Corresponding author: Claudia Hermes ( email@example.com )
Academic editor: Klaus Henle
© 2016 Claudia Hermes, Annika Döpper, H. Martin Schaefer, Gernot Segelbacher.
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: Hermes C, Döpper A, Schaefer MH, Segelbacher G (2016) Effects of forest fragmentation on the morphological and genetic structure of a dispersal-limited, endangered bird species. Nature Conservation 16: 39-58. https://doi.org/10.3897/natureconservation.16.10905
Throughout the tropics, pristine forests disappear at an alarming pace. This presents a severe threat to forest-dependent species. Especially dispersal-limited understory birds are affected by forest loss. We here explored the effects of habitat fragmentation on the genetic structure and the morphology of the Ecuadorian Tapaculo (Scytalopus robbinsi). This bird occurs only in a small range in the premontane cloud forests of southwestern Ecuador. The global population size is declining rapidly due to habitat loss and is currently estimated at only 3000 mature individuals. We caught a total of 28 Ecuadorian Tapaculos in forests of varying size in an area of about 40 km². From each bird, we took morphological measurements and a blood sample. This was used to develop a set of 10 species-specific microsatellite primers for genetic analysis and we found that the Ecuadorian Tapaculos display high levels of genetic diversity. Additionally, we identified dispersal corridors for the species across the landscape using a least-cost path analysis. Notably, we found that wing shape is related to forest size. Individuals in smaller fragments show adaptations of the wing morphology to enhanced mobility and better flight capacity. Our results suggest that the Ecuadorian Tapaculo may rapidly adapt its morphology to the level of habitat fragmentation. This potential can possibly mitigate the risk of local extinctions of the species due to human-caused forest loss and fragmentation.
El Oro Tapaculo, cloud forest, habitat fragmentation, wing morphology, genetic diversity, microsatellites
Forest loss and fragmentation are among the main drivers of species extinction in the Neotropics. For many forest-dependent species, the amount of available habitat as well as the connectivity between remaining forested patches decline. The sensitivity of a species to forest loss and fragmentation is related to the species’ functional traits (
Small populations are inherently vulnerable to genetic drift and loss of genetic diversity, which constitutes an extinction risk for populations (
Insectivorous, forest-dependent birds are particularly sensitive to the fragmentation of forests (
In this study, we examined the effects of forest fragmentation on the genetic and morphological structure of the Ecuadorian Tapaculo (Scytalopus robbinsi, Rhinocryptidae), a species almost unknown to science. This bird is endemic to the understory of cloud forests in southwestern Ecuador. In general, Tapaculos are among the species most sensitive to habitat fragmentation and are therefore considered an ideal model for assessing fragmentation effects on dispersal-limited species (
The ability of a species to cope with ongoing habitat fragmentation can determine its abilities to persist in a changing environment and avoid local extinction (
The Ecuadorian Tapaculo, also known as El Oro Tapaculo, is an insectivorous bird endemic to a small range (~ 1100 km2) on the western slopes of the Andes in southwestern Ecuador, at an elevation of 850–1500 m (
The only protected site within the range of the Ecuadorian Tapaculo is the private Buenaventura reserve in the canton Piñas (3.655°S, 79.744°W), established in 1999 by the Ecuadorian NGO Fundación Jocotoco. This reserve covers an area of 2300 ha in an elevation of 400–1500 m (Figure
Map of the study area in southwestern Ecuador. Forested areas are shaded grey, whereas white areas represent non-forested areas (mainly cow pastures). The Buenaventura reserve is circled by the dashed line. The bolt black line represents a highway cutting the reserve into a northern and a southern part, while minor roads are indicated by the thin lines.
