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Ethology Ecology & Evolution
ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/teee20
Diet of terrestrial anurans in an ephemeral and
simplified habitat during the dry season in the
Brazilian Cerrado
Reuber A. Brandão , Jéssica Fenker , Bruno E. Pires de Carmago Lopes , Vitor
M. de Alcantara de Sena & Beatriz D. Vasconcelos
To cite this article: Reuber A. Brandão , Jéssica Fenker , Bruno E. Pires de Carmago Lopes ,
Vitor M. de Alcantara de Sena & Beatriz D. Vasconcelos (2020): Diet of terrestrial anurans in an
ephemeral and simplified habitat during the dry season in the Brazilian Cerrado, Ethology Ecology
& Evolution, DOI: 10.1080/03949370.2020.1755373
To link to this article: https://doi.org/10.1080/03949370.2020.1755373
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Published online: 26 May 2020.
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Diet of terrestrial anurans in an ephemeral and simplified
habitat during the dry season in the Brazilian Cerrado
REUBER A. BRANDÃO
1,*
,JÉSSICA FENKER
2
,
BRUNO E. PIRES DE CARMAGO LOPES
1
,VITOR M. DE ALCANTARA DE SENA
1
and BEATRIZ D. VASCONCELOS
1
1
Laboratório de Fauna e Unidades de Conservação, Departamento de Engenharia
Florestal, Universidade de Brasília, Brasília, DF, CEP: 70.910-900, Brazil
2
Ecology and Evolution Division, Research School of Biology, Australian National
University, Canberra-ACT, 2612, Australia
Received 1 December 2019, accepted 1 April 2020
Amphibians often use ephemeral and simplified habitats during dry seasons
in tropical biomes. These simplified habitats can have less prey available, but only
a few studies focus on how their use affects frogs’diet. Here we studied the diet of
three terrestrial frogs (Adenomera sp., Ameerega berohoka, and Rhinella ocellata)at
a riverbank exposed only during the dry season in the Brazilian Cerrado biome.
Diets overlapped more than expected by chance and were composed mainly of social
insects (ants and termites). Prey volumes were not related to the size of frogs or their
head measurements. Frogs at the riverbank ingested less prey categories and fewer
prey items in comparison to studies conducted in more stable and complex environ-
ments. We suggest that frogs were attracted to riverbanks by the humidity and
availability of reproductive sites, opportunistically ingesting prey available in the
habitat. The abundance of social insects allowed the presence of frogs specialized in
ants, such as the bufonid Rhinella ocellata and the dendrobatid Ameerega berohoka.
KEY WORDS:ephemeral environment, trophic ecology, seasonality, Ameerega bero-
hoka,Adenomera sp., Rhinella ocellata, riverbank.
INTRODUCTION
Ephemeral habitats are often used by opportunistic species that explore tem-
poral opportunities for food, shelter, or mating (Levins 1968; Maurer & Sih 1996). The
density of opportunistic predators in these habitats can sometimes be higher than in
perennial habitats, which are more predictable and stable regarding resource avail-
ability (Reitsma et al. 2009; Sladecek et al. 2012) and, in turn, increase competition for
prey and space (Hagan et al. 1996).
*
Corresponding author: Reuber Albuquerque Brandão, Laboratório de Fauna e Unidades de
Conservação, Departamento de Engenharia Florestal, Universidade de Brasília, Brasília, DF, CEP:
70.910-900, Brasil (E-mail: reuberbrandao@gmail.com).
Ethology Ecology & Evolution, 2020
https://doi.org/10.1080/03949370.2020.1755373
© 2020 Dipartimento di Biologia, Università di Firenze, Italia
Different environments harbour different prey communities (Forstner et al.
1998;Françaetal.2004), and simplified ecosystems tend to have lower prey avail-
ability when compared to more complex environments, increasing competition
(Zacharias et al. 2007;Araújoetal.2009). Simplified and ephemeral ecosystems
can limit the presence of insects due to a lack of key resources, by the lower
complexity in habitat architecture or by affecting the establishment of colonies
(mainly for ants and termites) (Gardner et al. 1995;Goff&Win1997;Hansen
2000; Cagnolo et al. 2002; Fernandez-Marin et al. 2004). More complex habitats, in
contrast, can support more insects because they attract more species from the
regional pool of potential colonists, supporting larger, more stable, and richer insect
communities (Straw & Ludlow 1994). Accordingly, closely related predators that co-
occur synchronically in ephemeral habitats (such as the frogs studied here) can
present subtle differences in resource use, promoting low niche overlap (Dias &
Rocha 2007; Sabagh et al. 2010; De Oliveira et al. 2015; Fossette et al. 2017;Sovie
et al. 2019).
Studies focusing on how opportunistic species share or explore available
resources in seasonal and/or ephemeral habitats have highlighted the effects of spe-
cific biotic relationships or environmental characteristics on resource use (Heyer et al.
1975; Schwemmer et al. 2008; Ferrari et al. 2017; Sovie et al. 2019). Although the
marked seasonality of tropical biomes, as the Brazilian Cerrado, has deep effects on
anuran activities (Moreira & Barreto 1997; Colli et al. 2002; Prado et al. 2005), few
studies focused on the importance of ephemeral humid habitats as a source of dietary
resources for these animals during severe dry seasons. Moreover, these habitats can
ameliorate physiological constraints related to dehydration during the tropical dry
season (Anderson et al. 2017).
Understanding trophic relationships between anurans is essential to clarify the
role of these animals in nature (Forti et al. 2011), especially in complex food webs.
