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Environmental drivers of anuran calling phenology in a
seasonal Neotropical ecosystem
CHRISTOPHER M. SCHALK1,* AND DANIEL SAENZ2
1Ecology and Evolutionary Biology Program, Department of Wildlife and Fisheries Sciences, and
Biodiversity Research and Teaching Collections, Texas A&M University, 210 Nagle Hall, College
Station, Texas 77843, USA (Email: cschalk@tamu.edu), and 2Southern Research Station, US Forest
Service, Nacogdoches, Texas, USA
Abstract Temporal variation represents an important component in understanding the structure of ecological
communities and species coexistence. We examined calling phenology of an assemblage of anurans in the Gran
Chaco ecoregion of Bolivia by deploying automated recording devices to document nocturnally vocalizing amphib-
ians nightly at seven ponds from 20 January 2011 until 31 October 2011. Using logistic regression, we modelled
the relationships between temperature, rainfall and photoperiod with calling activity. There was a distinct seasonal
effect with calling activity concentrated in the rainy season with no species detected during the dry season from June
until the end of October. Calling activity was positively and significantly correlated with photoperiod in 9 of the 10
species analyzed, but there were distinct species-specific relationships associated with rainfall and temperature. All
of these species utilize ephemeral ponds as breeding sites, which can account for their reliance on rainfall as an
important driver in calling activity.Two prolonged breeders exhibited similar seasonal breeding patterns across the
rainy season, but differed in their response to daily abiotic factors, which might be attributed to the constraints
imposed by their reproductive mode. Explosive breeders needed several days of rain to elicit calling. Two pairs of
congeners had distinct species-specific relationships between their calling activity and abiotic factors, even though
the congeners shared the same reproductive mode, suggesting that the reproductive modes vary in the constraints
imposed on calling activity. The patterns observed suggest that calling phenology of tropical anurans is determined
by the interaction of exogenous factors (i.e. climatic variables) and endogenous factors (i.e. reproductive modes).
Key words: amphibian, Gran Chaco, photoperiod, reproductive mode, temporal community structure, weather.
INTRODUCTION
A central goal in ecology is to understand the factors
that drive the variation in species phenologies, as they
can provide insights to interactions and coexistence
among species (Schoener 1974). An organism’s
phenology, that is the occurrence of vital cyclic activi-
ties within the year, is the product of abiotic and/or
biotic factors, such as avoidance of predators or com-
petitors, or tracking certain seasonal resources such as
water, light or nutrients (Van Schaik et al. 1993;
Bradshaw & Holzapfel 2007). However, the relative
impact of these abiotic and biotic factors on an
organism’s phenology varies and is dependent on the
appropriate timeframe (i.e. short-term vs. long-term).
Activity cycles of ectothermic animals, such as
amphibians, are strongly influenced by abiotic factors,
principally temperature and rainfall, due to their per-
meable skin and aquatic reproduction (Duellman &
Trueb 1994; Hartel et al. 2007). The timing of these
events can have important consequences for the timing
of species interactions, and for those species with
complex life cycles (e.g. amphibians), this can carry
over to affect interactions occurring across multiple
life stages and influence community composition at
local scales (Parmesan 2007; Yang & Rudolf 2010;
Todd et al. 2011).
Anuran communities exhibit latitudinal variation in
the abiotic factors that drive reproductive activity,
and within an assemblage, exhibit species-specific
responses to these abiotic factors both in short-term
(daily) and long-term (seasonal) periods (Aichinger
1987; Moreira & Barreto 1997; Oseen & Wassersug
2002; Kopp & Eterovick 2006; Saenz et al. 2006; Both
et al. 2008; Canavero & Arim 2009; Canavero et al.
2009; Narins & Meenderink 2014). In their examina-
tion of geographic structure of community seasonality
in amphibians, Canavero and Arim (2009) suggest
that both latitude and diversity influence the
nestedness and segregation of amphibians across time.
Across regions, it is reported that anurans have longer
reproductive periods in the wet tropics than those
species occurring in tropical seasonal and temperate
regions (Duellman & Trueb 1994). In temperate
regions, temperature and rainfall, or their interaction,
*Corresponding author.
Accepted for publication May 2015.
Austral Ecology (2016) 41, 16–27
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© 2015 Ecological Society of Australia doi:10.1111/aec.12281
are the primary determinants of reproductive activity
within the breeding season, but their relative influence
varies by species (Bridges & Dorcas 2000; Oseen &
Wassersug 2002; Saenz et al. 2006; Steen et al. 2013).
In the tropics and subtropics, recent studies have
suggested that photoperiod, rather than temperature
and rainfall, is the most important predictor of anuran
activity (Both et al. 2008; Canavero et al. 2008;
Canavero & Arim 2009). However, even within the wet
tropics, the roles of abiotic factors on anuran repro-
ductive activity vary, ranging from not eliciting any
response (Inger & Bacon 1968) to a non-random dis-
tribution of breeding activity across the rainy season,
with abiotic factors such as rainfall being important
drivers (Crump 1974; Gottsberger & Gruber 2004).
