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Effects of parasitism by brown-headed cowbirds (Molothrus ater) on reproductive success of three frequent hosts in New Mexico.

Evidence that many populations of songbirds in North America are not reproducing at self-sustaining levels has drawn considerable attention to the brood-parasitic, brown-headed cowbird (Molothrus ater, Morrison et al., 1999; Smith et al., 2000; Ortega et al., 2005). The brown-headed cowbird is an obligate brood parasite that lays its eggs into nests of >200 species (Friedmann and Kiff, 1985). Parasitism by cowbirds may reduce reproductive success of hosts through removal of eggs of the host, reduced hatching success of the host, and through competition between nestlings of the cowbird and host (Rothstein, 1975x; Payne, 1977). In some habitats, cowbirds parasitize a considerable portion of the available hosts' nests (e.g., Elliot, 1978; Robinson, 1992; Goguen and Mathews, 1998). Further, parasitism by cowbirds may be an important limiting factor in some populations of endangered species (Robinson et al., 1995).

Although brood parasitism generally reduces nesting productivity of hosts (Payne, 1977), studies of nesting dynamics of hosts have demonstrated that outcome of a parasitism event depends upon a complex of interactions between parasite and host. Size of host, life-history traits (e.g., length of incubation, diet), and behavior may influence the impact of parasitism on a given host (Robinson et al., 1995; Ortega, 1998; Lorenzana and Scaly, 1999). For example, some hosts rarely are able to raise any of their own young from nests that are parasitized (Marvil and Cruz, 1989; Harris, 1991; Ortega and Ortega, 2003), while others suffer smaller costs (Weatherhead, 1989; Eckerle and Breitwisch, 1997; Clotfelter and Yasukawa, 1999; Ortega and Ortega, 2001). In addition to characteristics of hosts, decisions made by the cowbird, such as whether to remove an egg of the host or to multiply parasitize a host, may also affect success of the host, but these behaviors are poorly understood. An improved understanding of how these traits and behaviors influence outcome of a parasitism event would be useful in predicting demographic implications of parasitism on populations of the host (May and Robinson, 1985). Further, knowledge gained of these relationships from studies of common species may be applied practically as models for rare or threatened species.

We studied nesting behavior of the blue-gray gnatcatcher (Polioptila caerulea), plumbeous vireo (Vireo plumbeus), and western tanager (Piranga ludoviciana) in pinyon juniper (Pinus-Juniperus) woodlands in New Mexico. These species represent a range of body sizes and exhibit considerable variation in several basic life-history traits and behaviors, yet all are commonly parasitized in the majority of their nests within these woodlands (Goguen and Mathews, 1998). Here we compare effects of parasitism by cowbirds on these hosts to examine how physical and behavioral characteristics of hosts, and aspects of behavior of cowbirds, affect host-specific costs of parasitism. Specifically, our objectives were to: 1) measure frequencies and intensities of parasitism, responses of hosts, and effects of parasitism on productivity of hosts; 2) compare relative effects of parasitism in relation to differences in physical and behavioral traits; and 3) examine how aspects of behavior of cowbirds (i.e., removal of eggs of the host and multiple parasitism) further affect nesting success and productivity of hosts.

MATERIALS AND METHODS--Study Area--We collected nesting data in Colfax County, northeastern New Mexico, as part of a long-term study of behavior of brown-headed cowbirds. During this research, we established 14, 35-ha study plots within pinyon juniper habitats distributed among four adjacent properties, and we studied breeding-bird communities on a subset of plots each year during 1993-2002, except 2000 (NRA Whittington Center, four plots, 1993-1999; V-7 Ranch, four plots, 1993-1997; CS Ranch, two plots, 2001; Vermejo Park Ranch, four plots, 2001-2002). All properties were along the eastern edge of the foothills of the Sangre de Cristo Mountains at the western edge of the Great Plains. All properties also were largely undeveloped; however, two were seasonally grazed by cattle (V-7 Ranch, CS Ranch), one was grazed by American bison (Bison bison; Vermejo Park Ranch), and one was ungrazed by domestic livestock or bison (NRA Whittington Center; see Goguen and Mathews, 1998; Goguen et al., 2005, for detailed descriptions of study sites).

