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Review
SPECIAL ISSUE: Using Ideas from Behavioural Ecology
to Understand Plants
The behavioural ecology of climbing plants
Ernesto Gianoli
1,2
*
1
Departamento de Biologı
´
a, Universidad de La Serena, Casilla 554, La Serena, Chile
2
Departamento de Bota
´
nica, Universidad de Concepcio
´
n, Casilla 160-C, Concepcio
´
n, Chile
Received: 1 October 2014; Accepted: 2 February 2015; Published: 12 February 2015
Associate Editor: James F. Cahill
Citation: Gianoli E. 2015. The behavioural ecology of climbing plants. AoB PLANTS 7: plv013; doi:10.1093/aobpla/plv013
Abstract. Climbing plants require an external support to grow vertically and enhance light acquisition. Vines that
find a suitable support have greater performance and fitness than those that remain prostrate. Therefore, the location
of a suitable support is a key process in the life history of climbing plants. Numerous studies on climbing plant behav-
iour have elucidated mechanistic det ails of support searching and attachment. Far fewer studies have addressed the
ecological significance of support-finding behaviour and the factors that affect it. Without this knowledge, little pro-
gress can be made in the understanding of the evolution of support-finding behaviour in climbers. Here I review studies
addressing ecological causes and consequences of support finding and use by climbing plants. I also propose the use
of behavioural ecology theoretical frameworks to study climbing plant behaviour. I show how host tree attributes may
determine the probability of successful colonization for the different types of climbers, and examine the evidence of
environmental and genetic control of circumnutation behaviour and phenotypic responses to support availability .
Cases of oriented vine growth towards supports are highlighted. I discuss functional responses of vines to the interplay
betwe en herbivory and support availability under different abiot ic environments, illustrating with one study case
how results comply with a theoretical framework of behavioural ecology originally conceived for animals. I conclude
stressing that climbing plants are suitable study subjects for the application of behavioural–ecological theory. Further
research under this framework should aim at character izing the different stages of the support-finding process in
terms of their fit with the different climbing m odes and environmental settings. In particular, cost–benefit analysis
of climbing plant behaviour should be helpful to infer the selective pressures that have operated to shape current
climber ecological communities.
Keywords: Behavioural ecology; circumnutation; climbing plants; lianas; optimal foraging; support-searching; vines.
Introduction
Climbing plants need to attach themselves to an external
support—typically neighbouring plants—in order to grow
vertically to a significant extent and enhance light acqui-
sition. Trellis availability influences climber diversity in
forests (Garbin et al.2012), and cli mbers that fail to
encounter a trellis often show reduced growth and/or re-
production compared with those successfully climbing
onto an external support. This has been observed in for-
ests (Putz 1984; St ansbury et al.2007), open habitats
* Corresponding author’s e-mail address: egianoli@userena.cl
Published by Oxford University Press on behalf of the Annals of Botany Company.
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
1
(Gianoli 2002; Price and Wilcut 2007; Gonza
´
lez-Teuber
and Gianoli 2008) and controlled environments (Puntieri
and Pys
ˇ
ek 1993; Schweitzer and Larson 1999). Support
finding not only involves enhanced fitness but also trig-
gers changes in growth form, biomass allocation, morph-
ology and physiology (Raciborski 1900; Jaffe and Galston
1968a; Strong and Ray 1975; Ray 1987; Puntieri and Pys
ˇ
ek
1993; den Dubbelden and Oosterbeek 1995; Gianoli 2001,
2003). Therefore, the location (and colonization) of a suit-
able support is a key process in the life history of climbing
plants (Hegarty 1991).
Darwin’s observations on the oscillatory movements of
exploring stems and tendrils (circumnutation) somehow
founded the field of climbing plant behaviour (Darwin
1875). Since then, a plethora of studies on climbing
plant behaviour with regard to support searching and
attachment have elucidated mechanistic details at the
anatomical, biomechanical, physiological and cellular
levels (e.g. Tronchet 1945, 1946; Baillaud 1962; Jaffe
and Galston 1968a; Millet et al. 1988; Putz and Holbrook
1991; Silk and Hubbard 1991; Brown 1993, Weiler et al.
1993; Scher et al.2001; Kitazawa et al. 2005; Silk and
Holbrook 2005; Goriely and Neukirch 2006; Bowling and
Vaughn 2009; Stolarz 2009; Steinbrecher et al. 2010;
Bauer et al
.2011; Gerbode et al. 2012). However , far
fewer studies have addressed the ecological significance
of support-finding behaviour in climbing plants and the
factors that affect it (e.g. Pen
˜
alosa 1982 ; Larson 2000;
Gianoli and Molina-Montenegro 2005; Gonza
´
lez-Teuber
and Gianoli 2008) . Without this knowledge, limited pro-
gress can be made in the understanding of the evolution
of support-finding behaviour in climbers. Here, I review
studies that have addressed ecological causes and conse-
quences of support location and use by climbing plants.
