Download Understanding selection for long necks in different taxa

Biol. Rev. (2012), 87, pp. 616–630.
doi: 10.1111/j.1469-185X.2011.00212.x
616
Understanding selection for long necks
in different taxa
David M. Wilkinson1,∗ and Graeme D. Ruxton2
1 School
2
of Natural Science and Psychology, Liverpool John Moores University, Byrom Street, Liverpool, L3 3AF, UK
College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK
ABSTRACT
There has been recent discussion about the evolutionary pressures underlying the long necks of extant giraffes and
extinct sauropod dinosaurs. Here we summarise these debates and place them in a wider taxonomic context. We
consider the evolution of long necks across a wide range of (both living and extinct) taxa and ask whether there has
been a common selective factor or whether each case has a separate explanation. We conclude that in most cases
long necks can be explained in terms of foraging requirements, and that alternative explanations in terms of sexual
selection, thermoregulation and predation pressure are not as well supported. Specifically, in giraffe, tortoises, and
perhaps sauropods there is likely to have been selection for high browsing. It the last case there may also have been
selection for reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing.
For camels, wading birds and ratites, original selection was likely for increased leg length, with correlated selection for
a longer neck to allow feeding and drinking at or near substrate level. For fish-eating long-necked birds and plesiosaurs
a small head at the end of a long neck allows fast acceleration of the mouth to allow capture of elusive prey. A swan’s
long neck allows access to benthic vegetation, for vultures the long neck allows reaching deep into a carcass. Geese may
be an unusual case where anti-predator vigilance is important, but so may be energetically efficient low browsing. The
one group for which we feel unable to draw firm conclusions are the pterosaurs, this is in keeping with the current
uncertainty about the biology of this group. Despite foraging emerging as a dominant theme in selection for long necks,
for almost every taxonomic group we have identified useful empirical work that would increase understanding of the
selective costs and benefits of a long neck.
Key words: energetics, feeding, giraffe, neck, okapi, plesiosaur, pterosaur, Quetzalcoatlus, ratites, sauropod.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
II. The giraffe—the archetypal long-necked extant animal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Giraffe—a brief evolutionary history . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Potential explanations for the extremely long-neck of the giraffe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Are we wise to focus on the neck by itself? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) So why do giraffes have long necks? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
III. Other mammals and reptiles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IV. Long-necked birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) The Struthioniformes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Fish-eating long-necked birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Long-legged wading birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Geese . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Swans . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(6) Vultures . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(7) Summary: long-necked birds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
* Address for correspondence (E-mail: [email protected]).
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
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Evolution of long necks
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V. Sauropods—the archetypal long-necked extinct group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(1) Sauropods—the archetypal long-necked extinct animal . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(2) Sauropod necks as snorkels—aquatic explanations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(3) Sauropod long-necks—feeding explanations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(4) Long necks and sexual selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(5) Long necks and thermoregulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
(6) So why did sauropods have long-necks? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VI. Plesiosaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VII. Pterosaurs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
VIII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
IX. Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
X. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
‘It is interesting to observe. . . the peculiar shape of the
giraffe. . . its neck is lengthened to such a degree that the
giraffe, without standing up on its hind-legs, attains a height
of six meters’ (Lamarck, 1809; translation from Gould, 1998,
p. 305).
I. INTRODUCTION
The giraffe Giraffa camelopardis Linnaeus has been subject
of academic and popular comment in western culture for
over 2000 years, with its long neck being its most striking
and characteristic feature (Gould, 1998). It most famously
appears in biology textbooks as an example of Lamarck’s
evolutionary ideas—although he actually wrote only one
paragraph on giraffes, which is the source of our opening
quotation. Amongst other errors he overestimates its height,
which is closer to 5 m than the 6 m he cites (Kingdon, 2004).
However giraffes are not the only animals with unusually
long necks, there are others including many birds and extinct
groups such as the sauropod dinosaurs and plesiosaurs.
In all these taxa the question has been posed as to why
they have such strikingly long necks. This question has
implications well beyond the understanding of an interesting
aspect of natural history. It provides a useful way to
address more general questions about selection pressures
on morphology, as a long neck must impose significant
costs to an animal—for example creating a dead space that
makes re-breathing de-oxygenated air more likely and so
potentially reducing the efficiency of respiration. Focussing
on the neck could be considered a very atomistic (sensu
Gould, 1977, p. 393) way to address questions of selection
pressures and morphology. Ideally a structure—such as
a long neck—should be considered in the context of the
whole animal’s body. However, even philosophers with grave
reservations about a reductive approach in science admit that
such an approach—initially focusing on understanding parts
rather than complicated wholes - can be very powerful when
applied to an appropriate question (e.g. Midgley, 2001). In
constraining our approach to questions about the benefits and
costs of long necks, while keeping the whole animal context in
mind, we believe we define the problem in a way that should
allow progress to be made and testable ideas developed.
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In addition to the general theoretical interest in how the
benefits and costs of a long neck apply in any given species,
we believe the time is right for such a review as in recent
decades there have been several high-profile papers arguing
for reinterpreting the long necks of giraffes and sauropods
as sexually selected traits rather than feeding adaptations
(Simmons & Scheepers, 1996; Senter, 2007). These radical
reinterpretations have been challenged and we discuss the
relative merits of these different arguments in our review.
In attempting to understand the reasons behind the long
necks seen in a diverse variety of species, we consider that
a comparative approach is likely to be informative, as it is a
method that is ‘peculiarly suitable for the study of diversity’
(Mayr, 1982, p. 31).
In this review we first discuss extant long-necked animals—starting with a detailed discussion of the giraffe
as the archetypal long-necked animal—before discussing
extinct taxa, such as sauropods and plesiosaurs. We give
particular emphasis to giraffes (as the most extreme extant
long-necked vertebrate) and the sauropods (as the most
extreme long-necked animals known). However, where previous considerations of selective pressures towards a long
neck have focused on a single taxon, here we explore the
extent to which long necks across taxa can be explained
by a relatively small number of selection pressures or if
each case requires its own unique explanation. Throughout we attempt to draw attention to aspects that we
think would benefit from more empirical and/or theoretical
attention.
II. THE GIRAFFE—THE ARCHETYPAL
LONG-NECKED EXTANT ANIMAL
As the most dramatic long-necked animal of the extant fauna,
the giraffe has probably attracted more scientific attention
than any other long-necked taxon. Before describing and
evaluating the various theories that have been proposed
to explain giraffe neck evolution we briefly summarise
what is known of giraffe evolutionary history. Clearly the
timing and ecological context of the evolution of the
giraffe’s long neck could potentially offer insights into its
function.
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
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(1) Giraffe—a brief evolutionary history
The modern giraffe Giraffa camelopardalis has traditionally
been treated as a single species—albeit with significant
regional variation in coat pattern leading to around nine subspecies being described (Kingdon, 2004; Harris, Solounias
& Gerrraads, 2010). However because of a wide variety of
different coat patterns in single populations not all authors
have been enthusiastic about the utility of these various
subspecies (e.g. Matthews, 1971). Recent molecular analyses
(Brown et al., 2007) provide evidence for a long history of
reproductive isolation for many of these sub-species and
suggest that at least some of them could be raised to the
status of full species. However, these forms are all capable
of interbreeding and are treated as sub-species of Giraffa
camelopardalis in the recently published second volume of
Handbook of Mammals of the World’ (Skinner & Mitchell, 2011).
The Giraffidae currently contains only one other extant
species, the okapi Okapia johnstoni Sclater (Fig. 1), which is
restricted to African rainforest habitats (Skinner & Mitchell,
2011). The okapi is considered to have body proportions
similar to many ancestral members of the Giraffidae (Turner
& Antón, 2004), with the characteristic long-necked and longlegged shape of the giraffe being a more recent development.
The okapi has a very sparse fossil record, presumably because
its favoured habitats are not conducive to the preservation of
fossils (Harris et al., 2010).
