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Phyllomedusa
- 6(1), June 2007
37
Nocturnal position in the Panamanian Golden Frog,
Atelopus zeteki (Anura, Bufonidae), with notes on
fluorescent pigment tracking
Erik D. Lindquist1,2 , Scott A. Sapoznick2,3, Edgardo J. Griffith Rodriguez4, Peter B.
Johantgen5, and Joni M. Criswell6
1Department of Biological Sciences, Messiah College, One College Avenue, Grantham, Pennsylvania 17027, USA.
E-mail: quist@messiah.edu (present address).
2Department of Natural Sciences and Mathematics, Lee University, Cleveland, Tennessee 37311, USA.
3Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211, USA. E-mail: sashw6@mizzou.edu.
4Departamento de Zoología, Universidad de Panamá, Ciudad de Panamá, Panamá. E-mail: virolasboy01@yahoo.com.
5Shores Department, Columbus Zoo and Aquarium, 9990 Riverside Drive, P.O. Box 400, Powell, OH 43065, USA.
E-mail: pete.johantgen@columbuszoo.org.
6Department of Evolution, Ecology and Organismal Biology, The Ohio State University, Columbus, Ohio 43210, USA.
E-mail: criswell.13@osu.edu.
Received 4 October 2006.
Accepted 13 February 2007.
Distributed June 2007.
Phyllomedusa 6(1):37-44, 2007
© 2007 Departamento de Ciências Biológicas - ESALQ - USP
ISSN 1519-1397
Abstract
Nocturnal position in the Panamanian Golden Frog, Atelopus zeteki (Anura,
Bufonidae), with notes on fluorescent pigment tracking. The endangered
Panamanian golden frog, Atelopus zeteki, is a stream dweller of middle elevation rain
forests of the Panamanian isthmus. In order to better understand this species for
conservation, we set out to determine the nocturnal whereabouts of this diurnally active
animal. It was expected that adult males and juveniles might occupy different nocturnal
microhabitats based on differences in size, coloration and patterning. Findings
presented here demonstrate that adult males climb significantly higher than juveniles
at night and that movement distances to final resting positions also significantly
differed. This change in diurnal and nocturnal position in adult males may be related
to predator vigilance and avoidance. Lastly, this study demonstrated that individual
rain forest amphibians can be successfully tracked over short to moderate distances
in humid to wet environments using fluorescent pigments.
Keywords: Anura, Bufonidae, Atelopus zeteki, aposematic coloration, behavioral
ecology, climbing, fluorescent pigment.
Phyllomedusa
- 6(1), June 2007
38
Resumen
Posición nocturna en la rana dorada de Panamá, Atelopus zeteki (Anura,
Bufonidae), con notas respecto al rastreo con el uso de pigmentos fluorescentes.
La rana dorada de Panamá, Atelopus zeteki, una especie en peligro de extinción, habita
en los ríos de los bosques lluviosos de mediana elevación del istmo panameño. Con
el propósito de conocer mejor ésta especie para su conservación, decidimos determinar
los sitios de descanso nocturno de estos animales, los cuales se caracterizan por ser
activos durante el día. Suponíamos que los machos adultos y los juveniles podrían
ocupar micro hábitat distintos durante la noche, basándose en las diferencias en
tamaños y patrones de coloración. Los resultados presentados aquí demuestran que,
al caer la noche los machos adultos trepan significativamente más alto que los juveniles
y que la distancia de estos movimientos desde el punto inicial hasta la posición final
de descanso es también significativamente diferente. Estos cambios de posición durante
el día y la noche de los machos adultos podrían estar relacionados con una conducta
antipredatoria. Finalmente este estudio demuestra que con el uso de pigmentos
fluorescentes es posible rastrear anfibios en los bosques lluviosos con habitates
húmedos a mojados a través de distancias cortas a moderadas de manera exitosa.
Palabras clave: Anura, Bufonidae, Atelopus zeteki, coloración aposemática,
comportamiento de subir, ecología del comportamiento, pigmento fluorescente.