Amphibians are opportunistic predators feeding on a large number of invertebrates
and are preyed upon by vertebrates that rarely use arthropods as dietary items (Wilbur
& Fauth 1990; Sheppard & Harwood 2005; Brose et al. 2006). Hence, amphibians are
a vital element in food webs, particularly in tropical regions (Whiles et al. 2006;
Verburg et al. 2007; Zipkin et al. 2020).
Conversely, anuran diets are affected by seasonality, habitat/microhabitat use,
phylogeny, latitude, cranial morphology, body size, and physiology (Emerson 1985;
Duellman & Lizana 1994; Biavati et al. 2004; Hirai 2004; Grayson et al. 2005; López
et al. 2009; Ceron et al. 2019; Marques-Pinto et al. 2019). Although processes that
determine prey selection in frogs remain poorly understood, foraging mode, ontogeny,
phylogenetic inertia, prey toxicity, and microhabitat selection have been shown to
affect anuran diet composition at the local scale (Lima & Moreira 1993; Caldwell &
Vitt 1999; Hirai & Matsui 2001; França et al. 2004; Darst et al. 2005; Bonansea & Vaira
2007; Lima & Eterovick 2013).
However, competition for food is uncommon in anurans (Kuzmin 1995), and
wide niche overlaps are commonly reported between sympatric (and often closely
related) species in tropical environments (e.g. França et al. 2004; Santos et al. 2007;
Rodrigues et al. 2010; Marques-Pinto et al. 2019). Ephemeral habitats can present
opportunities to access poorly explored, but unpredictable, food resources (Griffiths
1997), that can affect prey selection by frogs. The foraging strategies of frogs can be
grouped into two broad types. The “ant-specialists”feeds mainly on colonial, slow-
moving and/or chitinized preys, such as ants and mites. The “non ant-specialists”feeds
2 R.A. Brandão et al.
on a larger variety of items, often ingesting softer preys, and usually avoiding ants
(Toft 1980).
The strong seasonality in the Brazilian Cerrado affects the spatial and temporal
occurrence of frogs (and their preys) along the landscape (Santoro & Brandão 2014).
Cerrado frogs usually show a high degree of dietary overlap through the conspicuous
ingestion of ants and termites (e.g. Moreira & Barreto 1996; Biavati et al. 2004; Araújo
et al. 2009; Marques-Pinto et al. 2019), which likely results from the high abundance of
these colonial insects in Cerrado habitats.
Herein, we evaluate how three species of terrestrial frog, belonging to three
different families, use alimentary resources in an ephemeral and simplified habitat,
corresponding to a sloping and unvegetated riverbank exposed by the lowering levels
of Noidori River during the Cerrado dry season. The frogs are the leptodactylid
Adenomera sp., the dendrobatid Ameerega berohoka and the bufonid Rhinella ocellata.
These three species were abundant along the riverbank, using the habitat for repro-
duction, feeding, shelter, and, probably, water balance. Additionally, this is the first
report on the diet of A. berohoka and R. ocellata.
We expected that: (1) frogs would be using opportunistically all available preys in
one of the fewhumid habitats available in the landscape, presenting higher niche overlap
than expected by chance, (2) morphological constraints imposed by amphibian body size
and head measurements are related to maximum prey size, prey number and/or prey
volume for each species, (3) since seasonally flooded habitats in Cerrado can prevent the
establishment of colonial insects, frogs would be feeding less on ants and termites than
closely related species in other Cerrado habitats, and, (4) the abundance and richness of
prey species used by frogs along the riverbank will be lower than the diet of related and
similar-sized species in stable and putatively richer environments.
MATERIAL AND METHODS
Studied area
The frog sampling was carried out along a segment on the margins of the Noidori River,
near its confluence with Mortes River, in Nova Xavantina Municipality, Mato Grosso State (14°
47ʹ55”S, 52°38ʹ31”W, 280 m a.s.l.). The 100 m sampling transect was placed along a shaded,
humid, and sloping riverbank with muddy soil (Fig. 1), from 22 to 25 August 2010. The riverbank
was covered by water during the rainy season and, when exposed, lacked green vegetation. The
transect substrate was characterized mainly of exposed soil and portions of leaf litter accumu-
lated and exposed roots on slope portions (Fig. 1). The river can reach a maximum level of 3 m
above the minimum water level at the end of the dry season, the time when we set our transect.
The period from the maximum to minimum water level varies from year to year, lasting 4 to 6
months. The vegetation above the riverbanks is composed of riparian forest, a forested physiog-
nomy found along medium to larger rivers, not forming galleries above the watercourse (Ribeiro
& Walter 1998). The climate corresponds to Köppen Aw (Tropical Savanna), with contrasting
climatic conditions between wet (October to March) and dry (April to September) seasons
(Alvares et al. 2013).
Studied species
The genus Adenomera Steindachner 1867 is composed of 20 ground-dwelling species
occurring from east Andes to Southern South America (Carvalho et al. 2019; Frost 2020). It is
Diet of frogs in an ephemerous habitat 3
a known species complex, with several undescribed species along this range (Angulo et al. 2003).
