Get 20M+ Full-Text Papers For Less Than $1.50/day. Start a 14-Day Trial for You or Your Team.

Learn More →

Temperate forest bird communities associated with a historic mining impact area: do tailing remnant effects modify their structure?

Temperate forest bird communities associated with a historic mining impact area: do tailing... Revista Brasileira de Ornitologia 27(2): 94–107. ARTICLE June 2019 Temperate forest bird communities associated with a historic mining impact area: do tailing remnant effects modify their structure? 1 1,2 1 Katia Lemus , José Fernando Villaseñor-Gómez , Francisco Roberto Pineda-Huerta & Javier Salgado-Ortiz Laboratorio de Investigación en Ornitología, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Morelia, Michoacán, Mexico. Corresponding author: jfvillasenorg@hotmail.com Received on 21 February 2019. Accepted on 04 June 2019. ABSTRACT: Birds contribute to the stability of ecosystems and represent a tool used to evaluate a variety of anthropogenic impacts. The area known as E l Oro-Tlalpujahua Mining District in central Mexico was subjected to significant environmental impacts as a result of ore extraction, including profound habitat transformations, landscape changes, and the accumulation of potentially toxic elements in their tailings (favoring its bioavailability and dispersion). After more than 60 years without extractive activities, there is no knowledge on extant remaining impacts on biological communities. Assuming the presence of negative impacts on birds, we compared the composition and abundance of bird communities in two locations, representing a site without exposure to tailings (S ) and another one with tailings deposition (S ). From June 2014 to June 2015, we recorded 2828 individuals of 108 avian species 1 2 in 369 point counts (S = 91, S = 95). The Chao1 indicator suggested we re corded 96% of the species present. We found a high 1 2 similarity in the general composition and abundance of bird species between communities (> 85%). However, there were significant differences in the abundances of 18 species (9 of them higher in the control site); these differences might result from differential effects of potentially toxic e lements on functional groups (such as feeding guilds), resource availability, as well as other factors not accounted for. Historically, mining activities in the area generated significant changes in the structure and composition of the forest, and disrupted ecological processes. Despite the fact that current conditions appear favorable to the relative stability of the bird community, specific p hysiological effects on some species of bir ds sixty years after the cessation of mineral extraction could occur. Further studies on physiological performance and the effects of potentially toxic e lements on local birds could unveil unknown effects at the individual level. KEY-WORDS: avian communities, diversity, El Oro-Tlalpujahua Mining District, mining tailings, remnant effects. INTRODUCTION composition of animal communities (Pickett & White 1985). In birds, these types of changes have been described Information on the diversity and abundance of species in previously by Ugalde-Lezama et al. (2012) and Manson communities represent the basis for assessing the quality & Jardel-Peláez (2009), who found the simplification of of their environment. Through monitoring it is possible to forest structure related to the decrease in the composition evaluate changes associated with different causal factors; of bird communities. comparisons on the occurrence of species in different To evaluate anthropogenic impacts on wildlife, it is environments, and the characterization of their relative desirable to have an indicator of the intensity and extent abundance is often presented as supporting evidence of the impacts; if significant, they might be reflected (Balmer 2002). in changes in the composition and/or abundance of Disturbance processes generated by human activities species at the community level. At the population level, involve habitat changes through the modification of impacts may be reflected in changes in survival rates land use for productive activities (e.g., agriculture and or reproductive success of species, or changes in their livestock), urban development, and mining activities, with distribution (Altaf et al. 2018, Mahmoud & Gan 2018, the resulting effects on soil and water (Manson & Jar del- Xu et al. 2018). Responses at the individual level are the Peláez 2009). These events at the landscape level modify most sensitive and usually have been assessed through the structure of vegetation and generate successional changes in physical and physiological conditions (e.g., processes that promote changes in the structure and height, weight, condition index, quantity of fat reserves) Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. During the 65 years after cessation of activities in (Pérez-Tris 1999). Few studies have explored the response Mina Dos Estrellas, the region has experienced ecological of birds to anthropogenic impacts resulting from mining succession that led to the reestablishment of secondary at the community level; most have focused on particular species (e.g., Garitano-Zavala et al. 2010, Rubio et al. temperate forest made up of tolerant and pioneer 2016), or ecological settings (e.g., Ouboter et al. 1999, tree species that survived the disturbance period on impoverished soil conditions (Muñiz-Castro 2008). Eagles-Smith et al. 2016). Because of the demands of wood and other Several authors recognize the need for environmental materials for the construction and maintenance of mine monitoring from geological, ecological, and public health perspectives (Boulet & Larocque 1988, Perotti et al. galleries, the surrounding areas, and even those far away 2017). Reclamation mining sites have sometimes been were also overexploited (Corona-Chávez & Uribe-Salas 2009). While the area was subjected to a strong mining perceived as sites potentially important for biodiversity impact, at the end of the mine's active life some nearby (Batty 2005). Mines that have operated for centuries are areas remained free from the effects of ore wastes, the source of pollutants that remain stored in tailings or the bottom of reservoirs, and their ecological effects deforestation, agriculture and cattle grazing. These areas in most cases have not been determined (Kossoff et al. offer the possibility of investigating if some remnant effects derived from mining in the past are maintained 2014). Globally, estimations of mercury released to the and affect bird communities. Considering the possibilities environment as a byproduct of the amalgamation for of extant impacts, we analyzed and compared the richness recovery of gold and silver indicate that there has been over 260,000 tons released between 1550 and 1930 (Lacerda and abundance of forest bird communities inhabiting 1997). Furthermore, for mining sites that historically tailings sites (abandoned approximately 65 years ago) and sites free from mine wastes, in order to determine ceased production and left a legacy of ecological impact, differences that might be indicative of remnant impacts little is known about the span and intensity of their on the avifauna. Facing a possible scenario of intense impacts (Balistrieri et al. 2002, Eisler 2004, Cristol et al. 2008, Ventakeswarlu et al. 2016). Some studies have and prolonged impact induced by the bioavailability of addressed aspects of geodynamics, bioavailability and potentially toxic elements in tailings, we expected bird communities away from tailings to be more diverse and transfer of elements in mine tailings, which are potentially have higher abundance at least for the most common toxic elements derived from mining runoff and water species, in comparison to the polluted area. currents (e.g., Rösner 1988, Perotti et al. 2017), as well as on soil and vegetation (O'Sullivan et al. 1999, Jacob & Otte 2004, Struckhoff et al. 2013), aquatic and terrestrial METHODS animals (such as benthic invertebrates, springtail insects, fish, amphibians, reptiles and birds), remediation, and Study area ecological restoration (Lefcort et al. 1988, Gonçalves- Rodriguez & Shraft 2001, Lock et al. 2003, Cristol et al. 2008, Márquez-Ferrando 2008). Data from historically The OTMD is situated in the limits of the states o o of Michoacan and Mexico (19 18'N; 100 09'W; important mining areas in the world is scarce, and there is Fig. 1) (Nieto-Monroy 2007), as part of the Trans- no documented information on possible remnant effects Mexican Volcanic Belt. At an elevation ranging from in reference to wildlife. The Oro-Tl alpujahua Mining District (OTMD) 2600 to 2850 m a.s.l., 45% of its surface is covered in central Mexico has been the site of ecological changes by secondary forest of Cedars (Cupressus lusitanica), Junipers (Juniperus deppeana), oaks (Quercus spp.), and associated with the settlement of a very important center th pines (Pinus spp.). Its climate is temperate sub-humid of gold and silver ore extraction, from the middle 19 to th with rainfall in summer (800–1100 mm per year), early 20 century (Corona-Chávez & Uribe-Salas 2009). Mina Dos Estrellas was an exceptional settlement in its and the soils are mainly represented by andosols and time, whose establishment and operation with major luvisols (INEGI 2009). The OTMD area is ad jacent to the polygons of the Monarch Butterfly Biosph ere infrastructure caused the almost complete deforestation Reserve (MBBR) (Coronado-Martínez 2016). Although of the original forests, and led to the creation of roads, OTDM is not part of the reserve, it has had influenc es landscape alteration, and the accumulation of waste materials from ore extraction, among others. As a result of within the protected area because of historical extraction continued activities, the area gradually accumulated tailings of materials in the past and tourism activities in the present (Ramírez-Ramírez 2001, SEMARNAT 2001, of momentous volume. These el ements have defined the Coronado-Martínez 2016). Due to the limited and environmental history of the region, and have stimulated specific features of the area, the study sites are included interest in understanding the long term consequences of disturbance in the area (Corona-Chávez et al. 2010). only in one site, without replicates. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Figure 1. The Oro-Tlalpujahua Mining District study area in central Mexico (EC = E l Castillo, S ; DE = Mina Dos Estrellas, S ). 1 2 Bird sampling and Howell & Webb (2005). Species considered in any concern category were defined a ccording to Norma Oficial Bird sampling was carried out in two study sites: a) a Mexicana NOM-059-SEMARNAT-2010, where native control site far from tailings (El Castillo, Tlacotepec, species of wild flora and fauna in Mexico considered in o o S ; 19.822 N; -100.145 W, 2750 m a.s.l.; Fig. 2A) and any conservation risk are listed (SEMARNAT 2010). b) a tailings site (Mina Dos Estrellas, Tlalpujahua, S ; o o 19.793 N; 100.156 W, 2648 m a.s.l.; Fig. 2B), both Data analysis within the municipality of Tlalpujahua, Michoacan. Vegetation in both sites resulted from a natural secondary We estimated the relative abundance and frequency of succession process and have similar structure and occurrence of bird species by site. The former was expressed composition (Osuna-Vallejo et al. 2016). To determine by the number of individuals in 100 point counts, and the composition and abundance of bird communities, the latter was evaluated through the percentage of counts every month from June 2014 to June 2015, we conducted where the species was recorded, which can reflect the a total of 369 point counts (10 min) (169 in the control detection probability of the species (Hutto et al. 1986). site S and 200 in the tailings site S ), located randomly We used the Completeness Index (Chao 1 1 2 every 200 m along independent paths, in which we estimator) to make a prediction of the expected species registered individuals detected visually and acoustically in the community based on our sampling (Chao et al. (by songs or calls) within a fixed 50 m radius (to avoid 2005). For each site we generated species accumulation bias due to detectability) (Hutto et al. 1986, Buskirk & curves to ensure sampling effort was adequate and to McDonald 1995). The taxonomic arrangement adopted compare richness among sites (Colwell & Coddington here was that proposed by the American Ornithological 1994). These analyses were performed in EstimateS 9.1.0 Society (AOS 2017), while the assignment of species to (Colwell 2013). seasonality categories was based on our own experience In order to compare the similarity of communities Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Figure 2. Control site, El Castillo, Tlacotepec, Michoacan (A); mining site, Mina Dos Estrellas (B), Photo authors: K.I. Lemus- Ramírez (A) and J.F. Villaseñor-Gómez (B). between sites, we computed the qualitative Sorensen one of the species to the similarity observed between index and the quantitative Morisita-Horn index using communities, and defines the most important species Excel 2013. The former index is based on species presence/ responsible for the observed pattern (Clarke 1993). absence data, and indicates the composition resemblance of the communities; while the latter considers the number RESULTS of individuals registered for each one of the species (Badii et al. 2007). To evaluate differences in species' abundance From June 2014 to June 2015 we conducted a total of 369 between sampling sites we applied a nonparametric point counts (169 in the control site S and 200 in the Mann-Whitney U test using IBM SPSS Statistics 20.0). tailings site S ), and detected a total of 4364 individuals We also used an Analysis of Similarity (ANOSIM) to (S = 2043, S = 2321) from 108 species and 30 families compare the degree of correspondence in the composition 1 2 (S = 97, S = 91); 85 are resident, 20 are winter visitors, of communities (sensu Blake 2007, Edwards et al. 2011); 1 2 two are considered transitory, and one is an introduced as this method evaluates a dissimilarity matrix, values of R resident species (Table 1). We identified ten functional closer to zero reflect very similar communities, and values or guild groups (groups of species in a community that close to unity reflect significant differences between the exploit the same set of resources in a similar manner, but communities being compared (PAST version 2.17 c). are not necessarily closely related taxonomically). In the two In order to gain further information about the species' study sites the insectivorous guild was the most abundant contribution to the differences between communities, we (S = 48% species, 35% individuals; S = 51% species, applied a Similarity Percentage Analysis SIMPER (PAST 1 2 35% individuals), followed by the omnivorous guild (S version 2.17 c), that breaks up the contribution of each Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. = 19% species, 30% individuals; S = 20% species, 23% individuals). In general, the communities showed very similar functional structure (species:  = 1.928, P = 0.993; individuals:  = 2.856, P = 0.970; Fig. 3). Species accumulation curves exhibited an asymptotic behavior suggesting an adequate sampling effort for the detection of most species in the area. The Completeness Index (CI = Sobs/Sest) that is computed along with log-linear 95% confidence intervals (CI), indicated the recording of 96% of species for the OTMD region. The number of estimated species for the control site S was 83% of the species recorded (117 estimated species, IC = 104–157 species), meanwhile for the tailings site S , the estimated species corresponded to 93% of the detected ones (98 estimated species, IC = 93–116 species). Eighteen species were exclusive to the control site S , ten were exclusive to the tailings site S , and 88 species were present in both communities (Table 1). All exclusive species for each site were rare and infrequently recorded. With respect to their relative abundances, our results showed that at the control site S , Ptiliogonys cinereus (Gray Silky-fly catcher), Hylocharis leucotis (White-eared Hummingbird), Spizella passerina (Chipping Sparrow), Regulus calendula (Ruby-crowned Kinglet), and Turdus Figure 3. Bar chart of (A) number of species and (B) migratorius (American Robin) were the most abundant individuals belonging to different guilds at two sites within species. Correspondingly, at the tailings site S , the species 2 the El Oro-Tlalpujahua Mining District area. Legend: C: with the greatest relative abundance were Setophaga Carnivorous, F: Frugivorous, G: Granivorous, I: Insectivorous, coronata (Yellow-rumped Warbler), P. cinereus, H. leucotis, N: Nectarivorous, O: Omnivorous. Table 1. Seasonal status and relative abundances of bird species recorded in a control site and a mining site at El Oro- Tlalpujahua Mining District, central Mexico. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Odontophoridae Colinus virginianus Northern Bobwhite PR 0.59 1.18 NR NR Columbidae Patagioenas fasciata Band-tailed Pigeon PR 0.59 0.59 NR NR Columbina inca Inca Dove PR 5.92 14.20 2.00 5.25 Cuculidae Geococcyx californianus Greater Roadrunner PR 0.59 0.59 NR NR Caprimulgidae Antrostomus arizonae Mexican Whip-poor-will PR NR NR 0.50 0.75 Trochilidae Colibri thalassinus Mexican Violetear PR 4.14 4.73 4.50 6.75 Eugenes fulgens Rivoli's Hummingbird PR 4.73 5.92 4.00 6.75 Lampornis clemenciae Blue-throated Humming. PR 1.78 2.96 2.50 3.75 Archilochus colubris Ruby-throated Humming. TR 1.18 1.18 NR NR Selasphorus platycercus Broad-tailed Hummingbird PR 1.78 1.78 0.50 0.75 Selasphorus rufus Rufous Hummingbird VI 0.59 0.59 0.50 0.75 Amazilia beryllina Berylline Hummingbird PR 0.59 1.18 3.00 6.00 Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name b 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Hylocharis leucotis White-eared Hummingbird PR 63.31 85.21 59.50 128.25 Accipitridae Accipiter cooperii** Cooper's Hawk VI 1.18 1.18 NR NR Buteo jamaicensis Red-tailed Hawk PR 0.59 0.59 NR NR Trogonidae Trogon mexicanus Mountain Trogon PR 4.14 5.92 NR NR Picidae Melanerpes formicivorus Acorn Woodpecker PR 9.47 15.98 18.50 64.50 Picoides scalaris Ladder-backed Woodpeck. PR 6.51 6.51 4.50 6.75 Picoides villosus Hairy Woodpecker PR 3.55 4.14 3.50 5.25 Colaptes auratus Northern Flicker PR 5.33 5.33 0.50 0.75 Tyrannidae Mitrephanes phaeocercus Tufted Flycatcher PR 8.28 8.88 5.50 10.50 Contopus pertinax Greater Pewee PR 14.79 15.98 12.00 18.00 Empidonax affinis Pine Flycatcher PR 0.59 0.59 NR NR Empidonax difficilis Pacific-slope F lycatcher VI 1.18 1.18 NR NR Empidonax occidentalis Cordilleran Flycatcher PR 12.43 13.02 10.00 17.25 Empidonax fulvifrons Buff-breasted F lycatcher PR 1.18 1.18 2.50 4.50 Sayornis nigricans Black Phoebe PR NR NR 0.50 1.50 Sayornis saya Say's Phoebe VI 0.59 1.18 NR NR Pyrocephalus rubinus Vermilion Flycatcher PR 2.96 5.33 0.50 0.75 Myiarchus tuberculifer Dusky-capped Flycatcher PR 1.78 2.37 1.50 3.00 Tyrannus vociferans Cassin's Kingbird PR 5.92 7.69 2.00 3.75 Tityridae Pachyramphus aglaiae Rose-throated Becard PR 0.59 0.59 0.50 1.50 Vireonidae Vireo huttoni Hutton's Vireo PR 5.92 7.10 5.50 9.00 Vireo cassinii Cassin's Vireo VI 4.73 5.92 2.50 4.50 Vireo plumbeus Plumbeous Vireo PR 0.59 0.59 0.50 0.75 Vireo gilvus Warbling Vireo PR 0.59 0.59 0.50 0.75 Corvidae Cyanocitta stelleri Steller's Jay PR 5.33 20.71 1.00 5.25 Corvus corax Common Raven PR NR NR 0.50 0.75 Hirundinidae Tachycineta thalassina Violet-green Swallow PR 0.59 0.59 1.50 2.75 Paridae Poecile sclateri Mexican Chickadee PR 3.55 8.28 1.00 4.50 Baeolophus wollweberi Bridled Titmouse PR NR NR 0.50 1.50 Aegithalidae Psaltriparus minimus Bushtit PR 8.88 56.21 9.00 116.25 Sittidae Sitta carolinensis White-breasted Nuthatch PR 23.08 29.59 12.00 18.75 Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Certhiidae Certhia americana Brown Creeper PR 0.59 0.59 NR NR Troglodytidae Catherpes mexicanus Canyon Wren PR 1.78 1.78 2.00 3.00 Troglodytes aedon parkmani House Wren (in part) VI 7.10 8.28 3.00 5.25 T. aedon brunneicollis House Wren (in part) PR 2.96 2.96 8.50 14.25 Thryomanes bewickii Bewick's Wren PR 10.06 11.83 18.00 34.50 Campylorhynchus gularis Spotted Wren PR 0.59 1.18 NR NR Regulidae Regulus satrapa Golden-crowned Kinglet VI 0.59 0.59 NR NR Regulus calendula Ruby-crowned Kinglet PR 35.50 57.99 29.50 69.00 Turdidae Myadestes occidentalis** Brown-backed Solitaire PR 12.43 15.38 22.50 38.25 Orange-billed Nightingale- Catharus aurantiirostris PR 0.59 0.59 4.00 7.00 Thrush Catharus occidentalis Russet Nightingale-Thrush PR 5.92 6.51 12.00 23.25 Catharus guttatus Hermit Thrush VI 0.59 1.18 NR NR Turdus assimilis White-throated Thrush PR 0.59 0.59 3.00 4.75 Turdus migratorius American Robin PR 33.14 56.80 33.00 86.25 Mimidae Melanotis caerulescens Blue Mockingbird PR 2.96 2.96 11.00 17.75 Toxostoma curvirostre Curve-billed Thrasher PR 7.10 8.88 7.50 12.75 Mimus polyglottos Northern Mockingbird PR NR NR 0.50 0.75 Ptiliogonatidae Ptiliogonys cinereus Gray Silky-fly catcher PR 25.44 99.41 37.50 163.50 Peucedramidae Peucedramus taeniatus Olive Warbler PR 18.93 21.30 13.00 19.50 Passeridae PR/ Passer domesticus House Sparrow 1.18 4.73 0.50 1.50 INTRO Fringillidae Euphonia elegantissima Elegant Euphonia PR NR NR 0.50 1.50 Haemorhous mexicanus House Finch PR 16.57 52.07 19.50 78.75 Spinus pinus Pine Siskin PR 4.14 8.88 3.00 9.75 Spinus psaltria Lesser Goldfinch PR 15.98 52.07 15.50 90.25 Passerellidae Arremon virenticeps Green-striped Brushfinch PR NR NR 0.50 1.50 Atlapetes pileatus Rufous-capped Brushfinch PR 2.96 3.55 3.50 9.00 Pipilo maculatus Spotted Towhee PR 15.38 18.93 20.50 38.25 Aimophila rufescens Rusty Sparrow PR 0.59 0.59 0.50 1.50 Melozone fusca Canyon Towhee PR 15.38 33.73 20.50 44.75 Oriturus superciliosus Striped Sparrow PR 5.33 14.79 NR NR Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name b 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Spizella passerina Chipping Sparrow PR 4.73 60.36 1.50 6.00 Spizella atrogularis Black-chinned Sparrow PR 1.18 2.96 NR NR Melospiza melodia Song Sparrow PR 1.18 1.78 2.50 5.25 Junco phaeonotus Yellow-eyed Junco PR 15.38 34.32 22.00 64.50 Icteridae Sturnella magna Eastern Meadowlark PR 0.59 0.59 NR NR Icterus bullockii Bullock's Oriole PR 2.96 4.14 1.50 3.75 Icterus abeillei Black-backed Oriole PR NR NR 3.00 9.75 Icterus parisorum Scott's Oriole PR 0.59 1.78 1.00 5.25 Molothrus aeneus Bronzed Cowbird PR 0.59 0.59 0.50 1.50 Molothrus ater Brown-headed Cowbird PR 0.59 2.37 0.50 0.75 Parulidae Mniotilta varia Black-and-white Warbler VI 1.78 1.78 1.00 1.50 Oreothlypis superciliosa Crescent-chested Warbler PR 21.30 32.54 13.00 23.25 Oreothlypis celata Orange-crowned Warbler VI 4.73 7.69 10.50 24.00 Oreothlypis crissalis Colima Warbler VI NR NR 1.00 1.50 Oreothlypis ruficapilla Nashville Warbler VI 0.59 0.59 0.50 0.75 Geothlypis tolmiei MacGillivray's Warbler VI NR NR 0.50 0.75 Setophaga ruticilla American Redstart TR 0.59 0.59 NR NR Setophaga coronata Yellow-rumped Warbler VI 17.16 56.21 35.50 168.00 Setophaga graciae Grace's Warbler PR NR NR 0.50 0.75 Setophaga nigrescens Black-throated Gray Warbl. VI 1.78 1.78 2.50 3.75 Setophaga townsendi Townsend's Warbler VI 14.20 33.73 15.50 49.50 Setophaga occidentalis Hermit Warbler VI 9.47 17.75 5.00 11.25 Basileuterus rufifrons Rufous-capped Warbler PR 2.37 2.96 4.50 9.50 Basileuterus belli Golden-browed Warbler PR 4.73 7.10 1.50 3.00 Cardellina pusilla Wilson's Warbler VI 5.92 5.92 7.50 12.00 Cardellina rubrifrons Red-faced Warbler VI NR NR 1.00 2.25 Cardellina rubra Red Warbler PR 2.37 3.55 2.50 5.25 Myioborus pictus Painted Redstart PR 22.49 26.04 12.50 20.25 Myioborus miniatus Slate-throated Redstart PR 2.37 3.55 1.00 1.50 Cardinalidae Piranga flava Hepatic Tanager PR 6.51 6.51 7.50 13.50 Piranga ludoviciana Western Tanager VI 2.96 2.96 1.00 1.50 Piranga bidentata Flame-colored Tanager PR 1.18 1.18 1.00 2.25 Pheucticus melanocephalus Black-headed Grosbeak PR 27.81 38.46 18.50 37.50 Passerina caerulea Blue Grosbeak PR 2.96 5.92 1.50 3.00 Thraupidae Cinnamon-bellied Diglossa baritula PR 1.78 4.73 0.50 0.75 flowerpier cer (a) Common name according to AOS (2017). ** Species under special protection (SEMARNAT 2010). (b) Seasonal status, PR: Permanent resident, VI: Winter visitant, TR: Transitory, INTRO: Introduced. (c) FRE = frequency (probability of presence in point counts; (d) ABU = relative abundance expressed in number of individuals in 100 point counts; (e) NR = Non recorded species. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Psaltriparus minimus (Bushtit) and Spinus psaltria (Lesser communities at the study sites were very similar to one Goldfinch) (Table 1). On the other hand, the species another (as it was also evident with ANOSIM), although with the highest frequency of occurrence in S were some species had clear differences in their abundance in H. leucotis, R. calendula, T. migratorius, P. cinereus and both sites (Table 2), such as S. coronata, M. caerulescens, Myioborus pictus (Painted Redstart); while in S , the most O. superciliosus, C. auratus, and T. mexicanus. frequent species were H. leucotis, P. cinereus, S. coronata, R. calendula, and Myadestes occidentalis (Brown-backed Solitaire) (Table 1). DISCUSSION The Mann-Whitney U test showe d no significant differences in the average number of species and Despite the fact that the OTMD has historically been individuals per count between sites (P > 0.1). However, very important for its economic prosperity, biological there were significant differences in the abundance of 18 inventories in the area are virtually non-existent. This species (Table 2). In reference to the similarity between work provides the first bir d species inventory for Mina sites, the Sorensen index revealed 85% qualitative Dos Estrellas and Tlacotepec, with 108 species (19.7% similarity, while the Morisita-Horn index showed 93% of those registered in the state of Michoacan) (Villaseñor- quantitative similarity. Gómez 2005), and 83% of the species recorded from The Analysis of Similarity (ANOSIM) indicated a Sierra Chincua at MBBR (SEMARNAT 2001), the high level of correspondence between both communities nearest area with available ornithological information. (R = 0.0445, P = 0.0001). On the other hand, the SIMPER According to the NOM-059 (SEMARNAT 2010), two analysis suggested that the few extant differences between species are under special protection: Accipiter cooperi them are attributable to 18 species (Table 3), which add (Cooper's Hawk) and M. occidentalis. up to 62% of the differences between sites. The SIMPER After 65 years of the cessation of extractive mining test gives greater weight to abundance, such that species activities, bird communities at the OTMD have a contributing to the differences between communities are high degree of similarity (85% qualitative and 93% those with the highest number of records. Overall the bird quantitative), a pattern that coincides with the results Table 2. Mean relative abundance of the species with signifi cant differences in abundance between study sites in El Oro- Tlalpujahua, Mining District, during 2014–2015. Individuals Feeding Mean Control Site, Mean Tilings site, Species P recorded guild El Castillo S (EE) Mina Dos Estrellas S (EE) 1 2 Setophaga coronata 145 Omn 0.237 (0.044) 0 (0) 0.001** Myadestes occidentalis 75 Fru 0.147 (0.032) 0.25 (0.034) 0.014* Sitta carolinensis 69 Gra 0.266 (0.042) 0.120 (0.023) 0.008** Myioborus pictus 68 Ins 0.248 (0.037) 0.130 (0.024) 0.010* Oreothlypis superciliosa 67 Ins 0.230 (0.036) 0.140 (0.026) 0.045* Melanerpes formicivorus 61 Omn 0.094 (0.022) 0.225 (0.035) 0.010* Thryomanes bewickii 56 Ins 0.100 (0.023) 0.195 (0.03) 0.028* Catharus occidentalis 40 Fru 0.065 (0.020) 0.145 (0.03) 0.043* Oreothlypis celata 33 Ins 0.059 (0.021) 0.115 (0.024) 0.043* Melanotis caerulescens 28 Ins/Fru 0.029 (0.013) 0.115 (0.023) 0.003** Troglodytes a. brunneicollis. 