Introduction
The Panamanian golden frog, Atelopus zeteki
Dunn (1933), is a bufonid that inhabits mountain
streams of the Cordillera Central in rain and
cloud forests in western-central Panama (Savage
1972, Cocroft et al. 1990, Lindquist and
Hetherington 1998a). Although historically
abundant, most golden frog populations have
become extirpated or currently are in decline
due to excessive collection and habitat
destruction (pers. obs.). In response to these
pressures in 1975, this species was listed under
endangerment Appendix I under the CITES
(CITES 2004). In the past ten years, the fungal
pathogen Batrachochytrium dendrobatidis has
caused the extinction of many Atelopus species
(Lips et al. 2005, 2006, Johnson 2006, Pounds
et al. 2006). Within three months of this
manuscript’s submission, each of our study
populations had been effectively driven to
extirpation (Lips et al. 2006, pers. obs. EDL,
EJGR). Life history and ecological data is
largely limited to descriptive work on this
species (Savage 1972, Miller 1987, Lindquist
and Hetherington 1998a). Acoustic and visual
communicative behaviors have been reported by
Lindquist and Hetherington (1996, 1998b), but
knowledge of territoriality, ritualized agonistic
displays, and microhabitat use remain
incomplete. Moreover, most data have been
gathered on males, as streamside sex ratios
strongly favor males during the majority of the
year. Diurnally, adult males have been observed
on the ground alongside or upon rocks and logs
in or near streams. Typical diurnal activity of
males includes foraging, calling, semaphoring,
and sporadic agonistic encounters (Lindquist &
Hetherington 1996, 1998b, pers. obs,). Casual
observations have indicated that adult male and,
on occasion, female golden frogs climb and
perch on vegetation near the stream banks at
night (Miller 1987, pers. obs.). The diurnal
whereabouts of both females and juveniles have
Lindquist et al.
Phyllomedusa
- 6(1), June 2007
39
been difficult to establish beyond occasional
stream and trail sightings during reproductive
migrations and metamorphic emergence
respectively (pers. obs.). It has been reported in
this and other Central American Atelopus
species that females and juveniles
predominantly seek cover under forest canopy
and/or in rock crevices along stream banks
(Crump 1986, G. Angehr pers. com.), although
no studies have been able to confirm this. Yet
the authors regularly have seen cryptic young in
the daytime and nighttime upon moss-covered
rocks bordering streams.
The study described here set out to establish
and quantify the nocturnal whereabouts of adult
males and juveniles, as compared to their
diurnal locations, and to determine if there was a
difference between age cohorts with respect to
perching position. Movements of adult females
are not reported in this study due to their
scarcity along the stream study sites (only three
were encountered during the study period).
The study discussed here employed pigment
tracking on a rain forest frog species. We set out
to test whether adult males climb to higher
nocturnal roosting sites and cover greater
distances to do so than do juveniles as witnessed
by casual observation. Establishing whether or
not these differences actually exist could offer
insights on potential selection pressures and/or
other aspects of the species’ biology. We
expected no difference in cohort movement
distance between population sites. Lastly, the
study set out to determine whether any
difference in final nocturnal perching positions
exists with respect to the stream edge.
Materials and Methods
During study trips taken in March 2001,
January 2002, July 2002 and January 2003, we
visited golden frog populations in the Parque
Nacional General Omar Torríjos – El Copé,
Coclé Province, Panamá (PNGOT, hereafter)
and a tributary to the Río Chame near Sorá,
Panamá Province, Panamá (Chame, hereafter).
The populations under investigation have been
identified as two unique evolutionary significant
units (ESU) and therefore the authors used
statistical treatments that included both pooled
and unpooled site data to clarify differences and
similarities (Zippel et al. 2007). Individuals
were assigned as juvenile (<28.2 mm) or adult
(>36.2 mm) by Snout-Vent Length (SVL). The
absence of this size class along streams is
corroborated by data gathered in a two year
study on the species (Lindquist et al. in prep.;
Griffith pers. obs.). Over the course of the study
period, 9 adult males (SVL 0 = 43.2 mm; range
= 39.5-46.7 mm) and 28 juveniles (SVL 0 =
16.3 mm; range = 9.9-26.8 mm) from PNGOT
and 13 adult males (SVL 0 = 41.8 mm; range =
36.2-44.8 mm) and 10 juveniles (SVL 0 = 22.7
mm; range = 15.2-28.2 mm) from Chame were
tracked.
