Cecilia Odette Carral-Murrieta, Michelle García-Arroyo, Oscar H. Marín-Gómez, J. Roberto Sosa-López, Ian MacGregor-Fors. 2020: Noisy environments: untangling the role of anthropogenic noise on bird species richness in a Neotropical city. Avian Research, 11(1): 32. DOI: 10.1186/s40657-020-00218-5
Citation:
Cecilia Odette Carral-Murrieta, Michelle García-Arroyo, Oscar H. Marín-Gómez, J. Roberto Sosa-López, Ian MacGregor-Fors. 2020: Noisy environments: untangling the role of anthropogenic noise on bird species richness in a Neotropical city. Avian Research, 11(1): 32. DOI: 10.1186/s40657-020-00218-5
Cecilia Odette Carral-Murrieta, Michelle García-Arroyo, Oscar H. Marín-Gómez, J. Roberto Sosa-López, Ian MacGregor-Fors. 2020: Noisy environments: untangling the role of anthropogenic noise on bird species richness in a Neotropical city. Avian Research, 11(1): 32. DOI: 10.1186/s40657-020-00218-5
Citation:
Cecilia Odette Carral-Murrieta, Michelle García-Arroyo, Oscar H. Marín-Gómez, J. Roberto Sosa-López, Ian MacGregor-Fors. 2020: Noisy environments: untangling the role of anthropogenic noise on bird species richness in a Neotropical city. Avian Research, 11(1): 32. DOI: 10.1186/s40657-020-00218-5
Among urban stimuli, anthropogenic noise has been identified to be one of the behavioral drivers of species that rely on acoustic signals for communication. Studies have shown both species-specific and assemblage responses to urban noise, ranging from the modulation of their acoustic frequencies and spatiotemporal adjustments to declines in species richness. In this study, we assessed the citywide relationship between two anthropogenic noise variables (noise levels recorded during bird surveys and daily average noise levels) and vegetation cover with bird species richness.
Methods
This study was conducted in the city of Xalapa (Mexico) through a 114 citywide point-count survey. We recorded bird communities at each sampling site. We measured noise levels using a sound level meter while performing point-counts. Then, we generated a map of average daily noise of the city using an array of 61 autonomous recording units distributed across the city of Xalapa and calculated daily noise levels for the 114 points. We ran a linear model (LM) to assess potential relationships between both point-count and daily (24 h) noise values and vegetation cover with bird richness.
Results
Results from the LM show: (1) a negative relationship between maximum point-count noise and avian species richness, (2) no relationship between 24 h noise and bird species richness, and (3) a positive relationship between vegetation cover and bird species richness.
Conclusions
Results provide evidence that decreases in urban bird species richness do not necessarily imply the permanent absence of species, suggesting that birds can temporarily fly away from or avoid sites when noisy, become cryptic while noisy events are occurring, or be undetected due to our inability to record them in the field during noisy events.
Strigiformes, the bird order known commonly as owls, comprise cryptically colored nocturnal birds that can be notoriously hard to identify in the field. Their mysterious nature is typified by the Brown Hawk Owl or Brown Boobook complex (Ninox [scutulata] sp.), an assemblage widely distributed across Asia with populations in various regions exhibiting differentiation with respect to phenology, vocalizations and plumage. This differentiation has led to confusion about the taxonomic status of these populations. Some authors suggest that the complex is a single species comprising as many as 13 subspecies (König et al. 2009). However, King (2002) analyzed bioacoustic and morphometric data and determined that the complex comprises three biological species: the Northern Boobook (Ninox japonica), which breeds from southeast Siberia to Taiwan and adjacent mainland China, and winters across Southeast Asia, the Chocolate Boobook (Ninox randi), which is endemic to the main Philippines (i.e. the Philippine archipelago with the exclusion of Palawan and satellite islands), and the Brown Boobook (Ninox scutulata), which is distributed across South and Southeast Asia to the Greater Sundas and Palawan (Fig. 1).
Figure
1.