All study plots were within 50 km of each other and were similar in habitat and elevation. In our study region, pinyon juniper habitat occupies a narrow zone along lower slopes of foothills between shortgrass prairie and mixed-conifer forests of ponderosa pine (Pinus ponderosa) and Douglas-fir (Pseudotsuga menziesii). All plots were covered by an open woodland dominated by pinyon pine (Pinus edulis), with scattered junipers throughout. The woody understory consisted of Gambel's (Quercus gambelli) and wavy-leaf (Q. undulata) oaks, alder-leaf mountain mahogany (Cercocarpus montanus), and skunkbush sumac (Rhus aromatica). Herbaceous understory generally was sparse, however, intrusions of shortgrass prairie dominated by blue grama (Bouteloua gracilis) were common, particularly at lower elevations.

Species Studied--We studied nesting behavior and reproductive success of the blue-gray gnatcatcher, plumbeous vireo, and western tanager (Table 1). All three species are insectivorous, migratory passerines that build above-ground, open-cup nests. All also are monogamous and typically single-brooded. Based on high rates of parasitism observed (Goguen and Mathews, 1998), all are acceptors of parasitism by cowbirds (sensu Rothstein, 1975b). The vireo and, particularly, the gnatcatcher, however, are known to desert some nests in association with parasitism (Marvil and Cruz, 1989; Goguen and Mathews, 1996). Response of the tanager to parasitism has not been studied previously.

Analyse--During May-July each year, 4-9 observers located and monitored nests of species of hosts on, and in, habitat surrounding a subset of the 14 study plots. We located nests by observing behavior of adults and following adults in their breeding activities. We visited plots about every other day to monitor status of parasitism and fate of each nest. Prior to analyses, we estimated date of initiation of clutch for each nest based on direct observation or by back-calculation from dates of hatching or fledging. We classified nests by status of parasitism (parasitized or unparasitized) and intensity of parasitism (number of eggs laid by cowbirds). Finally, we determined final size of clutch of the host (number of eggs of host present during incubation) for all nests that survived the egg-laying period and were checked during the incubation stage.

Because our data generally did not fit a normal distribution, we used non-parametric tests performed by SYSTAT, version 10 (Systat Software, Inc., Richmond, California). We used Pearson chi-square tests ([chi square]-value reported) to evaluate whether rates of parasitism varied among years for hosts. We used Spearman-rank correlation tests ([r.sub.s] value reported) to determine if intensity of parasitism was correlated among species of host across the 9 years. To test for within-season variation in rates of parasitism, we performed a Pearson chi-square test for each species of host using data from all years combined and grouped into ca. 2-week intervals that spanned the breeding season.

To determine if intensity of parasitism affected costs of parasitism on hosts, we further categorized parasitized nests as either singly parasitized (one cowbird egg) or multiply parasitized (>1 cowbird egg). For each species of host, we made the following comparisons: 1) we used Mann-Whitney U-tests (U-value reported) to compare size of clutch of host between unparasitized and singly parasitized nests, and between singly and multiply parasitized nests; 2) we used Gtests adjusted with the William's correction ([G.sub.adj] value reported) to determine if proportion of nests at which [greater than or equal to] 1 host hatched or [greater than or equal to] 1 host fledged differed between unparasitized and singly parasitized nests and between singly and multiply parasitized nests; and 3) we used Kruskal-Wallis tests (H-value reported) to determine if numbers of young of hosts fledged per nest, or per successful nest, differed among unparasitized, singly parasitized, or multiply parasitized nests. Last, we used Kruskal-Wallis tests to determine if numbers of young of hosts fledged per successful nest differed among the three species of hosts in unparasitized, singly parasitized, or multiply parasitized nests. In all cases in which comparisons involving Kruskal-Wallis tests indicated a significant difference, we used multiple Mann-Whitney U-tests to determine which categories differed.

RESULTS--We located and were able to determine status of parasitism of 288 nests of blue-gray gnatcatchers, 170 nests of plumbeous vireos, and 129 nests of western tanagers over the 9 years of study. Of these, 72.2, 71.2, and 31.0% of nests of gnatcatchers, vireos, and tanagers, respectively, were located before or during the egg-laying stage. Although we were less effective at finding nests of tanagers before incubation, most (84.5%) were located before the start of the nestling stage.

