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Notes on frugivory in Monstera and Philodendron (Araceae) from Costa Rica and Panama

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Abstract

Seed dispersal in aroids occurs mainly through animals (mainly by birds or mammals). However, the processes of seed dispersal and frugivory in diverse neotropical aroid genera such as Monstera and Philodendron are poorly known, especially in Central America. Here, illustrations and notes on frugivory of Philodendron popenoei and Philodendron crassispathum in Costa Rica are provided. Additionally, observations on bird and mammal frugivory in Monstera adansonii from Costa Rica and Panama are included.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
Notes on frugivory in
Monstera
and
Philodendron
(Araceae) from Costa Rica and
Panama.
Marco Cedeño-Fonseca
Programa de Posgrado en Biología / Herbario Luis Fournier Origgi (USJ), Universidad de
Costa Rica, San José, Costa Rica.
marcovf.09@gmail.com
*corresponding autor
Jose Pablo Castillo
Fundación Madre Tierra Verde. email: jp.birdscostarica@gmail.com
Orlando O. Ortíz
Herbario PMA, Universidad de Panamá, Estafeta Universitaria, Panama City, Republic of
Panamá email: ortizopma@gmail.com
Juan P. Ríos
Biodiversity Consultant Group (BCG), San Francisco, Ciudad de Panamá, Republic of
Panamá email: juanpr84@gmail.com
Lizeth Hidalgo Picado
Universidad Técnica Nacional Sede-Atenas / Ingeniería en Ciencias Forestales y Vida
Silvestre email: lizethphp@gmail.com
Jeffrey Flores Rojas
Programa de Posgrado en Biología / Herbario Luis Fournier Origgi (USJ), Universidad de
Costa Rica, San José, Costa Rica. email: Jeffrey.hfr5@gmail.com
Thomas B. Croat
Missouri Botanical Garden, P.O. Box 299, St. Louis, Missouri 63166–0299, U.S.A.
email: Thomas.Croat@mobot.org
Aroideana VOL 43 NOS 1&2, 2020 212
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
ABSTRACT
Seed dispersal in aroids occurs mainly
through animals (mainly by birds or
mammals). However, the processes of seed
dispersal and frugivory in diverse
neotropical aroid genera such as Monstera
and Philodendron are poorly known,
especially in Central America. Here,
illustrations and notes on frugivory of
Philodendron popenoei and Philodendron
crassispathum in Costa Rica are provided.
Additionally, observations on bird and
mammal frugivory in Monstera adansonii from
Costa Rica and Panama are included.
KEY WORDS
Dispersal, frugivory, Manacus candei,
Euphonia anneae, Habia rubica, Potos flavus,
Saguinus, Monstera, Philodendron.
INTRODUCTION
Araceae Juss., with 144 genera and about
3750 species (Boyce & Croat, 2018),
presents a wide diversity in its reproductive
morphology. The inflorescences consist of
a morphologically terminal spadix with
bisexual or unisexual flowers, and an
infructescence with fruits that are berries
containing one to numerous seeds in a more
or less fleshy pulp (Mayo et al. 1997). This
characteristic of the fruits makes them an
important food resource for the fauna of
the forests and open areas.
In general terms, seed dispersal in Araceae
occurs mainly through animals, principally
by ornithocory (Mayo et al. 1997), though
there are also reports that dispersal is
effected by mammals in some cases
(Hambali 1980). Monstera Adans. and
Philodendron Schott, are neotropical groups
that produce fleshy infructescences (Mayo
et al. 1997) which fit perfectly for the
dispersal syndrome mainly by birds.
However, like other very diverse genera of
Araceae, the processes of seed dispersal and
frugivory in Monstera and Philodendron are
poorly known, especially in Central America
(see Cedeño-Fonseca et al. 2019).
Cáceres (2004) reported the mammal
Philander frenata (Opossums) feeding of
infructescence on M. adansonii Schott in
southern Brazil, and Cardoso et al. (2011)
reported mammal Leontopithecus chrysomelas
(Golden-headed Lion Tamarins) feeding of
infructescence on Philodendron in Bahia,
Brazil. For Iguazu, Argentina Hirsch (2009)
reported that Nasua nasua (Coatis) feeding
of infructescences of Philodendron
bipinnatifidum Schott ex Endl.
In this article, one species of bird Habia
rubica (Vieillot, 1817) (Red-crowned Ant-
Tanager), that feed on the infructescences
of Monstera adansonii Schott and, one species
of bird Euphonia annae (Cassin, 1865)
(Tawny-capped Euphonia) and, one species
of mammal Potos flavus (Schreber, 1774)
(Kinkajou) that feed on the infructescences
of Philodendron are documented for the first
time for Costa Rica. For Panama, a species
of bird Thraupis episcopus (Linneo, 1766)
(Blue-gray Tanager), Thraupis palmarum
(Wied, 1821) (Palm Tanager), and Saguinus
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Figure 1. Habia rubica eating the fruits of Monstera adansonii in Atenas, Alajuela, Costa Rica. — Photo taken
from the video capture of Lizeth Hidalgo Picado.
