New Notes on the Ecology of the Epiphytic Gymnosperm and Panamanian Endemic Zamia pseudoparasitica
Philip Bell-Doyon1* and Juan Carlos Villarreal A.2
1Department of Wood and Forest Sciences, Laval University, Québec, QC, Canada. G1V 0A6. 2Department of Biology, Laval University, Québec, QC, Canada. G1V 0A6.*Corresponding author.
Neotropical Naturalist, No. 2 (2020)
Abstract
The Panamanian endemic cycad Zamia pseudoparasitica Yates was surveyed in the Omar Torrijos National Park, Provincia de Coclé, from May to July 2018. The species is the only strictly epiphytic gymnosperm and its life history is little known due to the inaccessibility of the plants. Using single-rope and prussik-knot tree climbing techniques, population density, seed dispersal strategy and ant-garden specificity were evaluated. Zamia pseudoparasitica is locally common in parts of the park with up to 24 individuals per hectare. No ripe ovulate cone was found, precluding the observation of seed dispersers. Almost a quarter of monitored plants presented an ant nest near or within its root system. The ants identified belonged to five genera: Camponotus, Cyphomyrmex, Megalomyrmex, Odontomachus, and Rogeria. Zamia pseudoparasitica has unique ecological attributes related to its peculiar life history. We believe the species should receive more attention from environmental authorities and the public to help preserve its habitat.
Resumen
La cícada endémica de Panamá Zamia pseudoparasitica Yates fue monitoreada en el parque nacional Omar Torrijos, Provincia de Coclé, entre mayo y julio de 2018. Es la única especie de gimnosperma estrictamente epífita y su historia natural es poco conocida debido a que la especie se encuentra a alturas poco accesibles (10-20 metros). Usando una técnica de escalado de árboles con un nudo prussik, evaluamos la densidad de la población, la estrategia de diseminación y la especificidad de jardines de hormigas. Zamia pseudoparasitica es bastante común en partes del parque nacional y se encuentran hasta 24 individuos por hectárea. No encontramos conos ovulados maduros así que no pudimos observar los diseminadores de las semillas. Aproximadamente, una de cuatro de las plantas monitoreadas tenía un jardín de hormigas en su sistema de raíces. Las hormigas identificadas pertenecían a cinco géneros: Camponotus, Cyphomyrmex, Megalomyrmex, Odontomachus y Rogeria. Zamia pseudoparasitica tiene características ecológicas únicas relacionadas a su hábit peculiar. La especie debería recibir más atención por parte de las autoridades y del publico para ayudar en la preservación de su hábitat.
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No. 2 Neotropical Naturalist 2020
New Notes on the
Ecology of the Epiphytic
Gymnosperm and
Panamanian Endemic
Zamia pseudoparasitica
Philip Bell-Doyon and
Juan Carlos Villarreal A.
NEOTROPICAL NATURALIST
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Cover Photograph: Lilisbeth Rodriguez, a young Panamanian biologist and great field companion,
investigating a large Zamia pseudoparasitica plant 15 meters above ground in Omar Torrijos National Park,
El Copé, Panama. Photograph © Philip Bell-Doyon
Neotropical Naturalist
P. Bell-Doyon and J.C. Villarreal A.
2020 No. 2
1
2020 NEOTROPICAL NATURALIST
New Notes on the Ecology of the
Epiphytic Gymnosperm and Panamanian Endemic
Zamia pseudoparasitica
Philip Bell-Doyon1* and Juan Carlos Villarreal A.2
Abstract - The Panamanian endemic cycad Zamia pseudoparasitica Yates was surveyed in the Omar
Torrijos National Park, Provincia de Coclé, from May to July 2018. The species is the only strictly
epiphytic gymnosperm and its life history is little known due to the inaccessibility of the plants. Using
single-rope and prussik-knot tree climbing techniques, population density, seed dispersal strategy and
ant-garden specificity were evaluated. Zamia pseudoparasitica is locally common in parts of the park
with up to 24 individuals per hectare. No ripe ovulate cone was found, precluding the observation
of seed dispersers. Almost a quarter of monitored plants presented an ant nest near or within its root
system. The ants identified belonged to five genera: Camponotus, Cyphomyrmex, Megalomyrmex,
Odontomachus, and Rogeria. Zamia pseudoparasitica has unique ecological attributes related to
its peculiar life history. We believe the species should receive more attention from environmental
authorities and the public to help preserve its habitat.
