Wading for Food:
The Driving Force of the Evolution of Bipedalism?
Algis Kuliukas MSc (Human
Evolution & Behaviour, UCL, 2001).
Paper
submitted to Nutrition and Health, August 2002.
Abstract
The recent discovery of sahelanthropus tchadensis has brought into focus once more questions about the factors which may have led some ape clades to begin to evolve those most distinguished human traits: large brain size and bipedality.
This find, the oldest putative hominid yet, as well as recent nutritional studies have both strengthened the idea that human evolution occurred in water-side rather than arid, open savannah grassland habitats.
Evidence is accumulating that suggests that the large human brain is most likely to have evolved in littoral and estuarine habitats rich in naturally occurring essential fatty acids.
This paper adds further weight to this
view, suggesting that another key human train, our bipedality, might also be
best explained as an adaptation to a water-side niche.
Evidence from apes in the
wild show that though preferring to keep dry, they do go into water when driven
to do so by hunger and tend to do so bipedally. A
new empirical study of captive bonobos found them to exhibit 2% or less
bipedality on the ground or in trees but over 90% when wading in water to
collect food.
A review of
The paleo-habitats
of the earliest known bipeds, and all the evidence reviewed here (as is that of
the newly discovered Sahelanthropus),
is consistent with the hypothesis that wading contributed to the adaptive pressure
towards bipedality.
Word Count (Main Body Only) :17,674 (inc.
tables 18,828, inc. charts 19,457)
Word Count (Total, inc. title, abstract, contents, acknowledgements
& References): 21,810
Contents
3.2 Analysis of empirical data of captive Pan paniscus
bipedality
3. Was Australopithecus
afarensis a wading ape?
3.1. In which ways did A. afarensis move: two modes or
three?
3.2 Predicting Lucy’s bipedal gait
3.3 Sideways wading – Is it morphologically plausible?
4. Paleoecological and Geographical Evidence
4.1 Paleo-habitat of the earliest bipeds
4.3 Paleo-ecological conclusions
List of illustrations
Figure 6 Time spent in various substrates
Figure 7 Time spent upright (supported & unsupported
bipedalism) in different substrates
Figure 8 Unsupported (only) Bipedality by substrate
Figure 11 Pelvis and femur of Pan/Gorilla (left), Pongo
(centre) and Homo (right)
Figure 16 A comparative profile plot of H. sapiens and P.
paniscus
List of Tables
Table 2 Description of Postural Modes
Table 5 Orrorin tugenensis site
Table 6 Ardipithecus ramidus sites
Table 7 Australopithecus anamensis sites
Table 8 Australopithecus afarensis sites
Table 9 Kenyanthropus platyops
1. Introduction
The recent discovery of sahelanthropus tchadensis ? Buden et al (2002) has brought into focus once more questions of what factors may have led some ape clades to begin to evolve those most distinguished human traits: large brain size and bipedality.
From the paleoecology of the find it is
rather clear that water was a significant part of his landscape. The fossils
were found at the site of the ancient ‘Mega’
Recent nutritional and biochemical studies have strengthened the idea that human evolution probably occurred in water-side habitats and not, as is still largely advocated in many paleoanthropological circles, a predominantly semi-arid savannah environment.
Broadhurst et al (2002) show that there is a growing body of biochemical evidence suggesting that one of the key human traits, our large brain, could not have evolved on the savannah where, they argue, the quantity of certain naturally occurring essential fatty acids (EFAs) such as docosahexanoic acid (DHA) and arachidonic acid (AA) in the food chain is too meagre to have driven (or even allowed) such a dramatic increase in brain size. They argue that a water-side habitat, where such EFAs especially necessary for brain growth are very plentiful, is consequently more likely to have been the place where humans evolved.
One of the other key traits that
distinguish humans from other apes is our bipedality. Since
Despite its simplicity, plausibility and consistency with evolutionary paradigms (Darwinian natural selection and the Crawford/Marsh notion of substrate driven evolution - ‘plastic heredity’) little serious scientific study has been undertaken about the plausibility that the first bipeds might have waded in water.