Map of East and Southeast Asia depicting the breeding range of the Brown Boobook (N. scutulata) (a) and the breeding and known wintering ranges of both the japonica lineage and the undetermined mitochondrial lineage (Lin et al. 2013) of the Northern Boobook (N. japonica) (b). Also included are sighting records from Bangkok (b(i)), Laem Phak Bia (b(ii)) (Round 2011; Upton 2014), and a 1963 specimen record from Trang (b(iii)) (Round 2011) in Thailand, as well as the recent specimen records from Singapore described in this study (b(iv)). The main Asian landmass stretching from mainland China to Russia, inclusive of Sakhalin island, is separately labelled owing to uncertainty over the exact breeding lineage within that range. Question marks refer to areas where the Northern Boobook are likely to winter but are presently under-surveyed with no confirmed records. Breeding and range maps were obtained and modified from the IUCN Red List of Threatened Species (BirdLife International and NatureServe 2014), and basemap and Thailand sightings were generated using QGIS v2.8.2-Wien (Quantum GIS Development Team, 2015) and edited on Adobe PhotoShop CS5 (Adobe, 2010)
At present knowledge, Ninox japonica occurs as two mitochondrially distinct populations—a nominate population that occurs in both Japan (including Ryukyu) and little islands off of Taiwan (e.g. Lanyu), and a resident population on the Taiwanese mainland said to be non-migratory due to year-round records of the taxon on the island (Lin et al. 2013). While the latter lineage has been identified based on DNA samples from the island of Taiwan only, unsampled breeding populations in mainland China and Russia may well be closely related or identical to this lineage. Lin et al. (2013) refer to this as an unnamed population, but it may well have a taxonomic name already if mainland populations are shown to belong with it: based on morphological considerations, many treatises nowadays refer to mainland populations as N. j. florensis (del Hoyo et al. 2015), a name based on type material from the wintering range in East Indonesia that may extend to Taiwan if future research can verify the connection between the type of florensis and mainland Chinese breeding populations. For the purposes of clarity and brevity, we will refer to this mitochondrial lineage as the "undetermined lineage" henceforth.
The wintering range of the migratory nominate form is unclear; there have been confirmed records from Wallacea, Borneo and Java, but the limits of its winter range further west remain unknown (Fig. 1). Additionally, morphological similarity between Northern and Brown Boobooks makes it difficult to confirm identification in the field where their ranges potentially overlap.
Recent advances in identification between Brown and Northern Boobooks based on wing: tail ratios, wing formulas (King 2002) and ventral markings (Round 2011) have led to new Northern Boobook winter records in mainland Southeast Asia, with several reports of the species in Thailand and a single new record from Kedah in peninsular Malaysia (Table 1). However, the range of variation in ventral patterning is not fully understood, which has led to some confusion with regards to distinguishing the two species in the field. For instance, individuals displaying ventral markings typical of Brown Boobooks (sensu Round 2011) have been photographed breeding across Japan (e.g., Morlan 2012), over 3000 km away from the nearest confirmed breeding locality of Brown Boobooks, indicating that Northern Boobooks, especially from Japan, may display similar ventral markings.
Table
1.
Winter records of Ninox japonica in mainland Southeast Asia
Location
Date
Record type and status
Source
Chiang Mai: Mae Rim:Ban Khi Lek
24/11/1970
Specimen: TISTR53- 1848; wing measurements and ventral plumage intermediate between scutulata and japonica; identification unconfirmed
On 23 March 2014, the carcass of a Ninox owl (ID CR059) was found near the Tanglin Halt estate in Singapore (01.3009500°N, 103.7930667°E). Close inspection of the bird revealed its ventral patterning to be indicative of the Northern Boobook (sensu Round 2011). This potentially represents the first country record of the Northern Boobook and extends the mainland wintering range of the species considerably further south. If substantiated with molecular methods, this record would constitute the first corroboration that Northern Boobooks winter on or just off the southern part of mainland Southeast Asia. We here present morphological measurements and cytochrome-b (cytb) sequences of this bird and additional specimens collected throughout the region to confirm their identity and to discuss Ninox taxonomy and field identification.
