floras and immune systems through early childhood exposure to pathogens rather than from genetic factors. This conclusion fits well with findings from recent microbiome research, including studies of the gut floras of monozygotic twins. Third, putrefaction rapidly, and with little investment of time and energy, provides many of the same benefits that one gets by cooking, because it effectively "pre-digests" meat and fat prior to ingesting them. Finally, we suggest that, by eating meat and fat in a putrefied state, early hominins could have acquired many of the benefits of cooking, but at much lower cost, and quite likely long before they gained control of fire. Until early hominins began acquiring fresh meat in substantial quantities, presumably by hunting, the most important benefits of cooking may have been in the plant food domain.
... In addition, carcasses are more difficult to be detected in dense forests than in open habitats not only for carnivores and other scavengers, including the hominins, as discussed later. Moreover, it is essential to note that a rapid detection of a carcass is more important for hominins than for carnivores, as the former cannot eat putrefied meat (Ragir et al., 2000;Espigares et al., 2013). Another aspect to consider in the access to scavengeable resources in a forest environment is the amount of flesh and other animal resources that are available in this type of habitat as well as the intensity of competition for them (see Rodríguez-Gó mez et al., 2016). ...
Article
The archaeopaleontological site of Dmanisi in Georgia, dated to ∼1.8 Ma, provides evidence on the first hominin dispersal out of Africa, while the sites of Barranco León and Fuente Nueva-3 in Spain, dated to ∼1.4 Ma, record the earliest hominin settlements in Europe. However, a number of issues related to the dispersal route, the climatic conditions and the ecological scenario of this dispersal event are subject to debate. In a recent paper in L’anthropologie, Agustí and Lordkipanidze (2019) proposed an alternative scenario for the arrival of hominins in the Caucasus, which they conceived as a forest refugium area during the Early Pleistocene, and discarded that their dispersal coincided with that of other members of the Ethiopian and Asian faunas, like the sabertooth Megantereon whitei or the giant hyena Pachycrocuta brevirostris. Our review of these issues suggests that: (i) the elongated sabers and reduced postcanine teeth of African M. whitei limited the ability of this predator to process the prey carcass, which resulted in scavengeable resources for the Dmanisi hominins; (ii) the mass estimate in excess of 100 kg obtained for the trochlear perimeter of the distal humerus of the hyena from Dmanisi shows that it can be confidently ascribed to the genus Pachycrocuta; (iii) the postcranial anatomy of the Dmanisi hominins was not advantageous for scavenging tree-stored prey; (iv) the laterally flattened upper canines of M. whitei could not withstand the loads that would result from climbing a prey carcass into a tree; (v) paleobotanical analyses suggest a temperate grassland ecosystem in Dmanisi, not dominant forest conditions, with enhanced aridity in the level of hominin occupation; (vi) similarly, the low frequency of arboreal pollen in the Levantine Corridor at ∼1.8 Ma points to more arid conditions than today in this area; (vii) many archaeopaleontological sites of the Rift Valley and its extension towards the Red Sea, the Levant and the Caucasus show evidence of tectonic, volcanic and/or hydrothermal events; and (viii) the delay of 400 ka in the arrival of hominins in Western Europe did not result from a lower availability of scavengeable resources.
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We trace the evolution of the hominin vocal tract in search of its "correlates" in human history. We highlight several possible relationships, including the possible role of tool use in facilitating the shrinking hominin craniofacial features, and the role of transmission in facilitating a phonetic culture.
Article
The human lineage transitioned to a more carnivorous niche 2.6 mya and evolved a large body size and slower life history, which likely increased zoonotic pathogen pressure. Evidence for this increase includes increased zoonotic infections in modern hunter-gatherers and bushmeat hunters, exceptionally low stomach pH compared to other primates, and divergence in immune-related genes. These all point to change, and probably intensification, in the infectious disease environment of Homo compared to earlier hominins and other apes. At the same time, the brain, an organ in which immune responses are constrained, began to triple in size. We propose that the combination of increased zoonotic pathogen pressure and the challenges of defending a large brain and body from pathogens in a long-lived mammal, selected for intensification of the plant-based self-medication strategies already in place in apes and other primates. In support, there is evidence of medicinal plant use by hominins in the middle Paleolithic, and all cultures today have sophisticated, plant-based medical systems, add spices to food, and regularly consume psychoactive plant substances that are harmful to helminths and other pathogens. We propose that the computational challenges of discovering effective plant-based treatments, the consequent ability to consume more energy-rich animal foods, and the reduced reliance on energetically-costly immune responses helped select for increased cognitive abilities and unique exchange relationships in Homo. In the story of human evolution, which has long emphasized hunting skills, medical skills had an equal role to play.
Chapter
However well the anatomy of the gastro-intestinal tracts of a wide range of mammals is described and quantified, there can be no real explanation of observed patterns without consideration of the mechanical and chemical properties of the food consumed, and of the digestive stages involved in its processing. This book aims to integrate findings from the many different types of investigations of mammalian digestive systems into a coherent whole. Using the themes of food, form and function, researchers discuss models of digestive processes, linking this with evolutionary aspects of food utilisation. Macroscopic and ultrastructural studies of the gastro-intestinal tract are also presented, as are physiological, ecological and biochemical aspects of the digestion of different food types. The book ends with an integrative chapter, bringing together the themes running through the earlier sections.
Chapter
However well the anatomy of the gastro-intestinal tracts of a wide range of mammals is described and quantified, there can be no real explanation of observed patterns without consideration of the mechanical and chemical properties of the food consumed, and of the digestive stages involved in its processing. This book aims to integrate findings from the many different types of investigations of mammalian digestive systems into a coherent whole. Using the themes of food, form and function, researchers discuss models of digestive processes, linking this with evolutionary aspects of food utilisation. Macroscopic and ultrastructural studies of the gastro-intestinal tract are also presented, as are physiological, ecological and biochemical aspects of the digestion of different food types. The book ends with an integrative chapter, bringing together the themes running through the earlier sections.