Tropical anurans are also particularly diverse in their
modes of reproduction (Duellman & Trueb 1994),
with many species possessing complex oviposition
behaviours such as terrestrial or arboreal oviposition,
or depositing their eggs in foam nests (Magnusson &
Hero 1991; Haddad & Prado 2005).These oviposition
strategies are believed to have evolved as a means
to reduce exposure of eggs and larvae to predators
(Magnusson & Hero 1991). However, these reproduc-
tive modes also impose constraints, and species need
to adjust their calling and breeding activity in accord-
ance with their reproductive mode (Gottsberger &
Gruber 2004).
Previous studies indicate multiple drivers influenc-
ing the calling activity of anurans across both daily and
seasonal time periods. However, many of the studies
conducted in tropical or subtropical regions have been
conducted over coarse (i.e. monthly or weekly) time
scales (e.g. Moreira & Barreto 1997; Both et al. 2008;
Canavero & Arim 2009; Canavero et al. 2009). In this
study, we utilized a fine-grain (i.e. daily timeframe)
approach to quantify the abiotic correlates of calling
activity in an assemblage of tropical anurans occurring
in the Gran Chaco ecoregion of south-eastern Bolivia
from the middle of the rainy season to the end of
the dry season. We describe the pattern of calling
phenology that arises from species-specific responses
to abiotic factors, specifically we discuss the potential
influence of life-history strategies (i.e. reproductive
strategy (prolonged vs. explosive breeders) and repro-
ductive mode) on the observed responses to these
extrinsic factors.
METHODS
Study system
Our study was conducted in the semi-arid thorn forests of
the Gran Chaco ecoregion of south-eastern Bolivia. The
region has a warm, rainy season (November–March) and a
cool, dry season (April–October). The surrounding forest in
this semi-arid region is predominately thorn forest; common
tree species include Schinopsis lorentzii and Aspidosperma
quebracho-blanco with cacti (e.g. Opuntia spp., Cleistocactus
baumannii and Eriocereus guelichii) and bromeliads constitut-
ing the common understorey plants (Navarro & Maldonado
2002). Our study sites were located in one the most xeric
regions of the Bolivian Chaco with annual rainfall and
temperature averaging 513 mm and 24.6°C, respectively
(Navarro & Maldonado 2002).
Anuran vocalization recordings
We collected audio recordings of nocturnally vocalizing
amphibians at seven ponds within the vicinity of the Isoceño
community of Yapiroa, one of approximately 25 indigenous
communities occurring near the Parapetí River in the indig-
enous territory of Isoso, Provincia Cordillera, Departmento
de Santa Cruz, Bolivia (19.60°S, 62.57°W; WGS 84). We
used automated recording devices (SM2 +Song Meters,
Wildlife Acoustics, Maynard, MA, USA), which allow for
consistent sampling across extended periods of time (Bridges
& Dorcas 2000), to record anuran vocalizations each night.
Song Meters were attached to nearby trees within 2 m of the
pond’s edge (one per pond). The seven breeding ponds that
were both artificial (n=5) and natural (n=2), and ranged in
their hydroperiod from temporary (n=6) to semi-permanent
(n=1). The Song Meters were deployed at the seven ponds
from 20 January 2011 (mid-way through the rainy season)
and recorded daily until 31 October 2011 (the end of the dry
season).The scope of our study includes data collected from
20 January 2011 to 31 October 2011. Each Song Meter was
set to record for 1 min at the start of each hour starting at
21.00 hours and ending at 01.00 hours, for a total of 5 min
per night. The recordings were saved to secure digital cards,
which were retrieved approximately every 2 weeks from each
Song Meter. We listened to and transcribed the recordings
and identified the vocalizations to species level and the
number of calling individuals of each species were estimated.
We followed the protocol of Saenz et al. (2006) when docu-
menting the number of calling individuals per species per
night; when the number of individuals per species calling was
≤4, we felt that we could accurately count the total number
of individuals calling; however, when >4 individuals were
calling, we assigned a value of 5, as it was impossible to
determine the exact number of individuals.Thus, the nightly
call intensity index of each species per pond could range from
0 (i.e. no individuals heard) to 25 (summed across five sam-
pling minutes).
Abiotic factors
Previous studies have recognized that anuran calling activity
varies across small spatial scales (Oseen & Wassersug 2002;
Saenz et al. 2006) and similar studies have collected site-
specific temperature and rainfall data. We relied on a cen-
trally located weather station sited within the community of
Yapiroa as the source for the temperature and rainfall data.
The maximum distance between a Song Meter and the
weather station was 2 km.The weather station consisted of a
HOBO Data Logging Rain Gauge and a HOBO Pro v2
ANURAN TEMPORAL PARTITIONING 17
© 2015 Ecological Society of Australia doi:10.1111/aec.12281
External Data Logger (Onset Computer Corporation,
Pocasset, MA, USA). The temperature data logger was
covered with an Onset Solar Radiation Shield to block its
exposure to direct sunlight. Temperature was measured to
the nearest 0.001°C and daily rainfall was measured to the
nearest 0.1 mm.We computed the number of hours of day-
light using Julian date and −19.6°S latitude for the study sites
(Kirk 1994).
Statistical analyses
As in similar studies (e.g. Saenz et al. 2006), we observed
several anuran species calling several days after a rain event.
