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582
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Plants People Planet. 2020;2:582–586.wileyonlinelibrary.com/journal/ppp3
Received: 14 July 2020
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Revised: 17 September 2 020
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Accepted: 22 S eptember 2020
DOI: 10.1002/ppp3.10161
FLORA OBSCURA
Trade-offs tip toward litter trapping: Insights from a little-
known Panamanian cloud-forest treelet
1 | INTRODUCTION
Each plant's development unfolds along many trade-off axes. One
common trade-off is engendered by the differential allocation of
tissues to harvest essential resources from the surrounding envi-
ronment. Generally, photosynthetic leaves capture light energy and
carbon dioxide, whereas roots take up water and mineral nutrients.
Since these specialized func tions are usually performed in sepa-
rate realms – above- and belowground, respectively – plants must
differentially invest in the construction of above- versus below-
ground organs to meet their resource requirements (e.g., Mokany
et al., 2006). Furthermore, plant s tend to develop leaf and root mor-
phology and placement to make efficient resource harvests (e.g.,
Valladares et al., 2002). Accordingly, design trade-offs also shape
plants’ adaptive architectures. In light of these broad trade-offs,
Quadrella antonensis (Woodson) Iltis & Cornejo (C apparaceae), a
shrub or small tree restricted to the understor y of a few montane
cloud forests in Panama, presents a paradox: why does it appear to
be so clearly adapted to capture and retain fine debris in “trash bas-
kets” (see Figure 1) when this necessarily reduces light absorption
and photosynthesis?
The most distinctive features of Q. antonensis are those that
inspired its common names (basurera, trash-basket plant) – clus-
ters of large leaves tightly spiraled along stem and branch tips.
These leaf-cluster baskets collect fine litter that falls from over-
topping vegetation. It is impossible for the leaves of the plant
to be arranged in a way that maximizes light and litter capture
simultaneously. An alteration in the leaf arrangement to avoid
self-shading or shading by captured litter would render the ar-
rangement relatively ineffective at litter capture. To cluster,
overlap, or otherwise arrange leaves to effec tively capture litter
unavoidably reduces light capture ef ficiency in an already shady
forest understory.
Why would natural selection favor a plant architecture that
partially obscures its necessary photosynthetic surfaces? In other
words, is there a counterbalancing advantage to litter trapping that
overcomes the obvio us carbon-balance costs? Here, we begin to ad-
dress this question using Q. antonensis.
2 | ECOLOGY OF LITTER TRAPPING IN
QUADRELLA ANTONENSIS
Neither Paul H. Allen, who collected the holotype (Allen collection
#2948; Missouri Botanical Garden barcode MO-107310) in 1942,
nor Robert E. Woodson, Jr., who briefly described the species with
the basionym Capparis antonensis (Woodson et al., 1948), discussed
the plant's distinctive lit ter-trapping habit. In a taxonomic treatment
of a non -li tte r-t r ap p in g con gen er, Il tis (1981) men tio ned the “eco log i-
cally remarkable ‘detritophilous’” C. antonensis and Dressler (1985)
pondered its “humilectic” (humus collecting) nature in some det ail.
Iltis and Cornejo (2010) subsequently revised the taxonomy to Q.
antonensis. Dressler, Iltis, and Cornejo assumed that litter trapping
was advantageous, presumably for nutrient acquisition. In support
of this assumption, Dressler (1985) noted that the plant produces
copious adventitious roots from its branches into the trash basket s
and that these roots clearly help retain litter and its resulting humus,
both within the baskets themselves and along a portion of the stem
or branch below each basket where the oldest leaves have dehisced
and fallen away.
In our study population in the Altos de C ampana National Park,
Republic of Panama and based on our unpublished estimates from
spor adic censuses over a 5-year period, we found that each well-de-
veloped leaf-cluster basket contains about 20 living leaves, each bas-
ket produces about two new leaves per year, and individual leaves
can sur vive more than 5 years. In addition, the primary or ground
root system is poorly developed (Dressler, 1985), except in small
saplings, whereas the aboveground adventitious roots (which are
present on plants as small as those having only four fully expanded
leaves) have both root hairs and arbuscular mycorrhizal associates.
