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J.R. Milks, J. Hibbard, and T.P. Rooney
22001177 NORTHEASTERN NATURALIST 2V4(o4l). :2542,0 N–5o2. 54
Exfoliating Bark Does Not Protect Platanus occidentalis
From Root-climbing Lianas
James R. Milks1, Justin Hibbard1, and Thomas P. Rooney1,*
Abstract - Lianas are structural parasites that depress growth, fertility, and survival rates of
their hosts, but the magnitude to which they alter these rates differ among host species. We
tested the hypothesis that Platanus occidentalis (Sycamore) would have fewer adventitiousroot
climbing lianas than other tree species. We reasoned that because Sycamore possesses
exfoliating bark, it would periodically shed newly-established lianas from the trunk. We
investigated the distribution of lianas on the trunks of trees ≥10 cm DBH in floodplains in
southwestern Ohio. Contrary to our predictions, Sycamore trees had significantly more lianas
than expected at 3 of 5 sites, and significantly fewer than expected at 1 site. In contrast,
Acer negundo (Boxelder) had less than half the lianas expected. We find no support for our
hypothesis that bark exfoliation protects Sycamore trees from climbing lianas, and suggest
possible mechanisms that might protect Box Elder from adventiti ous-root climbing lianas.
Introduction
Lianas are woody vines that use tree hosts for structural support. They often
depress the growth, fertility, and survival rates of their hosts (Givnish 1992, 1995;
Ingwell et al. 2010; Ladwig and Meiners 2009; Stevens 1987; van der Heijden
and Phillips 2009). Tree species have evolved different mechanisms to decrease
the number of lianas that successfully become established on their trunks. These
mechanisms include trunk spines, guarding ants, flexible trunks, compound leaves,
long leaves, and high relative-growth rates (Givnish 1995; Putz 1980, 1984). Putz
(1984) reported higher liana mortality rates on trees with trunk spines. Guarding
ants have been observed removing lianas from host trees, e.g., Azteca ants living
in the hollow internodes of Cecropia trees (Janzen 1973, Putz 1980). When lianas
grow from one tree canopy to another, flexible trunks can facilitate dislodging the
connection when trees sway in opposite directions (Putz 1984). Lianas attached to
long leaves or compound leaves become dislodged as those leaves are shed (Putz
1980, 1984). Trees with high relative-growth rates are more effective in breaking
twining lianas than slower-growing trees (Putz 1980).
The few studies that have examined the role of bark shedding as a defense
against lianas (e.g. Carsten et al. 2002. Sfair et al. 2016, Talley et al. 1996a) have
been confined to tropical species. Bark shedding would be expected to protect
against liana infestation because lianas would be shed along with pieces of bark.
This mechanism should be especially effective against lianas that climb via adventitious
roots (hereafter, root-climbing lianas) because they attach to bark to climb.
1Department of Biological Sciences, Wright State University, Dayton, OH 45435. *Corresponding
author - thomas.rooney@wright.edu.
Manuscript Editor: Elizabeth N. Hane
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521
Talley et al. (1996a) noted that bark shedding reduced lianas in 2 species of Australian
rainforest trees. Carsten et al. (2002) found a more complex pattern—liana
densities increased at intermediate levels of bark shedding but decreased at higher
levels of shedding. Sfair et al. (2016) found that trees with exfoliating bark did not
have fewer lianas, but species with exfoliating bark combined with other anti-liana
mechanisms had fewer lianas.
Temperate floodplains in the eastern US are well suited for studying liana–
host relationships. Floodplain forests are subject to several factors that increase
liana abundance including disturbance through periodic flooding (van der
Heijden and Philips 2008) and forest fragmentation (Londré and Schnitzer 2006).
Floodplains are also the primary habitat of Platanus occidentalis L. (Sycamore),
a bark-shedding deciduous tree in the eastern US (Burns and Hon kala 1990). Although
bark-shedding has been hypothesized to protect Sycamores from lianas
(Givnish 1992, 1995), to our knowledge, no previous studies have tested this hypothesis
for Sycamore.
In this study, we tested the hypothesis that a temperate-zone bark-shedding tree,
Sycamore, would have fewer root-climbing lianas than co-occurring species that
do not shed bark. We counted the number of root-climbing lianas on tree trunks in
5 floodplain forests in southwestern Ohio, and we predicted that Sycamore would
have fewer lianas than expected compared to non-bark–shedding species.