As the proper identification of species in this genus needs acoustic and genetic analysis, we
decided to treat the species at our study site as Adenomera sp. The genus Ameerega Bauer 1986 is
composed of 32 species, widely distributed in South America, especially in the Amazon (Frost
2020). Ameerega berohoka Vaz-Silva and Maciel 2011 is endemic to Central Brazil and little is
known about its natural history (Sant’Anna et al. 2017). The genus Rhinella Fitzinger 1826 is
composed of 92 species distributed throughout the Americas, from Southern Texas to Uruguay,
Central Argentina, and Chile, including one species that was introduced in several places around
the world (Frost 2020; M. Solé pers. comm.). Rhinella ocellata Günther 1858 is a small toad with
terrestrial habits, belonging to the R. margaritifera species group (Fouquet et al. 2007), that lives
near rivers and other waterbodies (Matavelli et al. 2014) in the states of Goiás, Maranhão, Bahia,
Mato Grosso, Minas Gerais, Tocantins, and Pará (Freitas et al. 2018).
The frogs were sampled by active searches (Crump & Scott 1994). Since these species were
active at day and nighttime, the sampling was performed in the mornings (from 8–12 hr) and at
night (16–20 hr), totalling 32 sampling hours. The distances between individuals, and from the
individuals to the river, were measured using a tapeline, whereas temperature and humidity were
gathered with a portable pen-like digital thermo-hygrometer.
Our study at Noidori river was part of a comprehensive inventory funded by a network of
Brazilian science institutions aiming to improve Biodiversity knowledge in the country (PPBio
and SISBIOTA programs), and all individuals were collected for further molecular, reproductive,
and physiological studies. Permissions were provided by Chico Mendes Institute for Biodiversity
Conservation (Instituto Chico Mendes de Conservação da Biodiversidade –ICMBio license
SISBIO 28,190–1).
All frogs were carefully placed in individual plastic bags and moved to the lab, where they
were euthanized using anaesthetic overdose (lidocaine 5%), fixed in 10% formalin, labelled, and
later housed at the Herpetological Collection of the University of Brasília (CHUNB). These
Fig. 1. —Riverbank of the Noidori river showing the aspect of the habitat during our sampling. Photo:
R.A. Brandão.
4 R.A. Brandão et al.
procedures are acknowledged by the National Council on Animal Experimentation Control
(CONCEA) as effective for avoiding animal suffering and pain (Brasil –MCTIC 2018).
In addition, we installed 20 pitfall traps filled with alcohol 70% and some detergent drops
to measure prey availability along the riverbank. These pitfalls were made using 500 mL dis-
posable cups placed 10 m apart in a transect that covered all microhabitats present along the
riverbank (litter, dead trunks, roots, bare soil, pebbles), distanced 20 to 120 cm from the river. No
frogs were captured by these traps. We decided to use only pitfall traps to sample arthropods
because the riverbank has very little litter accumulation, which negates other arthropod sampling
methods. Furthermore, cursorial preys are more commonly captured by pitfalls and are more
often located by sit-and-wait predators, like frogs.
We measured the snout-vent length (SVL), head length (HL), head width (HW), and head
height (HH) using digital callipers (up to 0.01 mm) of each frog. We removed the stomach
contents and we counted, identified (to the Order or Family, for ants), and measured all items
under a stereoscopic microscope.
Statistical analysis
We estimated prey volumes based on the ellipsoid formula proposed by Griffiths and
Myllote (1987):
V¼4π
=
3l
=
2w
=
2
2
where wcorresponds to item width and lis the item length. We also estimated prey frequencies
(proportion of stomachs containing each prey item), prey abundances (number of individual
preys by prey category), and volumetric proportions (proportion of each prey item volume by the
total prey volume). The prey category importance value index (IVI) was calculated using the
equation:
IVI ¼F%þN%þV%ðÞ
=
3
where F% represents the frequency proportion, N% the numeric proportion, and V% the volu-
metric proportion (Marques-Pinto et al. 2019).
In order to evaluate how many prey items were selected or avoided, we calculated the
electivity index proposed by Jacobs (1974):
D¼Rk Pk
=Rk þPkðÞ2RkpPkðÞ
where Drepresents Jacobs electivity index, Ris the proportion of a particular item in the diet, Pis
the proportion of the item in the environment. The index ranges from −1 to 1, with negative
values indicating that a particular item is avoided, values near zero indicate that a particular prey
item is captured in the same proportion as observed in the environment, whereas positive values
indicate active search by frogs. Therefore, we only used food items present in both diet and
pitfalls, in order to avoid bias.
We calculated the niche breadth for prey abundance for each species using the inverse of
Simpson index:
B¼1=Xpi^
2
ðÞ
where iis the resource category, pis the resource icategory proportion (Simpson 1949).
Pairwise niche overlap was calculated using Pianka index:
α¼U1jU2j
U1jðÞU2jðÞα2
Diet of frogs in an ephemerous habitat 5
where U1j is the proportion of resource jused by species 1and U2 j refers to the proportion of
resource juse by species 2(Pianka 1973). We evaluated if observed niche overlap was smaller
than expected by chance using the module Niche Overlap in the package “ECOSIM R”in software
R, with 1,000 randomizations. Niche overlap analysis by daily activity abundance (temporal
niche) was also performed aiming to evaluate if the species are overlapping in the temporal
space. We used the algorithm RA2, which is used when, even in the absence of interactions
between species, some resources are not available to some species. The RA2 algorithm replaces
the value of resources used in the original matrix by values between 0 and 1, but the resources not
used are kept as zeros (Gotelli & Entsminger 2003). The null hypothesis is that the observed niche
overlap is larger or similar to that expected by chance (simulated overlap). If the species are
partitioning dietary resources, the variance on the observed niche overlap is smaller than the
observed overlap simulated by chance.