I also propose the use of behavioural ecology theoretical
frameworks to study climbing plant behaviour. The article
focusses mainly on t wining plants, but also considers
cases from plants having the other two ‘active’ modes
of attachment: tendrils and adhesive roots (Darwin
1875; Isnard and Silk 2009).
Ecological Approaches to Climbing Plant
Behaviour
Host tree characteristics
Several host tree attributes may determine the probabil-
ity of colonization by climbers (Hegarty 1991). The size
(diameter) of supports influences their suitability for twin-
ing plants. Specifically, both theoretical and empirical
approaches show that when support diameter increases
beyond some point twining plants are unable to maintain
tensional forces and therefore lose attachment to the
trellis (Putz 1984; Putz and Holbrook 1991; Goriely and
Neukirch 2006; Carrasco-Urra and Gianoli 2009). That
these plants have problems to twine round a thick sup-
port was already pointed out by Darwin, citing Hugo von
Mohl’s obs ervati ons and reporting his own experiments
with shoots of the twining vine Wisteria sinensis (Sims)
Sweet, which could not climb onto a support nearly
15 cm wide (Darwin 1875). Field studies in tropical, sub-
tropical and temperate rainforests confirm that the rela-
tive abundance of stem twiners decreases with increasing
tree diameter (Putz 1984; Putz and Chai 1987; Carsten
et al. 2002; Carrasco-Urra and Gianoli 2009). In a tropical
rainfor es t, 90 % of stem twiners individuals with a diameter
at br east height (dbh) of ≤1 cm grew on trees with a dbh of
≤8cm(Nabe-Nielsen 2001). The support-size biomechanic-
al constraints for twining plants are intermediate compared
with tendril climbers, whose upper limit of usable trunk
diameter is even lower, and root climbers, which are not
constrained at all by large support diameters (Putz 1984;
Putz and Chai 1987; Putz and Holbrook 1991; Chalmers
and Turner 1994; DeWalt et al. 2000; Nabe-Nielsen 2001;
Carrasco-Urra and Gianoli 2009).Thereisalsoasignifi-
cant variation in the range of suitable support diameters
within a given climbing mode. Thus, Pen
˜
alosa (1982)
studied two twining lianas that differed in their degree
of morphological specialization (shoot architecture) and
found differential success rate of attachment across the
population of support diameters in a tropical rainforest.
As expected, vines may modify their climbing behaviour
when twining around supports of different diameters.
Thus, the ascent angle decreased with increasing support
diameter in Humulus lupulus L. (Bell 1958) and Dioscorea
bulbifera L. (Putz and Holb rook 1991; Scher et al.2001),
but the radius of curvature of the twining vine helix was
unaffected. It has been suggested that the climber’s coils
lose stability when the radius of curva ture of the helix
is no longer greater than the support radius (Putz and
Holbrook 1991).
Circumnutation behaviour and phenotypic responses
to support availability, which may determine the suitable
range of support sizes, should show—at least to some
extent—environmental and genetic control. It has
been shown that the shrub vs. vine growth forms in Toxico-
dendron diversilobum (Torr. & A.Gray) Greene are deter-
mined environmentally, mainly by support availability
(Gartner 1991). Darwin (1875) noted that the twining
vine Phaseo lus coccineus L. failed to twine round sticks
8–10 cm in diameter when tested in a room with lateral
light but the vines succeeded when placed outdoors. He
furthe r remarked that twiners f rom the tropics, or from
warmer temperate regions, seemingly are able to ascend
thicker trees (Darwin 1875). Whether twining plants from
warmer habitats are better endowed to exploit thick sup-
ports is yet to be demonstrated, and should be addressed
2 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
Gianoli — Behavioural ecology of vines
wi th a phylogeny-wise ana lysis since environment and
specie s may be confounded factors. In terestingly, a re-
cent study comparing climbing plants fro m temperate
and subtropical South America found that a greater pro-
portion of twiners occur in the subtropical, warmer area
(Durigon et al. 2014). With regard to genetic variation,
there is some evi dence of differences in circumnutation
behaviour and morphological plasticity in response to
support availability between congeneric twining vines
tested in a common environment (Convolvulus spp. and
Ipomoea spp., Atala and Gianoli 2008; Lonicera spp.,
Schweitzer and Larson 1999). However, at the withi n-
species level, the maternal family did not influence
phenotypic responses to support availability in I. purpurea
(L.) Roth (Gianoli and Gonza
´
lez-Teuber 2005). The quanti-
tative trait loci controllin g climbing abil ity have been
identified in a recombinant inbred line of common
bean, and most of these loci were found on the lower
half of a given lin kage group, suggesting the existence
of a major pleiotropic locus controlling the climbing
habit (Checa and Blair 2008). Experiments with mutants
of I. nil (L.) Roth have demonstrated a link between
circumnutatio n and gravisensing cells (Kitazawa et al.
