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Microhabitat Use and Spatial Distribution in Picado's Bromeliad Treefrog, Isthmohyla picadoi (Anura, Hylidae)

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Microhabitat use and spatial distribution in Picado's Bromeliad Treefrog, Isthmohyla picadoi (Anura, Hylidae). Isthmohyla picadoi is a Neotropical hylid frog found in upper humid montane forests of Costa Rica and Panama. The species is of particular interest because it continues to persist in an area in which the amphibian community has otherwise been decimated by the pathogenic fungus, Batrachochytrium dendrobatidis. Ground search, ladder climbing, and tree climbing techniques were used to locate 32 individuals; including adult males and females, juveniles, and metamorphosing frogs. The majority of frogs were found in bromeliads, although some individuals were found on plants of the Euphorbiaceae, Musaceae, and Heliconiaceae families. Most frogs were found in larger bromeliads (45 cm or wider). There was a positive correlation between SUL and bromeliad width within the population but not within maturity classes (adult males, adult females, all adults, non-metamorphosing juveniles), suggesting that juvenile and adult frogs differ in bromeliad usage. Ranges of SUL and body weight in this particular population are much greater than those reported in previous species accounts.
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Phyllomedusa
- 8(2), December 2009
125
Microhabitat use and spatial distribution in
Picado’s Bromeliad Treefrog, Isthmohyla picadoi
(Anura, Hylidae)
Adam M. M. Stuckert, Joshua P. Stone, Jennifer R. Asper, Michael G. Rinker, Cameron L.
Rutt, Nicole C. Trimmer, and Erik D. Lindquist
Department of Biological Sciences, Messiah College, One College Avenue, Grantham, PA 17027 USA. E-mails:
adammmstuckert@gmail.com, joshuapstone@gmail.com, jennifer.asper@gmail.com, mgrink@msn.com,
cameronrutt@gmail.com, nicoletrimmer@gmail.com, quist@messiah.edu.
Received 18 May 2009.
Accepted 25 November 2009.
Distributed December 2009.
Phyllomedusa 8(2):125-134, 2009
© 2009 Departamento de Ciências Biológicas - ESALQ - USP
ISSN 1519-1397
Abstract
Microhabitat use and spatial distribution in Picado’s Bromeliad Treefrog,
Isthmohyla picadoi (Anura, Hylidae). Isthmohyla picadoi is a Neotropical hylid frog
found in upper humid montane forests of Costa Rica and Panama. The species is of
particular interest because it continues to persist in an area in which the amphibian
community has otherwise been decimated by the pathogenic fungus, Batrachochytrium
dendrobatidis. Ground search, ladder climbing, and tree climbing techniques were
used to locate 32 individuals; including adult males and females, juveniles, and
metamorphosing frogs. The majority of frogs were found in bromeliads, although
some individuals were found on plants of the Euphorbiaceae, Musaceae, and
Heliconiaceae families. Most frogs were found in larger bromeliads (45 cm or wider).
There was a positive correlation between SUL and bromeliad width within the
population but not within maturity classes (adult males, adult females, all adults, non-
metamorphosing juveniles), suggesting that juvenile and adult frogs differ in
bromeliad usage. Ranges of SUL and body weight in this particular population are
much greater than those reported in previous species accounts.
Keywords: Anura, Hylidae, Isthmohyla picadoi, bromeliad, phytotelmata, upper
humid montane forest, Batrachochytrium dendrobatidis.
Phyllomedusa
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126
Introduction
Picado’s Bromeliad Treefrog, Isthmohyla
picadoi (Dunn 1937), formerly Hyla picadoi, is
a medium-sized Neotropical hylid frog (SVL:
27-32 mm; 34-35 mm) which inhabits
epiphytic bromeliads in humid montane forests
of Costa Rica and Panama (Duellman 2001,
Savage 2002, Faivovich et al. 2005). Tadpoles,
metamorphosing juveniles, and adults have all
been found together in bromeliads, suggesting
the possibility of an entirely arboreal life cycle
Resumen
Uso de microhábitats y distribución espacial de la rana arboricola de bromelia de Picado, Isthmohyla
picadoi (Anura, Hylidae). Isthmohyla picadoi es una rana Neotropical de la familia Hylidae que habita
en los bosques húmedos montanos de la parte alta de la región de Talamanca entre Costa Rica y Pana-
má. Esta especie es de interés en particular, porque continua sobreviviendo en una área afectada por el
hongo patogénico, Batrachochytrium dendrobatidis. Buscamos ranas al nivel del suelo, y en árboles,
subiendo tanto por escalera, como trepando por soga. Recolectamos datos correspondientes a 32
individuos, incluyendo machos y hembras adultos, juveniles, y ranas en metamorfosis. La gran mayoría
de las ranas fueron encontradas en bromelias grandes (45 cm o más de anchura), y algunos individuos
fueron localizados en plantas de las familias Euphorbiaceae, Musaceae, y Heliconiaceae. Se encontró
una correlación positiva entre la longitud hocico-urostilo (LHU) y la anchura de la bromelia dentro de
la población, pero ningúna correlación dentro de cada una de las clases de madurez (machos adultos,
hembras adultas, todos los adultos, y juveniles que no están en metamorfosis), lo que sugiere que los
adultos y juveniles usan diferentemente las bromelias. Estos datos también indican que los rangos de
tamaño tanto en la longitud hocico-cloaca (LHC) como en el peso de esta población son mucho mas
amplios que los descritos previamente para esta especie.
Palabras Claves: Anura, Hylidae, Isthmohyla picadoi, bromelia, phitotelmata, altos bosques húmedos,
Batrachochytrium dendrobatidis.
