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The global trend in plant twining direction
Article · May 2007
DOI: 10.1111/j.1466-8238.2007.00326.x
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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2007) 16, 795–800
Blackwell Publishing Ltd
RESEARCH
PAPER
The global trend in plant twining
direction
Will Edwards1*, Angela T. Moles2,3 and Peter Franks1
1
School of Tropical Biology, James Cook
University, Cairns, QLD 4878, Australia,
2
Department of Biological Sciences, Macquarie
University, NSW 2109, Australia, 3School of
Biological Sciences, Victoria University of
Wellington, PO Box 600, Wellington,
New Zealand
ABSTRACT
Aim To examine, at a global scale, patterns in the direction in which climbing
plants twine. We tested three hypotheses: (1) that twining direction is determined
randomly; (2) that twining direction is determined by apices following the apparent
movement of the sun across the sky; and (3) that twining direction is determined
by the Coriolis effect.
Location Seventeen sites spanning nine countries, both hemispheres and 65° of
latitude.
Methods Twining direction was recorded for the first c. 100 stems encountered
along transects through natural vegetation at each site.
Results Ninety-two per cent of the 1485 twining stems we recorded grew in righthanded helices, i.e. they twined in an anticlockwise direction. This is significantly
(P < 0.001) different from random. The proportion of stems twining right-handedly
(anticlockwise) was independent of both latitude (P = 0.33) and hemisphere (P = 0.63).
These data are inconsistent with the idea that twining direction is determined by
either the relative passage of the sun through the celestial sphere or by the Coriolis
effect. Thus, we reject all three of our hypotheses.
*Correspondence: Will Edwards, School of
Tropical Biology, James Cook University,
Cairns, QLD 4878, Australia.
E-mail: will.edwards@jcu.edu.au
Main conclusions The predominance of right-handed helical growth in climbing
plants cannot be explained by hypotheses attempting to link plant growth behaviour
and global location. One alternative hypothesis for our findings is that the widespread
phenomenon of anticlockwise twining arises as a function of microtubule orientation
operating at a subcellular level.
Keywords
Chirality, climbing plants, Coriolis, lianes, microtubules, twining, vines.
Global patterns in biological systems give insight into the basic
forces that shape the biosphere. In the last few decades there has
been considerable effort directed at documenting broad-scale
biogeographical patterns, and developing ecological theories that
may explain them. Examples of broad-scale patterns for which
much information has been gathered include latitudinal gradients
in species diversity (MacArthur, 1972), geographical range sizes
(i.e. Rapoport’s rule; Stevens, 1989) and body masses of animal
species (i.e. Bergmann’s rule; Mayr, 1963). Here we examine the
broad-scale pattern of twining direction in climbing plants.
Anecdotal reports suggest a general tendency for twining plants
to ascend their hosts in right-handed helices, corresponding to
anti-clockwise motion in the direction of growth (Gardner, 1970;
Hashimoto, 2002). Unlike other broad-scale biological phenomena,
however, the pattern in plant twining direction has (apparently)
attracted little attention amongst scientists. Consequently, there
is very little published empirical evidence to support this claim,
and no data on the global extent of any such bias in naturally
occurring plant communities. Here, we present quantitative
evidence of the broad-scale pattern of twining direction in plants
growing under natural conditions from a wide range of locations
and habitats from around the world, and explore three potential
underlying determinants of twining direction in climbing plants.
Whether or not the reported predominance of right-handed
helices represents a general phenomenon or is a result of each
plant’s response to its environment will have important implications
© 2007 The Authors
Journal compilation © 2007 Blackwell Publishing Ltd
DOI: 10.1111/j.1466-8238.2007.00326.x
www.blackwellpublishing.com/geb
INTRODUCTION
795
W. Edwards et al.
for our understanding of the nature of twining and its underlying basis. For example, if twining direction is associated with the
environment in which a plant exists, then bias in twining direction must arise as a biological response to the physical conditions
associated with its location. If, on the other hand, directional bias
in twining is a global phenomenon, then alternative explanations
for twining direction (independent of individual plant responses)
will be needed.