Although the Giraffidae is currently restricted to Africa
the group had a much wider distribution in the past; there
is a diverse collection of fossil giraffid species known from
eastern Europe around 9 million years ago (Agustí & Antón,
Fig. 1. A captive okapi Okapia johnstoni. Short-necked by the
standards of the giraffe Giraffa camelopardis but long-necked
by the standards of many other mammals. The okapi is
usually considered to exhibit body proportions similar to
typical ancestral members of the Giraffidae (Turner & Antón,
2004), illustrating an early tendency towards the evolution of
long necks in the Giraffidae. When first discovered, several
scientists interpreted it as a ‘degenerate giraffe’ but the
current interpretation of a more ‘primitive’ giraffid was quickly
established in a series of anatomical studies (Colbert, 1938).
David M. Wilkinson and Graeme D. Ruxton
2002). Indeed the genus Giraffa appears to have originated
in Asia and entered Africa between seven and five million
years ago, and so is a relatively recent addition to the
African fauna (Harris et al., 2010; Mitchell & Skinner,
2003; Turner & Antón, 2004). Mitchell & Skinner (2003)
and Harris et al. (2010) provided extensive reviews of the
relevant fossil record and were able to draw some tentative
conclusions about giraffe evolutionary history; suggesting
that that ‘Throughout the giraffid fossil record there is clear
evidence for progressive limb and neck elongation’ (Mitchell
& Skinner, 2003). Climate-driven vegetation changes from
about eight million years ago appear to have been the
main driver for the evolution of the classic giraffe body
shape—due to large areas of closed forest changing to
savannah/woodland/shrub biomes.
The modern giraffe G. camelopardalis appears in the African
fossil record approximately one million years ago (Mitchell
& Skinner, 2003). Over the preceding five million years
there were several species of giraffe, some smaller than the
extant species but with effectively modern body proportions,
although the details (both the exact dating of some fossils and
the validity of many of the suggested species) are uncertain
(Harris et al., 2010; Mitchell & Skinner, 2003). In addition
there were other giraffids that were in Africa prior to the
arrival of the long-necked variety. In particular Sivatherium, a
large robust giraffid with a relatively short neck, was widely
distributed in Africa when Giraffa arrived from Eurasia.
The various species of Sivatherium have been assumed to be
browsers or mixed feeders (Franz-Odendaal & Solounias,
2004) which later adapted to a grazing lifestyle, coexisting
with some of the species of ‘modern-looking’ giraffes—such
as G. jumae Leakey for several million years (Turner &
Antón, 2004). Stable isotope analysis now helps confirm that
most Sivatherium spp. and Girraffa spp. were mainly browsers
although some populations may have shown mixed grazing as
well as browsing (Harris et al., 2010). The modern giraffes followed an evolutionary path of becoming specialist browsers
of tall trees. Therefore giraffid evolutionary history appears
to show a tendency for longish necked animals—possibly
driven in part by the effects of climate change on vegetation—with the modern giraffe as an extreme version on this
trend which specializes on browsing trees. In addition the
fossils crucially show long necks and long legs evolving in
tandem.
As with sauropod dinosaurs (Sander & Clauss, 2008),
a long gracile neck requires a relatively small head. In
giraffes this appears to have been achieved by specializing in
carefully selecting nutritious foliage—so called ‘concentrate
selectors’ - rather than processing larger quantities of less
nutritious vegetation (Skinner & Chimimba, 2005). In selecting smaller shoots, the giraffe makes use of its long tongue
(Fig. 2A); a relatively light-weight solution which may help
to keep the weight of the head down. However the okapi
also has a long tongue used in a similar manner (Fig. 2B)
suggesting that while this adaptation may facilitate the evolution of a long neck it was not caused by the long-necked
condition.
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
Evolution of long necks
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Fig. 2. (A) A giraffe Giraffa camelopardis using its tongue in
feeding. ‘The finer shoots of trees and shrubs are pulled into
the mouth by curling the long tongue around them and are
held between the teeth in the lower jaw and the hard pad in
the upper. The leaves and other edible portions are stripped
off the twigs with a backwards pull of the head’ (Skinner &
Chimimba, 2005, p. 620). It is an obvious speculation that this
use of the tongue—and the associated loss of the upper incisors
and canines—may be weight-saving adaptations associated
with the evolution of the long neck. However, it is interesting
to note that a similar adaptation is seen in the okapi Okapia
johnstoni (B) which has a much shorter neck. So the long tongue
may pre-adapt the girraffids for evolving a long neck rather
than being an adaptation evolved in conjunction with the
long-neck. In addition to using the long tongue in feeding it
is also used in grooming. An okapi can lick all of its own
face during grooming—something impossible for many other
mammals (Skinner & Mitchell, 2011; D.M. Wilkinson, personal
observations).
(2) Potential explanations for the extremely
long-neck of the giraffe
The classic, and most obvious, explanation of why giraffes
have long necks is that it allows them to browse high in
the tree canopy. However a number of other explanations
are possible: such as sexual selection, increased vigilance,
thermoregulation, and the evolution of long necks as a
correlated response to selection for increasing leg length.
The most high-profile challenge to the classic ‘high-browse’
explanation comes from the sexual selection hypothesis of
Simmons & Scheepers (1996). Prior to their paper many
authors assumed that the ‘high-browse’ explanation was
obviously correct (e.g. Cott, 1975; Matthews, 1971), although
there were exceptions to this (e.g. Pincher, 1949; Brownlee,
1963). Indeed this ‘high-browse’ explanation dates back to
at least the start of the 19th Century (Gould, 1998).
Simmons & Scheepers (1996) argued against the highbrowse explanation and for a sexually selected one based on
a range of considerations. They found a lack of data from
the literature, and also from their own work in Namibia,
for giraffes making much use of their full height when
feeding, which they suggested cast doubt on the conventional
explanation. In favour of a sexual selection explanation,
they drew particular attention to the use of the neck in
male-male combat—a behaviour known as necking. This
is a spectacular behaviour, for example Cott (1975, p. 52)
described how ‘Rivals take up a position side by side, facing
in the same or opposite direction, lean against each other
with legs straddled apart, and use the head as a sledge
hammer’. Considerable force is involved, and Simmons &
Scheepers (1996) reviewed cases when one of the giraffes was
killed during the fight. Indeed Darwin (1871) described how
he had seen a hard plank of wood ‘deeply indented by a
single blow’ made by a captive animal. Presumably because
of this behaviour, male skulls are more robust than female
ones (Skinner & Chimimba, 2005). There is potentially
an important trade-off here for male giraffes, with sexual
selection increasing skull weight but the long neck selecting
for lighter skulls. Clearly this necking behaviour suggests the
neck is used in circumstances where sexual selection could
apply—the question is; was this the main selection pressure
that led to the long-necked adaptation or did the long neck
evolve for other reasons and then become co-opted to the role
in male-male aggression (an exaptation sensu Gould, 2002).
If a trait, such as giraffe neck length, is sexually selected
through mechanisms such as male competition one would
normally expect it to be much more pronounced in males
(Andersson, 1994) and to exhibit positive allometry (Gould,
1974; Green, 1992; Andersson, 1994), although there are
exceptions to both of these generalizations (Taylor et al.,
2011). A clear problem for the sexual selection explanation
for giraffe necks is that both males and females have long
necks, although Simmons & Scheepers (1996) present data
suggesting that male necks are larger than those of females.
In addition their data suggested that male giraffe necks
showed positive allometry (i.e. as giraffes get larger the neck
size increases at a greater rate than the rest of the body).
These results are certainly consistent with giraffe necks being
sexually selected. However, Mitchell, van Sittert & Skinner
(2009) failed to find any evidence for a difference in neck
sizes of male and female giraffes of the same body size and
demonstrated positive allometry in the necks of both male
and female giraffes. A key aspect of the study by Mitchell
et al. (2009) is that they measured neck length directly, while
Simmons & Scheepers (1996) inferred neck length from other
measurements which had originally been taken to investigate
different aspects of giraffe biology. So there appears to be no
convincing evidence for (or against) sexual selection in the
evolution of giraffe necks.
Simmons & Scheepers (1996) also claimed that there
was little evidence for substantial high browsing by giraffes.
This stimulated further research which has tended to
undermine this objection to the ‘high-browse’ theory (e.g.
Woolnough & du Toit, 2001; Cameron & du Toit, 2007). For
example exclosure studies in southern Africa have provided
experimental support for the idea that the ‘vertical elongation
of the giraffe body is an outcome of competition within
the browsing ungulate guild’ (Cameron & du Toit, 2007).
These studies provided strong circumstantial evidence for
competition for browse low on Acacia nigrescens trees which
giraffes could escape by accessing higher branches (Cameron
& du Toit, 2007). This question would benefit from additional
field studies and there is also the possibility of using captive
giraffes for studies of preferred height of feeding. However,
it is important to remember that high browsing could still
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
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provide an important selection pressure for a long neck, even
if such foraging happens only rarely: what is important is the
fitness value of high browsing. It may be that high browsing is
only exploited by giraffes when alternatives are not available,
but that the ability to exploit high foraging in such situations
has very high fitness value (avoiding starvation risk or at least
the need to travel long distances in search of food). Therefore
we would particularly welcome studies that explore whether
the occurrence of high browsing in giraffe can be linked to
ecological factors such as inter-specific competition for lower
browse, or dry season situations where food is generally
scarce.
One of the less widely discussed suggestions for the evolution of giraffe body shape is that it confers a thermoregulatory
advantage (Brownlee, 1963). The suggestion was that giraffe
body shape greatly increased surface area in relation to
body mass—so allowing greater heat loss—certainly they
are prone to hypothermia in captivity away from the tropics
(Skinner & Mitchell, 2011). However, there is an additional
way in which giraffe body shape could contribute to thermoregulation. By analogy with the ideas of Wheeler (1984)
on the evolution of upright stance in human evolution, a tall
‘vertical’ animal will have only a relatively small amount of
its body directly illuminated during the hottest part of the
day (when the sun is directly overhead) but have a large
surface area of its flanks raised into a potentially cooling
breeze above the boundary layer of reduced wind speeds
near to the ground surface. However the giraffe’s neck does
not appear to have the expected adaptations for a good
radiator—which should ideally be hairless and with a good
blood supply to the surface (as is the case with elephant
Loxodonta africanus Blumenbach ears). For example in the case
of human evolution, hair loss (and increased sweating rates)
has arguably increased our ability to shed heat (Wheeler,
1984; Ruxton & Wilkinson, 2011b). Work by du Toit &
Yetman (2005) suggests that giraffe make considerable use
of behavioural adaptations in combating high heat loads,
reducing their activity on hot days. Such behavioural adaptations are probably more important for thermoregulation
in the giraffe than its long neck.
As well as the potential thermoregulatory advantage,
Brownlee (1963) also suggested that the giraffe body plan was
an antipredator adaptation - the long neck aiding vigilance
and the large body size making it hard for a predator to
bring them down. Certainly adult giraffe suffer a low level
of predation. Studies in the Serengeti by Sinclair, Mduma &
Brashares (2003) found extremely low predation on adult
giraffes; although Owen-Smith & Mills (2008) reported
somewhat higher predation rates for the Kruger Park, in
South Africa, they were still low compared to many other
African ungulates. Predation rates on juveniles are higher,
however Cameron & du Toit (2005) found no evidence for
higher vigilance rates in mothers with calves—suggesting
that anti-predator vigilance is not a major reason for long
necks in giraffes. Giraffes use kicking with their front feet as a
defence against predators and have on several occasions been
recorded killing lions Panthera leo Linnaeus with a ‘single blow
David M. Wilkinson and Graeme D. Ruxton
of the front foot’ (Skinner & Chimimba, 2005). We are not
aware of any quantitative data that allow the identification of
the relative importance of vigilance versus physical defences
(such as kicking lions) in giraffe antipredator behaviour. In
both cases it is possible that the anti-predator advantages
of body shape could be secondary to other adaptations.
Indeed giraffe are so big that they would actually have a high
vantage point even if they had a shorter neck; suggesting
that size may be a more important anti-predator adaptation
than the vigilance advantages of height. However, fossils
provide circumstantial evidence that body size itself (as an
antipredator advantage) is not the primary reason for the
evolution of giraffe shape. In the last 4 million years there
have been several smaller species of giraffe in Africa—some
more similar in size to an eland Taurotragus oryx Pallas
(Mitchell & Skinner, 2003). Based on the ecology of the
modern Serengeti (e.g. Sinclair et al., 2003) animals this size
are likely to have suffered much higher predation levels. It
may also be relevant that most other African mammals that
avoid much adult predation because of their size have evolved
body bulk rather than height (e.g. elephant Loxodonta africana,
white rhinoceros Ceratotherium simum Burchell, African buffalo
Syncerus caffer Sparrman); the giraffes appears to be an
unusually gracile approach to avoiding predation through
size. In this context the extinct, but robust, giraffid Sivatherium
looks like a more normal approach to evading predation
through body size. To summarise, at the moment there is a
not a strong logical or empirical reason for expecting that
anti-predatory vigilance has been an important selector for
long necks. However, we would especially welcome studies
that compare the responses of giraffe feeding at different
heights to a standardised ‘‘threat’’ such as the approach of a
vehicle for populations that are not habituated to vehicles. As
regards natural predators, studies of the vigilance behaviour
of female giraffe with young offspring (which are much
more vulnerable to predators than adults) are particularly
instructive and more work like that of Cameron & du Toit
(2005) would be welcome.
(3) Are we wise to focus on the neck by itself?
As noted in Section I, most discussions of the striking body
shape of the giraffe have tended to focus on its long neck
and there are obvious problems in considering the neck
without taking the rest of the body into account. Could
the evolution of the long neck have been mainly driven by
selection pressures on other aspects of giraffe anatomy? For
example Pincher (1949) suggested that the long neck was
an adaptation to the lengthening of the legs—required if
a long-legged giraffe was still to be able to drink without
kneeling. [Note that several authors attribute this idea to
Colbert (1938); however we can find no explicit statement
of this hypothesis in Colbert’s (1938) okapi paper]. Certainly
most giraffe populations habitually drink—although a few
appear to survive without drinking, presumably relying on
water in their plant food (Skinner & Chimimba, 2005)—so
access to water may be important.
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Evolution of long necks
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If there is selection for height (either for ‘high browse’ or
vigilance) then leg length is likely to be as important as neck
length in achieving this height and the two should coevolve.
Indeed, one of the key insights from studies of fossil girrafids
is that the fossils show long necks and long legs evolving
in tandem. In addition there are other factors which could
affect leg length—such as running speed—which could
potentially have secondary effects on neck length. Against
this latter hypothesis is the fact that giraffes appear to be
comparatively slow runners with an estimated gallop speed
of 56 km h−1 , which as Skinner & Chimimba (2005, p. 619)
comment is ‘far less than some other species attain and
which is perhaps surprising in view of the tremendous length
of the legs’. This perhaps suggests that running speed was
not a primary selection factor for leg length. However, the
key point is that neck length could in principle be largely
driven by selection for leg length—a point we return to in
considering several long necked birds below. However in the
case of the giraffe it is not obvious what selection pressures
would produce the long legs. We note that although a longlegged short-necked animal could drink by crouching this is
not a generally observed phenomenon among animals. The
likely reason for this is that in many environments places with
water are also places of heightened predation risk (if only
because predators are attracted by their need to drink too)
and an animal down on its knees would not be able to make
a sufficiently quick escape from an onrushing predator. The
classic example of a large animal with longer legs than neck
is the elephant, and this has had to utilise an extraordinary
method of drinking—namely its trunk. Indeed the trunk is
an interesting adaptation that gives an animal the reach of
a long neck while allowing it to maintain a heaver skull and
teeth.
(4) So why do giraffes have long necks?
