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In this study, we describe for the first time facultative hemiepiphytism in Cecropia pachystachya Trécul growing on palms in the “Pantanal” wetland of Brazil and investigate ecological factors associated with this unexpected phenomenon. We sampled C. pachystachya seeds lodged in palm stems and recorded the seed rain to low stems, high stems and to the ground below and away from palms. We also tested seed germination on soil and stem substrates and measured the chemical composition of both substrates. Compared to freestanding conspecifics, hemiepiphytes of C. pachystachya were rare and displayed wider trunks but similar height. All hemiepiphytes were fixed on low stems by aerial roots encircling the palms and coalesced branches rooted into the ground. Most palm stems contained C. pachystachya seeds but a few concentrated seeds massively. Dispersal of seeds was 15 times greater to lower than higher portions of stems, and seven times higher below palms than elsewhere. Germination rates of C. pachystachya seeds did not differ between soil and stem substrates. The clayey stem substrate presented more Zn, K, P, Ca, Mg and Al than the sandy soil, which in turn presented more Fe and Cu. The exceptional occurrence of C. pachystachya as a facultative hemiepiphyte in the “Pantanal” wetland results from massive seed rain to lower regions of palm stems, where germination, mechanical stability and access to nutrients are conducive to establishment and subsequent growth. However, the rarity of hemiepiphytism in C. pachystachya indicates that opportunities for successful establishment rely on a combination of uncertain spatiotemporal conditions.
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Bizarre Cecropia pachystachya (Urticaceae) hemiepiphytic growth
on palms in the ‘‘Pantanal’’ wetland
Christiane E. Corre
Erich Fischer
Received: 25 August 2016 / Accepted: 21 November 2016
Botanical Society of Sao Paulo 2016
Abstract In this study, we describe for the first time fac-
ultative hemiepiphytism in Cecropia pachystachya Tre
growing on palms in the ‘‘Pantanal’’ wetland of Brazil and
investigate ecological factors associated with this unex-
pected phenomenon. We sampled C. pachystachya seeds
lodged in palm stems and recorded the seed rain to low
stems, high stems and to the ground below and away from
palms. We also tested seed germination on soil and stem
substrates and measured the chemical composition of both
substrates. Compared to freestanding conspecifics,
hemiepiphytes of C. pachystachya were rare and displayed
wider trunks but similar height. All hemiepiphytes were
fixed on low stems by aerial roots encircling the palms and
coalesced branches rooted into the ground. Most palm
stems contained C. pachystachya seeds but a few concen-
trated seeds massively. Dispersal of seeds was 15 times
greater to lower than higher portions of stems, and seven
times higher below palms than elsewhere. Germination
rates of C. pachystachya seeds did not differ between soil
and stem substrates. The clayey stem substrate presented
more Zn, K, P, Ca, Mg and Al than the sandy soil, which in
turn presented more Fe and Cu. The exceptional occurrence
of C. pachystachya as a facultative hemiepiphyte in the
‘Pantanal’’ wetland results from massive seed rain to lower
regions of palm stems, where germination, mechanical
stability and access to nutrients are conducive to estab-
lishment and subsequent growth. However, the rarity of
hemiepiphytism in C. pachystachya indicates that oppor-
tunities for successful establishment rely on a combination
of uncertain spatiotemporal conditions.
Keywords Aerial roots Attalea phalerata Bat dispersal
Hemiepiphytes Soil composition
Accumulation of litter and sediment on vegetation struc-
tures may provide microsites for seed deposition and
growth of a variety of other plants, resulting in the evo-
lution of different epiphytic life forms (Benzing 1990;
Nadkarni and Haber 2009; Hao et al. 2010,2011; Corre
et al. 2012). Hemiepiphytism has evolved on multiple
occasions in several angiosperm families, markedly in
Moraceae and Clusiaceae tropical trees (Nadkarni et al.
2001; Wanek et al. 2002). Hemiepiphytes germinate on
other plants (phorophytes) and have no access to the
ground during early growth, deriving water and nutrients
only from the host plant substratum at this stage (Zotz
2013). Aerial roots initially encircle the phorophyte, pro-
viding essential fixation and feeding, and then grow
downward to the soil. Hemiepiphytes may become free-
standing after coalescence of numerous aerial roots and
phorophyte decay. Therefore, availability of water and
nutrients on phorophyte substratum is critical for the initial
establishment of hemiepiphytes, and abundance of suit-
able host plants may limit them. In addition, the success of
Electronic supplementary material The online version of this
article (doi:10.1007/s40415-016-0339-y) contains supplementary
material, which is available to authorized users.
&Christiane E. Corre
Programa de Po
˜o em Ecologia e Conservac¸a
Universidade Federal de Mato Grosso do Sul,
Campo Grande, Mato Grosso do Sul 79070-900, Brazil
Centro de Cie
ˆncias Biolo
´gicas e da Sau
´de, Universidade
Federal de Mato Grosso do Sul, Campo Grande,
Mato Grosso do Sul 79070-900, Brazil
Braz. J. Bot
DOI 10.1007/s40415-016-0339-y
the hemiepiphytic growth form depends on consistent
interactions with seed dispersers to attain appropriate
phorophytes. In general, hemiepiphytic tree species show
effective seed dispersal through zoochoric diaspores
swallowed and defecated by vertebrates, but also by sec-
ondary dispersal by ants (Kaufmann et al. 1991; Passos and
Oliveira 2002; Teixeira et al. 2009; Munin et al. 2011).
Cecropia Loefl. (Urticaceae) is a conspicuous Neotrop-
ical genus of pioneer trees originated in northern Andean
regions of Colombia and Ecuador (Berg et al. 2005). Spe-
cies of Cecropia can occur densely in large second-growth
areas or scattered in treefall gaps of old-growth forests, in
different habitats from wet to dry (Parolin 2002; Damas-
ceno Ju
´nior et al. 2004; Faxina et al. 2015). The presence of
adventitious roots is common in the genus and these can
function for aeration and mechanical support, especially for
individuals growing in swamps (Barlow 1986; Berg et al.