Therefore, we could not discern whether a species calling
activity was an immediate response to precipitation or if it
was the result of a lag or build up in precipitation. We used
three different types of rainfall lag in our models. The first
type was categorical (catlag) and simply indicated the occur-
rence of rainfall ranging from 1 to 5 days prior to the calling
event. For example, catlag1 referenced rainfall 1 day prior to
the calling event, catlag2 referenced rainfall 2 days prior to
the calling event.The next lag type (rainlag) was the amount
of daily rainfall that occurred from one to five nights prior to
the calling event. For example, rainlag1 was the rainfall
amount from 1 day prior, whereas rainlag2 was the amount
of rainfall from 2 days prior to the calling event.The final lag
variable type (cumulrain) examined the effects of the cumu-
lative rainfall ranging from 1 to 5 days prior. For example,
cumulrain2 equalled the total cumulative rainfall from 1 and
2 days prior to the calling event.
We used logistic regression with generalized estimating
equations to test the relationship between the occurrence of
daily anuran calling activity (0 =no calling and 1 =calling)
and air temperature at 2100 h, daily rainfall, lags and accu-
mulation in rainfall, and day length. Because ponds were
repeatedly sampled, we used an autoregressive correlation
structure. We began with a simple model including tempera-
ture and day length. We then added rainfall on the day of
calling and variables reflecting lags and accumulation in rain-
fall (five models total). We used quasi-likelihood under the
independence model criterion, adjusted for the number of
parameters in the model (QICu) to compare models and
considered the model with the lowest QICu to be the best
model (Pan 2001).
RESULTS
We detected 14 species of anuran at our seven survey
ponds (Appendix S1). These species did not exhibit
much spatial partitioning in their use of calling sites as
many species overlapped considerably (Appendix S1).
Four species, Dermatonotus muelleri,Leptodactylus
elenae,Leptodactylus fuscus and Scinax fuscovarius, were
detected less on than 10 days during the survey period
(Appendix S2) and were excluded from analyses.
Seasonal and daily call patterns
We observed variation in calling activity across the wet
and dry seasons, as the majority of calling activity was
concentrated in the rainy season between the months
of January and the first week of April (Fig. 1,Table 1).
However, we detected three species calling in the
month of May after a large rainstorm: Physalaemus
biligonigerus,Pleurodema guayapae and Odontophrynus
americanus. No species was observed calling from June
until the beginning of October (Fig. 1). At the start of
the subsequent rainy season at the end of October we
detected L. fuscus calling for the first and only time
(Table 1).
We observed some variation in calling activity among
species within the rainy season (Figs 1 and 2). While
the number of individuals calling each night varied,
Leptodactylus bufonius and Phyllomedusa sauvagii called
Fig. 1. The most frequent calling anuran species recorded over the 285-day study from 20 January 2011 to 31 October 2011
in the Bolivian Chaco. Leptodactylus elenae,Leptodactylus fuscus,Dermatonotus muelleri and Scinax fuscovarius were excluded
because of small sample sizes. For species names, see Table 1.
18 C. M. SCHALK AND D. SAENZ
© 2015 Ecological Society of Australiadoi:10.1111/aec.12281
nearly daily during the rainy season (Figs 1 and 2).
Physalaemus albonotatus,P. biligonigerus,Rhinella major
and Scinax nasicus were detected every month from
January to April, but they called less frequently when
compared with L. bufonius and P. sauvagii (Figs 1 and
2,Table 1).The calling activity for Ceratophrys cranwelli
was concentrated towards the beginning of the sam-
pling period (Figs 1 and 2). As previously mentioned,
the calling activity of L. bufonius and P. sauvagii was
fairly continuous throughout the rainy season, whereas
the calling activity of P. albonotatus,P. biligonigerus and
to a lesser extent R. major and S. nasicus were detected
consistently for several days at a time (Figs 1 and 2).
The calling activity of other species like C. cranwelli,
R. schneideri,O. americanus and P. guayapae were
detected over much shorter timeframes, often a single
night (Figs 1 and 2).There was variation in the calling
activity even among these species; C. cranwelli calling
was concentrated at the beginning of the survey period,
whereas the calling activity of other species such as
P. guayapae and O. americanus occurred across a longer
time period of the rainy season.
Abiotic correlates of calling activity
Because no species was recorded calling between June
and early October, and only three species in late
October, we restricted data to 20 January 2011–27
June 2011 for the logistic regression analyses. The
average temperature at 2100 h during the entire survey
period (January–October) was 22.6°C (SD =5.0°C,
range =9.4–31.2°C) (Fig. 3). The total rainfall
recorded during the survey period was 466 mm and
the highest amount of daily rainfall recorded was
67.4 mm (Fig. 3). The average temperature at 21h00
from 20 January 2011 to 27 June 2011 was 22.5°C
(SD =4.1°C, range =9.4–30.1°C) (Fig. 3). The total
rainfall recorded from 20 January 2011 to 27 June
2011 was 384 mm and the highest amount of daily
rainfall recorded was 67.4 mm (Fig. 3).
The logistic regression models revealed significant
associations between the abiotic variables and calling
activity,with each species exhibiting a distinct relation-
ship, but some general trends were also observed
(Table 2). With the exception of O. americanus, the
calling activities of all species were significantly and
positively correlated with photoperiod. As another
general trend, the majority of species calling were sig-
nificantly and positively associated with the amount of
rainfall on the night of the calling event; the only
exceptions were R. schneideri,P. albonotatus (no asso-
ciation) and L. bufonius (significant negative associa-
tion) (Table 2).
