BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofitpublishers, academic institutions, research libraries, and research funders in the common goal of maximizing access tocritical research.

Associations Between Northern Mockingbirds and the ParasitePhilornis porteri in Relation to UrbanizationAuthor(s): Ariane Le Gros, Christine M. Stracey, and Scott K. RobinsonSource: The Wilson Journal of Ornithology, 123(4):788-796. 2011.Published By: The Wilson Ornithological SocietyDOI: http://dx.doi.org/10.1676/10-049.1URL: http://www.bioone.org/doi/full/10.1676/10-049.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in thebiological, ecological, and environmental sciences. BioOne provides a sustainable onlineplatform for over 170 journals and books published by nonprofit societies, associations,museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated contentindicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercialuse. Commercial inquiries or rights and permissions requests should be directed to theindividual publisher as copyright holder.

ASSOCIATIONS BETWEEN NORTHERN MOCKINGBIRDS AND THE

PARASITE PHILORNIS PORTERI IN RELATION TO URBANIZATION

ARIANE LE GROS,1,2,4 CHRISTINE M. STRACEY,1,3 AND SCOTT K. ROBINSON1

ABSTRACT.—We investigated associations between Northern Mockingbirds (Mimus polyglottos) and the nest parasite

Philornis porteri (Diptera: Muscidae), and how they vary with urbanization in northcentral Florida. Our goal was to

ascertain if the ‘parasite-release’ hypothesis could contribute to high reproductive success of Northern Mockingbirds in

urban areas. We collected 26 nests in 2007 and 73 in 2008 that had produced fledglings along an urbanization gradient, and

measured the number of nests parasitized and the number of P. porteri in the nests. Habitats differed in prevalence of

Philornis parasitism, but not directly in relation to urbanization. Parking lots and wildlife preserves had low levels of

parasitism, whereas residential neighborhoods and pastures had significantly higher parasitism prevalence. Parasite

prevalence was also significantly and positively affected by nest height and percentage of ground covered by buildings,

trees, and open areas in the study site. Our findings do not offer strong support for the ‘parasite-release’ hypothesis in

relation to urbanization, but suggest that vulnerability to parasites is habitat-specific. Received 2 April 2010. Accepted 27

June 2011.

Urbanization causes high local extinction ratesand replacement of many species by others thatsurvive well in urban areas (McKinney 2002, Blair2004, Gottschalk et al. 2007), which we refer to asurban-positive species (Stracey 2011). Numerousresearchers (Adams 1994, Gering and Blair 1999,McKinney 2002, Chace and Walsh 2006, Shochatet al. 2006, Fokidis et al. 2008) have hypothesizedthat changes in predation and food resources areresponsible for the success of urban-positivespecies. Few studies, however, have tested thehypothesis that urban-positive species are releasedfrom parasites that help regulate populations innative habitats. Urban species could be lessexposed to parasites either because hosts are inbetter condition and have better immune systems tofight parasites (Fokidis et al. 2008) or becausesome parasites are less prevalent in urban areas(Marcogliese 2005). Some authors (Lafferty 1997,Marcogliese 2004, Sures 2004, Marcogliese 2005)suggest parasites are frequently the first species tobe affected by ecosystem changes.

Parasites have an important role in structuringmany ecological communities (Minchella andScott 1991). They can regulate host populationsby increasing energetic demands, altering behav-ior, increasing mortality, reducing fecundity,altering nutritional status, reducing growth, mod-

ifying interspecific competition, enhancing sus-ceptibility to predation, and altering mate choiceand sex ratios (reviewed by Minchella and Scott1991). Loye and Carroll (1995) reviewed theeffects of ectoparasites on birds and found theyaffect nestling growth, body condition, andsurvival, as well as adult reproductive successand behavior. They concluded that blood-feeding,nest-dwelling parasites may significantly reducehost fitness. Tompkins et al. (2011) found thatparasites frequently mediate the success ofinvasive species. If a similar mechanism isoperating in urban habitats, an additional hypoth-esis for high abundance of urban-positive speciesmay be decreased parasitism.