Thermoplastic fluorescent pigments (JST-
300 series) were purchased from the Radiant
Color Company (Richmond, CA, USA) and
placed in 250 ml plastic containers. These
pigments range in particle size from 2 to 4 ìm
and are capable of indefinite storage. Five colors
were used in this study (JS-CH3020, JS-
GR3011, JS-OY3022, JS-OR3034, and JS-PK
3017). Pigment containers were kept in
individual Ziploc® freezer bags to reduce cross
contamination in the field. Dual-tube fluorescent
Coleman® lanterns were used for pigment
illumination. Lanterns were modified by
outfitting them with black fluorescent light tubes
(long wavelength UV BLB; 365 nm = dominant
ë) and inserting three mirrored glass panels
inside the bulb case to allow unidirectional light
projection and to enhance light intensity.
Individual animals were captured by hand
between 13:00 and 17:00 h. Subjects had
pigment applied within 90 min of capture and
were released immediately afterward. Pigment
application consisted of grasping an individual
dorsolaterally while placing much of the venter
into the fluorescent powder held in a plastic
container. Pigment contact included ventral
palmar, plantar, and abdominal surfaces. Once
Nocturnal position in the Panamanian Golden Frog, Atelopus zeteki (Anura, Bufonidae)
Phyllomedusa
- 6(1), June 2007
40
sufficiently applied, the animal was released
alongside the stream and the initial release area
was marked with fluorescent vinyl flagging to
indicate where to return at night for tracking. To
prevent cross contamination of trails, frogs were
powdered away from the site of release, and
placed at the location of capture. Investigators
returned to stream sites after dark (ca. 19:00 h)
to track pigmented individuals.
Once returning to each release site, the
pigment trail was then followed under black
light until the tracked subject was found.
Pigment residues left behind from contact with
substrate were remarkably robust. Once the
subject was found, nylon twine was overlaid
along the pigment trail (straight line distance
between tracks) and measured to obtain a total
distance tracked (TDT) in m. Fluorescent
colored twine was used to permit better visibility
under black light illumination of pigment tracks.
Vertical perch positions (Y) of individuals were
noted by measuring the perpendicular distance
from the final nocturnal perching location to the
substrate immediately below. If an individual
(n=3, all juveniles) was tracked to a burrow, a
vertical distance of zero was entered (see Figure
1). Likewise, horizontal perch positions (X) of
individuals were noted by measuring the
distance from the final nocturnal location to the
nearest stream edge. If an individual was found
at a location at or above the stream, a horizontal
distance of zero was entered. Afterward residual
pigment was rinsed from recovered frogs. Each
individual was tracked once to avoid pseudo-
replication error and to determine an estimate of
TDT, Y, and X for the two age classes identified
in this study. Statistical analyses and calcula-
tions in this study used the VassarStats Web Site
for Statistical Computation (Lowry, 2004).
Results
Vertical perch position
Findings from our study demonstrated that
adults and juveniles differentially utilize
nocturnal microhabitats with respect to vertical
distance from the substrate. Vertical distance
from substrate (Y) was significantly greater in
adult males (0 = 0.96 m; sd = 0.68) than in
juveniles (0 = 0.14 m; sd = 0.23) (P = <0.0001,
z = 4.85, nadult = 22, njuvenile = 38; Mann-Whitney
U test, one-tailed; data from pooled sites).
Within each population, detected differences in
Y were highly significant at PNGOT (P =
0.0002, z = 3.54, nadult = 9, njuvenile = 28; Mann-
Whitney U test, one-tailed) and at Chame (P =
0.0110, z = 2.29, nadult = 13, njuvenile = 10; Mann-
Whitney U test, one-tailed). A positive
correlation between SVL and Y for combined
sites is depicted in the scatter plot given in
Figure 1. Differences in Y were not significant
between adult males from both population sites
(0Chame = 0.86 m; sdChame = 0.57; 0PNGOT = 1.094
m; sdPNGOT = 0.84) (P = 0.3192, z = 0.47, nChame =
13, nPNGOT = 9; Mann-Whitney U test, one-
tailed). However, there appeared to be a
significant difference in Y between juveniles
from different populations (0Chame = 0.33 m;
sdChame = 0.35; 0PNGOT = 0.08 m; sdPNGOT = 0.13)
(P = 0.0294, z = 1.89, nChame = 28, nPNGOT = 10;
Mann-Whitney U test, one-tailed).
