Bird sensitivity to disturbance as an indicator of forest patch conditions: An issue in environmental assessments
Introduction
Human impacts on natural ecosystems are ubiquitous, environmentally damaging, and likely to continue for the foreseeable future (Vitousek et al., 1997, Foley et al., 2005). One important tool to minimize and regulate these impacts is the Environmental Impact Assessment (hereafter EIA) (Glasson and Salvador, 2000, Carroll and Turpin, 2002, Slootweg and Mollinga, 2010, Sánchez and Croal, 2012). An EIA is a multidisciplinary and systematic process of evaluating and mitigating the impacts of proposed human development actions, such as industries, housing, infrastructure, mining, agriculture, etc. (Kolhoff et al., 2010, Sánchez and Croal, 2012). An EIA typically includes a multidisciplinary Environmental Assessment (hereafter EA), which includes an assessment of the biodiversity occurring in a given area where a potential impact will occur (CONAMA Resolution 001/86, CONAMA Resolution 237/1997, SMA Resolution 49/2014 but see Glasson and Salvador, 2000). In Brazil, as in many countries (Rajvanshi et al., 2010), this biodiversity assessment component is meant to help decision makers evaluate the possible environmental consequences of development activities (Glasson and Salvador, 2000, Silveira et al., 2010, Sánchez and Croal, 2012).
The EA is often limited by funding and time constraints (Thompson et al., 1997, Vasconcelos, 2006, Rajvanshi et al., 2010, Silveira et al., 2010). Thus, the selection of ecological indicator species can help to expediently assess the ecological condition of the environment under study (e.g., Temple and Wiens, 1989, Dale and Beyeler, 2001, Niemi and McDonald, 2004, Syrbe et al., 2013), as they may act as a surrogate measurement of other biological groups not accessed (Carignan and Villard, 2002, Niemi and McDonald, 2004). Birds are frequently used as indicator species (Byron, 2000, Vasconcelos, 2006, Silveira et al., 2010, Straube et al., 2010, Chang et al., 2013), because they are relatively easy to sample in the field (Gardner et al., 2008), and they are good indicators of habitat quality (e.g., Temple and Wiens, 1989, Stotz et al., 1996, Bradford et al., 1998, Canterbury et al., 2000, Carignan and Villard, 2002, Sutherland et al., 2004, Sekercioglu, 2006, Sekercioglu, 2012, Chambers, 2008). The landmark book “Neotropical Birds: Ecology and Conservation” by Stotz et al. (1996) includes a database with a variety of biological and ecological parameters for all bird species in the Neotropics (see database A, hereafter referenced as Parker III et al., 1996, as recommended by the authors). Herein, the authors highlight that species are differentially vulnerable to human disturbance. They rank each Neotropical bird species’ “sensitivity to disturbance”, as “high”, “medium” or “low”. A common interpretation of this parameter is to deem the occurrence of birds of high-sensitivity at a given site as an indication of good environmental conditions (e.g., Anjos, 2006, Anjos et al., 2009, Anjos et al., 2010, Loures-Ribeiro et al., 2011). Consequently, this theoretical assumption fits the requirements of the Brazilian environmental legislation (item I, article 5° IBAMA Normative Instruction n.146/2007), which suggest biodiversity inventories in EA use ecological indicators (CONAMA Resolution 001/86, Straube et al., 2010). However, there is uncertainty as to how the “sensitivity to disturbance” parameter is representative of the ecological condition of a given site when used in this manner.
