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The Condor 111(1):2135

The Cooper Ornithological Society 2009

Avian Assemblages in Altered and Natural Grasslands

in the Northern Campos of Uruguay
A drin B. A zpiroz1,2 and John G. Blake
Department of Biology, Research Building 223,University of Missouri-St. Louis, One University Boulevard,
St. Louis, MO 63121-4499

Abstract. Alteration of habitat has been highlighted as the most important factor causing declines in popula-
tions of grassland birds. In this study we characterized bird assemblages in cultivated and natural grasslands under
four different agricultural schemes in Uruguay. We surveyed birds along transects to determine species richness,
composition, and population density along this agricultural gradient. Although species richness was lower in the
most natural grassland type (24 species), community composition and abundance patterns highlighted the impor-
tance of natural grasslands for the conservation of habitat specialists. An analysis of similarity showed that bird
communities in the four grassland types were distinct (ANOSIM global R = 0.68). Several species using grassland
facultatively were characteristic of cultivated habitats, whereas the opposite was true for grassland obligates and
natural grasslands. An indicator-species analysis further supported the association of grassland-facultative
and grassland-obligate birds with cultivated and natural grassland, respectively. Population-density patterns var-
ied by species; some were more abundant in cultivated habitats, others in natural grasslands, but threatened species
attained relatively high densities in natural grasslands only. Some threatened species, such as the Ochre-breasted
Pipit (Anthus nattereri) and Pampas Meadowlark (Sturnella defilippii), were largely restricted to natural grass-
lands, so their long-term survival will depend on the conservation of suitable patches of these habitat types.

Key words: bird abundance, diversity patterns, grasslands, Northern Campos, Pampas, Uruguay

Ensambles de Aves en Pastizales Modificados y Naturales en los Campos

del Norte de Uruguay
Resumen. La alteracin de hbitat ha sido resaltada como el factor ms importante responsable por las re-
ducciones poblacionales de especies de aves de pastizal. En este estudio caracterizamos los ensambles de aves
presentes en pastizales cultivados y naturales bajo cuatro tipos diferentes de actividades agrcolas. Se utiliz la
tcnica de muestreos con distancia para determinar la riqueza de especies de aves, la composicin y la densidad
poblacional a lo largo de este gradiente agrcola. Aunque la riqueza de especies fue menor en el tipo de pastizal en
estado ms natural (24 especies), los patrones de composicin de la comunidad y abundancia resaltaron la impor-
tancia de los pastizales naturales para la conservacin de los especialistas de hbitat. Un anlisis de similaridad
mostr que las comunidades de aves en los cuatro tipos de pastizales eran distintas (ANOSIM R global = 0.68),
y varias especies facultativas de pastizal fueron caractersticas de los hbitats cultivados, mientras que lo con-
trario ocurri con las aves obligatorias de pastizal y los pastizales naturales. La asociacin entre aves facultativas
y obligatorias de pastizal y pastizales cultivados y naturales, respectivamente, fue tambin corroborada por los
resultados de un anlisis de especies indicadoras. Los patrones de densidad poblacional variaron entre las espe-
cies de aves, siendo algunas ms abundantes en los hbitats cultivados mientras que otras lo fueron en pastizales
naturales; pero las especies amenazadas slo fueron registradas en densidades relativamente altas en pastizales
naturales. Algunas especies amenazadas como Anthus nattereri y Sturnella defilippii estuvieron restringidas prin-
cipalmente a los pastizales naturales, por lo que su supervivencia en el largo plazo depender de la conservacin
de parches apropiados de este tipo de hbitat.

communities, as well as substantial declines of some species

highly dependent on grassland habitats (Zimmerman 1988,
The ecology and conservation of grassland birds have re- Knopf 1994, Tucker and Heath 1994, Patterson and Best 1996,
ceived substantial attention during the last decade. Numer- Vickery et al. 1999, Murphy 2003). Declines of grassland birds
ous studies, most conducted in Europe and North America, worldwide have been recognized as a prominent wildlife con-
have documented changes in the composition of grassland bird servation crisis of the 21st century (Brennan and Kuvlesky

Manuscript received 15 July 2008; accepted 25 December 2008.

Current address: Buxareo 1311, 11300 Montevideo, Uruguay

The Condor, Vol. 111, Number 1, pages 2135. ISSN 0010-5422, electronic ISSN 1938-5422. 2009 by The Cooper Ornithological Society. All rights reserved. Please direct all
requests for permission to photocopy or reproduce article content through the University of California Presss Rights and Permissions website,
reprintInfo.asp. DOI: 10.1525/cond.2009.080111


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22 Adrin B. Azpiroz and John G. Blake