Field-site Description
We conducted this study in mature floodplain forests at 5 different parks in
southwestern Ohio (39.7ºN, 84.1ºW): Germantown, Huffman Dam, Sugarcreek,
and Taylorsville Metroparks in Montgomery County, and The Narrows Preserve
in Greene County. Montgomery County parks occur within the Great Miami River
Watershed and The Narrows Preserve lies within the Little Miami River Watershed;
both drain into the Ohio River. All sites consist of mature, secondary forest. Their
origin dates to the 1910s when, following the Great Dayton Flood of 1913, land was
acquired for flood-control purposes (Morgan 1951). Forest cover extends less than 200 m
perpendicular to the river corridor at all sites. Land use in both watersheds is predominantly
cultivated cropland. Forest cover, pasture, and urban development are
also present. Both watersheds are located within the Till Plains region of Ohio. This
glaciated landscape contains rolling hills, moraines, and outwash plains (Zimmerman
and Runkle 2010).
Floodplain forests are comprised of mature deciduous species. Sycamore and
Boxelder were the dominant tree species at our study sites. The invasive shrub
Lonicera maackii (Rupr.) Herder (Amur Honeysuckle) is common in the forestshrub
layer (Hutchinson and Vankat 1998).
Methods
We recorded the diameter at breast height (DBH) and species of each tree ≥10
cm DBH in a single 10 m x 300 m belt transect (total 0.30 ha) in mature floodplain
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forests at each park, and considered each park as a separate site. We placed transects
randomly within the forests, but in most cases, they were within 50 m of forest
edges due to the narrow dimensions and fragmented nature of the floodplain forests
in this region.
We tallied the number of root-climbing lianas present on the trunk of each tree
at 1.6 m above ground level. We did not attempt to distinguish between separate
individuals. Instead, we counted the number of stems present in a band around the
tree at the1.6-m sampling height. We chose root-climbing lianas because we predicted
that they would be susceptible to being shed by trees with exfoliating bark.
We collected data in the spring for 2 field seasons (2007 and 200 8).
We determined mean (± SE) number of lianas per tree, importance values (IV),
and expected numbers of lianas per tree species for each site. We calculated importance
values for each tree species by adding the relative DBH and relative density
of each species, then dividing by 2 and multiplying by 100. We calculated relative
DBH by dividing total DBH for each species by total DBH for all trees per site and
relative density by totaling all individual stems per species and dividing by the total
number of individual stems per site.
If lianas were randomly distributed among trees, we would expect the number
of lianas per tree species to be distributed in proportion to the IV of each tree species.
Importance values incorporate both the age/size and density; thus, tree species
with higher IVs would host more lianas than tree species with smaller IVs due to
increased surface area to which lianas could attach (Buron et al. 1998, Carsten et
al. 2002, Leicht-Young, et al. 2010, Reddy and Parthasarathy 2006, Talley et al.
1996a). We calculated the expected number of lianas per tree species as the product
of the number of lianas at a site and the tree species IV at the site, divided by 100.
We employed replicated goodness-of-fit (G) tests with Williams correction
for continuity to analyze differences between observed and expected lianas per
tree species of the 2 species with the highest IV, Sycamore and Acer negundo L.
(Box Elder), with each site considered a replicate (Sokal and Rohlf 1981). Calculations
were performed in Microsoft Excel 2008 for Mac and validated using
manual calculations.
Results
We measured 1145 trees comprising 18 species and counted 1417 root-climbing
lianas (mostly Toxicodendron radicans (L.) Kuntze [Poison Ivy] and a few Parthenocissus
quinquefolia (L.) Planch.) [Virginia Creeper]) in a total of 1.5 ha. Of the
18 tree species encountered, Sycamore and Box Elder had the highest IVs: 31.2 and
25.6, respectively. The remaining 16 species had a combined IV of 43.2.
We found 568 lianas (40.0%) growing on Sycamore. This number was significantly
greater than expected at 3 of 5 sites, significantly less at 1 site, and did not
differ from expected abundance at the remaining site (Table 1). When we pooled
the data across sites, Sycamore had 33% more root-climbing lianas than expected
(pooled G = 20.5, df = 1, P < 0.001). In contrast, we found only 142 (10.0%) lianas
on Boxelder, which had significantly fewer lianas than expected at 3 sites and
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did not differ from expected abundance at 2 sites (Table 1). When we pooled data
across sites, Box Elder had 55% fewer root-climbing lianas than expected (pooled
G = 67.7, df = 1, P < 0.001).