22 Ins 0.029 (0.013) 0.085 (0.020) 0.025* Cyanocitta stelleri 16 Omn 0.076 (0.027) 0.015 (0.011) 0.015* Tyrannus vociferans 15 Ins 0.065 (0.020) 0.020 (0.010) 0.049* Oriturus superciliosus 12 Omn 0.071 (0.025) 0 (0) 0.001** Catharus aurantiirostris 10 Fru 0.005 (0.005) 0.045 (0.016) 0.035* Colaptes auratus 10 Gra/Ins 0.053 (0.017) 0.005 (0.005) 0.005** Trogon mexicanus 10 Ins/Fru 0.059 (0.024) 0 (0) 0.004** Icterus abeillei 6 Ins 0 (0) 0.030 (0.012) 0.023* (a) Fru: Frugivorous; Gra: Granivorous; Ins: Insectivorous; Omn: Omnivorous. Non-parametric Mann-Whitney U tests: * P < 0.5 and > 0.1, ** P < 0.01; SE = Standard error. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Table 3. Contribution of the bird species to the differences between the communities at the control site and a mining site at El Oro-Tlalpujahua Mining District, central Mexico. Cumulative Species abundance Species abundance Contribution (%) Species percentage of the per count at the per count at the to the difference difference control site mining site Hylocharis leucotis 6.79 6.79 0.75 0.811 Setophaga coronata 5.18 11.97 0.525 0.237 Turdus migratorius 5.16 17.12 0.405 0.438 Ptiliogonys cinereus 4.96 22.08 0.465 0.325 Regulus calendula 4.53 26.61 0.32 0.432 Pheucticus melanocephalus 3.50 30.11 0.21 0.325 Haemorhous mexicanus 3.18 33.29 0.22 0.237 Junco phaeonotus 3.12 36.41 0.23 0.195 Melozone fusca 3.02 39.42 0.215 0.219 Myadestes occidentalis 2.83 42.26 0.25 0.148 Spinus psaltria 2.77 45.03 0.18 0.195 Pipilo maculatus 2.63 47.66 0.23 0.172 Sitta carolinensis 2.59 50.25 0.12 0.266 Myioborus pictus 2.50 52.75 0.13 0.249 Oreothlypis superciliosa 2.47 55.22 0.14 0.231 Setophaga townsendi 2.42 57.64 0.195 0.148 Melanerpes formicivorus 2.30 59.94 0.225 0.0947 Peucedramus taeniatus 2.22 62.16 0.13 0.195 of other studies. In southern Spain, at the Guadiamar Eucalyptus (Eucalyptus marginata) forest, and found that corridor, a severely contaminated environment at the avian communities were very similar after a period of Aznalcollar mine, in restoration since 2000, Márquez- 24 and 30 years, and that the bird communities could Ferrando (2008) found that the composition of bird reach up to 65% similarity within the first 4–5 years of communities exposed to mining waste remnants after abandonment, and 73.5% similarity after 16–17 years. eight years of abandonment was 80% similar to those at According to this, similarity of communities increases natural sites without exposure to mining wastes. Similarly, with time in disturbed environments, where natural Osipov & Biserov (2017) studied the succession of bird regeneration or restoration processes have taken place. communities in a Boreal Mountain-Valley landscape The area of OTMD has gone through a process of disturbed by gold mining in the Niman River (at the natural regeneration, in which those plant species most Bureya mountains, Russia); their findings indicate that tolerant to disturbance, and/or those that were exploited sites with tailings 35–40 years after abandonment were to a lesser extent, reestablished the vegetation on the area, similar in species composition to areas of valleys without and its composition and structure support very similar disturbance, even though density of species was lower in bird communities. The reestablishment of forests with the mining sites. On the other hand, abandoned tailing similar physiognomy in the study site may indicate the sites had a more complex successional vegetation and their presence of suitable resources that maintain similar bird communities of birds were more diverse and abundant, communities at both sites (McArthur & McArthur 1961). as were the mountain forest communities without However, differences in the abundance of 18 species also disturbance. Nichols & Watkins (1984) and Armstrong suggests the existence of specific effects. They might be & Nichols (2000) studied the avifaunal recolonization of related to the sensitivity to pollutants, differences in the rehabilitated bauxite mines in the Jarrah Forest of south- availability of specific resour ces (e.g., food, breeding sites, western Australia. They compared bird communities in feeding territories, perching structures), or other factors a forest where extraction started in 1963 in rehabilitated not taken into account (Loyn 1985, Gould & Mackey Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. 2015). For example, differences found in M. formicivorus Information on remnant effects of abandoned mines might reflect the presence of tall eucalyptus trees and is very scarce. It might prove useful to explore their effects snags at the tailings site (Mina Dos Estrellas), where most on animal communities under scenarios of revegetation individuals were recorded. As suggested, food resources, (natural succession) or restoration. Current information perching structures, and breeding sites can be some of the on mining impacts refers mostly to the response of biotic primary limiting factors in the species distributions and communities in active mining districts, where negative preferences within a given habitat (Cody 1985, Hutto effects have been found on birds, rodents, and vegetation. 1985, Jones 2001). In vertebrates, high concentrations of toxic elements are Studies on the effects of secondary succession in present in kidney and liver tissues, and they relate to their forests have shown that in general, early successional concentrations in the plants on which they feed (Espinosa- bird communities include more generalist granivorous, Reyes et al. 2014). Bioaccumulation of these elements omnivorous and insectivorous species, considered as is known to cause negative effects at the neurological pioneer species indicative of disturbance (Rangel-Salazar (lethargy), physiological (chronic stress and changes in et al. 2009, Becker et al. 2013). As succession progresses, DNA structure), behavioral (decrease of appetite), and structural diversity of vegetation increases and, depending reproductive level (low production of eggs in birds) (Festa on the community composition, specialized frugivorous, et al. 2003, Seewagen 2009, Chapa-Vargas et al. 2010), nectarivorous, and specialized insectivorous species (soil, contributing to the decline of biodiversity at contaminated bark, understory and foliage gleaning) colonize the sites. The rivers of Santa Cruz, San Pedro an d Colorado in habitat and increase in numbers (May 1982, Winkler Sonora, Mexico, which receive flows from copper mines, 2005, Rangel-Salazar et al. 2009). Becker et al. (2013) are very important sites for breeding and wintering birds, found that bird communities in restored mining areas in despite the negative impacts of their low water quality southern Brazil had similar species richness between sites (Sprouse 2005, Villaseñor-Gómez 2006); they have not after 10–20 years of abandonment, although differences been studied in detail. Little is known on the effects of in the abundance of species according to feeding guild potentially toxic elements in tailing residual soils and were evident: granivorous species decreased, whereas their bioavailability. It would be necessary to study tailing carnivorous, frugivorous, and nectarivorous increased chemistry, the exposure paths for those elements, and (especially those forests dependent species); omnivorous bio-magnification effects on functional groups or spe cific species remained stable. Their findings suggest that effects bird species that may be affected at the physiological level could be reflected t hrough changes in functional groups, (Hudson & Bouwman 2008). or can be species specific. In the case of OTMD, some While the establishment of the DMOT historically generalists, omnivorous and ground insectivorous species generated a significant disturbance in the ecosystem, 65 (M. formicivorus, S. coronata, J. phaeonotus and O. celata) years after the end of its activities current conditions seem were significantly more abundant in the tailings site, favorable for the maintenance of avian communities as meanwhile at the control site more specialized species a major component of the regional biodiversity, since such as nectarivorous and bark insectivores prevailed differences at the community level were not remarkable. (H. leucotis, R. calendula, S. carolinensis, M. pictus and Although it is not possible to assess the intensity of the O. superciliosa). Further study is needed to determine environmental effects caused by mining at DMOT in the whether these differences are attributable to the existence past, modification of the natural environment has left of remnant mining effects after 65 years of abandonment. permanent traces, such as soil derived from tailings and Dendrochronological analysis of trees at MBBR the absence of some tree species (such as Sacred Fir, A. suggested that individuals of Sacred Fir (Abies religiosa) religiosa, present in neighboring forests) that were not able are 106 years old, and those of Smooth-bark  Mexican to cope with changes. The relative geochemical stability Pine (Pinus pseudostrobus) are 120 years old. Evidence and the revegetation of tailings may indicate the existence indicates that the MBBR region has also been subjected of low intensity impacts at the present. Although there to historical disturbance regimes caused by logging is no evidence at this time, the bioavailability of some (Sáenz-Ceja 2015). The presence of old railway tracks in potentially toxic elements could trigger processes of bio- the core zone of MBBR at Sierra Chincua supports the magnification in some species, inducing negative health idea of active logging in the past. Probably, regeneration effects on bir d individuals in the region. Therefore, it is processes took place almost at the same time, and, as such, important to continue working on this subject and to the similarities in avian communities between MBBR and analyze some physiological indicators of performance OTMD may reflect the effects of succession in a wider (such as robustness, condition index, fat reserves, and the geographic area. We suggest that OTMD represents an Heterophile/Lymphocyte Index) in local birds, in order important habitat for resident and migratory bird species to evaluate their health and fitness. We also suggest to in the surroundings of MBBR. gain further insights on the role of vegetation structure, Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. C.J., Sauer J.R & Droege S. (eds.). Monitoring bird populations by functional responses of communities (through feeding point counts. Albany: Pacific Southwest Resear ch Station. guilds), and the current anthropogenic impacts that may Cody M.L. 1985. Habitat selection in birds. Orlando: Academic Press. be influencing bir d communities. Colwell R.K. 2013. EstimateS, version 9.1.0: statistical estimation of species richness and shared species from samples. http://purl.oclc.org/ estimates (Access on 05 August 2019). Colwell R.K. & Coddington J.A. 1994. Estimating terrestrial ACKNOWLEDGEMENTS biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London B: Biological Sciences 345: 101–118. This paper is part of the MSc. Dissertation of K.I. Corona-Chávez P. & Uribe-Salas J.A. 2009. Atlas cartográfico del Lemus-Ramírez (Grant 540656, CONACyT-Mexico). Distrito Minero El Oro-Tlalpujahua. Morelia: Universidad Michoacana de San Nicolás de Hidalgo. We recognize the financial support from Universidad Corona-Chávez P., Uribe-Salas J.A., Razo-Perez N., Martínez-Medina Michoacana de San Nicolás de Hidalgo (Coordinación de M., Maldonado-Villanueva R., Ramos-Arroyo Y.R. & Robles- Investigación Científica, Project “Avifauna de la región Camacho J. 2010. The impact of miningin the regional e cosystem: Tlalpujahua-El Oro: estructura de comunidades, uso de the Mining District of El Oro and Tlalpujahua, México. De Re Metallica 15: 21–34. hábitat y expresión de estrés ambiental (2014–2018)”. We Coronado-Martínez Y. 2016. El ecoturismo como opción para el are grateful to the staff of Mina Dos Estrellas (Museo desarrollo local sustentable en el Pueblo Mágico de Tlalpujahua, Técnico Minero Siglo XIX) and Ms. G. Duarte-Godinez Michoacán. MSc. Dissertation. Ciudad de México: Instituto for the permits to work on their property; R.A. Medina Politécnico Nacional. Cristol D.A., Brasso R.L., Condon A.M., Fovargue R.E., Friedman Nieves and J.C. Perez Magaña supported us during field S.L., Hallinger K.K., Monroe A.P. & White A.E. 2008. The activities. We also appreciate the effort and dedication of movement of aquatic mercury through terrestrial food webs. anonymous reviewers who helped to improve this work. Science 320: 335. Chao A., Chazdon R.L., Colwell R.K. & Shen T.J. 2005. A new statistical approach for assessing compositional similarity based on incidence and abundance data. Ecology Letters 8: 148–159. REFERENCES Chapa-Vargas L., Mejía-Saavedra J., Monzalvo-Santos K. & Puebla- Olivares F. 2010. Blood lead concentrations in wild birds from a Altaf M., Javid A., Khan A.M., Khan M.S.H., Umair M. & Ali Z. polluted mining region at Villa de la Paz, San Luis Potosi, Mexico. 