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J. Field Ornithol. 85(3):258–273, 2014DOI: 10.1111/jofo.12066Effects of urbanization on site occupancy and densityof grassland birds in tallgrass prairie fragmentsMelissa E. McLaughlin, William M. Janousek, John P. McCarty,and L. LaReesa Wolfenbarger1Department of Biology, University of Nebraska Omaha, 6001 Dodge Street, Omaha, Nebraska 68182, USAReceived 7 January 2014; accepted 22 May 2014ABSTRACT. Tallgrass prairies are among the most threatened ecosystems in the world. Remaining prairies tendto be small and isolated and many are associated with urban and suburban landscapes. We asked how urbanizationmight impact the conservation value of tallgrass prairie fragments for grassland birds by comparing the densities andthe probability of occurrence of Dickcissels (Spiza americana), Grasshopper Sparrows (Ammodramus savannarum),and Eastern Meadowlarks (Sturnella magna) across 28 grasslands surrounded by low, moderate, and high levelsof urbanization. We employed a hierarchical model selection approach to ask how variables that describe thevegetation structure, size and shape of grasslands, and urbanization category might explain variation in density andoccurrence over two breeding seasons. Occurrence of all three species was explained by a combination of vegetationand patch characteristics, though each species was influenced by different variables and only Eastern Meadowlarkoccurrence was explained by urbanization. Abundance of all three species was negatively impacted by urbanization,though vegetation variables were also prevalent in the best-supported models. We found no evidence that vegetationstructure or other patch characteristics varied in a systematic way across urbanization categories. Although ourresults suggest that grassland bird density declines with urbanization, urban tallgrass prairies still retain conservationvalue for grassland birds because of the limited availability of tallgrass prairie habitat and the limited impact ofurbanization on species occurrence.RESUMEN. Efectos de la urbanización sobre la ocupación de lugares y densidades de avesde pastizales en fragmentos de praderas con altos pastosLas praderas con altos pastos están entre los ecosistemas mas amenazados en el mundo. Los remanentes deestas praderas tienden a ser pequeños y aislados y muchos están asociados con paisajes urbanos y suburbanos. Nospreguntamos como la urbanización puede impactar el valor de conservación de los fragmentos de altos pastos enlas praderas para aves de pastizales por medio de la comparación de las densidades y probabilidad de ocurrenciade Spiza americana, Ammodramus savannarum y Sturnella magna en 28 praderas rodeadas por bajos, moderados yaltos niveles de urbanización. Empleamos un modelo jerárquico de selección para preguntar como variables quedescriben la estructura de vegetación, el tamaño y la forma de la pradera, y la categorı́a de urbanización puedenexplicar la variación en densidad y ocurrencia a lo largo de dos temporadas reproductivas. La ocurrencia de las tresespecies se explico por una combinación de vegetación y caracterı́sticas del parche, aunque cada especie fue afectadapor diferentes variables y solo la ocurrencia de Sturnella magna fue explicada por la urbanización. La abundancia delas tres especies fue afectada negativamente por la urbanización, aunque las variables de vegetación fueron tambiénpredominantes en los modelos mejor soportados. No encontramos evidencia de que la estructura de la vegetaciónu otras caracterı́sticas del parche variaron de una manera sistemática a lo largo de las categorı́as de urbanización.Aunque nuestros resultados siguieren que la densidad de las aves de praderas declina con la urbanización, la praderasurbanas de altos pastos todavı́a retiene un valor de conservación para las aves de praderas debido a la limitadadisponibilidad de altos pastos en los hábitats de praderas y el limitado impacto que tiene la urbanización sobre laocurrencia de especies.Key words: conservation, Dickcissel, Eastern Meadowlark, Grasshopper Sparrow, Great Plains, vegetation structureThe Tallgrass Prairie ecosystem of the NorthAmerican Great Plains is of high conservationconcern because most of its original extenthas been converted to high-intensity agriculture(Samson and Knopf 1994, Mac et al. 1998) andbecause few remaining prairies are protected andmanaged for conservation purposes (Hoekstra1Corresponding author. Email: lwolfenbarger@unomaha.edu Cet al. 2005, Aycrigg et al. 2013). In addition, areas of remaining prairie that are protected tend to be small, isolated fragments(Steinauer and Collins 1996). Many speciesof plants and animals have experienced population declines in response to this loss ofnative prairie habitat, but declines in populations of grassland birds have been particularly dramatic (Herkert 1995, Peterjohn andSauer 1999, Sauer et al. 2011). In response,2014 Association of Field Ornithologists258
