Elsevier

Ecological Indicators

Volume 66, July 2016, Pages 369-381
Ecological Indicators

Bird sensitivity to disturbance as an indicator of forest patch conditions: An issue in environmental assessments

https://doi.org/10.1016/j.ecolind.2016.02.006Get rights and content

Highlights

  • Bird sensitivity to disturbance (Parker III et al., 1996) was tested as ecological indicator.

  • Parker's classification failed to predict environmental conditions in patches in HML.

  • Only high sensitivity species locally functioned well as an ecological indicator.

  • Although flawed, Parker's classification was very used in environmental assessments.

  • This is the first argument of how Parker's classification is wrongly used as ecological indicator.

Abstract

An Environmental Assessment (EA) is one of the steps within the Environmental Impact Assessment process. Birds are often used in EA to help decision makers evaluate potential human impacts from proposed development activities. A “sensitivity to human disturbance” index, created by Parker III et al. (1996) for all Neotropical species, is commonly considered an ecological indicator. However, this parameter was created subjectively and, for most species, there have been no rigorous field test to validate its effectiveness as such. Therefore, in this study, we aim to: (1) evaluate if, at the local scale, birds from forest patches in a human-modified landscape (HML) may differ in sensitivity from Parker's sensitivity classification; (2) evaluate the effectiveness of the species richness value at each sensitivity level as an ecological indicator; (3) gather information on how often and in which manner Parker's classification has been used in EA. To do so, bird sampling was performed in eight forest patches in a HML over one year. Then, we created a local sensitivity to disturbance using information about threat, endemism, spatial distribution and relative abundance of all species in the study area. We found that 37% of the forest birds showed different local sensitivity levels when compared with Parker's classification. Our results show that only the richness of high-sensitivity species from our local classification fitted the ecological indicator assumptions helping the environmental conditions evaluation of the studied patches. We conclude that species richness of each Parker's bird sensitivity levels do not necessarily perform as an ecological indicator at the local scale, and particularly in HML. Nevertheless, Parker's Neotropical bird sensitivity classification was used in 50% of EA we reviewed. In these, 76% assumed that it was an accurate ecological indicator of the local forest conditions for birds. The lack of clear criteria used in Parker's classification allows diverse interpretations by ornithologists, and there is no agreement about the ecological meaning of each sensitivity level and what environmental conditions each level may indicate of. Therefore, the use of Parker's classification in EA may jeopardize accurate interpretations of proposed anthropogenic impacts. Furthermore, because a bird species’ sensitivity often varies between locations, we argue that Parker's generalized classification of bird sensitivity should not be used as an indicator of forest environmental conditions in EA throughout HMLs in Neotropics. Rather, local bird ecological indices should be explored, otherwise, erroneous predictions of the anthropogenic impacts will continue to be common.

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,

References (149)

  • R.B. Matlock et al.

    Avian communities in forest fragments and reforestation areas associated with banana plantations in Costa Rica

    Agric. Ecosyst. Environ.

    (2002)
  • F.P. Melo et al.

    On the hope for biodiversity-friendly tropical landscapes

    Trends Ecol. Evol.

    (2013)
  • J.P. Metzger et al.

    Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region

    Biol. Conserv.

    (2009)
  • J.C. Muñoz et al.

    Contribution of woody habitat islands to the conservation of birds and their potential ecosystem services in an extensive Colombian rangeland

    Agric. Ecosyst. Environ.

    (2013)
  • R. Pardini et al.

    The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia

    Biol. Conserv.

    (2009)
  • E.R. Alexandrino et al.

    Nest stolen: the first observation of nest predation by an invasive exotic marmoset (Callithrix penicillata) in an agricultural mosaic

    Biota Neotrop.

    (2012)
  • E.R. Alexandrino et al.

    Aves do campus Luiz de Queiroz (Piracicaba/SP) da Universidade de São Paulo: mais de 10 anos de observações neste ambiente antrópico

    Atualidades Ornitol.

    (2013)
  • P.L. Angermeier et al.

    Biological integrity versus biological diversity as policy directives

    BioScience

    (1994)
  • L. Anjos et al.

    Bird communities in natural forest patches in southern Brazil

    Wilson Bull.

    (1999)
  • L. Anjos et al.

    Effects of fragmentation on the bird guilds of the Atlantic Forest in North Paraná, Southern Brazil

    Ornitol. Neotrop.

    (2004)
  • L. Anjos

    Bird species sensitivity in a fragmented landscape of the Atlantic forest in southern Brazil

    Biotropica

    (2006)
  • L. Anjos et al.