This paper offers some new empirical evidence from captive bonobos which supports the hypothesis that the earliest bipeds may have been wading apes and that the motivation for doing so might have been the search for food. Furthermore it argues that traits in the fossil record of the most well known of the early bipeds - Lucy - which have remained controversial despite over twenty-five years of intense scrutiny - is not only consistent with the hypothesis but actually resolves many of the dilemmas and contradictions which remain if moving through water is not considered as a possible mode of locomotion.
Finally it proposes that the paleoecology of the earliest hominids is entirely consistent with this water-side based model for the evolution of humans.
The idea that bipedalism was first practiced in wading apes is not a popular one. It was first published in an English-language journal by Sir Alister Hardy FRS (1960) but has received little attention since. At least twelve other models, based upon purely terrestrial or arboreal models, are widely discussed including... Interestingly, most assume that food was a major motivator for the new behaviour locomotion.
No true consensus has yet arisen amongst these models to explain the
adoption of a bipedal mode of locomotion in hominids but one of the most promising
lines of investigation in this area has been to try to find analogues of
facultative bipedalism in extant apes. This approach was pioneered by Kevin Hunt who, in 1994,
published a landmark paper about an extensive study of wild chimpanzees (Pan troglodytes) in their natural
habitat in Gombe , Tanzania
In over 700 hours of
observation time he found that the chimpanzees studied spent less than 3% of
their time in a bipedal posture but that foraging for food in the lower
branches of trees was the most common motivation for doing so, when they did.
Following in Hunt’s
footsteps, Videan and McGrew (1999?) published findings from a similar study
comparing chimpanzee bipedalism with their sister clade bonobos (Pan paniscus)
in captive settings. They found similar levels of bipedalism between the two
and that food collecting was less of a motivator in captivity. ??
Neither study showed
any evidence for wading bipedalism, however this was hardly surprising as Videan
& McGrew’s study was conducted in enclosures that did not contain bodies of
water and Hunt’s study of wild chimpanzees merely demonstrated how, in their
typical habitat, chimpanzees usually avoid water completely.
The fact that
chimpanzees do not spend much time in and around water today, however, does not
mean the early ancestors of humans did not do so. Indeed it does not mean other
apes today do not do so either. The questions remain: how do apes behave when
they do move in water? And what
evidence is there that hominid ancestors may have done so?
The next two section will attempt to answer one of these questions each.
2. Wading in extant apes
The extant apes Pan troglodytes, Pan paniscus, Gorilla
and Pongo have not traditionally been
associated with wet habitats and have rarely been observed wading in the wild.
Indeed they have been considered so fearful of water that moats are often used
to contain them in captivity. There is consequently a remarkable scarcity of
scientific data about wading apes. A search of the literature revealed just how
little has been written about the phenomenon. Even anecdotal information is
rare although more recently, evidence (mainly film or photographic) has been
accumulating suggesting that all of the Hominoidae
may be more comfortable in water than might have been previously assumed.
Galdikas, Ellis and Sommer & Amman have all either commented about
orang-utans (Pongo) wading or have
published photographs showing such behaviours and Ashley Leiman of the Orangutan foundation made this
statement “Since 1986 I have visited Tanjung Puting National Park in Indonesia,
on numerous occasions. During this time I have frequently seen orangutans
wading bipedally in the swamp and river.”
Gorillas have also not traditionally been linked with water but Ellis
(1990:p57) provides anecdotal evidence in captive gorillas that they can swim.
Also Doran & McNeilage (1998:p121) and Parnell (2001:p294), studying
Western Lowland Gorillas in the field, provide evidence of splash displays and
feeding in the marshy swamps of Mbeli Bai. Parnell (2000, personal communication) observed
several bouts of bipedal wading in these animals and wrote….
Even chimpanzees, which have long been considered the most hydrophobic of
all the apes, turn out to be surprisingly fearless in water when they are sufficiently
driven by hunger to get their feet wet. Angus (1971:p51) and Nishida’s (1980) both
provide anecdotal evidence of chimpanzee locomotion in water. In addition to
this there has recently emerged some significant photographic footage of
chimpanzees wading bipedally in fairly deep (chest high) water from a research
student, Jess Tombs, working at a chimpanzee sanctuary in the Conkouati reserve
lagoon (See Tutin et al. 2001).