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Figure 2. Blue-gray Tanager (Thraupis episcopus) eating the fruits of Monstera adansonii in Panama City (Cerro
Ancón). — Photo Juan Ríos.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
geoffroyi (Pucheran, 1845) (Geoffroy's
Tamarin, Panamanian Tamarin, Red-crested
Tamarin or Rufous-naped Tamarin), eating
fruits of Monstera adansonii. These groups
could be considered as important seed
dispersers or removers of the mentioned
aroid species.
DOCUMENTATION IN
MONSTERA
Monstera has berries completely covered
with a thick layer with closely embedded
raphides beneath the style which helps to
prevent herbivory by providing a protective
layer (Mayo et al. 1997). However, at
maturity of the fruits the styles come off
simultaneously in large segments or all
together, thus exposing the pulp that
surrounds the seed. At this time the fruits
are available to be eaten without having to
ingest the raphides. In Monstera adansonii
subsp. laniata, developing infructescences
are erect, but when they mature they
become pendent, and it is at this stage that
simultaneous detachment of the stylar layer
occurs, exposing the pulp and seeds to
frugivores. Previous studies have reported
that both birds and mammals are their
potential fruit and seed dispersers (Vieira &
Izar 1999; Galetti et al. 2011).
Currently, Monstera adansonii represents a
polytypic species, which includes four
subspecies distributed throughout the
Neotropical region (Mayo & Andrade 2013).
The taxon that occurs in Central America
corresponds to Monstera adansonii Schott
subsp. laniata (Schott) Mayo & I.M.
Andrade, which is distributed from
Honduras to Colombia, Ecuador, Peru,
Venezuela and Caribbean region. In Costa
Rica and Panama, this taxon blooms
throughout the year (Grayum 2003; Ortíz
pers. obs.). Also, this taxon exhibits high
morphological variation and grows in
multiple habitats, such as lowland forests,
open areas (potreros), mangroves and
gallery forests (Cedeño-Fonseca 2019).
Observation 1: Frugivory of
Monstera
adansonii
in Costa Rica. In the
agroecological farm in Atenas, images and
videos were captured of Habia rubica
(Vieillot, 1817) (Red-crowned Ant-Tanager),
visiting infructescences of M. adansonii
several times and removing the fruits to
digest the pulp (Figure 1). This species
visited the infructescence for four days and
remained for more than 10 minutes on each
visit, perching on the petioles of the plant
to feed on the infructescence. When Habia
rubica takes the fruit, it strikes it against the
petiole in order to extract the pulp and
release the seed. The seed falls to the
ground near the host tree of the adult plant
where it will possibly germinate. This
situation could be an explanation of why
there was an adult plant and several
juveniles growing in the same host tree,
because the seeds are not dispersed for a
great distance. This behavior is observed in
the video available at the following link:
https://www.facebook.com/watch/?
v=503461826882658, made by Lizeth
Hidalgo Picado in September 2019.
Observation 2: Frugivory of
Monstera
adansonii
in Panama. On October 17,
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2019, at 10:15 a.m., along the urban forests
of Cerro Ancón in Panama City
(08°57'37"N, 079°32'60"W, 153 meters
above sea level), 4–5 individuals of Blue-
gray Tanager (Thraupis episcopus) (Figure 2),
and Palm Tanager (Thraupis palmarum) were
observed feeding on berries of Monstera
adansonii. These birds ate large amounts of
fruits for approximately 10 minutes. They
consumed the fruits individually (one by
one), ingesting them whole (including seeds
and pulp). The next day (Octuber 18, 2019)
at the same site in the afternoon (3:17 p.m.),
a small troop of five or six individuals of
Geoffroy's Tamarin monkeys (Saguinus
geoffroyi) was also feeding on the
infructescences of Monstera adansonii
(Figure 3 and 4). Before the
aforementioned sighting, the monkeys
seemed very curious, watching closely the
infructescences pecked by the birds (and
were attracted by the smell of the berries)
(see Figure 4). Subsequently, the monkeys
grabbed the infructescences with one or
both forelimbs and then nibbled it, mainly
in the middle part of the spadix, getting to
feed on the whole berries, including the
seeds. In total, the sighting of the monkeys
lasted approximately 20 minutes.
DOCUMENTATION IN
PHILODENDRON
In the genus Philodendron Schott, most of
the species have a spathe that completely re-
closes after anthesis, including the whole
spadix within it. Much later, after berries
have matured, the entire spathe usually
ruptures, breaking up into large or small
pieces and usually falling free to expose the
pistilate portion with its now plump and
sometimes colorful berries. Sometimes only
the apical portion of the spathe together
with the male part of the spadix fall free.
The berries are now exposed to animals for
eating and these may be devoured by birds,
mammals or ants.
