Herpetological Conservation and Biology 10(3):819–832.

Submitted: 30 January 2014; Accepted: 6 October 2015; Published: 16 December 2015.

AMPHIBIAN TROPHIC ECOLOGY IN INCREASINGLY

HUMAN-ALTERED WETLANDS

JAVIER ALEJANDRO LÓPEZ1,2,3, PABLO AUGUSTO SCARABOTTI1,2, AND ROMINA GHIRARDI1

1
Instituto Nacional de Limnología (CONICET-UNL). Ciudad Universitaria, Paraje El Pozo S/N, (3000) Santa Fe, Argentina
2
Departamento de Ciencias Naturales, Facultad de Humanidades y Ciencias (FHUC), Universidad
Nacional del Litoral (UNL), Paraje El Pozo S/N, (3000) Santa Fe, Argentina
3
Corresponding author, email: [email protected]

Abstract.―Habitat destruction and alteration are among the major causes of worldwide amphibian declines. Resource
limitation in altered environments can potentially affect trophic ecology of amphibians and contribute to decline. In this
work, we analyzed changes in resource availability and use, and the population abundance of eight amphibian species
from six wetlands that differ in type and degree of human disturbance. Food resource availability varied among sites and
the occurrence of some arthropods was correlated with type of disturbance regime. Diet evenness, richness, and niche
breadth were similar among sites or months. Nevertheless, diet composition showed significant variation among samples
for all species. Diet composition changes among populations were correlated with resource availability in four species
(Lysapsus limellum, Dendropsophus nanus, Hypsiboas pulchellus and H. punctatus), but not in the remaining species (D.
sanborni, H. raniceps, Scinax nasicus and S. squalirostris). These results suggest that species that are able to adjust their
diets according to prey availability may have an adaptive advantage in changing environments associated with
anthropogenic disturbances. Given the increasing rate of alteration of wetlands by urbanization, agriculture, and
livestock grazing, understanding trophic processes in these habitats is important for preserving the great biodiversity
living in these habitats.

Key Words.—flood plain ponds; habitat alteration; Hylidae; prey availability; trophic plasticity

INTRODUCTION sites (Petranka et al. 1993; Lemckert 1999; Vaira 2002).

Grazing and grassland burning for livestock alters plant
Amphibian populations are experiencing serious communities and thereby potentially damages breeding,
declines around the world, driven principally by direct feeding, and refuge habitats and can reduce amphibian
and indirect effects of habitat destruction and alteration diversity (Vaira 2002; Jansen and Healey 2003; Cano
(Alford and Richards 1999; Eskew et al. 2012). and Leynaud 2010). Habitat modification affects
Amphibian communities from the large Neotropical amphibians indirectly by reducing energy reserves and
wetlands are not exempt from the effects of energy allocated to growth and reproduction, and by
fragmentation and habitat alteration (Peltzer et al. 2003). affecting population dynamics and viability (Gray and
Sensitivity to habitat modification is species-specific, but Smith 2005; Brodeur et al. 2011). Brodeur et al. (2011)
for most species we lack information about how life- hypothesized that the body condition of frogs is reduced
history characteristics and habitat use may affect in human modified habitats because of decreased prey
population fluctuations and vulnerability to abundance, but the effect of human modifications on
environmental changes (McKinney 2002; Green 2003; amphibian feeding ecology has not been well studied
Ficetola and De Bernardi 2004). Although ecological (Kovács and Török 1995).
mechanisms of population decline are not clear, habitat Diets of amphibian vary seasonally and spatially in
modification is known to affect amphibian abundance, relation to the environment where they dwell (Maneyro
richness, and assemblage composition (Jansen and and Da Rosa 2004; Menin et al. 2005; Falico et al.
Healey 2003; Smallbone et al. 2011; Eskew et al. 2012). 2012b). Disturbance of ecosystems can affect not only
Habitat alteration can impact amphibian populations amphibians but also their arthropod prey, affecting
both directly and indirectly (Blaustein et al. 2010). resource uptake (Trueba et al. 1999; Prinzing et al. 2007;
Although destruction of breeding habitat may lead to Battles et al. 2013). Data on food resource availability
extirpation (Vaira 2003), deterioration of freshwater are essential to understand frog trophic ecology (Hirai
systems by urban wastes (Ficetola et al. 2011) and river and Matsui 2001; Hirai 2002; López et al. 2009), and a
flow-regulation by dams negatively affects amphibian relationship between diet composition and prey
diversity and abundance by reducing area of riparian availability has been demonstrated (Maneyro and Da
wetlands used for breeding (Eskew et al. 2012). Rosa 2004; López et al. 2009). Prey availability is
Selective logging also deteriorates refuge and breeding difficult to measure (Macale et al. 2008) and, therefore,

Copyright © 2015. Javier A. López 819

All Rights Reserved.
López et al.—Frog trophic ecology.

availability. We predict that prey composition will shift

along the anthropogenic habitat alteration gradient
studied, and that trophic plasticity (i.e., the capability to
shift diet in relation to prey availability) will differ
among amphibian species.