2005; Parolin et al. 2010). Cecropia obtusifolia Bertol. in
Colombia is an extraordinary reported case, as its roots
grow toward the nutrient-rich crown centre of nearby palms
and tightly encircle their stems and petioles often killing the
palms in manner similar to the behaviour of hemiepiphytic
strangler figs (Bernal and Balslev 1996). However, to the
best of our knowledge, the hemiepiphytic growth has not
been described for species of Cecropia (Gentry 1993; Berg
et al. 2005). Here, we describe the occurrence of facultative
hemiepiphytism in Cecropia pachystachya Tre
´cul on At-
talea phalerata Mart. ex Spreng. palms in the ‘‘Pantanal’
wetland of Brazil. Aside from reporting this phenomenon
for the first time, we also addressed its magnitude in the
local population and evaluated some critical ecological
factors that could allow its occurrence. To address the
magnitude, we asked how frequent and large hemiepiphytic
individuals of C. pachystachya are, compared to free-
standing conspecifics. With regard to ecological factors, we
assessed whether seed arrival and germination differ
between forest ground and palm stems, and whether avail-
able nutrients differ between forest soil and sediment
accumulated on palm stems.
Study site and species
We sampled C. pachystachya in forest patches (0.5–5 ha) in
the ‘‘Pantanal’’ floodplain, region of Miranda (19340S,
57010W), Southern Mato Grosso do Sul State, Brazil. The
‘Pantanal’’ is a major world wetland (160,000 km
) in the
centre of South America that includes the upper Paraguay
River basin (Almeida et al. 2015). Climate is classified as Aw
of Ko
¨ppen (Peel et al. 2007), with a marked dry season from
April to September and a rainy season from October to
March. Annual rainfall varies between years, from 800 to
1400 mm. Seasonal flood pulses alternate with severe
drought periods, and the landscape is mainly composed of
fields, temporary or permanent lakes, channels, riparian
forests and forest patches on slightly elevated terrains
(Almeida et al. 2015). Inundation intensity varies between
years and zones, from three to six months in length and from
one to four metres in depth (Moura
˜o et al. 2013; Cunha et al.
2014). The spatiotemporal heterogeneity of the wetland and
the influence of different surrounding vegetation types—
mainly ‘‘Cerrado’’, Chaco, Amazon and Atlantic Forest—
support a distinctive and rich biodiversity in the ‘‘Pantanal’
(Pott and Pott 1994; Alho et al. 2011; Moura
˜o et al. 2013).
Cecropia pachystachya is a dioecious tree widely dis-
tributed from southern Amazon to northern Argentina
(Berg et al. 2005), and an important invader in Southeast
Asia (Raphael et al. 2015). It is the only Cecropia in the
‘Pantanal’’ floodplain out of five congeners reported in the
surrounding uplands (Pott and Pott 1994). Flowering and
fruiting are year round, but most trees fruit during the wet
rather than in the dry season. Seeds are endozoochorous
dispersed by vertebrates, markedly bats at our study site
(Gonc¸alves et al. 2007; Teixeira et al. 2009). Seeds gen-
erally have high longevity and commonly form seed banks
in forests (Dalling et al. 1998). Cecropia pachystachya
tolerates flooding, depending on plant maturity (height) and
the duration of waterlogging (Damasceno Ju
´nior et al.
2004; Faxina et al. 2015). Seeds that are submerged up to
30–45 days germinate faster, but germination ability
decreases after longer submersion (C. Corre
ˆa and E. Fis-
cher, unpublished data). Individuals growing under flooded
condition exhibit lower photosynthetic rates, slower growth
and an increased number of stilt roots and lenticels than
those in unflooded condition (Batista et al. 2008).
Attalea phalerata (Arecaceae) is the commonest of nine
palm trees in the ‘‘Pantanal’’ (Pott and Pott 1994). Indi-
viduals occur sparsely inside forests and often densely
along forest borders, which are subject to longer and deeper
flood durations than forest interiors. Leaves have smooth
petioles with broad and invaginate sheaths joined at the
stem apex. Sheaths of dead leaves are persistent and cover
the entire stem, providing numerous microsites for the
deposition of sediment and organic material. Attalea
phalerata stems possess 70–500 persistent sheaths
depending on stem length (0.8–4.0 m) (Corre
ˆa et al. 2012).
It is the main host plant used by obligate hemiepiphyte figs
in the ‘‘Pantanal’’.
Data collection and analyses
To assess the proportion of C. pachystachya individuals
established on palm stems, we sampled all adult trees and
all palms in 1.9 ha of forests. Trees taller than 4 m were
C. E. Corre
ˆa, E. Fischer
considered adults, as this is approximately the minimal
height of flowering C. pachystachya. In addition, palm
individuals were inspected for the presence of seedlings or
juveniles of C. pachystachya. We also measured the height
(to ±0.1 m) and trunk diameter (to ±0.1 cm) at 1.3 m
height of all hemiepiphytic individuals and their nearest
freestanding conspecific. To evaluate the seed bank of C.
pachystachya in persistent sheaths of A. phalerata, and the
vertical distribution of seeds deposited along palm stems,
we extracted data from Corre
ˆa et al. (2012). They consisted
of the number of C. pachystachya seeds sampled in five
persistent sheaths below 1.5 m plus five sheaths above
1.5 m from 64 stems at our study site.
To evaluate the dispersal of C. pachystachya seeds (seed
rain) to palm stems and to the forest ground, we used seed
traps consisting of half-cylinders of PVC with 20 cm depth
and semicircular openings of 10 cm radius (314 cm
). The
shape and dimension of seed traps allowed their physical
attachment to palm stems and thus the simulation of an
enlarged persistent sheath (Fig. 1 in Supplementary mate-
rial). We perforated the traps at the bottom and internally
lined them with tissue to retain seeds and allow passage of
rainwater. At the beginning of rainy season (October), we
set up 24 blocks of four treatments among 24 forest patches
at least 150 m apart from each other. In each forest patch,
we haphazardly selected three individuals of A.phalerata
(C3 m tall) at least 50 m apart. We then attached one trap
to a high stem ([1.5 m) of the first palm (Fig. 1 in Sup-
plementary material) followed by one trap to a low stem
(*0.5 m) of the second palm (Fig. 2 in Supplementary
material), and a third trap was partly buried in forest
ground below the canopy of the third palm (Fig. 3 in
Supplementary material). In addition, in each forest patch,
a fourth seed trap was buried 2–5 m away from palm
canopies, at least 50 m distant from other traps. The
openings of ground traps were 10 cm above the surface of
the soil to avoid trapping adjacent material. We installed 96
seed traps in total, four per forest patch, but peccaries and
cattle removed eight ground traps before samples could be
collected. Thus, the final number of traps was 88, of which
24 fixed in high stems, 24 in low stems, 20 on ground
below palm canopies and 20 on ground apart from palms.