2018. Anthropogenic impact on the distribution of the birds in Journal of Environmental Science and Health A 45: 90–98. the tropical thorn forest, Punjab, Pakistan. Journal of Asia-Pacific Eagles-Smith C.A., Wiener J.G., Eckley C.S., Willacker J.J., Evers Biodiversity 11: 229–236. D.C., Marvin-DiPasquale M., Obrist D., Fleck J.A., Aiken G.R., AOS [American Ornithological Society]. 2017. American Lepak J.M., Jackson A.K., Webster J.P., Stewart A.R., Davis J.A., Ornithological Society's check-list of North American birds. http:// Alpers C.N. & Ackerman J.T. 2016. Mercury in western North www.americanornithology.org/content/checklist-north-and- America: a synthesis of environmental contamination, fluxes, middle-american-birds. bioaccumulation, and risk to fish and wildlife. Science of the Total Armstrong K.N. & Nichols O.G. 2000. Long term trends in avifaunal Environment 568: 1213–1226. recolonisation of rehabilitated bauxite mines in the Jarrah Forest Edwards D.P., Larsen T.H., Docherty T.D.S., Ansell F.A., Hsu W.W., of south-western Australia. Forest Ecology and Management 126: Derhé M.A., Hamer K.C. & Wilcove D.S. 2011. Degraded lands 213–225. worth protecting: the biological importance of southeast Asia's Badii M.H., Landeros J. & Cerna E. 2007. Patrones de asociación de repeatedly logged forests. Proceedings of the Royal Society of London especies y sustentabilidad. International Journal of Good Conscience B: Biological Sciences 278: 82–90. 3: 632–660. Eisler R. 2004. Mercury hazards from gold mining to humans, Balistrieri L.S., Box S.E., Bookstrom A.A., Hooper R.L. & Mahoney plants, and animals. Reviews of Environmental Contamination and J.B. 2002. Impacts of historical mining in the Coeur d'Alene River Toxicology 181: 139–198. Basin, p. 1–34. In: Balistrieri L.S. & Stillings L.L. (eds.). Pathways Espinosa-Reyes G., González-Mille D.J., Ilizaliturri-Hernández C.A., of metal transfer from mineralized sources to bioreceptors: a synthesis Mejía-Saavedra J., Cilia-López V.G., Costilla-Salazar R. & Díaz- of the mineral resources program's past environmental studies in the Barriga F. 2014. Effect of mining activities in biotic communities western United States and future research directions. Washington: of Villa de la Paz, San Luis Potosi, Mexico. BioMed Research U.S. Geological Survey. International 2014: 1–13. Balmer O. 2002. Species list in ecology and conservation: abundances Festa F., Cristaldi M., Ieradi L.A., Moreno S. & Cozzi R. 2003. The matter. Conservation Biology 16: 1160–1161. comet assay for the detection of DNA damage in Mus spretus from Batty L.C. 2005. The potential importance of mine sites for Donana National Park. Environmental Research 91: 54–61. biodiversity. Mine Water and the Environment 24: 101–103. Garitano-Zavala A., Cotín J., Borràs M. & Nadal J. 2010. Trace Becker R.G., Paise G. & Pizo M.A. 2013. The stru cture of bird metal concentrations in tissues of two tinamou species in mining communities in areas revegetated after mining in south Brazil. areas of Bolivia and their potential as environmental sentinels. Revista Brasileira de Ornitologia 21: 221–234. Environmental Monitoring and Assessment 168: 629–244. Blake J.G. 2007. Neotropical forest bird communities: a comparison Gonçalves-Rodriguez G. & Shraft B.W. 2001. Review of benthic of species richness and composition at local and region scales. invertebrate fauna in extremely acidic environments (pH ≤ 3). Condor 109: 237–255. Mine Water and the Environment 20: 114–121. Boulet M.P. & Larocque A.C.L. 1988. A comparative mineralogical Gould S.F. & Mackey B.G. 2015. Site vegetation characteristics are and geochemical study of sulfide mine tailings at two sites in New more important than landscape context in determining bird Mexico, U.S.A. Environmental Geology 33: 130–142. assemblages in revegetation. Restoration Ecology 23: 670–680. Buskirk W.H. & McDonald J.L. 1995. Comparison of point count Howell S.N.G. & Webb S. 2005. A guide to the birds of Mexico and sampling regimes for monitoring forest birds, p. 25–34. In: Ralph north Central America. New York: Oxford University Press. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Hudson A. & Bouwman H. 2008. Birds associated with a tailings Osipov S.V. & Biserov M.F. 2017. Population of birds in the Boreal storage facility and surrounding areas from a South African gold Mountain-Valley landscape disturbed by gold mining. Russian mine. African Journal of Ecology 46: 276–281. Journal of Ecology 48: 45–50. Hutto R.L. 1985. Habitat selection by nonbreeding, migratory land Osuna-Vallejo V., Lindig-Cisneros R.A., Sáenz-Romero C. & Cruz- birds, p. 455–476. In: Cody M.L. (ed.). Habitat selection in birds. de-León J. 2016. Ensayo de mesocosmos especies y procedencias Orlando: Academic Press. de coníferas en residuos mineros de Tlalpujahua, Michoacán. XX Hutto R.L., Pletschet S.M. & Hendricks P. 1986. A fixed-radius point Congreso Mexicano de Botánica. Ciudad de México: Sociedad count method for nonbreeding and breeding season use. Auk 103: Botánica de México. 593–602. Ouboter P.E., Landburg G.A., Quik J.H.M., Mol J.H.A. & van del INEGI [Instituto Nacional de Estadística, Geografía e Informática]. Lugt F. 1999. Mercury levels in pristine and gold mining impacted 2009. Prontuario de información geográfica municipal de aquatic ecosystems of Suriname, South America. AMBIO 41: los Estados Unidos Mexicanos: clave geoestadística 16093. 873–882. http://www3.inegi.org.mx/sistemas/mexic ocifras/datos- Pérez-Tris J. 1999. El peso de las aves en paso: ¿Una medida de geograficos/16/16093.pdf. (Access on 10 January 2016). condición física o acumulación de grasa? Revista de Anillamiento Jacob D.L. & Otte M.L. 2004. Long-term effects of submergence and 3: 11–15. wetland vegetation on metals in a 90-year old abandoned Pb-Zn Perotti M., Petrini R., D'Orazio M., Ghezzi L., Giannecchini R. & mine tailings pond. Environmental Pollution 130: 337–345. Vezzoni S. 2017. Thallium and other potentially toxic e lements Jones J. 2001. Habitat selection studies in avian ecology: a critical in the Baccatoio stream catchment (northern Tuscany, Italy) review. Auk 118: 557–562. receiving drainages from abandoned mines. Mine Water and the Kossoff D., Dubbin W.E., Alfredsson M., E dwards S.J., Macklin Environment 37: 1–11. M.G. & Hudson-Edwards K.A. 2014. Mine tailings dams: Pickett S.T.A. & White P.S. 1985. The ecology of natural disturbance characteristics, failure, environmental impacts, and remediation. and patch dynamics. Cambridge: Academic Press. Applied Geochemistry 51: 229–245. Ramírez-Ramírez M.I. 2001. Los espacios forestales de la Sierra de Angangueo Lacerda L.D. 1997. Global mercury emissions from gold and silver (estados de Michoacán y México), México: una revisión geográfica. P h.D. mining. Water, Air, & Soil Pollution 97: 209–221. Thesis. Mad rid: Universidad Complutense de Madrid. Lefcort H., Meguire R.A., Wilson L.H. & Ettinger W.F. 1988. Rangel-Salazar J.L., Enríquez P.L. & Sántiz-López E.C. 2009. Heavy metals alter the survival, growth, metamorphosis, and Variación de la diversidad de aves de sotobosque en el Parque antipredatory behavior of Columbia Spotted Frog (Rana Nacional Lagos de Motebello, Chiapas, México. Acta Zoológica luteiventris) tadpoles. Archives of Environmental Contamination Mexicana 25: 479–495. and Toxicology 35: 447–456. Rösner U. 1988. Effects of historical mining activities on surface Lock K., Janssens F. & Janssen C.R. 2003. Effects of metal water and groundwater: an example from northwest Arizona. contamination on the activity and diversity of springtails in an Environmental Geology 33: 224–230. ancient Pb-Zn mining area at Plombières, Belgium. European Rubio I., Martinez-Madrid M., Mendez-Fernandez L., Galarza A. & Journal of Soil Biology 39: 25–29. Rodriguez P. 2016. Heavy metal concentration in feathers of Little Loyn R.H. 1985. Bird population in successional forest of Mountain Egret (Egretta garzetta) nestlings in three coastal breeding colonies Ash Eucalyptus regnans in central Victoria. Emu 85: 213–231. in Spain. Ecotoxicology 25: 30–40. Mahmoud S.H. & Gan T.Y. 2018. Impact of anthropogenic climate Sáenz-Ceja J.E. 2015. Recostrucción dendrocronológica de la historia change and human activities on environment and ecosystem de establecimiento de Pinus pseudostrobus y Abies religiosa en services in arid regions. Science of the Total Environment 633: la Reserva de la Biosfera Mariposa Monarca. Ciudad de México: 1329–1344. Instituto de Investigaciones en Ecosistemas y Sustentabilidad. Manson R.H. & Jardel-Peláez E.J. 2009. Perturbaciones y desastres Seewagen C.L. 2009. Threats of environmental mer cury to birds: naturales: impactos sobre las ecorregiones, la biodiversidad y el knowledge gaps and priorities for future research. Bird Conservation bienestar socioeconómico, p. 131–184. In: Sarukán J. (ed.). International 20: 112–123. Capital Natural de México, v. 2: estado de conservación y tendencias SEMARNAT [Secretaría de Medio Ambiente y Recursos Naturales]. de cambio. Ciudad de México: CONABIO. 2001. Programa de manejo de la Reserva de la Biosfera Mariposa Márquez-Ferrando R. 2008. Las comunidades de aves y reptiles del Monarca. Ciudad de México: CONANP. corridor Verde del Guadiamar después del vertido minero de SEMARNAT [Secretaría de Medio Ambiente y Recursos Naturales]. Aznalcóllar. MSc. Dissertation. Granada: Universidad de Granada. 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010 May P.G. 1982. Secondary succession and breeding bird community de 30 de Diciembre del 2010. http://www.profepa.gob.mx/ structure: patterns of resource utilization. Oecologia 55: 208–216. innovaportal/file/435/1/NOM_059_SEMARNAT_2010.pdf McArthur R.H. & McArthur J.W. 1961. On bird species diversty. (Access on 02 April 2017). Ecology 42: 594–598. Sprouse T.W. 2005. Water issue on the Arizona-Mexico border. Tucson: Muñiz-Castro M.A. 2008. Sucesión secundaria y establecimiento de Water Resources Research Center. especies arbóreas nativas para restauración de Bosque Mesófilo de Struckhoff M.A., Stroh E.D. & Grabner K.W. 2013. Effects of mining- Montaña en potreros abandonados del centro de Veracruz. Ph.D. associated lead and zinc soil contamination on native floristic Thesis. Xalapa: Instituto de E cología A.C. quality. Journal of Environmental Management 119: 20–28. Nichols O.G. & Watkins D. 1984. Bird utilization of rehabilitated Ugalde-Lezama S., Alcántara-Carbajal J.L., Tarango-Arámbula bauxite minesites in western Australia. Biological Conservation 30: L.A., Ramírez-Valverde G. & Mendoza-Martínez G.D. 2012. 109–131. Fisonomía vegetal y abundancia de aves en un bosque templado Nieto-Monroy A.P. 2007. Variabilidad espacial y temporal de la con dos niveles de perturbación en el Eje Neovolcánico T ransversal. Hidrogeoquímica de arroyos del Distrito Minero El Oro-Tlalpujahua. Revista Mexicana de Biodiversidad 83: 133–143. Ph.D. Thesis. Guanajuato: Universidad de Guanajuato. Ventakeswarlu K., Nirola R., Kuppusamy S., Thavamani P., Naidu R. O'Sullivan A.D., McCabe O.M., Murray D.A. & Otte M.L. 1999. & Megharaj M. 2016. Abandoned metalliferous mines: ecological Wetlands for rehabilitation of metal mine wastes. Proceedings of impacts and potential approaches for reclamation. Reviews in the Royal Irish Academy B: Biology and Environment 99: 11–17. Environmental Science and Bio/Technology 15: 327–354. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Villaseñor-Gómez L.E. 2005. Aves, p. 101–103. In: Villaseñor-Gómez in deciduous and coniferous forest in the Sopron Mountains, L.E. & Leal-Nares O.A. (eds.). La biodiversidad en Michoacán. Hungary. Acta Silvatica et Lignaria Hungarica 1: 49–58. Estudio de estado. Ciudad de México: Comisión Nacional para el Xu X., Xie Y., Qi K., Luo Z. & Wang X. 2018. Detecting the Conocimiento y Uso de la Biodiversidad. response of bird communities and biodiversity to habitat loss Villaseñor-Gómez J.F. 2006. Habitat use and the effects of disturbance and fragmentation due to urbanization. Science of the Total on wintering birds using riparian habitats in Sonora, Mexico. Ph.D. Environment 624: 1561–1576. Thesis. Missoula: University of Montana. Winkler D. 2005. Ecological succession of breeding bird communities Associate Editor: Marcos P. Dantas. Revista Brasileira de Ornitologia 27(2): 2019 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Temperate forest bird communities associated with a historic mining impact area: do tailing remnant effects modify their structure?

Loading next page...