    Sobre o uso de níveis de sensibilidade de aves à fragmentação florestal na Avaliação da Integridade Biótica: um estudo de caso no norte do Estado do Paraná, sul do Brasil

    Rev. Bras. Ornitol.

    (2009)
  • L. Anjos et al.

    Position in the distributional range and sensitivity to forest fragmentation in birds: a case history from the Atlantic forest, Brazil

    Bird Conserv. Int.

    (2010)
  • A.Z. Antunes et al.

    Birds from Carlos Botelho Park state of São Paulo southeastern Brazil

    Biota Neotrop.

    (2013)
  • W.J. Arendt et al.

    Diversidad de aves en agropaisajes en la region norte de Nicaragua

    Ornitol. Neotrop.

    (2012)
  • M. Awade et al.

    Using gap-crossing capacity to evaluate functional connectivity of two Atlantic rainforest birds and their response to fragmentation

    Austral Ecol.

    (2008)
  • C. Banks-Leite et al.

    Edge effects as the principal cause of area effects on birds in fragmented secondary forest

    Oikos

    (2010)
  • C. Banks-Leite et al.

    Comparing species and measures of landscape structure as indicators of conservation importance

    J. Appl. Ecol.

    (2011)
  • G.A. Bencke et al.

    Áreas importantes para a conservação das aves no Brasil: parte 1, estados do domínio da Mata Atlântica

    (2006)
  • C.J. Bibby et al.

    Bird Census Techniques

    (2000)
  • D. Boscolo et al.

    Importance of interhabitat gaps and stepping-stones for Lesser Woodcreepers (Xiphorhynchus fuscus) in the Atlantic Forest, Brazil

    Biotropica

    (2008)
  • D. Boscolo et al.

    Is bird incidence in Atlantic forest fragments influenced by landscape patterns at multiple scales?

    Landsc. Ecol.

    (2009)
  • D. Boscolo et al.

    Isolation determines patterns of species presence in highly fragmented landscapes

    Ecography

    (2011)
  • D.F. Bradford et al.

    Bird species assemblages as indicators of biological integrity in Great Basin rangeland

    Environ. Monit. Assess.

    (1998)
  • P.M. Bressan et al.

    Fauna ameaçada de extinção no Estado de São Paulo

    (2009)
  • T.M. Brooks et al.

    Time lag between deforestation and bird extinction in tropical forest fragments

    Conserv. Biol.

    (1999)
  • T. Brooks et al.

    Deforestation and bird extinctions in the Atlantic forest

    Anim. Conserv.

    (1999)
  • H. Byron

    Biodiversity and Environmental Impact Assessment: A Good Practice Guide for Road Schemes

    (2000)
  • J.F. Candido

    The edge effects in a forest bird community in Rio Claro, São Paulo State, Brazil

    Rev. Bras. Ornitol.

    (2000)
  • G.E. Canterbury et al.

    Bird communities and habitat as ecological indicators of forest condition in regional monitoring

    Conserv. Biol.

    (2000)
  • V. Carignan et al.

    Selecting indicator species to monitor ecological integrity: a review

    Environ. Monit. Assess.

    (2002)
  • B. Carroll et al.

    Environmental Impact Assessment Handbook: A Practical Guide for Planners, Developers and Communities

    (2002)
  • V. Cavarzere et al.

    Avifauna da Estação Ecológica dos Caetetus, interior de São Paulo, Brasil

    Papéis Avulsos Zool.

    (2009)
  • V. Cavarzere et al.

    Birds from cerradão woodland, an overlooked forest of the Cerrado region, Brazil

    Papéis Avulsos Zool.

    (2011)
  • S.A. Chambers

    Birds as Environmental Indicators: Review of Literature. Parks Victoria Technical Series No. 55

    (2008)
  • R. Channell et al.

    Dynamic biogeography and conservation of endangered species

    Nature

    (2000)
  • R.L. Chazdon et al.

    Rates of change in tree communities of secondary Neotropical forests following major disturbances

    Philos. Trans. R. Soc. B

    (2007)
  • Comitê Brasileiro de Registros Ornitológicos

    Listas das aves do Brasil

    (2014)
  • CONAMA Resolution 001/86. Available in: http://www.mma.gov.br/port/conama/res/res86/res0186.html (accessed...
  • CONAMA Resolution 237/1997. Available in: http://www.mma.gov.br/port/conama/res/res97/res23797.html (accessed...
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