We collected all trapped material three times, in Novem-
ber, January and March, in order to avoid decreasing of
trap efficiency due to initial accumulation of material and
to cover the wet season when most fruiting trees occur. The
collected material was initially stored in paper bags and
then inspected in laboratory for counting of C.pachys-
tachya seeds.
For two different purposes, investigating available
nutrients in substrates and conducting experiments of seed
germination, we collected eight samples of 500 g of forest
soil (5 cm depth) and eight samples of 500 g of sheath
sediment, in eight forest patches. Samples of sediment
were from one palm per forest patch and samples of soil
were collected 50 cm away from the palms. For the ger-
mination experiment, we subsampled 50 g out of each
500 g sample and mixed the subsamples of the same type,
giving 400 g of each substrate assembled from eight forest
patches. We then separated 200 g of soil and 200 g of
sediment and washed them in slow-running clean water for
2 min in order to reduce the possibility of potential inhi-
bitors of germination. The washed substrates were then
placed in trays for atmospheric drying for two days, as well
as the remaining non-washed part of both substrates. In
each tray containing a different treatment—washed soil,
washed sediment, non-washed soil and non-washed sedi-
ment—we spread 200 intact seeds of C. pachystachya
randomly selected among seeds trapped in the field and
inspected trays daily to record germinated seeds during
40 days on a glasshouse bench. All treatments were equally
watered with substrates kept near field capacity. The
remaining soil and sediment samples from the eight forest
patches were individually sent for chemical–physical
analyses carried out by Age
ˆncia Estadual de Defesa Sani-
´ria Animal e Vegetal (IAGRO) (cf. Anonymous 1997).
Measured substrate traits included texture, proportion of
organic matter, pH, exchangeable quantities of Al and
quantities of essential macronutrients (P, K, Ca, Mg) and
micronutrients (Fe, Mn, Cu, Zn).
To test for differences in mean height and diameter
between hemiepiphytic and ground-established trees of C.
pachystachya, we used the student’s ttest. To test for
differences in the frequency of C. pachystachya seeds in
palm seed banks between high ([1.5 m) and low (\1.5 m)
stem height classes, we used the Chi-squared test of equal
frequencies. The same test was used for the evaluation of
differences of seed frequency among seed trap treatments
in the field and for differences among germination treat-
ments. To evaluate the similarity of chemical composition
between substrates, we used principal component analysis
(PCA) based on standardized values of pH, Al and eight
Hemiepiphytic growth
In 1.9 ha of semideciduous forest, we recorded seven
hemiepiphytes (3.7 ind ha
) and 134 freestanding
(70.5 ind ha
) trees of C. pachystachya, plus 153 indi-
viduals of A. phalerata (80.5 ind ha
) free of hemiepi-
phytes. We found no seedlings or juveniles of C.
pachystachya growing on palm stems and did not survey
them among ground-established plants. At least four
Bizarre Cecropia pachystachya (Urticaceae) hemiepiphytic growth on palms in the ‘‘Pantanal’
hemiepiphytes of C. pachystachya were females as they
presented infructescences. Trunk diameter was larger
(P\0.001, t=7.86, df =6) for hemiepiphytes than
ground-established conspecifics (38.9 ±9.43 cm, n=7,
and 22.8 ±6.48 cm, n=7, respectively), but height did
not differ (P=0.69, t=-0.42, df =6) between them
(8.8 ±1.11 m, n=7, and 8.9 ±0.84 m, n=7, respec-
tively). All individuals of C. pachystachya found as
hemiepiphytes started growth on low (\1.5 m) stems of A.
phalerata (Figs. 13). Several tiny roots of these individ-
uals developed horizontally around palm stems within the
remaining sheaths, in contrast to stilt roots that grow
obliquely downwards in freestanding C. pachystachya
trees. In addition to tiny roots around stems, other root
branches were geotropically oriented, coalesced and pro-
vided a strong functional link to the ground at the opposite
side that the plants were fixed to the palms (Figs. 13). All
aerial roots of C. pachystachya hemiepiphytes departed
from their low trunks that, in turn, were extensively free
upward and usually inclined in relation to the A. phalerata
stems; canopies of all C. pachystachya hemiepiphytes
surpassed those of their phorophytes in their height.
Seed bank and seed rain
Most A. phalerata stems (84%; 54/64) contained seeds of
C. pachystachya deposited on at least one out of 10 per-
sistent sheaths. In total, 1594 seeds were recovered from all
stems and these were distributed among 480 (75%) of the
640 persistent sheaths sampled. In spite of such a wide
occurrence of seeds among stems and among persistent
sheaths, few palm individuals concentrated seeds mas-
sively (Fig. 2). Among the 64 palm stems, the frequency of
C. pachystachya seeds did not differ (P=0.10, Yates’
corrected Chi squared =2.71) between high (n=671)
and low (n=923) stems, but extremely high seed abun-
dances occurred only on low stems (Fig. 4).
During seed trapping in the field, we recorded 3354
seeds of C. pachystachya among 88 seed traps, a general
frequency of more than 38 seeds per trap. Seven traps
contained 3122 seeds and the remaining traps had only 232
seeds, a pattern similar to the distribution of C. pachys-
tachya seeds among palm stems. Differential dispersal of
seeds among traps was consistent throughout the three
sampling dates, as those traps with more seeds at the first
Figs. 1–3. 1 Hemiepiphyte
Cecropia pachystachya tree on
(*7 m height) Attalea
phalerata palm (*4 m height)
in the ‘‘Pantanal’’ wetland,
Brazil. 2,3Aerial roots of the
tree involved the low stem,
coalesced and fixed to the
ground at the opposite side
C. E. Corre
ˆa, E. Fischer
inspection continued trapping increased number of seeds in
the second and third inspections. The frequency of trapped
seeds differed among treatments (Fig. 5) and was 15 times
higher in traps attached to low than to high A. phalerata
stems (97.5 and 6.1 seeds per trap, respectively), and seven
times higher in ground traps below palm canopies than in
ground traps away from palm plants (37.9 and 5.4 seeds per
trap, respectively).