Although several authors (e.g. Pincher, 1949; Simmons
& Scheepers, 1996) have questioned the most common
explanation for giraffe long necks—namely the highbrowse hypothesis—this still seems one of the most likely
explanations and there is now some limited field evidence
to suggest that giraffes do benefit from their height in
competition for food (Cameron & du Toit, 2007). However
further experimental data would be welcome. We agree with
Pincher (1949) that it is important to consider neck length
in the context of leg length and the two are likely to have
co-evolved; a long-legged giraffe would struggle to drink
without a long neck. In addition a combination of long legs
and neck appears to be a good way of achieving increased
height.
It is difficult to rule out fully other suggested hypothesis.
However because of the lack of sexual dimorphism the
sexually selected hypothesis looks unlikely. It is much more
plausible that long necks evolved for other reasons and
have been co-opted for male/male aggression. Advantages
to vigilance cannot be ruled out—although the fossil record
suggests that size by itself as an anti-predator adaptation is
unlikely to be the reason for the evolution of long legs and
necks. We also consider thermoregulation unlikely to be the
main selection pressure for giraffe height. Of course several
of these potential advantages may have contributed to the
evolution of long legs and neck, but on current knowledge
we consider the high-browse explanation likely to be the
principal selection pressure for the evolution of giraffe height
(achieved by increasing both leg and neck length together).
III. OTHER MAMMALS AND REPTILES
Here we briefly review the biology of several other longnecked extant mammals and reptiles. For example several
African gazelleine antelopes have rather long necks; such as
gerenuk Litocranius walleri (Brooke), dibatag Ammodorcas clarkei
Thomas, and dama gazelle Gazella dama Pallas. All of these
are mainly—or exclusively—browsers (Kingdon, 2004) and
so the long neck is plausibly an adaptation for reaching
higher foliage. Indeed the gerenuk, a specialist browser
(Leuthold, 1978) ‘habitually rises on its hindlegs to reach a
zone over 2 m high’ while feeding (Kingdon, 2004, p. 242)
so illustrating the importance of reaching high browse for
this species. Camels and llamas (Camelidae) have relatively
long necks—they typically feed by either grazing or a mix of
grazing and browsing (MacDonald, 2001; Matthews, 1971)
making it less likely that feeding is the primary selection
factor for a long neck. However they are long-legged fastmoving animals suggesting that this may be a case where
a long neck is primarily selected for by long legs. That is,
the neck allows a long-legged animal to reach the ground to
graze and drink, as discussed for the giraffe above and the
ostrich (see Section IV.1).
In extant reptiles a long neck for high browsing seems
very likely for many tortoise species because they often live
in relatively arid places where competition for vegetation
can be high, and because their heavy shell makes rearing up
on their hind legs impractical; in addition the need to tuck
things away in a shell means that a single long neck is more
attractive—in terms of ease of packing—than four long legs.
For example Taylor et al. (2011) illustrate a Galápagos giant
tortoise Geochelone nigra Quoy and Gaimond using its neck at
full stretch to reach high browse. They also point out that
these tortoises can use their necks in dominance displays.
So as with the giraffe a long neck can serve more than one
function. However, we feel that a high-browse explanation is
likely to be the primary adaptation with the neck then subject
to sexual selection—although in this case we are unaware of
relevant data to support our tentative conclusion.
IV. LONG-NECKED BIRDS
Birds are potentially an important group in discussing the
evolution of long necks because there is a large diversity of
long-necked types: from the ostrich Struthio camelus, to longnecked fish-eating birds, geese, flamingos, storks, cranes
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and vultures. Here we review some of the main types of
long-necked birds and the potential explanations for why
they have evolved such necks. Rather than trying to be
comprehensive we focus on several taxa that illustrate a
range of potential long-neck adaptations.
(1) The Struthioniformes
The classic examples of long-necked birds are the
‘ratites’ (Struthioniformes)—especially the ostrich, along
with the two rheas [Rhea americana Linnaeus and Pterocnemia
pennata (d’Orbigny)] and the emu Dromaius novaehollandiae
(Latham)—although the three species of Cassowary Casuarius
spp. are also relatively long necked. In addition a range of
large island-living ratites became extinct in the recent past,
in both New Zealand and on Madagascar (Benton, 2005).
These are of interest as they occurred on islands without
any large mammalian predators, so apparently ruling out
predation as the explanation for their large size, long necks
and long legs.
Folch (1992b) lists two main advantages of long neck to
the ostrich: (1) vigilance - looking over the top of grass for
predators; (2) access to food above ground level (although he
concedes that they do not often feed at full possible height).
In addition the highly flexible neck of the ostrich allows it
to more easily maintain the condition of its body feathers
via preening (Dzemski & Christian, 2007). Folch (1992b) also
mentions that the neck is bare of feathers (as are the legs)
but doesn’t discuss the possibility that this may give the neck
a role in thermoregulation. In addition Folch (1992b) points
out that the neck is used as a sexual signal by males. This
parallels suggestions of long necks evolving through sexual
selection for both giraffes (Simmons & Scheepers, 1996) and
sauropod dinosaurs (Senter, 2006). Dzemski & Christian
(2007) suggest that the ostrich’s long neck allows it to reach
a large amount of food with the minimum need to move
its body—an explanation we return to in the context of
sauropod dinosaurs in Section V.
While long necks are potentially good for vigilance, they
could also reveal the animal to predators - for example being
silhouetted against the sky in open country. Cott (1975,
p. 165) describes how ‘The female Ostrich, when attending
the nest by day, flattens her head and neck on the ground’.
This runs counter to the vigilance idea and may also often
run counter to what thermoregulation would suggest (a bare
neck held up into the breeze would presumably be useful
for cooling when sat on the nest in full sun). We note that
emus and rheas both have feathered necks; as such a role in
thermoregulation is only really relevant to the ostrich and is
not likely to be a general explanation of long necks in ‘ratites’.
Further, the relatively small surface area of the ostrich’s neck
does not make it a particularly effective radiator of excess
heat. In comparison, the wings can be flapped to provide
increased forced convection.
As with giraffes it is potentially relevant that the long neck
of ostriches, and other ratites, is associated with long legs. In
ostriches is it clear that these legs are an important adaptation
to living in open grasslands. Folch (1992b, p. 77) describes
David M. Wilkinson and Graeme D. Ruxton
how ‘its long, stout legs enable it to cover great distances
with the minimum of effort, when searching for its often
sparsely distributed food. They also represent formidable
weapons’. Ostriches are good runners and can reach speeds
of 70 km h−1 for short bursts (Folch, 1992b). Rheas and
emus are also birds of open plains—although emus can
live in a wider range of habitats—while the shorter necked
cassowaries (which share a common ancestor with emus) live
in rainforest (Folch, 1992a). This raises the question ‘is the
long neck in ostriches, and similar birds, largely a by-product
of selection for long legs? In this case the long neck would be
necessary to allow a long-legged terrestrial bird to reach the
ground for feeding and drinking. Ratitites, even the forestdwelling cassowaries—are commonly observed running,
often at high speeds (Folch, 1992a). Running speed appears
a more plausible primary selection pressure in the case of
ostriches than it does for the slower giraffe, so neck length
may well be determined by selection for leg length in this case.
(2) Fish-eating long-necked birds
Cormorants and shags (Phalacrocoracidae) and darters
(Anhingidae) both chase fish under water and have long
necks; cormorants and shags tend to be pursuit predators,
while darters are more stealth predators (Nelson, 2005).
Presumably their long necks are helpful in grabbing fish
underwater. Darters (e.g. Anhinga melonogaster Pennant) have
specific adaptations in their neck with modifications to the
8th and 9th vertebrae to form a ‘hinge’ allowing the head to
dart forward rapidly from an S-shaped position to grab fish
(Orta, 1992; Nelson, 2005). Cormorants and shags have a
similar, but not as well developed, adaptation to their neck
(Nelson, 2005). These morphological adaptations strongly
suggest that hunting is the main selection pressure for long
necks in these birds. However many birds which hunt fish
underwater (e.g. auks and penguins) have not evolved long
necks, illustrating a range of evolutionary solutions to this
problem. It is possible that the difference here is the distance
over which a predator usually chases its prey. In clear, surface
oceanic waters predators and prey can see each other from
a long distance away, and what is required to be a good
predator is a high cruising speed; the auks and especially the
penguins are adapted to this. However, in murkier waters
and waters with physical objects to hide within or behind
(shallow fresh waters and coastal waters) the predator will
see the prey only at very close range, and must be able
to accelerate its mouth rapidly to strike at the prey before
it disappears out of visual range again. This selects for a
long neck, because it is easier to accelerate a small head
than the whole body of the predator at such close-range. In
addition long necks potentially confer an advantage in nest
defence (from both neighbours and predators) by increasing
the effective pecking radius (Nelson, 2005).