Vol. 85, No. 3Grassland Birds in Urban Tallgrass Prairiesgrassland birds have become a conservationpriority, and concern over grassland birds hascontributed to efforts to protect and restoretallgrass prairies (Vickery et al. 1999).Many protected prairie remnants were established as part of municipal park systems and arefound in and around cities and towns (Schwartzand van Mantgem 1997, Bock and Bock 1998).Other prairie remnants are becoming engulfedby urban and suburban expansion. Increasingurbanization is of concern because it can alterthe composition of plant and animal communities, favoring invasive and non-native species(McKinney 2002, Alberti et al. 2003, Marzluffand Ewing 2008). Perhaps most importantly,urbanization may result in prairies becomingfragmented into smaller parcels, increasing theamount of edge and possibly increasing theisolation of prairies from each other (Hamer etal. 2006). Although agriculture has been responsible for much of the loss and fragmentationof native grassland habitat, urbanization maypresent special challenges for conservation ofgrassland species. Agricultural areas and theirsurrounding marginal areas may present fewerbarriers to movement and may even act assecondary habitat for some wildlife species. Inaddition, the potential for restoration to nativehabitat still exists on many agricultural lands,whereas conversion to urban areas is likely permanent (McKinney 2002, Marzluff and Ewing2008).The importance of actively managing tallgrassprairie fragments to maintain habitat qualitymay make them especially vulnerable to theeffects of urbanization. Prairie managers dependon a combination of prescribed fire and grazing to limit encroachment by trees and otherwoody species, prevent build-up of litter thatinterferes with the growth of young plants, andincrease plant heterogeneity (Knapp et al. 1999).Although mowing prairies may produce manyof these benefits (Collins et al. 1998), fire combined with grazing by either cattle (Bos taurus)or bison (Bison bison) are the preferred tools formanagement of tallgrass prairies. Urbanizationcan potentially limit the ability of managers touse these tools because of the risks to humansand property associated with prescribed fire andlarge grazers, which could result in less suitablevegetation structure (Johnson and Igl 2001,Marzluff 2001, Crooks et al. 2004). Prairiefragments surrounded by urbanized areas may259have more woody and invasive plant species(Chapman and Reich 2007), potentially leadingto reduced densities of native grassland birdspecies (Fitzgerald and Pashley 2000, Maestaset al. 2003, Davis 2004).Our current understanding of urbanizationand grassland birds is based primarily on shortor mixed-grass prairie in Colorado (Bock et al.1999, Haire et al. 2000, Lenth et al. 2006),and a study of grasslands in the eastern UnitedStates (Forman et al. 2002). In those studies,density, abundance, and presence of most nativegrassland bird species were negatively correlatedwith urbanization. However, the difficulty ofextrapolating across communities highlights theneed for additional research, specifically involving tallgrass prairie.Urbanization can have direct impacts on theuse of prairie fragments if birds avoid sites surrounded by more urban features. For grasslandecosystems, urbanization might also have indirect effects if increased urbanization results insmaller patches with more edge relative to theirsize, or if urbanization interferes with habitatmanagement, such as prescribed fire, resulting inless suitable vegetation structure (Johnson andIgl 2001, Marzluff 2001, Crooks et al. 2004).Previous studies indicate that the abundanceand reproductive success of grassland birds maybe influenced by vegetation structure (Hilden1965, Herkert 1994, Herkert et al. 1996, Winteret al. 2005, Chapman and Reich 2007). Nativegrassland birds respond to factors such as theamount of grass and forb cover (Rotenberryand Wiens 1980, Temple 2002), shrub density(Vickery 1996), and litter depth (Swengel andSwengel 2001). Thus, studies of the effects ofurbanization on grassland birds also need toaccount for these factors.We measured species occurrence and thedensity of grassland birds in tallgrass prairieslocated along an urban to rural gradient. Ourobjective was to determine how urbanizationmight impact the value of prairie fragments forgrassland bird conservation. If urbanization prevents active management, we expect the tallgrassprairie community to become degraded and lessattractive to grassland birds. We first addressedthis potential indirect impact of urbanizationby examining the hypothesis that grassland birdoccurrence and density are indirectly affectedby urbanization through a relationship withvegetation structure within prairie fragments.