Seed germination and substrate compositions
During 40 days of the glasshouse experiment, 420 out of
800 (52.5%) C. pachystachya seeds germinated. The fre-
quency of germination was higher (P\0.0001, v
on previously washed substrates (90% on soil and 70% on
stem sediment) than on non-washed substrates (25% on soil
and 26% on stem sediment), but the frequency of germi-
nation did not differ between soil and stem sediment
(Fig. 6). Germination started earlier on washed than non-
washed substrates with the frequency after 13 days on
washed substrates being similar to the frequency after
30 days on non-washed substrates (Fig. 6).
Chemical–physical traits differed between forest soil
and sediment from A. phalerata stems mainly due to dif-
ferences of pH, Zn, Cu and Fe, as evidenced through
loadings on PCA Component 1 (Fig. 7; Table 1). Forest
soil was sandy and presented neutral pH and less organic
matter than the clayey and moderately acid palm stem
sediment (Table 1). Compared to forest soil, stem sediment
showed one order of magnitude more Zn, almost five times
more K and two times more P, Ca, Mg and Al. The
amounts of Mn were approximately similar between the
substrates. Only Fe and Cu were proportionally more
abundant in forest soil, with the former being five times
higher in soil than in stem sediment. In addition to these
major differences between substrates, there was consider-
able variation among forest patches (samples) for the same
substrate, mainly due to differences of pH, Al and Mn
(Fig. 7; Table 1).
Our results show that C. pachystachya can grow as
hemiepiphytes in the ‘‘Pantanal’’ region of Brazil, a phe-
nomenon unreported for Cecropia but common for Cous-
sapoa Aubl. in the tribe Cecropieae (Berg et al. 1990).
Hemiepiphytes of C. pachystachya, however, were rare as
they accounted for only 5% of adult trees even though A.
phalerata phorophytes were common at the sites we sam-
pled. Furthermore, hemiepiphytic growth of C. pachys-
tachya is unusual because only the base of each tree is fixed
to palm stems. This contrasts with obligate hemiepiphytes
that firmly attach through numerous roots to their phoro-
phytes (Lo
´pez-Acosta and Dirzo 2015). Aerial roots of C.
pachystachya do not depart from branches or along trunk
extension as occurs in true hemiepiphytes (Harrison 2006;
Hao et al. 2011; Jim 2014). Therefore, the presence of
aerial roots in C. pachystachya normally adapted to
Fig. 4 Distributions of Cecropia pachystachya seed abundances on
high (a) and low (b) stems of Attalea phalerata palms in the
‘Pantanal’’ wetland, Brazil
Fig. 5 Frequency of Cecropia pachystachya seeds trapped in four
microhabitats: high on Attalea phalerata palm stems (high stem), low
on palm stems (low stem), on the ground below palm canopies (below
canopy) and on the ground out of palm canopy projections (outside
canopy), in the ‘‘Pantanal’’ wetland, Brazil. Different letters above
bars indicate significant (P\0.01) difference of seed arrival
frequencies (v
Bizarre Cecropia pachystachya (Urticaceae) hemiepiphytic growth on palms in the ‘‘Pantanal’
temporary flooding (Sposito and Santos 2001; Parolin et al.
2010) served the function of attaching the trees to palms.
The numerous coalescent roots in most hemiepiphytes
differ from typical freestanding C. pachystachya. If such
variation has a genetic basis, then only part of the popu-
lation may be able to grow on phorophytes.
Gravitational destabilization may also contribute to the
rarity of hemiepiphytes and we noted two unsuccessful
cases in our study region. One C. pachystachya tree had
fallen along with the host palm because the palm stem
broke at its base, and another had fallen alone and exhib-
ited roots partially detached from the palm. Such instability
can intensify if the height of attachment of C. pachystachya
on the palm stem increases, and thus it may constrain the
hemiepiphytes to lower palm stems. Individuals fixed to
low stems can root into the ground early and develop
strong coalesced roots that provide gravitational compen-
sation force at the opposite side of attachment to palm stem
(Soethe et al. 2006). In spite of the rarity and unusual
growth of C. pachystachya hemiepiphytes, they exhibited
heights similar to and trunk diameter larger than free-
standing conspecifics, indicating that hemiepiphytes are as
vigorous as or even more vigorous than ground-established
trees. Cecropia pachystachya decreases photosynthetic
rates during the floods (Batista et al. 2008) and hemiepi-
phytism reduces the time that trees are exposed to inun-
dation, which could favour more vigour.
Cecropia pachystachya forms a remarkable seed bank
on the stems of A. phalerata in the ‘‘Pantanal’’, as
demonstrated by the presence of seeds in more than 80% of
the surveyed stems. Indeed, C. pachystachya is the most
abundant of the 75 species that occur as seeds on A.
phalerata stems at the study site, including hemiepiphyte
figs (Corre
ˆa et al. 2012). Thus, the widespread occurrence
and heavy accumulation of C. pachystachya seeds create
plenty of opportunities for seedlings to establish on A.
phalerata in the ‘‘Pantanal’’. As the frequency of C.
pachystachya seeds in palm seed banks did not differ sig-
nificantly between high and low palm stems, the height of
seeds does not seem to prevent the occurrence of individ-
uals fixed at high stems, as strangler figs do (Harrison
2006; Jim 2014). However, the frequency of C. pachys-
tachya seed dispersal to traps was nearly two orders of
magnitude higher in low than high stems. This indicates
that the primary dispersers deposit seeds to a much greater
extent to low than high stems. Since seed frequency in low
and high stems differed in seed rain but not in their seed
bank, secondary dispersers are likely carrying seeds
upward along stems or removing seeds predominantly from
low stem to elsewhere. Ants may carry seeds upward or
away from palms, and flooding pulses may remove seeds
from low stems (Passos and Oliveira 2002; Corre
ˆa et al.