At our study site, Sánchez de Stapf (2001) demonstrated through
two manipulative field experiments that litter trapping is indeed ad-
vantageous. For her first experiment, she selected 40 plants, each
with two to six basket s, and on each plant she chose two simil ar bas-
kets on separate branches as a pair. For her second experiment, she
selected 80 small plants, each with a single apical basket, and paired
the plants by proximity. For each pair of baskets in each experiment,
she randomly chose one basket as a control. During the course of
This is an op en access arti cle under the ter ms of the Creative Commons Attribution L icense, which pe rmits use, dis tribu tion and reprod uction in any med ium,
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a year, she removed lit ter monthly from the treatment baskets and
compared new leaf production per basket with their paired control
baskets. Litter removal statistically significantly reduced new leaf
production per basket: for the first experiment from an average of
2.3 ± 0.7 (SD) new leaves in control basket s to 1.8 ± 1.1 in litter-re-
moval baskets (paired t test, p = .003) and for th e se con d ex per iment
from 3.3 ± 2.3 to 2.8 ± 2.1 (paired t test, p = .04). Therefore, Q.
antonensis plants appear both to invest in acquiring resources from
their litter baskets through adventitious root production, and ben-
efit from litter through increased productivity. Similar investments
and benefits are likely to occur to varying degrees in other litter
trapping shrubs and trees, but the presumed benefits have not been
investigated in detail.
3 | A BRIEF SURVEY OF LITTER TRAPPING
In a recent compre hensive review of “f ilter feeder s of the plant king-
dom,” Zona & Christenhusz (2015) defined litter trappers as “plants
that, by vir tue of growth habit and morphology, trap or channel fall-
ing debris… and use the nutrients derived from this detritus for their
own grow th.” They noted that defining this trait is challenging, as
litter trapping may be incidental, or in the case of some bromeliads,
aroids, and ferns, trapping primarily functions for the impoundment
of water. While li tter cap ture is com mon and wides pr ea d among epi-
phytes, the trait also occurs in at least 30 families and over 90 genera
of non-epiphytic terrestrial plants. Among trees and shrubs, litter
trapping is associated with “Schopfbaum” or “branched Schopfbaum”
(as in Q. antonensis) architecture, consisting of rosettes or crowns
of leaves borne on a single stem or at the ends of sparse branches
(Zona & Christenhusz 2015). Schopfbaum trees and shrubs account
for more than 40 genera of litter trappers, and have evolved in-
dependently multiple times within a few species-rich genera (e.g.,
Psychotria; Lachenaud & Jongkind, 2013).
A fur ther distinction – applied here to woody terrestrial litter
trappers – recognizes litter baskets created by rosettes of leaves
with short petioles, as in Q. antonensis, versus those in which the
litter falls between the leaves and is funneled by long petioles to
the base of the trunk or stem (Zona & Christenhusz, 2015). The long
petiolate form occurs in several species of palms and tree ferns.
Because long petioles trap litter beneath the canopy of leaves, litter
capture in these plants is less likely to affect light capture than in
short petiolate forms where leaf sur faces help trap litter.
The production of adventitious roots inside the accumulated litter
– a trait more convincingly indicative of an adaptive nutrient-uptake
fu n cti o n – is much less freq u ent l y fo u nd th an li t ter tr app ing it sel f (Zo n a
& Christenhusz, 2015). An example of an additional woody terrestrial,
litter-trapping species with adventitious roots is Q. dressleri, named by
Cornejo and Iltis (2010) to commemorate Robert Dressler's seminal
work on Panamanian terrestrial litter trappers. Like Q. antonensis, this
unbranched Schopfbaum treelet is restricted to forest understor y sites
on a few mountain tops in central Panama (east of and allopatric to
Q. antonensis’ geographic range). In a survey of litter trappers in the
Golfo Dulce region of Costa Rica, Weissenhoffer et al. (20 08) fou nd 24
terrestrial litter-trapping species, including eight species of palms (six
with adventitious roots in the accumulated humus) and eight species
of treelets (two with adventitious roots in the accumulated humus);
they noted that in the region – owing to their abundance – terrestrial
litter trappers “obviously play a significant ecological role.” Similarly,
Kenfack et al. (2007) reported that throughout the 50-ha Korup Forest
Dynamics Plot in C ameroon “the understor y is dominated by an odd
group of litter-trapping treelets,” including species with adventitious
roots (D. W. Thomas, pers. comm.). In the case of the coffee relative
Coffea magnistipula in West Africa, leaf blades funnel debris into cup-
like stipules and adventitious roots grow into the resulting humus
(Stoffelen et al., 1997). In any case, adaptive advant ages to terrestrial
litter trapping, or specific functions such as nutrient uptake by adven-
titious roots, mostly have been assumed rather than demonstrated or
tested.