Numerous recent studies measured the effectsof urbanization on host-parasite interactions alongan urban gradient (Gregoire et al. 2002, Reperantet al. 2007, Fokidis et al. 2008, Geue and Partecke2008, Page et al. 2008, Evans et al. 2009, Lehreret al. 2010). The frequency and the intensity ofroundworm (Baylisascaris procyonis) infection incommon raccoons (Procyon lotor), for example,decreased with urbanization (Page et al. 2008) andthe prevalence of some species of helminthparasites in red foxes (Vulpes vulpes) alsodecreased with urbanization (Reperant et al.2007). Similarly, for songbirds, individuals inurban areas generally had fewer blood parasites(Fokidis et al. 2008), fewer Ixodes ticks (Gregoireet al. 2002, Evans et al. 2009), and lower risk ofinfection by blood parasites (Geue and Partecke2008) than in rural areas. Lehrer et al. (2010),however, found that prevalence of Toxoplasmagondii in woodchucks (Marmota monax) waspositively related to urbanization. These studies

1 Florida Museum of Natural History, 305 Dickinson

Hall, P. O. Box 117800, Gainesville, FL 32611, USA.2 Current address: CRI, Universite Paris Descartes, 24 rue

du Faubourg Saint Jacques, 75014 Paris, France.3 Current address: Westminster College, 1840 South 1300

East, Salt Lake City, UT 84105, USA.4 Corresponding author;

e-mail: ariane.le.gros@gmail.com

The Wilson Journal of Ornithology 123(4):788–796, 2011

788

indicate that associations between parasites andtheir hosts can be either positively or negativelyaffected by urbanization.

Tompkins et al. (2011), in their review of theeffects of wildlife diseases on ecosystems,indicate a wider exploration of the effects ofparasites on invasive species’ success is needed.Further studies on the distribution and effects ofparasites in relation to urbanization are needed aslittle is known about how urbanization affectsparasites, and nest parasites in particular, and howthese changes can affect urban bird communities.

We investigated how the interaction betweenthe Northern Mockingbird (Mimus polyglottos)and its nest parasite (Philornis porteri; Diptera:Muscidae) varies with urbanization. Previousresearch (Fokidis et al. 2008, Stracey andRobinson in press) demonstrated the mockingbird,an urban-positive species, increases in abundancewith urbanization with peak densities occurring inresidential neighborhoods (Stracey 2010). Weconsidered the mockingbird a good model speciesto test if the ‘parasite-release’ hypothesis mightcontribute to the success of urban-positive spe-cies. Dipteran nest parasites are known to havedeleterious effects on nestlings and, at times,adults (Arendt 1985a, b; Hurtrez-Bousses et al.1998; Simon et al. 2004; Segura and Reboreda2011), and assessing their presence is much lessinvasive than assessing blood parasites. Mocking-bird nests are more likely to be infected by thisparasite than by fleas or mites (pers. obs.), andPhilornis parasites are known to have negativefitness consequences for nestlings, includinghigher mortality and decreased growth rates (Loyeand Carroll 1995, Dudaniec and Kleindorfer 2006,Galligan and Kleindorfer 2009, Kleindorfer andDudaniec 2009). Little is known, however, abouthow urbanization affects the abundance of P.porteri. We investigated how the distribution of P.porteri changed with urbanization. We predicted,based on the ‘parasite-release hypothesis’, that wewould find fewer parasitized nests and lowerintensities of parasitism (number of parasites perhost; sensu Margolis et al. 1982) in urban habitatswith the lowest levels of parasitism in residentialneighborhoods, where mockingbird density ishighest.

METHODS

Study Species.—The Northern Mockingbird isan open-cup nesting, altricial bird that occursthroughout the United States, southern Canada,

Mexico, and the West Indies (Derrickson andBreitwisch 1992). The breeding season in Floridastarts as early as late February and ends in earlyAugust, and a pair can nest from one to five timesduring the breeding season (Derrickson andBreitwisch 1992). Clutch size is between twoand six eggs, and nestlings remain in the nest12 days with both parents providing care (Der-rickson and Breitwisch 1992).

Philornis porteri occurs in southern Texas andFlorida (Dodge 1955, Kinsella and Winegarner1974) and has been observed on at least threespecies of birds: Northern Mockingbirds, EasternBluebirds (Sialia sialis), and Great CrestedFlycatchers (Myiarchus crinitus) (Kinsella andWinegarner 1974, Spalding et al. 2002). Larvaeare obligate subcutaneous parasites of nestlingsand feed on blood, other body fluids, and cellulardebris (Dudaniec and Kleindorfer 2006, Fessl etal. 2006). Adults are non-parasitic and may feedon decaying organic matter, fruits, or flowers(Dudaniec and Kleindorfer 2006, Fessl et al.2006). Philornis larvae are known to havenegative fitness consequences including reducedgrowth, diminished body condition, decreasedfledgling success, and increased nestling mortalityfor at least some hosts (Arendt 2006, Dudaniecand Kleindorfer 2006, Dudaniec et al. 2007,Rabuffetti and Reboreda 2007, Huber 2008,Galligan and Kleindorfer 2009). Females of mostspecies of Philornis lay eggs in the avian hosts’nests. The larvae of subcutaneous species, afterhatching, burrow under the nestlings’ skin wherethey feed until they are ready to pupate. They thenleave the nestlings, pupate in the nesting material,and emerge as adults 10 days later, allowingPhilornis to produce several generations per year(Glasgow and Henson 1957, Kinsella and Wine-garner 1974, Uhazy and Arendt 1986, Delannoyand Cruz 1991, Young 1993, Nores 1995,Spalding et al. 2002, Arendt 2006, Dudaniec andKleindorfer 2006, Fessl et al. 2006). The lifecycles of many Philornis parasites have beenpartially described, but little is known about P.porteri.