Our approach was, first, to determine on a global scale whether
the incidence of left- versus right-handed twining direction in
the stems of climbing plants differs significantly from random
(hypothesis one), and secondly, if the incidence was found to be
non-random (biased towards one direction), to test, by inference,
two further hypotheses that could link twining bias with geographical location.
The factors that control twining or determine twining direction are largely unknown. Randomness might be expected if
climbing direction is set as a function of both circumnutation
and a mechanical (thigmotropic) response initiated when a twining plant first contacts its supporting host (hypothesis one)
(Darwin, 1876; Darwin & Darwin, 1880). Because the location of
twining plants with respect to their potential hosts is determined
by non-directional seed dispersal and deposition patterns, twining plants are equally likely to first encounter a host stem on their
left as on their right. Thus, under this hypothesis, the incidence
of left- and right-handed twining direction should be more or
less equal.
Alternatively, finding a broad-scale bias in twining direction
would indicate that twining direction is under the influence of
one or more controlling stimuli that operate at such a scale.
Under this scenario, we were to test the influence of two such
stimuli. The first is the potential influence of the position of the
sun and its passage across the sky (a heliotropism). If plant apices
track the sun’s passage, handedness may be related to the global
position of the site in which a plant occurs (hypothesis two). For
a twining plant growing in the Southern Hemisphere, the passage
of the sun across the sky will be to its north for most of the year
(for plants below the tropics this will be true for all times of the
year). The reverse situation occurs for the Northern Hemisphere.
If the apices of climbing plants track the apparent east–west
movement of the sun across the sky while they cross the sunny
faces of trees (the south side in the Northern Hemisphere and the
north side in the Southern Hemisphere), climbing plants would
twine in right-handed helices in the Southern Hemisphere and
left-handed helices in the Northern Hemisphere. This hypothesis
further predicts that the incidence of twining in a particular
direction should be an increasing function of latitude, since the
sun can appear to the north or the south of the plant at low latitudes (depending on the time of the year) but its northerly or
southerly orientation is fixed at latitudes outside of the tropics.
The second broad-scale influence we were to test for in the
event of unequal incidence of left- and right-handed twining was
the Coriolis effect. The Coriolis effect is a phenomenon related to
the decrease in velocity experienced at the Earth’s surface as a
function of increasing latitude that appears to deflect moving
objects to the right in the Northern Hemisphere and to the left in
796
the Southern Hemisphere (Gill, 1982; Persson, 1998). We would
test the hypothesis that the direction of circumnutation in apices
(the rhythmic, elliptical movement in leader stems) of twining
plants is influenced by the Coriolis effect (hypothesis three). This
hypothesis predicts a simple switch from right-handed twining
in the Northern Hemisphere to left-handed twining in the
Southern Hemisphere.
MATERIALS AND METHODS
Surveys of twining direction were carried out on transects in
natural vegetation at 17 sites from nine countries: Argentina,
Australia, China, Mexico, New Zealand, Panama, Peru, the
Republic of Congo and Zambia, across five continents (Figure 1
& Table 1). Eleven sites were in the Southern Hemisphere and
six sites were in the Northern Hemisphere. The sites spanned
approximately 65° of latitude [41°04′ S (Kaitoke, New Zealand)
to 24°47′ N (Linares, Mexico)]. The direction of twining was
recorded for the first c. 100 stems that were climbing upwards
and that made at least two loops around another stem we
encountered along transects through natural vegetation. The
number of stems recorded at each site is reported in Table 1. We
scored stems on the basis of whether their growth represented
left- or right-handed directions by following the major growth
axis from the ground upwards on host plants. Right-handed
growth is recognizable as an increase in height from left to right
around trees (viewed from any angle) (Hashimoto 2002) (Fig. 1,
legend). All surveys except those from Cairns and Cape Tribulation
(Australia) were carried out by A. T. Moles.
We first tested whether there was a significant bias in the frequency of twining direction within sites via a simple chi-square
goodness-of-fit test using expected frequencies based on equal
proportions of left- and right-handed twining. We then examined the relationship between the percentage of plants at each site
twining right-handedly and latitude via linear regression. We
tested for differences in the proportion of right-handed helices
between hemispheres via a t-test. Because percentage data do not
meet the assumptions of standard statistical tests, all data on
twining direction were logit-transformed (Dytham, 1999) before
analysis. We had to subtract 0.5% from each of the three sites in
which 100% of the sampled plants twined anticlockwise, in order
to perform the logit transformation.