2012). On the other hand, the pattern of distribution of C.
pachystachya seeds among palm individuals was similar
between the seed rain and seed bank. Most seeds were
concentrated in a few palm individuals, while many palms
had a small number of seeds. This pattern may contribute
to the rarity of C. pachystachya hemiepiphytes if the
chance of growing on a palm depends largely on whether
massive amounts of seeds are present. Furthermore, if
germination proves to be higher among newly than old
Fig. 6 Accumulated number of Cecropia pachystachya seeds that
germinated in greenhouse during 30 days of tests on two substrates
(forest soil or sediment accumulated on sheaths along Attalea
phalerata stems), each one in two situations (natural or washed in
slow-running water prior to the tests). Significant (P\0.0001)
differences of germination frequencies occurred only between washed
and natural treatments, irrespective of whether on soil or stem
sediment (v
Fig. 7 Principal component analysis and 95% confidence ellipses for
the chemical composition (pH, P, K, Ca, Mg, Fe, Mn, Cu, Zn, Al) of
samples from forest soil (circles) and accumulated sediment on
Attalea phalerata stems (squares) in the ‘‘Pantanal’’ wetland, Brazil.
Components 1 and 2 explain 62% of variance (45 and 17%,
C. E. Corre
ˆa, E. Fischer
dispersed seeds, the continuous arrival of seeds toward low
stems would favour hemiepiphytes fixed at low rather than
high stems.
Dispersal of C. pachystachya seeds is directed to A.
phalerata palms in forest patches of the ‘‘Pantanal’’, as
demonstrated by the much higher seed trapping on stems or
below palm canopies than elsewhere on the forest floor.
The common fruit bats of ‘‘Pantanal’’, Artibeus planirostris
(Spix 1823) and Platyrrhinus lineatus (E. Geoffroy 1810),
most likely cause this pattern. Both species use C.
pachystachya fruits as a core food item (Teixeira et al.
2009; Munin et al. 2012) and feed on fruits while hanging
underneath A. phalerata canopies nearby fruit sources in
the ‘‘Pantanal’’ (Marinho Filho 1992). The palms are
abundantly distributed and provide suitable roosts with
dense canopies that are freely accessible to bats. These bats
get and leave feeding roosts many times each night and
perform U-shaped flights when entering or leaving roosts.
As they defecate in flight and during fruit handling as well
(Munin et al. 2011), stools are released in variable direc-
tions under palm canopies and consistently to palm stems.
Although bat individuals use different feeding roosts
through time, they show a high fidelity to a few canopies
(Marques and Fischer 2009). This behaviour probably
concentrates seeds of C. pachystachya to a small number of
the total available palms, consistent with the patterns we
recorded for seed banks and seed trapping among palm
individuals at our study site.
Our glasshouse experiment indicated that the germina-
tion of C. pachystachya seeds does not differ between the
substrate types, forest soil or stem sediments. However,
both substrates likely accumulate inhibitors of germination,
as indicated by the higher germination success of C.
pachystachya in previously washed than non-washed sub-
strates. If flood pulses in the ‘‘Pantanal’’ reduce inhibitors,
the germination of C. pachystachya seeds would be
stimulated in low stem parts freshly emerged after the
flooding peak, whereas high stem parts not subjected to
inundation would accumulate inhibitors. In addition, if
stem inundation increases germination, only part of palm
individuals would propitiate this condition at a given time
since A. phalerata occupies different topographic levels
and the flooding pulses are quite variable in the
The clay sediment on A. phalerata stems is richer in
nutrients than the sandy soil of forest patches of the
‘Pantanal’’, like other palms reported with rich substrates
for true hemiepiphytes and C. obtusifolia (Bernal and
Balslev 1996;Lo
´pez-Acosta and Dirzo 2015). Our results
demonstrate that the sediments accumulated on persistent
sheaths have considerably higher amounts of organic
matter and of six nutrients (P, K, Ca, Mg, Mn and Zn) than
forest soils, where only one micronutrient (Fe) was sig-
nificantly more available. Therefore, palm sediments can
offer nutritional benefits that may contribute to the vigor-
ous growth observed for C. pachystachya hemiepiphytes in
the ‘‘Pantanal’’. In addition, our observations of fruiting
hemiepiphytes support the hypothesis that A. phalerata
stems provide high-quality microhabitat suitable for female
reproductive function (Fischer and Santos 2001; Guillon
et al. 2006). The values of aluminium concentration in both
substrates were apparently low to cause negative effects on
plant growth (Steiner et al. 2012). Moreover, the acid pH of
stem sediment can prevent the accumulation of aluminium
in growing plants, although it may reduce seed longevity
compared to the proximate neutral pH of forest soil (Jansen
et al. 2002; Pakeman et al. 2012). Therefore, the mainte-
nance of viable seed banks in palm stems might depend
upon a continual arrival of seeds compared to soil seed
banks in forest patches of ‘‘Pantanal’’.
In conclusion, a variety of ecological factors may con-
tribute to the facultative occurrence of C. pachystachya
Table 1 Chemical composition
of forest soil and sediment
accumulated on stems of Attalea
phalerata palms, in the
‘Pantanal’’ wetland of Brazil,
and loadings of elements on
Components 1 and 2 of a
principal component analysis
(PCA) to evaluate the similarity
between substrates (see Fig. 7)
Elements Stem sediment (n=8) Forest soil (n=8) PCA loadings
Mean SD Range Mean SD Range Comp. 1 Comp. 2
pH 5.4 0.36 4.8-5.9 6.8 0.74 5.6–8.1 -0.31 0.49
Organic matter (%) [5 3.2 0.67 2.3–4.1
Al (meq 100 cm
) 0.6 0.12 0.4–0.8 0.4 0.12 0.2–0.6 0.27 -0.48
) 42.3 11.85 30.2–61.7 22.8 19.62 9.3–68.8 0.33 0.23
K (meq 100 cm
) 1.4 0.59 0.6–2.6 0.3 0.08 0.2–0.4 0.33 -0.30
Ca (meq 100 cm
) 10.7 3.03 7.9–17.5 6.8 2.75 4.1–11.8 0.33 0.28
Mg (meq 100 cm
) 5.8 4.41 1.3–12.1 3.8 5.14 0.4–13.2 0.16 0.12
Fe (mg dm
) 7.7 5.02 2.2–17.4 39.2 29.54 1.8–87.0 -0.37 -0.24
Mn (mg dm
) 70.4 31.88 27–118.8 55.0 26.02 27.5–107.0 0.18 0.40
Cu (mg dm
) 0.3 0.04 0.3–0.4 0.4 0.06 0.3–0.5 -0.36 -0.24
Zn (mg dm
) 29.2 9.79 11.5–40.5 2.5 0.76 1.1–3.6 0.43 -0.14
Bizarre Cecropia pachystachya (Urticaceae) hemiepiphytic growth on palms in the ‘‘Pantanal’
hemiepiphytes in the ‘‘Pantanal’’. Of particular importance
is the consumption of C. pachystachya fruits by dense
populations of fruit bats (Teixeira et al. 2009; Munin et al.