Study Sites.—Our study was conducted at sevensites in and around Gainesville, Florida, USAduring spring and summer 2007 and 2008. Allstudy sites were within 50 km of Gainesville andwere spread along an urbanization gradient. Thesesites were grouped into four types of habitat:wildlife preserve (1 site: Ordway-Swisher Bio-logical Station), pasture (2 sites), residential area

Le Gros et al. N URBANIZATION AND HOST-PARASITE INTERACTIONS 789

(2 sites) and parking lot (2 sites). Each site wasembedded within a larger area of the same type ofland use. The parking lots consisted of large areasof pavement for parking spaces, interspersed withbuildings and islands of mowed grass, shrubs, ortrees. The residential neighborhoods consisted ofa mosaic of roads, houses, and yards. The yardshad variable amounts of mowed grass andornamental shrubs and trees that were both nativeand nonnative. The pastures consisted of scatteredtrees and large areas of grass that were periodi-cally grazed by cattle. Fences in the pastures wereoften covered with vines and shrubs. The wildlifepreserve consisted of scrub trees and shrubsscattered among areas of short grass and bareground with an occasional large tree. These openareas were variably surrounded by pine (Pinusspp.) forests or xeric forests. Study sites werebetween 2.7 and 52.9 km apart. We calculated thepercentage of ground covered by buildings,pavement, grass, open areas (sum of pavementand grass), trees, and other (water or undeter-mined surface) for each study site based onGoogle Earth satellite images. We designatedwildlife preserve and pasture as rural land-use,and parking lot and residential areas as urbanland-use. We only sampled nests from ruralhabitats in 2007. The highest densities ofmockingbirds were in residential areas, followedby parking lot and wildlife preserve; pasture hadthe lowest densities (Stracey 2010).

Spatial Pattern of Prevalence and Intensityof Parasitism.—We searched each study site formockingbird nests. Active nests were monitoredevery 1–3 days until nestlings fledged or weredepredated. No botflies were detected on thenestlings during handling. We collected nests afternestlings fledged and placed them in sealed plasticbags. We only collected nests from which at leastone nestling fledged to ensure that if there wereparasites in the nest they had sufficient time topupate. We also noted the date when clutcheswere initiated, nest height, and the type of plantcontaining the nest.

We dissected each nest and counted the numberof pupae, pupal cases, and adult flies in thenesting material. Adult flies were identified by G.J. Steck (Florida Department of Agriculture andConsumer Services) and voucher specimens weredeposited in the collection of the Florida Depart-ment of Agriculture and Consumer Services. Allpupae, pupal cases, and adults were identified asP. porteri except a few pupal cases which

belonged to a parasite (a tachinid fly) of P.porteri. These pupal cases were excluded from thestudy.

The parasite intensity in each nest was definedas the number of pupae plus the number of pupalcases in the nest. The number of nestlings in a nestvaried from one to four, and we defined theaverage parasite intensity per nestling as the nestintensity divided by the number of nestlings athatching day. Average parasite intensity pernestling, however, is only an estimate of parasiteload because parasites may not be spread evenlyamong nestlings and may concentrate on one or afew nestlings (Christe et al. 1998). We calculatedthe proportion of parasitized nests in each site andfor each year.

