Research Article |
Corresponding author: Marcelo dos Santos Fernandes ( enzopipapipa@yahoo.com.br ) Academic editor: Ana Maria Leal-Zanchet
© 2020 Cristiano Lúcio Rodrigues, Thiago Borges da Silva, Wilfried Klein, Marcelo dos Santos Fernandes.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Rodrigues CL, da Silva TB, Klein W, dos Santos Fernandes M (2020) Analysis of abiotic factors associated with foam nests of Cuvier’s foam froglet (Physalaemus cuvieri) in southeastern Brazil. Neotropical Biology and Conservation 15(4): 675-688. https://doi.org/10.3897/neotropical.15.e57804
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Climate change may have significant impacts on amphibian diversity due to alterations in microhabitat conditions where these species occurs. Understanding the abiotic factors associated with a species’ microhabitat are therefore necessary to evaluate the impact they may suffer. Amphibians are exposed to changing microhabitat conditions at multiple life stages, since reproduction and larval development of most species depend on water, whereas adults frequently depend on terrestrial habitats. Physalaemus cuvieri is a Neotropical frog that uses foam nests for reproduction that may provide some protection for tadpoles against temperature and humidity fluctuations. Herein, foam nests of P. cuvieri were studied within vegetation around a pond, with the aim of analyzing the morphometric (depth, area and volume) relationships of foam nests with abiotic factors (humidity, temperature). Humidity 2 cm above the nests was significantly greater than 2 m from the nests. Temperature, measured at different depths of the nests, was significantly reduced by up to 10 °C when compared to atmospheric air temperatures above the nests. We conclude that foam nests facilitate a protective environment for eggs by regulating temperature and humidity to acceptable levels.
Area/volume relation, humidity, morphometric measurements, temperature, thermal conduction
Amphibian populations worldwide are declining. A growing concern among herpetologists is the influence of global warming on reproductive success, the quality of microhabitats, and interactions between amphibians and their pathogens (
The family Leptodactylidae Werner, 1896, with 220 species currently described (
Foam nests, produced through limb motions beating oviduct secretions into foam during egg deposition, are a feature of the genus Leptodactylus, shared by certain other leptodactylid genera including Physalaemus, and by the family Rhacophoridae, in South America and Australia (
The present study was carried out around a pond (20°21'44"S, 47°46'26"W; Fig.
Data were collected out on a single day in November 2012, between 15:00 and 18:00 hours, mapping 10 foam nests from P. cuvieri that were arranged on the banks of the lagoon, where males were seen vocalizing among the bushes (Fig.
Overview of study site located in Ituverava, northeastern state of São Paulo, southeastern Brazil. A) Study area as seen by a satellite image (Map data GoogleEarth, obtained on April 23, 2013), the yellow bar is equivalent to 100 m; B) Typical Cerrado vegetation on the lake shore of the study area; C) Individuals of Physalaemus cuvieri before nest building; D) A foam nest of Physalaemus cuvieri in the study area.
After mapping the nests in the study area, data on morphometric measurements were collected, such as: (1) depth (D), considered as the central vertical axis between the opening and the bottom of the nests, measured with the aid of a caliper (Eccofer); (2) area of ground covered by the nest (AS); and (3) volume (V). The perimeter shape of the nest opening was analyzed and varied between circular and elliptical, being considered elliptical when a clear longitudinal axis could be identified.
The variables AS and V were calculated using the following equations:
AS = π.r² Eq (1)
(for circular nests), r being the radius of the circumference;
AS = π.a.b Eq (2)
(for elliptical nests), a and b being respectively the largest and the smallest half axes of the ellipse;
V = π/6.a.b.c Eq (3)
(for circular and elliptical nests), a and b being the diameters of the nests, perpendicular to each other, and c being the depth of the nests (
Measurements of relative air humidity and air temperature were taken at 2 cm around the nests (RH0, T0, respectively) and 2 m above (RH2, T2, respectively) using a portable thermo-hygrometer (HT-300, INSTRUTHERM, Brazil). The temperatures of three depths within the nests were also measured: on the foams surface (TS), within the central part of the foam (TC) and on the ground of the foam (TG), using infrared thermometers (DT-3880 and DT-900, DELLT, Brazil). The thermal exchange between air and nests was interpreted based on data on thermal conduction and the area/volume ratio calculated by us.