Resumo
Uso de micro-habitats e distribuição espacial de Isthmohyla picadoi (Anura, Hylidae). Isthmohyla
picadoi é um anuro neotropical da família Hylidae que habita os bosques úmidos da porção alta da re-
gião de Talamanca, entre a Costa Rica e o Panamá. Essa espécie é de particular interesse porque conti-
nua sobrevivendo em uma área em que outras espécies da comunidade de anfíbios foram dizimadas pelo
fungo patogênico Batrachochytrium dendrobatidis. Os indivíduos foram localizados por procura no solo
e por técnicas de escalada com escadas e escalada de árvores. Foram coletados dados de 32 indivíduos,
incluindo machos e fêmeas adultos, juvenis e girinos em metamorfose. A grande maioria dos animais
foi encontrada em bromeliáceas grandes ( 45 cm de largura), embora alguns indivíduos tenham sido
localizados em plantas das famílias Euphorbiaceae, Musaceae e Heliconiaceae. Houve uma correlação
positiva entre o comprimento rostro-cloacal dos anuros e a largura das bromeliáceas dentro da popula-
ção mas não dentro das classes de maturidade (machos adultos, fêmeas adultas, todos os adultos, juve-
nis), sugerindo que os juvenis diferem dos adultos no uso das bromeliáceas. A amplitude de variação do
comprimento rostro-cloacal e do peso corpóreo dessa população foi muito maior do que aquela registra-
da em estudos anteriores com essa espécie.
Palavras-chave: Anura, Hylidae, Isthmohyla picadoi, bromeliáceas, fitotelmata, floresta úmida alto-
montana, Batrachochytrium dendrobatidis.
(Savage 2002). The rosette configuration of
bromeliad axils form tank-like phytotelmata, a
critical microhabitat for amphibians, plants,
insects, arachnids, crabs, and annelids (Maguire
1971, Fish 1983, Catling and Lefkovitch 1989,
Fragoso and Rojas-Fernandez 1996, Araújo
et al. 1997). Physical aspects of these
phytotelmata, specifically water temperature,
are important to amphibian species (Piotrowski
2004). Isthmohyla picadoi inhabits primary,
secondary, and transitional forests along the
Central and Talamancan Cordilleras of Costa
Stuckert et al.
Phyllomedusa
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127
Rica and western Panama from 2,000 to 2,200
m above sea level (asl) (Duellman 2001, Savage
2002, Solis et al. 2008). Scant information on
the natural history of this species is limited to
species accounts provided by (Duellman 2001,
Savage 2002) and a description of their
vocalization (Lindquist and Cossel 2007).
The population from the Cerro Punta region
of the Chiriquí highlands of western Panama is
of particular interest because it persists despite
catastrophic declines and extinctions of
amphibian species due to Batrachochytrium
dendrobatidis (Bd hereafter). Species that
disappeared rapidly after the 1994 Bd epidemic
were primarily those whose life cycle involved
direct contact with stream water (Lips 1999).
Although I. picadoi has long been considered
a canopy specialist, individuals have been found
on rocks in streams on at least two occasions
(Duellman 2001). These observations suggest
a potential mechanism of vertical stream-to-
canopy transfer as well as up-slope dispersion
of Bd. As I. picadoi has been encountered
within and near bromeliads containing high
Bd zoospore concentrations (Cossel and
Lindquist 2009), it is possible that individuals
which travel between streams and bromeliads
transmit the fungus to more terrestrial
habitats.
This study presents data on the microhabitat
use and spatial distribution of I. picadoi with
respect to various physical and structural
environmental parameters from a site in the
Chiriquí Highlands of western Panama. This
information may be crucial in understanding
why this species has persisted after the decline
or disappearance of the majority of amphibian
species in this region, which is attributed to the
Bd epidemic of 1994.
Materials and Methods
Study area
We studied a population of I. picadoi
immediately north of Guadalupe Arriba,
Chiriquí Province, in the Republic of Panama
(8o52’10.0” N, 82o34’0.5” W) between 3 and 29
January 2008 (Figure 1). For the purpose of our
study, we subdivided this area into four sites
based on the location of vocalizing clusters of
I. picadoi. These sites included primary,
secondary, and transitional riparian humid
forest, ranging in altitude from 1,950 to 2,300 m
asl (Table 1). Site 1 contained a transition area
between primary and secondary growth forest,
sites 2 and 3 were situated within primary
growth forest, and site 4 straddled the border of
a secondary forest and the edge of a botanical
garden and contained more bromeliads than any
other site. Sites 1-3 were located in the forest
preserve owned by Los Quetzales Lodge and
Spa, and site 4 was located in a small forest
tract in the Finca Dracula, owned by Andrés
Maduro. Both properties border the Parque
Internacional La Amistad and Parque Nacional
Volcán Barú.
Locating individuals
We located frogs via two techniques: 1)
thoroughly searching bromeliads (especially
leaf axils, interaxil spaces, and phytotelmata) at
random both at day and night; and 2)
triangulating male position immediately after
vocalizations were given (mostly from
epiphytes) at night. Epiphytic vegetation
(bromeliads and mosses) was searched at
heights from 0 to 33.5 m above the ground.
These epiphytes occupied tree limb and trunk
surfaces primarily on Sapium laurifolium
(Euphorbiaceae), Alnus acuminata (Betulaceae),
and one Schefflera sp. (Araliaceae). Trees and
epiphytes were searched using three methods:
ground searches, ladder searches, and climbing
using the Single Rope Technique (SRT) (Maher
2006). Ground searches entailed examining
fallen bromeliads or those within standing
reach. Ladder climbs employed a 7.3 m
extension ladder to access higher bromeliads.
Tree climbs using the SRT, which reached
heights up to 33.5 m, were used to sample
Microhabitat use and spatial distribution in Isthmohyla picadoi (Anura, Hylidae)
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bromeliads otherwise inaccessible to ground
and ladder searches. All bromeliads were
measured at the widest point across to the
nearest 5 cm increment using a pre-measured
metal hook tool (29” Mark O’Shea Signature
Series Hook, Midwest Tongs Inc.). Generally,
the longest width was found tangential to the
tree surface on which the bromeliad was anchored.