MATERIALS AND METHODS

Study area and site classification.—The Middle

Paraná River floodplain is a complex system of islands
with alluvial forests, wetlands, secondary rivers,
streams, and lagoons that covers 20,000 km2 of north-
eastern Argentina (Drago et al. 2003). This diversity of
landforms provides a large variety of terrestrial and
aquatic habitats for amphibians. The Paraná River has
flood pulses in which water elevations are approximately
2–3 m above mean levels with inter-annual variation in
flood magnitude. During high water periods, the river
connects with adjacent floodplain wetlands and a wide
exchange of organisms and nutrients occurs (Iriondo et
al. 2007). In this region, climate is damp and
mesothermal. The warmer months are November to
March, with a mean annual temperature of 18.4° C
(Peretti 1996). Annual precipitation is about 1,000 mm
and occurs mainly from October to April (Peretti 1996).
The banks of the Middle and Lower Paraná River
sustain the largest human habitation of the country, with
important harbors and industrial activities. In these
FIGURE 1. Study area in the alluvial valley of Paraná River (31º 40’
regions, development of infrastructure, advancement of
S, 60º 40’ W). Sites are at Sirgadero Island (S1, S2, S4, S5, S6) and farming and ranching, and increasing contamination can
the Natural Reserve of Universidad Nacional del Litoral (S3). be observed (Hamilton 1999; Lavilla 2002; López et al.
Symbols: dotted zones, urbanized areas (Santa Fe City urban or 2005a). Human activities such as alteration of water
suburban areas); white zones, high ground areas only inundated
during extraordinary floods; gray zones, low lands flooded
courses, hydraulic works, construction of reservoirs,
periodically or every few years; dark gray zones, permanent water drainage and refilling of wetlands, inadequate
bodies. management and overexploitation of resources, and
destruction of vegetation in the basin are transforming
rarely included in anuran dietary studies (Toft 1980). wetlands adjacent to the Paraná River into a mosaic of
Thus, the evaluation of resource availability is of central environments with different degrees of modification and
importance to understand the mechanisms through which fragmentation (Bonetto 1994; Neiff 1999; Peltzer et al.
habitat alteration affects amphibian trophic ecology. 2003). Many of these habitat changes have local
When anthropogenic disturbance of habitat leads to impacts, thus altered and pristine habitats exist in a
variation in composition and abundance of resources, the matrix within relatively small areas. Given that
ability to adjust diet to the more available resources may amphibian assemblages respond mainly to microhabitat
improve energy uptake and fitness, preventing characteristics and processes (Richter-Boix et al. 2007),
population decline (Gray and Smith 2005; Williams et this wetland system allows us to test the effect of local
al. 2006; Falico et al. 2012b). Highly specialized species habitat alterations on amphibian trophic ecology.
or those with specific and fixed trophic requirements We sampled six sites with different types and degrees
would have greater difficulties coping with of anthropogenic alteration in the alluvial valley of
environmental alterations that lead to changes in prey Middle Paraná River near the city of Santa Fe (Santa Fe
availability (Anderson et al. 1999; Williams et al. 2006). Province, Argentina). Five of the sites were on
The ability to adjust diet to resource availability has been Sirgadero Island (S1, S2, S4, S5, S6), and one site was in
referred to as trophic plasticity and is usually overlooked the Natural Reserve of Universidad Nacional del Litoral
in trophic studies (DeWitt and Scheiner 2004; Guedes et (S3; Fig. 1). Sampling sites were in a unique
al. 2009). Here we test the hypothesis that amphibians environmental unit (Crevasse Splays and Levees of the
shift their diet across increasingly human-disturbed Santa Fe and Coronda river channels; Marchetti et al.
wetlands as a function of changes in trophic resource 2013) and were < 8 km apart. The close proximity of the