FIGURE 1 The Panamanian trash-basket plant, Quadrella antonensis. (a) A small individual with a single apical leaf-cluster basket; (b) a
medium-sized individual with several leaf-cluster baskets; and (c) a close-up view of adventitious roots. Photographs (a-b) by K. E. Harms; (c)
by J. W. Dalling
(a) (b) (c)
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4 | BENEFITS OF LITTER TR APPING: A
CALL FOR MORE RESE ARCH INTO ITS
ADAPTIVE SIGNIFICANCE
Our observations and reports about other litter trappers suggest
the following mutually compatible potential advantages to litter
trapping across taxa. Plants may extract resources directly from in-
tercepted boluses of litter and humus (via roots or other absorptive
surfaces) – to increase overall nutrient uptake; to avoid competition
with other organisms foraging in the soil (e.g., by providing priority
access to nutrients such as potassium that are readily leached out of
organic matter); or to obtain better stoichiometric ratios of elements
from decomposition of fine litter than would be obtained from de-
composition sources on the ground (e.g., coarse woody debris, which
generally has higher C:N and C:P ratios than fine litter). Alternatively
or in concert, nutrients released from intercepted lit ter may be di-
rected via stemflow toward aboveground roots, or other absorptive
surfaces (e.g., Weissenhoffer et al., 2008, suggest cataphylls and leaf
bases in litter-trapping Clavija costaricana), or into the soil in which
the plants are rooted in the ground (Raich, 1983). Although most
published speculation about and research into the benefits to lit-
ter trapping focus on the plants’ nutrient economies (Benzing, 1990;
Ng, 1980; Zona & Christenhusz, 2015), there are several other po-
tential benefits.
Via litter trapping, plants might manipulate or otherwise inter-
act favorably with organisms from the broader community, possibly
even shaping species-interac tion webs to their advantage. Insects,
fungi, microbes, and other organisms live in their aboveground
“private compost heaps” (Dressler, 1985) and could provide myriad
benefits. For example, protective ants could live in the litter, spe-
cialized decomposers could live in the humus, or the milieu could
attract carnivores that dissuade or remove would-be herbivores.
In an intriguing example, Ngai and Srivastava (20 06) found that a
predator y tank-dwelling damselfly increased nutrient cycling in an
epiphytic, litter-, and water-trapping tank bromeliad. Reduced rates
of leaf herbivor y, owing to decreased apparency or physical acces-
sibility, could result from a combination of litter accumulation and
humus formation on live leaves. Aboveground deployment of fine
roots could reduce overall rates of root herbivory. Thermoregulation
is also a possibility, perhaps especially for species found in cold cli-
matic zones (similar to the thermoregulatory advantages afforded
to Andean Espeletia schultzii by retention of its own dead leaves;
Smith, 1979). In any case, very little work has been done to deter-
mine the potential for these types of possible benefits to litter trap-
ping for most terrestrial litter trappers.
5 | CONSERVATION CONCERNS
Demographic processes are slow in Q. antonensis. Plants grow slowly
and have very low reproductive output. During what appeared to be
a typical reproductive year at our Altos de Campana study site (based
on our casual observations over several years), Sánchez de Stapf
(2001) c arefully assessed each of 112 reproductively-sized individu-
als each month. All of these plants were >1.4-m tall, which is larger
than the smallest individual we have observed with flowers or fruits
at the site. Only 30 of these individuals produced flowers or fruits,
and among those only 10 fruits (none containing more than 14 seeds)
reached maturity – 3 on a single plant (Sánchez de Stapf, 2001). They
appear to be plant s living on an economic knife-edge – in shaded
sites where there is enough light to maintain a positive carbon bal-
ance, but where nutrients are in suf ficiently short supply that litter
trapping provides a net benefit. As researchers continue to study
litter trappers in the field, these life-history traits of slow growth and
infrequent reproduction may prove to be common among them, in
which case those with small overall population sizes are likely to be
especially sensitive to anthropogenic disturbances and threatened
with extinction.
Like many terrestrial litter trappers, Q. antonensis is globally rare.
It is only known from a few highland locations in central Panama,
most of which have tenuous prospects for long-term population
viabilit y. For example, our study population in Altos de Campana
National Park is embedded within and clearly influenced by an an-
thropogenically disturbed landscape (Terborgh, 1999).
6 | CONCLUDING REMARKS
As the list of terrestrial litter-trapping plants grows, we predict
that most will tend to be found where temperatures allow broad,
long-lived evergreen leaves, since deciduous leaves or needles are
likely less well-suited to capture and retention of fine litter. We also
predict that plants with adventitious roots in aboveground humus
will tend to occur where there is sufficient moisture throughout the
year to maintain aboveground humus formation and water – with
attendant mineral – uptake (Dressler, 1985). Finally, poor soil-borne
nutrient status (or possibly water-logged soil) is likely to be a key
condition tipping the balance toward litter trapping plus adven-
titious root formation. Even though we do not have nutrient data
for soils at our study site, characteristics of the site suggest very
poor nutrient status, including abundant Podocarpus trees, which are
generally reliable indicators of low nutrient soils (Palma et al., 2020;
Punyasena et al., 2011).