Data collection and animal care
To prevent further spread of Bd, latex gloves
were worn while capturing and handling each
frog and frogs were placed into individual
plastic bags. Further, any objects that came into
Figure 1 - Map of the sites 1-4 in the study area along the Río Chiriquí Viejo near Guadalupe Arriba, Chiriquí Province,
Panama.
contact with a frog (i.e. hands, equipment, all
surfaces) were wiped with 95% isopropyl
alcohol. Water temperature was investigated in
order to determine if physical aspects of the
phytotelmata were thermally detrimental to Bd
growth. For eleven of the bromeliads in which
frogs were found (widths= 25, 45, 45, 50, 65,
70, 80, 80, 92, 95, and 105 cm), a thermometer
was placed in the bromeliad’s phytotelm for at
least 24 hours to record the minimum and
maximum water temperatures. As a control, a
thermometer was also placed in the
phytotelmata of eighteen randomly selected
bromeliads for at least 24 hours. For each frog
collected ambient air temperature, bromeliad
Stuckert et al.
Phyllomedusa
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129
water temperature, height above the ground,
distance to canopy, calling activity, bromeliad
(or other plant) width, collector’s name, date
and time of capture were recorded. Distance to
canopy and ground measurements were taken
using a Bushnell Yardage Pro Trophy 5x20
Rangefinder.
Frogs were taken back to our field base
after collection. To promote ecdysis, a small
amount of rainwater was added to each bag,
where the frog remained for at least 24 hours.
After 24 hours, shed skin was removed from
the bag and placed in a labeled vial along
with an epidermal swab of the individual for
later detection of Bd. Using Savage’s key
(2002), individuals were positively identified
as I. picadoi by the presence of two odontoids
at the symphysis of the lower jaw. Frogs were
also weighed, measured for snout-vent length
(SVL) and snout-urostyle length (SUL), sexed
noting the presence of nuptial pads in adult
males or calling activity, and photographed.
Although SUL was used in the analyses due
to its lower variance, SVL is provided for
comparisons to previous publications on I.
picadoi.
After data and skin were collected from all
individuals found in a study site, frogs were
released back to the host tree on which they
were found. Animal care protocols were
reviewed and approved by the IACUC at the
Smithsonian Tropical Research Institute prior to
the commencement of our study, and research
and collection permits were obtained through
La Autoridad Nacional del Ambiente (ANAM).
No frogs died in this study.
Results
During the study, 32 individuals were
observed and captured from study areas 1 and
4 (n=2 and n=30, respectively): 15 males, 3
females and 14 juveniles; no tadpoles were
found in this study (Table 1). Juveniles
exhibited a body size (SUL) ranging from 14.20
to 21.10 mm. One juvenile appeared to possess
nuptial pads (SUL = 18.7 mm) and four others
were in the process of metamorphosis,
exhibiting tail buds. A linear relationship
between SUL and weight can be seen in Figure
2 (R2=0.9595, p<0.0001).
Accessing frogs
A total of 1,376 bromeliads were inspected
for frogs (site 1: 319, site 2: 248, site 3: 256,
site 4: 553). Of these, 530 (38.5%) were
Microhabitat use and spatial distribution in Isthmohyla picadoi (Anura, Hylidae)
Table 1 - Size (SUL and SVL) and mass of males, females, and juveniles including mean ( ), standard deviation (SD),
and range.
SUL (mm) SVL (mm) Weight (g)
31.50 33.95 2.07
SD 2.37 2.80 0.40
range 26.80-34.80 29.10-37.90 1.13-2.50
35.05 38.23 2.83
SD 2.18 2.09 0.07
range 32.90-37.25 36.50-40.50 2.75-2.85
17.13 19.23 0.42
SD 2.01 2.57 0.16
range 14.20-21.10 16.85-24.95 0.25-0.88
Juveniles
(n=14)
Males
(n=15)
Females
(n=3)
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130
Figure 2 - XY scatter plot showing the linear relationship
between SUL (mm) and weight (g)
(R2=0.9595, p<0.0001). Adult males, adult
females, and juveniles are depicted as
triangles, squares, and circles respectively.
Figure 3 shows the number of I. picadoi
found in bromeliads of different size classes
relative to our search effort, which was
representative of habitat availability in the sites.
Bromeliads smaller than 10 cm in width are too
small to create phytotelmata and as a result
cannot be utilized by I. picadoi; therefore,
Non-bromeliad Total
Study Elevation Ground Ladder Tree Plants with Total Bromeliads
Location (m) Searches Searches Searches Frogs Frogs/Site Searched
12,180-2,270 118 (1) 56 145 (1) 0 2 319
22,120-2,150 76 37 135 0 0 248
32,070-2,120 126 45 85 0 0 256
41,990-2,060 210 (3) 122 (3) 221 (7) 3 30 553
Table 2 - Number of bromeliads searched by each method for each location. The number of bromeliads/plants containing
frogs is indicated in parentheses.
Figure 3 - Bromeliad width categories in which I. picadoi
was encountered. Percentages lying within
each width category represent the percentage
of total bromeliads searched in this study.
examined from the ground, 260 (19%) were
investigated using a ladder, and 586 (42.5%)
were accessed via tree climbing (Table 2). Tree
climbs resulted in 18 of the 32 frogs (56.25%),
ladder climbs resulted in 7 frogs (21.875%), and
ground searches found 7 frogs (21.875%)
(Table 2). Frogs were encountered in only 1.7%
of all bromeliads searched.
Stuckert et al.
Searched Bromeliads by Size
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bromeliads in this size range were not included
in the data analyses. The remaining bromeliads
were split into five categories for data analyses.
No frogs were found in the smallest (10-19 cm)
bromeliad size category, (n=109, 8% of total).
In the 20-29 cm size category (n=238, 17% of
total), a single frog (3.125%) was found. Six
frogs (18.75%) were found in the 30-39 cm
size category, (n=289, 21% of total). In the
40-49 cm size category, (n=181; 13% of
total), 5 frogs (15.625%) were found. In the
largest size category (50+ cm), (n=559, 41%
of total), 16 frogs (50%) were found. Four
frogs (12.5%) were found on plants other than
bromeliads.