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sites ensured similarity of climatic conditions and alteration factors in two dimensions and use them in
assemblage of species able to colonize the sampling subsequent analysis as independent descriptors of habitat
sites. alteration. Analyses were performed in CANOCO
To evaluate human impact on the study area, we statistical package (Version 5).
defined six distinct categories of habitat alteration: (1)
fire in marginal vegetation is associated with cattle Sampling.—We sampled monthly at each of six sites
grazing, but frequency and extent vary among sites from the end of spring to the beginning of autumn
independent of stocking density; (2) hydraulic alteration (November 2004 to April 2005), equaling 36 samples,
by construction of artificial channels, dams, fence when feeding activity was concentrated (López et al.
slopes, and sand filling of swamps modifies flood pulses, 2011). We hand-captured eight species from the family
draining of rainwater, connections between lotic and Hylidae (Dendropsophus nanus: n = 658; D. sanborni: n
lentic habitats, water quality, and arthropod = 86; Hypsiboas pulchellus: n = 97; H. punctatus: n =
assemblages; (3) presence of livestock (i.e., cattle, 208; H. raniceps: n = 31; Lysapsus limellum: n = 581;
horses, and pigs) in the extensively farmed wetlands de- Scinax nasicus: n = 77; S. squalirostris: n = 48) that
vegetate the fixed routes between pens and grazing forage in riparian vegetation greatly affected by habitat
areas; (4) other vegetation alterations eliminate weeds alterations. We sampled all sites within a week during
adjacent to roads, houses and electrical lines, clear each month. We used a flashlight to search
natural forest, remove straw for roof thatch, etc., and microhabitats where frogs forage (rooted and floating
modify natural vegetation structure; (5) fragmentation macrophytes growing up to 1 m of water depth, about 2
impedes terrestrial animal dispersal and isolates ponds m offshore, and the periodically flooded zone beside
(e.g., the highway through a floodplain valley that water bodies, about 2 m onshore) through a transect
connects Santa Fe City with Paraná City and the large approximately 500 m long and 4 m wide.
sand filled areas for construction and other We standardized sampling effort by search time (the
infrastructure); and (6) deposition and accumulation of first two hours after sunset), duration, and transect area;
construction debris and urban solid waste alter habitat thus, species abundances were comparable among
structure and, as a result of the lack of control in waste samples (Heyer et al. 1994; Marsh and Pearman 1997).
composition, contaminate water bodies with a wide We sacrificed frogs in situ by immersing the animals in a
spectrum of chemicals. We scored the impact level in buffered anesthetic solution of benzocaine (Heyer et al.
the aquatic buffer zone (about 60 m from pond shore; 1994; European Commission 1997; Chen and Combs
see Semlitsch and Bodie 2003) on a scale from 0 to 3 for 1999). We did not perform stomach flushing because
each of the six alteration types; 0 = no alteration to 3 = selected species were too small and fragile (Macale et al.
maximum impact (modified from Peltzer et al. 2003). 2008) and we needed to obtain the entire digestive tract
We did not classify sites with respect to the total amount including the intestine to avoid overestimating larger
of habitat alteration a priori because we lacked prey (Peltzer et al. 2000; López et al. 2007; Macale et al.
information about the relative impact that each alteration 2008). This is especially important because the
type could have on amphibians to weight its effect. We abundant prey (in guts of frogs and in the environment)
used the impact scores as different independent variables were small (e.g., mites, collembolans). Within the
describing habitat alteration. To characterize variation studied assemblage, there were no threatened species
from habitat alteration factors and avoid (Vaira et al. 2012); population size and recruitment rate
multicollinearity, we used a nonmetric multidimensional were large enough (López et al. 2011) to assume that our
scaling analysis (NMDS; Faith et al. 1987). This method sampling exerted minimal effects even at the local
does not require linear relationships among variables and population level. Collected animals have been used for
can often summarize more information in fewer axes other studies (López et al. 2007, 2009, 2011; Antoniazzi
than other techniques (Manly 1986). NMDS compiles et al. 2013, 2014) and sampled populations have been
information from a distance matrix in a predetermined monitored subsequently. We did not observe any sign of
number of axes (called dimensions) and uses an index declining populations with the exception of those at the
called Stress to measure the extent to which derived two most altered sites (S6 and S5) where habitat has
distances differ from the original distances. As a been totally destroyed by a landfill.
distance measure we used Gower similarity coefficient Following the techniques described elsewhere (Hirai
(Gower 1971) because it considers combined absences and Matsui 2001; López et al. 2009), we estimated prey
(of alterations in our case) as informative (Moreno availability by sweep-netting with an entomological net
2001). We expected that two sites lacking a particular (handle length: 200 cm; hoop diameter: 40 cm; bag
type of alteration should be environmentally more depth: 80 cm; mesh size: 0.1 mm) in microhabitats
similar because absence of alteration would indicate where amphibians were captured. We made sweep-net
favorable conditions for amphibians and arthropods. samples simultaneously with amphibian captures, always
This method allowed us to express the multiple habitat by the same person, walking at the same speed and

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López et al.—Frog trophic ecology.

carried out in two 7-min zigzag transects (150m × 3 m), (equiprobable resource state). We used EcoSim
describing a 180° arc, parallel to the ground-water randomization algorithm 3 (RA3) because it retains the
surface, striking the top of rooted and floating niche breadth of each species (we did not find niche
macrophytes canopy with net ring. We combined data breadth variation among samples within a species; see
from both transects for the analysis (López et al. 2009). results), but randomizes which particular resource states
are used. It corresponds to a simple reshuffling of each
Environmental alteration, assemblage composition, row of the matrix (zero states reshuffled). We chose this
and resource availability.—We used multivariate option because we analyzed overlap among populations
ordination techniques to analyze the relationships among of each species, thus frogs of the same species should be
amphibian and prey assemblage structure and able to eat every prey item foraged in other populations.
environmental alterations. We used the matrix of Gotelli and Enstminger (2004) recommended using RA3
species composition at the different sites as dependent when the goal is to retain the amount of specialization,
variables and scores of NMDS as explanatory variables. but allow a species to potentially use other resource
From the matrix of prey taxa availability, we excluded states. Winemiller and Pianka (1990) have shown that
those taxa that represented < 10% of the total abundance. RA3 has good statistical properties for detecting non-
To select the appropriate ordination method (unimodal random niche overlap patterns and found that RA3 was
or linear), we carried out a Detrended Canonical usually superior to RA4 for this purpose. Vignoli and
Correspondence Analysis (DCCA) to obtain the length Luiselli (2012) suggested that RA2 performed much
of the gradient, an index that informs about the degree of better than RA3 at revealing community structure, but in
species turnover among samples (Legendre and our case RA3 successfully detected the diet structure of
Gallagher 2001; Lepš and Šmilauer 2003). Following frogs in six out of eight species and in environmental
the suggestion of Lepš and Šmilauer (2003) that prey availability; while RA2 detected diet structure in
maximum gradient lengths < 4 indicate linearity, we five frog species and food resources.
selected the linear method of Redundancy Analysis Finally, to study trophic plasticity among the
(RDA; amphibian assemblage maximum gradient length amphibians, we evaluated the correlation between the
= 0.919, prey assemblage maximum = 0.489). We variation of prey availability and the diet of the frog with
evaluated significance of canonical axes with Monte a Mantel test (Mantel 1967) in the software XLSTAT
Carlo tests (499 permutations). These analyses were (Version 7.5.3). Mantel test is a permutation method
performed in CANOCO statistical package (Version 5). that calculates a Pearson correlation coefficient between
two proximity matrices (similarity or dissimilarity) and
Trophic analysis.—To avoid underestimation of prey gives a P value on the null hypothesis of lack of
consumption, we included both stomach and intestine correlation. Euclidean distance dissimilarity matrixes
contents in diet analysis (Peltzer et al. 2000; López et al. (average linkage aggregation criteria) were built for diet
2007). We identified prey to the lowest possible taxon of each anuran species between sites and months
(generally Family). For each amphibian species, we (samples), which were correlated to analogue matrices
estimated diet evenness (Pielou 1966), richness, niche built based on prey availability. Due to the seasonal
breadth (Levins 1968), and mean number of prey per gut patterns of occurrence of amphibian species of the
at each site and sampled month. We compared these assemblage (López et al. 2011), we did not collect every
parameters among sites and months using Kruskal- species in all samples (month/site). We built matrices
Wallis tests followed by multicomparison Dunn tests for each species including those samples for which at
with GraphPad InStat software (Version 3.06; Table 3). least one individual was captured. For each anuran
We calculated niche breadths of species (Levins 1968) species, we used only prey availability data of samples
by summing the specimens from every site and month. for which diet data were available. As in other works,
We evaluated the similarity of frog diets (relative the diet of frogs usually included a few dominant prey
abundance of prey items) and prey availability items and many rare taxa (López et al. 2005b; Falico et
composition among months and sites using Pianka al. 2012b). Consequently, to prevent the inclusion of
(1973) niche overlap index (Ojk). To determine whether taxa with negligible weights in the analysis, we excluded
measured overlap values differed from those expected by prey items representing < 10% of relative abundance
chance, we performed a randomization analysis with either in the diet or in trophic resource availability
EcoSim software (Version 7). EcoSim performs Monte samples. For all statistical analysis we used an alpha
Carlo randomizations to create Pseudo-communities and level of 0.05.
then compares the patterns in these randomized
communities with those in the observed data matrix. In RESULTS
this analysis, the values of the original matrix were
randomized 1000 times. We assumed different resource Amphibian and prey assemblages.—NMDS
states to be equally abundant in the environment successfully summarized the information of the six types