Although we can speculate on the conditions that selectively
favor litter trapping, relatively little is known about the relative
costs and benefits of litter trapping across environment al con-
ditions. In addition, there has been no formal phylogenetic or
evolutionary assessment of ancestral conditions preceding litter
trapping. It is plausible that efficient and effective litter trapping
could evolve from incidental litter capture combined with pheno-
typically plastic production of adventitious roots (Herwitz, 1991;
Nadkarni, 1994). Similarly, we do not know how often – once ad-
opted and adaptively elaborated – litter trapping is evolutionarily
lost.
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Comparisons may be drawn between litter-trapping plants and
carnivorous and certain myrmecophilous plants in which mor-
phology is adapted for nutrient acquisition from prey and ants,
respectively (Thorogood & Bauer, 2020, discuss similar trade-offs
between photosynthetic potential and nutrient acquisition in car-
nivorous plants). The largely detritivorous pitcher plant, Nepenthes
ampullaria – from an otherwise almost entirely carnivorous genus
– illustrates th e functional simil ari ty of carnivorous and litter-trap-
ping habits (Moran et al., 2003). Via a cost-benefit model, Givnish
et al. (1984) proposed environmental conditions in which carnivory
and myrmecophily would be favored; they predicted that carnivor y
should be restricted to sunny, moist sites with low nutrient avail-
ability. By contrast they suggested that myrmecophily can occur in
shaded habitats where additional benefits beyond mineral nutrient
acquisition are possible, such as defense by ants. Like myrmecoph-
ily, litter trapping may offer selective advantages to occupying
shaded sites. For example, in shady environments, the construc-
tion cost of litter traps could be repaid over the long lifetimes of
the slow-growing component leaves, in contrast with the traps of
carnivorous plant s in sunny environment s, that appear to require
more frequent replacement to enable the plants to continue to
capture prey. In any case, litter-trappers would not be expected to
occur in open, sunny sites, because whence would the litter come?
As researchers continue to bring litter-trapping plants out of
obscurity, we need concerted efforts to determine the cost-bene-
fit balance for these species and the selective consequences that
tip the balance toward litter trapping. Litter-removal and addition
experiments across environmental gradients could be used to esti-
mate the cost, benefit, and net-benefit curves envisioned by Givnish
et al. (1984); stable isotope studies could be used to trace nitrogen
uptake and use.
Just as the tick-tock pendulum in a grandfather clock cannot si-
multaneously tick to the right and tock to the left, developmental
trade-offs render plants incapable of possessing all possible tools
of the plant trade, i.e., none can perform all possible functions with
maximal efficiency. Accordingly, the natural world is replete with
surprising, often obscure, adaptations like those found among the
litter trappers.
ACKNOWLEDGEMENTS
For their various contributions toward our understanding of the
Panamanian trash-basket plant, we thank Mireya Correa, Carmen
Galdames, and Bob Pearcy; we posthumously thank Bob Dressler
and Hugh Iltis (who once wrote to us that, coincidentally, he became
a graduate student of his “major professor” Robert Woodson in
1948, the same year in which Woodson described C. antonensis). For
indulging and sharing our interest s in the natural history of Panama,
and for comments on the manuscript, we thank Jessica Eberhard and
Astrid Ferrer.
AUTHOR CONTRIBUTIONS
All authors contributed toward the fieldwork, statistical analyses,
writing, and editing of the manuscript.
Kyle E. Harms1
James W. Dalling2,3
María N. Sánchez de Stapf4
1Department of Biological Sciences, Louisiana State University,
Baton Rouge, LA, USA
2Department of Plant Biology, University of Illinois at
Champaign-Urbana, Urbana, IL, USA
3Smithsonian Tropical Research Institute, Apartado Postal,
Ciudad de Panamá, República de Panamá
4Departamento de Botánica, Facultad de Ciencias Naturales,
Exactas y Tecnología, Universidad de Panamá, Ciudad de
Panamá, República de Panamá
Correspondence
James W. Dalling, Depar tment of Plant Biology, University of
Illinois at Champaign-Urbana, Urbana, IL 61801, USA.
Email: dalling@illinois.edu
ORCID
James W. Dalling https://orcid.org/0000-0002-6488-9895
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How to cite this art icle: Harms KE, Dalling JW, Sánchez de
Stapf MN. Trade-of fs tip toward litter trapping: Insights from a
little-known Panamanian cloud-forest treelet. Plants, People,
Planet. 2020;2:582–586. http s://doi.org/10.10 02 /ppp3.10161
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