Research Article |
Corresponding author: Henning Steinicke ( henning.steinicke@leopoldina.org ) Academic editor: Christoph Knogge
© 2015 Henning Steinicke, Bernd Gruber, Annegret Grimm, Wolf-Rüdiger Grosse, Klaus Henle.
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:
Steinicke H, Gruber B, Grimm A, Grosse W-R, Henle K (2015) Morphological shifts in populations of generalist and specialist amphibians in response to fragmentation of the Brazilian Atlantic forest. Nature Conservation 13: 47-59. https://doi.org/10.3897/natureconservation.13.7428
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Changes in morphological traits, such as body size, body condition, and leg length, are important indicators of changes to life history or habitat quality, which can affect the performance of individuals and therefore the persistence of populations under environmental change. Only very few studies assessed the effect of fragmentation on morphological traits. The few available studies on anurans found that in landscapes with less forest cover body size decreased. Therefore, we predict that body size should also be smaller in fragments compared to continuous forest. Body condition is a further trait closely related to individual performance and thus should decline with more adverse conditions, as is expected in fragments. We tested these hypotheses using snout-vent length, body mass, body condition, and tibia length as response variables. We collected data of a habitat generalist (Rhinella ornata) and a habitat specialist (Ischnocnema guentheri), both leaf-litter amphibian species, from three sites in a fragmented landscape (two isolated and one connected site) and one site in a contiguous part of the Atlantic Forest of Southeast Brazil. In the generalist species, snout-vent-length (SVL) and body mass were significantly lower in fragments compared to the contiguous forest control, whereas tibia length and body condition did not differ among sites. In contrast, SVL, body mass, and tibia length of the specialist species did not differ among sites, but body condition was marginally different among sites, being relatively low in one but not the other isolated fragment. The results indicate that different processes affect the morphology of the two species following habitat fragmentation.
Fragmentation, habitat loss, amphibians, body size, body condition, Brazilian Atlantic forest
Habitat loss and fragmentation are a major cause of biodiversity loss (
Changes in morphological factors are important indicators of changes in life history or habitat quality (
Various environmental factors are known to influence morphology and body condition. In amphibians, resource availability, predation risk, and temperature during larval development have been frequently identified as major determinants of body size and body condition. An increase in resource availability can lead to better body condition and a larger body size (e.g.,
Habitat loss and fragmentation create changes in the abiotic and biotic environment, therefore leading to changes in the quality of the remaining habitat (
Body condition declined and the level of stress hormones increased with the number of forest fragments in a study of the common toad (Bufo bufo) (
Since previous studies found that in more disturbed habitats and landscapes with less forest cover body size decreased in anurans (
The study was carried out in the Mata Atlântica, Brazil, in continuous forest of the Morro Grande Reserve and a fragmented landscape surrounding Caucaia do Alto (both approx. 23°40´S, 47°01´W), located 40 km southwest of São Paulo in the municipalities of Cotia and Ibiúna, Brazil. The forest reserve and the adjacent study area are located on the Atlantic Plateau of São Paulo at an altitudinal range of 860-1075 m above sea level (
We selected four sites: two isolated small forest fragments (Carmo Messias and Dito, referred to in the following as “iso1” and “iso2”, respectively), one small forest fragment (Alcides, referred to in the following as “connect”) connected by a forest corridor to a larger forest area, and a control site (“control”) within the continuous forest. Forest fragments covered an area of 5 ha each and contained no permanent/larger water bodies within the forest area or within a radius of 200 m outside the forest fragment. The continuous forest was about 9,400 ha in size. There was no permanent/larger water body present at the control site within a radius of 200 m.
We chose two leaf-litter dwelling forest species for comparison. We selected Rhinella ornata, a bufonid species, as a habitat generalist due to its high tolerance to matrix habitats. This species is distributed throughout the Atlantic Forest in the states of São Paulo and Rio de Janeiro (
We selected Ischnocnema guentheri for comparison. This species is distributed over large parts of the Mata Atlântica (
We established three parallel transects of 100 m each on each site. We sampled frogs by hand during the rainy seasons October 2003 until March 2004 and November 2004 until March 2005. We surveyed each site for five consecutive nights (21:00 – 01:00 local time) before sampling the next site. Once all sites had been sampled, the next round of sampling started again at the first site. The total search effort was 25 nights per site (2003/2004 15 nights per site, 2004/2005 10 nights per site).
We measured snout-vent-length (SVL) and tibia length (TL) of all captured individuals using a calliper with an accuracy of ±0.1 mm. We measured tibia length for the left body side. We weighed individuals using digital scales with an accuracy of ±0.1 g. We used photographical individual identification to eliminate data points of recaptured individuals. As juveniles were seldom captured, we only included the data of subadult and adult individuals in the analysis (R. ornata with a SVL ≥ 27 mm; I. guentheri with a SVL ≥ 10 mm). As knowledge on natural history of both species is scarce, we could not further separate subadult from adult individuals. Unless calling, sexes cannot be separated by external morphology in both species.
Opinions about which body condition index (BCI) to use are controversial in the literature (
We assessed differences in SVL, body mass, and BCI among sites by using an analysis of variance (ANOVA), after testing the assumption of normality of all variables used (Kolmogorov-Smirnov-Test: D = 0.5 – 0.7, all α > 0.05). For tibia length, we used an analysis of covariance (ANCOVA) to remove a potential influence of SVL in the comparison of sites. For significant results, we used the post-hoc Tukey’s Honestly Significant Difference test (Tukey’s HSD) for multiple comparisons to assess differences among individual sites.