Statistical Analyses.—We used R Software(2010: Version 2.12.1) to test the effect of year,month in which the nest was initiated, clutch size,land-use category (urban, rural), habitat (parkinglot, residential, pasture, wildlife preserve), studysite, nest height, and plant type (tree, shrub, vineor building/object) on parasitism status of the nest(parasitized or not parasitized) using logisticregression. The different study sites were alsodefined by ground-cover variables, and we testedthe effect of these variables (percentage ofbuildings, trees, and open areas) on parasitismstatus of the nest using logistic regression. Weused a stepwise selection process for both modelsbased on AIC to remove useless variables. Pvalues for the effect of the different variables wereobtained by performing a Type III sums-of-squareanalysis on the final models. We also analyzed theeffect of these variables on the number ofparasites per nestling for parasitized nests usingANCOVA. We log-transformed the data onparasite intensity per nestling to meet assumptionsof normality. We used a stepwise selectionprocess for both models based on AIC to removeuseless variables and P values for the effect of thedifferent variables were obtained by performing aType III sums-of-square analysis on the finalmodels.

RESULTS

We collected 73 nests in 2008 and 26 nestsexclusively from rural areas in 2007. Thirty-eightpercent of the nests were parasitized in 2008versus 42% in 2007 (Tables 1, 2). The number ofparasites in a nest ranged from 0 to 85 with amean 6 SE of 22.85 6 3.99 parasites in theparasitized nests in 2008, and from 0 to 88 with a

790 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 123, No. 4, December 2011

mean 6 SE of 22.73 6 7.64 parasites in

parasitized nests in 2007. There were many nests

with few parasites in both years, and few nests

with many parasites (Fig. 1A). Parasite intensity

per nestling followed that same trend, ranging

from 0 to 21.25 with a mean 6 SE of 6.59 6 1.15

parasites per nestling in parasitized nests in 2008

and from 0 to 88 with a mean 6 SE of 14.05 6

7.61 parasites per nestling in parasitized nests in

2007 (Fig. 1B).

Habitat had a significant effect on prevalence of

parasite infestation (x2 5 10.58, df 5 3, P 5

0.014). There were more nests parasitized in

residential areas and pastures than in parking lots

(pairwise Chi-square tests: x2 5 8.94, df 5 1, P 5

0.003, and x2 5 7.04, df 5 1, P 5 0.008,

respectively; Fig. 2). There was a non-significant

trend for more parasitized nests in residential

areas than in the wildlife preserve (x2 5 2.73, df

5 1, P 5 0.098; Fig. 2). Nest height also had a

positive effect on the probability of being infected

(x2 5 4.52, df 5 1, P 5 0.033). There was a trend

(x2 5 3.58, df 5 1, P 5 0.058) for nests later in

the year to have a higher probability of parasitism.

TABLE 1. Characteristics of parasite prevalence, parasite intensity, parasite intensity per nestling, and clutch size of

Northern Mockingbirds at each site during the 2007 breeding season, Gainesville, Florida. ORD 5 Ordway-Swisher

Biological Station, BRU 5 Beef Research Unit, and SF 5 Santa Fe River Ranch Beef Unit.

Land-use Rural

Habitat Preserve Pastures

Site ORD BRU SF

Sample size 9 11 6

Parasite prevalence 0.44 0.36 0.50

Mean parasite intensity 26.00 28.25 11.00

Standard error 7.15 20.35 6.51

Range 8–41 1–88 4–24

Mean parasite intensity/nestling 11.63 24.08 3.89

Standard error 3.39 21.35 2.06

Range 4.00–20.50 0.33–88.00 2.00–8.00

Mean clutch size 2.89 2.91 3.00

Standard error 0.26 0.21 0.26

Range 2–4 1–4 2–4

TABLE 2. Characteristics of parasite prevalence, parasite intensity, parasite intensity per nestling, and clutch size of

Northern Mockingbirds at each site during the 2008 breeding season, Gainesville, Florida. ORD 5 Ordway-Swisher

Biological Station, BRU 5 Beef Research Unit, SF 5 Santa Fe River Ranch Beef Unit, DUCK 5 Duckpond, CAPRI 5

Capri, OM 5 Oaks Mall, and BP 5 Butler Plaza.

Land-use Rural Urban

Habitat Preserve Pastures Residential areas Parking lots

Site ORD BRU SF DUCK CAPRI OM BP

Sample size 10 7 13 10 7 11 15

Parasite prevalence 0.20 0.43 0.69 0.70 0.57 0.18 0.13

Mean parasite intensity 4.00 49.67 22.89 17.29 23.50 19.50 2.50

Standard error 3.00 18.59 6.19 7.10 9.63 0.50 1.50

Range 1–7 22–85 1–63 1–52 1–41 19–20 1–4

Mean parasite intensity

per nestling 1.00 12.42 6.80 5.37 7.54 4.88 0.83

Standard error 0.75 4.65 2.04 2.34 2.69 0.13 0.50

Range 0.25–1.75 5.50–21.25 0.33–21.00 0.50–17.33 0.25–10.25 4.75–5.00 0.33–1.33

Mean clutch size 3.60 3.43 3.23 3.00 3.00 2.73 3.40

Standard error 0.16 0.43 0.20 0.26 0.31 0.33 0.16

Range 3–4 1–4 2–4 2–4 2–4 1–4 2–4

Le Gros et al. N URBANIZATION AND HOST-PARASITE INTERACTIONS 791

FIG. 1. Number of Northern Mockingbird nests collected in 2007 and 2008 according to (A) their number of parasites

and (B) number of parasites per nestling (total number of parasites divided by number of nestlings in the nest).