Methods
Tissue was sampled from the carcass as well as three presumable Brown Boobooks collected in Singapore that had been deposited in the Lee Kong Chian Natural History Museum (Additional file 1: Table S1). DNA extractions were carried out with GeneAll® DNA Purification kits as per the protocol for animal tissue. Polymerase chain reactions (PCR) were carried out in a C1000™ Thermal Cycler and cytb was amplified as per Cibois et al. (1999) and Dong et al. (2010) using the conditions stated in Sorenson et al. (1999). PCR amplifications were done in 20 μL reaction volumes, which comprised 2 μL 10 × Taq PCR buffer, 1.2 μL MgCl2 (25 mM), 1 μL of each primer (10 μm), 0.4 μL Fermentas Taq polymeras, 2 μL mtDNA template and 11.6 μL MilliQ water. PCR product clean up was carried out using ExoSAP-IT® and the BigDye® Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems Inc., Foster City, CA, USA) was used to cycle-sequence samples. Sequences were obtained by capillary electrophoresis using an Applied Biosystems 3130 × l Genetic Analyzer.
DNA sequences were assembled with CodonCode Aligner version 4.1 (CodonCode Corporation, http://www.codoncode.com) and aligned with MEGA 6.06 using ClustalW (Larkin et al. 2007; Tamura et al. 2013). The final alignment was 923 base pairs in length and contained no indels. We compared our four novel sequences with those of 32 individuals of the nominate form of Ninox japonica from Japan and Lanyu, 48 individuals of the presumably resident undetermined lineage from the main island of Taiwan and a single novel sequence of Ninox japonica from Brunei for a total sample size of 85 (Additional file 1: Table S1; Lin et al. 2013). Sequences were easily aligned, therefore unlikely to be paralogs. MEGA 6.06 was employed to construct phylogenetic trees using Neighbor-Joining (NJ), Maximum Parsimony (MP) and Maximum Likelihood (ML). For each analysis, 1000 bootstrap replicates were run. MP was run with all sites used for gap treatment, Tree-Bisection-Reconnection as the tree search method and other settings in default mode. The program jModelTest 2.1.4 (Darriba et al. 2012) was used to determine the best evolutionary model for ML. The results identified the Hasegawa, Kishino, and Yano model with parameters for gamma distribution (HKY + G) as the most suitable model for ML analysis. The outgroup for tree analyses was a cytb sequence of the Powerful Owl (Ninox strenua) downloaded from GenBank. DnaSP v5.10.01 (Librado and Rozas 2009) was used to calculate raw sequence divergence and nucleotide diversity between and within taxa.
The wing of the carcass retrieved in Singapore was measured by determining the distance between the foremost extremity of the carpus to the tip of the longest primary feather using the closed, flattened wing. Wing point measurements were determined by closing the wing and placing the tips of the primary feathers in order. The feathers were then splayed slightly and the primaries were measured in relation to the longest primary. The tail was measured by sliding a ruler between the retrices and the undertail coverts up to the base of the tail, and then flattening and measuring the longest tail feather. Wing and tail measurements were compared against those obtained for vouchered Brown and Northern Boobook specimens (King 2002).
Results
NJ, MP and ML analyses all yielded trees with identical topology. Three similar clades emerged from the phylogenetic analysis, with the first two clades representing the two genetically distinct Northern Boobook taxa (Lin et al. 2013). The first clade contained known Taiwanese breeders [the undetermined lineage identified by Lin et al. (2013)] and the second contained individuals from the migratory main population (Fig. 2). The Singaporean carcass and the Brunei sample were nested within the first clade, confirming that they are Northern Boobooks. Of the three tissue samples analyzed from the Lee Kong Chian Museum of Natural History, one sample (November 2000) also emerged within the undetermined lineage whilst the other two samples (July 2003; June 2004) formed a separate clade (Fig. 2). These latter two samples represent Brown Boobooks resident in Singapore as they were collected in summer months when no migrants are present.
