Notes on the breeding biology of common resident birds in an urbanized area of Hidalgo, Mexico

Notas sobre la biología reproductiva de aves residentes comunes en una zona urbanizada de Hidalgo, México

Iriana Zuria* and Georgina Rendón–Hernández

Centro de Investigaciones Biológicas, Universidad Autónoma del Estado de Hidalgo. Apartado Postal 69–1 Plaza Juárez, Pachuca, Hidalgo, 42001, México. *Correo electrónico: izuria@uaeh.edu.mx, izuria@yahoo.com.

Received: 23^rd June 2009
Revision accepted: 2^nd June 2010
Asociated editor: Patricia Ramírez Bastida

Abstract

We present data on the breeding biology and nest site characteristics of the six most frequent nesters in a small ecological reserve immersed in the city of Pachuca, Hidalgo, Mexico: Columbina inca (Inca Dove), Pyrocephalus rubinus (Vermilion Flycatcher), Campylorhynchus brunneicapillus (Cactus Wren), Toxostoma curvirostre (Curve–billed Thrasher), Pipilo fuscus (Canyon Towhee), and Carpodacus mexicanus (House Finch). We followed 65 active nests, mainly of C. mexicanus and C. brunneicapillus; density of nests reached up to 15 nests ha^–1 in some areas of the park. The main causes of reproductive failure in the failed nests (74%) were heavy storms and human disturbance. Nests were found on seven plant substrates, mainly on Cylindropuntia imbricata and Cupressus spp. Data on nest site characteristics, including the plants used for nesting, their average height and dbh, average height of the nest, clutch size, extent of the breeding season, and particular causes of nest failure is presented for each species. At the end we suggest some general management recommendations that will aid in the conservation of breeding birds in parks of central Mexico.

Key words: nest site characteristics, breeding phenology, reproductive failure, Pachuca, urbanization.

Resumen

Palabras clave: características del sitio de anidación, fenología reproductiva, fracaso reproductivo, Pachuca, urbanización.

Introduction

Collecting information on breeding biology and performance is an important part of many population ecology studies on birds, and it is often essential in identifying effective conservation measures (Green 2004). For many bird species that breed in Mexico, there is still very little published information on breeding phenology, nest site characteristics, nest microhabitat, and causes of reproductive failure, even for species that are widespread, conspicuous, or associated with human habitats. This knowledge is relevant for conservation and management purposes, especially in areas with high urbanization rates, like many places in Mexico, where urban growth is not well planned or regulated, resulting in the reduction, isolation, and degradation of habitat.

Urbanization is increasing especially in developing nations, and there is an urgent need to thoroughly review and comprehend its effects on wildlife in order to understand both the ecological implications of increasing urbanization, and how to mitigate its threat to biodiversity (McKinney 2002, Chamberlain et al. 2009). Several studies have analyzed the effects of urbanization on bird diversity and community composition (e.g., Beissinger and Osborne 1982; Blair 1996; Marzluff 2001; Chace and Walsh 2006, Donnelly and Marzluff 2006), but only a few have explored the urban impacts on bird breeding biology (reviewed by Chamberlain et al. 2009). The knowledge of nesting requirements, breeding seasons, and other aspects of the reproductive biology of resident birds in urbanized landscapes would help land managers and administrators to develop compatible management strategies with avifauna conservation.

Here we present some data on the breeding biology and nest site characteristics of the six most frequently encountered nesters in a small ecological reserve immersed in the city of Pachuca, Hidalgo, Mexico: Columbina inca (Inca Dove), Pyrocephalus rubinus (Vermilion Flycatcher), Campylorhynchus brunneicapillus (Cactus Wren), Toxostoma curvirostre (Curve–billed Thrasher), Pipilo fuscus (Canyon Towhee), and Carpodacus mexicanus (House Finch). Most studies on the breeding biology of these species have been done in North America, especially in Arizona, USA (reviewed by Hill 1993, Tweit 1996, Johnson and Haight 1996, Proudfoot et al. 2000, Wolf and Jones 2000, and Mueller 2004), and many authors report the need to study populations of these species in other regions. For example, Proudfoot et al. (2000) reported the need to study C. brunneicapillus populations in Mexico; Wolf and Jones (2000) concluded that most aspects of the life history of P. rubinus remain unknown, habitat requirements for the species need to be more clearly delineated, and the causes and rates of mortality, annual and lifetime reproductive success, and population regulation are areas needing further study; Mueller (2004) also reported the need for more studies on C. inca, stating that even though it is expanding its range in North America and thus generates little conservation concern, this species has not been the subject of enough research. We also identified the causes of reproductive failure for nesting birds in this area and propose some general management recommendations.