2005). Habitat modification, particularly that related to agri- jor threat to many grassland specialists (BirdLife International
cultural expansion and intensification, has been identified as 2000, Askins et al. 2007), we expected natural grasslands
one of the main causes of such declines (Askins et al. 2007). to support more species and higher densities of grassland-
In the Neotropical Region, the most important expanse of obligate birds (sensu Vickery et al. 1999) than do cultivated
grasslands is located in south-eastern South America and is lands, as well as more threatened taxa. Factors, such as habitat
known as the Ro de la Plata grasslands (Soriano 1992). This loss, that reduce niche availability should represent a particu-
region (ca. 700 000 km 2), which is included within the Pam- lar threat to species that are ecologically specialized (Owens
pas biome (sensu Stotz et al. 1996), is dominated by temperate and Bennett 2000). If the degree of habitat specialization is a
subhumid grasslands that extend from 28 to 38 S and cover valid surrogate for ecological specialization, the proportion of
the plains of east-central Argentina, Uruguay, and southern grassland-obligate species (sensu Vickery et al. 1999) should
Brazil (Soriano 1992). Although the original vegetation was be inversely related to the degree of habitat loss. Thus, obligate
a tall-grass steppe, intermingled with prairies, marshes, and grassland species should be less well represented in terms of
other edaphic communities, it has been heavily modified by species numbers and densities in habitats where alteration has
long-term human use (Bucher and Nores 1988). In some mesic been more drastic (i.e., croplands and planted pastures).
regions of the Pampas, more than 50% of the land is devoted
to agriculture (Vickery et al. 1999). METHODS
Presettlement information on grassland bird assemblages Study area
in the Pampas is limited, but evidence exists that the loss of
pristine habitats in the region, as a consequence of expansion This study was conducted in the Northern Campos subregion
of agriculture and livestock grazing, has affected bird popu- of the Ro de la Plata grasslands (Soriano 1992) within the
lations, producing marked decreases in abundances and local Pampas biome (sensu Stotz et al. 1996). This subregion ex-
extinctions of some species (e.g., Bucher and Nores 1988, Sori- tends through most of Rio Grande do Sul, Brazil, southeast-
ano 1992, Collar et al. 1992, Tubaro and Gabelli 1999). Recent ern Misiones and eastern Corrientes provinces in Argentina,
studies in the Flooding Pampa of eastern Argentina (defined and northern Uruguay (Bilenca and Miarro 2004). Within
and mapped by Soriano 1992) have shown that changes in the Northern Campos, the study area was located in south-
the structure of grasslands due to fire or grazing result in the ern Salto and northwestern Paysand departments (31 19 to
replacement of grassland specialists, highly dependent on 31 44S and 56 42 to 57 56W), and it was composed of
tall grasslands, by others that prefer short grasslands (Com- rolling topography in which low mesas and rocky outcrops
paratore et al. 1996, Isacch and Martnez 2001). These pat- are interspersed. The area has mesothermic and humid fea-
terns are similar to those reported in areas of North America tures (Soriano 1992), with a mean annual temperature of 19C
where declining grassland endemics have been replaced by and mean annual rainfall of 1300 mm (Lezama et al. 2006).
more widespread counterparts (Knopf 1994). In spite of these Cattle ranching is the major activity, mainly on natural pas-
recent efforts, patterns of avian diversity currently associated tures, but also on planted pastures, the latter found especially in
with various land-use practices in the Pampas have not been the west. Cropland, especially fields of wheat and barley, is also
fully characterized, and more studies are needed to further widespread in the west. The eastern part of the study region is
assess the role of landscape alteration in shaping bird assem- characterized by large expanses of natural grasslands that have
blages in South American grasslands. This is particularly im- never been plowed and are used for open-range livestock graz-
portant in Uruguay, located within the campos subregion ing. The study was conducted on ranches and farms around
of the Pampas, where agricultural lands are the most exten- Chapicuy, in the department of Paysand and San Antonio
sive wildlife habitat and, therefore, represent key habitats for and Cerros de Vera in the department of Salto. Large patches
biodiversity; the extent of croplands, pastures, and rangelands of each habitat type (500 to 1200 ha) were selected within
greatly exceeds the areas set aside as wildlife reserves (OEA each of these areas.
1992, World Resource Institute 2007).
Here, we present results of the first study to examine the Habitat descriptions and species
effects of land-use practices on grassland bird communities definitions and categories
in the Northern Campos of Uruguay, a region defined and
The study focused on birds that inhabit grassland (sensu Vick-
mapped by Soriano (1992). A major goal of this study was to
ery et al. 1999) and grassland-like habitats. Habitats were clas-
determine the relative value for grassland bird conservation of
sified into four categories on the basis of different cultivation
areas under different management schemes. First, we charac-
and grazing regimes.
terized the distribution and seasonality of birds associated with
croplands, pasturelands, and two types of native grasslands. 1. Crop habitat (Crop) was represented by barley fields in-
Second, we compared species richness and abundance of bird tegrated into a system of livestock grazing in which the
communities found in each of these four habitat types. Because crop is rotated with planted pastures that are grazed after
habitat loss related to agriculture has been indicated as a ma- the crop is harvested. In fact, this habitat type consisted

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Grassland Bird Diversity in Northern Uruguay 23

of three different management phases: (1) barley fields dominica) and six species of Hirundinidae. