Ariovaldo Antonio Giaretta

Using δ13C stable isotopes to quantify individual-level diet variation

Individual-level diet variation can be easily quantified by gut-content analysis. However, because gut contents are a ‘snapshot’ of individuals’ feeding habits, such cross-sectional data can be subject to sampling error and lead one to overestimate levels of diet variation. In contrast, stable isotopes reflect an individual’s long-term diet, so isotope variation among individuals can be interpreted as diet variation. Nevertheless, population isotope variances alone cannot be directly compared among populations, because they depend on both the level of diet variation and the variance of prey isotope ratios. We developed a method to convert population isotope variances into a standardized index of individual specialization (WIC/TNW) that can be compared among populations, or to gut-content variation. We applied this method to diet and carbon isotope data of four species of frogs of the Brazilian savannah. Isotopes showed that gut contents provided a reliable measure of diet variation in three populations, but greatly overestimated diet variation in another population. Our method is sensitive to incomplete sampling of the prey and to among-individual variance in fractionation. Therefore, thorough sampling of prey and estimates of fractionation variance are desirable. Otherwise, the method is straightforward and provides a new tool for quantifying individual-level diet variation in natural populations that combines both gut-content and isotope data.

Reproductive ecology and behaviour of a species of Adenomera (Anura, Leptodactylinae) with endotrophic tadpoles: Systematic implications

The species of the Leptodactylus fuscus group and those of the genus Adenomera lay their eggs in underground chambers. According to current systematic arrangement of these genera, this behaviour is convergent. Here we describe reproduction, courtship, tadpole morphology, calls, chamber structure, and populational phenology of an Adenomera species, and compare some of these features with those of other species of the genus and with species of Leptodactylus of the fuscus and pentadactylus groups. We tested the tadpoles of the Adenomera sp. and those of Leptodactylus labyrinthicus (pentadactylus group) for their foam‐making abilities. There was sexual dimorphism in size; males averaged 22.0 mm and females 24.3 mm in snout–vent length. Males called from late September to late February; calling often began about 2–3 h before sunset. Males called exclusively in open (non‐forest) areas. Egg clutches were found around male calling sites. Males excavated spherical chambers which had a direct entrance. During mating, the male led the female towards a previously excavated chamber. Territorial interactions (aggressive calls and fights) occurred when an intruder male approached a calling male. Late‐stage tadpoles and newly metamorphosed juveniles were found within underground chambers. Clutch size averaged 10.6; eggs averaged 3.7 mm in diameter and were cream coloured. Tadpoles had horny beaks, but no labial tooth; spiracle was present. All tested groups of tadpoles generated foam within 10 h. As we report for Adenomera sp., the males of Leptodactylus species of the fuscus group lead the female to a previously excavated chamber. Tadpole foam‐making behaviour was reported in Leptodactylus of the fuscus group and was previously unknown for any species of Adenomera or for Leptodactylus of the pentadactylus group. The way in which the tadpoles of Adenomera sp., Leptodactylus spp. (of the fuscus group) and L. labyrinthicus made foam was quite similar. The foam‐making behaviour of the studied tadpoles may act to avoid compaction of the tadpoles at the bottom of the basin or underground chamber, avoiding overcrowding and increasing respiratory and excretory efficiency. As presently recognized, the phylogenetic position of Adenomera suggests that reproductive major behavioural features are convergent with some Leptodactylus species. Alternatively, our data point to close phylogenetic relationships between Adenomera and Leptodactylus of the fuscus and pentadactylus groups, reinforcing the paraphyletic nature of the genus Leptodactylus.

The nested assembly of individual-resource networks.

1. Much of the current understanding of ecological systems is based on theory that does not explicitly take into account individual variation within natural populations. However, individuals may show substantial variation in resource use. This variation in turn may be translated into topological properties of networks that depict interactions among individuals and the food resources they consume (individual-resource networks). 2. Different models derived from optimal diet theory (ODT) predict highly distinct patterns of trophic interactions at the individual level that should translate into distinct network topologies. As a consequence, individual-resource networks can be useful tools in revealing the incidence of different patterns of resource use by individuals and suggesting their mechanistic basis. 3. In the present study, using data from several dietary studies, we assembled individual-resource networks of 10 vertebrate species, previously reported to show interindividual diet variation, and used a network-based approach to investigate their structure. 4. We found significant nestedness, but no modularity, in all empirical networks, indicating that (i) these populations are composed of both opportunistic and selective individuals and (ii) the diets of the latter are ordered as predictable subsets of the diets of the more opportunistic individuals. 5. Nested patterns are a common feature of species networks, and our results extend its generality to trophic interactions at the individual level. This pattern is consistent with a recently proposed ODT model, in which individuals show similar rank preferences but differ in their acceptance rate for alternative resources. Our findings therefore suggest a common mechanism underlying interindividual variation in resource use in disparate taxa.

Reproduction, phenology and mortality sources of a species of Physalaemus (Anura: Leptodactylidae)

Physalaemus cf. fuscomaculatus is a foam-nesting frog of seasonally dry environments of south-eastern Brazil. We report on the reproduction and other natural history features of this species. Population parameters were based on trapped specimens. The advertisement call is described. The calling and spawning season is coincident with the rainy period. Calling and spawning were performed in ponds. Most of the adults were trapped in October and the juveniles during wetter months and the beginning of the dry season. At the end of the reproductive season, the median size of adults lowered. Egg clutches averaged 2350 eggs, each egg being about 1.4 mm in diameter. Males were more abundant than females in traps. Communal foam nests were frequent, involving up to 40 individual nests. Tadpoles entered the water within about 40 h. Maggots (Diptera) infested egg clutches; water bugs and mammals preyed upon adults. In this region, the dry/cold season may be so difficult for survival that early maturation at small size would be advantageous. The male-biased sample may be related to the greater motility of males. The rapid abandonment of the foam by the tadpoles and communal nesting may help to reduce predation by maggots. Skin toxins were not effective in deterring predation upon adults. The call of P. cf. fuscomaculatus differs from that of other species in the biligonigerus group and can help to define the specific status of the studied population.

On the natural history of the South American pepper frog, Leptodactylus labyrinthicus (Spix, 1824) (Anura: Leptodactylidae)

Some species of Leptodactylus of the L. pentadactylus group lay their eggs outside water but the tadpoles need to reach water to complete the larval phase; other species complete development in terrestrial nests. Here we present details of the reproduction of L. labyrinthicus in south‐eastern Brazil. The proportion of tadpoles and trophic eggs in aged egg clutches was determined, as well as the growth of the tadpoles while in the nest. The gut contents of tadpoles that were in egg clutches of frogs were analysed. Adult males did not differ from females in size and had hypertrophied forearms and an enlarged spine on the thumb. Reproduction was initiated with the first rains of August/September and extended to mid‐January. Calling and spawning occurred at permanent or temporary water bodies. The foam nests were built in excavated basins outside of, but close to the water. The male determined the place of the basin construction; after amplexus, the female completed the excavation. The amplexus was axillary. One female spent the day after spawning in the foam. The eggs were pale grey, the yolk averaging 2.3 mm in diameter. The mean number of eggs was 2101 per egg clutch. The number of tadpoles in individual nests varied between 0.05% and 11.40% in relation to the total laid eggs. The tadpoles entered water when rains flooded the basin. The tadpoles grew to 12 times the weight of an individual egg while in the nest; no nesting tadpole was beyond stage 25. The longest time we followed tadpoles in a nest was 25 days. Tadpoles were found preying upon eggs of three other frog species and upon conspecific eggs. Males fought by grasping each other in a belly‐to‐belly position; the powerful arms and the thumb spines represent weapons. Even though males can reach maturity in the season following birth, small size would prevent them from establishing their own territory. All the species of the L. pentadactylus group may build their foam nests within excavated basins. The basins may protect the eggs and embryos from cannibalistic tadpoles and may have an anti‐desiccation effect. In order to produce trophic eggs, the female may delay laying additional unfertilized eggs until after the male has abandoned the foam nest. Anuran eggs represent an important food item for tadpoles after they leave the nest.