 
/lp/springer-journals/temperate-forest-bird-communities-associated-with-a-historic-mining-HERJFmvbZQ

References (77)

Publisher
Springer Journals
Copyright
Copyright © Sociedade Brasileira de Ornitologia 2019
eISSN
2178-7875
DOI
10.1007/bf03544453
Publisher site
See Article on Publisher Site

Abstract

Revista Brasileira de Ornitologia 27(2): 94–107. ARTICLE June 2019 Temperate forest bird communities associated with a historic mining impact area: do tailing remnant effects modify their structure? 1 1,2 1 Katia Lemus , José Fernando Villaseñor-Gómez , Francisco Roberto Pineda-Huerta & Javier Salgado-Ortiz Laboratorio de Investigación en Ornitología, Facultad de Biología, Universidad Michoacana de San Nicolás de Hidalgo, Ciudad Universitaria, Morelia, Michoacán, Mexico. Corresponding author: jfvillasenorg@hotmail.com Received on 21 February 2019. Accepted on 04 June 2019. ABSTRACT: Birds contribute to the stability of ecosystems and represent a tool used to evaluate a variety of anthropogenic impacts. The area known as E l Oro-Tlalpujahua Mining District in central Mexico was subjected to significant environmental impacts as a result of ore extraction, including profound habitat transformations, landscape changes, and the accumulation of potentially toxic elements in their tailings (favoring its bioavailability and dispersion). After more than 60 years without extractive activities, there is no knowledge on extant remaining impacts on biological communities. Assuming the presence of negative impacts on birds, we compared the composition and abundance of bird communities in two locations, representing a site without exposure to tailings (S ) and another one with tailings deposition (S ). From June 2014 to June 2015, we recorded 2828 individuals of 108 avian species 1 2 in 369 point counts (S = 91, S = 95). The Chao1 indicator suggested we re corded 96% of the species present. We found a high 1 2 similarity in the general composition and abundance of bird species between communities (> 85%). However, there were significant differences in the abundances of 18 species (9 of them higher in the control site); these differences might result from differential effects of potentially toxic e lements on functional groups (such as feeding guilds), resource availability, as well as other factors not accounted for. Historically, mining activities in the area generated significant changes in the structure and composition of the forest, and disrupted ecological processes. Despite the fact that current conditions appear favorable to the relative stability of the bird community, specific p hysiological effects on some species of bir ds sixty years after the cessation of mineral extraction could occur. Further studies on physiological performance and the effects of potentially toxic e lements on local birds could unveil unknown effects at the individual level. KEY-WORDS: avian communities, diversity, El Oro-Tlalpujahua Mining District, mining tailings, remnant effects. INTRODUCTION composition of animal communities (Pickett & White 1985). In birds, these types of changes have been described Information on the diversity and abundance of species in previously by Ugalde-Lezama et al. (2012) and Manson communities represent the basis for assessing the quality & Jardel-Peláez (2009), who found the simplification of of their environment. Through monitoring it is possible to forest structure related to the decrease in the composition evaluate changes associated with different causal factors; of bird communities. comparisons on the occurrence of species in different To evaluate anthropogenic impacts on wildlife, it is environments, and the characterization of their relative desirable to have an indicator of the intensity and extent abundance is often presented as supporting evidence of the impacts; if significant, they might be reflected (Balmer 2002). in changes in the composition and/or abundance of Disturbance processes generated by human activities species at the community level. At the population level, involve habitat changes through the modification of impacts may be reflected in changes in survival rates land use for productive activities (e.g., agriculture and or reproductive success of species, or changes in their livestock), urban development, and mining activities, with distribution (Altaf et al. 2018, Mahmoud & Gan 2018, the resulting effects on soil and water (Manson & Jar del- Xu et al. 2018). Responses at the individual level are the Peláez 2009). These events at the landscape level modify most sensitive and usually have been assessed through the structure of vegetation and generate successional changes in physical and physiological conditions (e.g., processes that promote changes in the structure and height, weight, condition index, quantity of fat reserves) Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. During the 65 years after cessation of activities in (Pérez-Tris 1999). Few studies have explored the response Mina Dos Estrellas, the region has experienced ecological of birds to anthropogenic impacts resulting from mining succession that led to the reestablishment of secondary at the community level; most have focused on particular species (e.g., Garitano-Zavala et al. 2010, Rubio et al. temperate forest made up of tolerant and pioneer 2016), or ecological settings (e.g., Ouboter et al. 1999, tree species that survived the disturbance period on impoverished soil conditions (Muñiz-Castro 2008). Eagles-Smith et al. 2016). Because of the demands of wood and other Several authors recognize the need for environmental materials for the construction and maintenance of mine monitoring from geological, ecological, and public health perspectives (Boulet & Larocque 1988, Perotti et al. galleries, the surrounding areas, and even those far away 2017). Reclamation mining sites have sometimes been were also overexploited (Corona-Chávez & Uribe-Salas 2009). While the area was subjected to a strong mining perceived as sites potentially important for biodiversity impact, at the end of the mine's active life some nearby (Batty 2005). Mines that have operated for centuries are areas remained free from the effects of ore wastes, the source of pollutants that remain stored in tailings or the bottom of reservoirs, and their ecological effects deforestation, agriculture and cattle grazing. These areas in most cases have not been determined (Kossoff et al. offer the possibility of investigating if some remnant effects derived from mining in the past are maintained 2014). Globally, estimations of mercury released to the and affect bird communities. Considering the possibilities environment as a byproduct of the amalgamation for of extant impacts, we analyzed and compared the richness recovery of gold and silver indicate that there has been over 260,000 tons released between 1550 and 1930 (Lacerda and abundance of forest bird communities inhabiting 1997). Furthermore, for mining sites that historically tailings sites (abandoned approximately 65 years ago) and sites free from mine wastes, in order to determine ceased production and left a legacy of ecological impact, differences that might be indicative of remnant impacts little is known about the span and intensity of their on the avifauna. Facing a possible scenario of intense impacts (Balistrieri et al. 2002, Eisler 2004, Cristol et al. 2008, Ventakeswarlu et al. 2016). Some studies have and prolonged impact induced by the bioavailability of addressed aspects of geodynamics, bioavailability and potentially toxic elements in tailings, we expected bird communities away from tailings to be more diverse and transfer of elements in mine tailings, which are potentially have higher abundance at least for the most common toxic elements derived from mining runoff and water species, in comparison to the polluted area. currents (e.g., Rösner 1988, Perotti et al. 2017), as well as on soil and vegetation (O'Sullivan et al. 1999, Jacob & Otte 2004, Struckhoff et al. 2013), aquatic and terrestrial METHODS animals (such as benthic invertebrates, springtail insects, fish, amphibians, reptiles and birds), remediation, and Study area ecological restoration (Lefcort et al. 1988, Gonçalves- Rodriguez & Shraft 2001, Lock et al. 2003, Cristol et al. 2008, Márquez-Ferrando 2008). Data from historically The OTMD is situated in the limits of the states o o of Michoacan and Mexico (19 18'N; 100 09'W; important mining areas in the world is scarce, and there is Fig. 1) (Nieto-Monroy 2007), as part of the Trans- no documented information on possible remnant effects Mexican Volcanic Belt. At an elevation ranging from in reference to wildlife. The Oro-Tl alpujahua Mining District (OTMD) 2600 to 2850 m a.s.l., 45% of its surface is covered in central Mexico has been the site of ecological changes by secondary forest of Cedars (Cupressus lusitanica), Junipers (Juniperus deppeana), oaks (Quercus spp.), and associated with the settlement of a very important center th pines (Pinus spp.). Its climate is temperate sub-humid of gold and silver ore extraction, from the middle 19 to th with rainfall in summer (800–1100 mm per year), early 20 century (Corona-Chávez & Uribe-Salas 2009). Mina Dos Estrellas was an exceptional settlement in its and the soils are mainly represented by andosols and time, whose establishment and operation with major luvisols (INEGI 2009). The OTMD area is ad jacent to the polygons of the Monarch Butterfly Biosph ere infrastructure caused the almost complete deforestation Reserve (MBBR) (Coronado-Martínez 2016). Although of the original forests, and led to the creation of roads, OTDM is not part of the reserve, it has had influenc es landscape alteration, and the accumulation of waste materials from ore extraction, among others. As a result of within the protected area because of historical extraction continued activities, the area gradually accumulated tailings of materials in the past and tourism activities in the present (Ramírez-Ramírez 2001, SEMARNAT 2001, of momentous volume. These el ements have defined the Coronado-Martínez 2016). Due to the limited and environmental history of the region, and have stimulated specific features of the area, the study sites are included interest in understanding the long term consequences of disturbance in the area (Corona-Chávez et al. 2010). only in one site, without replicates. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Figure 1. The Oro-Tlalpujahua Mining District study area in central Mexico (EC = E l Castillo, S ; DE = Mina Dos Estrellas, S ). 1 2 Bird sampling and Howell & Webb (2005). Species considered in any concern category were defined a ccording to Norma Oficial Bird sampling was carried out in two study sites: a) a Mexicana NOM-059-SEMARNAT-2010, where native control site far from tailings (El Castillo, Tlacotepec, species of wild flora and fauna in Mexico considered in o o S ; 19.822 N; -100.145 W, 2750 m a.s.l.; Fig. 2A) and any conservation risk are listed (SEMARNAT 2010). b) a tailings site (Mina Dos Estrellas, Tlalpujahua, S ; o o 19.793 N; 100.156 W, 2648 m a.s.l.; Fig. 2B), both Data analysis within the municipality of Tlalpujahua, Michoacan. Vegetation in both sites resulted from a natural secondary We estimated the relative abundance and frequency of succession process and have similar structure and occurrence of bird species by site. The former was expressed composition (Osuna-Vallejo et al. 2016). To determine by the number of individuals in 100 point counts, and the composition and abundance of bird communities, the latter was evaluated through the percentage of counts every month from June 2014 to June 2015, we conducted where the species was recorded, which can reflect the a total of 369 point counts (10 min) (169 in the control detection probability of the species (Hutto et al. 1986). site S and 200 in the tailings site S ), located randomly We used the Completeness Index (Chao 1 1 2 every 200 m along independent paths, in which we estimator) to make a prediction of the expected species registered individuals detected visually and acoustically in the community based on our sampling (Chao et al. (by songs or calls) within a fixed 50 m radius (to avoid 2005). For each site we generated species accumulation bias due to detectability) (Hutto et al. 1986, Buskirk & curves to ensure sampling effort was adequate and to McDonald 1995). The taxonomic arrangement adopted compare richness among sites (Colwell & Coddington here was that proposed by the American Ornithological 1994). These analyses were performed in EstimateS 9.1.0 Society (AOS 2017), while the assignment of species to (Colwell 2013). seasonality categories was based on our own experience In order to compare the similarity of communities Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Figure 2. Control site, El Castillo, Tlacotepec, Michoacan (A); mining site, Mina Dos Estrellas (B), Photo authors: K.I. Lemus- Ramírez (A) and J.F. Villaseñor-Gómez (B). between sites, we computed the qualitative Sorensen one of the species to the similarity observed between index and the quantitative Morisita-Horn index using communities, and defines the most important species Excel 2013. The former index is based on species presence/ responsible for the observed pattern (Clarke 1993). absence data, and indicates the composition resemblance of the communities; while the latter considers the number RESULTS of individuals registered for each one of