Field work was carried out between December 2013 and May 2014 and between November 2014 and January 2015 in the Buenaventura reserve, and near Ñalacapa, about 5 km south of Buenaventura (Figure
For bird capturing, we used mist-nets and tape recordings of the song of male Ecuadorian Tapaculos as a decoy. If an individual approached the playback, observers herded it into the net. The Ecuadorian Tapaculo’s secretive behavior, very good vision and excellent maneuverability made the capturing very challenging. We captured 28 males. Birds were ringed with a standard aluminum ring and color-banded individually. Then, individuals were weighed and the lengths of tail, tarsus, wing, primary feathers and the first secondary feather were measured. From each individual, we took a blood sample from the brachial vein. To minimize stress, birds were handled within less than 10 minutes of capture and released unharmed to the same sites. Blood samples were stored in 99.8% ethanol and transferred into a -20 °C freezer.
To obtain an index for body size, we carried out a principal component analysis (PCA) for all the morphological variables that we recorded. As variables differed in their numerical range, they were z-standardized prior to the analysis. A second PCA for the variables wing length and length of the feathers P9 to S1 provided an index for the wing shape. For both PCAs, missing values (e.g., caused by feather molt) were replaced by the mean. Additionally, we quantified the body condition of each individual using the scaled mass index (
We extracted DNA from the blood samples and compiled a set of 10 species-specific microsatellite primers (for a description of the primer development see Suppl. material
Landscape barriers disrupting or decreasing connectivity between individuals or populations can be quantified and qualified by the creation of a resistance map, which allocates a specific resistance value to each cell of the land cover grid according to the mobility of the species (
To assess isolation by distance, we tested for relationships between the genetic and the geographic distances between the individuals. Geographic distance was expressed by Euclidian distance between territories as well as by LCP length and LCP cost. In GENALEX 6.5 (
Using the R package HIERFSTAT, we tested whether genetic diversity has been reduced since the species was discovered in 1990. Accounting for the difference in sample size between the two groups, we compared allelic richness of the 26 samples we took in 2013–2015 with those of seven museum specimen collected in 1990–1991 in the same area (from the tissue collection at the Zoological Museum Copenhagen; sample numbers 125057, 125070, 125071, 125072, 126057, 126058 and 126167).
Additionally, we tested for a potential decline in the effective population size in the past with the program MSVAR 1.3 (
The first four principal components (PCs) of the PCA of body size accounted for 71.92% of the variance of 14 morphological variables (Table
Body size of Ecuadorian Tapaculos. Principal component analysis for the body size of 28 Ecuadorian Tapaculos, with the loadings, eigenvalues and variance of the first four principal components (threshold: 0.35; bold font).
|PC 1||PC 2||PC 3||PC 4|
Wing shape of Ecuadorian Tapaculos. Principal component analysis for the wing shape of 28 Ecuadorian Tapaculos, with the loadings, eigenvalues and variance of the first three principal components (threshold: 0.35; bold font).
|PC 1||PC 2||PC 3|
For both PCAs, we detected a marginally significant relationship between PC 1 and forest size (PCA of body size: P = 0.057; tau = -0.273; and PCA of wing shape: P = 0.063; tau = -0.267; Kendall correlation). None of the other PCs correlated with forest size (all P > 0.12; Kendall correlation). Similarly, there was no relationship between the body condition of birds and the size of the forest fragments (P = 0.76; tau = 0.044; Kendall correlation).
Allelic richness of the museum samples was 3.80 ± 0.75, while that of the recently collected samples was 3.59 ± 0.57. Therefore we concluded that genetic diversity has not changed within the last ~ 25 years. The STRUCTURE analysis showed no clear population substructure. K = 1 yielded the highest probability, indicating that most likely all samples belonged to the same population. However, error bars were highly overlapping amongst the estimates for different numbers of clusters (Figure
Mean ± SD of the log-likelihood for K = 1 to 8 distinct genetic populations. Strong support for K = 1 indicates that most likely all the samples stem from the same genetic group.
With the least-cost path analysis, we could identify a dispersal corridor for Ecuadorian Tapaculos across the study area, which circumvented the valley between the northern and southern part (Figure
Modelling the population demography yielded evidence of a severe population decline in the past. All potential scale reduction factors were < 1.1, so we concluded that chains converged well (
In this study, we investigated the genetic and morphological structure of the Ecuadorian Tapaculo, an endangered bird endemic to the understory of premontane cloud forests in southwestern Ecuador. In the study population, genetic diversity has remained constant within the last 25 years, even though the global population has declined dramatically. Despite the fact that forests are highly fragmented and the species has only limited dispersal abilities, we did not detect a structuring into genetically distinct sub-populations on a scale of 40 km². Notably forest size influenced bird morphology, with individuals in larger fragments having rounder wings than their conspecifics in smaller forests.