Finally, in bonobos too (the least studied of the great apes) there seems to be growing evidence that they are less fearful of water and show a greater tendency to wade than their chimpanzee cousins. Uehara (1976), de Waal (1996:p185), de Waal & Lanting (1999:p79-82) all document anecdotal evidence of bonobos moving in water in the wild.
What is lacking in the
literature, however, is a specific study into the way extant apes move in water.
It is this gap in the knowledge base that this paper attempts to begin to fill.
2.2 Analysis of
empirical data of captive Pan paniscus bipedality
Ten captive bonobos were studied at Planckendael wild-life park on the 12th April and 13th/14th June 2001 . They have a sheltered enclosure
which leads directly to a large island surrounded by a moat. Eight of the ten
bonobos in the group were studied.
The principle behind the study and the methodology used was largely based upon Hunt's (1994) work with some changes.
The most obvious difference was that this study was with captive bonobos not wild chimpanzees. Secondly, the study focused on the substrate in which the bipedalism was observed rather than the behavioural context in which it occurred. In this regard it specifically undertook to identify and quantify the types of locomotion exhibited in water.
All observations were made via this method (a Sony digital handy cam with 25 frames/sec precision.) Over fours hours of continual bonobo behaviour was recorded for detailed, in some cases frame-by-frame, analysis later. Thus, in three days, it was possible to generate potentially 14,400 lines of, continuous second-by-second, data to analyse. (Although actually, because the technique allowed long periods of inactivity to be ‘skipped’, the actual number of data items recorded in the database was 1,319.)
Postural categories were based upon the work of Hunt (1994).
The most significant ones for this study were:
Table 1 Description of Postural Modes
|
Postural Mode |
Description |
|
Bipedal |
Unsupported bipedalism. Subject stood or walked without the aid of upper limbs. |
|
Upright |
Supported bipedalism. Subject stood or walked with most of the body mass on the hind legs but using upper limbs for balance. |
|
Knuckle-walking |
Quadrupedal posture or movement. |
|
Swinging |
Brachiating whilst above the ground. |
|
Sitting |
Sitting. |
A mixture of observation techniques was used. Five focal studies were undertaken when one animal was followed continually for a half-hour slot. One hour's worth of observations were recorded of isolated, real or anticipated instances of contextual wading behaviour.
Inducing
Wading Behaviour
It is well known to staff at Planckendael that visitors to the bonobos often throw food items to them. This behaviour is strongly discouraged, but nonetheless the food is keenly accepted. Often these pieces of food fall short of their intended destination and, instead, drop into the large moat which surrounds it. When this happens the bonobos simply wade in and claim it.
One difficulty was that although it would undoubtedly have been very easy to induce the bonobos to wade into the moat, the authorities at Planckendael did not permit any such experimentation. Their reasoning was understandable: They did not want to be seen condoning the widely held practice of visitors throwing food to the animals. Also they are getting increasingly nervous about the prospect of the bonobos escaping the enclosure as they get more comfortable in the water.
This policy inevitably impacted on this study. Instead of controlling the wading events, the observations had to be predominantly reactive: waiting for and anticipating children (usually) to throw in pieces of food into the moat. This meant that the overall amount of time that bonobos were observed in water was very small (only about two minutes) however, workers at Planckendael have gone on record stating that their wading behaviour is very typical.
This study was primarily focused on the substrate that the bipedalism took place so four substrates were defined:
- Terrestrial, where the individual was at least partly touching land.
- Arboreal, where he or she was above the ground and not touching it. At Planckendael there are not many trees in the enclosure but there are a variety of climbing apparatus which were classified as arboreal nonetheless.
- "In Water", where no part of it was still touching dry ground.
- "Partly in water", where at least one part of the body was touching dry ground.
2.2.2 Results
Substrates
used
As expected, analysis of focal study data (only) clearly showed that bonobos prefer the terrestrial substrate (72.63%), with arboreality taking up almost all the other time (27%). Only 0.37% of time was spent in contact with water (See Fig. 6).
Figure 6 Time spent in various substrates
Although the absolute percentages displayed here should not be taken too literally, there is no doubt that bonobos generally prefer not to enter the water.