Figure
2.
Phylogram of Brown Boobook (N. scutulata) and Northern Boobook (N. japonica) samples. Annotated numbers are Neighbor-Joining, Maximum Likelihood and Maximum Parsimony bootstrap values, respectively. Only nodes with at least two bootstrap values > 90 are annotated. Black arrows indicate samples collected in Singapore and red arrow indicates sample from Brunei. Tree topology used is from NJ tree
Analysis of raw sequence divergence between clades showed that Ninox scutulata exhibited a divergence of 2.1-2.6 % from the two Ninox japonica clades, whilst the nominate clade of Ninox japonica showed a smaller divergence of 1.6 % from the undetermined lineage (Table 2).
Table
2.
Matrix of p-divergences between taxa (below diagonal) and p-divergences within each sampled taxon (along diagonal, italic)
The wing and tail measurements of the Singaporean carcass were 217 mm and 114 mm, respectively, giving a wing:tail ratio of 1.90 (Table 3). These results, combined with wing morphology measurements (Table 4) provided morphological confirmation that our specimen was a Northern Boobook as diagnosed by King (2002).
Table
3.
Comparison of morphological measurements across Ninox sp. and the Singaporean carcass (in italic)
Wing
Tail
Wing/tail ratio
Ninox japonica
220.8 (214.0–226.8)
115.8 (107.5–122.6)
1.91 (1.75–2.03)
Ninox scutulata
195.7 (182.4–213.3)
109.5 (100.3–115.0)
1.78 (1.69–1.87)
Singapore carcass CR059
217.0
114.0
1.90
Average values are provided in mm with range given in brackets. Values highlighted show instances where measurement range overlaps with values from Singapore carcass
All previous records of Northern Boobooks in mainland Southeast Asia have relied on visual identification based on the ventral markings or measurements based on wing:tail ratios (Round 2011). However the full extent of intra-specific variation in ventral markings within Northern and Brown Boobooks is not well understood, making it difficult to distinguish the two species visually. Our molecular results constitute a considerable southward extension of the wintering range of > 1400 km from a previous winter record (Phetchaburi; Table 1) confirmed by measurements. It is possible that the wintering range of Northern Boobooks may even include Sumatra based on its proximity to Singapore. This discovery represents a new avian country record for Singapore. We show here that in cases where visual identification is challenging, genetic analysis is a handy tool for clarifying species identity.
Of the three additional Singaporean tissue specimens used as a comparison, two were Brown Boobooks as expected, but surprisingly the third also emerged as a Northern Boobook. The fact that two out of four randomly collected boobooks in Singapore refer to Northern rather than Brown Boobooks suggests that the recently procured carcass is not an accidental stray, but that Northern Boobooks may be regular annual visitors to the island. Given that Singapore has one of the best-known national avifaunas in the world (Wang and Hails 2007; Chisholm et al. 2015), it seems that this seasonal visitor may have been overlooked due to confusion with the island's resident Brown Boobook. The procurement date of one specimen in November suggests that Northern Boobooks are not mere migrants but may overwinter on the island.
The Northern Boobooks identified from Singapore and Brunei were not of the migratory Japanese population but of the undetermined mitochondrial lineage. This lineage has been reported year-round in Taiwan including breeding in March (Lin et al. 2013)—the month of procurement of the carcass in Singapore. Our discovery suggests that some populations of the undetermined mitochondrial lineage are long-distance migratory, whereas others are not. While we cannot rule out that Taiwan harbors both migratory and non-migratory populations, we consider it more likely that the undetermined mitochondrial lineage extends to genetically unsampled parts of the breeding range of the Northern Boobook across the East Asian mainland from South China north all the way to Russia. If true, it is likely that the provenance of the migratory populations of this lineage lies in the more northerly parts of their distribution, such as northeast China (Heilongjiang Province) and eastern Siberian Russia.