RESULTS
We found overwhelming bias in the direction of twining. In total,
1372 (92.4%) of all 1485 plants we encountered produced righthanded helices and were climbing up their hosts in an anticlockwise direction (Table 1 & Fig. 1). This is significantly more than
expected if twining was equally likely to occur in both directions
(χ2 = 553.3, d.f. = 16, P < 0.0001). The mean per site percentage
of plants twining in a right-handed direction was 92.5% (range
67–100%).
There was no evidence for a relationship between the percentage of right-handed stems at each site and either latitude (F1,16 =
1.02, P = 0.33) or hemisphere (t = 0.444, d.f. = 7.16, P = 0.63)
© 2007 The Authors
Global Ecology and Biogeography, 16, 795–800, Journal compilation © 2007 Blackwell Publishing Ltd
The global trend in plant twining direction
Figure 1 Global distribution of the 17 study sites, and the percentage of plants producing either left- (open segment) or right-handed (filled
segment) helices at each site. Right-handed growth is recognizable as an increase in height from left to right (see legend). Site details, country,
sample sizes, vegetation types and results are provided in Table 1.
Table 1 Sample size, location, vegetation description and the results of surveys of plant twining direction along transects in 17 sites spanning
nine countries and approximately 65° latitude.
Site location
Number
of stems
right-handed
Number
of stems
left-handed
Percentage
of stems
right-handed
Latitude
Longitude
Vegetation
Bariloche, Argentina
BCI, Panama
Cairns, Australia
Cape Tribulation, Australia
Chajul, Mexico
Chamela, Mexico
Jujuy, Argentina
81
89
97
121
17
92
98
0
11
5
13
3
0
2
100.00
89.00
95.10
90.30
85.00
100.00
98.00
41°01′ S
09°09′ N
16°55′ S
16°05′ S
16°06′ N
19°30′ N
23°45′ S
71°49′ W
79°51′ W
145°46′ E
145°47′ E
90°59′ W
105°03′ W
64°51′ W
Kabo, Republic of Congo
Kaitoke, New Zealand
Kuringai NP, Australia
Lamington NP, Australia
Linares, Mexico
Los Amigos, Peru
Royal NP, Australia
Serenje, Zambia
Tucuman, Argentina
96
99
67
58
30
68
93
83
87
4
1
33
4
0
11
7
2
13
96.00
99.00
67.00
93.55
100.00
86.08
93.00
97.65
87.00
02°08′ N
41°04′ S
33°34′ S
28°13′ S
24°47′ N
12°33′ S
34°09′ S
13°15′ S
26°46′ S
16°11′ E
175°10′ E
151°18′ E
153°08′ E
99°31′ W
70°06′ W
151°02′ E
30°03′ E
65°20′ W
Xishuangabanna, China
96
4
96.00
21°57′ N
101°12′ E
Nothofagus forest
Tropical rain forest
Tropical rain forest
Tropical rain forest
Tropical rain forest
Tropical dry forest
Yungas (seasonally dry
subtropical woodland)
Tropical rain forest
Temperate rain forest
Woodland (Eucalypt)
Subtropical rain forest
Thornscrub
Tropical rain forest
Temperate rain forest
Mateshi (vine thicket)
Yungas (seasonally dry
subtropical woodland)
Rain forest
© 2007 The Authors
Global Ecology and Biogeography, 16, 795–800, Journal compilation © 2007 Blackwell Publishing Ltd
797
W. Edwards et al.
Figure 2 Scatterplot of the percentage of plants producing
right-handed helices (logit scale) versus latitude for each of the
17 study sites. Also shown are boxplots for the distribution of the
percentage of right-handed helices in each hemisphere. There was
no effect of latitude or hemisphere on twining direction. Site details,
country, sample sizes and vegetation types are provided in Table 1.