All three species were parasitized in the majority of nests in most years (Table 2). For all species, some variation in rate of parasitism was apparent among years; however, this variation was statistically significant only for the tanager ([[chi square].sub.8] = 48.0, P < 0.001; Table 2). Parasitized nests of all species commonly received >1 cowbird egg, although intensity of parasitism (mean number of cowbird eggs per parasitized nest) was not strongly correlated among species across years (gnatcatcher versus vireo, [r.sub.s] = 0.25; gnatcatcher versus tanager, [r.sub.s] = 0.44; vireo versus tanager, [r.sub.s] = 0.06; Table 2). Of 226 parasitized nests of gnatcatchers, 61.1% were parasitized with a single cowbird egg, 27.9% contained two, 9.7% contained three, 0.9% contained four, and 0.4% contained five. Of 142 parasitized nests of vireos, 52.1% contained one cowbird egg, 30.3% contained two, 9.2% contained three, 7.0% contained four, and 2.8% contained five. Of 93 parasitized nests of tanagers, 72.2% contained one cowbird egg, 16.7% contained two, 5.6% contained three, and 5.6% contained four. We confirmed status of parasitism, but were unable to acquire a final count of cowbird eggs for two additional nests of gnatcatchers and five additional nests of tanagers.

Within-season Patterns of Nesting and Parasitism--For all three hosts across all years, earliest nests of the season typically were initiated during the second or third week of May, with the peak period of first initiation of clutchns during the last week of May to the first week of June (Table 3). Renesting attempts continued through the first week of July for the vireo and tanager, but consistently continued through mid July for gnatcatchers. There was little apparent variation in rates of parasitism across the season for the vireo or tanager. For the gnatcatcher, rates of parasitism were consistent in May and June, but tended to drop after early July (Table 3).

Effects of Parasitism on Productivity of Host--Unparasitized nests contained more eggs of hosts, on average, than parasitized nests for all species of hosts suggesting that cowbirds removed eggs (Table 4). On average, size of clutch of singly parasitized nests was reduced relative to unparasitized nests by 0.3 eggs for the vireo and by 0.8 eggs for the gnatcatcher and tanager. In multiply parasitized nests, reduction in size of clutch was even more substantial, with two or three instances for each species in which all eggs of the host were removed (Table 4).

Parasitism increased the probability that a nest failed by reducing likelihood that eggs of the host hatched, likelihood that host young survived to fledging, or both (Table 5). Parasitism by cowbirds had a particularly large impact on productivity of the two smaller hosts; both the gnatcatcher and vireo rarely fledged any of their own young from parasitized nests, regardless of the number of cowbird eggs. In fact, when considering only nests that had [greater than ore equal to] 1 young (host or cowbird) survive to fledging, the number of young fledged by the host from unparasitized nests did not differ among hosts (H = 1.0, P = 0.606), but the tanager fledged more of its young, on average, than the gnatcatcher or vireo from both singly (H= 19.7, P < 0.001) and multiply parasitized nests (H= 10.4, P = 0.006; Table 6).

Gnatcatchers never fledged both their own young and young of cowbirds from the same nest, and were only successful at fledging young of hosts from parasitized nests in rare cases in which cowbird egg(s) failed to hatch, typically due to late-laying. Vireos similarly experienced a high cost of parasitism, fledging both young of hosts and cowbirds from the same nest in only one instance. In this instance, the single egg of a cowbird was laid during the egg-laying period of the host, but hatched at about the same time as eggs of the host rather than 3 days before, as was typical. Tanagers, in contrast, commonly fledged their own young from parasitized nests and often fledged mixed broods; tanagers fledged [greater than or equal to] 1 of their own young at 19 (82.6%) of 23 singly parasitized nests that also fledged a cowbird, and at 7 (41.2%) of 17 multiply parasitized nests that also fledged at least one cowbird. Further, tanagers often fledged >1 young of the host with a cowbird, even in multiply parasitized nests; of 19 singly parasitized nests from which mixed broods fledged, 68.4% fledged [greater than or equal to] 2 young tanagers; of 7 multiply parasitized nests from which mixed-broods fledged, 57.1% fledged ?2 young tanagers.