We used multiple regressions to access the effect of frog’s head and size measurements and
the volume (expressed by prey cubic root) and length of the largest ingested prey using R v.3.2.2
(R Core Team 2010). For these analyses, we used the largest intact prey found in each stomach.
We removed the predator size effect using an isometric vector aiming to evaluate the effect
of head morphology in prey capture. We log-transformed each morphometric variable prior to
the analysis for all individuals. We regressed all morphometric variables against a size-isometric
variable to obtain size-adjusted residuals. The isometric variable was obtained by multiplying an
isometric eigenvector defined as P
−0.5
(P = number of variables) by the sum of the log-
transformed variables (Somers 1989). The significance of multiple regressions was tested using
ANOVA, and we performed linear regressions to examine the effect of each variable on the
model.
RESULTS
Species diets
We captured 53 individuals of Adenomera sp., of which 47 presented stomach
contents, ranging from 1 to 25 items per stomach (2.55 ± 0.38). We found 11 orders,
distributed in 120 food items. The species niche width was 5.07. Formicidae,
Coleoptera, and Isoptera were the most important items according to IVI (Table 1).
We captured 41 individuals of Ameerega berohoka, of which 32 presented stomach
contents, ranging from 1 to 6 items per stomach (5.16 ± 0.18). We found 10 orders,
distributed in 164 food items. The species niche width was of 6.79. Diptera,
Formicidae, and Coleoptera were the most important items (Table 1). We captured
19 individuals of Rhinella ocellata, of which 15 presented stomach contents, ranging
from 1 to 15 items per stomach (6.13 ± 0.73). We found only three orders, distributed
in 92 food items. The species niche width was 1.33. Formicidae was the most impor-
tant item (Table 1).
We found 376 prey items in the diet of the three frog species, distributed in 18
categories, whereas pitfalls resulted in the capture of 132 invertebrates, distributed in
11 orders (Table 2). The main invertebrates found in pitfalls were ants (39%), beetles
(19%) and flies (12%). We decide to evaluate electivity using pitfall data instead of
pooled categories found in stomachs aiming to avoid the effect of active searching in
frogs in insect selection. Moreover, the categories found in the stomachs that were not
recorded in the traps were represented by very few individuals, adding bias in the
electivity comparisons.
Adenomera sp. showed preference for termites and tricopterans, while collembo-
lans and acari were avoided. Coleopterans and spiders were selected according to the
6 R.A. Brandão et al.
Table 1.
Diet summary of Adenomera sp., Ameerega berohoka, and Rhinella ocellata at a riverbank in Noidori river during dry season, depicting relative abundance (N
%), relative frequency (F%), relative volume (V%), and important relative index (IRI).
Adenomera sp.
(n = 53)
Ameerega berohoka
(n = 41)
Rhinella ocellata
(n = 19)
N% F% V% IRI N% F% V% IRI N% F% V% IRI
Acari ––––0.14 0.14 0.1 0.13 0.03 0.07 –0.03
Araneae 0.04 0.03 0.37 0.15 0.03 0.03 0.01 0.02 ––––
Blattodea 0.25 0.24 0.06 0.18 0.04 0.04 0.16 0.08 ––––
Isoptera
Coleoptera 0.20 0.21 0.15 0.18 0.15 0.13 0.29 0.19 0.11 0.17 0.15 0.14
Collembola ––––0.15 0.15 0.03 0.11 ––––
Diptera 0.08 0.09 0.06 0.08 0.19 0.19 0.21 0.20 ––––
Hemiptera 0.07 0.07 0.22 0.12 –––– ––––
Hymenoptera 0.29 0.28 0.06 0.21 0.20 0.21 0.15 0.19 0.86 0.77 0.85 0.82
Formicidae
Hymenoptera ––––0.03 0.03 0.01 0.03 ––––
Non-Formicidae
Lepidoptera 0.01 0.01 0.01 0.01 –––– ––––
Mantodea ––––0.01 0.01 0.01 0.01 ––––
Neuroptera 0.01 0.01 0.01 0.01 –––– ––––
Orthoptera 0.03 0.03 0.06 0.04 –––– ––––
(Continued )
Diet of frogs in an ephemerous habitat 7
Table 1.
(Continued)
Adenomera sp.
(n = 53)
Ameerega berohoka
(n = 41)
Rhinella ocellata
(n = 19)
N% F% V% IRI N% F% V% IRI N% F% V% IRI
Pseudoscorpiones 0.01 0.01 0.01 0.01 –––– ––––
Thysanoptera ––––0.01 0.01 0.01 0.01 ––––
Trichoptera 0.03 0.03 0.01 0.02 0.06 0.16 0.03 0.05 ––––
The total number of prey and the volume per species are based on grouped stomachs. Preys with the highest indexes of importance for each species are in
bold.
8 R.A. Brandão et al.
abundance found in the environment (Fig. 2). Ameerega berohoka showed preference
for collembolans, tricopterans, Acari, and Diptera, while ants and spiders were
avoided. Ameerega berohoka consumed beetles according to their abundance in the
environment (Fig. 2). Rhinella ocellata showed preference only for ants, whereas all
other orders were avoided (Fig. 2).
Table 2.
Invertebrates captured in pitfalls placed
along a transect in the Noidori river dur-
ing dry season, showing their abundance
(N) and relative abundance (N%).