Discussion
We found no support from our data for the hypothesis that bark-shedding
protects Sycamore from root-climbing lianas. Sycamores had either the same as
or more than the expected number of lianas at 4 sites out of 5 sites, whereas we
predicted that the species would have fewer than expected lianas. This result contrasts
with Talley et al. (1996a), who found that bark-shedding trees in Queensland,
Australia, tropical forests had fewer than expected root-climbing lianas. Carsten et
al. (2002) found that root-climbing lianas increased on trees with intermediate bark
roughness and levels of bark-shedding and decreased at high levels of shedding and
on trees with smooth bark. It is possible that Sycamore falls within the intermediate
range of the bark-texture scale of Carsten et al. (2002). One possible test would be
to compare individual Sycamore trees for differences in bark-shedding levels and
liana loads because individual Sycamores vary in levels of bark shedding, with
some trees shedding nearly all bark and others shedding very little (J.R. Milks,
pers. observ.). Alternatively, exfoliating bark alone may be an ineffective anti-liana
mechanism (Sfair et al. 2016).
In contrast to Sycamore, Boxelder had either the expected number of lianas or
significantly fewer lianas than expected. Other studies have also noted fewer than
expected lianas on the closely related Acer saccharum Marsh. (Sugar Maple). Both
Talley et al. (1996b) and Leicht-Young et al. (2010) found fewer than expected
Poison Ivy lianas on Sugar Maple in forests in Alabama, Indiana, and Michigan.
Possible reasons for the differences between liana abundance between Sycamore
and Boxelder include leaf size, bark morphology, and bark chemistry. Putz
Table 1. Number of tree stems, importance values (IV) per species per site, observed liana abundance,
expected liana abundance, and G-values for goodness of fit. For G-values, ns = not significant, *P less than
0.05, **P < 0.005.
Observed # Expected #
Species/site # of stems IV per site of lianas of lianas G-value
Acer negundo (Box Elder)
Germantown 120 58.4 11 13.4 1.0 ns
Huffman 94 26.8 44 169.7 163.8**
Narrows 88 20.6 75 108.4 14.5**
Sugarcreek 6 4.2 0 7.1 14.4**
Taylorsville 38 14.3 12 18.3 2.7 ns
Platanus occidentalis (Sycamore)
Germantown 24 18.3 5 4.2 0.2 ns
Huffman 36 18.0 143 114.0 8.5**
Narrows 105 37.8 269 175.0 77.9**
Sugarcreek 50 46.7 127 79.4 55.1**
Taylorsville 77 41.0 24 52.5 28.9**
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(1984) found that trees with leaves >50 cm in length protected trees from lianas on
Barro Colorado Island, Panama. Plants that shed such large leaves are more likely
to dislodge attached lianas, compared to plants with smaller leaves (Putz 1984).
Although Sycamore generally has larger leaves than Boxelder, most are less than 25 cm
in length, making leaf size an unlikely mechanism of liana shedding in eastern
temperate-floodplain forests. Bark morphology (smooth versus furrowed) is also
unlikely to be an important mechanism, because this factor has been tested in other
forest types with mixed results (Boom and Mori 1982, Carsten et al. 2002). In our
study, Boxelder had slightly furrowed bark. Bark morphology by itself is unlikely
to explain our results, although it warrants further study.
One unexplored possibility is that allelopathic chemicals in the bark of some
maple species may protect them from root-climbing lianas. Talley et al. (1996b)
found that allelopathic chemicals in Sugar Maple bark (as well as chemicals in the
bark of other tree species) could inhibit liana seedling germination and growth in
the southern US, and differences in the presence of allelopathic chemicals influenced
liana distribution on host trees. Talley et al. (1996a) found similar patterns
in Australia. It is possible that bark chemistry may also protect maple species from
clinging lianas, although our study did not investigate that possibility.
This study is, to our knowledge, the first to demonstrate that bark shedding in
Sycamore does not protect that species from liana infestation. We also showed that
Boxelder has either the same or fewer than expected number of lianas, which is also
a new finding. Future investigations could examine host preferences for different
species of lianas in temperate floodplains, and whether variability in bark shedding
among individual Sycamore individuals affects liana loads.
Acknowledgments
The idea for this project was first suggested by T. Givnish. We thank Mike Bottomley
for statistical consulting, and 2 reviewers for constructive comments in an early draft of
this manuscript. Raw data from this study can be accessed at https://figshare.com/articles/
VineShedding_SW_Ohio_csv/3125773.