Observation 3: Bird-frugivory in
Philodendron popenoei
. On March 25,
2019, two Euphonia annae individuals were
registered feeding on the fruits of
Philodendron popenoei growing at
approximately 10 m from the ground in a
mature forest near Ojo de Agua, Pocora,
Limón, at 1180 meters above sea level.
These birds were in a mixed flock with
Chlorospingus flavopectus (Lafresnaye, 1840)
(Common Chlorospingus) and Tangara
icterocephala (Bonaparte, 1851) (Silver-
throated Tanager). Both male and female
birds removed the mucilaginous berries
while they remained perched near the
infructescence (Figures 5–6), grabbing one
ripe fruit at a time and crushing it with their
beaks several times to ingest the pulp and
seed, and then they dropped the small
wasted parts to the ground. It is important
to add that Stiles and Skutch (1989) cite the
consumption of Anthurium as another genus
of Araceae that is part of the varied diet of
this frugivorous bird. In addition to the
photographs, a video was made available at
https://youtu.be/I0v6IUBufVo.
Philodendron popenoei Standl. & Steyerm., is a
Central American species, which grows at
medium elevations (0 to 1000 m), mainly in
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Figure 3. Geoffroy's tamarin monkeys (Saguinus geoffroyi) feeding on the infrutescence of Monstera adansonii.
Photo Juan Ríos.
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Figure 4. Geoffroy's tamarin monkeys (Saguinus geoffroyi) watching the infructescences of Monstera adansonii
(as attracted by the smell of the berries). — Photo Juan Ríos.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
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Figure 5. Male Euphonia annae perched on the spadix while it feeds on the mature fruits of Philodendron
popenoei. — Photo Pablo Castillo.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
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Figure 6. Male and female Euphonia annae perched respectively on the petiole and spathe of Philodendron
popenoei while they feed on its fruits. — Photo Pablo Castillo.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
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Figure 7. Potos flavus eating the fruits of Philodendron crassispathum in the protective zone Las Tablas,
Puntarenas, Costa Rica. — Photo Jeffrey Flores.
Cedeño-Fonseca, et. al., 2020 Notes on frugivory in Monstera and Philodendron (Araceae) ...
the inner part of the forests or rarely in
open areas and edges of the mature forest.
Observation 4: Mammal-frugivory in
Philodendron crassispathum
. On August
3, 2019, at 7:20 p.m., in the Sura region in
the Las Tablas protective zone at
approximately 2000 m, an individual of
Potos flavus (Kinkajou) was observed feeding
on the mature infructescences of
Philodendron crassispathum (Figure 7). The
plant was near the canopy, about 20 m high,
with hanging stems. The mammal was
hanging, holding only with its hind legs, and
with one of its forelegs it held the peduncle
and with the other it sustained the mature
infructescence. Potos flavus was in this
position for several minutes, then observed
the lights and left through the forest canopy
branches. Philodendron crassispathum Croat &
Grayum is an endemic species of Costa
Rica and Panama, which grows at elevations
of 1100 to 2600 m.
ACKNOWLEDGEMENTS
We thank Alan Barboza and Ruddy Fallas
for the support given on the tour to the
Sura region in the Las Tablas protective
zone. We also thank Ranzeth Gómez
Navarro for his collaboration in the field
observations on the dispersers of Monstera
adansonii in Costa Rica.
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A taxonomic revision is presented of the three taxa of Monstera (Araceae) recognized for Bahia State, Brazil:– M. adansonii subsp. blanchetii (stat. nov.), M. adansonii subsp. klotzschiana (stat. nov.) and M. praetermissa; a fourth taxon, not so far recorded from the state, M. adansonii subsp. laniata (stat. nov.), is distinguished from subsp. blanchetii. The two highly variable subspecies of Monstera adansonii were further investigated by morphometric study of herbarium specimens. These two taxa were distinguished using principal coordinates analysis (classical multidimensional scaling) and linear discriminant analysis; the most important diagnostic characters are stigma length and width, stigmatophore length, style apex size and leaf perforation number. Discrimination on leaf characters alone was over 90% successful – subsp. blanchetii differs most significantly from subsp. klotzschiana in higher values for perforation number and leaf base angle. Descriptions, illustrations, geographical and conservation status information and a key to the taxa are provided. Two neotypes are proposed (M. maximilianii Engl., M. klotzschiana Schott) and discussions of the typifications are provided. (© 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim)
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Revisión taxonómica del género Monstera (Araceae) en Costa Rica
  • M Cedeño-Fonseca
Cedeño-Fonseca, M. 2019. Revisión taxonómica del género Monstera (Araceae) en Costa Rica.
The dispersal of taro by common palm civet
  • G G Hambali
Hambali, G.G. 1980. The dispersal of taro by common palm civet. IFS (Intern. Found. Sci.) Prov. Rept. No. 5: 29-34.
A Guide to the Birds of Costa Rica
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Stiles, F.G. y A.F. Skutch. 1989. A Guide to the Birds of Costa Rica. Ithaca, Nueva York: Cornell University Press.