Throughout the study area, we found no genetic structuring among Ecuadorian Tapaculos, indicating that a substantial amount of gene flow is still maintained. Even though the Ecuadorian Tapaculo is a bad disperser, migration between different forest fragments seems not to be blocked. We expected that habitat fragmentation in the range of the species produced genetically distinct populations in different forest fragments, as it was shown for a similar species (
Gene flow across the study area is not impeded by barriers and Mantel-tests between genetic and geographic distances suggest isolation by distance (IBD). In theory, IBD can lead to considerable genetic differentiation even at small scales (Wright 1943). In the most extreme dispersal event observed in the Ecuadorian Tapaculo, an individual crossed 245 m of un-forested habitat to establish a territory in a remote forest fragment (
Genetic diversity of Ecuadorian Tapaculos in the study area remained constant between 1990 and 2015. On a global scale however, population size and most likely also genetic diversity still decrease. Even though the result of the analysis of past population demography yielded a high level of uncertainty and should therefore be treated with caution, it gave evidence of a severe population decline. The Buenaventura reserve remains until now the only protected site within the distribution range of the Ecuadorian Tapaculo. Around the reserve, forests are heavily fragmented and degraded; mostly, patches are smaller than 100 ha and consist of young secondary stands. The constant level of genetic diversity in the study population over 25 years, which is presumably attributable to the establishment of the reserve, shows that a negative population trend can be stopped. However, in order to achieve a change for the better on the scale of the global population of Ecuadorian Tapaculos, it would be necessary to protect remaining forests throughout the entire distribution range, which, in view of ongoing deforestation, seems implausible. In general, Tapaculos are among the understory species most sensitive to fragmentation and are therefore seen as umbrella species for conservation planning (
While several studies have already addressed the effects of forest fragmentation on the genetic structure of a population, its effects on individual morphology are far less examined. However, the degree of habitat fragmentation can cause different morphological adaptations in birds (
Ecuadorian Tapaculos have short, round wings and only limited flight capacities; they do rarely fly distances longer than 3 m and move mainly by walking or hopping (
Wing morphology is highly heritable in birds (
In the study population, phenotypic divergence in wing shape could arise in sympatry. Even though the individuals in the study area were not genetically differentiated at neutral markers, the morphological changes are likely promoted by the isolation by distance we discovered over the study area. Moreover, the differences in the level of forest fragmentation likely exert a selective pressure, which is strong enough to produce distinct phenotypes despite the homogenizing effect of gene flow. If the diverging selective pressures are high, a new beneficial allele can fix quickly and affect the genome (
Funding: The project was funded by Mohammed bin Zayed Species Conservation Fund (grant number 13257994) and Sweden Club300 Bird Protection.
Conflict of interest: The authors declare that they have no conflict of interest.
Ethical approval: All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Permissions to conduct field work (No. 005-IC-FAN-DPEO-MAE) and to export samples (No. 05-2014-FAU-DPAP-MA) were granted by Ministerio de Ambiente and Ministerio de Agricultura, Ganadería, Acuacultura y Pesca, Ecuador.
We thank Jeroen Jansen, Arne Pinnschmidt and Hannes Kampf for their great assistance during field work and Niels Krabbe for his valuable advice in the preparation of this study. We thank the Tissue Collection at the Zoological Museum Copenhagen for lending us their blood samples of the Ecuadorian Tapaculo. Stefanie Hartmann kindly assisted in the analysis of past population demography. We are grateful to Fundación de Conservación Jocotoco and the landowners in the Ñalacapa area for permission to mist-net on their land. The article processing charge was funded by the German Research Foundation (DFG) and the University of Freiburg in the funding programme Open Access Publishing.