Horizontal perch position
Study results indicated that adults and
juveniles did not differentially utilize nocturnal
microhabitats with respect to X. Both juvenile
and adult X positions were variable (Xmin-juvenile =
0.35 m, Xmax-juvenile = 4.6 m, 0juvenile = 1.79 m, sd
juvenile = 1.12 m; Xmin-adult = 0 m, Xmax-adult = 6.35 m,
0adult = 1.25 m, sd adult = 1.10 m; data from pooled
sites). An analysis of variance of X showed no
difference between juveniles and adults exists (P
= <0.0001, F = -2.2596, nadult = 22, njuvenile = 38;
ANOVA; data from pooled sites).
Total distance tracked
This study determined that subjects were
capable of being followed to a maximum TDT of
16.65 m with fluorescent pigments in streamside
Lindquist et al.
Phyllomedusa
- 6(1), June 2007
41
Figure 1 - XY scatter plot showing correlation between snout-vent length (SVL) and vertical distance from substrate
(Y). Individuals represented by markers: open (General Omar Torrijos National Park) and solid (Chame River);
circle (individual above ground) and square (below ground).
Figure 2 - XY scatter plot showing correlation between snout-vent length (SVL) and total distance tracked (TDT).
Individuals represented by circular markers: open (General Omar Torrijos National Park) and solid (Chame
River).
Nocturnal position in the Panamanian Golden Frog, Atelopus zeteki (Anura, Bufonidae)
Phyllomedusa
- 6(1), June 2007
42
tropical rain forest habitat. TDT was
significantly longer in adult males (0 = 7.06 m;
sd = 3.96) than in juveniles (0 = 2.22 m; sd =
1.09) (P = <0.0001, z = 5.13, nadult = 22, njuvenile =
38; Mann-Whitney U test, one-tailed; data for
pooled sites). Within each population, detected
differences in TDT were significant at PNGOT
(0juvenile = 2.09 m, sd juvenile = 0.92 m; 0adult = 5.43
m, sd adult = 1.82 m) (P = 0.0001, z = 3.88, nadult =
9, njuvenile = 28; Mann-Whitney U test, one-tailed)
and at Chame (0juvenile = 2.58 m, sd juvenile = 1.46
m; 0adult = 8.18 m, sdadult = 4.68 m) (P = 0.002, z
= 2.88, nadult = 13, njuvenile = 10; Mann-Whitney U
test, one-tailed). A positive correlation between
SVL and TDT for combined sites is depicted in
the scatter plot given in Figure 2. There was also
a significant difference in TDT between the two
populations (0Chame = 5.74 m; sdChame = 4.57 m;
0PNGOT = 2.90 m; sdPNGOT = 1.86) (P = <0.0084, z
= 2.39, nChame = 23, nPNGOT = 37; Mann-Whitney
U test, one-tailed). This likely was due to having
a juvenile constituency of 75.65% at the
PNGOT sample compared to 38.46% of Chame.
Lastly, there exists a significant correlation
between Y and TDT for pooled data (P = <
0.0001, t = -8.81, npooled; paired t-Test for
Correlated Samples, one tailed).
Pathways to nocturnal positions
In this study we found that movement
distance from the release site to the nocturnal
perch positions in adult males varied
dramatically, but generally involved finding the
base of a woody plant (e.g. shrub or liana) and
climbing to a leaf, leaf axil, or branch that was
away from the plant’s main trunk. Occasionally
herbaceous vines were used. Large ferns were
also used as perch sites for adults, with the tips
of fronds being primarily used. Rarely were
adults found at the base of branches or leaves.
Juveniles generally took their nocturnal position
in rock crevices or on the ends of small fern
fronds or shrubs. The riparian habitat at each
study site has potentially climbable herbaceous
and woody vegetation from ground level to
approximately 25 m high that, aside from height,
could have served as suitable perching sites.