Responses of Hosts to Parasitism by Brown-headed Cowbirds--The primary response to parasitism was acceptance of the cowbird egg by all three hosts, although both the gnatcatcher (four cases observed) and vireo (two cases) buried some cowbird eggs that were laid prior to completion of the nest under the lining of the nest. All three species also deserted some nests in association with parasitism. Based only on nests located before the incubation stage, gnatcatchers deserted 36.2% of 163 parasitized nests, vireos deserted 30.6% of 98 parasitized nests, and tanagers deserted 24.2% of 29 parasitized nests. Of the 59 parasitized nests deserted by gnatcatchers, 23.7% were parasitized and deserted before the gnatcatcher laid an egg, 47.4% appeared to be deserted in response to reduction in size of clutch (deserted following the disappearance of [greater than or equal to] 2 eggs, presumably due to removal of eggs by cowbirds), and the remaining 28.8% were deserted soon after the parasitic event while still containing several eggs. Of the 30 parasitized nests deserted by vireos, 40.0% were parasitized and deserted before the vireo laid an egg, 26.7% were deserted following reduction in size of clutch, and the remaining 33.3% were deserted soon after the parasitic event while still containing several eggs. Of the seven parasitized nests deserted by tanagers, 42.9% were parasitized and deserted before the tanager laid an egg, 42.9% were deserted following reduction in size of clutch, and the remaining 14.3% were deserted soon after the parasitic event while still containing several eggs. Unparasitized nests rarely were deserted; rates of desertion of unparasitized nests that were located before or during egg-laying and that avoided predation through incubation were 11.1% for gnatcatchers (n = 36 nests), 5.9% for vireos (n = 17), and 0.0% for tanagers (n = 10).

DISCUSSION--Influence of Traits of Host on Costs of Parasitism--All three hosts experienced high rates of parasitism by cowbirds throughout their breeding season and suffered reduced productivity in parasitized nests. Costs of parasitism were negatively correlated to body size of host. Considering only nests that fledged young, presence of a single cowbird egg reduced the expected productivity of the western tanager by 52%, the plumbeous vireo by 70%, and the bluegray gnatcatcher by 89%. This reduction was more severe in multiply parasitized nests. Larger size at hatching allows a nestling of the host to better compete for food with a cowbird (Eckerle and Breitwisch, 1997), and may allow hatchlings of hosts that are larger than cowbirds to compensate for a shorter length of incubation by cowbirds. Given that adults of larger species also generally have higher rates of food provisioning (Saether, 1994), nestlings of large hosts may be more likely to obtain food because adults are able to deliver more food than a single cowbird can consume. In this study, the larger egg, and presumably size of hatching, of tanagers relative to cowbirds may have allowed nestlings of tanagers to tolerate competition with a cowbird, although the cowbird generally hatched 1-2 days earlier. Thus, tanagers rarely lost full broods when parasitized. That said, tanagers in this study appeared to be impacted by parasitism more than expected, given their size. Trine et al. (1998) showed that larger hosts (>30 g) usually suffered reductions in productivity of <30%, despite often being multiply parasitized. Productivity of the 30-g western tanager was reduced by 52% in singly parasitized nests, and 71% in multiply parasitized nests. This unusually large impact may relate to low availability of food and, thus, a lower rate of provisioning, in the arid pinyon juniper woodlands; Smith and Arcese (1994) noted that cost of parasitism was reduced when food supplies were increased artificially.

For the two smaller hosts, parasitism almost always lead to failure of their entire brood, and young of these hosts rarely fledged from parasitized nests when a cowbird hatched prior to, or on the same day as, eggs of the host. For these smaller species, however, failures of nests often were not related directly to limitations caused by small size (e.g., competitive ability of nestlings, rate of provisioning by adults).

For the plumbeous vireo, a long incubation period relative to the cowbird appears to be the primary cause for its poor success. Many hosts that are similar in size to the vireo, but have lengths of incubation comparable to that of a cowbird, regularly fledge both a cowbird and their own young from parasitized nests (e.g., dark-eyed junco Junco hyemalis; Wolf, 1987; chipping sparrow Ortega and Ortega, 2001; yellow warbler Dendroica petechia; Ortega, 1998; prothonotary warbler Protonotaria citrea; Hoover, 2003). In species with long periods of incubation (i.e., >13 days), however, early hatching of a cowbird often leads to cessation of incubation by the host, and reduced hatching success of remaining eggs (Rothstein, 1975a; McMaster and Scaly, 1999). Further, the head-start afforded a cowbird in these situations increases the competitive disadvantage already facing young of smaller hosts. Plumbeous vireos primarily were impacted by parasitism through starvation of nestlings in competition with a cowbird. Cowbirds generally hatched [greater than ore equal to] 2 days prior to vireos, and although some vireo eggs hatched in most nests, these young rarely survived >2 days. In the single case where both a vireo and cowbird fledged, the cowbird egg hatched nearly simultaneous with the young of the host eliminating this additional competitive advantage. In central Colorado, plumbeous vireos experienced a similar reduction in productivity in response to parasitism (76% reduction based on all parasitized nests), and also were successful primarily in parasitized nests only when the cowbird and young of the host were of similar age (Marvil and Cruz, 1989; Chace et al., 2000).

