Giants, Dwarfs and the Environment - Metamorphic Trait Plasticity in the Common Frog

In order to understand adaptation processes and population dynamics, it is central to know how environmental parameters influence performance of organisms within populations, including their phenotypes. The impact of single or few particular parameters in concert was often assessed in laboratory and mesocosm experiments. However, under natural conditions, with many biotic and abiotic factors potentially interacting, outcomes on phenotypic changes may be different. To study the potential environmental impact on realized phenotypic plasticity within a natural population, we assessed metamorphic traits (developmental time, size and body mass) in an amphibian species, the European common frog Rana temporaria, since a) larval amphibians are known to exhibit high levels of phenotypic plasticity of these traits in response to habitat parameters and, b) the traits' features may strongly influence individuals' future performance and fitness. In 2007 we studied these metamorphic traits in 18 ponds spread over an area of 28 km 2. A subset of six ponds was reinvestigated in 2009 and 2010. This study revealed locally high variances in metamorphic traits in this presumed generalist species. We detected profound differences between metamorphing froglets (up to factor ten); both between and within ponds, on a very small geographic scale. Parameters such as predation and competition as well as many other pond characteristics, generally expected to have high impact on development, could not be related to the trait differences. We observed high divergence of patterns of mass at metamorphosis between ponds, but no detectable pattern when metamorphic traits were compared between ponds and years. Our results indicate that environment alone, i.e. as experienced by tadpoles sharing the same breeding pond, can only partly explain the variability of metamorphic traits observed. This emphasizes the importance to assess variability of reaction norms on the individual level to explain within-population variability

Study ponds assigned according to the results of the k-means clustering.

<p>Ponds are plotted in the first two principal components using 16 abiotic habitat characteristics, explaining 40.53 % of data variance. Ponds with emigrating <i>Rana temporaria</i> metamorphs are indicated by filled, non-emigration ponds by open triangles. Loadings of the components are given in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089982#pone.0089982.s003" target="_blank">Table S3</a>.</p

<i>Rana temporaria</i> metamorphs from two different ponds in the study area.

<p>Although being in the same developmental stage and emigrating at the same date, the differences in size, proportion and vitality are obvious. Individual left: 10.2 mm, 0.09 g, right: 17.2 mm, 0.56 g, 23 July 2009.</p

Pond characteristics and metamorphic traits.

<p>Visualization of environmental parameters in relation to <i>Rana temporaria</i> metamorphic mass (median) and development time (median). Values are colour-coded, warm colours indicating higher values. Ponds (bottom) are ordered according to their values for the respective trait, the values for the respective environmental parameter are given in the column above. There is no correlation between traits and environmental parameter visible (rows).</p

Metamorphic mass <i>of Rana temporaria</i> for five ponds in the years 2007, 2009 and 2010.

<p>For values of size and development time, see Table S7.</p

ANOVA for mass, size, and development time of metamorphosing <i>Rana temporaria</i>.

<p>Given are the data for five ponds and three years. df  =  degrees of freedom.</p

Summary of metamorphing <i>Rana temporaria</i> juveniles and predator- and tadpole-density in the respective ponds in 2007.

<p>Survival rate was based on an average of 1117 eggs per clutch. For metamorphic traits, mean, coefficient of variance (CV), as well as minimum and maximum size and mass of individuals for each pond is given. For predator- and tadpole-density, mean and SD of all samplings, number of sampling events and total number of box samplings summed up for realized samplings are given (see methods for detailed description). For pond abbreviations, see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089982#pone.0089982-Grzinger1" target="_blank">[31]</a>.</p><p>cl.  = clutches; meas.  = measured, devel.time = development time, samp.  = samplings: events/total samplings.</p

Most important parameters (see Table S1) describing the pattern of <i>Rana temporaria</i> metamorphosis mass in study ponds.

<p>Emigration mass in study ponds (n = 10, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0089982#pone-0089982-g004" target="_blank">Figure 4</a>) is described according to: log(mass) ∼x × development-time +z × development-time². Given are the parameter combinations for the coefficients of slope (x) and bend (z) of the curve in the linear mixed model, which showed the lowest AICc (Akaike Information Criterion for finite sample sizes) after model selection (i.e. ΔAICc = AICc_i−AICc_min, <200). ‘Pond’ was used as random factor. Akaike mass  =  normalized relative likelihood of the model given the data.</p