The internal taxonomy of the Northern Boobook N. japonica is confused: subspecies florensis was described on the basis of a wintering specimen from the island of Flores (eastern Indonesia); it has been attributed to breeding populations from northern mainland Asia (such as eastern Siberian Russia and northeastern China) presumably because of its large size. If true, this name would apply to the undetermined mitochondrial lineage of Lin et al. (2013), of which Taiwanese birds would then be a resident subset. Additional genetic research including mainland breeding populations of Northern Boobooks is urgently needed to confirm this hypothesis. Further, the use of high resolution genome-wide SNP data will help provide a more comprehensive understanding of the taxonomy of these boobooks.
Conclusions
Analysis of mitochondrial DNA has extended the wintering range of Northern Boobooks in Southeast Asia and suggests that most winterers in the Sundaic region may refer to a mitochondrial lineage of uncertain taxonomic status that has previously been documented from Taiwan but may breed over large parts of mainland Eastern Asia. A genetic research into mainland breeders is urgently required to characterize the geographic distribution of this undetermined mitochondrial lineage. Future taxonomic research may show that the name florensis, based on a wintering individual from the island of Flores, refers to this lineage.
Additional file
Authors' contributions
FER conceived of and designed the study, KRS conducted molecular genetic and analytical work, KRS and FER wrote the manuscript, DJXT provided samples, KS provided sequences and PDR provided information on Ninox japonica records from across Southeast Asia. All authors read and approved the final manuscript.
Acknowledgements
We would like to thank David Bakewell for details on a potential record in Kedah, and Joe Morlan for making his photo of a Japanese breeder available online. We are grateful to the Lee Kong Chian Natural History Museum for providing us with samples. This research was funded by the National University of Singapore (NUS) Faculty of Science and Department of Biological Sciences through grants WBS R-154-000-570-133 and R-154-000-583-651, respectively.
Ethics statement
Lab work was conducted in accordance with NUS's Office of Safety, Health and Environment regulations.
Competing interests
The authors declare that they have no competing interests.
Arroyo-Solís A, Castillo JM, Figueroa E, López-Sánchez JL, Slabbekoorn H. Experimental evidence for an impact of anthropogenic noise on dawn chorus timing in urban birds. J Avian Biol. 2013;44:288–96.
Barber JR, Crooks KR, Fristrup KM. The costs of chronic noise exposure for terrestrial organisms. Trends Ecol Evol. 2010;25:180–9.
Beaugeard E, Brischoux F, Henry P-Y, Parenteau C, Trouvé C, Angelier F. Does urbanization cause stress in wild birds during development? Insights from feather corticosterone levels in juvenile house sparrows (Passer domesticus). Ecol Evol. 2019;9:640–52.
Bermúdez-Cuamatzin E, Ríos-Chelén AA, Gil D, Macías-Garcia C. Experimental evidence for real-time song frequency shift in response to urban noise in a passerine bird. Biol Lett. 2011;7:36–8.
Bibby CJ, Burgess ND, Hill DA, Mustoe S. Bird census techniques. London: Academic Press; 2000.
Blickley JL, Word KR, Krakauer AH, Phillips JL, Sells SN, Taff CC, et al. Experimental chronic noise is related to elevated fecal corticosteroid metabolites in lekking male greater sage-grouse (Centrocercus urophasianus). PLoS ONE. 2012;7:e50462.
Bonier F, Martin PR, Wingfield JC. Urban birds have broader environmental tolerance. Biol Lett. 2007;3:670–3.
Carbó-Ramírez P, Zuria I. The value of small urban greenspaces for birds in a Mexican city. Landscape Urban Plan. 2011;100:213–22.
Castillo-Campos G. Vegetación y flora del municipio de Xalapa, Veracruz. Instituto de Ecología: UNESCO; 1991.
Chepesiuk R. Decibel hell: the effects of living in a noisy world. Environ Health Perspect. 2005;113:A34–41.