2005).
Tree features such as bark roughness and flakiness may
also influence support use by climbers ( Putz 1980, 1984;
Putz and Chai 1987; Campbell and Newbery 1993; Talley
et al.1996; Carsten et al.2002; Campanello et al.2007;
van der Heijden et al. 2008). Bark flakiness has been con-
sidered an adaptation of trees against liana infestation,
assuming that lianas may be unable to climb trees with
rapidly shed bark because it implies loosing points of an-
chorage (Talley et al. 1996; Carsten et al. 2002). However,
field evidence suggests that liana infestation is not par-
ticularly deterred in tree species that shed bark frequently
(Carsten et al. 2002; Carrasco-Urra and Gianoli 2009;
Jime
´
nez-Castillo and Lusk 2009): climbers somehow
manage to use as supports trees with peeling bark. On
the other hand, the frequency of stem twiners in a rainfor-
est did increase with bark roughness (Carsten et al. 2002).
Interestingly, Darwin (1875) observed in k idney beans
that the stem’s axial twisting increased with support
roughness, thus suggesting that twisted stems might be
more rigid and that it could be advantageous to deal with
rugged supports. Silk and Holbrook (2005) s howed that
the torsion of the twining stem was determined by helical
parameters that vary with support diameter.
Herbivory and support availability
Successful climbing by twining vines not only may help
avoid shading by co-o cc urring taller plants, but also
may place climbers beyond ground he rbivores. There is
field evidence th at prostrate, unsupported vines suffe r
more herbivore damage than plants climbing onto neigh-
bouring vegetation (Gianoli and Molina-Montenegro
2005; Gonza
´
lez-Teuber and Gi anoli 2008 ; Gianoli and
Carrasco-Urra 201 4). Moreover, with in a forest com-
munity, the identity of the supporting t ree to which
the climber is associated influences herbivore damage
(Sasal and Sua
´
rez 2011; E. Gianoli and F. Carrasco-Urra,
unpubl. data). In agreement with a hypot hesis of adap-
tive climbing behaviour, it ha s been shown that circum-
nutation behaviour, measured as the twining rate on
experimental supports, was enhanced in several Convol-
vulaceae vines receiving leaf damage (Gianoli and
Molina-Montene gro 2005; Atala and Gianoli 2008). This
induced t wining—compared with undamaged p lants—
did not result from increased stem growth rate (Gianoli
and M olina-Montenegro 2005 ; Atala and Gianoli 2008),
which somewhat challenges the notion that circumnuta-
tion is intrinsically a growth movement (Mugnai et al.
2007). In C. arvensis L. the induced twining occurred simi-
larly in both sun and shade conditions, and it was paral-
leled by an increase in photosynthetic rate, but only
under shade (Gianoli and Molina-Montenegro 2005). This
suggests that enhanced twi ning under low light entails
an extra demand for resources by these vines. When
stems of the twiner C. chilensis Pers. were clipped mimick-
ing rabbit grazing in a semiarid shrubland, there was an in-
creased production of tendril-like lateral stems that
facilitated climbing in shade conditions (Gonza
´
lez-Teuber
and Gianoli 2008). This phenomenon granted protection
against herbivores by promoting the association with
nurse plants (cacti and thorny shrubs); interestingly, such
induction of tendril-like stems following damage only oc-
curred in the shade, which is a cue of the presence of the
nurse plant (Gonza
´
lez-Teuber and Gianoli 2008). Induced
twining was also observed in I. purpurea after subjecting
plants to folivory by snails as well as to exposure to conspe-
cific volatiles (released from ground leaves) (Atala et al.
2014). In summary, the described phenomena of climbing
plant behaviour in response to herbivory and abiotic condi-
tions are likely to occur in natural ecological communities.
The exogenous application of jasmonic acid, a ubiq-
uitous mediator of defensive responses in plants
(Wasternack and Parthier 1997; Farmer et al. 2003),
caused induced twining in I. purpurea as did leaf damage
(Atala and Gianoli 2008). This could be a rather general
response, as the application of jasmonate on the climbing
plant Bryonia dioica caused tendril coiling (Falkenstein
et al. 1991; Weiler et al. 1993). With regard to abiotic regu-
lation of the phenomenon, water stress had contrasting
effects on induced twinin g (Atala et al.2011). On the
one hand, moderate drought, which increases trichome
density on stems of I. purpurea (
Atala and Gianoli
2009a), enhanced the twining response (Atala et al.
AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
3
Gianoli — Behavioural ecology of vines
201 1). This result is consistent wit h the finding that tri-
chomes facilitate climbing in this species as they function
like ratchets (Silk and Holbrook 2005), which are analo-
gous to hooks used by some climbing pla nts (Bauer
et al. 2011). On the other hand, severe water stress lim-
ited the induced twining in I. purpurea (Atala and Gianoli
2009b; Atala et al. 2011), probably because extreme
drought elicits plant responses that c ounterac t ph eno-
typic responses to herbivory (Quezada and Gianoli 2010).
Going back to the issue of the helical geometry of
twining vines, Darwin (1875) noted that the terminal
internodes made first a close spire, securing plant attach-
ment during windy conditions, but the following spires
were more open. This agrees w ith observations that a
loosely coiled, old vine segment can be sustained by
one or two tight younger coils (Putz and Holbrook 1991).
It is also consistent with biomechanical experiments
showing that forces pulling down a twining vine will
tend to stabilize the plant–support interaction (i.e. the
normal load exerted by the vine towards the support
increases linearly wi th axial downward tension), unless
the forces are applied close to the vine tip, because the
twining vine is weak in compression (Silk and Holbrook
2005). Thus, grazing herbivores pulling down the climbing
plant would not succeed: they would tear the vine before
getting it to slip down. Interestingly, when documenting
induced twining in Ipomoea vines, it was observed that
leaf damage mimicking insect herbivory caused a reduc-
tion in the angle of ascent within the first three gyres in
all tested species (I. purpurea, I. tricolor Cav., I. nil)(Atala
and Gianoli 2008). Thus, vines respond to leaf damage as
if they were twining around a thicker support (see above).
Whether reduced angles of ascent in twiners translate into
enhanced appression of the support remains to be tested,
but related evid ence suggests the opposite (Putz and
Holbrook 1991; Silk and Hubbard 1991; Scher et al. 2001).
Oriented growth and vine ‘decisions’
From an adaptive standpoint, an expected feature of
climbing plant behaviou r is that vines should be able to
locate their supports and grow towards them. After con-
ducting several simple experiments indoors, Darwin
(1875) concluded that tendrils of Bignonia capreolata
L. actively grow towards the dark, a phenom enon he
later termed ‘apheliotropism’ (Darwin 1880). He remarked
that circumnutation in these tendrils was extremely
irregular, often staying static, that the apheliotropic move-
ment was a modified circumnutation, and that this vine
depended on apheliotropism to find tree trunks (Darwin
1880). One century later, experiments by Strong and Ray
(1975) in a tropical forest showed that seedlings of the
root climber Monstera tenuis K.Koch are attracted to the
darkness, which is associated with the trees in the forest,
and coined the term ‘skototropism’. Importantly, once the
tree is found, the vine switches back and starts growing to-
wards light (Strong and Ray 1975). Most documented
cases of skototropism correspond to root climbers (Ray
1987; Hegarty 1991; Metcalfe 2005; Kato et al.2012), but
tendril-bearers can also exhibit this support-finding behav-
iour. Thus, apart from B. capreolata and its skototropic ten-
drils described by Darwin (1875), it has been reported that
Dolichandra unguis-cati (L.) L.G.Lohmann (another Bignonia-
ceae) shows intra-plant variation in light response: the claw-
like tendrils are skototropic and the shoot tips are positively
phototropic (Lee and Richards 1991).
The above-described cases somewhat lend support to
earlier claims that some climbing plants, including
tendril-bearers (Cyclanthera pedata (L.) Schrad.) and
stem twiners (Cuscuta gronovii Willd. ex Roem. & Schult.),
were able to chan ge their circ umnutation patter ns in
order to reach support targets (Tronchet 1946, 1977);
these reports were received with a degree of scepticism
(Roussel 1978; Putz and Holbrook 1991). In the case of
Cuscuta there is now solid evidence that these parasitic
vines locate their host plants via orie nted growth. Thus,
experiments have proved that Cuscuta pentagona En-
gelm. seedlings grow towards regions of lowe red red :
far-red radiation ratio (a signal of the presence of
chlorophyll-bearing organi sms, Ballare
´
et al. 1987; Orr
et al.1996), and that they can locate host plants in the
dark fol lowing volatile chemi cal cues (Runyon et al.