the species (Badii et al. 2007). To evaluate differences in species' abundance From June 2014 to June 2015 we conducted a total of 369 between sampling sites we applied a nonparametric point counts (169 in the control site S and 200 in the Mann-Whitney U test using IBM SPSS Statistics 20.0). tailings site S ), and detected a total of 4364 individuals We also used an Analysis of Similarity (ANOSIM) to (S = 2043, S = 2321) from 108 species and 30 families compare the degree of correspondence in the composition 1 2 (S = 97, S = 91); 85 are resident, 20 are winter visitors, of communities (sensu Blake 2007, Edwards et al. 2011); 1 2 two are considered transitory, and one is an introduced as this method evaluates a dissimilarity matrix, values of R resident species (Table 1). We identified ten functional closer to zero reflect very similar communities, and values or guild groups (groups of species in a community that close to unity reflect significant differences between the exploit the same set of resources in a similar manner, but communities being compared (PAST version 2.17 c). are not necessarily closely related taxonomically). In the two In order to gain further information about the species' study sites the insectivorous guild was the most abundant contribution to the differences between communities, we (S = 48% species, 35% individuals; S = 51% species, applied a Similarity Percentage Analysis SIMPER (PAST 1 2 35% individuals), followed by the omnivorous guild (S version 2.17 c), that breaks up the contribution of each Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. = 19% species, 30% individuals; S = 20% species, 23% individuals). In general, the communities showed very similar functional structure (species:  = 1.928, P = 0.993; individuals:  = 2.856, P = 0.970; Fig. 3). Species accumulation curves exhibited an asymptotic behavior suggesting an adequate sampling effort for the detection of most species in the area. The Completeness Index (CI = Sobs/Sest) that is computed along with log-linear 95% confidence intervals (CI), indicated the recording of 96% of species for the OTMD region. The number of estimated species for the control site S was 83% of the species recorded (117 estimated species, IC = 104–157 species), meanwhile for the tailings site S , the estimated species corresponded to 93% of the detected ones (98 estimated species, IC = 93–116 species). Eighteen species were exclusive to the control site S , ten were exclusive to the tailings site S , and 88 species were present in both communities (Table 1). All exclusive species for each site were rare and infrequently recorded. With respect to their relative abundances, our results showed that at the control site S , Ptiliogonys cinereus (Gray Silky-fly catcher), Hylocharis leucotis (White-eared Hummingbird), Spizella passerina (Chipping Sparrow), Regulus calendula (Ruby-crowned Kinglet), and Turdus Figure 3. Bar chart of (A) number of species and (B) migratorius (American Robin) were the most abundant individuals belonging to different guilds at two sites within species. Correspondingly, at the tailings site S , the species 2 the El Oro-Tlalpujahua Mining District area. Legend: C: with the greatest relative abundance were Setophaga Carnivorous, F: Frugivorous, G: Granivorous, I: Insectivorous, coronata (Yellow-rumped Warbler), P. cinereus, H. leucotis, N: Nectarivorous, O: Omnivorous. Table 1. Seasonal status and relative abundances of bird species recorded in a control site and a mining site at El Oro- Tlalpujahua Mining District, central Mexico. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Odontophoridae Colinus virginianus Northern Bobwhite PR 0.59 1.18 NR NR Columbidae Patagioenas fasciata Band-tailed Pigeon PR 0.59 0.59 NR NR Columbina inca Inca Dove PR 5.92 14.20 2.00 5.25 Cuculidae Geococcyx californianus Greater Roadrunner PR 0.59 0.59 NR NR Caprimulgidae Antrostomus arizonae Mexican Whip-poor-will PR NR NR 0.50 0.75 Trochilidae Colibri thalassinus Mexican Violetear PR 4.14 4.73 4.50 6.75 Eugenes fulgens Rivoli's Hummingbird PR 4.73 5.92 4.00 6.75 Lampornis clemenciae Blue-throated Humming. PR 1.78 2.96 2.50 3.75 Archilochus colubris Ruby-throated Humming. TR 1.18 1.18 NR NR Selasphorus platycercus Broad-tailed Hummingbird PR 1.78 1.78 0.50 0.75 Selasphorus rufus Rufous Hummingbird VI 0.59 0.59 0.50 0.75 Amazilia beryllina Berylline Hummingbird PR 0.59 1.18 3.00 6.00 Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name b 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Hylocharis leucotis White-eared Hummingbird PR 63.31 85.21 59.50 128.25 Accipitridae Accipiter cooperii** Cooper's Hawk VI 1.18 1.18 NR NR Buteo jamaicensis Red-tailed Hawk PR 0.59 0.59 NR NR Trogonidae Trogon mexicanus Mountain Trogon PR 4.14 5.92 NR NR Picidae Melanerpes formicivorus Acorn Woodpecker PR 9.47 15.98 18.50 64.50 Picoides scalaris Ladder-backed Woodpeck. PR 6.51 6.51 4.50 6.75 Picoides villosus Hairy Woodpecker PR 3.55 4.14 3.50 5.25 Colaptes auratus Northern Flicker PR 5.33 5.33 0.50 0.75 Tyrannidae Mitrephanes phaeocercus Tufted Flycatcher PR 8.28 8.88 5.50 10.50 Contopus pertinax Greater Pewee PR 14.79 15.98 12.00 18.00 Empidonax affinis Pine Flycatcher PR 0.59 0.59 NR NR Empidonax difficilis Pacific-slope F lycatcher VI 1.18 1.18 NR NR Empidonax occidentalis Cordilleran Flycatcher PR 12.43 13.02 10.00 17.25 Empidonax fulvifrons Buff-breasted F lycatcher PR 1.18 1.18 2.50 4.50 Sayornis nigricans Black Phoebe PR NR NR 0.50 1.50 Sayornis saya Say's Phoebe VI 0.59 1.18 NR NR Pyrocephalus rubinus Vermilion Flycatcher PR 2.96 5.33 0.50 0.75 Myiarchus tuberculifer Dusky-capped Flycatcher PR 1.78 2.37 1.50 3.00 Tyrannus vociferans Cassin's Kingbird PR 5.92 7.69 2.00 3.75 Tityridae Pachyramphus aglaiae Rose-throated Becard PR 0.59 0.59 0.50 1.50 Vireonidae Vireo huttoni Hutton's Vireo PR 5.92 7.10 5.50 9.00 Vireo cassinii Cassin's Vireo VI 4.73 5.92 2.50 4.50 Vireo plumbeus Plumbeous Vireo PR 0.59 0.59 0.50 0.75 Vireo gilvus Warbling Vireo PR 0.59 0.59 0.50 0.75 Corvidae Cyanocitta stelleri Steller's Jay PR 5.33 20.71 1.00 5.25 Corvus corax Common Raven PR NR NR 0.50 0.75 Hirundinidae Tachycineta thalassina Violet-green Swallow PR 0.59 0.59 1.50 2.75 Paridae Poecile sclateri Mexican Chickadee PR 3.55 8.28 1.00 4.50 Baeolophus wollweberi Bridled Titmouse PR NR NR 0.50 1.50 Aegithalidae Psaltriparus minimus Bushtit PR 8.88 56.21 9.00 116.25 Sittidae Sitta carolinensis White-breasted Nuthatch PR 23.08 29.59 12.00 18.75 Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Certhiidae Certhia americana Brown Creeper PR 0.59 0.59 NR NR Troglodytidae Catherpes mexicanus Canyon Wren PR 1.78 1.78 2.00 3.00 Troglodytes aedon parkmani House Wren (in part) VI 7.10 8.28 3.00 5.25 T. aedon brunneicollis House Wren (in part) PR 2.96 2.96 8.50 14.25 Thryomanes bewickii Bewick's Wren PR 10.06 11.83 18.00 34.50 Campylorhynchus gularis Spotted Wren PR 0.59 1.18 NR NR Regulidae Regulus satrapa Golden-crowned Kinglet VI 0.59 0.59 NR NR Regulus calendula Ruby-crowned Kinglet PR 35.50 57.99 29.50 69.00 Turdidae Myadestes occidentalis** Brown-backed Solitaire PR 12.43 15.38 22.50 38.25 Orange-billed Nightingale- Catharus aurantiirostris PR 0.59 0.59 4.00 7.00 Thrush Catharus occidentalis Russet Nightingale-Thrush PR 5.92 6.51 12.00 23.25 Catharus guttatus Hermit Thrush VI 0.59 1.18 NR NR Turdus assimilis White-throated Thrush PR 0.59 0.59 3.00 4.75 Turdus migratorius American Robin PR 33.14 56.80 33.00 86.25 Mimidae Melanotis caerulescens Blue Mockingbird PR 2.96 2.96 11.00 17.75 Toxostoma curvirostre Curve-billed Thrasher PR 7.10 8.88 7.50 12.75 Mimus polyglottos Northern Mockingbird PR NR NR 0.50 0.75 Ptiliogonatidae Ptiliogonys cinereus Gray Silky-fly catcher PR 25.44 99.41 37.50 163.50 Peucedramidae Peucedramus taeniatus Olive Warbler PR 18.93 21.30 13.00 19.50 Passeridae PR/ Passer domesticus House Sparrow 1.18 4.73 0.50 1.50 INTRO Fringillidae Euphonia elegantissima Elegant Euphonia PR NR NR 0.50 1.50 Haemorhous mexicanus House Finch PR 16.57 52.07 19.50 78.75 Spinus pinus Pine Siskin PR 4.14 8.88 3.00 9.75 Spinus psaltria Lesser Goldfinch PR 15.98 52.07 15.50 90.25 Passerellidae Arremon virenticeps Green-striped Brushfinch PR NR NR 0.50 1.50 Atlapetes pileatus Rufous-capped Brushfinch PR 2.96 3.55 3.50 9.00 Pipilo maculatus Spotted Towhee PR 15.38 18.93 20.50 38.25 Aimophila rufescens Rusty Sparrow PR 0.59 0.59 0.50 1.50 Melozone fusca Canyon Towhee PR 15.38 33.73 20.50 44.75 Oriturus superciliosus Striped Sparrow PR 5.33 14.79 NR NR Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. El Castillo Mina Dos Estrellas Family Seasonal (S Control site) (S Mining site) Common name b 1 2 status c d c d Species FRE S ABU S FRE S ABU S 1 1 2 2 Spizella passerina Chipping Sparrow PR 4.73 60.36 1.50 6.00 Spizella atrogularis Black-chinned Sparrow PR 1.18 2.96 NR NR Melospiza melodia Song Sparrow PR 1.18 1.78 2.50 5.25 Junco phaeonotus Yellow-eyed Junco PR 15.38 34.32 22.00 64.50 Icteridae Sturnella magna Eastern Meadowlark PR 0.59 0.59 NR NR Icterus bullockii Bullock's Oriole PR 2.96 4.14 1.50 3.75 Icterus abeillei Black-backed Oriole PR NR NR 3.00 9.75 Icterus parisorum Scott's Oriole PR 0.59 1.78 1.00 5.25 Molothrus aeneus Bronzed Cowbird PR 0.59 0.59 0.50 1.50 Molothrus ater Brown-headed Cowbird PR 0.59 2.37 0.50 0.75 Parulidae Mniotilta varia Black-and-white Warbler VI 1.78 1.78 1.00 1.50 Oreothlypis superciliosa Crescent-chested Warbler PR 21.30 32.54 13.00 23.25 Oreothlypis celata Orange-crowned Warbler VI 4.73 7.69 10.50 24.00 Oreothlypis crissalis Colima Warbler VI NR NR 1.00 1.50 Oreothlypis ruficapilla Nashville Warbler VI 0.59 0.59 0.50 0.75 Geothlypis tolmiei MacGillivray's Warbler VI NR NR 0.50 0.75 Setophaga ruticilla American Redstart TR 0.59 0.59 NR NR Setophaga coronata Yellow-rumped Warbler VI 17.16 56.21 35.50 168.00 Setophaga graciae Grace's Warbler PR NR NR 0.50 0.75 Setophaga nigrescens Black-throated Gray Warbl. VI 1.78 1.78 2.50 3.75 Setophaga townsendi Townsend's Warbler VI 14.20 33.73 15.50 49.50 Setophaga occidentalis Hermit Warbler VI 9.47 17.75 5.00 11.25 Basileuterus rufifrons Rufous-capped Warbler PR 2.37 2.96 4.50 9.50 Basileuterus belli Golden-browed Warbler PR 4.73 7.10 1.50 3.00 Cardellina pusilla Wilson's Warbler VI 5.92 5.92 7.50 12.00 Cardellina rubrifrons Red-faced Warbler VI NR NR 1.00 2.25 Cardellina rubra Red Warbler PR 2.37 3.55 2.50 5.25 Myioborus pictus Painted Redstart PR 22.49 26.04 12.50 20.25 Myioborus miniatus Slate-throated Redstart PR 2.37 3.55 1.00 1.50 Cardinalidae Piranga flava Hepatic Tanager PR 6.51 6.51 7.50 13.50 Piranga ludoviciana Western Tanager VI 2.96 2.96 1.00 1.50 Piranga bidentata Flame-colored Tanager PR 1.18 1.18 1.00 2.25 Pheucticus melanocephalus Black-headed Grosbeak PR 27.81 38.46 18.50 37.50 Passerina caerulea Blue Grosbeak PR 2.96 5.92 1.50 3.00 Thraupidae Cinnamon-bellied Diglossa baritula PR 1.78 4.73 0.50 0.75 flowerpier cer (a) Common name according to AOS (2017). ** Species under special protection (SEMARNAT 2010). (b) Seasonal status, PR: Permanent resident, VI: Winter visitant, TR: Transitory, INTRO: Introduced. (c) FRE = frequency (probability of presence in point counts; (d) ABU = relative abundance expressed in number of individuals in 100 point counts; (e) NR = Non recorded species. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Psaltriparus minimus (Bushtit) and Spinus psaltria (Lesser communities at the study sites were very similar to one Goldfinch) (Table 1). On the other hand, the species another (as it was also evident with ANOSIM), although with the highest frequency of occurrence in S were some species had clear differences in their abundance in H. leucotis, R. calendula, T. migratorius, P. cinereus and both sites (Table 2), such as S. coronata, M. caerulescens, Myioborus pictus (Painted Redstart); while in S , the most O. superciliosus, C. auratus, and T. mexicanus. frequent species were H. leucotis, P. cinereus, S. coronata, R. calendula, and Myadestes occidentalis (Brown-backed Solitaire) (Table 1). DISCUSSION The Mann-Whitney U test showe d no significant differences in the average number of species and Despite the fact that the OTMD has historically been individuals per count between sites (P > 0.1). However, very important for its economic prosperity, biological there were significant differences in the abundance of 18 inventories in the area are virtually non-existent. This species (Table 2). In reference to the similarity between work provides the first bir d species inventory for Mina sites, the Sorensen index revealed 85% qualitative Dos Estrellas and Tlacotepec, with 108 species (19.7% similarity, while the Morisita-Horn index showed 93% of those registered in the state of Michoacan) (Villaseñor- quantitative similarity. Gómez 2005), and 83% of the species recorded from The Analysis of Similarity (ANOSIM) indicated a Sierra Chincua at MBBR (SEMARNAT 2001), the high level of correspondence between both communities nearest area with available ornithological information. (R = 0.0445, P = 0.0001). On the other hand, the SIMPER According to the NOM-059 (SEMARNAT 2010), two analysis suggested that the few extant differences between species are under special protection: Accipiter cooperi them are attributable to 18 species (Table 3), which add (Cooper's Hawk) and M. occidentalis. up to 62% of the differences between sites. The SIMPER After 65 years of the cessation of extractive mining test gives greater weight to abundance, such that species activities, bird communities at the OTMD have a contributing to the differences between communities are high degree of similarity (85% qualitative and 93% those with the highest number of records. Overall the bird quantitative), a pattern that coincides with the results Table 2. Mean relative abundance of the species with signifi cant differences in abundance between study sites in El Oro- Tlalpujahua, Mining District, during 2014–2015. Individuals Feeding Mean Control Site, Mean Tilings site, Species P recorded guild El Castillo S (EE) Mina Dos Estrellas S (EE) 1 2 Setophaga coronata 145 Omn 0.237 (0.044) 0 (0) 0.001** Myadestes occidentalis 75 Fru 0.147 (0.032) 0.25 (0.034) 0.014* Sitta carolinensis 69 Gra 0.266 (0.042) 0.120 (0.023) 0.008** Myioborus pictus 68 Ins 0.248 (0.037) 0.130 (0.024) 0.010* Oreothlypis superciliosa 67 Ins 0.230 (0.036) 0.140 (0.026) 0.045* Melanerpes formicivorus 61 Omn 0.094 (0.022) 0.225 (0.035) 0.010* Thryomanes bewickii 56 Ins 0.100 (0.023) 0.195 (0.03) 0.028* Catharus occidentalis 40 Fru 0.065 (0.020) 0.145 (0.03) 0.043* Oreothlypis celata 33 Ins 0.059 (0.021) 0.115 (0.024) 0.043* Melanotis caerulescens 28 Ins/Fru 0.029 (0.013) 0.115 (0.023) 0.003** Troglodytes a. brunneicollis. 