Invertebrate N N%
Formicidae 51 0.39
Coleoptera 25 0.19
Diptera 16 0.12
Isoptera 15 0.11
Acari 10 0.08
Aranae 6 0.05
Hemiptera 3 0.02
Trichoptera 2 0.02
Dermaptera 1 0.01
Blattodea 1 0.01
Hymenoptera 1 0.01
Collembola 1 0.01
Total 132
-1.0
-0.5
0.0
0.5
1.0
Formicidae
Coleoptera
Diptera
Isoptera
Acari
Aranae
Trichoptera
Collembola
Jacob's Elective Index
Prey Items
Fig. 2. —Jacobs’Electivity Index resulting from the comparison of invertebrate rate frequencies in the
pitfalls and stomachs of Adenomera sp. (tracing), Ameerega berohoka (grey) and Rhinella ocellata (black)
stomach contents in the Noidori riverbank. The index ranges from −1 (negative electivity –avoided) to + 1
(positive electivity –active search for prey category).
Diet of frogs in an ephemerous habitat 9
Frogs at the Noidori riverbank presented less items and ingested fewer prey
items per stomach than closely related or similar-sized frogs in other localities, includ-
ing Cerrado habitats, suggesting that the simplified and ephemerous habitat we stu-
died had less available prey when compared to more stable and complex habitats
(Table 3). The prey richness ingested by R. ocellata and Adenomera sp. was smaller
than the richness observed for related or similar-sized species (R. ocellata:Z=−3.6,
P< 0.001, Adenomera sp.: Z = −2.17, P= 0.03). Ameerega berohoka ingested similar
prey richness (Z = −1.56, P= 0.12), but the abundance of ingested prey was much
lower than for other related species (Table 3).
Niche overlap
The diet overlap was larger than the expected by chance (mean of simulated
index = 0.175, observed index = 0.181, P< 0.185), suggesting that the species are not
partitioning preys. The temporal overlap was larger than the expected by chance
(mean of simulated index = 0.173, observed index = 0.187, P< 0.111), indicating that
species were active at similar times along the day.
Relationship between prey length and volume and anuran morphology
Body size and head measurements were related to prey length only for
Adenomera sp. (F= 2.870, P< 0.035), being related to head height and width. Prey
length was not related to body size or to head measurements in Ameerega berohoka
(F= 0.127, P< 0.971) and Rhinella ocellata (F= 0.295, P< 0.874). As the variance on
prey length was similar for the three species, we did not find a model that explained
the relationship between frog’s morphology and prey length, suggesting that frogs
were capturing all available prey when they were detected, regardless of their size.
Accordingly, frog head morphology was only related to prey morphology for
Adenomera sp., the smallest species in our study. The body size and head measure-
ments were not related to prey volume for Adenomera sp. (F= 2.022, P< 0.110),
Ameerega berohoka (F= 0.310, P< 0.869), or Rhinella ocellata (F= 0.145, P< 0.961).
DISCUSSION
The frogs in our study area are not selecting preys based on morphological or
ecological (competitive) constraints. Prey length and volume are not related (Ameerega
berohoka and Rhinella ocellata) or are only weakly related (Adenomera sp.) to frog body
size or head morphology, suggesting that their diets are based on small preys, often the
most available. Ants, which make up about 70% of the animal biomass from humid
environments (Holldobler & Wilson 1990) and termites, which correspond to most of
the animal biomass in the Cerrado biome (Redford 1984) were very abundant in the
habitat and compose most of the diet of the studied species. The ingestion of these
small preys can affect the expected relationship between frog morphology and prey
size (Toft 1980), especially in our study area, where two of the species (A. berohoka and
R. ocellata) can be considered ant-specialists (sensu Toft 1980).
10 R.A. Brandão et al.
Table 3.
Diet comparisons for some species of Rhinella spp. (Bufonidae), Ameerega spp. (Dendrobatidae), and Adenomera spp. (Leptodactylidae), showing the richness
of prey categories, abundance of prey items by stomach (from original publication), and the most relevant prey items for localities in South America.
Taxa Prey categories
richness
Prey items per stomach
(Mean ± SD)
Most relevant dietary
items Locality Reference
Bufonidae
R. azarai 8 NA Ants Corrientes (ARG) Ingaramo et al. (2012)
R. bergi 7 NA Ants Corrientes (ARG) Duré et al. (2009)
R. bergi 10 NA Ants, beetles Miranda, MS (BRA) Piatti and Souza
(2011)
R. dorbignyi 22 23.15 ± 23.60 Ants, crickets Buenos Aires Province
(ARG)
Isacch and Barg (2002)
R. fernandezae 7 NA Ants and beetles Corrientes (ARG) Duré et al. (2009)
R. fernandezae 20 NA Ants, hymenopterans San Javier Department
(ARG)
Peltzer et al. (2010)
R. fernandezae 19 NA Ants, isopods San Javier Department
(ARG)
Peltzer et al. (2010)
R. granulosa 8 25.40 ± 21.26 Ants Maldonado (URU) Rosa et al. (2002)
R. granulosa 9 33 Ants, beetles Rio São Francisco, BA
(BRA)
Damasceno (2005)
R. granulosa 9 26.80 ± 14.10 Ants, termites Chapada Diamantina, BA
(BRA)
Santana and Juncá
(2007)
R. granulosa 7 NA Ants Corrientes (ARG) Duré et al. (2009)
R. granulosa 3 NA Ants Villavicencio (COL) Astwood-Romero et al.
(2016)
R. hoogmoedi 21 14.33 ± 16.12 Ants, mites Guaramiranga, CE (BRA) Britto et al. (2013)
(Continued )
Diet of frogs in an ephemerous habitat 11
Table 3.