Blue-gray gnatcatchers are among the smallest of hosts of cowbirds (Friedmann, 1963). Thus, it is not surprising that nestlings of gnatcatchers did not survive competitive interactions with cowbirds, even when they hatched simultaneously. As a result, on a per-nest basis, it appears that gnatcatchers produced almost no young in this population. This result, however, is misleading to some degree due to desertion of nests. Desertion of nest is a common response to parasitism by many hosts (Friedmann, 1963). Unlike hosts that eject the cowbird egg, however, nest-deserting species tend to be inconsistent in their response to parasitism (Graham, 1988; Hill and Scaly, 1994; Budnik et al., 2001). In most species, desertion does not appear to occur in response to the cowbird egg, per se. Rather, it may be a response to an inappropriately timed laying of an egg by a cowbird (e.g., egg laid by cowbird prior to that of the host; Rothstein, 1975x), or to reduction in size of clutch in association with parasitism (Rothstein, 1982; Hill and Scaly, 1994; Kosciuch et al., 2006). These appear to be plausible explanations for most desertions of nests observed in this study; >66% of desertions by all three hosts occurred at nests that were either parasitized prior to initiation of clutch by host, or at nests that suffered substantial reductions in size of clutch. Some desertions also could have occurred in response to encounters of hosts with the cowbird at the nest (Strausberger and Burhans, 2001). Regardless of the cue, desertion of parasitized nests may increase fitness of the host by providing the host with a new opportunity to obtain an unparasitized clutch (Goguen and Mathews, 1996; Budnik et al., 2001; Kershner et al., 2001). This is particularly true for small species or species with long periods of incubation.

Influence of Behavior of Brown-headed Cowbirds on Costs of Parasitism--Aspects of behavior of cowbirds also influenced the impact of parasitism via removal of eggs of the host or multiple parasitism. Removal of eggs of the host by cowbirds represents an obvious cost for hosts. In fact, for many larger hosts, it often represents the primary cost of parasitism (e.g., Eckerle and Breitwisch, 1997; Clotfelter and Yasukawa, 1999; Trine, 2000). For smaller species of hosts that normally fail to raise any young from parasitized nests, like the vireo and gnatcatcher, this cost may ultimately be minimal. For these species, cost of removal of eggs by cowbirds is only realized if eggs of the cowbird fail to hatch. In some cases, removal of eggs by cowbirds may even indirectly benefit small hosts; if removal of eggs leads to desertion of nest, then a host that previously was likely to have raised only a cowbird obtains a new opportunity to acquire an unparasitized clutch.

Multiple parasitism can further amplify costs of parasitism via increased rates of removal of eggs of hosts by cowbirds and increased interspecific competition for food. In some cases, hosts that are affected minimally by single parasitism can suffer the loss of entire broods in multiply parasitized nests (Robinson et al., 1995). In this study, in a few rare cases for each of the hosts, nests failed when all eggs of the host were removed and replaced with [less than or equal to] 4 eggs of cowbirds. Overall, however, productivity of multiply parasitized nests only differed from that of singly parasitized nests in the case of the tanager (Table 6). This result easily is explained by high costs of single parasitism for the gnatcatcher and vireo. For these species, a single cowbird egg typically resulted in failure of all eggs of hosts allowing little opportunity for additional cowbird eggs to further reduce success. Tanagers, on the other hand, were able to fledge mixed broods, and were impacted by a higher rate of removal of eggs of the host by cowbirds and increased competition for food in multiply parasitized nests.

Associate Editor was Michael S. Husah.

We thank managers of the NRA Whittington Center, V-7 Ranch, Vermejo Park Ranch, and CS Ranch for generously allowing us access to their properties. We also thank the many field assistants who helped locate and monitor nests, and L. Borrero for translating the abstract. Funding and support for this research was provided by the National Biological Service, National Fish and Wildlife Foundation, Zoological Society of Milwaukee County, Department of Range and Wildlife at Texas Tech University, Department of Wildlife Ecology at the University of Wisconsin-Madison, and by the School of Forest Resources at Pennsylvania State University.

Submitted 19 November 2007. Accepted 22 July 2008.

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WOLF, L. 1987. Host parasite interactions of brown-headed cowbirds and dark-eyed juncos in Virginia. Wilson Bulletin 99:338-350.

