Volume 11 Issue 1
Apr.  2020
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Article Contents
Abstract
Background
Methods
Results
Discussion
Conclusions
Supplementary information
Acknowledgements
Authors' contributions
Availability of data and materials
Ethics approval and consent to participate
Consent for publication
Competing interests
References
Related Articles
Oscar Humberto Marín-Gómez, Michelle García-Arroyo, Camilo E. Sánchez-Sarria, J. Roberto Sosa-López, Diego Santiago-Alarcon, Ian MacGregor-Fors. 2020: Nightlife in the city: drivers of the occurrence and vocal activity of a tropical owl. Avian Research, 11(1): 9. DOI: 10.1186/s40657-020-00197-7
Citation: Oscar Humberto Marín-Gómez, Michelle García-Arroyo, Camilo E. Sánchez-Sarria, J. Roberto Sosa-López, Diego Santiago-Alarcon, Ian MacGregor-Fors. 2020: Nightlife in the city: drivers of the occurrence and vocal activity of a tropical owl. Avian Research, 11(1): 9. DOI: 10.1186/s40657-020-00197-7
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Nightlife in the city: drivers of the occurrence and vocal activity of a tropical owl

  • 1.

    Red de Ambiente y Sustentabilidad, Instituto de Ecología A.C., Carretera antigua a Coatepec 351, El Haya, 91073 Xalapa, Veracruz, Mexico

  • 2.

    Departamento de Ciencias Naturales y Matemáticas, Pontificia Universidad Javeriana Cali, 760044 Cali, Colombia

  • 3.

    Centro Interdisciplinario de Investigación para el Desarrollo Integral Regional Unidad Oaxaca (CIIDIR), Instituto Politécnico Nacional, Oaxaca, Mexico

  • 4.

    Dirección de Cátedras, Consejo Nacional de Ciencia y Tecnología (CONACYT), Mexico City, Mexico

  • 5.

    Red de Biología y Conservación de Vertebrados, Instituto de Ecología A.C, 91073 Xalapa, Veracruz, Mexico

Funds: 

OHM-G and MG-A were supported by the graduate Grant provided by the National Council of Science and Technology CONACYT 417094

OHM-G and MG-A were supported by the graduate Grant provided by the National Council of Science and Technology 416452

as well as the Doctoral and Master Program of the Instituto de Ecología, A.C. INECOL, Xalapa

JRSL thanks CONACYT project Grant 251526

a chair fellowship at CIIDIR researcher number 1640

a chair fellowship at CIIDIR project number 1781

More Information
    Graphical Abstract
    • Abstract
  • Background 

    Cities differ from non-urban environments by the intensity, scale, and extent of anthropogenic pressures, which can drive the occurrence, physiology, and behavior of the organisms thriving in these settings. Traits as green cover often predict the occurrence patterns of bird species in urban areas. Yet, anthropogenic noise and artificial light at night (ALAN) could also limit the presence and disrupt the behavior of birds. However, there is still a dearth of knowledge about the influence of urbanization through noise and light pollution on nocturnal bird species ecology. In this study, we assessed the role of green cover, noise, and light pollution on the occurrence and vocal activity of the Mottled Owl (Ciccaba virgata) in the city of Xalapa (Mexico).

    Methods 

    We obtained soundscape recordings in 61 independent sites scattered across the city of Xalapa using autonomous recording units. We performed a semi-automated acoustic analysis of the recordings, corroborating all Mottled Owl vocalizations. We calculated two measures of anthropogenic noise at each study site: daily noise (during 24 h) and masking noise (mean noise amplitude at night per site that could mask the owl's vocalizations). We further performed generalized linear models to relate green cover, ALAN, daily noise, and masking noise in relation to the owl's occurrence (i.e., detected, undetected). We also ran linear models to assess relationships among the beginning and ending of vocal activity with ALAN, and with the anthropogenic and masking noise levels at the moment of which vocalizations were emitted. Finally, we explored variations of the vocal activity of the Mottled Owl measured as vocalization rate across time.