(Fig. 2). That is, twining plants growing at low latitudes were just
as likely to produce right-handed helices as those growing at
higher latitudes, and right-handed twining direction was equally
prevalent in the Northern and Southern Hemispheres. We therefore reject the hypotheses that twining direction is a product of
either the Coriolis effect or the apparent movement of the sun
across the sky.
DISCUSSION
Our results confirm previously unverified claims that the
production of right-handed helices is a general phenomenon
among twining plants. The vast majority (92%) of stems of
twining plants found in a wide range of vegetation types and
geographical locations across the globe grew by twining in a
right-handed direction.
The results show that at a global scale the distribution of
left- and right-handed helical growth in twining plants is nonrandom, and indeed is heavily biased to right-handed forms.
Thus, we reject the first hypothesis, i.e. that twining direction
is determined by a thigmotropic response in association with
circumnutation and with the position of first contact between
twining stem and support structure (Darwin & Darwin, 1880).
This is consistent with a recent study using a non-twining gravitropic mutant cultivar of Japanese morning glory (Pharbitis nil
or Ipomoea nil), Shidareasagao (weeping) (Kitazawa et al., 2005),
which suggests that although circumnutation may play a role
in winding, thigmotropism appears to have little influence
(Kitazawa et al., 2005).
Numerical dominance of anticlockwise twining occurred
independent of hemisphere and latitude. Thus, we also reject the
hypotheses that twining direction is determined by the apparent
movement of the sun across the sky (hypothesis two) or by the
Coriolis effect (hypothesis three).
798
The tendency towards right-handedness in twining direction
cannot be the result of selective forces operating on mechanical
strength either. The two dominant forces providing mechanical
strength in twining plants are axial tensions and normal loads
(Silk & Holbrook, 2005). Axial tensions operate tangentially to
the helix created by the plant’s stem, while normal loads act in
the horizontal plane, towards the centre of the supporting pole
(Silk & Holbrook, 2005), and neither force is determined by
twining direction. At present we know of no alternative adaptive
hypothesis capable of explaining the bias towards right-handedness
independent of latitude and hemisphere. In this context, the
over-representation of right-handed twining that we observed
may have no functional basis. What, then, may explain this
pattern?
In many animal taxa, directional asymmetries have been linked
with microtubule orientation and operation. For example, early
cloning of genes associated with asymmetry in mice coded for
tubulin-based cilia, including two microtubule-based motors
(Nonaka et al., 1998; Okada et al., 1999; Baum, 2006). These cilia
occur in ordered rows and rotate in a clockwise direction that
generates a leftward flow of extracellular fluid that gives rise to
asymmetry (Horikawa et al., 2006). Similarly, microtubule alignment has been proposed as the basis for > 90% right-handed helices in the shells of snails under natural conditions (Schilthuizen
& Davidson, 2005), and > 99% dextral (right-handed) internal
organ orientation in nematodes (as well as many other metazoans
with external bilateral symmetry) (Wood, 1998).
Evidence from the study of plant root growth suggests that
microtubules could also provide a possible explanation for directional asymmetries in twining plants. In plant cells, cortical
microtubules are thought to guide the deposition of microfibrils:
strands of structural cellulose that constitute a major mechanical
element of the plant cell wall (Hussey, 2002). Cellulose microfibrils determine the final shape of plant cells by channelling
non-directional turgor pressure during cell expansion. (We note,
however, that while microtubules are most often parallel to
microfibrils and help to align them, microfibril alignment also
occurs independent of microtubules in some cases; see Baskin,
2001; Somerville, 2006).
In roots, arrays of cortical microtubules can align transversely,
helically or longitudinally to the primary growth axis. Liang et al.
(1996) demonstrated that the orientation of microtubule arrays
was consistent at specific locations in the roots of maize and
arabidopsis. In both species, rapidly elongating cells displayed
transverse arrays, ‘followed by helical arrays with consistent
right-handed organization, followed in maize (and probably also
in arabidopsis) by longitudinal and finally left-handed helical
arrays’ (Liang et al., 1996, p. 13). When microtubules (and thus
microfibrils) are transverse (as in normal elongating cells), in
order for the cell to expand cross-linking glycans between microfibrils are cut. This allows the cellulose microfibrils to move apart
under pressure, and cells to expand perpendicular to microtubule
orientation and in line with the principal apical/basal growth
axis (Lloyd & Chan, 2002). Two recent studies have shown
that the early development of helical microtubule orientation
can cause root growth to be ‘twisted’ in the opposite direction
© 2007 The Authors
Global Ecology and Biogeography, 16, 795–800, Journal compilation © 2007 Blackwell Publishing Ltd
The global trend in plant twining direction
of rotation to the microtubule array (Furitani et al., 2000,
Thitamadee et al., 2002).