Phytotelmic associations
Frogs were primarily found in or on plants
of the Bromeliaceae family (n=28; 87.5%);
however, two frogs were found on Heliconia
lankisteria (Heliconiaceae), one on Ensete
ventricosum (Musaceae), and another on
Sapium laurifolium (Euphorbiaceae). Widths of
bromeliads containing frogs ranged from 25 to
105 cm.
There was a significant positive Spearman
rank-order correlation between frog size (SUL)
and bromeliad width (n=24, rs=0.6697,
p=0.0003, d.f.=22) (Figure 4). However, there
was no statistical significance between SUL and
bromeliad width within any of the maturity
classes (adults, non-metamorphosing juveniles,
adult males, or adult females). Metamorphic
juveniles (n=4) with tail buds were not included
in any statistical analyses relating to bromeliad
choice as all were found emerging from the
same natal bromeliad, indicating parental
choice.
Phytotelmic water temperature
We found a significant difference in
minimum phytotelmic water temperatures
within bromeliads with and without frogs
(frog=10.04oC, no frog=9.35oC, p=0.0455,
z=1.69, nfrog=11, nno frog=18; Mann-Whitney U
test, one-tailed,). However, this was not the case
for the thermal maxima of phytotelmic water
(frog=14.23oC, no frog=13.86oC, p=0.1357,
z=1.1, nfrog=11, nno frog=18; Mann-Whitney U test,
one-tailed). This suggests that in cool montane
microhabitats, minimum phytotelmic water
temperature may be an important environmental
variable determining suitability of bromeliads to
I. picadoi.
Spatial positioning
Vertical positioning for I. picadoi was
particularly variable with respect to distance
from the ground ( =9.98 m; std. dev.=8.41 m;
min=0 m; max=22.5 m; Spearman rank-order;
n=28; rs=0.3112; p=0.1069) (Figure 5) and
distance to the canopy limit ( =13.76 m;
std. dev.=9.93 m; min=0 m; max=34 m;
Spearman rank-order; n=28; rs=-0.2908;
p=0.1332) (Figure 6).
Figure 4 - The relationship between bromeliad width
(cm) and SUL (mm) is shown below. The four
metamorphic juveniles with tail buds excluded
from the statistical trend analysis are circled.
Adult males, adult females, and juveniles are
depicted as triangles, squares, and circles
respectively.
Microhabitat use and spatial distribution in Isthmohyla picadoi (Anura, Hylidae)
Phyllomedusa
- 8(2), December 2009
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Discussion
This study provides new insights into the
biology, microhabitat requirements, and spatial
distribution of a species with scant natural
history information available. This study reveals
the species’ overall size maximum (SVL) is
larger than once thought, with individuals in our
study population exceeding the sizes reported
in Duellman (2001) and Savage (2002). The use
of bromeliads as phytotelmic sources is
critically important for this species, although
individuals were found on plant species of three
other families (Euphorbiaceae, Musaceae, and
Heliconiaceae). No frogs were found in
bromeliads smaller than 25 cm, perhaps
indicating a minimum phytotelmic size
requirement for the species. In addition, there
was a direct correlation between SUL and
bromeliad width in the overall population.
However, this is not statistically significant
Figure 5 - SUL (mm) and weight (g) of each I. picadoi
and their respective spatial distribution relative
to the distance above the ground (m) at time
and place of capture. Adult males, adult
females, and juveniles are depicted as
triangles, squares, and circles respectively.
Figure 6 - SUL (mm) and weight (g) of each I. picadoi
and their respective spatial distribution relative
to the distance to the canopy limit (m) at time
and place of capture. Adult males, adult
females, and juveniles are depicted as
triangles, squares, and circles respectively.
within any of the maturity classes of these frogs
(all adults, adult males, adult females, and non-
metamorphosing juveniles) suggesting that the
correlation is significant largely due to a
juvenile preference for smaller phytotelmic
hosts. This is potentially a result of differences
in bromeliad usage between adults and juveniles.
While adults likely use bromeliads for breeding
– supported by the four metamorphosing
juveniles found together in a relatively large
bromeliad for their size – the focus of juveniles
may be on feeding and finding refuge. A larger
sample size of I. picadoi would further elucidate
size choice in these amphibians across maturity
classes and as a whole. Differences in bromeliad
usage by age class may imply differences in
lifestyles (i.e. a more mobile juvenile lifestyle
and a more stationary, and perhaps territorial,
adult lifestyle), which would have implications
in both the species’ survival in areas infected
by Bd as well as transmission of the fungus.
Stuckert et al.
Phyllomedusa
- 8(2), December 2009
133
Although collecting temperature data over a
longer duration of time would be advantageous
to clarify the interaction of temperature and
phytotelmic water sources, temperature data
gathered in this study indicate that these frogs
may select for bromeliads containing a higher
minimum phytotelmic water temperature. In
effect, this could influence bromeliad size
choice in this species as larger bromeliads,
which contain more water, should moderate the
effects of cool montane nights. Data from these
phytotelmic water sources fall within the
thermal optimal range for Bd in this study, and
likely do not provide refugia for amphibians
adversely affected by chytridiomycosis. Yet this
I. picadoi population still thrives where many
other species have disappeared, likely because
of its primarily arboreal habits (pers. obs.).
The occurrence of metamorphic juveniles
still possessing tail buds implied that our
research in January coincided with the end of
the breeding season in this region. We found no
amplectant pairs, egg masses, or tadpoles,
further supporting this hypothesis. Two adults
were found on a large bromeliad (width=105
cm) containing four metamorphic juveniles;
however, one escaped before a positive
identification of sex could be determined. This
may provide anecdotal evidence which supports
K. Lips’ report that parents remain close to their
young through metamorphosis (Savage 2002).
Many males were still actively calling despite
the lack of observed breeding activity. Lastly,
we recognize that our highly biased sex ratio
was likely a result of our method of discovery—
using vocalizations in some areas to increase
sample sizes—and therefore is probably
unrelated to actual operational sex ratios.