2012), whose behaviour provides continuous seed dispersal
to A. phalerata palms. Nutrient availability and a shorter
duration under flooded conditions would aid fast and vig-
orous growth of C. pachystachya on palms. However, the
attachment of hemiepiphytes is apparently limited to low
palm stems, where gravity stabilization of trees appears to
be feasible. In addition, seed arrival is very high and
inhibitors of germination may be somewhat reduced by
flooding pulses in low parts of the palm stems. However,
only a small proportion of the palms receives C. pachys-
tachya seeds massively and the potential benefits after
inundation are rather ephemeral. These factors, summed to
potentially intrinsic limitation of most C. pachystachya
individuals in producing sufficient aerial roots to efficiently
fix on palms and then reach the forest floor, could explain
the rarity of hemiepiphytic trees at the study site.
Acknowledgements We thank J Celso, LC Corre
ˆa, LF Carvalho, N
Cunha, N Penatti and S Ferreira for field assistance in the ‘‘Pantanal’’,
F Gonc¸alves, LC Corre
ˆa and S Ferreira for assistance during the lab
work, and SCH Barrett for comments on early draft. This work was
supported by Fundac¸a
˜o de Apoio ao Desenvolvimento do Ensino,
ˆncia e Tecnologia do Estado de Mato Grosso do Sul (23/200.009/
2008), Coordenac¸a
˜o de Aperfeic¸oamento de Pessoal de Nı
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Bizarre Cecropia pachystachya (Urticaceae) hemiepiphytic growth on palms in the ‘‘Pantanal’
... Hemiepiphytes are plants that germinate epiphytically but establish root contact with the ground in a later ontogenetic stage (for a complete terminology of structurally dependent plants, see Zotz [2016]). Terrestrial shrub and tree species that occasionally show such growth are thus accidental or facultative hemiepiphytes (Coomes et al., 2005;Corrêa & Fischer, 2017;Dawes & Burns, 2020;Gaxiola et al., 2008;Newton & Healey, 1989;Winoto-Lewin & Kirkpatrick, 2020). ...
Vascular epiphytes are an important component of many ecosystems and constitute a substantial part of global plant diversity. In this context, accidental epiphytism, i.e. the opportunistic epiphytic growth of typically terrestrial species, deserves special attention as it provides crucial insights into the global distribution of vascular epiphytes and the initial evolution of epiphytic lineages. Even though accidental epiphytes have been mentioned in the literature for more than a century, they have been neglected in most epiphyte studies. Only recently accidental epiphytism was investigated more thoroughly. Therefore, the aim of this article was to provide a comprehensive review of the ecological basis and the evolutionary relevance of this common but largely disregarded phenomenon and to highlight open questions and promising research directions. Our central statement that potentially any species could grow epiphytically given the availability of suitable microhabitats and successful dispersal is backed up by a compilation of observations of accidental epiphytes from numerous ecosystems with diverse climates, even including semi‐arid Mediterranean ones. There are a variety of arboreal microhabitats with environmental conditions conforming to the ecological niche of typical terrestrial species, with the availability of such microhabitats depending on the interaction of local climate conditions, host tree age and host species identity. Whenever suitable microhabitats are available in tree crowns, accidental epiphytism is primarily limited by dispersal. In an evolutionary context, the conquest of the forest canopy represents an ecological opportunity where accidental epiphytes act as link between the terrestrial and the epiphytic life form. We discuss two fundamental scenarios with sympatric speciation, selective pressure, autopolyploidy, and allopatric speciation as underlying mechanisms in the transition from terrestrial to epiphytic growth. In conclusion, we argue that accidental epiphytism is a substrate and dispersal dependent phenomenon and that both from an individual perspective and from an evolutionary perspective epiphytism reflects the occupation of suitable but previously unexploited arboreal microhabitats. Acknowledging the fundamental principles that plant growth is opportunistic and that dispersal is a stochastic process can decisively improve our understanding of species distributions and other ecological patterns, as in the case of accidental epiphytism.
... Among the three genera of Cecropieae, hemiepiphytic growth dominates in Coussapoa (Berg, 1990), and there are scattered reports of facultative hemiepiphytic growth in species of Pourouma (Benavides et al., 2006;Dobzhansky and Murca-Pires, 1954;Ramírez, 1977), while hemiepiphytic growth is clearly exceptional (and again facultative) in Cecropia (C. pachystachya, Corrêa and Fischer, 2017). Arboreality also differs within a given genus. ...
Hemiepiphytic plants are defined by their ontogeny. They germinate on a host tree but later establish root contact with the soil. Most hemiepiphytes remain structurally dependent on their host for their entire life, but some, often referred to as stranglers, develop pseudotrunks that allow them to outlive their host. Unfortunately, the terminology used to describe hemiepiphytes and other structurally dependent plants (epiphytes, vines, lianas, nomadic vines, etc.) is highly inconsistent, which causes much ambiguity. Published reports frequently use the term “hemiepiphyte” without providing evidence, and it is often unclear whether conclusions are based on data, observations, or conjecture. Moreover, many hemiepiphytic species are facultatively terrestrial to varying degrees, which further complicates classifying them. In order to address these issues, we performed a thorough, critical review of the literature and provide an in-depth account of current knowledge regarding the morphology, physiology, ecology, and evolution of hemiepiphytes. Based on published works and our substantial field experience, we summarize the taxonomic distribution of hemiepiphytes among vascular plants, which includes c. 800 species in c. 30 families of ferns and angiosperms. We identify numerous, promising avenues of research on this fascinating group of plants, and make a case for adopting an explicit and unambiguous approach to describing hemiepiphytes and to naming life forms in research projects, on voucher specimens, and in the scientific literature.