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TABLE 1. Correlation coefficients between nonmetric

multidimensional scaling (NMDS) analysis axes and semiquantitative
variables of anthropogenic environmental alteration (AEA).
Abbreviations of types of anthropogenic environmental alteration are
Fire: burning of marginal vegetation; Hydraul.alter.: modification of
natural hydrology in relation to flood pulse and draining of rainwater
by construction of artificial channels or dams; Livestock: presence of
cattle, horses, and pigs; Veg.alter.: vegetation alterations due to weed
elimination or logging; Fragm.: habitat fragmentation by roads, dams
or fence slopes; and Landfill: deposition and accumulation of
construction debris and solid urban wastes.

NMDS1 NMDS2
AEA Types (Livestock & Landfill) (Damming)

Fire 0.9735 ˗0.1452

Hydraul.alter. 0.11 0.9272

FIGURE 2. Plot of Nonmetric multidimensional scaling analysis
(NMDS) based on Gower dissimilarity index of the environmental
Livestock 0.6981 ˗0.5112 alterations. NMDS procedure computed configuration in 25
iterations, with stress value 0.00043542. Abbreviations: fire, burning
Veg.alter. 0.9102 ˗0.1343 of marginal vegetation; hydraul.alter., modification of natural
hydrology in relation to flood pulse and draining of rainwater by
construction of artificial channels or dams; livestock, presence of
Fragm. 0.4046 0.8698 cattle, horses, and pigs; veg.alter., vegetation alterations due to weed
elimination or logging; fragm., habitat fragmentation by roads, dams
Landfill 0.7889 ˗0.1018 or fence slopes; landfill, deposition and accumulation of construction
debris and solid urban wastes.

negatively related to Livestock and Landfill.

of alteration in two axes (stress value = 0.00043542). Assemblages of sites S1, S2 and S4 (grouped at the
The first NMDS axis was related to livestock presence bottom of triplot) were characterized by greater
and landfill activities and summarizes information from abundance of Hypsiboas species, which were related to
four of the analyzed environmental alterations (named lower alteration levels. In particular, H. punctatus and H.
hereafter Livestock & Landfill). The second NMDS axis raniceps showed increased abundances in sites with low
was related to modifications of natural hydrology of the alteration impacts.
water bodies and habitat fragmentation (named hereafter We identified 105 taxa (mainly at the level of Family)
Damming; Table 1; Fig. 2). Sites were distributed along from the net-sampled prey. Most of the prey belonged to
the gradient of environmental alterations defined by Insecta (90.74%) and Arachnida (9.05%). Prey
NMDS axes. Site S6 was the most disturbed habitat composition changed along the habitat alteration
showing high scores for the axes named Damming and gradient (Fig. 3b). RDA showed differentiation among
Livestock & Landfill. Site S5 was also highly disturbed sites according to environmental alteration (Monte Carlo
and exhibited large values of Livestock & Landfill. test of significance of canonical axes: pseudo-F = 2.4; P
Sites S2, S3 and S4 were moderately disturbed; S3 was = 0.004). The most altered sites showed greater
associated with Damming; and S2 and S4 with Livestock abundances of Hemiptera, Orthoptera, Coleoptera and
& Landfill. Finally, S1 was the least altered site, with Acari. Some flying prey, such as Diptera and
low values on both axes (Fig. 2). Hemiptera, had high relative abundances and were
Although most species occurred at every site, RDA evenly distributed among the six sampled sites (Table 2).
showed that amphibian assemblage structure varied in The most abundant arthropods available were two
association with the type of alteration (Monte Carlo test families of dipterans, Chironomidae and Culicidae.
of significance of canonical axes: pseudo-F = 2.5, P = Chironomids exceeded 10% of available prey in all sites
0.002; Fig. 3a). Dendropsophus nanus and Lysapsus and were particularly abundant in S3. In contrast,
limellum were abundant in every site (their abundance culicids exceeded 10% of available prey in the three
ranging from 28% to 46% and 13% to 45% of all least altered sites. Muscidae (Diptera) were also
captures, respectively). Dendropsophus species showed abundant, but their abundance was more related to
their greatest abundances in the most altered sites, S5 livestock presence and landfill. Formicidae were
and S6 (grouped at the top of the triplot). Site S3, abundant in sites with alterations of natural hydraulic
associated with higher levels of damming, presented an regime (Damming). Entognatha (springtails and related
assemblage composed largely of D. nanus and Scinax taxa principally in the family Sminthuridae) were
species. Abundance of frogs in the genus Scinax was abundant in S1, a site with slight alteration (Table 2).