This study suggests that I. picadoi can
utilize a much wider range of habitats than
originally described. Individuals were
encountered at variable heights above the
ground (0 to 22.5 m) with maximum heights
extending much higher than the shrub and
stream heights previously reported (Duellman
2001, Savage 2002). Site 1, a transition area
between primary and secondary growth forest,
yielded 2 frogs. The vast majority of frogs
(n=30) were found at site 4, which consisted
predominantly of secondary forest and had a
greater density of bromeliads than any other
site. This site was the most disturbed of our four
sites. Sites 2 and 3, regions of primary growth,
yielded no frogs. This indicates that although I.
picadoi was formerly thought to be a species of
primary montane forest (Duellman 2001,
Savage 2002), this species has a tolerance to
disturbance and can survive in secondary and
transitional forests as well as a botanical garden
containing bromeliads or other species with
phytotelmic water sources. This is significant
for conservation efforts aimed at this species
and may play a role in the species’ persistence
after the Bd epidemic in the region. Although
much more is yet to be learned about the natural
history of Isthmohyla picadoi, this study
provides invaluable insights into microhabitat
use and spatial distribution.
Acknowledgements
We would like to thank Carlos Alfaro of the
Los Quetzales Lodge and Spa, Andrés Maduro
of Finca Dracula, and their staff for their
willingness to allow us to research on their
properties, as well as providing exceptional
hospitality to our research group. We thank the
Emerging Scholars Network, the Christian
Scholars Foundation, and Messiah College for
providing funding for this endeavor. We are
grateful to the Smithsonian Tropical Research
Institute IACUC for reviewing and approving
our animal care protocols. We are likewise
indebted to La Autoridad Nacional del
Ambiente for providing research and collection
permits (SE/A-114-07) for this study. Lastly, we
thank John Cossel of Northwest Nazarene
University for his canopy field assistance,
Molly Lindquist for her support of the research
team, and the anonymous reviewers for their
comments provided on previous drafts of this
manuscript.
Microhabitat use and spatial distribution in Isthmohyla picadoi (Anura, Hylidae)
Phyllomedusa
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134
References
Lindquist E. D. and J. O. Cossel. 2007. Hyla picadoi
(NCN). Vocalizations. Herpetological Review 38: 438–
440.
Lips, K. R. 1999. Mass mortality and population declines
of anurans at an upland site in western Panama.
Conservation Biology 13: 117–125.
Maguire, B. 1971. Phytotelmata biota and community
structure determination in plant-held waters. Annual
Review of Ecology and Systematics 2: 439–464.
Maher, J. 2006. Canopy access – beyond basic single rope
technique. URL: http://www.treeclimbercoalition.org/
pdfs/CFR.pdf. Captured on 28 August 2007.
Piotrowski, J. S., S. L. Annis and J. E. Longcore. 2004.
Physiology of Batrachochytrium dendrobatidis, a
chytrid pathogen of amphibians. Mycologia 96: 9–15.
Richardson, B. A. 1999. The bromeliad microcosm and the
assessment of faunal diversity in a Neotropical forest.
Biotropica 31: 321–336.
Savage, J. M. 2002. The Amphibians and Reptiles of Costa
Rica a herpetofauna between two continents, between
two seas. Chicago. University of Chicago Press. 934 pp.
Solís F., R. Ibáñez, K. Lips, G. Chaves, J. Savage, C.
Jaramillo, Q. Fuenmayor, F. Bolaños, and E. Lindquist.
2008. Isthmohyla picadoi an online reference.
URL: http://www.iucnredlist.org/details/55600.
Captured on 13 May 2009.
Araújo, V. A., S. K. Melo, A. P. A. Araújo, M. L. M.
Gomes, and M. A. A. Carneiro. 1997. Relationship
between invertebrate fauna and bromeliad size.
Brazilian Journal of Biology 67: 611–617.
Catling, P. M. and L. P. Lefkovitch. 1989. Associations of
vascular epiphytes in a Guatemalan cloud forest.
Biotropica 21: 35–40.
Cossel, J. O., and E. D. Lindquist. 2009. Batrachochytrium
dendrobatidis in arboreal and lotic water sources in
Panama. Herpetological Review 40: 45–47.
Duellman, W. E. 2001. The Hylid Frogs of Middle
America. 2nd ed. Society for the Study of Amphibians
and Reptiles. 1180 pp.
Faivovich, J., C. F. B. Haddad, P. C. A. Garcia, D. R.
Frost, J. A. Campbell, and W. C. Wheeler. 2005.
Systematic review of the frog family Hylidae, with
special reference to Hylinae: phylogenetic analysis and
taxonomic revision. Bulletin of the American Museum
of Natural History 294: 1–240.
Fish, D. 1983. Phytotelmata: fauna and flora. Pp. 1–27 in
J. H. Frank. and L. P. L. Louinbos (eds.), Phytotelmata
– terrestrial plants as hosts for aquatic insect
communities. Medford. Plexus Publishing Inc.
Fragoso, C. and H. Rojas-Fernandez. 1996. Earthworms
inhabiting bromeliads in Mexican tropical rain forests:
ecological and historical determinants. Journal of
Tropical Ecology 12: 729–734.
Stuckert et al.
... In these areas, the cumulative time individuals of a species spend in riparian habitats significantly increases the likelihood of decline [5,[9][10][11][12]. Therefore, even in these hotspots of chytridiomycosis-driven declines, a proportion of species are less affected [9,13,14], a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 especially those with arboreal, bromeliad-associated habits [15][16][17][18]. The reasons for these differential infection and disease dynamics of Bd have been suggested to be multifactorial and dependent on local environmental-, host-and pathogen-associated factors [13,[19][20][21][22][23][24]. ...