Whether or not mechanisms associated with the twisting of
plant roots can be extended to explanations for twining direction
in stems is uncertain, and should only be considered as a hypothesis at present. First, while some authors have argued that
regular oscillation and a high degree of curvature in arabidopsis
roots (a phenomenon knows as root waving) reflects circumnutation (Simmons et al., 1995; Rutherford & Masson, 1996;
Migliaccio & Piconese, 2001), Thompson & Holbrook (2004)
have demonstrated that much of this behaviour should be expected
given the simple mechanical relationship between the size of roots
and root tips, and the impedance of root growth due to the substrate.
Second, we know of no previous study that has examined cortical
microtubule or microfibril arrays in the shoots of twining plants.
Patterns of left–right handedness in plant organs appear to be
much less constant than our results for twining direction. For
example, Spiranthes australis produces a helical arrangement of
flowers on inflorescences. In self-pollination experiments, both
left- and right-handed inflorescences are produced with equal
frequency (Callos & Medford, 1994), and the spiral phyllotaxis in
leaf arrangement of Nicotiniana tabacum also occurs equally in
both left- and right-handed forms (Hashimoto, 2002). In the
coconut palm (Cocos nucifera), spiral phyllotaxy producing
left- and right-handed forms is similarly not an inherited trait
(Toar et al., 1979, Minorsky & Bronstein, 2006). However, in
C. nucifera, left- and right-handed forms are non-randomly distributed at a global scale: right-handed forms predominate in the
Northern Hemisphere and left-handed forms in the Southern
Hemisphere (Davis & Davis, 1987). Recent evidence suggests
that asymmetry in phyllotaxy in coconut palms results from
geomagnetic variability between locations rather than a simple
Northern Hemisphere–Southern Hemisphere effect (Minorsky
& Bronstien, 2006). While this appears to be true in coconut
palms, the pattern in twining we report shows over-representation
of right-handed helices in both hemispheres. Thus, it is unlikely
that asymmetries in coconut palm phyllotaxy and plant twining
have similar causes.
The mechanism provided by the microtubule orientation
hypothesis explains our data better than any alternative at
present. If the microtubule basis for asymmetric growth in roots
of maize and arabidopsis is also shown to be the cause of helical
growth of shoots in twining species, one question still remains:
why is microtubule orientation biased? Within arabidopsis,
mutations can lead to both left-handed (Thitamadee et al., 2002)
and right-handed (Furitani et al., 2000) forms. Twining plants
are a polyphyletic grouping, the twining habit having evolved
independently many times (Schnitzer & Bongers, 2002). Across
all twining plants, there must have existed numerous opportunities
for mutations resulting in patterns of microtubule orientation
producing either left- or right-handed pathways. Indeed, there
have been claims that twining handedness can be constant within
a species, but differ between species (Gardner, 1970; Hashimoto,
2002; Hussey, 2002; Thitamadee et al., 2002). However, these
claims are mostly anecdotal and have not been accompanied by
quantitative data. Species identities were not recorded in our
surveys. This is an important next step. We acknowledge that
there is some potential for random taxonomic bias or bias in
twining stem size associated with species that may have occurred
in individual sites, and that these effects could give rise to the
over-representation of one helical form or another. However, we
consider it very unlikely that either effect repeatedly operated to
produce a consistently high proportion of right-handed forms
across independent locations. We have begun to investigate the
occurrence of left- and right-handed helices in a phylogenetic
framework.