Species richness, relative abundance, and habitat of reproduction of terrestrial frogs in the Triângulo Mineiro region, Cerrado biome, southeastern Brazil

Based on field observations and pitfall sampling, we determined the species richness, relative abundance, and reproductive habitat of terrestrial frogs in three municipalities in the Triângulo Mineiro region, south Cerrado biome, in southeastern Brazil. We found thirty-two species of terrestrial frogs, belonging to the families Brachycephalidae, Bufonidae, Cycloramphidae, Dendrobatidae, Leiuperidae, Leptodactylidae and Microhylidae. Most of the species were found in open areas and reproduced in human-generated environments, such as artificial lakes (10 species) and ponds (14 species). Dominance was high, with Physalaemus cuvieri Fitzinger, 1826 (Leiuperidae) representing 48% of sampled frogs. A larger number of individuals was captured in the wet season, when most of the species were reproducing. Compared to other areas of Cerrado biome, the Triângulo Mineiro sites presented a larger number of species, which may be attributed to the larger sampled area and greater sampling effort, lower altitude and presence of human generated habitats. The richness of terrestrial frogs was also larger than that in some forested localities in southeastern Brazil, indicating that the number of species cannot be explained only by precipitation and type of vegetation cover. The greater abundance of individuals during the wet season may be related to a greater movement of adults to breeding sites and to juvenile recruitment/dispersion. The heterogeneity of environments in the Cerrado biome, including its several isolated highlands, contributes to its high (local and regional) diversity of frogs.

Predation on foam nests of leptodactyline frogs (Anura: Leptodactylidae) by larvae of Beckeriella niger (Diptera: Ephydridae)

The presence of maggots of the fly Beckeriellaniger (Ephydridae) in nests of six syntopic South American leptodactyline frogs is reported. The number of tadpoles of Physalaemus cuvieri leaving infested and non-infested nests were compared, and behavioural plasticity at the time of nest departure in the presence and absence of maggots was tested for. Maggots were found in nests of all species with exposed foam nests (four Physalaemus and two Leptodactylus species). The maggots remained in the nests of P. cuvieri for up to 3 days; adults emerged from pupae after 7 days. While in the nests the maggots consumed eggs, embryos, and tadpoles. The levels of infestation increased from the beginning to the middle of the rainy season. Mortality caused by the maggots represented an important source of mortality (mean 74%) of eggs and embryos of P. cuvieri, and probably, of the other species. The time of emergence from nests by the tadpoles of P. cuvieri was shorter (up to 21 h earlier) in infested nests. The tadpoles that left the infested nests were at the same, or a less-developed stage than tadpoles in non-infested nests. The variation in the degree of infestation, with lower values at the beginning and the increase to the middle of the rainy season, suggests that the flies may be an obligatory predator on foam nests. For tadpoles of P. cuvieri, entering the water at a later developmental stage may be important to avoid aquatic predators. Conversely, leaving infested nests at the earliest possible stage may represent a strategy to avoid maggot predation. The longer time before emergence of tadpoles of P. cuvieri from non-infested nests corroborates the hypothesis that, among leptodactyline frogs, the foam nest is a predator avoidance adaptation in the aquatic media.