22 Ins 0.029 (0.013) 0.085 (0.020) 0.025* Cyanocitta stelleri 16 Omn 0.076 (0.027) 0.015 (0.011) 0.015* Tyrannus vociferans 15 Ins 0.065 (0.020) 0.020 (0.010) 0.049* Oriturus superciliosus 12 Omn 0.071 (0.025) 0 (0) 0.001** Catharus aurantiirostris 10 Fru 0.005 (0.005) 0.045 (0.016) 0.035* Colaptes auratus 10 Gra/Ins 0.053 (0.017) 0.005 (0.005) 0.005** Trogon mexicanus 10 Ins/Fru 0.059 (0.024) 0 (0) 0.004** Icterus abeillei 6 Ins 0 (0) 0.030 (0.012) 0.023* (a) Fru: Frugivorous; Gra: Granivorous; Ins: Insectivorous; Omn: Omnivorous. Non-parametric Mann-Whitney U tests: * P < 0.5 and > 0.1, ** P < 0.01; SE = Standard error. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Table 3. Contribution of the bird species to the differences between the communities at the control site and a mining site at El Oro-Tlalpujahua Mining District, central Mexico. Cumulative Species abundance Species abundance Contribution (%) Species percentage of the per count at the per count at the to the difference difference control site mining site Hylocharis leucotis 6.79 6.79 0.75 0.811 Setophaga coronata 5.18 11.97 0.525 0.237 Turdus migratorius 5.16 17.12 0.405 0.438 Ptiliogonys cinereus 4.96 22.08 0.465 0.325 Regulus calendula 4.53 26.61 0.32 0.432 Pheucticus melanocephalus 3.50 30.11 0.21 0.325 Haemorhous mexicanus 3.18 33.29 0.22 0.237 Junco phaeonotus 3.12 36.41 0.23 0.195 Melozone fusca 3.02 39.42 0.215 0.219 Myadestes occidentalis 2.83 42.26 0.25 0.148 Spinus psaltria 2.77 45.03 0.18 0.195 Pipilo maculatus 2.63 47.66 0.23 0.172 Sitta carolinensis 2.59 50.25 0.12 0.266 Myioborus pictus 2.50 52.75 0.13 0.249 Oreothlypis superciliosa 2.47 55.22 0.14 0.231 Setophaga townsendi 2.42 57.64 0.195 0.148 Melanerpes formicivorus 2.30 59.94 0.225 0.0947 Peucedramus taeniatus 2.22 62.16 0.13 0.195 of other studies. In southern Spain, at the Guadiamar Eucalyptus (Eucalyptus marginata) forest, and found that corridor, a severely contaminated environment at the avian communities were very similar after a period of Aznalcollar mine, in restoration since 2000, Márquez- 24 and 30 years, and that the bird communities could Ferrando (2008) found that the composition of bird reach up to 65% similarity within the first 4–5 years of communities exposed to mining waste remnants after abandonment, and 73.5% similarity after 16–17 years. eight years of abandonment was 80% similar to those at According to this, similarity of communities increases natural sites without exposure to mining wastes. Similarly, with time in disturbed environments, where natural Osipov & Biserov (2017) studied the succession of bird regeneration or restoration processes have taken place. communities in a Boreal Mountain-Valley landscape The area of OTMD has gone through a process of disturbed by gold mining in the Niman River (at the natural regeneration, in which those plant species most Bureya mountains, Russia); their findings indicate that tolerant to disturbance, and/or those that were exploited sites with tailings 35–40 years after abandonment were to a lesser extent, reestablished the vegetation on the area, similar in species composition to areas of valleys without and its composition and structure support very similar disturbance, even though density of species was lower in bird communities. The reestablishment of forests with the mining sites. On the other hand, abandoned tailing similar physiognomy in the study site may indicate the sites had a more complex successional vegetation and their presence of suitable resources that maintain similar bird communities of birds were more diverse and abundant, communities at both sites (McArthur & McArthur 1961). as were the mountain forest communities without However, differences in the abundance of 18 species also disturbance. Nichols & Watkins (1984) and Armstrong suggests the existence of specific effects. They might be & Nichols (2000) studied the avifaunal recolonization of related to the sensitivity to pollutants, differences in the rehabilitated bauxite mines in the Jarrah Forest of south- availability of specific resour ces (e.g., food, breeding sites, western Australia. They compared bird communities in feeding territories, perching structures), or other factors a forest where extraction started in 1963 in rehabilitated not taken into account (Loyn 1985, Gould & Mackey Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. 2015). For example, differences found in M. formicivorus Information on remnant effects of abandoned mines might reflect the presence of tall eucalyptus trees and is very scarce. It might prove useful to explore their effects snags at the tailings site (Mina Dos Estrellas), where most on animal communities under scenarios of revegetation individuals were recorded. As suggested, food resources, (natural succession) or restoration. Current information perching structures, and breeding sites can be some of the on mining impacts refers mostly to the response of biotic primary limiting factors in the species distributions and communities in active mining districts, where negative preferences within a given habitat (Cody 1985, Hutto effects have been found on birds, rodents, and vegetation. 1985, Jones 2001). In vertebrates, high concentrations of toxic elements are Studies on the effects of secondary succession in present in kidney and liver tissues, and they relate to their forests have shown that in general, early successional concentrations in the plants on which they feed (Espinosa- bird communities include more generalist granivorous, Reyes et al. 2014). Bioaccumulation of these elements omnivorous and insectivorous species, considered as is known to cause negative effects at the neurological pioneer species indicative of disturbance (Rangel-Salazar (lethargy), physiological (chronic stress and changes in et al. 2009, Becker et al. 2013). As succession progresses, DNA structure), behavioral (decrease of appetite), and structural diversity of vegetation increases and, depending reproductive level (low production of eggs in birds) (Festa on the community composition, specialized frugivorous, et al. 2003, Seewagen 2009, Chapa-Vargas et al. 2010), nectarivorous, and specialized insectivorous species (soil, contributing to the decline of biodiversity at contaminated bark, understory and foliage gleaning) colonize the sites. The rivers of Santa Cruz, San Pedro an d Colorado in habitat and increase in numbers (May 1982, Winkler Sonora, Mexico, which receive flows from copper mines, 2005, Rangel-Salazar et al. 2009). Becker et al. (2013) are very important sites for breeding and wintering birds, found that bird communities in restored mining areas in despite the negative impacts of their low water quality southern Brazil had similar species richness between sites (Sprouse 2005, Villaseñor-Gómez 2006); they have not after 10–20 years of abandonment, although differences been studied in detail. Little is known on the effects of in the abundance of species according to feeding guild potentially toxic elements in tailing residual soils and were evident: granivorous species decreased, whereas their bioavailability. It would be necessary to study tailing carnivorous, frugivorous, and nectarivorous increased chemistry, the exposure paths for those elements, and (especially those forests dependent species); omnivorous bio-magnification effects on functional groups or spe cific species remained stable. Their findings suggest that effects bird species that may be affected at the physiological level could be reflected t hrough changes in functional groups, (Hudson & Bouwman 2008). or can be species specific. In the case of OTMD, some While the establishment of the DMOT historically generalists, omnivorous and ground insectivorous species generated a significant disturbance in the ecosystem, 65 (M. formicivorus, S. coronata, J. phaeonotus and O. celata) years after the end of its activities current conditions seem were significantly more abundant in the tailings site, favorable for the maintenance of avian communities as meanwhile at the control site more specialized species a major component of the regional biodiversity, since such as nectarivorous and bark insectivores prevailed differences at the community level were not remarkable. (H. leucotis, R. calendula, S. carolinensis, M. pictus and Although it is not possible to assess the intensity of the O. superciliosa). Further study is needed to determine environmental effects caused by mining at DMOT in the whether these differences are attributable to the existence past, modification of the natural environment has left of remnant mining effects after 65 years of abandonment. permanent traces, such as soil derived from tailings and Dendrochronological analysis of trees at MBBR the absence of some tree species (such as Sacred Fir, A. suggested that individuals of Sacred Fir (Abies religiosa) religiosa, present in neighboring forests) that were not able are 106 years old, and those of Smooth-bark  Mexican to cope with changes. The relative geochemical stability Pine (Pinus pseudostrobus) are 120 years old. Evidence and the revegetation of tailings may indicate the existence indicates that the MBBR region has also been subjected of low intensity impacts at the present. Although there to historical disturbance regimes caused by logging is no evidence at this time, the bioavailability of some (Sáenz-Ceja 2015). The presence of old railway tracks in potentially toxic elements could trigger processes of bio- the core zone of MBBR at Sierra Chincua supports the magnification in some species, inducing negative health idea of active logging in the past. Probably, regeneration effects on bir d individuals in the region. Therefore, it is processes took place almost at the same time, and, as such, important to continue working on this subject and to the similarities in avian communities between MBBR and analyze some physiological indicators of performance OTMD may reflect the effects of succession in a wider (such as robustness, condition index, fat reserves, and the geographic area. We suggest that OTMD represents an Heterophile/Lymphocyte Index) in local birds, in order important habitat for resident and migratory bird species to evaluate their health and fitness. We also suggest to in the surroundings of MBBR. gain further insights on the role of vegetation structure, Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. C.J., Sauer J.R & Droege S. (eds.). Monitoring bird populations by functional responses of communities (through feeding point counts. Albany: Pacific Southwest Resear ch Station. guilds), and the current anthropogenic impacts that may Cody M.L. 1985. Habitat selection in birds. Orlando: Academic Press. be influencing bir d communities. Colwell R.K. 2013. EstimateS, version 9.1.0: statistical estimation of species richness and shared species from samples. http://purl.oclc.org/ estimates (Access on 05 August 2019). Colwell R.K. & Coddington J.A. 1994. Estimating terrestrial ACKNOWLEDGEMENTS biodiversity through extrapolation. Philosophical Transactions of the Royal Society of London B: Biological Sciences 345: 101–118. This paper is part of the MSc. Dissertation of K.I. Corona-Chávez P. & Uribe-Salas J.A. 2009. Atlas cartográfico del Lemus-Ramírez (Grant 540656, CONACyT-Mexico). Distrito Minero El Oro-Tlalpujahua. Morelia: Universidad Michoacana de San Nicolás de Hidalgo. We recognize the financial support from Universidad Corona-Chávez P., Uribe-Salas J.A., Razo-Perez N., Martínez-Medina Michoacana de San Nicolás de Hidalgo (Coordinación de M., Maldonado-Villanueva R., Ramos-Arroyo Y.R. & Robles- Investigación Científica, Project “Avifauna de la región Camacho J. 2010. The impact of miningin the regional e cosystem: Tlalpujahua-El Oro: estructura de comunidades, uso de the Mining District of El Oro and Tlalpujahua, México. De Re Metallica 15: 21–34. hábitat y expresión de estrés ambiental (2014–2018)”. We Coronado-Martínez Y. 2016. El ecoturismo como opción para el are grateful to the staff of Mina Dos Estrellas (Museo desarrollo local sustentable en el Pueblo Mágico de Tlalpujahua, Técnico Minero Siglo XIX) and Ms. G. Duarte-Godinez Michoacán. MSc. Dissertation. Ciudad de México: Instituto for the permits to work on their property; R.A. Medina Politécnico Nacional. Cristol D.A., Brasso R.L., Condon A.M., Fovargue R.E., Friedman Nieves and J.C. Perez Magaña supported us during field S.L., Hallinger K.K., Monroe A.P. & White A.E. 2008. The activities. We also appreciate the effort and dedication of movement of aquatic mercury through terrestrial food webs. anonymous reviewers who helped to improve this work. Science 320: 335. Chao A., Chazdon R.L., Colwell R.K. & Shen T.J. 2005. A new statistical approach for assessing compositional similarity based on incidence and abundance data. Ecology Letters 8: 148–159. REFERENCES Chapa-Vargas L., Mejía-Saavedra J., Monzalvo-Santos K. & Puebla- Olivares F. 2010. Blood lead concentrations in wild birds from a Altaf M., Javid A., Khan A.M., Khan M.S.H., Umair M. & Ali Z. polluted mining region at Villa de la Paz, San Luis Potosi, Mexico. 