CHRISTOPHER B. GOGUEN,* DAVID R. CURSON, AND NANCY E. MATHEWS

Biology Program, Pennsylvania State University, 76 University Drive, Hazleton, PA 18202 (CBG) Audubon Maryland-DC 243 7 Eastern Avenue, Baltimore, MD 21224 (DRC) Nelson Institute for Environmental Studies, University of Wisconsin, 70 Science Hall, Madison, WI 53 706 (NEM)

* Correspondent: cbg10@psu.edu
TABLE 1--Characteristics of the three avian hosts
and the brown-headed cowbird. (a)

 Brown-
 Blue-gray Plumbeous Western headed
Characteristic gnatcatcher vireo tanager cowbird

Average mass
 of egg (g) 1.0 2.0 3.4 2.5
Average mass of
 adult female (g) 6 17 30 35
Length of incubation
 period (days) 13 14-15 13 10-12
Length of nestling
 period (days) 13 13-14 11-12 10-11

(a) Most information is from Ellison (1992), Curson and Goguen
(1998), Hudon (1999), and Lowther (1993), but mass of
brown-headed cowbird is for females captured on our study area
during May June 1995-1996 (n = 34), average mass of egg for
blue-gray gnatcatchers is from Wetherbee and Wetherbee (1951),
and other masses of eggs are from samples from our study area:
plumbeous vireo (n = 20); western tanager (n = 6); and
brown-headed cowbird (n = 22).

TABLE 2--Annual rates of parasitism of three avian hosts nesting in
pinyon juniper (Pinus, juniperus) woodlands in northeastern New
Mexico, 1993-1999 and 2001-2002.

Host 1993 1994 1995 1996 1997

Blue-gray gnatcatcher
 n (a) 21 27 22 40 54
 Parasitized (%) 81.0 77.8 86.4 85.0 74.1
 Eggs/nest (b) 1.3 1.4 1.5 1.7 1.3
Plumbeous vireo
 n (a) 13 19 26 17 19
 Parasitized (%) 92.2 89.5 84.6 76.5 63.2
 Eggs/nest (b) 2.1 1.5 1.6 2.2 1.6
Western tanager
 n (a) 16 9 11 17 15
 Parasitized (%) 100 100 54.5 41.2 33.3
 Eggs/nest (b) 1.5 1.3 1.0 2.2 1.2

Host 1998 1999 2001 2002 Total

Blue-gray gnatcatcher
 n (a) 27 41 35 21 288
 Parasitized (%) 66.7 92.7 80.0 61.9 79.2
 Eggs/nest (b) 1.7 1.8 1.5 1.5 1.5
Plumbeous vireo
 n (a) 25 29 8 14 170
 Parasitized (%) 88.0 89.7 75.0 85.7 83.5
 Eggs/nest (b) 1.8 2.2 1.2 1.2 1.8
Western tanager
 n (a) 22 13 8 18 129
 Parasitized (%) 90.9 92.3 62.5 100 76.0
 Eggs/nest (b) 1.7 1.7 2.4 1.4 1.6

(a) Number of nests for which we were able to confirm parasitism
status.

(b) Mean number of eggs of brown-headed cowbirds laid per
parasitized nest.

TABLE 3--Seasonal rates of parasitism of three avian hosts
nesting in pinyon juniper (Pinus, juniperus) woodlands
in northeastern New Mexico, 1993-1999 and 2001-2002. Rates
are based on nests from all years combined.

 Proportion of nests parasitized
 (number of nests)
Seasonal
interval (a) Blue-gray Plumbeous Western
 gnatcatcher vireo tanager

Before 25 May 0.80 (25) 0.76 (25) 0.67 (9)
25 May-7 June 0.85 (106) 0.85 (75) 0.71 (77)
8-22 June 0.77 (66) 0.82 (34) 0.90 (29)
23 June-7 July 0.73 (48) 0.90 (20) 0.80 (5)
After 7 July 0.58 (19) 0 (1) --

(a) Proportion of nests parasitized did not vary among
seasonal intervals for the blue-gray gnatcatcher ([[chi
square].sub.4] = 8.3, P = 0.081), plumbeous vireo ([chi
square].sub.3] = 1.9, P = 0.593), and western tanager
([[chi square].sub.3] = 4.3, P = 0.231).

TABLE 4--Distribution of size of clutch, of three avian hosts
based on status of parasitism by brown-headed cowbirds
(Molothrus ater) in pinyon juniper (Pinus-Juniperus) woodlands in
northeastern New Mexico, 1993-1999 and 2001-2002.