Resumen - La cícada endémica de Panamá Zamia pseudoparasitica Yates fue monitoreada en el parque
nacional Omar Torrijos, Provincia de Coclé, entre mayo y julio de 2018. Es la única especie de gimnosperma
estrictamente epífita y su historia natural es poco conocida debido a que la especie se encuentra a alturas
poco accesibles (10-20 metros). Usando una técnica de escalado de árboles con un nudo prussik, evaluamos
la densidad de la población, la estrategia de diseminación y la especificidad de jardines de hormigas. Zamia
pseudoparasitica es bastante común en partes del parque nacional y se encuentran hasta 24 individuos por
hectárea. No encontramos conos ovulados maduros así que no pudimos observar los diseminadores de las
semillas. Aproximadamente, una de cuatro de las plantas monitoreadas tenía un jardín de hormigas en su
sistema de raíces. Las hormigas identificadas pertenecían a cinco géneros: Camponotus, Cyphomyrmex,
Megalomyrmex, Odontomachus y Rogeria. Zamia pseudoparasitica tiene características ecológicas únicas
relacionadas a su hábit peculiar. La especie debería recibir más atención por parte de las autoridades y del
publico para ayudar en la preservación de su hábitat.
Introduction
The Neotropical genus Zamia (Zamiaceae, Cycadales) includes 81 accepted species
names (Calonje et al. 2018, 2019), many of which have a very restricted range. It is
arguably the most ecologically diverse genus of cycads (Jones 2002). Panama has
seventeen species of which twelve are endemic, including Zamia pseudoparasitica
Yates—the only known strictly epiphytic gymnosperm (Stevenson 1993; Taylor et al.
2008, 2012, 2014). The naturalist of the H.M.S. Herald, Berthold Seemann (1854), first
published the name Zamia pseudoparasitica. He referred to an epiphytic Zamia described
by J. Yates and collected by J. Warszewicz in Chagres, Provincia de Panamá. Dressler
(1975) brought the strange epiphyte back into botanists’ sight after recollecting the
plant near Santa Fe, Provincia de Veraguas. The morphology has been well-documented
(Stevenson 1993, Taylor et al. 2012) and we recently uncovered a specialized symbiotic
1Department of Wood and Forest Sciences, Laval University, Québec, QC, Canada. G1V 0A6.
philipbelldoyon@gmail.com. 2Department of Biology, Laval University, Québec, QC, Canada. G1V 0A6.
juan-carlos.villarreal-aguilar@bio.ulaval.ca
Manucript Editor: Klaus Mehltreter
2:1-7
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P. Bell-Doyon and J.C. Villarreal A.
2020 No. 2
2
bacteriome within the coralloid roots of the species (Bell-Doyon et al. 2020). The weevil
beetle Notorhopalotria taylori Tang and O'Brien has been identified in staminate cones
and seems to be the main pollinator (O’Brien and Tang 2015). The beetle may be attracted
by an odor-mediated push-pull mechanism (Terry et al. 2007). Zamia pseudoparasitica
is classified as “near threatened” on the IUCN red list (Taylor 2010), mainly because of
deforestation and poaching (Stevenson et al. 2003). For example, in the Donoso region
(Provincia de Colón), 13,600 hectares of intact landscape will be deforested due to copper
mining (First Quantum Minerals 2017). Donoso harbors thousands of Z. pseudoparasitica
individuals and the mining activities threaten one of the largest known populations
(Villarreal, pers. obs.). This paper aims to provide novel ecological information and to
raise awareness about this peculiar and precious species of cycad.