    Results 

    The presence of Mottled Owls increased with the size of green cover and decreased with increases in both artificial light at night and noise levels. At the temporal scale, green cover was positively related with the ending of the owl's vocal activity, while daily noise and ALAN levels were not related to the timing and vocal output (i.e., number of vocalizations). Furthermore, the Mottled Owl showed a marked peak of vocal activity before dawn than after dusk. Although anthropogenic noise levels varied significantly across the assessed time, we did not find an association between high vocal output during time periods with lower noise levels.

    Conclusions 

    Spatially, green cover area was positively related with the presence of the Mottled Owl in Xalapa, while high noise and light pollution were related to its absence. At a temporal scale, daily noise and ALAN levels were not related with the timing and vocal output. This suggests that instead of environmental factors, behavioral contexts such as territoriality and mate interactions could drive the vocal activity of the Mottled Owl. Further studies need to incorporate a wider seasonal scale in order to explore the variation of different vocalizations of this species in relation to environmental and biological factors.

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  • Extra-pair paternity (EPP) has received great attention during recent decades, after Trivers (1972) argued that males should seek additional copulations, while females should choose males that could increase the genetic quality or the genetic constitution of offspring. Several hypotheses have been put forward to achieve a better understanding of the potential benefits of this behaviour. Empirical studies have found support for different benefits, although most attention has been given to the "good genes" hypothesis, predicting that females use male phenotypic cues to assess male genetic quality from which the offspring might benefit (Westneat et al. 1990; Birkhead and Møller 1992; Hasselquist et al. 1996; Griffith et al. 2002). Alternatively, "compatible genes" where the genes of an extra-pair male fit better with the genes of the female than those of the social partner may increase offspring fitness (Kempenaers et al. 1999; Tregenza and Wedell 2000; Griffith and Immer 2009). Females' benefits from EPP may also include fertility insurance (Birkhead and Møller 1992; Sheldon 1994; Schmoll and Kleven 2016) and access to resources (Wolf 1975; Gray 1997). However, these benefits have received less empirical support (Griffith et al. 2002). Social mates pay the main costs are loss of parental care (Birkhead et al. 1993; Suter et al. 2009), while costs of partner assessment (Petrie and Kempenaers 1998) and transmission of sexually transmitted diseases (Sheldon 1993) have also been suggested for males and females involved in EPP.

    The Hamilton and Zuk hypothesis predict that females should choose mates with signals reliably reflecting resistance against parasites in the context of sexual selection (Hamilton and Zuk 1982; Møller 1990). Males expressing resistance to parasites may provide more parental care, as they suffer lower rates of parasites (Milinski and Bakker 1990), but also transmit resistance genes to offspring, which also benefit females (Hamilton and Zuk 1982). Regardless of the explanation, males revealing their resistance to potential female partners will more likely obtain extra-pair copulations. This was demonstrated for instance in the House Finch (Carpodacus mexicanus) in which carotenoid-based feather coloration was negatively correlated with the amount of feather-degrading bacteria (Shawkey et al. 2009), while poor male condition was related to the presence of other parasites (Thompson et al. 1997). Thus, males signalling his phenotypic quality including resistance to parasitism will more easily access to females including extra-pair females.

    However, extra-pair copulations would also imply the transmission of microorganisms between males and females, which may have beneficial (Lombardo et al. 1999) or pathogenic effects. Costs of EPP associated to parasitism and/or antiparasitic defences are in case scarcely studied. As examples of parasites' transmission during copulation, Ring-necked Pheasants (Phasianus colchicus) are known to transmit ectoparasites from male to female during copulation (Hillgarth 1996). Thus, as mating with several partners will expose individuals to potential parasite transmission, this could affect both individuals and the outcome of the reproductive event. Any males with superior resistance should be better to avoid potential costs or simply be better adapted to reduce the consequences for the costs of extra-pair paternity. Since birds usually signal their antiparasitic capabilities throughout plumage brightness (Hamilton and Zuk 1982), related characters should also play a crucial role describing which males could gain multiple mating. Hence, understanding potential relationships between parasites and defence mechanisms should help understand the underlying mechanisms behind EPP (Westneat and Stewart 2003).