Discussion
Some of the statistical differences detected
between juveniles from each study population,
with respect to Y, might be explained by the
disparate sizes between juveniles from the two
populations, genetic (ESU) differences, or small
sample sizes (see Figures). Nonetheless, a clear
trend exists for adult male A. zeteki to perch
significantly higher than juveniles in both
pooled and unpooled data sets. Also, the
statistically significant difference in TDT
between populations might be explained by
differences in the age cohort constituency
(sample size) within populations and may not
necessarily represent actual differences between
populations. Lastly, the strong correlation
between Y and TDT in this study may attest to
the fact that individuals that climb higher at
night move further to do so than those that stay
lower to the ground. TDT was measured in this
study in large part to detect and quantify the
complexity of paths taken to nocturnal roosting
positions as well as to determine the viability of
fluorescent pigment tracking for this species.
Although statistical differences were not
detected, X was measured specifically to gauge
preferences with respect to the primary water
source.
The information provided in this study is
intended to help conservation efforts in two
ways. The first application is that nighttime
stream surveys by national park authorities can
be better completed by knowing the range in
perch heights for adults and juveniles. Second,
this information will help zoos and aquariums
that currently hold living A. zeteki in their
collections for captive breeding. It is anticipated
that information of this nature would assist
breeding professionals in arranging enclosures
in ways that might reduce stress on captive
animals and potentially increase reproductive
success and output.
Lindquist et al.
Phyllomedusa
- 6(1), June 2007
43
The benefits of using fluorescent pigment
tracking in this study were surprising. This
technique allowed us to track the actual paths
chosen by individual animals. Paths taken to
final roosting destinations were complex for
adult males, involving trunk, branch, and vine
climbing, yet were generally uncomplicated and
restrictive for juveniles which generally
remained near the ground. In addition to
microhabitat utilization, another advantage
afforded by this technique is its resilience
against light to moderate rainfall. In numerous
cases of moderate rainfall, the investigators set
out to return to sites expecting a complete loss
of pigment tracks, yet found most intact. Four
juveniles and six adult males (not included in
tracking data sets) were pigmented and had their
tracks removed by heavy rains. Yet, in some
cases, pigments could withstand brief distances
of swimming by the subject. The success rate for
tracking this species with fluorescent pigments
in this study was 60 of 70 total attempts
(85.7%). Pigment use was most effective in dry
conditions, yet surprisingly suitable in the
tropical rain forests and cloud forests in which
this species resides.
Lastly, the reality that adult males
nocturnally perch significantly higher than
juveniles possibly may be adaptive for many
reasons. One possible impetus to drive adult
males to climb vegetation at night, as opposed to
burrowing, hiding in rock crevices, and/or
maintaining daytime position, could be due to
shifting predator detection strategies. It was
evident that a full size range of perches was
available at all heights for both juveniles and
adults; likewise for crevice sizes on the ground.
Anti-predator vigilance would largely be visual
during daytime, whereas perching upon
vegetation at night might allow the tactile
sensation of an approaching predator via the
movement of the perch branch. This may be
important for adults that cannot find hiding
places that are unreachable by predators.
Presumably, this would not be a problem for
substantially smaller juveniles. Potential
nocturnal stream dwelling predators such as
Liophis epinephalus (Reptilia, Colubridae), are
known to be capable of metabolizing key skin
toxins in Central American Atelopus
(Shindelman et al. 1969, Brown et al. 1977,
Daly et al. 1987, Pounds 2000, Yotsu-Yamashita
et al. 2004). Predation of adult A. zeteki by L.
epinephalus has been witnessed firsthand by two
of us (EJGR and EDL). Changing location based
on a shift in sensory cues to improve predator
vigilance from day to night might be the most
logical explanation.
Acknowledgements
This work was undertaken as part of the
Proyecto Rana Dorada (Project Golden Frog)
conservation initiative and in part was funded by
grants from the American Zoo and Aquarium
Association’s Disney Conservation Endowment
Fund, Lee University Faculty Scholarship grants
(EDL), and by the Garden Clubs of America
(SAS). Special thanks are given to B. Lewis, A.
Wisnieski, N. Ellis, and E. Kiester for their
assistance in refinement of the technique.
Likewise we appreciate M. Freake, J. Sander,
and K. Terry for assisting in taking
measurements. We thank G. Diehl for the
information on track persistence with respect to
rainfall. We also are indebted to G. Diehl and K.
Larson for reviews of earlier manuscripts.
Animal care protocol review was provided by
Lee University. Finally, we thank La Autoridad
Nacional del Ambiente for providing permits for
this work.
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