The calling activity of Phyllomedusa sauvagii
and Scinax nasicus were significantly and positively
Ta b l e 1. Calling activity and reproductive modes of 14 species of anurans in the Gran Chaco by month from 20 January 2011
to 31 October 2011
Family and species
Month
RM January February March April May June July August September October
Bufonidae
Rhinella major 1x x xx
Rhinella schneideri 1x x x
Ceratophryidae
Ceratophrys cranwelli 1x x x
Hylidae
Phyllomedusa sauvagii 3x x xx
Scinax fuscovarius 1x x x
Scinax nasicus 1x x xx
Leptodactylidae
Leptodactylus bufonius 4x x xx x
Leptodactylus elenae 4x x
Leptodactylus fuscus 4 x
Physalaemus albonotatus 2x x xxx
Pleurodema guyapae 2x x xxx x
Microhylidae
Dermatonotus muelleri 1x
Odontophryidae
Odontophrynus americanus 1x x xxx x
The x symbol indicates that the species was observed calling in the month indicated. Blank cells represent no calling detected in
that month for a given species.The species reproductive mode (RM) sensu Haddad and Prado (2005): 1 =Aquatic oviposition and
exotrophic, aquatic tadpoles in lentic water (RM 1),2 =Oviposition in floating foam nest and exotrophic, tadpoles in lentic water
(RM 11), 3 =Oviposition on vegetation above water,exotrophic tadpoles drop into lentic water (RM 24), 4 =Oviposition and early
larval stages in foam nest in subterranean nests, subsequent nest flooding, and exotrophic tadpoles in lentic water (RM 30)
ANURAN TEMPORAL PARTITIONING 19
© 2015 Ecological Society of Australia doi:10.1111/aec.12281
20 C. M. SCHALK AND D. SAENZ
© 2015 Ecological Society of Australiadoi:10.1111/aec.12281
correlated with photoperiod, rainfall on the night of
the calling event, and lags in the amount or occurrence
of rainfall (Table 2). Calling activity varied slightly
between the two species of Physalaemus; although each
species exhibited similar responses to rainfall and pho-
toperiod, they differed in their response to tempera-
ture: P. albonotatus calling was significantly negatively
associated with temperature, whereas P. biligonigerus
exhibited no relationship (Table 2). Similarly, the
other pair of congeners, the two Rhinella species, dif-
fered in their calling activity. The main differences
being that on the night of calling, R. major activity was
positively correlated with rainfall and temperature,
whereas R. schneideri exhibited no relationship with
rainfall, and a significant negative association with
temperature (Table 2). Ceratophrys cranwelli and
P. guayapae exhibited the same associations between
calling activity and abiotic variables (Table 2). Calling
activity in O. americanus was positively associated with
amount of rainfall on the night of the calling event, but
negatively associated with cumulative amount of rain-
fall after 4 days (Table 2).
DISCUSSION
Usually generalized as being explosive breeders
(Duellman 1999), our study demonstrates that
anurans of the Gran Chaco ecoregion span the spec-
trum of breeding activity of prolonged and explosive
breeders (Wells 1977). There was no single abiotic
factor that was the dominant driver in calling activity
in any of the 10 species analyzed; rather, we observed
that at least two abiotic factors (rainfall and photo-
period) were influencing the calling activity in
Chacoan anurans. Similar studies in tropical and sub-
tropical regions found that anurans exhibited a range
of responses to climatic factors, ranging from rainfall
being the most important variable associated with
calling activity to no association between anuran
reproductive activity and rainfall and/or temperature
(Inger & Bacon 1968; Crump 1974; Gottsberger &
Gruber 2004; Kopp & Eterovick 2006). However,
some recent studies have identified photoperiod as the
predominant driver in reproductive activity in the
tropics and subtropics (Both et al. 2008; Canavero &
Arim 2009). In our study, we found that photoperiod
was an important driver of calling activity in 9 of the
10 species analyzed (O. americanus being the excep-
tion) in addition to rainfall and/or temperature. Our
study design could account for the fact that photo-
period was not the only abiotic variable driving calling
activity in the Chaco frog assemblages as compared
with similar seasonal tropical and subtropical assem-
blages; sites in those studies were surveyed monthly as
compared with nightly monitoring as in our study
(Both et al. 2008; Canavero & Arim 2009). In some
instances, the abiotic variables used varied in the time
period over which they were collected; rainfall and
temperature were monthly averages, whereas photo-
period was calculated from the day of the survey
(Canavero & Arim 2009).We have shown that in most
instances, amount of rainfall on the night of the calling
Fig. 2. Call intensity scores for 10 species of anurans each night at seven ponds from 20 January 2011 to 31 October 2011:
(a) Ceratophrys cranwelli, (b) Leptodactylus bufonius, (c) Phyllomedusa sauvagii, (d) Physalaemus albonotatus, (e) Physalaemus
biligonigerus, (f) Pleurodema guayapae, (g) Rhinella schneider i, (h) Odontophrynus americanus, (i) Rhinella major and (j) Scinax
nasicus. Ponds were located within the vicinity of the Isoceño community of Yapiroa, Cordillera Province, Santa Cruz Depart-
ment, Bolivia.
◀
Fig. 3. Daily rainfall (mm; solid line) and air temperature at 2100 h (°C; dashed line) collected from a centrally located weather
station in the Isoceño community ofYapiroa, Cordillera Province, Santa Cruz Department, Bolivia from 20 January 2011 to 31
October 2011. Total accumulated rainfall during the survey period was 466 mm.