    By definition, secondary sexual traits are important for gaining multiple mating, and these traits are often reflected in colour and brightness (Baker and Parker 1979), which, as mentioned before, usually reveals resistance of individuals to parasitic infection (Hamilton and Zuk 1982). Several secondary sexual traits, including feather coloration, are condition-dependent, hence indicating high-quality individuals (Andersson 1994). It is known for instance that more colourful individuals in the Greater Flamingo (Phoenicopterus roseus) had higher breeding success (Amat et al. 2011), and that plumage brightness was related to chick development in Blue Tits (Cyanistes caeruleus) (Senar et al. 2002), both results suggesting a direct link between feather coloration and important fitness components. Thus, any characteristics that prevented feather deterioration or enhance parasite resistance will be sexually selected and, consequently, should predict the strength of sexual selection. The uropygial gland is a good candidate trait, mainly because its main function is to protect feathers from degradation agents including microorganisms (Moreno-Rueda 2017; Azcárate-García et al. 2020) but also because its size or volume of secretion predicts selection pressures due to ectoparasites (Magallanes et al. 2016).

    The objective of this study was to test the prediction relating EPP and the size of the uropygial gland among 60 bird species. The relationship between the size of the uropygial gland and bacterial diversity has been investigated several times (Møller et al. 2009; Jacob et al. 2014). Secretions from the uropygial gland have been demonstrated to act as antiparasitic defence in some species, although generally assumed for many species, especially against feather-degrading bacteria (Jacob and Ziswiler 1982; Møller et al. 2009; Ruiz-Rodríguez et al. 2009), which can affect interspecific interactions such as predation (Møller et al. 2010), but also sexually selected feathers (Ruiz-Rodríguez et al. 2015). Simultaneously, secretions from the uropygial gland have been shown to increase colour intensity (Amat et al. 2011) and affect plumage brightness (Moreno-Rueda 2010). However, the relationship between EPP and the uropygial gland remains poorly understood. Here we provide, to our knowledge, the first test of the hypothesis that the level of EPP is positively related to the size of the uropygial gland, which will suggest a direct link between uropygial gland and the strength of sexual selection.

    Uropygial gland

    Uropygial gland data from Jacob and Ziswiler (1982)

    We extracted information on the size of the uropygial gland using Jacob and Ziswiler (1982) as a source. We assumed that a larger uropygial gland could produce more secretions than a smaller gland, which was demonstrated at an intraspecific level in Barn Swallows (Hirundo rustica) (Møller et al. 2009) and is discussed at the interspecific level by Soler et al. (2012).

    Extra-pair paternity data

    Estimates of species-specific extra-pair paternity rate were extracted from Griffith et al. (2002). Extra-pair paternity was defined as the proportion of offspring that was extra-pair offspring. In a second data set we used the proportion of broods that held extra-pair offspring. Data since 2002 were extracted from the Web of Science. In total, estimates of both EPP and uropygial gland size were available for 60 species (Additional file 1: Table S1).

    Body mass

    Body mass was extracted from Dunning (2008).

    Comparative analysis

    Species characteristics are not statistically independent because they share their evolutionary history. We adjusted for this dependence using comparative analyses. We controlled for phylogenetic uncertainty, using phylogenetic relationships among species. This was done by using 100 phylogenetic ultrametric trees for all the species included in the analysis from https://birdtree.org/ (accessed April 2020). All models were fitted to the different trees by using Bayesian phylogenetic models from the MCMCglmm package (Hadfield 2010). The MCMC algorithm was set to 2, 000, 000 iterations, with a burn-in period of 100, 000 and a thinning interval of 1000. Geweke's convergence diagnostic was used for Markov chains, giving a z-score of the first 10% and last 50% of the means in the chain (Geweke 1992). The models use the frequency of EPP (proportion of broods with extra-pair paternity) as response variable, and log10-transformed uropygial gland size from Jacob and Ziswiler (1982), log10-transformed body mass from Dunning (2008) and sample sizes for EPP as explanatory continuous variables. Model 1 assumes Poisson distribution, while Model 2 assumes Gaussian distribution, and these models are further weighted for sample size to account for uneven sampling effort (Garamszegi and Møller 2010). Tests of the random effect of phylogeny for the 100 phylogenetic trees was performed and assessed as heritability (h2), a measure of phylogenetic signal ranging between zero and one (Hadfield 2010). For all the independent factors (log10-transformed uropygial gland size, log10-transformed body mass and sample sizes for EPP), the averaging estimates, lower and upper values of the confidence interval (95% CI), calculated as upper and lower 95% credibility interval values of the estimates of the 100 models, the 95% CI for the 100 models for pMCMC values, z-score of the Geweke's convergence diagnostic, effective sample sizes and autocorrelations are reported.