260M. E. McLaughlin et al.Next, we asked whether the occurrence anddensity of birds was affected by the size andshape of prairie fragments and by the degreeof urbanization surrounding them. There area significant number of prairie remnants in andaround urban areas and, although there are compelling reasons to maintain them for social andeducational purposes (Miller and Hobbs 2002),the question remains whether small fragmentsof tallgrass prairie still retain their conservationvalue as surrounding landscapes become moreurbanized (Shafer 1997).METHODSStudy area. We studied tallgrass prairiefragments in and around Omaha and Lincoln,Nebraska, and Council Bluffs, Iowa (Mount2013). Prior to European settlement, the regionwas dominated by tallgrass prairie, but is nowdominated by suburban and urban areas surrounded by row-crop agricultural fields. Sitesincluded remnant tallgrass prairies that havebeen protected, as well as sites that have beenrestored from agriculture to tallgrass prairie.We included all accessible urban and suburbanprairie remnants, whereas rural sites were selected from among available grasslands nearestto the urban areas. All sites are managed in asimilar fashion by prescribed burning, grazing,or mowing. Prairies burned in the spring werenot surveyed that season. In 2011, we surveyed20 sites. Extreme flooding the summer of 2011resulted in the loss of five rural grasslands locatedat DeSoto and Boyer Chute National WildlifeRefuges along the Missouri River. In addition,two sites used in 2011 were burned in the springof 2012. In 2012, we retained 13 original sitesand added eight new sites.We quantified urbanization surroundingeach study site based on 1-m-resolutiondigital orthoimagery acquired by the U.S.Farm Service Agency in 2010 and obtainedfrom the Nebraska Department of Natural Resources -2012-1-2-meter). Images were imported into ArcGIS 10.1 (ESRI2010) and the boundaries of each study sitewere digitized. We created a 1600-m bufferaround the borders of each grassland and usedArcGIS to create 500 random points withineach buffer. Land use under each of the pointswas visually classified as buildings, roads, andJ. Field Ornithol.other impermeable surfaces (i.e., parking lotsand driveways), lawn, agricultural, trees, wetlands, grassland, or open water. In addition,we used ArcGIS to determine the area (m2 )and perimeter (m) of the digitized grasslandboundaries and then calculated the ratio of theperimeter to the area (hereafter, edge-to-interiorratio) of each grassland site.Bird surveys. We sampled grassland birdspecies richness and density during the 2011 and2012 breeding seasons using distance samplingat point transects (Thomas et al. 2009). Surveyswere done within 4 h after sunrise from 10 Mayto 10 June 2011, and from 14 May to 10 June2012. We surveyed each site three times duringeach breeding season, visiting each site early inthe survey period, in the middle, and then latein the survey period. We included each visit inanalyses. Points were located near the center ofthe grassland and, when possible, at least 100m from all prairie edges. For small sites, pointswere located as far from edges as possible. Duringeach count, we recorded all birds seen or heardduring a 10-min period and their distances fromthe point location (Thomas et al. 2009). Surveyswere not conducted when wind speeds were 20 km/h or when it was raining.Vegetation sampling. We measured vegetation structure at each grassland between 27May and 13 June 2011, and between 29 Mayand 21 June 2012. We used ArcGIS 10.1(ESRI 2010) to select nine random points forvegetation sampling in each grassland patch andlocated these points in the field using GPS. Wemeasured vertical vegetation structure followingRotenberry and Wiens (1980) and Martin etal. (1997). This method is based on recordingthe number of “hits” of grass, forbs, and shrubswithin 10-cm height intervals on a 110-cm pole.We calculated the mean height of vegetationdensity using the total hits weighted by themidpoint of each height interval. We used thepoint-centered quarter method at each point tomeasure forb and shrub density around eachrandom point (Cottam and Curtis 1956).Statistical analysis. We used the Wardmethod for hierarchical clustering to categorizelevels of urbanization of our study sites (high,moderate, or low) based on the percentage ofsurrounding areas classified as urban (i.e., lawn,roads, impervious surfaces, and buildings: JMPv. 10.0.2, SAS Institute, Cary, NC; Mount2013). Based on these clusters, we incorporated