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López et al.—Frog trophic ecology.

FIGURE 3. Redundancy analysis triplots using: (a) amphibian assemblage composition and habitat alteration gradient (centered and standardized
by species; abundances ln (x+1) transformed and applying Hellinger standardization; eigenvalue axes 1 = 0.0859, 2 = 0.0473; species-
environment pseudo-canonical correlations axes 1 = 0.6367, 2 = 0.5138; explanatory variables account for 13.3% of total variation; cumulative
explained fitted variation axes 1 = 64.5%, 2 = 100%; Monte Carlo test of significance of canonical axes -499 unrestricted permutations-: pseudo-
F = 2.5; P = 0.002); and (b) using more important arthropod orders of the trophic resources availability (items with more than 10% of relative
abundance in any of the sites) and habitat alterations gradient (proportions of total abundance Arcsin transformed and applying Hellinger
standardization; eigenvalues axes 1 = 0.0989, 2 = 0.0277; species-environment pseudo-canonical correlations axes 1 = 0.7299, 2 = 0.4924;
explanatory variables account for 12.7% of total variation; cumulative explained fitted variation axes 1 = 78.11%, 2 = 100%; Monte Carlo test of
significance of canonical axes -499 unrestricted permutations-: pseudo-F = 2.4; P = 0.004).

Trophic analysis.—Diet evenness, richness, and niche nanus = 10.16, D. sanborni = 6.19, H. pulchellus = 25,
breadth did not vary significantly among sites or months H. punctatus =38.58, H. raniceps = 4.87, L. limellum =
(Table 3). There was seasonal variation in the number of 10.53, S. nasicus = 7.07 and S. squalirostris = 9.64.
prey consumed by D. nanus and H. punctatus, although Overlap among samples (month/site) was modest to
no significant differences were found among any pair of low for the diet of eight species and prey availability
months (Dunn test: P > 0.05 in all cases). For L. (Table 4). Except for H. pulchellus and S. nasicus,
limellum, multicomparison Dunn tests showed observed overlap was higher than expected by chance
significant differences in mean number of prey per gut (Table 4). For species except D. nanus, diet overlap
between S4 and S1 (ranks mean difference = 15.5; P < among samples was lower than available prey overlap
0.05) and between S4 and S6 (ranks mean difference = among samples (Table 4).
16.35; P < 0.05). Niche breadth by species was: D.

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TABLE 2. Relative abundance (percentages) of food resource taxa at six study sites, showing values for invertebrate groups that exceed 5%.
Mites were identified at Subclass level, Acari.

Class, Order, Family S1 S2 S3 S4 S5 S6

Entognatha
Entomobryomorpha 4.86 1.37 5.99 3.15 2.52 11.73
Entomobryidae 4.86 1.37 5.99 3.15 2.52 11.73
Poduromorpha - - 0.3 - - -
Symphypleona 16.44 6.86 0.63 4.4 4.53 0.38
Sminthuridae 16.44 6.86 0.63 4.4 4.53 0.38
Insecta
Blattaria 0.02 0.31 0.02 0.27 0.28 0.11
Coleoptera 1.93 5.42 1.49 10 11.59 3.22
Coleoptera larvae 0.16 0.49 0.08 0.80 7.48 0.09
Dermaptera 0.004 - - - - -
Diptera 44.12 43.09 50.91 43.75 32.44 34.17
Chironomidae 11.00 12.71 29.31 12.19 10.89 11.09
Chloropidae 1.90 0.45 0.47 1.23 1.48 6.45
Culicidae 14.94 11.05 13.78 5.96 7.87 6.90
Dolichopodidae 3.69 5.75 0.63 4.88 3.51 2.13
Muscidae 9.29 8.75 2.49 14.52 5.40 4.20
Hemiptera 13.35 17.74 13.24 11.99 12.81 24.89
Cercopidae 2.60 1.72 3.05 1.08 1.94 10.92
Cicadellidae 6.98 8.23 1.47 4.40 5.00 8.81
Hymenoptera 2.65 2.69 11.42 3.91 2 2.34
Formicidae 1.80 1.47 10.92 3.33 1.61 1.69
Lepidoptera 0.07 0.26 0.85 0.19 0.1 0.34
Mantodea 0.01 0.17 0.03 0.01 0.07 -
Neuroptera 0.02 0.01 0.27 - - 0.02
Odonata 3.32 2.85 1.26 0.87 1.19 2.97
Orthoptera 1.45 8.69 0.71 3.89 13.24 8.89
Tettigonidae 0.98 5.29 0.34 1.96 11.94 5.22
Thysanoptera 5.54 0.51 4.16 0.88 5.71 2.67
Phlaeotripidae 4.40 0.25 2.70 0.43 5.07 2.05
Trichoptera 0.13 0.23 0.08 0.13 - 0.05
Indeterminate larvae 0.51 0.2 0.29 1.59 0.99 0.07
Arachnida
Acari 3.41 6.30 2.14 10.51 6.82 4.34
Araneae 1.99 2.81 6.21 4.34 3.22 3.74
Malacostraca
Isopoda - - - 0.08 - -
Gastropoda
Pulmonata 0.18 0.51 - 0.04 2.49 0.07