792 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 123, No. 4, December 2011

Year, clutch size, land-use category, study site,

and plant type did not have a significant effect on

parasitism status of the nest. The percentage of

building, tree, and open area all had a positive

effect on the probability of a nest to be parasitized

(Table 3; x2 5 6.67, df 5 1, P 5 0.010; x2 5

7.73, df 5 1, P 5 0.005, and x2 5 7.60, df 5 1, P

5 0.005, respectively). There was no effect of any

variable on parasite intensity per nestling.

DISCUSSION

The prevalence of P. porteri differed among

habitats with fewer parasites in nests in the

wildlife preserve and parking lots than in pasturesand residential areas (Fig. 2). This result was not

consistent with the parasite-release hypothesiswhich indicates parasitism would decrease with

urbanization. The percentages of buildings, trees,and open areas positively affected the probabilityof being parasitized. The relationship among

these three parameters and urbanization, however,is not straightforward and their interactions could

explain the observed habitat effects. The percent-age of ground covered by buildings increases withurbanization, but the percentage of ground

covered by trees tends to decrease with urbani-zation. The percentage of open areas does notseem to be correlated with urbanization as it is

lowest in residential areas and highest in pastures(Table 3). Little is known about the life cycle of

P. porteri and it is difficult to explain the patternof higher prevalence of parasitism at moderatelevels of urbanization. It could be tied to

abundance of food resources for adult flies,presence of predators of adult flies including

their parasites, distance between nests, or othermechanisms. We detected at least one parasite ofP. porteri (a tachinid fly found at the wildlife

preserve), but we know nothing of the abundanceof this parasite or even the identity of potential

predators of adult flies.

The abundance of the host could also influencethe prevalence of parasitism by providing more or

fewer nests in which the parasites can lay eggs.High densities of hosts could result in a dilutioneffect (Ostefeld and Keesing 2000), i.e., a lower

proportion of mockingbird nests being parasitized.Fewer hosts would result in a higher proportion of

nests being parasitized. Our results, however,showed little relationship between host densityand parasite prevalence as the highest parasite

prevalence was in habitats with both high

FIG. 2. Proportion of parasitized Northern Mocking-

bird nests in each habitat. WP 5 wildlife preserve, PAST 5

pasture, RES 5 residential, and PL 5 parking lot. Asterisks

show habitats with significantly different parasite preva-

lence. WP and RES were significantly different at the 10%

level but not 5%.

TABLE 3. Percentage of ground covered by buildings, open areas (sum of pavement and grass), trees, and other (water

or undetermined surface) calculated for each Northern Mockingbird study site from satellite images, Gainesville, Florida,

2007–2008. ORD 5 Ordway-Swisher Biological Station, BRU 5 Beef Research Unit, SF 5 Santa Fe River Ranch Beef

Unit, DUCK 5 Duckpond, CAPRI 5 Capri, OM 5 Oaks Mall, and BP 5 Butler Plaza.

Land-use Rural Urban

Habitat Preserve Pastures Residential areas Parking lots

Site ORD BRU SF DUCK CAPRI OM BP

Buildings 0.00 0.14 0.37 7.06 28.49 25.91 22.58

Open areas 23.53 70.17 71.79 13.10 38.65 52.93 60.40

Trees 72.21 28.16 26.24 79.60 32.78 19.52 16.07

Other 4.26 1.53 1.60 0.24 0.08 1.64 0.95

Le Gros et al. N URBANIZATION AND HOST-PARASITE INTERACTIONS 793

(residential) and low (pastures) host densities. Wedid not consider other hosts of P. porteri, whichmight affect host-specific parasitism rates (Ost-feld and Keesing 2000). Kleindorfer and Duda-niec (2009), for example, found that parasiteintensity was significantly higher for nests withmany close heterospecific neighbors in a relatedspecies of botfly. P. porteri has been documentedin nests of two other species: Eastern Bluebirds(Spalding et al. 2002) and Great CrestedFlycatchers (Kinsella and Winegarner 1974,Spalding et al. 2002), both of which occurred inwildlife preserves, pastures, and residential areas,but were uncommon in parking lots (CMS,unpubl. data). We do not have data on parasitismrates of these species, nor do we know ifadditional species also serve as hosts.