ANURAN TEMPORAL PARTITIONING 21
© 2015 Ecological Society of Australia doi:10.1111/aec.12281
Ta b l e 2. Results of the best-fit logistic regression models for ten species of anurans in the Bolivian Gran Chaco
Species Variable Estimate SE LCL95 −UCL95 Z P
Rhinella major Intercept −18.8 1.19 −15.8 <0.0001
Temperature 0.06 0.01 −21.1 to −16.4 5.02 <0.0001
Photoperiod 1.26 0.11 0.04 to 0.09 11.93 <0.0001
Rainfall 0.04 0.01 1.05 to 1.46 5.3 <0.0001
Catlag1 0.98 0.2 0.03 to 0.06 4.99 <0.0001
Catlag2 0.07 0.16 0.6 to 1.37 0.44 0.6603
Catlag3 −0.19 0.15 −0.24 to 0.38 −1.25 0.2104
Catlag4 0.31 0.13 −0.49 to 0.11 2.33 0.0199
Catlag5 −0.01 0.28 0.05 to 0.57 −0.04 0.967
Rhinella schneideri Intercept −31.0 2.96 −36.8 to −25.2 −10.5 <0.0001
Temperature −0.18 0.04 −0.27 to −0.1 −4.2 <0.0001
Photoperiod 2.66 0.29 2.1 to 3.22 9.27 <0.0001
Rainfall −0.04 0.03 −0.1 to 0.02 −1.31 0.191
Catlag1 0.92 0.28 0.38 to 1.47 3.3 0.001
Catlag2 −0.72 0.29 −1.28 to −0.16 −2.53 0.0115
Catlag3 −0.78 0.51 −1.78 to 0.22 −1.52 0.1274
Catlag4 −0.5 0.41 −1.31 to 0.31 −1.21 0.225
Catlag5 −0.14 0.38 −0.89 to 0.6 −0.38 0.7054
Ceratophrys cranwelli Intercept −83.6 16.2 −115.3 to −51.9 −5.16 <0.0001
Temperature −0.34 0.13 −0.59 to −0.1 −2.73 0.0064
Photoperiod 6.91 1.41 4.15 to 9.66 4.91 <0.0001
Rainfall 0.19 0.05 0.09 to 0.29 3.72 0.0002
Catlag1 1.34 0.3 0.76 to 1.93 4.54 <0.0001
Catlag2 0.24 0.32 −0.38 to 0.87 0.77 0.44
Catlag3 −1.53 0.31 −2.13 to −0.93 −5<0.0001
Catlag4 2.05 0.34 1.38 to 2.73 5.96 <0.0001
Catlag5 0.22 0.31 −0.4 to 0.83 0.7 0.487
Phyllomedusa sauvagii Intercept −29.3 3.14 −35.5 to −23.1 −9.33 <0.0001
Temperature 0.01 0.02 −0.02 to 0.04 0.59 0.5558
Photoperiod 2.3 0.26 1.8 to 2.8 8.99 <0.0001
Rainfall 0.02 0 0.01 to 0.03 4.88 <0.0001
Rainlag1 0.04 0.01 0.02 to 0.06 3.59 0.0003
Rainlag2 0.03 0.01 0.02 to 0.04 4.29 <0.0001
Rainlag3 0.03 0.01 0.01 to 0.05 3.7 0.0002
Rainlag4 0.01 0 0 to 0.01 1.37 0.1716
Rainlag5 0.01 0 0.01 to 0.02 4.22 <0.0001
Scinax nasicus Intercept −33.6 4.98 −43.4 to −23.8 −6.75 <0.0001
Temperature −0.06 0.05 −0.17 to 0.05 −1.06 0.2906
Photoperiod 2.57 0.43 1.73 to 3.41 6 <0.0001
Rainfall 0.05 0.01 0.03 to 0.07 5.36 <0.0001
Rainlag1 0.06 0.01 0.03 to 0.09 4.15 <0.0001
Rainlag2 0.03 0.01 0 to 0.06 2.18 0.0295
Rainlag3 0.02 0.01 0 to 0.04 1.75 0.0796
Rainlag4 0.03 0 0.03 to 0.04 7.38 <0.0001
Rainlag5 0.02 0.01 0 to 0.03 2.08 0.0371
Leptodactylus bufonius Intercept −40.0 5.01 −49.8 to −30.2 −7.98 <0.0001
Temperature 0.1 0.04 0.03 to 0.17 2.94 0.0033
Photoperiod 3.06 0.38 2.32 to 3.8 8.09 <0.0001
Rainfall −0.07 0.02 −0.1 to −0.04 −4.33 <0.0001
Catlag1 0.12 0.23 −0.33 to 0.56 0.52 0.6036
Catlag2 0.08 0.2 −0.31 to 0.48 0.4 0.6871
Catlag3 0.31 0.21 −0.11 to 0.72 1.44 0.149
Catlag4 0.03 0.2 −0.37 to 0.42 0.14 0.8859
Catlag5 0.64 0.08 0.49 to 0.8 8.29 <0.0001
22 C. M. SCHALK AND D. SAENZ
© 2015 Ecological Society of Australiadoi:10.1111/aec.12281
event, lags in rainfall and/or daily temperature (along
with photoperiod) were important drivers in calling
activity for all of the anuran species. As our study
highlights, we stress the importance of using abiotic
data collected across similar timeframes when
attempting to elucidate the factors driving calling
phenology in tropical anurans.