Resolving the question of what controls microtubule orientation could provide deeper insights into the nature of directional
bias in twining plants. One possible explanation might be that
microtubule directional bias reflects the chiral purity that exists
in the terrestrial biosphere (19 of the 20 biologically important
amino acids are left-handed; the other is achiral) (Goldanski &
Kuzman, 1991). Left-handed amino acids give rise to predominantly right-handed helices in proteins (Novotny & Kleywegt,
2005). Tests of correspondence between the chirality of proteins,
microtubule arrays and twining direction will be required to test
this hypothesis. If true, the global pattern of dominance of righthanded twining forms may thus reflect the chance events that
determined chiral purity.
In summary, we have shown a global tendency for climbing
plants to twine in an anticlockwise direction. This tendency cannot be explained by the side of the climbing stem that first
encounters a host, by apices following the apparent movement of
the sun across the sky, by the Coriolis effect or by differences in
mechanical strength. As noted by Hussey (2002), in reference to
von Marilaun (1902), different directions of twining may be
determined by subcellular forces. An investigation of cell wall
structure in left- and right-handed stems will be required to test
the idea that this global pattern in twining direction might be
due to the interplay between the chirality of biological molecules
and the orientation of microtubule arrays.
ACKNOWLEDGEMENTS
We thank Nina Babiuk for first posing this question to us, Tang
Yong, Sarah Boulter and Benjamín Magaña for their help with
data collection, and Linda Beaumont for help in producing
Fig. 1. An Australian Research Council grant supported A. T.
Moles, and funded her international data collection. Tobias
Baskin and one anonymous referee provided invaluable advice
and suggestions, especially in relation to microtubule operation
and orientation.
REFERENCES
Baskin, T. (2001) On the alignment of cellulose microfibrils by
cortical microtubules: a review and a model. Protoplasma, 215,
150–171.
Baum, B. (2006) Left-right asymmetry: actin-myosin through
the looking glass. Current Biology, 16, R502–R504.
Callos, J.D. & Medford, J.I. (1994) Organ positions and pattern
formation in the shoot apex. Plant Journal, 6, 1–7.
© 2007 The Authors
Global Ecology and Biogeography, 16, 795–800, Journal compilation © 2007 Blackwell Publishing Ltd
799
W. Edwards et al.
Darwin, C. (1876) The movement and habits of climbing plants.
Appleton, New York.
Darwin, C. & Darwin, F. (1880) The power of movement in plants.
John Murray, London.
Davis, T.A. & Davis, B. (1987) Association of coconut foliar
spirality with latitude. Mathematical Modelling, 8, 730–733.
Dytham, C. (1999) Choosing and using statistics: a biologist’s
guide. Blackwell Science, Oxford.
Furitani, I., Watanabe, Y., Prieto, R., Masukawa, M., Suzuki, K.,
Naoi, K., Thitamadee, S., Shikanai, T. & Hashimoto, T. (2000)
The SPIRAL genes are required for directional control of cell
elongation in Arabidopsis thaliana. Development, 127, 4443–
4453.
Gardner, M. (1970) The ambidextrous universe. Penguin, Victoria,
Australia.
Gill, A.E. (1982) Atmosphere–ocean dynamics. Academic Press,
New York.
Goldanskii, V. & Kuzman, V.V. (1991) Chirality and the cold
origin of life. Nature, 352, 114.
Hashimoto, T. (2002) Molecular genetic analysis of left-right
handedness in plants. Philosophical Transactions of the Royal
Society, Biological Sciences, 357, 799 – 808.
Horikawa, N., Tanaka, Y., Okada, Y. & Takeda, S. (2006) Nodal
flow and the generation of left-right asymmetry. Cell, 125,
33 –45.
Hussey, P.J. (2002) Microtubules do the twist. Nature, 417,
128 –129.
Kitazawa, D., Hatakeda, Y., Kamada, M., Fujii, N., Miyazawa, Y.,
Hoshino, A., Iida, S., Fukaki, H., Terao Morita, M., Tasaka, M.,
Suge, H. & Takahashi, H. (2005) Shoot circumnutation and
winding movements require gravisensing cells. Proceedings of
the National Academy of Sciences USA, 102, 18742 –18747.
Liang, B.M., Dennings, A.M., Sharp, R.E. & Baskin, T.I. (1996)
Consistent handedness of microtubule helical arrays in maize
and Arabidopsis primary roots. Protoplasma, 190, 8–15.