 Percentage of nests,
 by size of clutch

Host Parasitism n 0 1 2

Blue-gray Unparasitized nests 60 0 0 6.7
gnatcatcher Singly parasitized 123 0.8 7.3 16.3
 Multiply parasitized 77 2.6 19.5 23.4
 All parasitized 200 1.5 12.0 19.0

Plumbeous Unparasitized nests 28 0 0 3.6
vireo Singly parasitized 63 0 3.2 12.7
 Multiply parasitized 56 3.6 10.7 25.0
 All parasitized 119 1.7 6.7 18.5

Western Unparasitized nests 30 0 0 23.3
tanager Singly parasitized 47 0 8.5 25.5
 Multiply parasitized 31 9.7 19.4 35.5
 All parasitized 78 3.8 12.8 29.5

 Percentage of nests,
 by size of clutch
 Mean
Host Parasitism 3 4 5 (SD) (b)

Blue-gray Unparasitized nests 15.0 50.0 28.3 4.0 (0.8)
gnatcatcher Singly parasitized 32.5 32.5 10.6 3.2 (1.1)
 Multiply parasitized 41.6 13.0 0 2.4 (1.0)
 All parasitized 36.0 25.0 6.5 2.9 (1.2)

Plumbeous Unparasitized nests 28.6 67.9 0 3.6 (0.6)
vireo Singly parasitized 34.9 47.6 1.6 3.3 (0.8)
 Multiply parasitized 42.9 17.9 0 2.6 (1.0)
 All parasitized 38.7 33.6 0.8 3.0 (1.0)

Western Unparasitized nests 10.0 60.0 6.7 3.5 (0.9)
tanager Singly parasitized 53.2 12.8 0 2.7 (0.8)
 Multiply parasitized 32.3 3.2 0 2.0 (1.0)
 All parasitized 44.9 9.0 0 2.4 (1.0)

(a) Size of clutch is number of eggs of the host observed in a nest;
numbers are percentage of nests observed with the associated size
of clutch, and includes only nests that survived the egg-laying
stage.

(b) Mean size of clutch was significantly larger in unparasitized
nests than in singly parasitized nests for the blue gray gnatcatcher
([U.sub.s] = 2,169.5, P < 0.001) and western tanager
([U.sub.s] = 368.5, P < 0.001), and was not significant for the
plumbeous vireo ([U.sub.s] = 697, P = 0.077). For all three species,
mean size of clutch of singly parasitized nests was significantly larger
than that of multiply parasitized nests (blue-gray gnatcatcher,
[U.sub.s] = 2,943.5, P < 0.001; plumbeous vireo, [U.sub.s] = 1,064.0,
P < 0.001; western tanager, [U.sub.s] = 451.0, P = 0.003).

TABLE 5--Effect of parasitism by brown-headed cowbirds (Molothrus
ater) on hatching and fledging success of three avian hosts
nesting in pinyon juniper (Pinus, juniperus) woodlands in
northeastern New Mexico, 1993-1999 and 2001-2002.

 Number Percentage
 of of nests
Host nests hatched (a)
Blue-gray gnatcatcher
 Unparasitized 50 64.0
 Singly parasitized 129 45.0
 Multiply parasitized 80 31.3
Plumbeous vireo
 Unparasitized 25 64.0
 Singly parasitized 62 51.6
 Multiply parasitized 64 45.3
Western tanager
 Unparasitized 31 83.9
 Singly parasitized 53 71.7
 Multiply parasitized 35 48.6

 Percentage Mean number
 of of young of
 successful host fledged/
Host nests (b) nest (SD) (c)
Blue-gray gnatcatcher
 Unparasitized 42.0 1.40 (1.80)
 Singly parasitized 4.7 0.15 (0.65)
 Multiply parasitized 2.5 0.06 (0.40)
Plumbeous vireo
 Unparasitized 52.0 1.44 (1.62)
 Singly parasitized 14.5 0.29 (0.88)
 Multiply parasitized 6.3 0.11 (0.48)
Western tanager
 Unparasitized 67.7 2.13 (1.67)
 Singly parasitized 49.1 0.82 (0.97)
 Multiply parasitized 25.7 0.49 (0.92)

(a) Percentage of nests at which at [greater than or equal to] 1
eggs of the host hatched. For the blue-gray gnatcatcher, rate of
hatching was greater in unparasitized nests than in singly
parasitized ([G.sub.adj] = 5.2, P = 0.023), and was greater in
singly parasitized nests than in multiply parasitized ([G.sub.adj]
= 3.9, P = 0.048). For the plumbeous vireo, rate of hatching did
not differ by status of parasitism (P > 0.05). For the western
tanager, rate of hatching did not differ between unparasitized and
singly parasitized nests ([G.sub.adj] = 1.6, P = 0.206), but was
greater in singly parasitized nests than in multiply parasitized
nests ([G.sub.adj] = 4.7, P = 0.030).