The permanency of breeding sites utilized by
anurans may also influence their response to abiotic
factors. Rainfall tends not to influence calling activity
of anurans that utilize semi-permanent breeding
ponds, whereas anurans that rely on temporary breed-
ing sites depend on rainfall for the establishment and
continued persistence of ponds and to stimulate
calling activity (Saenz et al. 2006; Steen et al. 2013). In
the nearby Chiquitano region of Bolivia, rainfall is an
important driver of calling activity as several species of
anurans that utilized temporary ponds (Schulze et al.
2009). All of the Chacoan anurans detected in this
study utilize ephemeral ponds as breeding sites, which
likely explains their significant and positive associa-
tions with nightly rainfall or lags in rainfall on previous
nights, highlighting that rainfall is an important driver
in their calling activity.
There was interspecific variation in the responses to
these abiotic factors, and even those species that exhib-
ited similar seasonal activity patterns or those with
similar reproductive modes appeared to be responding
Ta b l e 2. Continued
Species Variable Estimate SE LCL95 −UCL95 Z P
Physalaemus albonotatus Intercept −25.5 3.23 −31.9 to −19.2 −7.91 <0.0001
Temperature −0.11 0.02 −0.15 to −0.08 −6.17 <0.0001
Photoperiod 1.99 0.26 1.47 to 2.5 7.56 <0.0001
Rainfall 0 0.01 −0.02 to 0.03 0.16 0.8761
Catlag1 0.61 0.36 −0.1 to 1.31 1.69 0.0907
Catlag2 1.33 0.23 0.88 to 1.78 5.78 <0.0001
Catlag3 0.26 0.15 −0.03 to 0.55 1.75 0.08
Catlag4 0.51 0.24 0.03 to 0.98 2.08 0.0376
Catlag5 0.29 0.21 −0.12 to 0.71 1.37 0.1707
Physalaemus biligonigerus Intercept −18.0 2.37 −22.6 to −13.3 −7.57 <0.0001
Temperature −0.01 0.02 −0.06 to 0.03 −0.51 0.6069
Photoperiod 1.32 0.23 0.86 to 1.77 5.67 <0.0001
Rainfall 0.04 0.01 0.02 to 0.06 3.26 0.0011
Catlag1 1.3 0.17 0.97 to 1.64 7.62 <0.0001
Catlag2 0.68 0.13 0.42 to 0.94 5.05 <0.0001
Catlag3 −0.08 0.11 −0.3 to 0.14 −0.71 0.4797
Catlag4 0.84 0.1 0.64 to 1.04 8.17 <0.0001
Catlag5 0.32 0.18 −0.03 to 0.67 1.81 0.0706
Pleurodema guayapae Intercept −24.4 4.76 −33.7 to −15.1 −5.13 <0.0001
Temperature −0.15 0.07 −0.29 to −0.02 −2.29 0.0223
Photoperiod 2.02 0.51 1.01 to 3.02 3.92 <0.0001
Rainfall 0.09 0.02 0.06 to 0.12 5.7 <0.0001
Catlag1 1.19 0.19 0.82 to 1.56 6.35 <0.0001
Catlag2 0.11 0.47 −0.81 to 1.04 0.23 0.8146
Catlag3 −0.89 0.19 −1.27 to −0.51 −4.62 <0.0001
Catlag4 1.31 0.19 0.95 to 1.67 7.06 <0.0001
Catlag5 −0.33 0.24 −0.8 to 0.14 −1.39 0.1636
Odontophrynus americanus Intercept −3.91 2.88 −9.55 to 1.73 −1.36 0.174
Temperature 0.05 0.03 −0.01 to 0.11 1.58 0.1146
Photoperiod −0.03 0.32 −0.66 to 0.61 −0.08 0.9377
Rainfall 0.07 0.01 0.05 to 0.09 7.35 <0.0001
Cumulrain2 0.03 0.02 −0.01 to 0.08 1.54 0.1234
Cumulrain3 0.02 0.02−−0.01 to 0.06 1.23 0.2189
Cumulrain4 −0.03 0.01 −0.05 to −0.01 −3.2 0.0014
Cumulrain5 0.01 0.01 0 to 0.02 1.45 0.146
The probability of each species calling was modelled with the following variables: 2100 h air temperature, photoperiod,
amount of rainfall on the night of the calling event, a lag referencing the occurrence of rainfall ranging from 1 to 5 days prior
(catlagX, where X corresponds to the number of days prior to calling), a lag indicating the amount of rainfall occurring from
1 to 5 days prior to the calling event (rainlagX, where X corresponds to the number of days prior to calling) and/or a lag in
cumulative rainfall that occurred from 1 to 5 days prior to the calling date (cumulrainX, where X corresponds to the number of
days prior to calling). LCL95 =95% lower confidence level, UCL95 =95% upper confidence level.