(Continued)
Taxa Prey categories
richness
Prey items per stomach
(Mean ± SD)
Most relevant dietary
items Locality Reference
R. hoogmoedi 19 15.25 ± 11.58 Ants Michelin Reserve, BA
(BRA)
Castro-Santos (2016)
R. humboldti 12 NA Beetles, ants, termites Albania, La Guajira (COL) Blanco-Torres (2019)
R. margaritifera 7 NA Ants Villavicencio, Meta (COL) Astwood-Romero et al.
(2016)
R. margaritifera 3 40.30 ± 14.20 Ants Paguana (PER) Toft (1980)
R. margaritifera 23 36.50 Ants and beetles Reserva Cuzco Amazónico
(PER)
Parmelee (1999)
R. margaritifera 24 40.88 Ants Yasuní National Park
(ECU)
Menéndez-Guerrero
(2001)
R. ocellata 3 6.13 ± 0.73 Ants Noidori river, MT (BRA) Present study
R. proboscidea 44 59.78 ± 99.89 Ants Manaus and Jatapú, AM
(BRA)
Borges et al. (2019)
R. scitula 16 NA Ants Serra da Bodoquena, MS
(BRA)
Maragno and Souza
(2011)
Dendrobatidae
A. berohoka 11 5.16 ± 0.18 Ants, flies, beetles Noidori river, MT (BRA) Present study
A. bilinguis 49 47.70 ± 3.60 Ants, termites Cuyabeno, Sucumbios
(COL)
Caldwell (1996)
A. braccata 13 39.70 ± 40.60 Ants, acari Chapada Guimarães, MT
(BRA)
Forti et al. (2011)
A. flavopicta 21 13.04 ± 17.51 Ants, termites Several localities, GO
(BRA)
Biavati et al. (2004)
12 R.A. Brandão et al.
A. flavopicta 12 NA Lepidopteran larvae,
termites
ESEC Pirapitinga, MG
(BRA)
Lima and Eterovick
(2013)
A. trivittata 5 56.30 ± 21.70 Ants Panguana (PER) Toft (1980)
A. trivittata 14 NA Ants, termites Juruti, PA (BRA) Luiz et al. (2015)
A. picta 4 14.50 ± 2.80 Ants Panguana (PER) Toft (1980)
A. picta 19 33.20 Ants Reserva Cuzco Amazónico
(PER)
Parmelee (1999)
A. picta 5 NA Ants Serra da Bodoquena, MS
(BRA)
Landgref-Filho et al.
(2019)
Leptodactylidae
Adenomera sp. 24 6.2 Beetles, larvae Reserva Cuzco Amazónico
(PER)
Parmelee (1999)
Adenomera sp. 11 2.55 ± 0.38 Ants, beetles, termites Noidori river, MT (BRA) Present study
A. andreae 20 NA Crickets, termites, Ants Mineração, RO (BRA) Vitt and Caldwell
(1994)
A. andreae 12 25.36 ± 4.52 Ants, larvae, collembola Caracari, RR (BRA) Caldwell and Vitt
(1999)
A. andreae 18 NA Ants North of Manaus, AM
(BRA)
Sabagh et al. (2012)
A. andreae 12 NA Termites, blattidae Mineração, RO (BRA) Vitt and Caldwell
(1994)
A. hylaedactyla 19 NA Termites, larvae Mineração, RO (BRA) Vitt and Caldwell
(1994)
A. hylaedactyla 10 NA Termites, spiders Santana, AP (BRA) Sanches et al. (2019)
A. hylaedactyla 10 NA Ants, termites, beetles Plácido de Castro, AC
(BRA)
Almeida et al. (2019)
(Continued )
Diet of frogs in an ephemerous habitat 13
Table 3.
(Continued)
Taxa Prey categories
richness
Prey items per stomach
(Mean ± SD)
Most relevant dietary
items Locality Reference
A. marmorata 13 NA Isopods, ants Ilha Grande, RJ (BRA) Almeida-Gomes et al.
(2007)
A. marmorata 15 NA Ants, spiders, crickets Salto Morato, PR (BRA) Santos-Pereira et al.
(2015)
A. dyptix 17 NA Ants, beetles, springtail,
spiders
Northwest Argentina
(ARG)
Zaracho et al. (2012)
A. thomei 16 NA Ants, isopods, spiders,
beetles
Michelin Ecol. Reserve,
BA (BRA)
Rebouças and Solé
(2015)
We included only studies carried with closely related or similar-sized species and we use the original nomenclature. During the production of the present
manuscript, Pacheco and collaborators published a paper on diet and morphology of Ameerega berohoka and A. picta from preserved areas in Southwest
Brazil, showing that the diets of these species are largely dominated by ants (available at: https://doi.org/10.1080/01650521.2020.1746098).
14 R.A. Brandão et al.
The frogs of the genera Adenomera feed mainly on ants, beetles, termites, and insect
larvae (Duellman 1978; Caldwell & Vitt 1999; Parmelee 1999; Almeida-Gomes et al. 2007;
Rebouças & Solé 2015; Santos-Pereira et al. 2015). However, diets can vary depending on
locality. Isopods, for example, were important prey in the diet of A. thomei in the Atlantic
Forest in northeastern Brazil, and for A. marmorata intheAtlanticRainforestofthe
southeastern coast (Almeida-Gomes et al. 2007;Rebouças&Solé2015) but were not
ingested by A. marmorata in southern Brazil (Santos-Pereira et al. 2015)orbyAdenomera
species in the Amazon (Duellman 1978; Caldwell & Vitt 1999; Parmelee 1999). This
geographical differentiation in diet might explain the existence of different Adenomera
species in very different habitats, including in our studied area, where Adenomera sp.
principally ate ants, termites and beetles, and preferred mites and tricopterans.