There was significant co-variation between diet and

environments (Guedes et al. 2009). Herein, the response
prey availability for D. nanus, H. pulchellus, H. to spatial-temporal changes in trophic resources differed
punctatus, and L. limellum (Table 4). Thus, samplesamong analyzed anuran species. Responses were not
(site/months) with greater similarity in environmental
phylogenetically structured, as closely related species
prey composition also were the samples with greater diet
(e.g. Dendropsophus nanus and D. sanborni; Faivovich
similarity for these four species. The co-variationet al. 2005) significantly differed in their feeding
between diet and prey availability was non-significant
plasticity. Indeed, species considered to be more plastic
for the remaining species. belonged to three different genera (Dendropsophus;
Hypsiboas and Lysapsus), two of which had members
DISCUSSION considered to be among the less plastic group of species
(Dendropsophus and Hypsiboas).
Feeding plasticity contributes to the adaptive Although most species occurred at every studied site,
evolution of populations exposed to new or altered species relative abundances varied in association with

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López et al.—Frog trophic ecology.

TABLE 3. Comparison of evenness (E), richness (R), niche breadth (Nb) and mean number of prey per gut (n) for diet of amphibians among study
sites and sampled months with outcomes (H) of Kruskal-Wallis tests. An asterisk (*) indicates statistical significance at P < 0.05.
Species Variable E R Nb n

Dendropsophus nanus sites H 2.031 5.686 5.596 2.883

P 0.845 0.338 0.348 0.718
months H 9.128 8.682 4.05 14.19
P 0.104 0.122 0.542 0.014*
Dendropsophus sanborni sites H 5.241 8.671 4.635 5.29
P 0.387 0.123 0.462 0.382
months H 5.693 9.327 9.351 6.184
P 0.337 0.097 0.095 0.289
Hypsiboas pulchellus sites H 0.894 6.609 5.911 4.58
P 0.925 0.158 0.206 0.333
months H 5.084 9.044 9.27 2.387
P 0.279 0.06 0.055 0.665
Hypsiboas punctatus sites H 3.218 8.148 5.558 4.181
P 0.522 0.086 0.235 0.382
months H 7.446 1.254 1.696 9.845
P 0.114 0.869 0.791 0.043*
Hypsiboas raniceps sites H 6.737 2.032 1.735 6.67
P 0.241 0.804 0.884 0.245
months H 2.235 6.051 6.881 7.201
P 0.816 0.301 0.23 0.206
Scinax nasicus sites H 3.101 5.578 3.881 3.467
P 0.541 0.233 0.432 0.483
months H 6.253 3.892 8.272 5.1
P 0.282 0.565 0.142 0.404
Scinax squalirostris sites H 7.209 3.86 5.094 2.393
P 0.206 0.57 0.405 0.793
months H 5.474 0.644 1.494 5.488
P 0.361 0.986 0.914 0.359
Lysapsus limellum sites H 12.48 12.72 6.939 15.245
P 0.29 0.26 0.225 0.009*
months H 6.604 6.162 9.306 3.502
P 0.252 0.291 0.097 0.623

type of alteration. Dendropsophus species seem to be habitat disturbance gradients (Basset et al. 2008),
less affected by analyzed alterations. Lysapsus limellum,although these changes do not necessarily imply an
although abundant at every site, was more common in overall reduction of diversity (Battles et al. 2013). Non-
the less altered environments. Scinax species were less flying arthropods such as spiders and ants could be
abundant in environments heavily affected by livestock negatively affected by floods when nests and
and landfill, while Hypsiboas species were associated subterranean refuges are inundated (Prinzing et al.
with a low degree of habitat alteration. Differences in 2007). Thus, dam construction can favor the occurrence
amphibian assemblages among sites could not solely be of more terrestrial taxa. Dragonflies also may be
attributed to trophic resource dissimilarities, despite the
favored by the fragmentation of large permanent lakes
expectation that changes in prey availability due to local
into smaller semipermanent ponds because of reduced
habitat characteristics certainly contribute to structurefish predation on eggs and aquatic larvae (Welborn et al.
amphibian assemblages. 1996). Xerothermophilic coleopterans, orthopterans,
and mites may have been favored by riparian vegetation
Shifts in prey composition.—As predicted, prey alterations produced by livestock and landfill (Lambeets
composition changed with habitat alteration of wetlands. et al. 2009). Collembolans are sensitive to changes in
The structure of arthropod assemblages changes across leaf litter humidity, plant cover, fire, and other habitat