Study Site and Method
Zamia pseudoparasitica was surveyed from May to July 2018 in the Omar Torrijos
National Park, Provincia de Coclé, between 500 and 1100 meters above sea level. The
study site is an undisturbed rainforest located 18 kilometers away (straight line) from the
Donoso border and the closest mining site. Trails were carefully scouted for the presence
of Z. pseudoparasitica (Fig. 1) and georeferenced every time at least one individual was
sighted. At each point, we noted the number of plants per tree and evaluated the presence of
cones. Plant population density per hectare was estimated based on a 25 m linear buffer zone
Figure 1. Zamia pseudoparasitica with an ovulate cone located more than 20 m above ground in the Omar
Torrijos National Park, Coclé, Panama. See how the branch is densely crowded by epiphytes. Credit photo:
Maycol Madrid. Used with permission.
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P. Bell-Doyon and J.C. Villarreal A.
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Figure 2. Trail map (with 25 m buffer zones in gray) representing the distribution of sterile and fertile Zamia
pseudoparasitica in the surveyed area. The coordinates and exact location of the population are not shown to
protect the species from poachers, but they are available to researchers upon request.
Figure 3. Plant size and number of leaves for the 95 individuals evaluated. A. Frequency distribution of plants
according to their number of leaves; B. Mean number of leaves per size category (Very small n=4; Small
n=30; Medium n=40; Large n=19; Very large n=2).
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P. Bell-Doyon and J.C. Villarreal A.
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(approximate average visibility) on both sides of the monitored trails using ArcGIS (Fig.
2). The total area surveyed was 34.1 hectares along 7.38 km of trails. Because the number
of individuals varied greatly among trails, we evaluated density independently for each of
the four trails. For one of the most densely populated trails, we noted the relative size and
the number of leaves of each plant. Relative size was visually assessed to five categories
from ground level. We plotted descriptive data (Fig. 3) in R (https://www.r-project.org/).
A camera trap was set up in front of the only accessible ovulate cone for six consecutive
weeks. Regular observation periods were conducted of three of the most developed ovulate
cones to observe seed-dispersers. We used a single-rope and prussik-knot tree climbing
technique to reach 55 plants up to 15 m above ground. We dug out by the base of the cycad
to expose its roots. When ants were observed, we collected two to three individuals with
larvae from the root system of Z. pseudoparasitica.
Results and Discussion
Zamia pseudoparasitica did not recolonize 50-year old adjacent secondary growth.
Plants seem to grow mainly on large horizontal branches and in branch forks, on many
species of canopy trees and at any height apart from the uppermost and thinnest canopy
branches. In the undisturbed forest, we counted from ground level a total of 422 individuals
of which 19 were fertile (seven staminate and 12 ovulate plants). The smallest fertile plant
was a medium-sized cycad with only four leaves. Population density varied from 2.8 to 24.7
plants per hectare, depending on the trail, for an average of 12.4 plants per hectare in the
total surveyed area (34.1 ha). Density is likely to be underestimated because: 1. failure to
detect all individuals and; 2. a seemingly single large plant from ground level sometimes
turned out to be an agglomeration of many individuals of varying sizes, once we climbed
up the trees. For the 95 plants evaluated, the mean number of leaves per plant was 5.8 and
the most common plants were of medium size (n = 40) (Fig. 3). We believe the demographic
pattern may indicate that the local population is not at risk, with many individuals in all
size categories, and the presence of several fertile plants. The longest leaf we have seen
was about 2 m and the smallest 20 cm long. None of the ovulate cones were ripe, hence
no observation of sarcotesta consumption nor seed dispersal was made. We couldn’t assess
whether there is a seasonal pattern in cone ripening. Seeds may be dispersed by arboreal
mammals as in aroids (Vieira and Izar 1999). However, we believe that, as has been
suggested before (Stevenson 1993), medium to large fruit-eating bats (e. g. Artibeus spp.)
might be particularly good candidates because they: 1) tend to be abundant in Neotropical
forests (Rex et al. 2008), 2) consume the skin and pulp of some larger fruits (e.g. Eugenia
spp., Spondias spp.) without damaging the seeds (Ortega and Castro-Arellano 2001),
3) transport food-items to a secondary site before eating it (Morrison 1978), and 4) use
olfactory cues to locate ripe fruits (Rieger and Jakob 1988). The smell of ripe mucilaginous
sarcotesta from ovulated cones of Z. pseudoparasitica has been described as “rank/sour”
(Stevenson 1993), a typical smell of bat-consumed flowers (Helve rsen and Winter 2003).