Considering other Ameerega species occurring in the Cerrado, A. braccata pre-
sented higher prey richness than observed for A. berohoka (39.70 ± 46.60 items by
stomach, Forti et al. 2011), and ingested a larger number of ants, Acari, Coleoptera,
Isoptera, and Hymenoptera, with ants, termites, and beetles the most voluminous
ingested items. Ameerega flavopicta also ingested more preys (13.04 ± 17.51, Biavati
et al. 2004)thanA. berohoka, although the diet of A. flavopicta can vary according to
habitat. Comparing the diet of a pooled sample containing individuals from four
localities from the State of Goiás, Biavati et al. (2004) found ants, termites,
Coleoptera, and Acari as the most common ingested items, while termites, ants,
Blattaria (excluding Isoptera), Orthoptera, and Coleoptera were the most voluminous
preys. This similarity in diets of A. berohoka and A. flavopicta may reflect their close
relationship (Guillory et al. 2019). Conversely, Lima and Eterovick (2013)foundthat
small temporal differences on habitat use affected the species diet: at the shores of
a reservoir during the dry season it was composed mainly of Acari, Lepidoptera
larvae and spiders (in number) and by Acari, spiders, Lepidoptera larvae and
Coleoptera (in volume), while inside a close trench filled with water during the
rainy season, frogs ingested mainly Lepidoptera larvae and termites (for number
and volume), and ants were not a relevant prey item. The diet of A. picta in Serra
da Bodoquena National Park was composed of only five categories, being dominated
by ants, beetles, and Diptera (Landgref-Filho et al. 2019). Ameerega berohoka ingested
a larger number of small items as Diptera, Collembola, and Acari, while Coleoptera,
Diptera, termites, and ants were the most voluminous ingested items, but preferring
collembolans, tricopterans, Acari, and Diptera. Formicidae are relevant prey items
for different Ameerega species (Landgref-Filho et al. 2019), and the ingestion of ants
can be related to sequestration of alkaloids (Mebs et al. 2010), but ants were ingested
by A. berohoka in a smaller proportion than found in the environment, while
A. flavopicta prefered lepidoptera larvae in the study of Lima and Eterovick (2013).
Myrmecine ants are considered the main source of alkaloids for dendrobatids,
mantellids, and bufonids (Melanophryniscus) (Mebs et al. 2010; Moskowitz et al.
2018). Since Ameerega flavopicta [and probably all other Cerrado species in the
genus (see Darst et al. 2005; Mebs et al. 2010)] is not less toxic than other
Amazonian dendrobatids (Mortari et al. 2004), it is possible that Cerrado species are
capturing alkaloids from other exogenous sources, as termites, beetles, or mites
(Biavati et al. 2004; Mortari et al. 2004; Saporito et al. 2007a), including A. berohoka.
The diet of Rhinella ocellata was largely composed of ants (90%), suggesting
a more specialized diet when compared to Adenomera sp. or A. berohoka.Antswere
also the most relevant item for other related or similar-sized species (Isacch & Barg
2002; Santana & Juncá 2007; Maragno & Souza 2011). Although other species of
Diet of frogs in an ephemerous habitat 15
Rhinella in the Cerrado also ingest a large number of ants, their diets included more
prey types than R. ocellata, often feeding, along with ants, on Isoptera, Coleoptera,
and Acari (Moreira & Barreto 1996;Santana&Juncá2007; Batista et al. 2011;
Maragno & Souza 2011). Our result shows that the poorly known R. ocellata has
a very narrow diet at the site and future studies may clarify if this is also the case in
other localities. Similar specialization in ants was also reported for the related
species R. hoogmoedi in Atlantic Forest of northeastern Brazil (Castro-Santos 2016).
Previous studies have shown that some poisonous frogs and toads from the
genera Ameerega, Melanophryniscus, and Rhinella tend to consume ants and mites
(Toft 1980,1995; Caldwell 1996; Darst et al. 2005; Quiroga et al. 2011), arthropods
that are sources of alkaloids (Saporito et al. 2007a). Although Melanophryniscus toads
that feed only fruit flies in captivity lose their skin alkaloids (Hantak et al. 2013), we
are unaware of studies on skin secretion composition on species belonging to the
groups of R. margaritifera (+ R. ocellata) and R. granulosa, as well on circumstantial
exogenous sources of alkaloids for these species.
Alkaloids and other substances often found in dendrobatids and bufonids skin
secretion are obtained from the diet and are stored in skin glands (Saporito et al.
2007a;Hantaketal.2013). However, the consumption of these preys depends on
their density and distribution in the environment, and differences in ingestion rates
can occur throughout the year (Saporito et al. 2007b; Bull & Hayes 2009;Moskowitz
et al. 2018). Although Ameerega flavopicta ingested fewer ants than related species
occurring in the Amazon (Biavati et al. 2004; Lima & Eterovick 2013), ants were
relevant in the diet of other related species in the Cerrado biome (Forti et al. 2011;
Landgref-Filho et al. 2019;presentstudy).Interestingly,socialinsects,ingeneral,
are relevant prey even for Ameerega species occurring in the Amazon (Luiz et al.