Croci S, Butet A, Clergeau P. Does urbanization filter birds on the basis of their biological traits? Condor. 2008;110:223–40.
Czech B, Krausman PR, Devers PK. Economic associations among causes of species endangerment in the United States. Bioscience. 2000;50:593–601.
De Camargo-Barbosa KV, Rodewald AD, Ribeiro MC, Jahn AE. Noise level and water distance drive resident and migratory bird species richness within a Neotropical megacity. Landsc Urban Plan. 2020;197:103769.
Dudzinski K, Jeanette T, Justin G. Communication in marine mammals. In: Perrin W, Wursig B, Thewissen JGM, editors. Encyclopedia of marine mammals. London: Academic Press; 2009. p. 260–9.
Eldredge N, Horenstein S. Concrete jungle: New York City and our last best hope for a sustainable future. Oakland: University of California Press; 2014.
Escobar-Ibáñez JF, MacGregor-Fors I. Peeking into the past to plan the future: assessing bird species richness in a neotropical city. Urban Ecosyst. 2016;19:657–67.
Evans KL, Newson SE, Gaston KJ. Habitat influences on urban avian assemblages. Ibis. 2009;151:19–39.
Evans KL, Chamberlain DE, Hatchwell BJ, Gregory RD, Gaston KJ. What makes an urban bird? Global Change Biol. 2011;17:32–44.
Falfán I, Muñoz-Robles CA, Bonilla-Moheno M, MacGregor-Fors I. Can you really see 'green'? Assessing physical and self-reported measurements of urban greenery. Urban for Urban Gree. 2018;36:13–21.
Federal Aviation Association (FAA): Fundamentals of noise and sound; 2018.. Accessed 02 Dec 2019.
Fischer RA, Valente JJ, Guilfoyle MP, Kaller MD, Jackson SS, Ratti JT. Bird community response to vegetation cover and composition in riparian habitats dominated by Russian olive (Elaeagnus angustifolia). Northwest Sci. 2012;86:39–52.
Fontana CS, Burger MI, Magnusson E. Bird diversity in a subtropical South-American City: effects of noise levels, arborisation and human population density. Urban Ecosyst. 2011;14:341–60.
Fröhlich A, Ciach M. Nocturnal noise and habitat homogeneity limit species richness of owls in an urban environment. Environ Sci Pollut Res. 2019;26:17284–91.
Fuller RA, Warren PH, Gaston KJ. Daytime noise predicts nocturnal singing in urban robins. Biol Lett. 2007;3:368–70.
Gil D, Honarmand M, Pascual J, Pérez-Mena E, Macías Garcia C. Birds living near airports advance their dawn chorus and reduce overlap with aircraft noise. Behav Ecol. 2015;26:435–43.
González-Oreja JA. Relationships of area and noise with the distribution and abundance of songbirds in urban greenspaces. Landsc Urban Plan. 2017;158:177–84.
González-García F, Straub R, García JAL, MacGregor-Fors I. Birds of a neotropical green city: an up-to-date review of the avifauna of the city of Xalapa with additional unpublished records. Urban Ecosyst. 2014;17:991–1012.
Goodwin SE, Shriver G. Effects of traffic noise on occupancy patterns of forest birds. Conserv Biol. 2011;25:406–11.
Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, et al. Global change and the ecology of cities. Science. 2008;319:756–60.
Habib L, Bayne EM, Boutin S. Chronic industrial noise affects pairing success and age structure of ovenbirds Seiurus aurocapilla. J Appl Ecol. 2007;44:176–84.
Halfwerk W, Slabbekoorn H. A behavioural mechanism explaining noise-dependent frequency use in urban birdsong. Anim Behav. 2009;78:1301–7.
Herrera-Montes MI, Aide TM. Impacts of traffic noise on anuran and bird communities. Urban Ecosyst. 2011;14:415–27.