ANURAN TEMPORAL PARTITIONING 23
© 2015 Ecological Society of Australia doi:10.1111/aec.12281
to different abiotic factors (Gottsberger & Gruber
2004). Two species, Leptodactylus bufonius and
Phyllomedusa sauvagii, had nearly the same pattern in
seasonal calling activity; they were prolonged breeders
(Wells 1977) across the entire rainy period.The physi-
ology of these two species may provide insights as to
their consistent, continuous reproductive activity;
L. bufonius is one of the few Chacoan anurans with
prolonged spermatogenesis occurring almost across
the entire year (Cei 1949a). Phyllomedusa sauvagii is
well-known for its ability to limit its water loss with the
waxy secretion that it produces and coats across its
skin (Shoemaker et al. 1972), thus allowing these frogs
to remain active even during the driest periods. Even
though these species were similar in their seasonal
activity patterns, differences occurred in their daily
calling patterns, particularly in their response to
rainfall. Calling activity of L. bufonius was negatively
associated with daily rainfall, whereas P. sauvagii
showed a positive response. In addition, the calling
activity of both species was positively associated with
lags in rainfall, but calling in P. sauvagii was positively
associated with the amount of rainfall from the previ-
ous nights, whereas L. bufonius called when rain
occurred the previous nights, although the amount of
rainfall was not important.The difference in the repro-
ductive mode of these two species may provide some
explanation to the observed differences in call
patterns. Prior to calling, an L. bufonius male excavates
an underground nest chamber where it breeds with a
female and the nest is later capped with mud (Cei
1949b; Reading & Jofré 2003). Once the nest is sealed,
the tadpoles can persist for over 40 days or until heavy
rainfall floods the nest allowing the tadpoles to enter a
nearby pond (Philibosian et al. 1974; Cei 1980;
Reading & Jofré 2003).Thus, the condition of the mud
and the reproductive mode of this species may con-
strain its daily breeding activity. During nights of heavy
rainfall, L. bufonius may not be able to construct or
maintain the integrity of the nest chamber as it could
collapse in on itself and cover recently oviposited eggs
with mud; however, the occurrence of rainfall on pre-
vious nights may leave the mud still malleable, thereby
allowing the male to construct the nest chamber.
Newly sealed nests are also vulnerable to predation if
the nest breaks apart too soon; Reading and Jofré
(2003) observed that newly sealed L. bufonius nests
that were quickly inundated with water broke down
and the egg masses were preyed upon by heterospecific
tadpoles. Phyllomedusa sauvagii is unique in this assem-
blage in that it is the only species in the system that
oviposits on vegetation overhanging ponds (Perotti
1997). As Gottsberger and Gruber (2004) observed in
other species of Phyllomedusa that possess the same
reproductive mode, calling activity in P. sauvagii coin-
cides with high amounts of rainfall occurring across
several days, and after the ponds have filled with water.
This ensures that the chance of the eggs desiccating is
low as they develop and that when they finally hatch,
the tadpoles will drop into a well-established pond that
has little risk of drying (Gottsberger & Gruber 2004).
A similar pattern was also observed in the Chiquitano
dry forest of Bolivia, where Phyllomedusa boliviana
exhibited prolonged calling activity over an artificial
pond (Schulze et al. 2009).
The patterns of calling activity of C. cranwelli,
O. americanus,P. guayapae and S. nasicus are indicative
of explosive breeders (sensu Wells 1977); although
they were detected nearly every month in the rainy
period, they called only over short periods (i.e. one to
several days). Ceratophrys cranwelli,O. americanus and
S. nasicus oviposit their eggs directly in the water (Cei
1980; Perotti 1997), whereas P. guayapae constructs a
flattened foam nest, but its eggs are often exposed even
while in the foam nest and vulnerable to predators
(Schalk 2012; Valetti et al. 2014). Many tadpoles in
the tropics have omnivorous or carnivorous feeding
habits and are known to prey upon eggs and tadpoles
of heterospecifics (Heyer et al. 1975; Magnusson &
Hero 1991; Altig et al. 2007; Schalk et al. 2014). Given
that the eggs of C. cranwelli,O. americanus,P. guayapae
and S. nasicus are exposed and vulnerable to predators
(Magnusson & Hero 1991), these species may breed
over short periods as a means to limit exposure of their
eggs to heterospecific tadpoles and other potential
predators (e.g. invertebrates (CMS, unpubl. data) or
killifishes (Montaña et al. 2012)) as the pond is colo-
nized by predators over time.While the calling activity
of these explosive breeders was positively correlated
with daily rainfall, all four species were positively cor-
related to lags in rainfall, particularly with the day
before calling occurred. Explosive breeders tend to
utilize ephemeral sites, to which they often need to
migrate as the ponds are formed (Wells 1977; Saenz
et al. 2006). The highly fossorial species can remain
inactive for long periods (Cei 1980; Valetti et al.
2014), and therefore, they likely need several days of
rain to stimulate their emergence and migration to
their breeding sites. Similarly, the hylid S. nasicus
needs to migrate from their arboreal refugia to their
breeding sites, which may explain a similar pattern in
its calling activity.
In the lowland tropical forest of French Guiana,
Gottsberger and Gruber (2004) observed a temporal
partitioning of species breeding and calling activity in
accordance to their reproductive mode. If reproductive
mode imposes constraints on breeding activity in all
anurans, then we would expect to see an emerging
pattern where species with the same reproductive
mode exhibit a similar response to the abiotic factors,
as was observed in Gottsberger and Gruber (2004).