2006). The evolution of this highly specialized host loca-
tion behaviour presumably results from strong selective
pressure s relat ed to the para sitic lifestyle because, in
order to survive, Cuscuta seedlings m ust attach to a
host plant shortly after emergence; othe rwise their en-
ergy reserves are exh austed. Thus, in a greenhouse ex-
periment with autotrophic Ipomoea species there was
no correlation between the red : far-red ratio in coloured
stakes or corn plants and the frequency of vines twining
around them (Price and Wilcut 2007).
Do comm unity-level studies support the notion that
climbers do not find support/hosts merely by chance? A
number of field studies, conducted in almost all forest
types, have shown as sociations between climbing plant
species and tree species that are statis tically different from
what would be expected by chance (Hegarty 1991
; Campbell
and Newbery 1993; Chalmers and Turner 1994; Talley et al.
1996; Chittibabu and Parthasarathy 2001; Carste n et al.
2002; Mun
˜
oz et al.2003; Nesheim and Økland 2007;
Leicht-Young et al. 2010; Blick and Burns 2011). Conse-
quently, host selection or host specificity has often been
invoked to explain these patterns. An alternative explan-
ation could consider the occurrence of convergence in mi-
crosite preference between vines and trees (Blick and
Burns 2011). Apart from the tree traits possibly explaining
4 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
Gianoli — Behavioural ecology of vines
differen tial suscep tibility to vine infestation, the under-
lying mechanisms or the adaptive value of these patterns
are rarely reported or discussed. This information is
needed in order to determine the reliability and ecologic-
al significance of field patterns.
A central question that could be asked is whether vines
actually make ‘decisions’ when it comes to support
searching and selection. Apart from the evidence of
oriented growth towards trees or experimental stakes dis-
cussed above, it could be added that climbing plants may
reject a part icular support. Th is was first described by
Darwin for tendrils in B. capreolata initially seizing but
then loosing sticks that were inappropriate (Darwin
1875). A similar phenomenon is observed when herb-
aceous twining vines get in contac t with a very t hick
trunk and wind up on themselves instead of attempting
to twine around it (a hopeless try, in view of the diameter
constraints discussed above). In the case of annual vines,
Darwin (1875) remarked that, even without support
diameter constraints, it would be maladaptive to twine
around thick—and hence large—trees, as these vines
would hardly reach high-light layers by the end of the
growing season.
The ‘self-twining’ (i.e. vine stems twining around each
other) often occurs when vines grow beyond the height
of a short support and then go up and down it, or when
they fail to encounter a suitable support (Darwin 1875).
What is the adaptive value of self-twining? To keep on cir-
cumnutating seems to be meaningless as new available
supports would rarely appear, it would be energy-
consu ming, and—for a given species—circumnutation’s
rangecannotbeextendedbeyondsomepointbecause
of biomechanical constraints: the diameters of circumnu-
tation by shoot tips range from a few centimetres to over
1m (Putz and Holbrook 1991). Ideally, twining vines
should have a dual system, with trailing, skototropic
stems searching for supports in addition to (or gi ving
rise to) circumnutating stems. However, the closest
known case did not prove efficient in this regard. Thus,
the twining liana I. phillomega (Vell.) House produces
creeping shoots (stolons) with high elongation rates
under shade conditions, while twining shoots are pro-
duced in high-light conditions; but stolons did not switch
to twining stems once support was found (Pen
˜
alosa
1983). A more efficient strategy is deployed by Syngonium
root climbers, where a slender, skototropic prostrate stem
searches for supports across the forest floor, but if a tree is
not found after 2 m of extension (30 internodes), the
plant reverts to the original, ‘sessile’ rosette form; the
shoot alternates indefinitely between both forms until a
tree is located (Ray 198 7). Overall, climbers rarely show
such functional division of labour among orthotropic (ver-
tical) an d plagiotropic (horizontal) shoots (Larson 2000;
Gianoli 2001; Valladares et al. 2011). Some climbing plants
seem to have a ‘give-up’ time concerning support finding.
Darwin (1875) found that the twining hop (H. lupul us)
stopped circumnutation after 5 days (37 revolutions) fail-
ing to find a support. Likewise, when the tip of a prostrate
shoot of th e climber Lonicera sempervirens touches the
ground, circumnutation sto ps; it may resume after con-
tinued growth, but often in a different compass direction
(Larson 2000). Long-lived species may have further
chances: if searcher shoots of some lianas in a tropical
rainforest fail to find a support, they fall over and are re-
placed by another shoot (Putz 1984).