Methods

The study was conducted in a small ecological reserve immersed in the city of Pachuca (Figure 1), an area with a high rate of population growth (mean annual growth rate for the period 2000–2005 up to 9.0%, INEGI 2008) and high population density (about 1,411 people per km², INEGI 2008). The reserve, called "Parque Ecológico Cubitos", has an extension of 90 ha, and it is located between 20°06'33"–20°07'39"N and 98°44'60"–98°45'00"W, with an elevation of 2,300 m. The natural vegetation is represented by open scrub forest or arid tropical scrub (Rzedowski 1994). The dominant species are agaves (Agave lechuguilla, A. salmiana), yucca (Yucca filifera), several cacti species (Cylindropuntia imbricata, Opuntia streptacantha, O. spinulifera, O. robusta, Stenocactus sp., Coryphantha sp.), and the non–native pepper tree or pirul (Schinus molle), among others (COEDE 2004). A smaller portion of the park is covered by introduced vegetation, including several species of pines (Pinus cembroides, P. torreyana, P. pinceana), cypress (Cupressus guadalupensis, C. macrocarpa), and other trees like pirul and privet (Ligustrum japonicum). The park is divided in two main areas: a small area designed for recreational purposes, that includes the area covered by introduced vegetation, and an area where human access is restricted.

The avifauna includes 76 species, 21 considered permanent residents (Zuria et al. 2009). Some of the mammals present in the park are potential nest predators: Bassariscus astutus (ringtail), Spermophillus variegatus (rock squirrel), Urocyon cinereoargenteus (gray fox), and domestic dogs and cats (Tirado–Aviles 2009).

We surveyed different areas of the park for nests between June 2005 and December 2006. We followed the methods described by Ralph et al. (1993) for locating and monitoring nests. Nests were located mainly during nest construction by searching and following birds with nesting material. Direct searches were also conducted in trees and shrubs where adults were frequently observed.

We recorded the location of each nest using a GPS, and we also recorded the following: bird species, state of the nest (active, inactive, in construction, completed, adults incubating, etc.), nest content (number of eggs, chicks or fledglings), nest substrate (i.e., species of plant containing the nest), plant height (cm), plant dbh (diameter at breast height in cm; however, for cacti we used the diameter of the main stem at 5 cm above the ground), and nest height (cm). We used a one–way analysis of variance (ANOVA) or a Kruskal–Wallis test (non–parametric alternative) to compare plant and nest height between species. The Tukey test (or the Dunn's method for the non–parametric test) was used for a posteriori comparisons of means when the previous analyses indicated significant effects (Sokal and Rohlf 1995). Analyses were performed using SigmaStat ver. 3.5. All nests were checked every three days and we recorded any change in status and the date it occurred. From all our observations we constructed a breeding calendar for each of the six species considered.

For each nest we also obtained hatching success or the percentage of eggs that hatched from the nests (Gore and Kinnison 1991), and nest success or the percentage of nests that fledged at least one young. We also identified the causes or reproductive failure based on nest and egg remains, and classified them in the following categories: "nest destroyed by rain" which included nests partly destroyed on the plant or on the floor that were found after a heavy storm; "nest destroyed by a predator" consisted of nests found in the original place, but without its contents, with hair, tracks or excrement in the vicinity; "human disturbance" included nests that completely disappeared, with footprints in the vicinity, or when we saw evidence that the tree had been pruned; and "unknown" (Green 2004).

Results

We were able to follow 65 active nests, most of them being of Carpodacus mexicanus and Campylorhynchus brunneicapillus (Table 1). Density of nests reached up to 15 nests ha^–1 in some areas of the park, especially in the area covered by introduced trees, where Carpodacus mexicanus, Columbina inca, and Pipilo fuscus were the most abundant nesters; C. brunneicapillus nests were abundant in the area covered by natural vegetation. The hatching and nest success were variable among species (Table 1), Toxostoma curvirostre was the most successful nester since two out of the three nests fledged at least one young, while C. brunneicapillus had the lowest nest success (Table 1). In general, 74% of the nests failed; most nests that failed (54%) were destroyed by heavy storms, in particular, the most affected species were C. brunneicapillus, C. mexicanus, C. inca, and Pyrocephalus rubinus. Six percent of the failed nests were destroyed by humans, who stole chicks and damaged nests during maintenance operations (e.g., pruning); Pipilo fuscus and Carpodacus mexicanus were most affected by human activities. We could not determine the causes of nest failure in 35% of the failed nests, and we only registered two events of nest predation.

Nests were found on seven plant substrates, mainly on Cylindropuntia imbricata and Cupressus spp. (Figure 2). Most frequently used substrate varied among species; for example, Campylorhynchus brunneicapillus nested mainly on Cylindropuntia imbricata, while Carpodacus mexicanus used Cupressus macrocarpa (Table 2). In general, we found significant differences in plant heights used by the species (H = 36.17, d.f. = 5, P < 0.001). Carpodacus mexicanus nested in significantly taller plants than Campylorhynchus bruneicapillus (Table 2), while all other comparisons between species were not significant. We also found significant differences in nest heights (F = 6.32, d.f.= 5, 67, P < 0.001), and again the only significant difference was between Carpodacus mexicanus and Campylorhynchus bruneicapillus (Table 2).

The extent of the breeding season for each species showed that Carpodacus mexicanus presented the longer breeding season, since we observed individuals involved in breeding activities from January to November. Pyrocephalus rubinus presented the shorter breeding period. May, June and July can be considered the most important months of the breeding season in the park because all species were nesting (Table 3).

Discussion

The six species considered in this study reproduce in the park, and we observed fledglings for all of them. Although these species can be common in urbanized landscapes, it is still necessary to study some aspects of their breeding biology, especially south of the USA. Knowledge of the breeding seasons, nesting requirements and causes of failure is fundamental in order to design adequate management strategies, especially for Latin American countries, where these factors are rarely considered in urban development or when designing green areas in cities.

Overall, the most frequently used nesting substrates in the park were cane cholla (Cylindropuntia imbricata) and cypress trees (Cupressus spp.). These two species represent the two types of nesting substrates present in our study site: native plants common in the natural vegetation and introduced vegetation. The presence of both types of substrates probably favors a more diverse bird breeding community, and particular plant species can be used in order to attract some birds. For example, most nests of Campylorhynchus brunneicapillus were found on cane cholla, knowledge that can be used for management purposes. It has been reported that some birds prefer to nest under the greater protective cover of exotic plants than native plants, but more studies are needed in order to understand if introduced vegetation could be acting as a population sink for some species, because predators may also be using these areas for foraging (Chace and Walsh 2006). Nesting substrates and nest heights for the six species studied coincide with previous reports for North America (reviewed by Hill 1993, Johnson and Haight 1996, Tweit 1996, Proudfoot et al. 2000, Wolf and Jones 2000, Mueller 2004).

In general, clutch sizes for most species were in the low end of the clutch size range reported in the literature (Table 1). Lower clutch sizes have been observed in urban landscapes, especially for species living at high densities, which may experiment a greater competition for food in the breeding season that could lead to lower clutch sizes (Chamberlain et al. 2009).

More studies are needed to understand how natural and artificial food may influence demographic differences, especially in urbanized landscapes.

Few studies have explored the urban impacts on reproductive success (Chace and Walsh 2006). Identifying the causes of nest failure in urbanized landscapes is also important in order to understand bird demography and productivity, which in turn may allow us to adopt adequate management strategies. In our study, heavy precipitations, accompanied by high winds, observed during the rainy season (May to October), were the main cause of reproductive failure. In 2005 and 2006 the mean annual precipitation was below average in this region of Mexico (CNA 2008); however, during 2005 hurricane activity was above average (Rosengaus and Hernández–Unzón 2005) with seven hurricanes affecting Mexico, and with several storms registered in the state of Hidalgo (CNA 2008). Heavy precipitation has been reported before as the most important cause of reproductive failure (e.g., DeSante and Geupel 1987). However, some species are able to renest two or three times after a nest has been destroyed. It is known that Campylorhynchus brunneicapillus (Proudfoot et al. 2000), Toxostoma curvirostre (Tweit 1996), Pipilo fuscus (Johnson and Haight 1996) and Carpodacus mexicanus (Hill 1993) can renest several times in a single nesting season. So it is possible that many of the nests we observed later in the season were second or third nesting attempts. Human disturbance was the second cause of reproductive failure, especially in areas of the park where human access was permitted for recreational purposes. People stole chicks and destroyed nests during maintenance operations (e.g., pruning). We registered only a few nest predation events. However, it is possible that predation could have been higher since we were not able to identify the cause of failure for many nests. A large number of nest predators like domestic cats and dogs, as well as gray foxes, have been observed in the park. In Mexico, abandoned cats and dogs roam freely in urbanized landscapes and sometimes form feral populations that are not managed adequately. It is known that domestic predators are responsible for the high predation rates observed in many urban settings (Hoover et al. 1995, Jokimâki and Huhta 2000, Haskell et al. 2001, Chace and Walsh 2006, Forrest and Clair 2006).