2015), and diverse strategies of alkaloid capturing and evolution of skin toxicity are
expected to occur within different lineages in the Neotropics (see Darst et al. 2005),
including circumstantial sequestration from termites or other arthropods.
We suggest that ants play an important role in the evolution of diet in Rhinella
margaritifera (including R. ocellata) species group. Ants also dominated the diet of the
related species R. hoogmoedi in Atlantic Forest (Britto et al. 2013; Castro-Santos 2016)
and were the most relevant item in the diet of R. scitula in the Cerrado (Maragno &
Souza 2011). Ants seem to be relevant prey items for Rhinella toads in the Neotropics,
whereas Coleoptera probably get more relevance in large-sized species belonging to
the Rhinella marina species group (e.g. Sabagh & Carvalho-e-Silva 2008; Duré et al.
2009; Leite-Filho et al. 2015).
Our findings reject our initial prediction of low ingestion of ants and termites
along the Noidori riverbank. This finding could be the result of three possibilities: (i)
the frogs were foraging out of the riverbank and were posteriorly attracted to the
riverbank for humidity or reproduction, (ii) cursorial ants and termites were also
attracted to the riverbank by the humidity or another resource (such as litter), estab-
lishing ephemeral nests on the available dead logs, or (iii) phylogenetic constraints
affected prey selection, mainly for species that capture alkaloid precursors in their
diet.
The finding of soft-bodied insects (as Dermaptera) and water-related preys (as
Trichoptera) in stomachs suggests that frogs were foraging at the riverbank, and not
only in the drier habitats some meters away. We also directly observed Ameerega
berohoka preying on an ant during the diurnal sampling. Apparently, social insects
(ants and termites) were also attracted to the riverbank corresponding to 49% of
16 R.A. Brandão et al.
arthropods captured by pitfall traps. The abundance of ants and termites allows active
prey selection by Rhinella ocellata and Ameerega berohoka, whereas less abundant prey
was opportunistically added to their diet.
Frogs at the Noidori riverbank are ingesting less prey (abundance and richness)
than similar-sized or related species in the Cerrado and in other biomes (Table 3),
suggesting that prey is less available along the riverbank than in more stable and
perennial habitats. In this context, phylogenetic driven diets can constrain coloniza-
tion or individual fitness in simplified habitats, including circumstantial toxicity loss
(Moskowitz et al. 2018). Therefore, the colonization and use of resources in
a simplified and ephemeral system seem to be associated with the ability of these
frogs to use the different prey that are available in the different habitats or by the
abundance of social insects even in ephemeral tropical environments.
As previously hypothesized, the simplified and ephemeral habitat represented by
the Noidori riverbank affected frogs’diets through the low richness of the prey com-
munities. These habitats can affect the foraging behaviour of frogs, which, in turn,
may affect individual fitness, especially for species that depend on diet for defence.
Despite the phenology of some insect Orders, insect abundance and diversity in
Cerrado is not affected by seasonality (Pinheiro et al. 2002), and the poorer availability
of prey along the riverbank reflects habitat simplicity.
Summarizing, these frogs seem to have been attracted to the riverbank due to the
humidity, where they use the available prey, including cursorial ants and termites. As
expected, the composition of amphibian communities in ephemeral seasonal environ-
ments seems to be more related to the capacity of displacement and colonization by
opportunistic species than to the sharing of resources in a competitive perspective.
ACKNOWLEDGEMENTS
We thank Adrian Garda, Diego Santana, Mirco Solé, and two anonymous reviewers for
relevant commentaries on previous versions of the manuscript. Jos Barlow improved our language
use. To Gabriel Horta and Dhego Ramon for help during fieldwork. To Guarino Colli and Eddie
Lenza for the opportunity to work at Noidori river, under PPBIO and SISBIOTA program. To
Instituto Chico Mendes de Conservação da Biodiversidade for providing research permits (28190-1).
DISCLOSURE STATEMENT
No potential conflict of interest was reported by the authors.
ORCID
Reuber A. Brandão http://orcid.org/0000-0003-3940-2544
Jéssica Fenker http://orcid.org/0000-0002-7430-3886
Bruno E. Pires de Carmago Lopes http://orcid.org/0000-0001-8549-457X
Vitor M. de Alcantara de Sena http://orcid.org/0000-0002-5478-8193
Beatriz D. Vasconcelos http://orcid.org/0000-0003-0101-8969
Diet of frogs in an ephemerous habitat 17
ETHICAL STANDARD
This study was approved by Instituto Chico Mendes de Conservação da Biodiversidade
(Research permits: 28190-1) and is in accordance with Brazilian laws on the ethical use of
animals for research purposes, as stated by Conselho Nacional de Controle de Experimentação
Animal. All specimens were carefully euthanized avoiding stress, pain or suffering, posteriorly
fixed using standard protocols, and housed in Coleção Herpetológica da Universidade de Brasília
for further studies on genetics, evolution, reproduction, and taxonomy.
AUTHOR CONTRIBUTION
R.A. Brandão designed the experiment, collected data in the field, analyzed data, and wrote
the manuscript; J. Fenker collected data in the field and wrote the manuscript; B. Lopes analyzed
data and wrote the manuscript; V. Sena analyzed data and wrote the manuscript; B.D.
Vasconcelos performed data analysis and wrote the manuscript.
SUPPLEMENTAL DATA
Supplemental data for this paper can be accessed on the https://doi.org/10.1080/03949370.
2020.1755373.
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