Data were analyzed using the statistical software GraphPad Prism 5. After testing for normal distribution, the correlations between depth, area and volume of the nests were evaluated, as well as the area/volume ratios of the nests with the internal temperatures, using a two-tailed Pearson’s correlation. To test for possible differences between the relative humidity around and 2 m above nests, a paired Student’s t-test was performed, as well as a two-tailed Pearson’s correlation. To test for possible differences between foam nest temperatures, a Repeated Measured One-Way analysis of variance (ANOVA) were used, followed by Tukey’s post-hoc test. Data are given as mean ± standard error of the mean (SEM) and a significance of p ≤ 0.05 was considered (
The foam nests of P. cuvieri were arranged at a distance of up to two meters from the edge of the pond and with an average distance of one meter between each other. At the border of the pond, the foam nests were uniformly distributed below the vegetation, composed mainly by families Poaceae and Cyperaceae, close to the plant’s body, protected from sunlight. The nests presented morphometric measurements of low variability, except for volume (Fig.
Morphometric and abiotic characterization of Physalaemus cuvieri foam nests. A) Foam nest measurements: depth (D), area of ground covered by the nest (AS), nest volume (V); B) Measurements of relative air humidity 2 meters above the nests (RH2) and 2 cm around the nests (RH0); C) temperature measurements taken 2 m above the nests (T2), 2 cm around the nests (T0), on the foams surface (TS), within the central part of the foam (TC), and on the ground of the foam nest (TG).Horizontal bars indicate mean and the whiskers indicate SEM. Different letters indicate significantly differences between values.
While the use of foam nest as reproductive strategy among anurans is well known in the literature (e.g.
The P. cuvieri nests showed relatively low variation in the morphometric variables analyzed, such as depth (11.5 ± 1.0 cm) and surface site (54.3 ± 13.2 cm2), except for volume (249.1 ± 26.3 cm3), as shown by the individual data points in Fig.
The greater relative humidity of the air around the P. cuvieri nests, when compared to two meters above them, could be explained by the microclimate generated by the evapotranspiration of the vegetation associated with the nests, by the humidity of the soil near the pond, as well as the lower wind velocity within the vegetation. In contrast, air temperatures around the nests did not differ from those at two meters above ground. The great incidence of sunlight in the study area throughout the day and greatly degraded shrub vegetation, providing only few shaded areas, result in high temperatures, even close to the ground. According to
The air temperatures around the nests were significantly greater when compared to the surface, central and bottom temperatures of the foam nests, being some 10 °C lower in the center and at the bottom of the nest. A similar pattern has been observed for a Leptodactylus labyrinthicus (Spix, 1824) population from the same pond (
Studies on foam nests of Engystomops pustulosus (Cope, 1864) floating on water are somewhat contradictory regarding temperature variations. While
The low area/volume ratio seems, however, also to be important for thermal relationships, as a low nest surface exposed to air would reduce heat exchange between P. cuvieri nests and air. The lower the area/volume ratio, the smaller the surface and center temperatures would be and vice versa. Another factor that could contribute to the observed reduction in nest temperatures is the vertical orientation of the P. cuvieri nests, which increase the distance between the eggs/larvae and the outside air. The low thermal conductivity of the air (
Building foam nests as reproductive strategy has evolved independently several times among anurans (
We conclude, that (1) the foam nests of P. cuvieri are exposed to a wetter microclimate when compared to the air above the vegetation, (2) the foam nests of P. cuvieri showed internal temperatures well below atmospheric values in the period during which the measurements were taken, and (3) the morphometry and foam of P. cuvieri nests seem to influence the way in which they perform thermal exchanges with their surroundings, maintaining a stable temperature suitable for the development of eggs, embryos, and larvae. However, more detailed studies are needed in order to understand how nest temperatures might fluctuate over a 24-hour periods or over an entire incubation period, and to establish the thermal sensitivity of P. cuvieri eggs and tadpoles from different populations to such temperature variations.
We would like to thank Jonathan Richard Codd for carefully revising the manuscript, and Fernando Luís Medina Mantelatto, for the valuable suggestions during the study and preparation of this manuscript.