Birds nesting in urbanized landscapes must tolerate many annoying factors in order to reproduce successfully, for example human disturbance (e.g., noise, human presence, management practices, etc.), pollution, predators (Haskell et al. 2001), and the presence of different or exotic nesting substrates (Reichard et al. 2001). However, green spaces in urban areas are important for many birds because they represent the only places where birds can find adequate nesting substrates and feeding opportunities. It is still possible to improve breeding conditions for birds in urban areas if adequate management practices are adopted. Based on our observations, we suggest some general management recommendations that will aid in the conservation of breeding birds in parks of central Mexico: (1) maintenance operations should be limited or restricted while birds are nesting, therefore it is necessary to know the breeding calendar of the species that inhabit the green area. In particular for Parque Ecológico Cubitos, maintenance operations should be minimized from May to July. (2) Populations of domestic cats and dogs, and other invasive predators that roam vegetated areas should be controlled. (3) A program to educate park administrators, managers and the general public on the importance of birds in urban areas should be developed and implemented.

Acknowledgements

We are grateful to the following institutions for their generous support: SEMARNAT–CONACYT, FOSEMARNAT–2004–01–195 "Efectos de urbanización sobre comunidades de aves y mamíferos en los municipios de Pachuca de Soto y Mineral de la Reforma, Hidalgo, México: El Parque Ecológico Cubitos"; PROMEP, SEP, PROMEP/103.5/06/1759–UAEHGO–PTC–317 "Caracterización de los bordes agrícolas y su avifauna en agroecosistemas del estado de Hidalgo"; and FOMIX Hidalgo 95828 (second phase) "Diversidad Biológica del Estado de Hidalgo". We appreciate helpful comments on the manuscript by two anonymous reviewers.

Literature cited

Beissinger, S.R. and D.R. Osborne. 1982. Effects of urbanization on avian community organization. Condor 84:75–83.         [ Links ]

Blair, R.B. 1996. Land use and avian species diversity along an urban gradient. Ecological Applications 6:506–519.         [ Links ]

Chace, J.F. and J.J. Walsh. 2006. Urban effects on native avifauna: a review. Landscape and Urban Planning 74:46–69.         [ Links ]

Chamberlain, D.E., A.R. Cannon, M.P. Toms, D.I. Leech, B.J. Hatchwell, and K.J. Gaston. 2009. Avian productivity in urban landscapes: a review and meta–analysis. Ibis 151:1–8.         [ Links ]

CNA (Comisión Nacional del Agua). 2008. Precipitación media mensual. Comisión Nacional del Agua, Servicio Meteorológico Nacional. <http://smn.cna.gob.mx> (accessed July 2008).         [ Links ]

COEDE (Consejo Estatal de Ecología). 2004. Programa de manejo del Área Natural Protegida Estatal Parque Ecológico Cubitos. Consejo Estatal de Ecología. Pachuca, Hidalgo.         [ Links ]

DeSante, D.F. and G.R. Geupel. 1987. Landbird productivity in central coastal California: the relationship to annual rainfall, and a reproductive failure in 1986. Condor 89:636–653.         [ Links ]

Donnelly, R. and J.M. Marzluff. 2006. Relative importance of habitat quantity, structure, and spatial pattern to birds in urbanizing environments. Urban Ecosystems 9:99–117.         [ Links ]

Forrest, A. and C.C. St. Clair. 2006. Effects of dog leash laws and habitat type on avian and small mammal communities in urban parks. Urban Ecosystems 9:51–66.         [ Links ]

Gore, J.A. and M.J. Kinnison. 1991. Hatching success in roof and ground colonies of Least Terns. Condor 93:759–762.         [ Links ]

Green, R.E. 2004. Breeding biology. Pp. 57–83. In: W.J. Sutherland, I. Newton, and R.E. Green (eds.). Bird Ecology and Conservation. A Handbook of Techniques. Oxford University Press. New York.         [ Links ]

Haskell, D.G., A.M. Knupp, and M.C. Schneider. 2001. Nest predator abundance and urbanization. Pp. 243–258. In: J.M. Marzluff, R. Bowman, and R. Donnelly (eds.). Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers. Norwell, Massachusetts.         [ Links ]