    Uropygial gland size and EPP

    When corrected for phylogeny in comparative analyses, there was a significant positive relationship between level of EPP and size of the uropygial gland for both models (Fig. 1) and body mass, but not with sample sizes for EPP (Table 1). The size of the uropygial gland is from previous studies known to correlate positively with body size (Møller et al. 2010) and the amount of wax produced (Elder 1954; Møller et al. 2009; Pap et al. 2010). Hence, we assume that the size of the uropygial gland represents the relative amount of wax and, thus, larger amounts of the antiparasitic defence properties that can affect the integrity of feathers, hence give plumage in better condition (Azcárate-García et al. 2020) as well as their coloration and brightness (Amat et al. 2011; Moreno-Rueda 2017).

    Figure  1.  Association between residuals of rate of extra pair paternity and volume of the uropygial gland of the 60 avian species considered in the study after controlling for the effect of body mass. Line is the regression line and size of circles are proportional to log10-transformed sample size used to estimate extra pair paternity in each species
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    Table  1.  Relationships with prevalence of extra-pair paternity (EPP) using comparative analysis
    Model Estimate Lower 95% CI Upper 95% CI ESS lower 95% CI ESS upper 95% CI Autocorrelation lower 95% CI Autocorrelation upper 95% CI (z-score) Lower 95% CI (z-score) Upper 95% CI pMCMC (‒95%CI) pMCMC (+95%CI)
    Model 1
    Uropygial gland size 1.260 0.101 2.473 1885.762 1938.241 ‒0.006478 0.002344 ‒0.05068 0.39434 0.030 0.034
    Body mass ‒1.657 ‒3.035 ‒0.312 1892.864 1944.279 ‒0.005594 0.002843 ‒0.38670 0.08815 0.015 0.022
    N EPP 3.382 2.668 4.115 1889.632 1948.191 ‒0.002031 0.007548 ‒0.35252 0.21599 0.000 0.000
    Phylogeny (h2) 0.98753 0.02968 0.99831
    Model 2
    Uropygial gland size 0.182 0.049 0.316 1877.943 1931.508 ‒0.00669 0.00251 ‒0.19885 0.22043 0.009 0.014
    Body mass ‒0.272 ‒0.420 ‒0.124 1893.361 1931.874 ‒0.00625 0.00293 ‒0.28063 0.13554 0.001 0.002
    Phylogeny (h2) 0.57187 0.21314 0.84883
    Summary of MCMCglmm models with frequency of EPP as the response variable and Log10-transformed uropygial gland size, Log10-transformed body mass and total number of nests per species sampled for EPP (N EPP) as explanatory continuous variables. The models assume Poison (Model 1) and Gaussian (Model 2) distributions and the random effect of phylogeny was tested for each of the 100 phylogenetic trees considered and assessed as heritability (h2). For each factor, we report the average of estimates, as well as the lower and upper values of the confidence interval (95% CI), which were calculated respectively on the lower and upper 95% credibility interval values of the estimates of the 100 models. We also report 95% CI of the 100 models (i.e., one for each of the phylogenetic trees considered) for pMCMC values, z-scores of the Geweke's convergence diagnostic, effective sample sizes (ESS), and autocorrelations. Values in italics are statistically significant (pMCMC < 0.05).
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    The main finding in this study is that the size of the uropygial gland is positively related to the level of EPP at the interspecific level. This is in line with the predictions regarding the role of secretions of the uropygial gland in both antimicrobial defence and plumage brightness (Moreno-Rueda 2017). The specific function of the uropygial gland on these two processes, however, remains unknown.