Theoretical Frameworks to Study Climbing
Plant Behaviour
Plant behaviour involves rapid morphological or physio-
logical responses to events or environmental changes
(Karban 2008). Theoretical frameworks from behavioural
ecology, traditionally applied to animals, have been suc-
cessfully used to study plant behaviour (Marshall and
Folsom 1991; Dudley and File 2007; Cahill and McNickle
2011; Jensen et al.2011; Karst et al. 2012; Gagliano
et al. 2014) . Climbing plants have shown pat terns of
herbivory-induced chemical d efences (Gianoli et al.
2007) that conform to optimal defence theory (Zangerl
and Rutledge 1996). However, theoretica l approaches
from behavioural ecology have not been applied to the
study of climbing plant behaviou r. Ray (1992) described
what he termed foraging behaviour in trop ical Araceae
climbers, characterizing shoot developmental patterns
(length and diameter of internodes) in both trailing and
climbing stems through the forest. In general terms, for-
aging behaviour in plants refers to their capacity of pla-
cing resource-acquiring structures (leaves and root tips)
selectively within their habitat, where essential resources
are usually heterogeneously distributed ( Hutchings and
De Kroon 1994). In the case of climbing plants, support
finding brings about enhanced access to light resources
(see above), but only then vines should fully display
resource-acquiring struct ures. Accordingly, leaf expan-
sion is delayed relative to stem extension in erect leader
shoots of twiners and tendril climbers, thereby reducing
stem load and facilitating support searching (Raciborski
1900; Baillaud 1962; French 1977). Field observations in-
dicate that the maximu m length t hese leafless leader
shoots can attain before falling over (‘searcher shoot
length’, Putz 1984) is species specific and largely deter-
mines the distance a climber can traverse between sup-
ports in the forest (Putz 1984). The capacity to span
between supports is very important for the ecology
of vines; however, to my knowledge, no study has specif-
ically addressed phenotypic plastic ity or evolution ary
AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
5
Gianoli — Behavioural ecology of vines
responses in searcher shoot length. In the following dis-
cussion of theoretical app roaches to climbing plant be-
haviour, I will focus on foraging behaviour, specifically
with regard to support searching.
Jensen et al. (2011) sh owe d in the sensitive plant
Mimosa pudica L., which rapidly folds its leaves when
touch ed, that the anti-predator behaviour (time to leaf
reopening after stimulation) was sustained longer under
high-light conditions tha n under shading. This pattern
supp orts prediction s of animal- derived theory based on
an optimality approach to anti-predation behaviour
using stochastic dynamic programming (SDP) models
(Lima 1998; Hutchinson and McNamara 2000). Specif-
ically, the SDP model predicts that individuals are more
willing to take predation risks during foraging when ener-
getically stressed (Lima 1998). The theoretical framework
of state-dependent decision-making under predation risk
(Lima 1998) can be applied to a case of twining vines
facing leaf damage with and without support availability
and under contrasting abiotic environments. The study
evaluated the effect of the light environment and support
availability on the induc tion of tropane alkaloids (chem-
ical defences) after leaf damage in C. arvensis (Gianoli
et al. 2007), considering that herbivory pressure in the
field is greater for prostrate vines compared with climbing
vines (≈80 % vs. ≈40 % leaves showing damage; Gianoli
and Molina-Montenegro 2005). The assumptions are that
(i) alkaloid induction (difference between damaged and
undamaged plants) is a measure of anti-predator behav-
iour, (ii) internode length is a proxy for vine foraging and
(iii) the shade environment is where plants are energetic-
ally stressed. The prediction wo uld be that vines should
show reduced anti-predator behaviour and increased for-
aging in the shade (fewer resources available). However,
this pattern should be observed only in the moderate her-
bivory scenario (climbing vines: 40 % leaf damage). In the
case of prostrate vines growing under a strong herbivory
pressure (80 % leaf damage), anti-pred ator behaviour
should not be relaxed because it would be maladaptive,
but enhanced vine foraging should hold. This is based on
the fact that beyond some level of predation risk animals
modify their (formerly adaptive) behaviour to adjust to the
new environmental challenges (Lima and Dill 1990; Brown
et al. 2006). Results of the twining vine study supported the
predictions from the SDP model for optimal anti-predation
behaviour under energy stress. Thus, in climbing vines (i.e.
low predation risk) anti-predator behaviour was reduced
and vine foraging was increased in the shade, while in
prostrate vines (i.e. high predation risk) both anti-predator
behaviour and vine foraging were greater in the shade
(Gianoli et al. 2007) (Fig. 1). Thi s analysis adds evidence
to the notion that theoretical frameworks from animal be-
havioural ecology may also apply to plants.