Mode
of posture and locomotion in water
The contextual data and focal data together were used to determine the levels of bipedality in different substrates.
Although only 37 seconds was spent in water with no contact with dry land at all, almost 92% of this time was spent in an upright (supported or unsupported bipedal) posture.
A larger proportion of time (121 seconds) was spent in water with some part of the body touching dry land. Apes in this substrate were upright for over 50% of the time. When terrestrial or arboreal, which accounted for over 99% of time for the group, the level of bipedality dropped to around or below 2%.
Figure 8 Unsupported (only) Bipedality by substrate
3.2.3 Discussion
The bonobos observed at Planckendael spent very little time in water and only did so at all because visitors threw food items (itself not encouraged) too weakly to reach them.
However there is no doubt that the amount of time they spent in the water was, very much, determined by human behaviour and it would seem that at least some individuals could have been induced into the water at will, in response to being offered food. Bonobos almost always entered the water feet first and adopted a bipedal posture even when the moat was shallow enough for them to have done so quadrupedally.
3.3 Conclusions
The anecdotal and observational evidence presented here clearly indicates that, although extant apes prefer not to get wet, they are more than prepared to do so if they are given a strong enough incentive to do so and that hunger is usually sufficient reason. In answer to the question ‘how do extant apes move in water?’ the answer would appear to be: bipedally. Or at least, it is far more likely to be bipedal than on land.
Equally clear is that in deep enough water, they have little choice but to move bipedally or swim. As only Gorilla out of the four great apes have been reported to be able to swim Ellis (1991:p55) it would seem that wading may occasionally be a life-saving behaviour in the wild.
It is difficult to imagine any other scenario with such a clear-cut, immediate survival benefit for moving bipedally as the one provided by waist deep water but it does beg a serious question: If a putative ancestor was regularly exposed to such a life-threatening habitat, wouldn’t they have been more likely, instead, to have evolved the ability to swim?
The next section investigates this problem and attempts to answer the question ‘what evidence is there that hominid ancestors may have waded bipedally?’
3. Was Australopithecus afarensis a wading ape?
In the 1970s
Instead he suggested that Australopithecines in displaying uniqueness in their morphology may have been functionally unique too. He wrote (p 329) “They therefore displayed either a totally new and unknown manner of locomotion which would be unique in its own right (and which we will judge unlikely), or they possessed such a mixture of locomotor abilities, therefore anatomical adaptations, and therefore, in turn, bony morphologies, as to be rendered unique through being curious functional and morphological mosaics.”
It was not the objective of this study to
concern itself with the phylogeny of the Australopithecines, although that is
clearly of some relevance. The objective, in this section, is to question its
curious morphology. Specifically, it is to consider
We have seen that bipedal wading is not so unusual a mode of locomotion in the Hominoidae after all. All of them have demonstrated that they are capable and prepared to move in this way when necessary. It would seem likely, therefore, that their ancestors were also capable of the same but what actual evidence is there in the fossil record that this was the case?
Firstly it should be considered if the A. afarensis morphology has already been adequately explained in terms of its locomotor repertoire by existing models.
This will be tackled in three parts. In the first, the debate about the general locomotor repertoire of A. afarensis is discussed. In the second the attempts to relate her peculiar pelvic morphology to its potential functionality, and specifically her gait, are reviewed. Finally the third discusses the possibility that if A. afarensis did wade bipedally perhaps they had a way of doing so that was different to extant hominoids today.
3.1. In which ways did A. afarensis move: two modes
or three?
Starting with the basics, the question must be asked: Was Lucy arboreal, terrestrial, a bit of both or what?
The debate thus far about the way A. afarensis moved (e.g. as summarised
by Stern 2001) has been primarily focused on how arboreal she was and how
human-like her undoubted bipedality manifested itself. The discussion seems to
attempt to place Lucy on a linear scale with totally erect human-like, bipedality
at one end and a totally arboreal climbing repertoire at the other. This
essentially ‘bi-modal’ locomotory repertoire made
sense because it naturally fitted the two substrates she was assumed to have
moved in. She walked on the ground or climbed in the trees, the question was simply:
how much in each?