Vol. 85, No. 3Grassland Birds in Urban Tallgrass Prairiesurbanization as a categorical variable in ouranalyses. We used ANOVA to test whetherthere were significant differences among thecategories of urbanization in vegetation characteristics (forb density, shrub density, meanvegetation height, and total grass hits) andsite characteristics (area and edge-to-interiorratio). We chose these vegetation characteristicsbecause each describes a different aspect ofvegetation in grassland habitats. Forb densityand shrub density provide an indication ofthe structural diversity of the grassland, meanvegetation height provides an indication of vegetation height, weighted by vegetation density,and total grass hits indicate the overall densityof grass (Fisher and Davis 2010). Summarydescriptions of habitat variables are presentedas means SE.Although we recorded all species seen orheard during bird surveys, our analyses arelimited to three obligate grassland bird species(Dickcissels [Spiza americana], GrasshopperSparrow [Ammodramus savannarum], and Eastern Meadowlarks [Sturnella magna]) for whichwe recorded sufficient observations to analyzetheir densities and occurrence. Other obligate grassland bird species, including Henslow’sSparrows (Ammodramus henslowii), Bobolinks(Dolichonyx oryzivorus), Western Meadowlarks(Sturnella neglecta), and Sedge Wrens (Cistothorus platensis), were not abundant enough forus to analyze the effects of urbanization onoccurrence or density.We used a model selection approach to determine the effect of urbanization on the occurrence and density of Dickcissels, GrasshopperSparrows, and Eastern Meadowlarks (Burnhamand Anderson 2002). Because other variablesmay also influence the occurrence and densityof grassland obligate species, we employed ahierarchical approach that compared modelsfrom three candidate model sets that included(1) year, (2) measures of vegetation structure,and (3) urbanization and patch characteristics(Hamer et al. 2006, Winter et al. 2006, Klug etal. 2009). Within each candidate set, we assessedwhether the inclusion of possible covariates(year and vegetation characteristics) increasedthe explanatory power of the models. If theydid, these variables were carried forward intosubsequent model sets in the hierarchy. We carried forward variables when they occurred in thetop-ranking model and when there was strong261support for the top-ranking model comparedto the null. We evaluated the AIC weight of thetop ranking model compared to the null model’sAIC weight, which is a measure of the strength ofevidence for one model over another (Burnhamet al. 2011). We considered models equivalentwhen the ratio between the weights was 2,which would indicate that the top-rankingmodel was less than twice as likely as the null.For the occurrence analysis, the hierarchy wasas follows: (1) year, (2) vegetation (mean grasshits, mean vegetation height, forb density, andshrub density; Table 1) and (3) urbanization andpatch characteristic (area and edge-to-interiorratio; Table 1). For the density analysis, we firstmodeled a detection function and then followedthe same hierarchy as for the occurrence analysis(Table 2). We analyzed the multicollinearity ofmean forb density, mean shrub density, meanvegetation height, total grass hits, and edgeto interior ratio using VIF (variance inflationfactor); all had VIF 1.5, indicating no evidenceof multicollinearity of the variables used in ourmodels. Because of the significant correlationbetween area and edge-to-interior ratio (Pearsoncorrelation test, 2011: r 0.65, N 20,P 0.001; 2012: r 0.69, N 21, P 0.001) and variance inflation ratio 2.0, we didnot include both of these variables in the samemodels (Table 1).To analyze the effect of year, vegetation characteristics, and patch characteristics on occurrence of Dickcissels, Grasshopper Sparrows, andEastern Meadowlarks, we used mixed effects,nominal logistic regressions using the glmerfunction from the lme4 package in R 2.15.2(Bates et al. 2012, R Core Team 2013). The nullmodel was the model with only “site” includedas a random effect.To model detection and density of Dickcissels, Grasshopper Sparrows, and EasternMeadowlarks, we used the package “unmarked”in R 3.0.2 (R Core Team 2013). We usedthe generalized distance sampling “gdistsamp”within the package to model the detection function and to analyze the effect of site covariates ondensity (Table 2; Chandler et al. 2011, Fiske andChandler 2011). When modeling the detectionfunction, we tested whether observer effects,wind speed, or both of these covariates affecteddetection. We standardized continuous covariates (wind speed, vegetation characteristics, sitearea, and edge-to-interior ratio) to a mean of zero
262M. E. McLaughlin et al.J. Field Ornithol.Table 1. Model selection results for testing hypotheses about the effects of vegetation and patch characteristicson grassland bird occurrence.DickcisselsVegetation Characteristics YearVegetation Height YearYearForb Density Veg H YearGrass Hits YearShrub Density Veg H YearGrass Hits Veg H YearShrub Density YearForb Density YearForb Density Shrub Density Veg H YearGrass Hits Forb Density Veg H YearForb Density Grass Hits YearGrass Hits Shrub Density Veg H YearForb Density Shrub Density YearShrub Density Forb Density Grass Hits Veg H YearShrub Density Forb Density Grass Hits YearPatch YearEdge YearArea YearYearUrban Edge YearUrban YearGrasshopper SparrowsVegetation Characteristics YearShrub Density YearShrub Density Grass Hits Vegetation Height YearShrub Density Grass Hi
Urbanization can have direct impacts on the use of prairie fragments if birds avoid sites sur-rounded by more urban features. For grassland ecosystems, urbanization might also have indi-rect effects if increased urbanization results in smaller patches with more edge relative to their size, or if urbanization interferes with habitat
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