... In their epiphytic life stage, juvenile hemiepiphytes are typically more subjected to water limitations than in their later soil-rooted life stage, which is reflected by various physiological and anatomical characteristics (Putz and Holbrook 1986;Holbrook and Putz, 1996;Liu et al., 2014). Nutrient supply, however, is not necessarily lower for epiphytic individuals, as juvenile hemiepiphytes often grow in accumulations of nutrient rich arboreal soil (Putz and Holbrook 1986;Corrêa and Fischer 2017). We assume that the observed intraspecific differences between epiphytic and terrestrial individuals in our study are the result of phenotypic plasticity rather than genetically fixed differences. ...
Vascular epiphytes are mainly associated with tropical and subtropical forest ecosystems. However, the frequent occurrence of accidental epiphytes in temperate forests proves that epiphytic growth of vascular plants is possible in tree crowns at these latitudes. Comparing the abiotic conditions of epiphytic and terrestrial microhabitats in conjunction with intraspecific differences in functional traits of the inhabiting plants, we identified limitations to vascular epiphytism in the study area in a Central European low mountain range. We determined light availability, winter temperatures, soil moisture, nutrient concentrations, and pH of arboreal soil in crotches of broad-leaved trees and in the immediate vicinity of each tree on the ground. Similarly, we quantified total plant water content, relative foliar chlorophyll content, specific leaf area (SLA), leaf dry matter content (LDMC), root-mass fraction, and aboveground nutrient concentrations of 110 pairs of epiphytic and terrestrial conspecifics. Water and nutrient availability were generally high in crotches filled with arboreal soil, suggesting better growth conditions than on the ground. A trophic advantage of epiphytic individuals over terrestrial conspecifics can be deduced from higher plant nutrient concentrations, higher SLA, and lower LDMC. Advantageous growth conditions might even result in higher growth rates and higher fitness of epiphytic individuals. Our findings highlight that vascular epiphytism in the study area is not necessarily limited by abiotic conditions but at least partly by the availability of old and structurally diverse trees providing suitable microhabitats. Accordingly, management actions in these secondary forest ecosystems should incorporate the preservation of old and large deciduous trees in order to sustain arboreal microhabitats and the associated biota.
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This chapter provides an overview on flowering and fruiting phenology, pollination and seed dispersal syndromes of species occurring in the capões (natural forest patches) of the southern Pantanal wetland, Brazil. We monthly sampled three to five different capões from May 1999 to May 2000 for all reproductive plant individuals and recorded their habits, numbers of open flowers, unripe and ripe fruits. The dataset comprised 52 capões in total. We classified the species into pollination and seed dispersal syndromes based on flower and fruit traits, respectively. In total, we recorded 248 flowering species and 111 fruiting species. According to floral traits, melittophily (47%) was the most frequent pollination syndrome, whereas anemophily was recorded for only 3% of the species. Zoochory was the most frequent seed dispersal syndrome (64%), followed by anemochory (19%) and autochory (17%). Epizoochory represented 5% of the zoochoric species. The present study highlights the high resource availability for pollinators and seed dispersers in the capões throughout the year, with a peak during the rainy season. In addition, we show that most plant species in these forest patches depend on biotic vectors for reproduction, thereby ensuring the maintenance of biological diversity in the Pantanal.
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Neotropical fruit bats are important dispersers of endozoochorous seeds, and the passage of seeds through their guts can affect germination. We asked whether the passage of Cecropia pachystachya (Urticaceae) seeds through guts of bats influences their germination behavior, specifically the proportion of germinated seeds and onset and speed of germination. We collected seed sets from bat feces and directly from ripe fruits monthly for a total of 6 months, in the urban area of Campo Grande, Central Brazil. Seeds were stored in glycerol until the germination experiment. During the experiment, for 45 days we maintained seed sets in a germinator and recorded daily seed development. Through redundancy correlation analysis, the interaction between seed source (fruits or bat feces) and time of storage explained 78% of variation in the germination parameters—the onset and speed of germination and the percentage of germinated seeds. Through data generated from random resamples, seed sets defecated by bats presented slower germination speed than seeds from ripe fruits, but onset of germination and proportion of germinated seeds did not differ between seeds passed or not passed through Artibeus lituratus and Artibeus planirostris. Overall, our results support that fruit bats are safe dispersers of C. pachystachya and promote asynchrony of germination among seeds, which may favor parental fitness in less predictable environments.
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The flora of the Atlantic Rainforest of Mato Grosso do Sul, southwestern Brazil, has not been inventoried in spite of being the westernmost inland region of this domain. We present an inventory of the riparian flora of inland Atlantic Forest in Mato Grosso do Sul. We describe the species distribution along three habitats with contrasting flood conditions: non-flooded, seasonally flooded, and swampy forests. The inventory consisted of sampling every reproductive individual, during 12 months on 1.12 ha of plots inside a 24 ha study area. We recorded 1967 individuals of 253 species and 72 families. The most representative families in number of species were Asteraceae (27), Fabaceae (19), Myrtaceae (17), Cyperaceae (12), Rubiaceae, Solanaceae and Orchidaceae (10 each). The most abundant reproductive species were Guarea macrophylla (169 individuals), Miconia chamissois (85) and Conyza bonariensis (80). Eleven species of six families were recorded for the first time in Mato Grosso do Sul, two of them endemic to the Atlantic Forest - Passiflora jilekii and Capanema micromera. We found 119 species exclusively in non-flooded habitat, 19 in seasonally flooded habitat, and 31 in swampy forest. Guarea macrophyllawas the most frequent species in swampy forest, and Gochnatia polymorpha in non-flooded. The riparian forest flora at the study site resembles the Atlantic Forest and includes wide distribution riparian species; the variation of flood conditions among habitats favors its richness. Our records add new occurrences for Mato Grosso do Sul and new distribution ranges for some plant species, what arises concern upon the local biodiversity conservation. Key words: flood gradient; plant distribution; plant richness; riparian forest; semideciduous forest
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Cecropia is a pioneer genus from the Neotropics, whilst Macaranga is an ecological analog with a center of distribution in Southeast Asia. In the past few decades, introduced populations of Cecropia spp. have spread rapidly in Singapore, Malaysia, and Indonesia. In Singapore, Cecropia pachystachya now occupies habitats that would have been expected to be occupied by Macaranga gigantea. We conducted germination experiments under 0, 20, 50, and 70 % shading and measured the survival rates and functional traits of the seedlings of these two species from material collected in Singapore. Seeds of C. pachystachya germinated in 3-12 days, whereas seeds of M. gigantea germinated from day 13 onwards. Germination success for C. pachystachya was between 90.3 % under full-light conditions and 55.8 % under 50 % shading, while for M. gigantea only 69.1 % of seed germinated under full-light conditions and germination completely failed when seeds were shaded by 20 % or more. The seedlings of C. pachystachya also had higher survival rates, faster shoot and root biomass accumulation, larger leaves, and lower total water content than those of M. gigantea. Thus overall, C. pachystachya possesses traits that may provide a competitive edge over the native M. gigantea and will be advantageous for its spread given the increasing proliferation of disturbed landscapes in tropical Southeast Asia.