Like most cycads, Z. pseudoparasitca possesses primary, secondary, and apogeotropic
coralloid roots (Taylor et al. 2008). Some ant species are known to create garden-like
structures within the root system of a wide range of epiphytic angiosperm families
(Davidson 1988). Those ant-gardens are known to contribute to nutrient uptake in
epiphytic tropical plants, including Bromeliaceae and Asclepiadaceae (Gonçaives et al.
2016, Treseder et al. 1995). Ants were found with larvae in the root system of 13 out of 55
plants reached by climbing. Neither specificity nor correlation with plant size was evident,
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P. Bell-Doyon and J.C. Villarreal A.
2020 No. 2
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ants with larvae were found in large and small plants growing from 2 to 15 meters above
ground. Odontomachus hastatus Fabricius (n = 2) and O. erythrocephalus Emery (n =
2) were the only two ant species observed managing an extensive garden-like structure
crowned by diverse epiphytes including Z. pseudoparasitica. Other ants identified to genus
(Camponotus (n = 3), Cyphomyrmex (n = 1), Megalomyrmex (n = 3), and Rogeria (n = 2))
only had small and localized breeding colonies within the tertiary root system of the cycad.
Odontomachus and Camponotus species are known to manage ant-gardens in bromeliads
(Camargo and Oliveira 2012, Leroy et al. 2017). Cyphomyrmex and Megalomyrmex are
fungi-growing ant genera (Mueller et al. 2001, Murakami and Higashi 1997) and Rogeria
are tiny ants of very little-known habits (Lapolla and Sosa-Calvo 2006). Many species of
epiphytic plants were crowded around the cycads where garden-forming ants were found;
we therefore believe that these may not associate specifically w ith Z. pseudoparasitica.
Conclusion
The absence of Z. pseudoparasitica from adjacent 50-year old secondary growth
highlights the value of undisturbed forests for long-term in-situ conservation of
viable populations. Its endemism to Panama and unique epiphytic habit make Zamia
pseudoparasitica a promising candidate to promote as a flagship species (Caro 2010).
Currently, the plant is only classified as “near-threatened” in the IUCN red list (Taylor
2010). We stress the need for revaluating its conservation status in this decade considering
the growing threat from mining activities. Such intensive mining poses a real threat to large
populations (e.g. Donoso) located outside of protected areas. We suggest the creation of
a network of small protected areas (10-50 ha) in the Donoso region to protect pockets of
particularly high cycad density without significantly curbing mining interests in the region.
Future research should focus on population size and turnover, genetic diversity, and seed
dispersal.
Acknowledgments
We would like to thank the Cycad Society and the Smithsonian Tropical Research
Institute (STRI) for providing grants necessary to the success of this project. To Dra.
Noris Salazar Allen for her invaluable support at STRI and in Panama. To profs. Roberto
Cambra and Jorge Mendieta from the University of Panama for identifying the ants and
sharing insights on cycads. To Maycol Madrid and Lilisbeth Rodriguez for their very
precious help in logistics and sampling. This project was part of the research led by J.C.
Villarreal (Université Laval, STRI) and K. Saltonstall (STRI) and financed by SENACYT
(Panama; Contract No. 12-2018-4-FID16-237) which aims at documenting the genomic
diversity of endemic species and their endophytes. The program Établissement de nouveaux
chercheurs universitaires - FRQNT-206943 (Québec) and the Research Chair of Canada
on the genomics of the symbiosis between gymnosperms and microbes also participated in
funding.
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