The “sensitivity to disturbance” parameter was created over 25 years ago. It was based on the authors’ expertise, as well as reports and experience from other ornithologists about the relative frequency (high, medium, or low) of each species found in association with disturbed patches of its preferred habitat (J.W. Fitzpatrick personal communication, but see “Guide to the databases” on Parker III et al., 1996). While it was a groundbreaking and highly instructive work in 1996, there is considerable subjectivity in the rankings, and there is now significant evidence that it may be outdated or flawed. For example, some species listed as medium-sensitivity (e.g., Picazuro Pigeon – Patagioenas picazuro; Flavescent Warbler – Myiothlypis flaveola) and high-sensitivity (e.g., Gray-necked Wood-Rail – Aramides cajaneus; Uniform Finch – Haplospiza unicolor; Pavonine Cuckoo – Dromococcyx pavoninus; Red-crowned Ant-Tanager – Habia rubica) are frequently reported at highly impacted sites such as cities and agricultural landscapes (e.g., Willis and Oniki, 1987, Willis and Oniki, 2002, Pozza and Pires, 2003, Franz et al., 2010, Cruz and Piratelli, 2011, Ferraz et al., 2012, Alexandrino et al., 2013). Thus, in order to assess the validity of using Parker's classification, it is important to evaluate whether species respond to human disturbance as expected from this parameter. Besides, taking into consideration that a species conservation status may vary at different geographical scales (Milner-Gulland et al., 2006, Brito et al., 2010), we may question whether the pan-Neotropical scale used in Parker's classification can efficiently reflect the status of a species’ population at regional or local scales.
Henle et al. (2004) warn that interactions of species traits and environmental conditions must be considered to predict species sensitivity to human disturbance or habitat fragmentation, a procedure not used in Parker's classification. Only two studies have tested the consistency of Parker's “sensitivity to disturbance” classification in representing the effects of forest habitat loss and fragmentation on birds in Atlantic Forest patches (Ribon et al., 2003, Anjos, 2006). Besides, there is relatively little research assessing the variability in sensitivity of forest birds to anthropogenic disturbances and fragmentation effects at local scales in human-modified landscapes (HML) (e.g., Ribon et al., 2003, Anjos, 2006, Piratelli et al., 2008, Anjos et al., 2009, Anjos et al., 2010, Anjos et al., 2011, Loures-Ribeiro et al., 2011). This contributes to uncertainty about using Parker's classification in EAs.
Therefore, we test if, at the local scale, forest bird species from patches in a HML may show different levels of sensitivity to disturbance than Parker's classification. To do so, we developed a local metric of sensitivity to disturbance using threat status, endemism, spatial distribution and relative abundance of the species in the study area. We then evaluate the effectiveness of using Parker's classification as an ecological indicator of the effects of the forest habitat loss and fragmentation, by comparing the two classifications. Finally, we review the frequency and manner of use of Parker's classification in EA from a wide range of projects that were environmentally licensed in the last two decades. We conclude with a discussion of the shortcomings of and risk associated with using Parker's classification in EA.
Section snippets
Study site selection
Field surveys were conducted in the Corumbataí River basin, in east-central São Paulo State (22°04′46″ S to 22°41′28″ S; 47°26′23″ W to 47°56′15″ W), Brazil (Fig. 1). This river basin was originally covered by semi-deciduous seasonal forest (Atlantic forest biome) and sparse savannah woodland (Cerrado biome). However, after years of human modification, it is now composed of small (e.g., Charqueada with around ∼15,000 inhabitants) to medium cities (e.g., Rio Claro with ∼200,000 inhabitants) (
Local sensitivity to disturbance for forest species
In 447 observation hours, we documented 191 species, 144 of which are forest species (see Appendix F for the rarefaction curves for each sampled patch). Our local classification included eight threatened species and 13 endemic species (one of Cerrado and 12 of Atlantic Forest). Additionally, there were 103 forest species with at least five records in point counts, which were included in the ISA test. Forty-seven species showed non-random distributions between patches, while 56 had a
Local sensitivity to disturbance
Our results show that the level of sensitivity to forest habitat loss and fragmentation for forest species is not necessarily the same at continental (Neotropical) and local scales. Comparing our local classification with previous research that tested forest bird sensitivity to habitat loss and fragmentation effects in Atlantic Forest patches, we identified a lack of pattern of sensitivity for some species at local scales. For example, Habia rubica was considered a good bioindicator for large
Acknowledgements
We are grateful to the Forest Science Department and “Luiz de Queiroz” College of Agriculture (Brazil) and the Department of Biology, University of Utah (USA), where this research was performed. We also thank all of the landowners who allowed us access to the forest patches in their property. We thank Alexandre C. Franchin, Luiz dos Anjos and Carlos Candia-Gallardo by the fruitful discussions, as well as the paper reviewers. This research was funded by FAPESP (Processes 2010/05343-5,
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