(3) Long-legged wading birds
Flamingos (Phoenicopteridae) are a striking example of longnecked birds, indeed in these birds the ‘neck and legs are
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Evolution of long necks
623
longer, relative to body size, than in any other group of birds’
(del Hoyo, 1992, p. 508). As with giraffes these animals have
both long necks and long legs. For wading birds it seems
logical to assume that the long legs evolved to allow them
to wade in deeper water without breath-holding. However,
Hale (1980) pointed out that this is an assumption and that
the long legs of waders may have evolved for other reasons,
such as in helping them to become airborne or seeing over
tall vegetation. Wading could be a secondary adaptation
once long legs have developed for other reasons; while this is
logically correct we consider the most plausible explanation
for long legs in these birds is likely to be for wading in water
(since the other selection pressures would also apply to large
birds that have no connection with water—and no such
general trend in large birds is evident).
For wading birds it follows that if you make the legs longer
to wade in deeper water then you need a longer neck to
reach the water when it is not deep (or sediments at the
bottom when it is deep). Similar arguments apply to herons,
although here they are catching fish not just sieving water
as with flamingos. Other wading birds also have reasonably
long necks—such as black-winged stilts Himantopus himantopus
Linnaeus or Avocets Recurvirostra avosetta Linnaeus. In these
birds the necks are not as extended as those of the flamingos,
storks or herons, presumably because their long bills do part
of the job of reaching water/sediments, so reducing the need
for a very long neck. Indeed in the true waders (sub-order
Charadrii) there is usually a positive correlation between leg
length and bill length (Hale, 1980).
Cranes are another long-legged and long-necked
group—indeed some species are over 1.5 m tall (Archibald
& Meine, 1996). Cranes exhibit a wider range of feeding
behaviours, however the majority of extant species ‘display
adaptations to more aquatic conditions’ (Archibald & Meine,
1996, p. 61)—so we consider it likely that the long-necked
condition evolved for similar reasons to other ‘wading’ birds.
However, the long neck of cranes is used as part of the
mating display ‘dances’ for which many crane species are
famous (Archibald & Meine, 1996; Matthiessen, 2002); here
the most plausible scenario is that the long neck has become
the target of sexual selection, after originally having evolved
for feeding purposes.
of the body could also be considered ‘neck’ when it comes to
considering the reach.
There are at least two other plausible reasons for geese
having long necks; using them to reach underwater food
and/or in vigilance behaviour. Taylor et al. (2011) note that,
in addition to increasing their reach in grazing, the necks
of geese also allow them to ‘grub’ for aquatic vegetation.
However this behaviour is not as common as in swans.
The use of the long neck in vigilance behaviour by birds
in a goose flock is a standard example in animal behaviour
texts (e.g. Slater, 1999; Krause & Ruxton, 2002). In a
large flock of geese the long neck allows an individual bird
to look over the backs of its grazing companions (Fig. 3).
Vigilance may be particularly important in such large birds
that take a significant time to get airborne in response to
any threat. Therefore geese appear to be a good example of
a group where a long neck provides a range of advantages,
with no obvious primary adaptation for the long-necked
morphology.
(5) Swans
The most obvious reason for swans having long necks is
reaching food, in this case by up-ending to reach food
on the bottom of ponds etc. (Lack, 1974). Indeed John
Ray gave this explanation at the end of the 17th Century,
describing it as showing God’s wisdom in the design of swans
(Birkhead, 2008). Certainly this is an important feeding
mechanism in many swan populations. In a study of a
wintering flock of Whooper swans Cygnus cygnus (Linnaeus)
in Ireland, O’Donoghue & O’Halloran (1994) found that
feeding with head and neck submerged was an important
foraging activity (ranging from 8.9% to 48.2% of feeding
during the winter-long study), as was upending during the
early winter (up to 81.4%). This illustrates that the long neck
of swans can be very important in accessing submerged
food and also potentially grit needed for the gizzard.
(4) Geese
Geese typically obtain a large proportion of their food
through grazing (Carboneras, 1992; Cabot, 2009). This has
led to the suggestion that their long necks may function in
a similar way to that discussed in Section V for sauropod
dinosaurs—namely sweeping their heads and necks from
side to side to increase the amount of vegetation they can
reach without having to move their large bodies (Taylor
et al., 2011).We note however that in the case of geese this
effect is likely to be quite small as they weigh much less than
sauropods (reducing the gains from limiting their movements)
and their necks are relatively shorter. However, the position
of the feet in geese, close to the tail, means that the front part
Fig. 3. Grazing barnacle geese Branta leucopsis. Note the birds
with their heads raised in a vigilant posture surrounded by
grazing conspecifics and how the long necks give them a view
of their surroundings relatively unobscured by the grazing birds
with lowered heads.
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624
Feeding with head and neck submerged was also found
to be a very important feeding category for wintering mute
swans Cygnus olor (Gmelin) in Ireland (Keane & O’Halloran,
1992). As with geese there are the additional advantages
of increasing grazing efficiency and vigilance—however in
many swan species feeding by upending seems particularly
important.
(6) Vultures
Several vulture species—especially the Griffon vultures Gyps
spp.—have relatively long necks and one explanation for
this is that it may help in reaching into carcasses during
feeding. Indeed Gyps spp. ‘often thrust their heads and necks
deep into a carcass’ (Thiollay, 1994, p. 75). This seems
very plausible given that vultures (because of their high
vantage point) often arrive at a carcass before scavenging
mammals, but conspicuously lack the mammals’ ability to
break a carcass up. Thus such vultures are often required to
access the valuable parts of the carcass through the mouth
and anus, where there is soft tissue that they can break
through (Houston, 2001). These necks often have bare areas
of skin on them, which most plausibly functions to reduce
fouling during feeding but could also have a role in thermoregulation as the neck is well supplied with blood vessels
(Houston, 1985). Indeed recent modelling and experimental
work suggests that vulture necks could potentially function
in thermoregulation (Ward et al., 2008). However, vultures
have a low-energy lifestyle that avoids strenuous activity. This
suggests that thermoregulation is unlikely to be the principal
reason for long necks. However, as with other long-necked
animals, it is obviously possible that more than one selection pressure could have contributed to the evolution of this
condition.
(7) Summary: long-necked birds
The above discussion of long necks in birds illustrates that
there is no single adaptive explanation for long necks that
is likely to apply to all animals. For example swans have
long necks to facilitate taking food from the bottom of shallow water bodies while shags and darters use their necks
in grabbing fish underwater. However, for most of the bird
and mammal species discussed above feeding adaptations
appear to be the main explanation for long necks (although
the feeding methods differ among these species). The ostrich
and other ratites may be an exception to this with neck
length potentially responding to selection for longer legs for
reasons unconnected with a specific feeding advantage to
a long neck. However the occurrence of sub-fossil ratites
on predator-free islands at least suggests that a predation
threat is not required for long necks and legs to evolve;
again suggesting that feeding adaptations rather than running speed are possibly involved in explaining neck lengths
of these birds. In the case of the ostrich and some cranes
the long neck has also become incorporated into mating
displays.
David M. Wilkinson and Graeme D. Ruxton
V. SAUROPODS—THE ARCHETYPAL
LONG-NECKED EXTINCT GROUP
If the giraffe is the archetypal long-necked extant animal
then the most famous extinct examples must be the sauropod
dinosaurs, closely followed by the plesiosaurs.