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TABLE 4. Diet overlap and trophic plasticity of eight hylid frog species. Pianka’s (1973) niche overlap index (O jk) depicts similarity of relative
abundance of prey among samples (months and sites). Statistical significance (P) of measured overlap values among samples (Ojk obs) indicates
difference from what would be expected by chance (Ojk exp). Prey with < 10% relative abundance were excluded from the analysis. For trophic
plasticity, Mantel tests indicate the Pearson correlation coefficients (r) of dissimilarity matrices (Euclidean distance, average linkage aggregation
criteria) of the diet of frogs and environmental prey composition. The genus Dendropsophus abbreviated Dendro.

Diet overlap Dendro. Dendro. Hypsiboas Hypsiboas Hypsiboas Scinax Scinax Lysapsus
and plasticity nanus sanborni pulchellus punctatus raniceps nasicus squalirostris limellum prey
Ojk obs 0.484 0.422 0.166 0.296 0.279 0.184 0.321 0.346 0.465
Ojk exp 0.239 0.165 0.145 0.16 0.176 0.189 0.146 0.196 0.292
P(obs ≤ exp) 1 1 0.877 1 0.999 0.473 1 1 1
P(obs ≥ exp) < 0.001 < 0.001 0.123 < 0.001 0.001 0.527 < 0.001 < 0.001 < 0.001
r 0.293 ˗0.060 0.309 0.229 0.279 ˗0.249 0.195 0.164
P 0.023 0.299 0.021 0.047 0.074 0.051 0.158 0.008

perturbations (Trueba et al. 1999). Their abundance populations is driven principally by a turnover in
(mainly Sminthurids) in the study area decreased with taxonomic composition of prey taxa. According to other
increasing site perturbation (cattle overgrazing, fire, and studies (Menin et al. 2005; López et al. 2007; Falico et
bulldozing). The alteration in riparian areas can lead to al. 2012b), taxonomic identity of principal prey items
significant changes in aquatic and semi-aquatic changes among populations, probably as a result of local
hemipterans composition even though species richness prey availability, while the number (and their
may not be affected and some families may increase ecomorphological characteristics) of primary versus
their abundance under intermediate habitat disturbances accessory prey remains relatively stable.
(Dias-Silva et al. 2010; Bianchi et al. 2014). It has been proposed that the decrease or absence of
The dispersal ability of flying insects (e.g. dipterans some prey resources may negatively affect amphibians
and hemipterans) and their capacity to recolonize sites or cause the decline of entire populations (Blaustein and
after the periodical floods (Montalto and Paggi 2006) Wake 1995), but generalist species should be less
might explain their abundance in all sampled sites, susceptible to fluctuations in any particular food type
compared to small non-flying insects (e.g. mites and than species that forage in a more specialized way
springtails). Particularly, chironomids are among the (Williams et al. 2006). In our study, species such as D.
most diverse and abundant insects of the Paraná River nanus, D. sanborni, H. punctatus, and H. pulchellus, and
wetlands (Montalto and Paggi 2006; Zilli and Paggi to a lesser degree S. nasicus and S. squalirostris, that
2013). The diversity of species with different life feed on superabundant prey, such as chironomids, should
histories within nonbiting midges, hoppers, and be less vulnerable to perturbations in the riparian
froghoppers, allows the presence of assemblages with environment occurring in the floodplain. In the same
different species of these insects and maintain their way, species feeding on ants could be favored in sites
abundance throughout the environmental gradient of with damming alterations. In spite of the abundance of
wetlands (Zilli and Paggi 2013). ants in dammed sites, studied frogs fed only secondarily
on this resource (but see Peltzer and Lajmanovich 2000).
Differences in diet composition and trophic This is probably associated with physiological
plasticity.—The few studies that analyzed the direct restrictions on the consumption of formic acid in ants
effect of habitat alteration on trophic niche dimension of (Zug and Zug 1979).
amphibians have found some degree of diet change Most authors have described the studied species as
among habitats with different degrees of fragmentation, generalist feeders (Basso 1990; Duré and Kehr 2001;
hydroperiod, and vegetation composition (Kovács and Menin et al. 2005; Macale et al. 2008; Falico et al.
Török 1995; Falico et al. 2012b). In the studied species, 2012a) and, in a few cases, as specialist or intermediate
we found a greater diet similarity among populations feeders (between generalist and specialist; Basso 1990;
inhabiting environments with similar habitat alterations, Peltzer and Lajmanovich 2000, 2001; Maneyro and Da
independent of site location, reinforcing the idea that Rosa 2004; Macale et al. 2008). Foraging designations
human disturbance of habitat affects amphibian trophic have differed among authors. For example, D. sanborni
niche dimension, and that each disturbance conveys a has been characterized as a specialist (Macale et al.
different impact on biota. Moreover, the general 2008), intermediate (Basso 1990), and generalist forager
absence of variation of diet diversity and mean number (Menin et al. 2005). Dendropsophus nanus has similarly
of prey per gut indicates that diet change among been identified as a specialist (Basso 1990; Macale et al.

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López et al.—Frog trophic ecology.