Instituto Nacional de Estadística y Geografía (INEGI). Prontuario de la información geográfica municipal de los Estados Unidos Mexicanos. Xalapa, Veracruz de Ignacio de la Llave: Clave geoestadística; 2009.
Jacot A, Hendrik R, Forstmeier W. Individual recognition and potential recognition errors in parent–offspring communication. Behav Ecol Sociobiol. 2010;64:1515–25.
Johnson MTJ, Munshi-South J. Evolution of life in urban environments. Science. 2017;358:eaam8327.
Kamenov A. The noisiest cities in the U.S. In: City-Data.com comprehensive information about United States; 2016. . Accessed 10 Dec 2019.
Kennedy C, Pincetl S, Bunje P. The study of urban metabolism and its applications to urban planning and design. Environ Pollut. 2011;159:1965–73.
Lee JGH, MacGregor-Fors I, Yeh PJ. Sunrise in the city: disentangling drivers of the avian dawn chorus onset in urban greenspaces. J Avian Biol. 2017;48:955–64.
Leonard ML, Horn AG. Does ambient noise affect growth and begging call structure in nestling birds? Behav Ecol. 2008;19:502–7.
Li J, Heap AD. A review of spatial interpolation methods for environmental scientists. Geoscience Australia, Record 2008/23; 2008.
Luther D, Gentry K. Sources of background noise and their influence on vertebrate acoustic communication. Behaviour. 2013;150:1045–6.
Luther DA, Phillips J, Derryberry EP. Not so sexy in the city: urban birds adjust songs to noise but compromise vocal performance. Behav Ecol. 2016;27:332–40.
MacGregor-Fors I. How to measure the urban-wildland ecotone: redefining 'peri-urban' areas. Ecol Res. 2010;25:883–7.
MacGregor-Fors I, García-Arroyo M. Who is who in the city? Bird species richness and composition in urban Latin America. In: MacGregor-Fors I, Escobar-Ibáñez JF, editors. Avian ecology in Latin American Cityscapes. Cham: Springer International Publishing; 2017. p. 33–55.
MacGregor-Fors I, Schondube JE. Gray vs green urbanization: Relative importance of urban features for urban bird communities. Basic Appl Ecol. 2011;12:372–81.
Maldonado JM. Ciudades y contaminación ambiental. Revista de Ingeniería. 2009;30:66–71.
Marín-Gómez OH, MacGregor-Fors I. How early do birds start chirping? Dawn chorus onset and peak times in a Neotropical city. Ardeola. 2019;66:327–41.
Marzluff JM. A decadal review of urban ornithology and a prospectus for the future. Ibis. 2016;159:1–13.
McAlexander TP, Gershon RRM, Neitzel RL. Street-level noise in an urban setting: assessment and contribution to personal exposure. Environ Health. 2015;14:18.
McKinney ML. Urbanization, biodiversity, and conservation. Bioscience. 2002;52:883–90.
McLaughlin KE, Kunc HP. Experimentally increased noise levels change spatial and singing behaviour. Biol Lett. 2013;9:20120771.
Melles S, Glenn S, Martin K. Urban bird diversity and landscape complexity: species-environment associations along a multiscale habitat gradient. Conserv Ecol. 2003;7:5.
Merchant ND, Fristrup KM, Johnson MP, Tyack PL, Witt MJ, Blondel P, et al. Measuring acoustic habitats. Methods Ecol Evol. 2015;6:257–65.
Nemeth E, Pieretti N, Zollinger SA, Geberzahn N, Partecke J, Miranda AC, et al. Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities. Proc R Soc B. 2013;280:20122798.
Ortega CP, Francis CD. Effects of gas-well-compressor noise on the ability to detect birds during surveys in northwest New Mexico. Ornithol Monogr. 2012;74:78–90.
Parris KM, Velik-Lord M, North JMA. Frogs call at a higher pitch in traffic noise. Ecol Soc. 2009;14:25.
Patricelli GL, Blickley JL. Avian communication in urban noise: causes and consequences of vocal adjustment. Auk. 2006;123:639–49.