Hill, G.E. 1993. House Finch (Carpodacus mexicanus). In: A. Poole and F. Gill (eds.). The birds of North America No. 46. The birds of North America, Inc. Philadelphia, Pennsylvania.         [ Links ]

Hoover, J.P., M.C. Brittingham, and L.J. Goodrich. 1995. Effects of forest patch size on nesting success of Wood Thrushes. Auk 112:146–155.         [ Links ]

INEGI (Instituto Nacional de Estadística y Geografía). 2008. Datos de Hidalgo. Estadísticas a propósito del día mundial de la población. Pachuca de Soto, Hidalgo, Instituto Nacional de Estadística, Geografía e Informática. México. <http://www.inegi.org.mx/inegi/contenidos/espanol/prensa/contenidos/estadisticas/2009/poblacion13.doc> (accessed November 2008).         [ Links ]

Johnson, R.R. and L.T. Haight. 1996. Canyon Towhee (Pipilo fuscus). In: A. Poole and F. Gill (eds.). The birds of North America. The birds of North America, Inc. Philadelphia, Pennsylvania.         [ Links ]

Jokimâki, J. and E. Huhta. 2000. Artificial nest predation and abundance of birds along an urban gradient. Condor 102:838–847.         [ Links ]

Marzluff, J.M. 2001. Worldwide urbanization and its effects on birds. Pp. 19–47. In: J.M. Marzluff, R. Bowman, and R. Donnelly (eds.). Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers. Norwell, Massachusetts.         [ Links ]

McKinney, M.L. 2002. Urbanization, biodiversity, and conservation. BioScience 52:883–890.         [ Links ]

Mueller, A.J. 2004. Inca Dove (Columbina inca). In: A. Poole (ed.). The birds of North America Online, Cornell Laboratory of Ornithology. Ithaca, New York. <http://bna.birds.cornell.edu/BNA/account/IncaDove/> (accessed May 2009).         [ Links ]

Proudfoot, G.A., D.A. Sherry, and S. Johnson. 2000. Cactus Wren (Campylorhynchus brunneicapillus). In: A. Poole and F. Gill (eds.). The birds of North America No. 558. The birds of North America, Inc. Philadelphia, Pennsylvania.         [ Links ]

Ralph, C., G.R. Geupel, P. Pyle, T.E. Martin, and D.F. DeSante. 1993. Handbook of field methods for monitoring landbirds. General Technical Report PSW–GTR–144. United States Department of Agriculture. Albany, California.         [ Links ]

Reichard, S.H., L. Chalker–Scott, and S. Buchanan. 2001. Interactions among non–native plants and birds. Pp. 179–223. In: J.M. Marzluff, R. Bowman, and R. Donnelly (eds.). Avian ecology and conservation in an urbanizing world. Kluwer Academic Publishers. Norwell, Massachusetts.         [ Links ]

Rosengaus, M. and A. Hernández–Unzón. 2005. Resumen de la temporada de ciclones tropicales 2005 en México. Comisión Nacional del Agua. Servicio Meteorológico Nacional. México, DF.         [ Links ]

Rzedowski, J. 1994. Vegetación de México. Limusa. México, DF.         [ Links ]

Sokal, R.R., and F.J. Rohlf. 1995. Biometry: The principles and practice of statistics in biological research. W.H. Freeman and Company. New York.         [ Links ]

Tirado–Aviles, A.V. 2009. Patrones de depredación de nidos artificiales en una reserva ecológica inmersa en la zona urbana de Pachuca, Hidalgo. Tesis de licenciatura, Universidad Autónoma del Estado de Hidalgo. Pachuca, Hidalgo.         [ Links ]

Tweit, R.C. 1996. Curve–billed Thrasher (Toxostoma curvirostre). In: A. Poole and F. Gill (eds.). The birds of North America. The birds of North America, Inc. Philadelphia, Pennsylvania.         [ Links ]

Wolf, B.O. and S.L. Jones. 2000. Vermilion Flycacther (Pyrocephalus rubinus). In: A. Poole and F. Gill (eds.). The birds of North America, No. 484. The birds of North America, Inc. Philadelphia, Pennsylvania.         [ Links ]

Zuria, I., J. Bravo–Cadena, and H. Caballero–Quiroz. 2009. Guía de aves del Parque Ecológico Cubitos, Pachuca, Hidalgo.         [ Links ]