... Thirty-two bromeliads and twelve sampling locations derived from the main stream running through CNP were selected for sampling. Large bromeliads (circumference >45 cm) were sampled in order to allow sufficient water volumes (30 ml) to be withdrawn and due to the preference of bromeliad-associated amphibians for larger specimens [16]. For each bromeliad and stream site, GPS coordinates, canopy openness (improved Moosehorn design [35]), water pH (pH test kit, JBL GmbH & co, Neuhofen Germany), water temperature and ambient air temperature were recorded. ...
... Although the IUCN dataset used for these calculations also include non-peer reviewed literature and expert opinions, it does indicate a clear difference in the conservation status and susceptibility to Bd of bromeliad-and stream-associated amphibians in Central America. This agrees with previous studies suggesting that Central American amphibian species associated with bromeliads may be less affected in Bd outbreaks than riparian species in the same region [15][16][17][18]. Within Cusuco National Park (CNP), this same trend is observed: there are three declining riparian amphibian species in which chytridiomycosis is a suspected driver, while no negative population trends are reported for the bromeliad-associated species [18,25]. ...
Article
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The fungal pathogen Batrachochytrium dendrobatidis (Bd) drives declines and extinctions in amphibian communities. However, not all regions and species are equally affected. Here,we show that association with amphibian aquatic habitat types (bromeliad phytotelmata versus stream) across Central America, results in the odds of being threatened by 'Bd' being five times higher in stream micro-habitats as appose to that of bromeliads. This differential threat of 'Bd' was supported in our study by a significantly lower prevalence of 'Bd' in bromeliad-associated amphibian species compared to riparian species in Honduran cloud forests. Evidence that the bromeliad environment is less favorable for 'Bd' transmission is exemplified by significantly less suitable physico-chemical conditions and higher abundance of 'Bd'-ingesting micro-eukaryotes present in bromeliad water. These factors may inhibit aquatic 'Bd' zoospore survival and the development of an environmental reservoir of the pathogen. Bromeliad phytotelmata thus may act as environmental refuges from 'Bd', which contribute to protecting associated amphibian communities against chytridiomycosis-driven amphibian declines that threaten the nearby riparian communities.
... Picado's Bromeliad Treefrog, Isthmohyla picadoi (Dunn 1937), is an arboreal, bromeliad-dwelling species found in primary, secondary, and transitional humid montane forests of Costa Rica and Panama (Duellman 2001;Faivovich et al. 2005;Savage 2002;Solis et al. 2008). Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source water temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other amphibian species in the region due to Bd (Lips 1999). ...
... Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source water temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other amphibian species in the region due to Bd (Lips 1999). Although no data on the population exists prior to the arrival of Bd, the population currently appears to be stable based on the number of vocalizations heard throughout the study site over multiple years ranging from 2000 to 2008 (pers. ...
... obs.). Stuckert et al. (2009) suggested I. picadoi may be a potential vector of vertical stream-to-canopy Bd zoospore transfer as well as stream-to-terrestrial dispersal. However, their study did not present evidence of Bd infection in I. picadoi, nor any correlation between infection in I. picadoi and presence of Bd in phytotelmata. ...
Article
Full-text available
The pathogenic fungus Batrachochytrium dendrobatidis (Bd) has been implicated as the cause of many global am-phibian declines (Berger et al. 1998; Bosch et al. 2001; Briggs et al. 2005; Longcore et al. 1999; Ron and Merino 2000; Skerratt et al. 2007). Central American amphibians have experienced substantial declines (Stuart et al. 2004, 2008) and Bd has been identified as the cause in a number of these (Crawford et al. 2010; Lips et al. 2006). A more thorough understanding of the natural history and ecology of Bd is still needed, and knowl-edge of the geographic distribution of this fungal pathogen is important for biological conservation (Adams et al. 2007; Young et al. 2001). Likewise, modes of Bd dispersal are poorly understood; amphibians and water sources are implicated as the primary vectors, but birds and soil are potentially im-portant vectors as well (Johnson and Speare 2005). Bd has also been implicated in historic die-offs in the highlands of western Panama (Lips 1999; pers. obs) and has been detected in environmental water gathered from both lotic and lentic sources (arboreal phytotelmata) in the region (Cossel and Lindquist 2009). Picado's Bromeliad Treefrog, Isthmohyla picadoi (Dunn 1937), is an arboreal, bromeliad-dwelling species found in primary, secondary, and transitional humid montane for-ests of Costa Rica and Panama (Duellman 2001; Faivovich et al. 2005; Savage 2002; Solis et al. 2008). Stuckert et al. (2009) found that I. picadoi inhabits phytotelmata with source wa-ter temperatures that fall within the reproductive thermal range of Bd in laboratory settings as found by Piotrowski et al. (2004). The population of I. picadoi from the highlands of western Panama studied by Stuckert et al. (2009) persists despite catastrophic declines and extinctions of other am-phibian species in the region due to Bd (Lips 1999). Although no data on the population exists prior to the arrival of Bd, the population currently appears to be stable based on the number of vocalizations heard throughout the study site over multiple years ranging from 2000 to 2008 (pers. obs.). Stuck-ert et al. (2009) suggested I. picadoi may be a potential vector of vertical stream-to-canopy Bd zoospore transfer as well as stream-to-terrestrial dispersal. However, their study did not present evidence of Bd infection in I. picadoi, nor any cor-relation between infection in I. picadoi and presence of Bd in phytotelmata. In this study, we set out to determine: 1) whether Bd is detectable in the population of I. picadoi at the study site described by Stuckert et al. (2009) and Cossel and Lindquist (2009); and if so, 2) the prevalence of infection; and 3) whether any connection exists between Bd infections in individual frogs and phytotelmic water sources. We studied a population of I. picadoi immediately north of Guadalupe Arriba, Chiriquí Province, in the Republic of Panama (8.869444°N, 82.566806°W) between 3 and 29 Janu-ary 2008 [same population as Stuckert et al. (2009)]. Study sites included primary, secondary, and transitional riparian humid forest, ranging in elevation from 1,950 to 2,300 m el-evation. Sites were located in a private forest preserve owned by Los Quetzales Lodge and Spa, and in a small forest tract in the Finca Dracula, owned by Andrés Maduro. Both proper-ties border the Parque Internacional La Amistad and Parque Nacional Volcán Barú. We located I. picadoi, via two techniques: 1) randomly searching bromeliads (leaf axils and phytotelmata) at both day and night; and 2) triangulating male nocturnal position immediately after vocalization. Epiphytic bromeliads and mosses were searched at heights ranging from 0 to 33.5 m AMPHIBIAN DISEASES AMPHIBIAN DISEASES
... [7,12,13,14]). Several bromeliad traits are associated with the presence of anurans, including humidity, water availability and phytotelmata size [15][16][17][18]. More generally, the high microhabitat stability of phytotelmata makes them potentially important refuges during adverse environmental conditions. ...
