A Multiscale Approach Indicates a Severe Reduction in Atlantic Forest Wetlands and Highlights that São Paulo Marsh Antwren Is on the Brink of Extinction

<div><p>Over the last 200 years the wetlands of the Upper Tietê and Upper Paraíba do Sul basins, in the southeastern Atlantic Forest, Brazil, have been almost-completely transformed by urbanization, agriculture and mining. Endemic to these river basins, the São Paulo Marsh Antwren (<i>Formicivora paludicola</i>) survived these impacts, but remained unknown to science until its discovery in 2005. Its population status was cause for immediate concern. In order to understand the factors imperiling the species, and provide guidelines for its conservation, we investigated both the species’ distribution and the distribution of areas of suitable habitat using a multiscale approach encompassing species distribution modeling, fieldwork surveys and occupancy models. Of six species distribution models methods used (Generalized Linear Models, Generalized Additive Models, Multivariate Adaptive Regression Splines, Classification Tree Analysis, Artificial Neural Networks and Random Forest), Random Forest showed the best fit and was utilized to guide field validation. After surveying 59 sites, our results indicated that <i>Formicivora paludicola</i> occurred in only 13 sites, having narrow habitat specificity, and restricted habitat availability. Additionally, historic maps, distribution models and satellite imagery showed that human occupation has resulted in a loss of more than 346 km2 of suitable habitat for this species since the early twentieth century, so that it now only occupies a severely fragmented area (area of occupancy) of 1.42 km2, and it should be considered Critically Endangered according to IUCN criteria. Furthermore, averaged occupancy models showed that marshes with lower cattail (<i>Typha dominguensis</i>) densities have higher probabilities of being occupied. Thus, these areas should be prioritized in future conservation efforts to protect the species, and to restore a portion of Atlantic Forest wetlands, in times of unprecedented regional water supply problems.</p></div

Occurrence of <i>Formicivora paludicola</i>.

<p>A) Example of LANDSAT 8 satellite image visually scanned in the search for marshes to be surveyed. Numbers 1 and 2 indicate new areas of occurrence <i>Formicivora paludicola</i>. B) Circles represent areas of previously known occurrence that still possess the species; Stars represent new areas of occurrence discovered during our field surveys; Numbers 1 and 2 indicate the same areas of A; Green areas represent Random Forest model projections of areas climatically suitable for <i>F</i>. <i>paludicola</i>. The EOO (extent of occurrence) was estimated at 1,268 km² and ES-EOO (environmental suitability in extent of occurrence) at 1,245 km².</p

13 best models tested for probabilities of occupancy of <i>Formicivora paludicola</i>.

<p>N. parameters = number of parameters estimated by the model; AICc = Akaike Information Criterion value with correction for small samples; ΔAICc = difference between each model and the best model; AICc weight = Akaike weights (ωi) (the conditional probability for each model).</p><p>13 best models tested for probabilities of occupancy of <i>Formicivora paludicola</i>.</p

Averaged estimates of βs for models covariates.

<p>The values indicate the relationship between variables and the probability of occupancy of <i>Formicivora paludicola</i>.</p><p>Averaged estimates of βs for models covariates.</p

Species Distribution Model results and surveyed areas.

<p>Green areas represent Random Forest projections of areas climatically suitable for São Paulo Marsh Antwren (<i>Formicivora paludicola</i>). Grey shading represents urban areas. Circles represent areas known to possess <i>F</i>. <i>paludicola</i> that were used in occupancy models. Triangles represent areas visited for the distribution model validation where the species is absent. Diamonds represent areas visited three times for occupancy models surveys where the species is absent. Stars represent new areas discovered to possess <i>F</i>. <i>paludicola</i> that were used in the occupancy models. Crosses represent areas where the species could be extinct. Some validation localities are not shown on the map.</p

Differences between density of cattail (<i>Typha dominguensis</i>) in sites where <i>Formicivora paludicola</i> is absent or present.

<p>Orange dots represent average values.</p

Plant invasion: Another threat to the São Paulo Marsh Antwren (<i>Formicivora paludicola</i>), a species on the verge of extinction

<div><p>During the past 100 years in densely populated south-eastern Brazil, wetlands have been severely transformed due to urbanization, agriculture and mining. The recently discovered São Paulo Marsh Antwren (<i>Formicivora paludicola</i>) is endemic to these wetlands, and is listed as “Critically Endangered” by the IUCN. The species is only found in an area of 1.42 km², it has a sparse and fragmented distribution, low dispersal capacity, and has probably lost around 300 km² of habitat in the past 100 years. Furthermore, very little is known about <i>F</i>. <i>paludicola</i> natural history, and so it is difficult to construct a robust conservation plan. Using Kernel home range estimations and the Adjusted-SD/Torus Shift test (a novel tool for animal-habitat association studies), we showed that the species avoids patches of the alien invasive ginger lily (<i>Hedychium coronarium</i>). Given the high density of their population (3.6 mature individuals/ha), <i>F</i>. <i>paludicola</i> could thrive in relatively small areas of suitable wetlands protected from human occupation and water contamination, however special attention should be paid to biological invasions, which may represent a serious threat to the remaining populations. Protecting a few small wetlands used by <i>F</i>. <i>paludicola</i> would be an important step towards general conservation and restoration of Atlantic Forest wetlands and its endemic endangered species.</p></div

<i>Formicivora paludicola</i> home range estimates.

<p><i>Formicivora paludicola</i> home range estimates.</p

Occurrence of <i>Formicivora paludicola</i>.

<p>Circles and triangles indicate marshes where São Paulo Marsh Antwren (<i>Formicivora paludicola</i>) is found at Upper Tietê Basin and Upper Paraíba do Sul Basin (south-eastern Brasil). Triangles indicate the three sites where we examined animal-habitat association. Modified from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0189465#pone.0189465.ref027" target="_blank">27</a>].</p

Adjusted-SD results.

<p>Adjusted-SD results.</p