Paul MJ, Meyer J. Streams in the urban landscape. Annu Rev Ecol Evol S. 2001;32:333–65.
Perillo A, Mazzoni LG, Passos LF, Goulart VD, Duca C, Young RJ. Anthropogenic noise reduces bird species richness and diversity in urban parks. Ibis. 2017;159:638–46.
Picket STA, Cadenasso ML, Grove JM, Nilon CH, Pouyat RV, Zipperer WV, et al. Urban ecological systems: linking terrestrial ecological, physical, and socioeconomic components of metropolitan areas. Annu Rev Ecol Syst. 2001;32:127–57.
R Core Team. R: A language and environment for statistical computing; 2019. .
Ralph CJ, Droege S, Sauer JR. Managing and monitoring birds using point counts: standards and applications. In: Ralph CJ, Sauer JR, Droege S, editors. Monitoring bird populations by point counts. USDA Forest Service, Pacific Southwest Research Station, General Technical Report PSW-GTR-149; 1995.
Sanborn A. Acoustic communication in insects. In: Capinera JL, editor. Encyclopedia of entomology. Dordrecht: Springer; 2008. p. 33–8.
Santiago-Alarcon D, Delgado-V CA. Warning! Urban threats for birds in Latin America. In: MacGregor-Fors I, Escobar-Ibáñez JF, editors. Avian ecology in Latin American Cityscapes. Cham: Springer International Publishing; 2017. p. 125–42.
Schütz C, Schulze CH. Functional diversity of urban bird communities: effects of landscape composition, green space area and vegetation cover. Ecol Evol. 2015;5:5230–9.
Slabbekoorn H. Songs of the city: noise-dependent spectral plasticity in the acoustic phenotype of urban birds. Anim Behav. 2013;85:1089–99.
Slabbekoorn H, den Boer-Visser A. Cities change the songs of birds. Curr Biol. 2006;16:2326–31.
Slabbekoorn H, Yang X-J, Halfwerk W. Birds and anthropogenic noise: singing higher may matter. Am Nat. 2012;180:142–5.
Sol D, Lapiedra O, González-Lagos C. Behavioural adjustments for a life in the city. Anim Behav. 2013;85:1101–12.
Stirnemann IA, Ikin K, Gibbons P, Blanchard W, Lindenmayer DB. Measuring habitat heterogeneity reveals new insights into bird community composition. Oecologia. 2015;177:733–46.
Warren PS, Katti M, Ermann M, Brazel A. Urban bioacoustics: it's not just noise. Anim Behav. 2006;71:491–502.
Movin, N., Gamova, T., Surmach, S.G. et al. Using bioacoustic tools to clarify species delimitation within the Blakiston's Fish Owl (Bubo blakistoni) complex. Avian Research, 2022.
DOI:10.1016/j.avrs.2022.100021
4.
Gwee, C.Y., Eaton, J.A., Ng, E.Y.X. et al. Species delimitation within the Glaucidium brodiei owlet complex using bioacoustic tools. Avian Research, 2019, 10(1): 36.
DOI:10.1186/s40657-019-0175-4
5.
Yee, S.A., Puan, C.L., Chang, P.K. Territorial and duet calls of three Malaysian owl species. Sains Malaysiana, 2018, 47(7): 1439-1445.
DOI:10.17576/jsm-2018-4707-11
Table
3.
Comparison of morphological measurements across Ninox sp. and the Singaporean carcass (in italic)
Wing
Tail
Wing/tail ratio
Ninox japonica
220.8 (214.0–226.8)
115.8 (107.5–122.6)
1.91 (1.75–2.03)
Ninox scutulata
195.7 (182.4–213.3)
109.5 (100.3–115.0)
1.78 (1.69–1.87)
Singapore carcass CR059
217.0
114.0
1.90
Average values are provided in mm with range given in brackets. Values highlighted show instances where measurement range overlaps with values from Singapore carcass
DownLoad:
Email Alerts
RSS Feeds