Optimalit y models based on economic decisions have
long been used to study animal foraging behaviour (Opti-
mal Foraging theory; Emlen 1966; MacArthur and Pianka
1966; Charnov 1976; Pyke 1984; Krebs and Davies 1993)
and may well be used to better understand climbing
plant behaviour. In fact, Darwin, after concluding that—
unlike tendrils—twining stems are not irr itable, pointed
outthatitwasnotexpected‘asnaturealwaysecono-
mizes her means, and irritability would have been super-
fluous’ (Darwin 1875); this alludes to an optimality
approach. The value of Darwin’s analogies between
plant strategies and economic concepts has been high-
lighted earlier (Drouin and Deroin 2010).
The rationale behind the economics of prey choice for
predators may be applied to climbing plants, with prey
≈ support, particularly focussing on the different modes
of attachment (Putz and Chai 1987; Carsten et al.2002;
Llorens and Leishman 2008; Carrasco-Ur ra and Gianoli
2009). Actual prey value, which drives prey choice under
an optimality approach, depends on the ratio between
the prey’s energy value (E
i
) and the associated handling
and s earch times (h
i
+ S
i
)(Krebs and Davies 1993). For
vines, the support’s energy value depends on ligh t har-
vest after attaining maximum height on it, and hence
could be roughly equated to tree height (Fig. 2). However,
actual energy gain may be influenced by other extrinsic
and intrinsic factors, such as canopy ope nness (det er-
mined by both the focus tree and the neighbouring
Figure 1. Anti-predator behaviour, measured as leaf alkaloid concen-
tration (¼ density of points), and foraging behaviour, measured as
internode length, in C. arvensis vines (Gianoli et al.2007). Experimen-
tal plants were subjected to a factorial array of light availability (sun
vs. shade) and support availability (climbing vs. prostrate vines). Field
data indicate that predation (herbivory) risk is much higher on pros-
trate vines. Results verified the hypothesis that vines should show re-
duced anti-predator behaviour and increased foraging in the shade
(fewer resources available). This agrees with animal-derived theory
that posits that individuals are more willing to take predation risks
during foraging when energetically stressed (Lima 1998).
6 AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
Gianoli — Behavioural ecology of vines
trees) and intrinsic features of the vine (only a fraction of
lianas reach the forest canopy, Putz 1980, 1984; Gerwing
2004). Handling time results in energy expenditure (Krebs
and Davies 1993), and in the case of vines it is associated
with the process of securing the attachment to the sup-
port. Handling time should increase with trellis diameter
(≈ lower ascent angle, Bell 1958; Putz and Holbrook 1991;
Scher et al. 2001) and vary with the degree of specializa-
tion of the climbing mechanism (Gentry 1991) (Fig. 2). For
instance, both grasping by tendrils (Jaffe and Galston
1968b; Ma and Yen 1989) and circumnutation plus normal
loads by stem twiners (Silk and Hubbard 1991; Stolarz
2009) are more ATP-consuming than the rather passive
mechanisms of leaning on hosts shown by scrambling
or hook climbers (Hegarty 1991; Isnard and Silk 2009).
Searching time will depend on the density of trellises in
a given habitat, taking into account that for some climb-
ing mechanisms (tendril-bearers, stem twiners) thick
supports are not suitable.
Interestingly, components of support value may trade-
off. Thus, thin supports may be easy to climb but result in
a short final height for the vine (low h andling time, low
energy value), while t hick sup ports may be hard to
climb but result in a tall final height (high handling
time, high energ y value) (Fig . 3). Exceptions to this
could be observed in those cases where vines ascend by
climbing older vines (i.e. relatively thin and tall supports)
(see Putz 1984). Trade-offs among components of
foraging, particularly among those with a known—or
assumed—relations hip with fitness (fitness currenc y,
Pyke 1984), are major constraints fo r the evolution of
adaptive foraging behaviour (Krebs and Davies 1993). A
more complex scenario may arise considering that fitness
currencies may vary with the climbing mechanism and/or
life history of vines. Thus, the premise that the energy value
of the support depends on light harvest after attaining
maximum height on it assumes that the plant aims at
maximizing growth and carbon gain. Howev er, field studies
have shown that some vine species prioritize growth rate
and carbon gain, while other species display traits enhan-
cing survival in low light (Gilbert et al. 2006; Valladares et al.
2011; Gianoli et al. 2012). Moreover, the species’ climbing
mechanism influences its photosynthetic acclimation and
abundance in contrasting light environments (Carter
and Teramura 1988; Teramura et al. 1991) such as those
found along the vertical light gradient in the forest.