Recently however, evidence of another mode to her locomotory repertoire may have been found that might complicate this picture. Richmond & Strait (2000) found notches on distal radii that were analogous to similar structures found in chimpanzees and gorillas associated with knuckle-walking. Their findings suggest that “bipedal hominids evolved from a knuckle-walking ancestor that was already terrestrial” (p 382).
They conclude that “Pre-bipedal locomotion is probably best characterised as a repertoire of terrestrial knuckle-walking, arboreal climbing and occasional suspensory activities, not unlike those observed in chimpanzees today”.
In the same journal Collard & Aiello (2000) review the finding and discuss the dilemma posed by it. On the one hand it could be argued that the knuckle-walking traits are “non-functional retentions from the common ancestor of hominoids and African apes,” “The alternative idea” they reason “that A. afarensis combined knuckle-walking, bipedalism and climbing - is somewhat counterintuitive, because it implies the use of two entirely different modes of terrestrial locomotion.”
The issue of phylogeny is fundamental to this particular debate. It is possible that A. afarensis evolved from a knuckle walking ancestor, even though it no longer did so itself, in which case it could be argued that the traits were just “evolutionary baggage” from the past. However that argument might be seen as a little convenient to some. The same paper found that A. africanus, a putative descendant of A. afarensis, had lost those traits. If they were phylogenetically related and if the knuckle-walking traits were evolutionary baggage in A. afarensis, why did they then disappear in A. africanus? Baggage is baggage.
Furthermore, recent research has indicated that inferring phylogeny from skeletal structures is more unreliable than had been considered in the past (Gibbs, Collard & Wood 2000), adding further weight to the argument that the traits were functional, and others have highlighted the plasticity of bone during lifetimes. Oxnard (1983: p97) said “There is now every good reason for believing that most biological materials, especially bone, must be considered as anisotropic, poroelastic, materials.”
To conclude: The most parsimonious explanation for the knuckle-walking traits of A. afarensis has to be, simply, that A. afarensis was a knuckle walker.
This is indeed counterintuitive if one assumes that A. afarensis moved only in the terrestrial and arboreal substrates. However if one considers that its bipedality was primarily for moving in water, then the dilemma disappears. Seen this way A. afarensis had three modes of locomotion for three different substrates: climbing and brachiating for the trees; knuckle-walking on solid ground and wading in water. It is claimed here that a clearer explanation has not, thus far, been suggested.
3.2 Predicting Lucy’s bipedal gait
Whether A. afarensis had two or three modes of locomotion nobody doubts that they were, at least in some way, bipedal.
The
Not surprisingly too, there have been many excellent reviews of A. afarensis morphology. The reader is urged to refer to Aeillo & Dean (1999:Chs.14,19,20-21), which compares human, great ape and australopithecine bipedal morphology in a systematic and clear way.
Several elements of the post-cranial skeleton have been recognised as indicating her bipedality although, for brevity, only those concerned with the pelvis and femur (and not for instance vertebrae or feet) will be considered here.
Possible
functional significance of the australopith femuro-pelvic complex
One of the most remarkable aspects of the A. afarensis pelvis is its pronounced iliac crest. A thorough morphometric study (Marchal 1999) comparing hominid pelvis morphologies concluded this was the clearest difference between them, noting that it was “very different from the human condition.” (p355).
This and other differences are reviewed by
Aiello & Dean (1999:p451-453) where it was further observed that the A. afarensis pelvis further differs from
the human condition “in their extreme width” not only at the iliac crests and
at the acetabulae but also with a very platypelloid (flattened dorso-ventrally)
pelvic inlet.
It has been difficult to explain convincing functional reasons for these features.
Aeillo & Dean (p 451) suggest “there are two current interpretations” and then go on to describe the morphological features that the proponents of human-like upright walking and the so-called “bent-hip, bent-knee gait” (from now on referred to as ‘BHBK’) use to back their arguments.
BHBK
versus Fully Upright versus Wading
The first specimens (a piece of proximal
tibia and a distal femur) to be retrieved from Hadar in
Lovejoy added further weight to this view
later when AL 288-1 was analysed a couple of years later, arguing that the wide
lateral flare of the pelvis indicated that they were used as abductors of the
pelvis on an extended thigh, as with humans during walking. This view was the most
logical interpretation especially after recent work (e.g. Patriaco
1981) had demonstrated, with myoelectric plots, the
importance of the muscles involved with abduction in the human bipedal gait.