2008), intermediate (Peltzer and Lajmanovich 2000), studies and wetland conservation programs.
and generalist (Menin et al. 2005). The lack of prey Determining the effects of habitat alteration on
availability data in these studies may have lead to amphibian populations requires an understanding of
misleading classifications of the foraging patterns of ecological relationships that exceed the analysis of
frogs (López et al. 2009). On the one hand, our results species patterns of occurrence and their relationship to
support the classification of D. nanus, H. pulchellus, H. abiotic factors (Smallbone et al. 2011). To maintain
punctatus and Lysapsus limellum as generalist feeders, ecological structure of wetland landscapes, it is
capable of adjusting their diet to prey shifts and having particularly important to preserve vegetation structure
greater niche breadth. Generalist foragers typically have and hydrological regime (Tilton 1995). For example,
highly flexible diet breadth that depends on the relative preventing use of fire as a management strategy for
value and availability of different food types (Stephens livestock grazing would undoubtedly help to protect
and Krebs 1986) and may opportunistically prey upon amphibians and their prey habitats, preserving in turn the
momentously abundant resources (Falico et al. 2012a). natural interactions and dynamics of populations. As the
This may explain differences in niche breadth reported use of riparian environments or large rivers for
among authors (Duré and Kehr 2001; Menin et al. 2005; agricultural or industrial purposes increases (Lavilla
Macale et al. 2008; Falico et al. 2012a; and this study). 2002), understanding the ecological process affected by
On the other hand, D. sanborni, H. raniceps, S. nasicus, habitat alteration represents an important initial task to
and S. squalirostris could be classified as intermediate preserve the great biodiversity of floodplain habitats.
feeders (Basso 1990; Peltzer and Lajmanovich 2001).
They may have a wide niche breadth (e.g., S. nasicus: Acknowledgments.—We thank Veronica Williner for
Peltzer and Lajmanovich 1999), but also display less critical reading of the manuscript and useful suggestions.
trophic flexibility, thereby increasing their susceptibility Javier Muzon and María Celeste Medrano provided
to fluctuations in food resources. invaluable assistance with arthropod identification.
The association between prey selection and seasonal Collection of animals was authorized by the
or geographical changes in prey availability has been Environmental Agency of Santa Fe Province from
analyzed for few amphibian species (Measey 1998; Argentina (Administrative Resolution 0046-2004)
Maneyro and Da Rosa 2004; Peltzer et al. 2010). The (Secretaría de Estado de Medio Ambiente y Desarrollo
higher trophic plasticity observed in L. limellum, D. Sustentable de la Provincia de Santa Fe, Argentina) and
nanus, H. pulchellus, and H. punctatus can be use of specimens followed the ethical rules in
considered an adaptive advantage in changing accordance with animal care guidelines of Regional and
environments (DeWitt and Scheiner 2004). In this way, National Fauna Administrators, Argentina. Financial
the ability to follow spatiotemporal variations in prey support was provided by fellowships of the National
availability, by shifting diet composition, would allow Council of Scientific and Technical Research of
these species to improve resource acquisition. However, Argentina (Consejo Nacional de Investigaciones
most of species (with the exception of P. limellum and Científicas y Técnicas, CONICET) to J.A. López, P.A.
H. raniceps) showed a tendency to feed on Scarabotti and R. Ghirardi.
superabundant prey like chironimids, which would
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JAVIER A. LÓPEZ is an Assistant Researcher of the National Council of Scientific and Technical Research
(CONICET) at National Institute of Limnology (INALI; CONICET-UNL) and teacher at Department of
Natural Sciences of the Facultad de Humanidades y Ciencias, Universidad Nacional del Litoral, in Santa Fe
City, Argentina. He received his doctoral degree in 2009 from the Universidad Nacional de La Plata
(Argentina) working in amphibian trophic ecology. His research interests include life history, ecology, and
conservation of amphibians. Currently he is studying growth rates, longevity, and genetics of wild
populations of frog species traditionally exploited as food resources by local communities. (Photographed
by Javier A. López).

PABLO A. SCARABOTTI is an Assistant Researcher of the National Council of Scientific and Technical
Research (CONICET) at National Institute of Limnology (INALI; CONICET-UNL) and teacher at
Department of Natural Sciences of the Facultad de Humanidades y Ciencias, Universidad Nacional del
Litoral, in Santa Fe City, Argentina. He obtained a doctoral degree at the Universidad Nacional de
Córdoba (Argentina) in 2009. His research focuses on community ecology and environmental biology of
fishes and amphibians. His topics of research include the adaptive plasticity to environmental stressors
(hypoxia and predators) and community patterns of aquatic vertebrates in large river floodplains.
(Photographed by Javier A. López).

ROMINA GHIRARDI is an Assistant Researcher of the National Council of Scientific and Technical
Research (CONICET) at National Institute of Limnology (INALI; CONICET-UNL) and teacher at the
Facultad de Ciencias de la Salud in the Universidad Católica de Santa Fe, in Santa Fe City, Argentina. She
received her doctoral degree in 2012 from the Universidad Nacional de La Plata (Argentina) working on
distribution of the chytrid fungus Batrachochytrium dendrobatidis (Bd) in Argentina and analyzing the
environmental variables that favor the development of the fungus in the wild. In addition, she is evaluating
the situation of the amphibians infected with Bd in relation to the conservation status of species, the
frequency of positive individuals in different populations, and the mortality rate in the wild. Currently she
is starting the analysis of other amphibian pathogens in the Order Saprolegniales in wild populations.
(Photographed by Javier A. López).

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