Literature Cited
Boom, B.M., and S.A. Mori. 1982. Falsification of 2 hypotheses on liana exclusion from
tropical trees possessing buttresses and smooth bark. Bulletin of the Torrey Botanical
Club 109:447–450.
Burns, R.M., and B.H. Honkala. 1990. Silvics of North America: 2. Hardwoods. Agriculture
Handbook 654. US Department of Agriculture Forest Service, Washington, DC.
877 pp.
Buron, J., D. Lavigne, K. Grote, R. Takis, and O. Sholes. 1998. Association of vines and
trees in second-growth forest. Northeastern Naturalist 5:359–36 2.
Carsten, L.D., F. A. Juola, T.D. Male, and S. Cherry. 2002. Host associations of lianas in a
southeast Queensland rainforest. Journal of Tropical Ecology 18:107–120.
Givnish, T.J. 1992. Nature green in leaf and tendril. Science 256:1339–13 41.
Givnish, T.J. 1995. Plant stems: Biomechanical adaptation for energy capture and influence
on species distributions. Pp.. 3–49, In B.L. Gartner (Ed.). Plant Stems: Physiology and
Functional Morphology. Academic Press, San Diego, CA. 460 pp.
Northeastern Naturalist Vol. 24, No. 4
J.R. Milks, J. Hibbard, and T.P. Rooney
2017
525
Hutchinson, T.F., and J.L. Vankat. 1998. Landscape structure and spread of the exotic shrub
Lonicera maackii (Amur Honeysuckle) in southwestern Ohio forests. American Midland
Naturalist 139:383–390.
Ingwell, L.L., S.J. Wright, K.K. Becklund, S.P. Hubbell, and S.A. Schnitzer. 2010. The
impact of lianas on 10 years of tree growth and mortality on Barro Colorado Island,
Panama. Journal of Ecology 98:879–887.
Janzen, D.H. 1973. Dissolution of mutualism between Cecropia and its Azteca ants. Biotropica
5:15–28.
Ladwig, L.M., and S.J. Meiners. 2009. Impacts of temperate lianas on tree growth in young
deciduous forests. Forest Ecology and Management 259:195–200.
Leicht-Young, S.A., N.B. Pavlovic, K.J. Frohnapple, and R. Grundel. 2010. Liana habitat
and host preferences in northern temperate forests. Forest Ecology and Management
260:1467–1477.
Londré, R.A., and S.A. Schnitzer. 2006. The distribution of lianas and their change in abundance
in temperate forests over the past 45 years. Ecology 87:2 973–2978.
Morgan, A.E. 1951. The Miami Conservancy District. McGraw-Hill, New York, NY. 504 pp.
Putz, F.E. 1980. Lianas vs. trees. Biotropica 12:224–225.
Putz, F.E. 1984. How trees avoid and shed lianas. Biotropica 16:19–23.
Reddy, M.S., and N. Parthasarathy. 2006. Liana diversity and distribution on host trees in 4
inland tropical dry evergreen forests of peninsular India. Tropical Ecology 47:109–123.
Sfair, J.C., A.L.C. Rochelle, A.A. Rezende, J. van Melis, R.J. Burnham, V. de L. Weiser, and
F.R. Martins. 2016. Liana avoidance strategies in trees: Combined attributes increase
efficiency. Tropical Ecology 57:559–566.
Sokal, R.R., and F.J. Rohlf. 1981. Biometry, 2nd Edition. W.H. Freeman and Company, New
York, NY. 859 pp.
Stevens, G.C. 1987. Lianas as structural parasites: The Bursera simaruba example. Ecology
68:77–81.
Talley, S.M., W.N. Setzer, and B.R. Jackes. 1996a. Host associations of 2 adventitiousroot–
climbing vines in a north Queensland tropical rain forest. Biotropica 28:361–366.
Talley, S.M., R.O. Lawton, and W. N. Setzer. 1996b. Host preferences of Rhus radicans
(Anacardiaceae) in a southern deciduous hardwood forest. Ecolog y 77:1271–1276.
Van der Heijden, G.M.F,. and O.L. Phillips. 2008. What controls liana success in Neotropical
forests? Global Ecology and Biogeography 17:373–383.
Van der Heijden, G.M.F. and O.L. Phillips. 2009. Liana infestation impacts tree growth in
a lowland tropical moist forest. Biogeosciences 6:2217–2226.
Zimmerman, C.L., and J.R. Runkle. 2010. Using ecological land units for conservation
planning in a southwestern Ohio watershed. Natural Areas Journal 30:27–38.