(1) Sauropods—the archetypal long-necked extinct
animal
The sauropod dinosaurs included the largest terrestrial
animals ever to evolve (Alexander, 1998; Sander & Clauss,
2008; Sander et al., 2011). A long neck is characteristic
of these dinosaurs, although a few short-necked species
are known (Rauhut et al., 2005). Sauropods were an
extremely successful group, with around 120 genera currently
described, dominating many terrestrial ecosystems for over
100 million years (Sander & Clauss, 2008). A variety of
explanations have been suggested for their long necks. One
of the commonest of these is as a feeding adaptation—either
allowing them to reach high browse or a wider range of lowgrowing plants without having to move. However, as with
giraffes, a range of other possibilities have been suggested,
such as sexual selection or allowing them to wade in deep
water. As Sander & Clauss (2008) pointed out, sauropods
had very simple teeth and did not masticate their food—this
allowed them to have remarkably small heads for an animal
of their size, potentially important in allowing the evolution
of long necks. Indeed Charig (1979) memorably describes
the typical sauropod as having a ‘remarkably long neck’
combined with a ‘ridiculously small head’. For obvious
engineering reasons relatively small heads are a characteristic
of almost all long-necked animals.
(2) Sauropod necks as snorkels—aquatic
explanations
The classical reconstructed image of a sauropod shows it
standing in - often deep - water using its long-neck like
a snorkel to breathe while it wades (e.g. Fig. 4 and the
well-known illustrations by Zdenĕk Burian in Špinar, 1973).
Indeed the first published life reconstruction of a sauropod
(painted by Charles Knight in 1897) showed snorkelling
animals (Taylor, 2010). However by the 1970s sauropods
were being increasingly reconstructed as terrestrial and
rather giraffe-like (e.g. Charig, 1979; Desmond, 1975) and
by the mid-1980s there was a clear consensus that these
animals were capable of being fully terrestrial (Taylor, 2010).
This reassessment was part of a more general change in
the way many dinosaurs were viewed during the 1970s, as
more ‘energetic, active and capable animals’ (Gould, 1980,
p. 216). There are two main reasons why sauropods have
been reconstructed as standing in deep water, both of which
were falling out of favour by the 1970s; namely support
for their massive bulk and thermoregulation. If standing in
deep water was an important adaptation then clearly the
long neck could have evolved as a snorkel - however there
were concerns that water pressure may have prevented them
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Evolution of long necks
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Fig. 4. Brontosaurus (now called Apatosaurus) drawn by
L.R. Brightwell for Huxley & Wells et al. (1931) The Science
of life - a widely read popular encyclopaedic treatment of biology
in the late 1920s that achieved ‘massive sales’ over several
decades (Bowler, 2009). The original figure caption explained
that Brontosaurus ‘almost certainly lived in swamps and pools
browsing on lush aquatic vegetation’. Note the silhouette of a
modern dog for scale.
breathing (Charig, 1979). Water pressure acting to compress
the rib cage increases linearly with depth; this is why human
snorkels are generally shorter than 50 cm. Human divers
requiring to inhale at deeper depths utilise the increasedpressure gases of SCUBA to aid them in rib-cage expansion.
For a sauropod to use its long neck as a snorkel it would
have required strong muscles to aid chest expansion against
several metres of water pressure; there is no evidence for the
attachment of such muscles.
The reason that workers in the past have assumed that
sauropods used water as a buoyancy aid is the well-known
relationship between bone strength and animal size. The
ability of a bone to withstand compression forces is related
to its cross-sectional area (length2 ), while the animal’s weight
increases in proportion to its volume (length3 ). So an animal
three times as high (but otherwise geometrically identical
to the smaller version) would have limbs able to withstand
nine times the weight but would actually weigh 27 times
more (Maynard Smith, 1968). However, during the second
half of the 20th Century it became clear that sauropod leg
bones were strong enough to support estimated body weights
and also many fossil sauropod footprints were discovered
that did not seem to have been formed underwater. More
recently there has been a realisation that parts of the skeleton
were extensively pneumatised, as in modern birds, and this
has tended to reduce the estimates of body mass (Sander
et al., 2011). Because of these lines of evidence a sauropod
aquatic lifestyle has largely been abandoned by dinosaur
workers, ruling out one potential selection pressure for long
necks (Alexander, 1998). In general, bones break not from
axial compression but from bending moments. Elephants
generally avoid steep inclines and ground that is slippery,
uneven and/or friable (Moss, 2000) and this is generally seen
as behaviour that reduces the risk of such a large animal
falling. We think it likely that sauropods moved slowly and
with similar care, thus greatly reducing the potential loads
on their legs.
The alternative reason for visualising sauropods standing
in water is that such huge animals may have been at risk
of overheating—the extent of this problem will depend on
their basal metabolic rates (BMR); this is a controversial
area with the possibility of significant variations in BMR
during an organism’s lifespan (Sander & Clauss, 2008).
However, in many circumstances an animal standing in
water is likely to lose heat more quickly than one in the air
(Ruxton, 2001), so if overheating was a significant problem
for these animals some version of the snorkel explanation
cannot be completely ruled out. Note that unlike the
buoyancy support idea—which would require the animal
to be mainly restricted to water—the thermoregulatory
hypothesis only requires use of water when heat stressed, and
so is more compatible with the evidence for locomotion on
land seen in the dinosaur track-way data. Note further that
concerns about thermoregulatory problems associated with
large size in sauropods have reduced as estimates of their
likely metabolism have been revised downwards (Sander
et al., 2011).
(3) Sauropod long-necks—feeding explanations
The most common explanation for long necks in sauropods
is as a feeding adaptation. There are two widely discussed
explanations—high feeding in trees and allowing an animal
to reach a greater amount of lower growing vegetation
without the energetic costs of moving its large body weight
(Martin, 1987; Sander et al., 2011). Potentially a given animal
could have used both strategies, but for convenience we
discuss each in turn. More generally the key idea is that the
long neck allows sauropods to access ‘food other animals
could not’ both in tall trees and along river banks and lake
margins (Sander, Christian & Gee, 2009) and/or forage in a
more energy efficient manner (e.g. Christian, 2010; Ruxton
& Wilkinson, 2011a).
The possibility that sauropods fed high in trees has been
discussed since the late 19th Century (Desmond, 1975), however it appears to have been given relatively little emphasis
for the first half of the 20th Century because many workers
assumed these animals to be partially or wholly aquatic.
During the 1970s, with the switch to reconstructing these
dinosaurs as more terrestrial, giraffe-like reconstructions
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
626
became more common. For example Alexander (2006,
p. 1851) describes Brachiosaurus as being ‘generally (and plausibly) restored with its neck sloping steeply up, in a giraffe-like
posture.’ However, these giraffe-like reconstructions are controversial on several grounds. Firstly there are disagreements
over interpretation of fossil neck vertebrae and what they
suggest about the degree of neck flexibility (e.g. Stevens &
Parrish, 1999; Dzemski & Christian, 2007), with recent textbooks tending to be sceptical about the more extreme claims
of giraffe-like posture for many sauropods (e.g. Benton, 2005).
In addition some authors express extensive doubts about the
implications of long necks both because of the high blood
pressure required to get blood to a head several meters
above heart height (Seymour & Lillywhite, 2000), and also
the energetic and engineering implications of the postulated
very large hearts (Seymour, 2009a, b). Not all authors agree
that these arguments rule out giraffe-like behaviour (e.g.
Alexander, 2006; Christian, 2010; Sander et al., 2009), however the giraffe-like reconstructions appear to have lost some
popularity compared to the period from the late 1970s until
the late 1990s (Siegwarth, Smith & Redman, 2011).
What can be concluded with confidence about the plausibility of giraffe-like behaviour? In principle it would seem
straightforward to establish whether high blood pressure was
a serious constraint for a large giraffe-like sauropod. However, although calculating the pressure required in raising a
liquid to a given height requires only High School physics,
the biological implications of these calculations are more
complex and open to rival interpretations. In addition there
is much scope for ‘interpretation’ in attempts to rearticulate
a sauropod’s neck vertebrae to try to establish the degree
of flexibility. An alternative approach would be to identify
the type of plants being eaten (low-growing taxa versus trees).