(b) A successful nest fledged [greater than or equal to] 1 young of
the host. For the blue-gray gnatcatcher, proportion of successful
nests was greater in unparasitized than singly parasitized nests
([G.sub.adj] = 34.4, P < 0.001), but did not differ between singly
and multiply parasitized nests ([G.sub.adj] = 0.6, P = 0.439). For
the plumbeous vireo, proportion of successful nests was greater in
unparasitized nests than in singly parasitized nests ([G.sub.adj] =
12.0, P < 0.001), but did not differ between singly and multiply
parasitized nests ([G.sub.adj] = 2.3, P = 0.129). For the western
tanager, proportion of successful nests did not differ between
unparasitized and singly parasitized nests ([G.sub.adj] = 2.8, P =
0.094), but was greater in singly parasitized nests than in
multiply parasitized nests ([G.sub.adj] = 4.8, P = 0.028).

(c) Mean number of young of the host fledged/nest was greater in
unparasitized nests than in singly parasitized nests for blue-gray
gnatcatchers (US = 2,007.0, P < 0.001), plumbeous vireos (US =
447.5, P < 0.001), and western tanagers ([U.sub.S] = 442.0, P <
0.001). Mean number of young of the host fledged/nest did not
differ between singly and multiply parasitized nests for any host
(P > 0.05).

TABLE 6--Mean number of young of hosts and brown-headed cowbirds
(Molothrus ater) fledged based on intensity of parasitism and
including only nests that fledged ?1 young of hosts and
brown-headed cowbirds. Nests were in pinyon juniper (Pinus-Juniperus)
woodlands in northeastern New Mexico, 1993-1999 and 2001-2002.

 Singly
Host Unparasitized parasitized
Blue-gray gnatcatcher
 n 21 38
 Mean number
 of hosts fledged
 (SD) (a) 3.33 (1.06) (a) 0.50 (1.13) (b)
 Mean number
 of brown-headed
 cowbirds
 fledged (SD) 0 0.82 (0.39)
Plumbeous vireo
 n 13 20
 Mean number of
 hosts fledged
 (SD) (a) 3.00 (0.82) (a) 0.90 (1.37) (b)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 0 0.70 (0.47)
Western tanager
 n 21 28
 Mean number of
 hosts fledged
 (SD) a 3.14 (0.91) (a) 1.5 (0.84) (b)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 0 0.82 (0.39)

 Multiply All
Host parasitized multiply
Blue-gray gnatcatcher
 n 27 20
 Mean number
 of hosts fledged
 (SD) (a) 0.19 (0.68) (b) 0.25 (0.79)
 Mean number
 of brown-headed
 cowbirds
 fledged (SD) 1.07 (0.47) 1.00 (0.46)
Plumbeous vireo
 n 24 16
 Mean number of
 hosts fledged
 (SD) (a) 0.29 (0.75) (b) 0.38 (0.89)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 1.21 (0.72) 1.06 (0.68)
Western tanager
 n 19 12
 Mean number of
 hosts fledged
 (SD) a 0.90 (1.10)c 1.33 (1.15)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 1.47 (0.77) 1.33 (0.78)

 Doubly only >2
 eggs of brown
Host headed cowbird
Blue-gray gnatcatcher
 n 7
 Mean number
 of hosts fledged
 (SD) (a) 0
 Mean number
 of brown-headed
 cowbirds
 fledged (SD) 1.29 (0.49)
Plumbeous vireo
 n 8
 Mean number of
 hosts fledged
 (SD) (a) 0.13 (0.35)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 1.50 (0.76)
Western tanager
 n 7
 Mean number of
 hosts fledged
 (SD) a 0.14 (0.38)
 Mean number of
 brown-headed
 cowbirds
 fledged (SD) 1.71 (0.76)

(a) Mean number of young of hosts fledged differed among
unparasitized, singly parasitized, or all multiply parasitized
nests for the blue-gray gnatcatcher (Kruskal-Wallis test; H = 55.1,
P < 0.001), plumbeous vireo (H = 28.7, P < 0.001), and western
tanager (H = 31.8, P < 0.001). Within species, means followed by
different letters differ significantly.
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Author:Goguen, Christopher B.; Curson, David R.; Mathews, Nancy E.
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1USA
Date:Mar 1, 2009
Words:6991
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