2018. Anthropogenic impact on the distribution of the birds in Journal of Environmental Science and Health A 45: 90–98. the tropical thorn forest, Punjab, Pakistan. Journal of Asia-Pacific Eagles-Smith C.A., Wiener J.G., Eckley C.S., Willacker J.J., Evers Biodiversity 11: 229–236. D.C., Marvin-DiPasquale M., Obrist D., Fleck J.A., Aiken G.R., AOS [American Ornithological Society]. 2017. American Lepak J.M., Jackson A.K., Webster J.P., Stewart A.R., Davis J.A., Ornithological Society's check-list of North American birds. http:// Alpers C.N. & Ackerman J.T. 2016. Mercury in western North www.americanornithology.org/content/checklist-north-and- America: a synthesis of environmental contamination, fluxes, middle-american-birds. bioaccumulation, and risk to fish and wildlife. Science of the Total Armstrong K.N. & Nichols O.G. 2000. Long term trends in avifaunal Environment 568: 1213–1226. recolonisation of rehabilitated bauxite mines in the Jarrah Forest Edwards D.P., Larsen T.H., Docherty T.D.S., Ansell F.A., Hsu W.W., of south-western Australia. Forest Ecology and Management 126: Derhé M.A., Hamer K.C. & Wilcove D.S. 2011. Degraded lands 213–225. worth protecting: the biological importance of southeast Asia's Badii M.H., Landeros J. & Cerna E. 2007. Patrones de asociación de repeatedly logged forests. Proceedings of the Royal Society of London especies y sustentabilidad. International Journal of Good Conscience B: Biological Sciences 278: 82–90. 3: 632–660. Eisler R. 2004. Mercury hazards from gold mining to humans, Balistrieri L.S., Box S.E., Bookstrom A.A., Hooper R.L. & Mahoney plants, and animals. Reviews of Environmental Contamination and J.B. 2002. Impacts of historical mining in the Coeur d'Alene River Toxicology 181: 139–198. Basin, p. 1–34. In: Balistrieri L.S. & Stillings L.L. (eds.). Pathways Espinosa-Reyes G., González-Mille D.J., Ilizaliturri-Hernández C.A., of metal transfer from mineralized sources to bioreceptors: a synthesis Mejía-Saavedra J., Cilia-López V.G., Costilla-Salazar R. & Díaz- of the mineral resources program's past environmental studies in the Barriga F. 2014. Effect of mining activities in biotic communities western United States and future research directions. Washington: of Villa de la Paz, San Luis Potosi, Mexico. BioMed Research U.S. Geological Survey. International 2014: 1–13. Balmer O. 2002. Species list in ecology and conservation: abundances Festa F., Cristaldi M., Ieradi L.A., Moreno S. & Cozzi R. 2003. The matter. Conservation Biology 16: 1160–1161. comet assay for the detection of DNA damage in Mus spretus from Batty L.C. 2005. The potential importance of mine sites for Donana National Park. Environmental Research 91: 54–61. biodiversity. Mine Water and the Environment 24: 101–103. Garitano-Zavala A., Cotín J., Borràs M. & Nadal J. 2010. Trace Becker R.G., Paise G. & Pizo M.A. 2013. The stru cture of bird metal concentrations in tissues of two tinamou species in mining communities in areas revegetated after mining in south Brazil. areas of Bolivia and their potential as environmental sentinels. Revista Brasileira de Ornitologia 21: 221–234. Environmental Monitoring and Assessment 168: 629–244. Blake J.G. 2007. Neotropical forest bird communities: a comparison Gonçalves-Rodriguez G. & Shraft B.W. 2001. Review of benthic of species richness and composition at local and region scales. invertebrate fauna in extremely acidic environments (pH ≤ 3). Condor 109: 237–255. Mine Water and the Environment 20: 114–121. Boulet M.P. & Larocque A.C.L. 1988. A comparative mineralogical Gould S.F. & Mackey B.G. 2015. Site vegetation characteristics are and geochemical study of sulfide mine tailings at two sites in New more important than landscape context in determining bird Mexico, U.S.A. Environmental Geology 33: 130–142. assemblages in revegetation. Restoration Ecology 23: 670–680. Buskirk W.H. & McDonald J.L. 1995. Comparison of point count Howell S.N.G. & Webb S. 2005. A guide to the birds of Mexico and sampling regimes for monitoring forest birds, p. 25–34. In: Ralph north Central America. New York: Oxford University Press. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Hudson A. & Bouwman H. 2008. Birds associated with a tailings Osipov S.V. & Biserov M.F. 2017. Population of birds in the Boreal storage facility and surrounding areas from a South African gold Mountain-Valley landscape disturbed by gold mining. Russian mine. African Journal of Ecology 46: 276–281. Journal of Ecology 48: 45–50. Hutto R.L. 1985. Habitat selection by nonbreeding, migratory land Osuna-Vallejo V., Lindig-Cisneros R.A., Sáenz-Romero C. & Cruz- birds, p. 455–476. In: Cody M.L. (ed.). Habitat selection in birds. de-León J. 2016. Ensayo de mesocosmos especies y procedencias Orlando: Academic Press. de coníferas en residuos mineros de Tlalpujahua, Michoacán. XX Hutto R.L., Pletschet S.M. & Hendricks P. 1986. A fixed-radius point Congreso Mexicano de Botánica. Ciudad de México: Sociedad count method for nonbreeding and breeding season use. Auk 103: Botánica de México. 593–602. Ouboter P.E., Landburg G.A., Quik J.H.M., Mol J.H.A. & van del INEGI [Instituto Nacional de Estadística, Geografía e Informática]. Lugt F. 1999. Mercury levels in pristine and gold mining impacted 2009. Prontuario de información geográfica municipal de aquatic ecosystems of Suriname, South America. AMBIO 41: los Estados Unidos Mexicanos: clave geoestadística 16093. 873–882. http://www3.inegi.org.mx/sistemas/mexic ocifras/datos- Pérez-Tris J. 1999. El peso de las aves en paso: ¿Una medida de geograficos/16/16093.pdf. (Access on 10 January 2016). condición física o acumulación de grasa? Revista de Anillamiento Jacob D.L. & Otte M.L. 2004. Long-term effects of submergence and 3: 11–15. wetland vegetation on metals in a 90-year old abandoned Pb-Zn Perotti M., Petrini R., D'Orazio M., Ghezzi L., Giannecchini R. & mine tailings pond. Environmental Pollution 130: 337–345. Vezzoni S. 2017. Thallium and other potentially toxic e lements Jones J. 2001. Habitat selection studies in avian ecology: a critical in the Baccatoio stream catchment (northern Tuscany, Italy) review. Auk 118: 557–562. receiving drainages from abandoned mines. Mine Water and the Kossoff D., Dubbin W.E., Alfredsson M., E dwards S.J., Macklin Environment 37: 1–11. M.G. & Hudson-Edwards K.A. 2014. Mine tailings dams: Pickett S.T.A. & White P.S. 1985. The ecology of natural disturbance characteristics, failure, environmental impacts, and remediation. and patch dynamics. Cambridge: Academic Press. Applied Geochemistry 51: 229–245. Ramírez-Ramírez M.I. 2001. Los espacios forestales de la Sierra de Angangueo Lacerda L.D. 1997. Global mercury emissions from gold and silver (estados de Michoacán y México), México: una revisión geográfica. P h.D. mining. Water, Air, & Soil Pollution 97: 209–221. Thesis. Mad rid: Universidad Complutense de Madrid. Lefcort H., Meguire R.A., Wilson L.H. & Ettinger W.F. 1988. Rangel-Salazar J.L., Enríquez P.L. & Sántiz-López E.C. 2009. Heavy metals alter the survival, growth, metamorphosis, and Variación de la diversidad de aves de sotobosque en el Parque antipredatory behavior of Columbia Spotted Frog (Rana Nacional Lagos de Motebello, Chiapas, México. Acta Zoológica luteiventris) tadpoles. Archives of Environmental Contamination Mexicana 25: 479–495. and Toxicology 35: 447–456. Rösner U. 1988. Effects of historical mining activities on surface Lock K., Janssens F. & Janssen C.R. 2003. Effects of metal water and groundwater: an example from northwest Arizona. contamination on the activity and diversity of springtails in an Environmental Geology 33: 224–230. ancient Pb-Zn mining area at Plombières, Belgium. European Rubio I., Martinez-Madrid M., Mendez-Fernandez L., Galarza A. & Journal of Soil Biology 39: 25–29. Rodriguez P. 2016. Heavy metal concentration in feathers of Little Loyn R.H. 1985. Bird population in successional forest of Mountain Egret (Egretta garzetta) nestlings in three coastal breeding colonies Ash Eucalyptus regnans in central Victoria. Emu 85: 213–231. in Spain. Ecotoxicology 25: 30–40. Mahmoud S.H. & Gan T.Y. 2018. Impact of anthropogenic climate Sáenz-Ceja J.E. 2015. Recostrucción dendrocronológica de la historia change and human activities on environment and ecosystem de establecimiento de Pinus pseudostrobus y Abies religiosa en services in arid regions. Science of the Total Environment 633: la Reserva de la Biosfera Mariposa Monarca. Ciudad de México: 1329–1344. Instituto de Investigaciones en Ecosistemas y Sustentabilidad. Manson R.H. & Jardel-Peláez E.J. 2009. Perturbaciones y desastres Seewagen C.L. 2009. Threats of environmental mer cury to birds: naturales: impactos sobre las ecorregiones, la biodiversidad y el knowledge gaps and priorities for future research. Bird Conservation bienestar socioeconómico, p. 131–184. In: Sarukán J. (ed.). International 20: 112–123. Capital Natural de México, v. 2: estado de conservación y tendencias SEMARNAT [Secretaría de Medio Ambiente y Recursos Naturales]. de cambio. Ciudad de México: CONABIO. 2001. Programa de manejo de la Reserva de la Biosfera Mariposa Márquez-Ferrando R. 2008. Las comunidades de aves y reptiles del Monarca. Ciudad de México: CONANP. corridor Verde del Guadiamar después del vertido minero de SEMARNAT [Secretaría de Medio Ambiente y Recursos Naturales]. Aznalcóllar. MSc. Dissertation. Granada: Universidad de Granada. 2010. Norma Oficial Mexicana NOM-059-SEMARNAT-2010 May P.G. 1982. Secondary succession and breeding bird community de 30 de Diciembre del 2010. http://www.profepa.gob.mx/ structure: patterns of resource utilization. Oecologia 55: 208–216. innovaportal/file/435/1/NOM_059_SEMARNAT_2010.pdf McArthur R.H. & McArthur J.W. 1961. On bird species diversty. (Access on 02 April 2017). Ecology 42: 594–598. Sprouse T.W. 2005. Water issue on the Arizona-Mexico border. Tucson: Muñiz-Castro M.A. 2008. Sucesión secundaria y establecimiento de Water Resources Research Center. especies arbóreas nativas para restauración de Bosque Mesófilo de Struckhoff M.A., Stroh E.D. & Grabner K.W. 2013. Effects of mining- Montaña en potreros abandonados del centro de Veracruz. Ph.D. associated lead and zinc soil contamination on native floristic Thesis. Xalapa: Instituto de E cología A.C. quality. Journal of Environmental Management 119: 20–28. Nichols O.G. & Watkins D. 1984. Bird utilization of rehabilitated Ugalde-Lezama S., Alcántara-Carbajal J.L., Tarango-Arámbula bauxite minesites in western Australia. Biological Conservation 30: L.A., Ramírez-Valverde G. & Mendoza-Martínez G.D. 2012. 109–131. Fisonomía vegetal y abundancia de aves en un bosque templado Nieto-Monroy A.P. 2007. Variabilidad espacial y temporal de la con dos niveles de perturbación en el Eje Neovolcánico T ransversal. Hidrogeoquímica de arroyos del Distrito Minero El Oro-Tlalpujahua. Revista Mexicana de Biodiversidad 83: 133–143. Ph.D. Thesis. Guanajuato: Universidad de Guanajuato. Ventakeswarlu K., Nirola R., Kuppusamy S., Thavamani P., Naidu R. O'Sullivan A.D., McCabe O.M., Murray D.A. & Otte M.L. 1999. & Megharaj M. 2016. Abandoned metalliferous mines: ecological Wetlands for rehabilitation of metal mine wastes. Proceedings of impacts and potential approaches for reclamation. Reviews in the Royal Irish Academy B: Biology and Environment 99: 11–17. Environmental Science and Bio/Technology 15: 327–354. Revista Brasileira de Ornitologia 27(2): 2019 Remnant effects of mining on temperate forest bir d communities Lemus et al. Villaseñor-Gómez L.E. 2005. Aves, p. 101–103. In: Villaseñor-Gómez in deciduous and coniferous forest in the Sopron Mountains, L.E. & Leal-Nares O.A. (eds.). La biodiversidad en Michoacán. Hungary. Acta Silvatica et Lignaria Hungarica 1: 49–58. Estudio de estado. Ciudad de México: Comisión Nacional para el Xu X., Xie Y., Qi K., Luo Z. & Wang X. 2018. Detecting the Conocimiento y Uso de la Biodiversidad. response of bird communities and biodiversity to habitat loss Villaseñor-Gómez J.F. 2006. Habitat use and the effects of disturbance and fragmentation due to urbanization. Science of the Total on wintering birds using riparian habitats in Sonora, Mexico. Ph.D. Environment 624: 1561–1576. Thesis. Missoula: University of Montana. Winkler D. 2005. Ecological succession of breeding bird communities Associate Editor: Marcos P. Dantas. Revista Brasileira de Ornitologia 27(2): 2019

Journal

Ornithology ResearchSpringer Journals

Published: Jun 1, 2019

Keywords: avian communities; diversity; El Oro-Tlalpujahua Mining District; mining tailings; remnant effects

There are no references for this article.