It is unclear if urbanization affects the distri-bution of P. porteri. This parasite may benefitfrom changes caused by moderate levels ofhuman land modification, such as in pasturesand residential areas. Residential areas in Gaines-ville still contain native vegetation and arecharacterized by moderate percentages of groundcovered by buildings (7.06 and 28.49% at ourstudy sites) and pavement (5.80 and 19.44% atour study sites, Table 3). This pattern has alsobeen documented for the Brown-headed Cowbird(Molothrus ater), a brood parasite, which reacheshighest abundance at moderate levels of urbani-zation (Chace et al. 2003), although undoubtedlyfor different reasons. Our findings offer weaksupport, at best, that the ‘parasite-release’ hy-pothesis could explain why urban-positive specieslike mockingbirds are so successful in urbanareas. Only the most extreme urban environmentsappear to offer a refuge from botflies and birdsnesting in habitat with the most natural vegetationalso had a refuge from high levels of botflyparasitism. Our results are difficult to interpretwithout a more complete understanding of theecological factors that affect the distribution of P.porteri. The importance of P. porteri selectivepressure on mockingbirds relative to both otherparasites and other factors (i.e., food andpredators) is unknown. Our study highlights thelimitations in our understanding of how urbani-zation affects bird communities through itseffects on parasites. Given the potential ofparasites to have an important ecological role instructuring bird communities, continued researchinto the affects of urbanization on parasites isvital.

ACKNOWLEDGMENTS

We thank G. J. Steck for identifying the parasite, Judit

Ungvari-Martin for assistance with nest dissection, and

Steve Daniels, T. J. Richard, and R. E. Hanauer for help

with field work. We thank Butler Plaza, the Oaks Mall, the

University of Florida Beef Research Units, Ordway-

Swisher Biological Station, and all homeowners who

granted permission to work on their properties.

LITERATURE CITED

ADAMS, L. W. 1994. Urban wildlife habitats. University of

Minnesota Press, Minneapolis, USA.

ARENDT, W. J. 1985a. Philornis ectoparasitism of Pearly-

eyed Thrashers. I. Impact on growth and development

of nestlings. Auk 102:270–280.

ARENDT, W. J. 1985b. Philornis ectoparasitism of Pearly-

eyed Thrashers. II. Effects on adults and reproduction.

Auk 102:281–292.

ARENDT, W. J. 2006. Adaptations of an avian supertramp:

distribution, ecology, and life history of the Pearly-

eyed Thrasher (Margarops fuscatus). USDA, Forest

Service, International Institute of Tropical Forestry.

General Technical Report IITF-GTR-27. San Juan,

Puerto Rico.

BLAIR, R. 2004. The effects of urban sprawl on birds at

multiple levels of biological organization. Ecology and

Society 9 (5):2. http://www.ecologyandsociety.org/

vol9/iss5/art2/

CHACE, J. F. AND J. J. WALSH. 2006. Urban effects on

native avifauna: a review. Landscape and Urban

Planning 74:46–69.

CHACE, J. F., J. J. WALSH, A. CRUZ, J. W. PRATHER, AND H.

M. SWANSON. 2003. Spatial and temporal activity

patterns of the brood parasitic Brown-headed Cowbird

at an urban/wildland interface. Landscape and Urban

Planning 64:179–190.

CHRISTE, P., A. P. MØLLER, AND F. DE LOPE. 1998.

Immunocompetence and nestling survival in the House

Martin: the tasty chick hypothesis. Oikos 83:175–179.

DELANNOY, C. A. AND A. CRUZ. 1991. Philornis parasitism

and nestling survival of the Puerto Rican Sharp-

shinned Hawk. Pages 93–103 in Bird–parasite inter-

actions: ecology, evolution, and behaviour (J. E. Loye

AND M. Zuk, Editors). Oxford Ornithology Series,

Oxford, United Kingdom.

DERRICKSON, K. C. AND R. BREITWISCH. 1992. Northern

Mockingbird (Mimus polyglottos). The birds of North

America. Number 7.

DODGE, H. R. 1955. New muscid flies from Florida and the

West Indies (Diptera: Muscidae). The Florida Ento-

mologist 38:147–151.