Intrapopulation Diet Variation in Four Frogs (Leptodactylidae) of the Brazilian Savannah

Abstract Age and sex-based as well as individual-level diet variation are known to occur in many natural populations, and may have important ecological and evolutionary implications. In the case of individual-level diet variation, most examples come from species-poor, temperate communities, and it is currently believed that it results from population niche expansion following interspecific competitive release. We investigated and measured the intrapopulation diet variation in four species of frogs, Leptodactylus ( = Adenomera) sp., Eleutherodactylus cf. juipoca, L. fuscus, and Proceratophrys sp., that are part of species-rich frog communities of the Brazilian Cerrado. Specifically, we investigated age and sex-related, as well as individual-level, diet variation. We measured individual-level diet variation with the IS index of individual specialization, which is a measure of the degree of overlap between individual niches and the population niches. We found no ontogenetic shifts or sex-related differences in the types of prey consumed. However, we found evidence of individual-level diet variation in the four studied species (IS ˜ 0.2–0.5). There was a negative correlation between IS and the population niche width (r  =  –0.980; P < 0.0001), indicating that interindividual diet variation is more pronounced in more generalized populations. This pattern suggests that individual niche widths remain constrained even when population niche breadth is wide, consistent with the presence of functional trade-offs. We found no evidence that these trade-offs arise from morphology, since there was no diet–morphology correlation. We hypothesize that trade-offs have a behavioral or physiological basis, which needs further investigation. This is the first documented case of individual-level diet variation in a diverse tropical community, indicating that this phenomenon is not restricted to competitive release-driven niche expansion in temperate, depauperate communities.

Reproductive ecology and behavior of Thoropa miliaris (Spix, 1824) (Anura, Leptodactylidae, Telmatobiinae)

Ecologia e Comportamento Reprodutivo de Thoropa miliaris (Spix, 1824) (Anura, Leptodactylidae, Telmatobiinae). As especies de Thoropa estao distribuidas no sul e sudeste do Brasil e tem girinos semiterrestres em ambientes rochosos. Aqui apresentamos dados complementares sobre reproducao, cuidado paternal e canibalismo por girinos em T. miliaris. Machos guardioes foram testados quanto a perturbacoes as suas desovas. As desovas foram postas em faixas de umidade na rocha; os ovos foram postos em camada unica e estavam aderidos a superficie da rocha, raizes e uns aos outros. Os girinos eclodiram entre quatro e seis dias apos a oviposicao. O numero de ovos em duas desovas foi 750 e 1190; os ovos eram cinza e a porcao vitelinica mediu cerca de 1,7 mm em diâmetro; 2,3 mm com a capsula gelatinosa. Foram observadas interacoes agressivas entre os machos. Os machos permaneceram com suas desovas durante a noite e reagiram agressivamente as perturbacoes experimentais. Girinos em estagios tardios foram vistos canibalizando ovos. Uma desova em uma faixa de umidade recem formada morreu por desidratacao. As faixas de umidade na rocha sao os unicos locais onde os ovos e os girinos podem se desenvolver e representam um fator limitante para a reproducao porque sao raras. Para as femeas, a selecao de faixas umidas recem formadas deve representar um balanco entre as vantagens em ocupar lugares livres de girinos canibais e/ou competidores e os riscos de perda de prole por desidratacao. Nossos resultados nao apoiam Cycloramphinae como um taxon valido, indicando que as similaridades morfologicas e comportamentais entre as especies de Thoropa e Cycloramphus devem ser interpretadas como convergencia.

Food habits and ontogenetic diet shifts of the litter dwelling frog proceratophrys boiei (wied)

Here is described the diet of Proceratophrys boiei (Wied, 1825), a leaf litter frog of the Atlantic Forest, and test for relationships between frog size and prey size and type. The diet was determined by stomach content analysis. In 38 frogs, was found 76 prey items belonging to 23 taxa. Insects predominate in the diet and the most frequent categories were coleopterans (39.4% of total volume) and orthopterans (25.0%). There was a positive correlation between frog size and volume of prey taken. The most important ontogenetic shift in prey type was an increase in the consume of coleopterans and insect larvae with increasing frog size.