    Previous studies have documented transmission of microorganisms from males to females through mating events (Hillgarth 1996; Westneat and Rambo 2000) and other social events (Brown et al. 2001). This mechanism is one of few, but still poorly understood costs of EPP. However, the related costs can be of crucial importance in order to maintain this behaviour (Westneat and Stewart 2003), and mechanisms to reduce the costs are expected. The size of the uropygial gland is positively related to the amount of secretions produced for a variety of species (Elder 1954; Møller et al. 2010; Pap et al. 2010) as the gland is made up of tubules where secretion of the substances occur (Jacob and Ziswiler 1982), and secretions are hypothesized to have antiparasitic substances (Moreno-Rueda 2017). Hence, selection for defence through uropygial gland secretions could be an important factor for fitness components such as reproductive success (Whittaker et al. 2013) and survival (Merino et al. 2000; Møller et al. 2010; Magallanes et al. 2017).

    Both Møller et al. (2010) and Soler et al. (2012) documented a relationship between bacterial abundance and load with size of the uropygial gland, with the substances secreted by the gland hypothesised to act as antimicrobial defence. Here, we demonstrated that, when corrected for phylogeny, the level of EPP was positively related to uropygial gland size. Due to the potential transmission of bacteria through mating (Hillgarth 1996; Westneat and Rambo 2000), the relatively increased size of the uropygial gland, and hence amount of wax, could be an important defence mechanism to reduce this cost. Hence, we suggest that the increased size of the uropygial gland, and further the amount of wax, may have arisen as coevolutionary responses to reduce the associated costs of EPP.

    Species with higher intraspecific levels of EPP often show more intense selection on secondary sexual traits, caused by greater variance in reproductive success (Yezerinac et al. 1995; Møller 1997; Whittingham and Dunn 2005). Furthermore, there is a negative relationship between secondary sexual ornaments and the loss of within-pair paternity (Møller and Ninni 1998). Several hypotheses have linked the intensity of secondary sexual traits to parasite resistance, such as the Hamilton-Zuk (1982) hypothesis. The size of the uropygial gland has been shown to correlate positively with secondary sexual traits (Moreno-Rueda 2010), plumage brightness (Møller and Mateos-González 2019) and colour intensity (Amat et al. 2011). Moreover, ornamental feathers are more easily degraded by bacteria (Ruiz-Rodríguez et al. 2015; Azcárate-García et al. 2020), and individuals with larger uropygial glands were those better protecting their ornamental feathers from degradation, which could result in more attractive plumage (Ruiz-Rodríguez et al. 2015). Hence, secretions from the uropygial gland can be an important factor promoting the acquisition of gain extra-pair copulations since several of these are likely to be condition-dependent (Andersson 1994).

    In light of this finding, uropygial gland is likely influenced by sexual selection, but more research is needed in order to acquire a better understanding of the role of the uropygial gland in EPP. Studies using a representative measure of feather bacteria are needed to investigate the effect of uropygial gland secretions in relation to EPP. Furthermore, a similar interspecific investigation is needed regarding plumage brightness and coloration, although a positive relationship is found in species-specific studies (Galvan and Sanz 2006; Moreno-Rueda 2010; Amat et al. 2011). However, these two processes are not mutually exclusive, and they may act simultaneously as described here.

    Here we demonstrate, to our knowledge, the first finding of a positive relationship between the size of the uropygial gland and the level of EPP. This, together with previous findings of the role of uropygial gland, suggest that the size of uropygial gland size could be selected for through exaggeration of secondary sexual traits and/or signalling antimicrobial defence mechanism. This provides important insight to the role of secretions by the uropygial gland on EPP. Future investigations should focus on the effect of uropygial gland secretions and explore the relationship between EPP and size of uropygial gland at an intraspecific level.

    Supplementary information accompanies this paper at https://doi.org/10.1186/s40657-020-00226-5.

    We would like to thank Camilla Marnor, Simen C. Karlsen, Mikael A. Sætre and Per H. Rishøi for discussion of the literature in early parts of the study. Jordi Moya help us to implement R' scripts to perform the analyses of the 100 phylogenetic trees considered at the same time.

    APM conceived the idea. APM extracted the data. JJS made the comparative analyses. APM and JSS wrote the paper. All authors read and approved the final manuscript.

    The data on which this paper was made are fully available at the appendix of the manuscript.

    Not applicable.

    Not applicable.

    The author declares no competing interests.

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