DUDANIEC, R. Y. AND S. KLEINDORFER. 2006. Effects of the

parasitic flies of the genus Philornis (Diptera:

Muscidae) on birds. Emu 106:13–20.

DUDANIEC, R. Y., B. FESSL, AND S. KLEINDORFER. 2007.

Interannual and interspecific variation in intensity of

the parasitic fly, Philornis downsi, in Darwin’s

finches. Biological Conservation 139:325–332.

EVANS, K. L., K. J. GASTON, S. P. SHARP, A. MCGOWAN,

M. SIMEONI, AND B. J. HATCHWELL. 2009. Effects of

794 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 123, No. 4, December 2011

urbanization on disease prevalence and age structure in

Blackbird Turdus merula populations. Oikos 118:774–

782.

FESSL, B., B. J. SINCLAIR, AND S. KLEINDORFER. 2006. The

life-cycle of Philornis downsi (Diptera: Muscidae)

parasitizing Darwin’s finches and its impacts on

nestling survival. Parasitology 133:739–747.

FOKIDIS, H. B., E. C. GREINER, AND P. DEVICHE. 2008.

Interspecific variation in avian blood parasites and

haematology associated with urbanization in a desert

habitat. Journal of Avian Biology 39:300–310.

GALLIGAN, T. H. AND S. KLEINDORFER. 2009. Naris and

beak malformation caused by the parasitic fly,

Philornis downsi (Diptera: Muscidae), in Darwin’s

Small Ground Finch, Geospiza fuliginosa (Passeri-

formes: Emberizidae). Biological Journal of the

Linnean Society 98:577–585.

GERING, J. C. AND R. B. BLAIR. 1999. Predation on artificial

bird nests along an urban gradient: predation risk or

relaxation in urban environments. Ecography 22:532–

541.

GEUE, D. AND J. PARTECKE. 2008. Reduced parasite

infestation in urban Eurasian Blackbirds (Turdus

merula): a factor favoring urbanization? Canadian

Journal of Zoology 86:1419–1425.

GLASGOW, L. L. AND R. HENSON. 1957. Mourning Dove

nestlings infested with larvae of Philornis. Wilson

Bulletin 69:183–184.

GOTTSCHALK, M. S., D. C. DE TONI, V. L. S. VALENTE, AND

P. R. P. HOFMANN. 2007. Changes in Brazilian

Drosophilidae (Diptera) assemblages across an urban-

ization gradient. Neotropical Entomology 36:848–862.

GREGOIRE, A., B. FAIVRE, P. HEEB, AND F. CEZILLY. 2002.

A comparison of infestation patterns by Ixodes ticks in

urban and rural populations of the Common Blackbird

Turdus merula. Ibis 144:640–645.

HUBER, S. K. 2008. Effects of the introduced parasite

Philornis downsi on nestling growth and mortality in

the Medium Ground Finch (Geospiza fortis). Conser-

vation Biology 141:601–609.

HURTREZ-BOUSSES, S., J. BLONDEL, P. PERRET, J. FABREGU-

ETTES, AND F. RENAUD. 1998. Chick parasitism by

blowflies affects feeding rates in a Mediterranean

population of Blue Tits. Ecology Letters 1:17–20.

KINSELLA, J. M. AND C. E. WINEGARNER. 1974. Notes on

the life history of Neomusca porteri (Dodge), parasitic

on the nestlings of the Great-crested Flycatcher in

Florida. Journal of Medical Entomology 11:633.

KLEINDORFER, S. AND R. Y. DUDANIEC. 2009. Love thy

neighbor? Social nesting pattern, host mass and nest

size affect ectoparasite intensity in Darwin’s Tree

Finches. Behavioral Ecology and Sociobiology 63:

731–739.

LAFFERTY, K. D. 1997. Environmental parasitology: what

can parasites tell us about human impacts on the

environment? Parasitology Today 13:251–255.

LEHRER, E. W., S. L. FREDEBAUGH, R. L. SCHOOLEY, AND

N. E. MATEUS-PINILLA. 2010. Prevalence of antibodies

to Toxoplasma gondii in woodchucks across an urban-

rural gradient. Journal of Wildlife Diseases 46:977–

980.

LOYE, J. AND S. CARROLL. 1995. Birds, bugs and blood:

avian parasitism and conservation. Trends in Ecology

and Evolution 10:232–235.

MARCOGLIESE, D. J. 2004. Parasites: small players with

crucial roles in the ecological theater. EcoHealth

1:151–164.

MARCOGLIESE, D. J. 2005. Parasites of the superorganism:

are they indicators of ecosystem health? International

Journal for Parasitology 35:705–716.