... More salamanders were found in bromeliads with larger phytotelmata and cooler water. This is broadly in concordance with previous studies that have reported that humidity, water availability, and phytotelm size have been reported to play a major role in anuran microhabitat selection [15][16][17][18]. Such correlations are potentially driven by the role of bromeliad phytotelmata as refuges from temperature extremes and low humidity [7,12,19]. ...
Article
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Bromeliad phytotelmata are frequently used by several Neotropical amphibian taxa, possibly due to their high humidity, microclimatic stability, and role as a refuge from predators. Indeed, the ability of phytotelmata to buffer against adverse environmental conditions may be instrumental in allowing some amphibian species to survive during periods of environmental change or to colonize sub-optimal habitats. Association between bromeliad traits and salamanders has not been studied at a fine scale, despite the intimate association of many salamander species with bromeliads. Here, we identify microhabitat characteristics of epiphytic bromeliads used by two species of the Bolitoglossa morio group (B. morio and B. pacaya) in forest disturbed by volcanic activity in Guatemala. Specifically, we measured multiple variables for bromeliads (height and position in tree, phytotelma water temperature and pH, canopy cover, phytotelma size, leaf size, and tree diameter at breast height), as well as salamander size. We employed a DNA barcoding approach to identify salamanders. We found that B. morio and B. pacaya occurred in microsympatry in bromeliads and that phytotelmata size and temperature of bromeliad microhabitat were the most important factors associated with the presence of salamanders. Moreover, phytotelmata with higher pH contained larger salamanders, suggesting that larger salamanders or aggregated individuals might modify pH. These results show that bromeliad selection is nonrandom with respect to microhabitat characteristics, and provide insight into the relationship between salamanders and this unique arboreal environment.
... Despite E. salvaje not being associated with 'traditional' sites for Bd transmission i.e. streams, pools and bromeliads, there is potential for Bd transmission into canopy environments through residue left on vegetation from other sympatric amphibian species that move between aquatic and terrestrial habitats (Kolby et al. 2015a), as well as potentially being transmitted by wind, waterfall spray and rainfall (Kolby et al. 2015b). Studies outside of Cnp have suggested that canopy-dwelling frogs may act as vectors for Bd (Stuckert et al. 2009;Lindquist et al. 2011), and that the damp arboreal refuges they inhabit (e.g. bromeliads) might serve as chytrid reservoirs (Cossel & Lindquist, 2009). ...
Article
Full-text available
Cusuco National Park (CNP), a montane cloud forest in north-western Honduras, harbours what is thought to be among the last known populations of the Endangered Copán Fringe-limbed Tree Frog, Ecnomiohyla salvaje. This paper provides novel information that may inform the conservation status of this species whilst simultaneously building on its poorly known natural history. We add to the four total confirmed adult records from 1982-2014 by reporting an additional three adult individuals encountered between 2014 and 2018. Additionally, we provide the first descriptions of two late stage tadpoles (herein referred to as metamorphs), which adds to the information given on adults and earlier life stages in the species authority paper. We also correct and include formal photographs for the original known, but as yet ‘unvouchered’ E. salvaje observation in 2009 at CNP. We present morphometrics for most individuals encountered, as well as details of their natural habitat, defensive behaviour and ecology. Our observations of E. salvaje support the hypothesis that this canopy adapted species may be dependent on tree holes within intact forest. Being a tree-hole breeding species, the simultaneous presence of adult E. salvaje in tree holes with late stage tadpoles nearby, suggests that there may be an element of parental care towards offspring. Skin swabs from four E. salvaje individuals were tested via QPCR analysis for the presence of amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd); all these individuals tested positive for Bd, with infection loads ranging 0.24 - 53.96 Bd Genomic Equivalents. These results may have significant implications for the conservation of E. salvaje, considering chytridiomycosis likely led to severe population declines and/or the possible extinction of its congener E. rabborum.
... Based on the IUCN criterion, this frog should be assessed in a more restrictive EN category. All the 1900-2650Dunn 1937, Duellman 1970, Lips 1998, Savage 2002, Stuckert et al. 2009, Frost 2016 Isthmohyla zetecki NT Unidentified 1200-1804 Dunn 1937, Duellman 1970, Savage 2002, Frost 2016 Osteocephalus deridens Osteocephalus planiceps ...
Article
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Bromeliads constitute a good example of symbiosis with organisms that spend their entire life cycle inside the plants, and often depend on them to breed. The bromeliads benefit from this interaction by increasing their nutrients intake. Conservation efforts tend to focus on a single endangered species, but in symbiotic associations, the viability of one species depends on that of the other. Based on IUCN criteria, any species that depends on another to complete its life cycle should be assigned a conservation status equivalent to that of the host taxon, where appropriate. We gathered published plus fieldwork data on the frog-bromeliad mutualism and compiled a checklist of 99 bromeligenous frogs species associated to 69 bromeliad hosts, and found threatened bromeliads hosting non-threatened frogs. We found that 62% bromeligenous frogs inhabit unspecified bromeliads. Finally, we propose strategies for improving understanding and conservation of the frog-bromeliad mutualism.
... Isthmohyla species, such as bromeliad-dwelling I. picadoi and I. zeteki and pond-breeding I. pseudopuma, persist in Bd-positive areas (Stuckert et al., 2009) and were considered less susceptible (Table 2). ...