Lloyd, C. & Chan, J. (2002) Helical microtubule arrays and spiral
growth. The Plant Cell, 14, 2319–2324.
MacArthur, R.D. (1972) Geographical ecology: patterns in the
distribution of species. Harper & Row, New York.
von Marilaun, K.A. (1902) The natural history of plants, their
forms, growth, reproduction and distribution (transl. by F.W.
Oliver with the assistance of Lady Busk and M.F. Macdonald).
Blackie, London.
Mayr, E. (1963) Animal species and evolution. Harvard University
Press, Cambridge, MA.
Migliaccio, G.D. & Piconese, S. (2001) Spiralizations and tropisms in Arabidopsis. Trends in Plant Science, 6, 561–565.
Minorsky, P.V. & Bronstein, N.B. (2006) Natural experiments
indicate that geomagnetic variations cause spatial and temporal
variations in coconut palm asymmetry. Plant Physiology, 142,
40 –44.
Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A. & Kanai,
Y. (1998) Randomization of left-right asymmetry due to loss of
nodal cilia generating leftward flow of extraembryonic fluid in
mice lacking KIF3B motor protein. Cell, 95, 829 – 837.
800
View publication stats
Novotny, M. & Kleywegt, G.J. (2005) A survey of left-handed
helices in protein structures. Journal of Molecular Biology, 347,
231–241.
Okada, Y., Nonaka, S., Tanaka, Y., Saijoh, Y., Hamada, H. &
Hirokawa, N. (1999) Abnormal nodal flow precedes situs
inversus in iv and inv mice. Molecular Cell, 4, 459–468.
Persson, A. (1998) How do we understand the Coriolis force?
Bulletin of the American Meteorological Society, 79, 1373 –1385.
Rutherford, R. & Masson, P.H. (1996) Arabidopsis thaliana sku
mutant seedlings show exaggerated surface-dependent alteration in root growth vector. Plant Physiology, 111, 987–998.
Schnitzer, S.A. & Bongers, F. (2002) The ecology of lianas
and their role in forests. Trends in Ecology & Evolution, 17,
223–230.
Schilthuizen, M. & Davidson, A. (2005) The convoluted evolution
of snail chirality. Naturwissenschaften, 92, 504–515.
Silk, W.K. & Holbrook, N.M. (2005) The importance of frictional interactions in maintaining the stability of the twining
habit. American Journal of Botany, 92, 1820–1826.
Simmons, C., Soll, D. & Migliaccio, F. (1995) Circumnutation
and gravitropism cause root waving in Arabidopsis thaliana.
Journal of Experimental Botany, 46, 143–150.
Somerville, C. (2006) Cellulose synthesis in higher plants.
Annual Review of Cell and Developmental Biology, 22, 53–78.
Stevens, G.C. (1989) The latitudinal gradients in geographical
range: how so many species co-exist in the tropics. The American Naturalist, 133, 240–256.
Thitamadee, S., Tuchihara, K. & Hashimoto, T. (2002) Microtubule basis for left-handed helical growth in Arabidopsis.
Nature, 417, 193–196.
Thompson, M.V. & Holbrook, N.M. (2004) Root-gel interactions and the root waving behavior of Arabidopsis. Plant
Physiology, 135, 1822–1837.
Toar, R.E., Rompas, T.M. & Sudasrip, H. (1979) The noninheritance of the direction of foliar spiral in coconut. Experientia, 35, 1585–1587.
Wood, W.B. (1998) Handedness asymmetry in nematodes.
Seminars in Cell & Developmental Biology, 9, 56–60.
BIOSKETCHES
Will Edwards is a senior lecturer in tropical ecology.
His interests are rainforest diversity, seed dispersal and
decisions involved in optimal foraging.
Angela Moles’ interests are in the ecology and evolution
of seed size, and in global patterns in plant traits. Data for
the present paper were gathered while Angela was
establishing study sites for a worldwide study of herbivory.
Peter Franks is a senior lecturer in plant physiology,
with research interests in xylem function and the
regulation of plant gas exchange.
Editor: Martin Sykes
© 2007 The Authors
Global Ecology and Biogeography, 16, 795–800, Journal compilation © 2007 Blackwell Publishing Ltd