MARGOLIS, L., G. W. ESCH, J. C. HOLMES, A. M. KURIS,

AND G. A. SCHAD. 1982. The use of ecological terms

in parasitology (Report of an Ad Hoc Committee of

the American Society of Parasitologists). Journal of

Parasitology 68:131–133.

MCKINNEY, M. L. 2002. Urbanization, biodiversity, and

conservation. BioScience 52:883–890.

MINCHELLA, D. J. AND M. E. SCOTT. 1991. Parasitism: a

cryptic determinant of animal community structure.

Trends in Ecology and Evolution 8:250–254.

NORES, A. I. 1995. Botfly ectoparasitism of the Brown

Cacholote and the Firewood-Gatherer. Wilson Bulletin

107:734–738.

OSTEFELD, R. S. AND F. KEESING. 2000. Biodiversity and

disease risk: the case of Lyme diseases. Conservation

Biology 14:722–728.

PAGE, L. K., S. D. GEHRT, AND N. P. ROBINSON. 2008.

Land-use effects on prevalence of raccoon roundworm

(Baylisascaris procyonis). Journal of Wildlife Diseas-

es 44:594–599.

R SOFTWARE. 2010. Version 2.12.1. Developed by R

Foundation, Vienna, Austria. www.r-project.org

RABUFFETTI, F. L. AND J. C. REBOREDA. 2007. Early

infestation by botflies (Philornis seguyi) decreases

chick survival and nesting success in Chalk-browed

Mockingbirds (Mimus saturninus). Auk 124:898–906.

REPERANT, L. A., D. HEGGLIN, C. FISCHER, L. KOHLER, J.

M. WEBER, AND P. DEPLAZES. 2007. Influence of

urbanization on the epidemiology of intestinal hel-

minths of the red fox (Vulpes vulpes) in Geneva,

Switzerland. Parasitology Research 101:605–611.

SEGURA, L. N. AND J. C. REBOREDA. 2011. Botfly

parasitism effects on nestling growth and mortality

of Red-crested Cardinals. Wilson Journal of Ornithol-

ogy 123:107–115.

SHOCHAT, E., P. S. WARREN, S. H. FAETH, N. E. MCINTYRE,

AND D. HOPE. 2006. From patterns to emerging

processes in mechanistic urban ecology. Trends in

Ecology and Evolution 21:186–191.

SIMON, A., D. THOMAS, J. BLONDEL, P. PERRET, AND M. M.

LAMBRECHTS. 2004. Physiological ecology of Medi-

terranean Blue Tits (Parus caeruleus L.): effects of

ectoparasites (Protocalliphora spp.) and food abun-

dance on metabolic capacity of nestlings. Physiolog-

ical and Biochemical Zoology 77:492–501.

SPALDING, M. G., J. W. MERTINS, P. B. WALSH, K. C.

MORIN, D. E. DUNMORE, AND D. J. FORRESTER. 2002.

Burrowing fly larvae (Philornis porteri) associated

with mortality of Eastern Bluebirds in Florida. Journal

of Wildlife Diseases 38:776–783.

STRACEY, C. M. 2010. Pattern and process in urban bird

communities: what makes the Northern Mockingbird

Le Gros et al. N URBANIZATION AND HOST-PARASITE INTERACTIONS 795

an urban adapter? Dissertation. University of Florida,

Gainesville, USA.

STRACEY, C. M. 2011. Resolving the urban nest predator

paradox: the role of alternative foods for nest

predators. Biological Conservation 144:1545–1552.

STRACEY, C. M. AND S. K. ROBINSON. In Press. Does nest

predation shape urban bird communities? Studies in

Avian Biology.

SURES, B. 2004. Environmental parasitology: relevancy of

parasites in monitoring environmental pollution.

Trends in Parasitology 20:170–177.

TOMPKINS, D. M., A. M. DUNN, M. J. SMITH, AND S.

TELFER. 2011. Wildlife diseases: from individuals to

ecosystems. Journal of Animal Ecology 80:19–38.

UHAZY, L. S. AND W. J. ARENDT. 1986. Pathogenesis

associated with philornid myasis (Diptera: Muscidae)

on nestling Pearly-eyed Thrashers (Aves: Mimidae) in

the Luquillo rain forest, Puerto Rico. Journal of

Wildlife Diseases 22:224–237.

YOUNG, B. E. 1993. Effects of the parasitic botfly Philornis

carinatus on nestling House Wrens, Troglodytes

aedon, in Costa Rica. Oecologia 93:256–262.

796 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 123, No. 4, December 2011