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Aluminum (Al3+) toxicity is a major limiting factor to crop productivity in acid soils. The effects of aluminum on root and shoot growth of physic nut (Jatropha curcas L.) young plants and, the uptake and distribution of phosphorus, calcium, magnesium and aluminum in the roots and shoots were investigated in the present study. Plants were grown in 2.5L pots in a greenhouse. After fourteen days of adaptation to nutrient solution, plants were exposed to Al concentrations of 0, 370, 740, 1,100 and 1,480 mu mol L-1, corresponding to an active Al3+ solution of 13.3, 35.3, 90.0, 153.3 and 220.7 mu mol L-1, respectively. The dry matter partitioning between roots, stems and leaves, and the concentrations of P, Ca, Mg and Al in plant tissue, were measured after 75 days exposure to Al. The increasing level of Al3+ activity in solution progressively decreased the growth of the shoot and root of physic nut plants, and at the two highest active Al3+ levels, plants showed morphological abnormalities typical of the toxicity caused by this metal. Higher Al3+ activity reduced P concentrations in leaves and Ca and Mg in leaves and roots of physic nut, demonstrating the effect of Al on the uptake, transport and use of these nutrients by plants. The Al accumulated preferentially in the roots of physic nut, whereas only a small amount was transported to shoots.
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The present study aimed at analyzing the spatio-temporal variability of the Pantanal vegetation cover, the largest tropical wetland in the world. A principal component analysis (PCA) was applied to a complete annual dataset of filtered EVI2 images (based on a 12-year average over the 2001–2012 period). There was about 99 % variance concentration in the first three components, with the respective loading responses and distributions (maximum, minimum and changes in the sign of the eigenvector loadings) matching the most significant seasonal interruptions. The first three principal components showed the essential aspects of the spatio-temporal variability of the local phenology, i.e. the cumulative greenness throughout the year, the later and more generalized senescence associated with the drought season climax, and the early senescence associated with sandy portions. Our results enabled the detection of homologous areas regarding vegetation density and the time and intensity of senescence. As the water availability throughout the year—the most important parameter for regional vegetation—is largely a function of geology (sediment grain size and vertical neotectonic), a geobotanic analysis of the Pantanal wetlands was also possible. Our PCA-based approach was able to capture the essentials of the phenological/environmental variability, with potential for application in other ecosystems with complex vegetation cover and functioning.
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De los aspectos más notables de las plantas es su diversidad de formas de vida, en respuesta a la variabilidad ambiental a diferentes escalas. Una forma de vida con poca atención en el ámbito de la investigación ecológica, es la de las plantas hemiepífitas: aquellas que se desarrolla en una fase de su ciclo de vida sobre la copa de otras plantas. Este trabajo presenta una revisión de los aspectos más relevantes de la historia de vida del hábito hemiepífito primario, especificamene de las hemiepífitas estraguladoras, incluyendo su importancia taxonómica y estructural para muchos ecosistemas tropicales, desde bosques montanos hasta llanuras inundables. Si bien es conocido que estas plantas utilizan como forofito a una gama de especies arbóreas, se expone a las palmas como un forofito frecuente para el establecimiento de plantas hemiepífitas, haciendo especial enfasis en la asociación Ficus spp.-Sabal spp., como uno de los casos más representativos debido a su abundancia y amplitud de distribución geográfica. Estas asociación esta favorecida por la acumulación. de materia orgánica que generan un sustrato rico en nutrientes sobre las palmas, aquí discutimos el valor de este sistema como modelo para estudiar y entender mejor la ecología evolutiva de las plantas considerando la trilogía ambiente físico-plantas-ambiente biótico
Figs (Ficus spp., Moraceae) are considered a classic example of plants with fleshy fruits adapted for seed dispersal by vertebrates, usually mammals or birds. Partially covering the endocarp of each individual drupelet of F. microcarpa is a fleshy, discrete lipid-containing exocarp that suggests adaptation for seed dispersal by ants. This structure is highly attractive to ants. F. microcarpa drupelets from which the fleshy exocarp was experimentally removed were much less likely to be transported by ants than those with this structure intact. The exocarps retained their attractiveness to ants and were not visibly altered following passage of the entire fruit through the gut of a frugivorous bird, the Indian Hill Mynah (Gracula religiosa). Germination percentage was not significantly affected by gut passage or exocarp removal. These results suggest that F. microcarpa has a two-stage seed dispersal system, in which primary dispersal by vertebrates is followed by secondary dispersal by ants. Dispersal aided by ants may be of significance in the biology of this exotic hemiepiphyte in southern Florida, where it is naturalized and appears to be spreading.
The importance of the plants that dwell in forest canopies is becoming increasingly recognized in relation to understanding biodiversity. The upper tree canopy of many forest ecosystems fosters extremely diverse plant communities, which include vascular and nonvascular epiphytes, hemiepiphytes, and parasites. Canopy-dwelling plants contribute substantially to overall forest biodiversity and biocomplexity by providing resources for arboreal vertebrates, invertebrates, and microbes, and by participating in nutrient and water cycling and gas and energy exchanges.
Many plants have two root systems that differ in origin. One is the primary root system whose origin can be traced back to the radicle developed during embryogenesis. The other is an adventitious root system which arises on parts of the plant not originating from the embryonic root — that is, the roots arise on parts of the shoot. Adventitious roots usually initiate endogenously from tissue within the parent plant (see Chapter 4) though a few cases of exogenous origin are known [1]. Roots which arise on the primary root out of the usual acropetal sequence that characterises lateral roots, either as a normal part of development or after experimental treatment, are sometimes also called adventitious. The term adventive can perhaps be applied to such roots to distinguish them from roots of shoot origin.