However, in our study, congeners with the same repro-
ductive modes exhibited different responses to the
abiotic factors in their daily calling activity. The two
24 C. M. SCHALK AND D. SAENZ
© 2015 Ecological Society of Australiadoi:10.1111/aec.12281
pairs of congeners occurring in this system (R. major/
R. schneideri and P. albonotatus/P. biligonigerus), did not
partition themselves spatially in their use of calling
sites, nor temporally as they overlapped in their calling
activity across the latter half of the rainy season. The
reproductive modes of some species impose stronger
constraints on the reproductive activity as compared
with others (Gottsberger & Gruber 2004). Both
species of Physalaemus and Rhinella breed only when a
pond has already formed; Physalaemus species create
floating foam nests that contain eggs, while both
species of Rhinella oviposit directly in the water.Thus
a pond needs to be newly formed or already estab-
lished for breeding to commence as compared with
L. bufonius for example (Cei 1949b).The reproductive
modes of Rhinella spp. and Physalaemus spp. may not
impose strong constraints on when these species are
able to breed once a pond is formed, which may allow
them to exhibit different responses to the abiotic factor
and partition calling activity over short time periods,
reducing their overlap. Studies have shown that in
other communities, species partition themselves
acoustically, spatially and temporally as a means to
reduce competition (Crump 1974; Hödl 1977;
Duellman & Pyles 1983). It is unclear as to why these
species exhibit the temporal partitioning observed.
Reproductive character displacement, that is the
accentuation of differences in courtship behaviour
in sympatric populations relative to differences in
allopatric populations may provide a mechanism
underlying the observed pattern (Brown & Wilson
1956). In anurans, most studies of reproductive char-
acter displacement typically focus on differences in
mating calls or female mate choice in allopatric and
sympatric populations of frogs (Blair 1974; Gerhardt
1994). However, other aspects associated with court-
ship behaviour, such as the selection of calling sites
could be explored in this framework; the observed
pattern may be the result as a means to reduce com-
petition for calling sites. Höbel and Gerhardt (2003)
observed that males of the green tree frog (Hyla
cinerea) called from higher perch sites when syntopic
with the congener Hyla gratiosa. In the Chaco,
each congeneric pair utilizes the same type of calling
site at the breeding ponds; Rhinella schneideri and
R. major call from the edges of ponds (Cei 1980;
Schalk & Morales 2012), whereas P. albonotatus and
P. biligonigerus call from the water’s surface and among
emergent vegetation (Cei 1980; Schalk 2010). Given
that there is high overlap in the types of calling sites
used by each congeneric pair, suitable calling sites may
be limited around breeding ponds. Thus, these popu-
lations may diverge in the environmental conditions
that drive calling activity, allowing the males to segre-
gate temporally and gain access to calling sites that
may be otherwise unavailable.To further explore these
mechanisms, the calling activity of allopatric popula-
tions of each of the congeneric pair of these species
would need to be compared with the syntopic pattern
observed in this study.In addition, these patterns high-
light that those studies that group and generalize
species breeding activity by their reproductive mode
(e.g., Gottsberger & Gruber 2004) may not be able
to detect the subtle, species-specific differences in
breeding activity, especially across short (i.e. daily)
timeframes.
This study highlights the importance of weather on
regulating the timing of reproductive phenology in this
assemblage of tropical anurans. Our understanding of
how exogenous (i.e. climatic variables) and endog-
enous factors (i.e. reproductive modes) interact to
influence the temporal partitioning of these species
can provide insights on the structure of larval assem-
blages and the interactions occurring within the breed-
ing ponds (Todd et al. 2011). Amphibians exhibit the
strongest response to climate warming scenarios by an
earlier onset of breeding phenology (Parmesan 2007),
thus our results could have implications to under-
standing potential climate change scenarios and the
mistimed species interactions that occur as a result
(Yang & Rudolf 2010; Todd et al. 2011; Saenz et al.
2013). Although extreme weather events (e.g.,
drought) can negatively affect amphibian reproductive
activity (Jansen et al. 2009), our study suggests that
even subtle changes in environmental factors, such as
an increase in the intermittent period between rainfall,
may impact the calling phenology of tropical anurans.
ACKNOWLEDGEMENTS
We thank the Capitania del Alto y Bajo Isoso (CABI)
for permission to conduct research in Isoso, and R.L.
Cuellar for providing logistical support while in
Bolivia. K. Rivero at the Museo Noel Kempff Mercado
assisted with permit support. We thank J. Childress
and N. Aall for their assistance with transcribing frog
calls, N. Koerth for assistance with statistical analyses,
and C.G. Montaña and two anonymous reviewers for
constructive comments on the manuscript. Support
was provided by the National Science Foundation’s
Graduate Research Fellowship Program, the Applied
Biodiversity Science NSF−IGERT Program at Texas
A&M University (NSF−IGERT Award # 0654377),
and the Southern Research Station, U.S. Forest
Service. This is publication number 1503 of the Bio-
diversity Research and Teaching Collections at Texas
A&M University.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in
the online version of this article at the publisher’s
web−site:
Appendix S1. Occurrence of calling males across
seven surveyed ponds.
Appendix S2. Call intensity scores for the four rare
species of anurans each night.
ANURAN TEMPORAL PARTITIONING 27
© 2015 Ecological Society of Australia doi:10.1111/aec.12281