Lovejoy consequently promoted an essentially human-like gait for A. afarensis even though its femuro-pelvic complex was quite different, morphologically.
Later, however, Stern & Susman (1983) stressed that other traits, such as curved phalanges, indicated a strong adaptation to arborealism. They suggested therefore that A. afarensis could not have been fully adapted to the kind of bipedalism we understand and suggested that instead it exhibited a more chimp-like, intermediate form, BHBK.
Further evidence in favour of BHBK was found by workers such as Tardieu (1991), Berge (1994) and Abitbol (1994).
After studying displacements of centre of gravity. Tardieu proposed a “rope-walker” gait model for chimpanzees and early bipeds suggesting that their low centre of gravity meant that their “bipedal dynamic equilibrium was still precarious.”
Berge performed biomechanical studies on A. afarensis reconstructions based on two different (one ape-like and one human-like) gluteus muscle arrangements. She concluded (p271) “The present results lead to the conclusion that the bipedalism of Australopithecus must have differed from that of Homo. Not only did Australopithecus have less ability to maintain hip and knee extension during the walk, but also probably moved the pelvis and lower limb differently.” She characterised it as a “sort of waddling gait” with large rotatory movements of the pelvis and shoulders around the vertebral column.
And Abitbol
(1994) cast serious doubt on the notion that A. afarensis walked in a fully-upright manner by challenging the
way that her hip joints have been reconstructed in models to date, in
particular the assumption that the hip joints “are aligned in a vertical plane”
(p211). He concluded (p225) “one may justifiably wonder if Lucy’s erect posture
might not reflect some characteristics of nonhuman-like bipedal posture and
locomotion.”
Those in favour of a fully-upright mode were bolstered recently however when the BHBK hypothesis was countered by Crompton et al. (1998). Through predictive dynamic computer modelling, they were able to suggest that BHBK would have been energetically very inefficient and would also have generated an excessive heat load to the individual. They conclude (1998 p 71) “It is thus difficult to envisage a selective pressure sufficient to bring about the undoubted bipedal adaptations of this species, if it habitually utilised ‘bent-hip-bent-knee’ bipedal walking.”
Stern (1999:p567) replied to this by suggesting that his colleges “never doubted that BHBK walking is more energetically costly” but that (p569) “the extra cost would have been small.” His last words on the matter were (p569) “It was only when life on the ground overwhelmed in selective importance any use of trees for feeding and escape, that the human ancestor was free to evolve the highly efficient mode of bipedalism with which we are personally familiar.”
The debate rages on today with no prospect of consensus in sight. A salvo from the trees, followed by a retort from the ground. Perhaps peace may be found by questioning their common assumption that the lifestyle of A. afarensis was not influenced by water.
Three positions on the bi-modal locomotor axis for A. afarensis are considered.
Terrestrial
Human-Like Model
In the paper by Crompton et al. (1998), BHBK was suggested to have been energetically less efficient but this was based upon the unspoken assumption that her bipedality was purely terrestrial. Therefore no computer model was devised to test how BHBK would have performed in water. If they had, they might have come to a very different conclusion.
It would seem logical that, whilst wading, a significant amount of Lucy’s body weight would have been supported by inherent hydrostatic buoyancy, reducing the assumed (terrestrial) costs of maintaining that posture. This buoyancy could also explain the characteristically small, relative to body size, femoral head (Aiello & Dean 1999:p470-1) found in australopithecines which is normally interpreted as being correlated with the stress load resulting from body mass. Those volunteers who practiced BHBK for the waddling races in the swimming pool found it quite a comfortable, if unnatural, mode to adopt.
Their other main objection to BHBK, that it would have resulted in excessive heat generation, could also be easily countered if one assumed its bipedality was due to wading, simply because of the significant cooling effect of water.
Thus if A. afarensis was at least in part a wading ape Crompton et al’s published specific objections to the BHBK gait could be withdrawn.
BHBK
Model
Ironically Berge (1994) used the same terrestrial assumption in arrivi