We captured a total of 499 individuals of the selected species, comprising 116 R. ornata and 383 I. guentheri. After removing juvenile individuals from the data, 54 and 376 individuals respectively were kept for the analyses. An overview of captures and measurements per species and site is given in Table
Mean ± one standard deviation (SD) of morphological traits of the studied species in the four study sites. Abbreviations: control = control site, connect = connected site, iso1 and iso2 = isolated site one and two; BCI: body condition; N: sample size; SVL: snout-vent-length; TL: tibia length. [BCI calculated as SMI]
N | SVL (mm) | TL (mm) | BCI | Body mass (g) | |
---|---|---|---|---|---|
I. guentheri | |||||
control | 18 | 20.0±2.4 | 13.9±1.5 | 0.78±0.10 | 0.74±0.24 |
connect | 60 | 21.4±4.4 | 15.0±3.1 | 0.75±0.20 | 0.94±0.49 |
iso1 | 136 | 20.2±5.1 | 14.0±3.9 | 0.70±0.22 | 0.84±0.62 |
iso2 | 162 | 19.6±7.0 | 13.4±5.5 | 0.78±0.33 | 0.94±0.86 |
R. ornata | |||||
control | 9 | 57.8±22.2 | 26.5±9.2 | 6.46±0.54 | 19.9±19.1 |
connect | 6 | 51.2±12.5 | 23.9±6.3 | 6.65±0.72 | 11.3±5.9 |
iso1 | 26 | 39.4±8.5 | 18.3±4.0 | 7.04±1.30 | 5.3±4.0 |
iso2 | 13 | 44.4±12.2 | 20.1±6.2 | 6.61±1.42 | 8.2±8.0 |
In R. ornatasnout-vent-length (SVL) and mass differed significantly among sites (ANOVA: F = 5.03, α < 0.01; and F = 5.7, α < 0., respectively). Both were highest for the control site, with the difference to “iso1” being statistically significant in a Tukey’s HSD (α < 0.01) and that to “iso2” being marginally significant (α = 0.09) for SVL and significant (α = 0.05) for mass. Both were intermediate in the connected small site. Tibia length (TL) did not differ among sites when accounting for differences in SVL (ANCOVA: F = 0.41, α = 0.7). BCI calculated as SMI did not differ among sites (ANOVA: F = 0.726, α = 0.5). The same was the case when using residuals of the regression of ln mass on lnSVL as BCI (ANOVA: F = 0.64, α = 0.9).
Snout–vent length and body mass of I. guentheri did not differ significantly among sites (ANOVA: F = 1.35, α = 0.26 and F = 0.84, α = 0.47, respectively). Likewise, TL did not differ significantly among sites when the effect of SVL was accounted for (ANCOVA: F = 0.84, α = 0.5). BCI based on SMI was highest in the control site and one isolated site and lowest in the other isolated site (Table
Our results partly support the predicted effects of fragmentation on phenotypic characteristics (smaller snout-vent-length, shorter legs, and lower body mass, and body condition in fragments compared to continuous habitat). Individuals of the generalist species R. ornata were smaller in fragmented habitats compared to the control site, while body condition did not differ among sites. For the specialist species I. guentheri body condition differed marginally significantly among sites and was highest in the control site and in one isolated fragment but lowest in the other isolated fragment. The other morphological traits did not differ among sites. Thus, the habitat generalist and the habitat specialist showed different morphological responses to habitat fragmentation.
The reduced body size in R. ornata and the lower body mass of I. guentheri in the most severely affected (small isolated) site(s) are in line with previous studies in lizards and amphibians that found a reduced body size in landscapes with low forest cover, in fragments, and in disturbed compared to undisturbed habitats (
In fragments that do not retain suitable aquatic habitats eggs have to be deposited in water bodies in the matrix. Eggs and aquatic larvae have to deal with changes in biotic and abiotic parameters of reproduction ponds within the matrix. Ponds inside and outside of forests usually will differ in physical conditions (
For frogs with a direct development much less is known about the factors that determine development and the morphology of hatchling and subsequently adult anurans than for pond breeding anurans.
The results for body condition suggest that the quality of the terrestrial habitat was not negatively affected for the habitat generalist R. ornata despite body mass being significantly lower in isolated fragments. For the habitat specialist I. guentheri habitat quality seems to have been negatively affected in one but not the other isolated fragment. This suggests that the study sites differed in food resource quality or physiological stress that translate into energetic costs for the latter species in some fragments but not in others. While fragmentation of tropical forests has a large effect on species composition and abundance in invertebrates (
Edge effects on abiotic conditions, such as an increase in temperature and a decrease of humidity, affect a larger fraction of a small than a large patch or continuous forests (
In conclusion, the effects of fragmentation on size and body condition differed between the habitat generalist and the habitat specialist. This suggests that the two species are affected by different processes driving morphological shifts in the wake of habitat fragmentation, and that for specialists these processes may differ among fragments. The observation that in the same study region as ours habitat specialists among small mammals showed an increase in body condition with fragmentation (
We are grateful to M. Dixo and J.-P. Metzger for technical support and scientific advice, C. Guimarães and A. Bispo on behalf of numerous persons for their help in the field, R. Nali (SABESP) for accommodation, private landowners for letting us work on their properties, two anonymous reviewers and C. Knogge for their helpful comments, and to C. Knogge for administrative and logistic support. This project was funded within the Brazilian-German bilateral research programme “Science and Technology for the Mata Atlântica” by the German Federal Ministry of Education and Research (BMBF FKZ 01LB020A1).