All support’s components taken together (energy value,
handling time and search time) could lead to predictions of
‘favourite’ ecosystems for particular vine forms or species,
and forest types and/or successional stages appear as
good predictors of such differential suitability. There are
some general patterns described in the literature, such
as Durigon et al. (2014), but functional explanations are
wanting. For instance, root climbers are not constrained
by thick tree trunks (Putz and Holbrook 1991; Carrasco-Urra
and Gianoli 2009), often show an efficient searching strat-
egy for shaded habitats: skototropism (Hegarty 1991;
Figure 3. Components of support value ( prey profitability) for
climbing plants may show a trade-off because of the intrinsic asso-
ciation between tree diameter and tree height (dashed line). Thin
trees are easy to climb (low handling time) but result in short heights
(low energy value), while the opposite occurs for thick trees. Highest
and lowest support values are shown in blue and red, respectively.
Figure 2. The hypothetical optimal tree size for vines (tree size in-
cludes both tree diameter and height) should vary with the climbing
mechanism: tendril-bearers, stem twiners and root climbers. Benefits
( energy values) are assumed to increase with tree height because
light harvest by climbing plants increases with height; the curve is fur-
ther assumed to flatten out because most vines are not able to climb
up to the top of canopy trees. Costs ( handling times) increase with
tree diameter particularly for ten dril-bearers and stem twin ers be-
cause of biomechanical constraints: they fail to attach to thick trunks
(see text); root climbers are free from this constraint but costs are
assumed to increase slightly in very thick trunks—and hence old
trees—because of the expected greater competition with other
vines or epiphytes. Therefore, the optimal tree size, determined at
the maximum distance between the cost and benefit curves, should
be largest for root climbers and smallest for tendril-bearers.
AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
7
Gianoli — Behavioural ecology of vines
Lee and Richards 1991) , but their attachment to trees
should be challenged in open an d dry habitats because
adventitious roots may suffer desiccation at high irra-
diances (Carter and Teramura 1988; Teramura et al.
1991). Therefore, it was no surprise to find that, globally,
root climbers were more frequent in forests with greater
precipitation and reduced seasonality, and that increasing
temperature reduced root-climber occurrence in tropical
sites (Durigon et al.2013).
Concluding Remarks
Climbing plants account for a significant component of
plant evolution, diversity and abundance and play a
major role in forest communities and ecosystems (Putz
and Mooney 1991; Schnitzer and Bongers 2002; Gianoli
2004; Dura
´
n and Gianoli 2013; Schnit zer et al. 2015).
Mo reover, the relative abunda nc e of woody climbers is
increasing in tropical forests (Phillips et al. 2002; Schnitzer
and Bongers 2011) and several of the most aggressive in-
vasive plants worldwide are vines (Holm et al. 1991).
Therefore, from several different standpoints it is of para-
mount importance to understand the ecological fact ors
and physiological mechanisms that determine the vines’
successful use of neighbouring vegetation as support.
In this overview I have identified main issues of climb-
ing plant behaviour, most of them tracing back to Dar-
win’s seminal observations, which dese rve further
ecological inquiry. Other aspects of climbing plant behav-
iour, such as patterns of twining handedness (Darwin
1875; Edwards et al.2007; Burnham and Revilla-Minaya
2011) or support-finding benefits in des ert vines, which
grow in environments where light availability is not limit-
ing (Rundel and Franklin 1991; Krings 2000; Parsons
2006), still wait for ecological explanations.
I have shown that climbing plants are suitable study
subjects for the application of behavioural–ecological
theory. Optimality models are particularly useful because
they often provide testable, quantitative predictions
(Krebs and Davies 1993). Further research under this the-
oretical framework should aim at characterizi ng the dif-
ferent stages of the support-finding process (s earch
time, handling time) in terms of (i) their fit with the differ-
ent climbing modes and environmental settings and (ii)
their association with plant fitness. In particular, cost–
benefit analysis of climbing plant behaviour should be
helpful to infer the selective pressures that have operated
to shape current climber ecological commu nities (see
Rowe et al. 2004). This should be followed by phenotypic
selection analyses of field data and the determination of
the genetic basis of the key plant traits (e.g. Saldan
˜
a et al .
2007; Gianoli and Saldan
˜
a2013) in order to understand
their potential for evolutionary responses.
Sources of Funding
The study was supported by FONDECYT (Fondo Naciona l
de Desarrollo Cientı
´
fico y Tecnolo
´
gico—Chile) grant
1140070.
Conflicts of Interest Statement
None declared.
Acknowledgements
I thank J. C. Cahill for the invitation to contribute to this
special issue and F. E. Putz for thoughtful comments
that significantly improved an e ar li er version of the
manuscript.
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AoB PLANTS www.aobplants.oxfordjournals.org & The Authors 2015
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Gianoli — Behavioural ecology of vines