Article
Full-text available
Amphibians around the world are declining from threats that cannot currently be mitigated, making it impossible to safeguard some species in their natural habitats. Amphibians in the mountainous neotropics are one example where severe disease-related declines prompted calls for the establishment of captive assurance colonies to avoid extinctions. We surveyed experts in Panamanian amphibians to determine the probability of avoiding chytridiomycosis-related extinctions using captive breeding programs. We ranked Panamanian amphibian species by perceived susceptibility to chytridiomycosis, then calculated the likelihood of avoiding extinction as the product of three probabilities, which include (1) finding sufficient founder animals, (2) successfully breeding these species in captivity and (3) becoming extinct in the wild. The likelihood of finding enough animals to create a captive founding population was low for many rare species, especially for salamanders and caecilians. It was also low for frogs which were once regularly encountered, but have already disappeared including Atelopus chiriquiensis, Craugastor emcelae, C. obesus, C. punctariolus, C. rhyacobatrachus, Ecnomiohyla rabborum, Isthmohyla calypsa and Oophaga speciosa. Our results indicate that captive breeding could improve the odds of avoiding extinction for species that have severely declined or are likely to decline due to chytridiomycosis including Atelopus certus, A. glyphus, A. limosus, A. varius, A. zeteki, Anotheca spinosa, Gastrotheca cornuta, Agalychnis lemur and Hemiphractus fasciatus. Priority species that experts predicted were highly susceptible to chytridiomycosis that might also benefit from ex situ management include Craugastor tabasarae, C. azueroensis, C. evanesco, Strabomantis bufoniformis and Colostethus panamansis. In spite of high levels of uncertainty, this expert assessment approach allowed us to refine our priorities for captive amphibian programs in Panama and identify priority conservation actions with a clearer understanding of the probability of success.
... Isthmohyla picadoi was described from the southwestern slope of Volcán Barba, Cantón de Santa Barbara, Provincia de Heredia, in the Cordillera Central of north-central Costa Rica (Dunn, 1937; Savage, 1974). It inhabits the Lower Montane and Montane Rainforest life zones, approximately between 1900 and 2800 m asl, where it is markedly associated with bromeliad phytotelmata, that serve as calling site, mating place and nursery ground (Stuckert et al., 2009). It is only exceptionally found on rocks in streams (Duellman, 2001). ...
Article
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I report an episode of anuran mortality and decline in the Reserva Forestal Fortuna, Chiriquí, Panama. The symptoms of decline at this site include population reductions, the presence of dead or dying adults, and tadpole abnormalities. Streamside anurans were abundant and diverse in 1993–1995, were restricted to a few streams in December 1996–January 1997, and then became rare throughout the reserve in July–August 1997. Between December 1996 and January 1997, I found 54 dead or dying frogs belonging to 10 species, and 12% of tadpoles had abnormalities of the oral disc. In July–August 1997 I monitored nine streams 37 times and captured only six individuals, whereas 13 terrestrial surveys along five trails resulted in 18 captured individuals. No dead or dying animals were found during those two months, but 11% of tadpoles had mouthpart abnormalities. Necropsies revealed that 18 of 18 dead anurans had a fungal infection of the skin; because this fungus was the only infection shared among all dead frogs, I suggest that it killed them and contributed to the decline of these populations. The presence of mouthpart abnormalities during a period of adult mortality suggests that this symptom may also be linked to the fungus infection. Clinical signs of decline in the anurans of Fortuna are similar to those found in the anurans of Monteverde and Las Tablas, Costa Rica, and I hypothesize that this pathogen was involved in the declines at all three sites.
Article
Data were collected on epiphyte occurrence on tree trunks of four diameter classes in a Guatemalan cloud forest in order to document the vascular epiphyte flora and to explore aspects of species associations. Of the 68 species recorded, the largest groups were the Orchidaceae (29 species) and the Polypodiaceae (18 species). Conditional clustering and constellation analyses revealed associations of small, closely related species on smaller and consequently younger trunks, and associations of larger, less closely related species on larger, and hence older, trunks. The associations of small species possess characteristics correlated with the earlier stages of plant succession and the density-independent and non-equilibrium diversity model. The associations of larger species possess characteristics correlated with the later stages of plant succession and appear to approach equilibrium in species composition.
Article
The faunas of tank bromeliads were sampled over two years in three forest types at different elevations in the Luquillo Experimental Forest, Puerto Rico, and the diversity of their animal communities compared. Bromeliad plants behaved as islands in that, within forests, the species richness and abundance of their animal communities were significantly and positively correlated with increase in plant size. The amount of canopy debris they accumulated was similarly correlated with increase in plant size. Overall diversity was lowest in the dwarf forest, where plants were uniformly small. Animal communities were stable from year to year, and could be characterised for each forest type and for compartments within the plant. They showed a pattern of high dominance, which increased with elevation (Mc-Naughton index 37, 54, and 73, respectively, for the tabonuco, palo Colorado, and dwarf forest). Alpha-diversity for sites sampled in each year reflected net primary productivity (NPP) of the forest, declining with increasing elevation when animal abundance measures were used (jackknife estimates of Simpson's diversity index 6.54 & 11.04 [tabonuco], 3.53 & 6.22 [palo Colorado], and 2.75 & 2.17 [dwarf forest]). Species richness over the two years, however, was highest in the intermediate palo Colorado forest (187 species), compared to 146 and 88 in the tabonuco and dwarf forests, respectively. These figures were close to jackknife estimates of maximum species richness. The difference in species richness between tabonuco and palo Colorado forests was significant in one year only. In addition to NPP, other factors, such as litter quality and the structural complexity of the habitat in the palo Colorado forest, may have influenced species richness. The most abundant species in individual plants were also the most widely occurring, confirming known patterns of abundance and distribution in other functional groups. Diversity within bromeliad microcosms at different elevations supported known relationships between diversity, productivity, and habitat complexity along gradients and was not related to differences in the total bromeliad habitat available for colonization.