However currently all past claims for fossilized sauropod gut
contents or coprolites are considered questionable (Sander
et al., 2011)—so this approach cannot currently settle the
matter. Recently Christian (2010) published simple models which suggest that from an energetic perspective high
browsing in trees would have been a favourable adaptation,
despite the increased costs in metabolic rate associated with
this posture, if the resources were spaced out and so being
able to reach more of one tree could offset the costs of moving
between trees. It is worth making two more points which are
not often discussed in the sauropod literature: (1) given that
African elephants Loxodonta africana can reach high foliage by
pushing over substantial trees, a long neck is not the only
available option for high browsing in an animal the size
of a large sauropod (50+ metric tonnes). Indeed systematic
tree felling by sauropods is an intriguing possibility, with
substantial ecological implications. However, we note that
the small mouth size of the sauropods would limit the rate at
which they could consume the vegetative parts of felled trees
(allowing smaller animals to share the fruits of its labours).
Tree felling is a difficult idea to test however, Siegwarth
et al. (2011) suggest that ‘Whether the sauropods felled trees
might be determined from micro-fractures or bone bruises on
their scapulae or sterna plates’. (2) Even with its head held
David M. Wilkinson and Graeme D. Ruxton
horizontal a Brachiosaurus would have been able to access
vegetation 6 m above the ground (higher than a modern
giraffe can reach!). So an upright neck is not essential for
feeding on relatively high tree foliage.
There is much less controversy about the practicality of
low browsing. In this case the difficulty is in identifying
the advantage of sauropod neck length in such situations.
This contrasts with the high-browsing explanation where the
physiological and anatomical practicalities are controversial
but the advantage of being able to access otherwise outof-reach foliage appears obvious. One possibility is that
the long neck allowed sauropods to reach plants growing
along lakes or river banks without having to stand on soft
ground—horsetails Equisetum spp. are often mentioned in
this context and assumed to be a potentially highly nutritious
food source (e.g. Hummel et al., 2008; Stevens & Parrish,
1999; Sander et al., 2011). However, modern horsetails have
a range of anti-herbivore adaptations - being extensively
impregnated with silica, containing alkaloids such as nicotine
and also containing thiaminase which breaks down the
vitamin thiamine. Indeed Mabberley (2008) speculates that
these may have all evolved as anti-dinosaur adaptations.
Beds of horsetails—and other species such as cycads which
also contain a range of toxins—may not have been as
biochemically accessible as some dinosaur workers assume.
Further, in the context of feeding along rivers and lakesides,
we might expect such large animals to be particularly cautious
about their footing on slippery substrata near to water (see
discussion in Section V.2 on risk of falling).
The other main possibility for low browsing is that the
long neck makes feeding more energetically efficient. A long
neck would allow a larger swathe of food to be exploited
without the animal having to expend energy on moving its
heavy body. A recent simple proof-of-concept model suggest
that the observed neck length of 9 m in some Brachiosaurus
(Giraffatitan according to some authors e.g. Taylor et al., 2011)
specimens would reduce the overall cost of foraging by 80%
compared to an individual with a neck just long enough to
reach the ground (Ruxton & Wilkinson, 2011a).
(4) Long necks and sexual selection
The idea that giraffe long necks might be sexually selected
(Simmons & Scheepers, 1996) prompted Senter (2007) to
suggest that sauropod necks may also have been sexually
selected. He argued that if necks are not raised in a giraffelike posture then there would be no obvious survival value
to long necks, but that growing them would incur significant
cost—therefore long necks have the requirements of a
sexually selected handicap (e.g. Zahavi & Zahavi, 1997).
He also provided some evidence that during sauropod
evolutionary history neck length did not scale allometrically
with body size—which Simmons & Scheepers (1996)
considered a sign of sexual selection. Recently Taylor et al.
(2011) provided a detailed discussion of these ideas that
suggested that the sexual selection hypothesis is unlikely.
They argued that a combination of use for high browse
and/or energetically efficient grazing means that Senter
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society
Evolution of long necks
627
(2006) overestimated the cost of long necks and that
his allometic calculations are suspect due to an overrepresentation of one group of sauropods (mamenchisaurids)
in his analysis. In addition Taylor et al. (2011) stressed the
lack of sexual dimorphism in sauropod necks (as discussed in
Section II for giraffes). We agree with this analysis and see
no strong evidence for sexual selection in sauropod necks.
However as with giraffes it is possible that long necks that
had evolved for feeding may on occasions have also taken on
a secondary role in sexual behaviour.
(5) Long necks and thermoregulation
Another potential advantage to long necks (and long tails) is
thermoregulation (Sander et al., 2011). These would increase
the surface area in relation to volume compared to a similarsized animal without a long neck or tail, so facilitating heat
loss. However long necks and tails would also potentially
increase direct solar heating of an animal. In this context
a vertically held neck (as sometimes reconstructed for
Brachiosaurs e.g. Sander & Clauss, 2008) would function
more efficiently for heat loss than horizontally held necks
(cf. Wheeler, 1984; Ruxton & Wilkinson, 2011b). Unless
most sauropods held their neck vertically this problem may
make it less probable that thermoregulation was the primary
adaptation for long necks. However, there is clearly scope
for more modelling in this area.
(6) So why did sauropods have long-necks?
The most plausible explanation for long necks in sauropods
appears to be as a feeding adaptation. However it is currently
unclear if this was mainly for high or low browse. We consider
it unlikely that the selection pressures were identical on all
sauropods and individuals of different species may have
experienced different selection pressures—and interactions
of selection pressures—for both low and high browsing
(Ruxton & Wilkinson, 2011a). We find the evidence of other
explanations for sauropod long necks (e.g. snorkelling, sexual
selection and thermal regulation) unconvincing and think
they are likely to have been, at best, minor long-neck selection
pressures—with feeding the main reason for long necks.
VI. PLESIOSAURS
Plesiosaurs share more than a long neck with sauropods; they
also have a body plan that is unknown in the current fauna.
As Fortey (2010, p. 160) wrote ‘it is perversely satisfying that
nature could concoct a combination in the Jurassic never
seen before nor after: a fish-eater longer than a man with
a long, often flexible neck.’ Indeed when the first plesiosaur
material was described in the early 19th Century there were
initially concerns that the fossils were a hoax—so strange
did they seem (Rudwick, 2008).
As with the case of sauropods, reconstructing the ecology of
such non-analogue vertebrates is challenging. We know they
had relatively small mouths and many species ate fish and
molluscs such as ammonites (Benton, 2005; Fortey, 2010) so these long-necked marine reptiles could be filling a similar
role to the long-necked fish-eating birds discussed in Section
IV.2. Some species appear to have been more specialised
with thin, evenly spaced teeth that may have been used for
straining small prey from the water, analogous to modern
crabeater seals Lobodon carcinophage Hombra and Jacquinot
catching crustaceans (Martill, Taylor & Duff, 1994). In
such a situation the long neck could facilitate a side-toside feeding movement as the animal swam through a group
of small crustaceans. In addition the stomach contents of
two Australian Plesiosaurs (elasmosaurids) mainly comprised
benthic invertebrates (McHenry et al., 2005). Clearly different
species used the long neck for feeding in different ways.
As with modern cormorants and darters, fish-eating
plesiosaurs probably did not take fish larger than would fit
in their gullet. By analogy with these birds we would expect
them to be essentially ambush predators—a mode of hunting
that would be easier in shallow water with reduced visibility
or obstacles to hide behind. Massare (1988) approached this
problem by using calculations of drag to estimate swimming
speed for Mesozoic marine reptiles. Her results suggested that
plesiosaurs would have had speeds intermediate between the
faster ichthyosaurs and the slower marine crocodiles and
mosasaurs. These rankings of swimming speeds seem to
be qualitatively sensible based on analogies with current
animals, however the exact mechanism of swimming in
plesiosaurs is still controversial (Benton, 2005). Consideration
of swimming speeds led Massare (1988) to suggest that
plesiosaurs were not pursuit predators but an ambush-style
hunting technique was more likely, especially for the longer
necked species; for example, attacking ‘prey from below
before being detected’ (Massare, 1988, p. 200). Another
possibility is that such big ectotherms could have held their
breath for long periods of time and so could have sat in
wait for prey at the bottom of deeper waters. But since they
appear to have been visual hunters they could not have seen
prey coming if they were at the bottom of waters any deeper
than 100–200 m.
Therefore we consider the most plausible explanation is
that a typical plesiosaur used their necks to allow rapid
acceleration of their heads in catching prey—in a similar
manner to modern cormorants, shags and darters. This is a
style of hunting relying more on surprise than on swimming
speed. One potential prediction from this is that there may
have been differences in the habitats used by plesiosaurs and
the faster swimming ichthyosaurs, which were more likely to
have been pursuit predators. However no clear difference is
seen in the fossil record with both taxa occurring as fossils in
the same sediments (e.g. Martill et al., 1994; Forrest & Oliver,
2003; O’Keefe et al., 2009). However as Martill et al. (1994)
pointed out there are difficulties in drawing firm conclusions
from such data as with modern large marine vertebrates (e.g.
Cetaceans) we know that oceanic forms sometimes come
into shallow water—both by both accident and design.
Plesiosaurs raise another interesting question: if long necks
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628
were so advantageous [plesiosaurs are found from the late
Triassic though the Jurassic and Cretaceous (Benton, 2005)]
why are there no long-necked whales or crocodilians? We
see no obvious answer to this question, except to appeal to
evolutionary constraints of the bauplan of these groups.
VII. PTEROSAURS
As with sauropods and plesiosaurs, the pterosaurs were
another long-necked group of Mesozoic vertebrates. Over
100 species have been described and are they considered
to have been predominantly small fish-eaters during the
Jurassic which diversified into a wider range of niches during
the Cretaceous (Benton, 2005). As with sauropods, pterosaurs
underwent a reinterpretation during the 1970s and 1980s as
active, highly proficient flyers, rather than ‘glorified, reptilian
gliders’ (Unwin, 1987).
Although the flight ability of pterosaurs has come to be
viewed as much better than previously thought, there is still
a widespread assumption that they ‘probably took off from
trees or cliffs, or jumped into the air after a short run’ (Benton, 2005, p. 229). Following from this is the common idea
that these animals caught fish from the surface water while
in flight. However if they were adapted to low-speed flight
(e.g. Palmer, 2011) they may have been able to take off from
the water surface and this potentially allows a much larger
range of feeding behaviour, as seen in extant long-necked fisheating birds: diving from the water surface as in cormorants or
plunge diving as in the (superficially pterosaur shaped) brown
pelican Pelecanus occidentalis Linnaeus (Nelson, 2005). Clearly
the question ‘could pterosaurs take off easily from the water
surface?’ is a key one for pterosaur biology—if the answer is
‘yes’ then many of the selection pressures that apply to modern fish-eating birds are likely to be relevant to pterosaurs. It
is interesting that the few modern birds that do feed on fish
caught in flight (Skimmers Rynchops spp.) only have a slightly
lengthened neck compared to related species, while many
surface-feeders and plunge-divers have much longer necks.
Some of the longest pterosaur necks, in proportion to
body size, are seen in the giant species with wingspans of over
(possibly well over) 10 m (Whitton, 2010). Many of these large
pterosaurs, such as Quetzalcoatlus, are more commonly found
in terrestrial sediments rather than the marine sediments
more typical for smaller pterosaurs (Whitton & Naish,
2008). The ecology of these animals has been reconstructed
as variously, ‘typical’ fishing pterosaurs (albeit very large
ones), carrion feeders or ground predators—with Whitton &
Naish (2008) preferring ground-hunting predators. Recently
Henderson (2010) argued that their reconstructed body mass
was such that they were probably secondarily flightless,
although most authors have assumed they could fly (reviewed
by Whitton, 2010). One obvious speculation about their
feeding ecology is that they could have been carrion
feeders—effectively Mesozoic vultures—specializing in the
bodies of large dinosaurs. This idea has the advantage of
helping to explain their huge size, as sauropods provided
David M. Wilkinson and Graeme D. Ruxton
a carrion source much larger than any available today.
Several reasons have been put forward as making carrion
feeding unlikely, namely the lack of a ‘hooked’ jaw tip
and the relative inflexibility of the neck compared to modern
vultures (Whitton & Naish, 2008). However we speculate that
the very long neck may have been important in reaching into
the centre of large sauropod carcasses and for aerodynamic
reasons this neck may have had to be reasonably stiff.
Certainly these objections seem to fall short of ruling out a
vulture-like life style—if they could fly. Flight would have
been crucial to the location of large carcasses which would
presumably have been rare and so the question of the flying
ability of these large pterosaurs remains crucial.
The fact that pterosaurs are so different from any extant
taxa currently makes any suggestions about their ecology
in general, and the selective advantages of long necks in
particular, very speculative. Indeed their oddness is illustrated
by the fact that they seem to the only long-necked group
that have managed to retain relatively large (and heavy?)
heads—this is especially true of larger pterosaurs such
as Quetzalcoatlus. However, it appears likely that the long
necks were involved with feeding—initially in catching fish
and later modified for a wider range of food sources. Our
main conclusion based on this brief review of pterosaur
necks is that their flying ability seems to be a key question
which is potentially solvable and which would greatly inform
speculations about other aspects of their biology (including
neck length). Two key questions are could they take off from a
water surface following diving for fish and could the very large
species fly - if not this would appear to conclusively rule out
carrion feeding, as finding carcasses would be energetically
too costly without flight (cf. Ruxton & Houston, 2004).
VIII. CONCLUSIONS
(1) In this review we considered long necks in a
wider taxonomic framework than any previous study. Our
motivation was to explore whether we can detect common
themes in selection pressures for long necks. We believe that
broadly almost all cases of long necks can be explained in
terms of foraging requirements, and alternative explanations
in terms of sexual selection, thermoregulation and predation
pressure are not as well supported empirically and/or
logically.
(2) In summary for giraffe, tortoises, and perhaps
sauropods there is likely to have been selection for high
browsing. In sauropods there may also have been selection for
reaching otherwise inaccessible aquatic plants or for increasing the energetic efficiency of low browsing. For camels,
wading birds and ratites, the original selection pressure was
probably for increased leg length, with correlated selection
for a longer neck to allow feeding and drinking at or near substrate level. For fish-eating long-necked birds and plesiosaurs
a small head at the end of a long neck allows fast acceleration
of the mouth to allow capture of elusive prey. A swan’s long
neck allows access to benthic vegetation, for vultures the long
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Evolution of long necks
629
neck allows reaching deep into a carcass. Geese may be an
unusual case where anti-predator vigilance is important, but
so may be energetically efficient low browsing.
(3) The one group for which we feel unable to draw firm
conclusions is the extinct flying pterosaurs, but this is in
keeping with the great current uncertainty and disagreement
about the fundamentals of ecology and physiology in this
group.
(4) Despite foraging emerging as a dominant theme in
selection for long necks, for almost every taxonomic group
we have identified useful empirical work that would increase
understanding of the selective costs and benefits of a long
neck. Thus we hope our work serves as a trigger for others
to investigate long necks—not just in the iconic giraffe and
sauropods, but also in the more easily overlooked (literally
and metaphorically) long-necked species.
IX. ACKNOWLEDGEMENTS
We thank Laura Bishop for discussion of fossil giraffes,
Adrian Lister for discussing elephant trunks and Johan du
Toit for many helpful suggestions on an earlier version of the
manuscript.
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(Received 26 August 2011; revised 20 November 2011; accepted 23 November 2011; published online 16 December 2011)
Biological Reviews 87 (2012) 616–630 © 2011 The Authors. Biological Reviews © 2011 Cambridge Philosophical Society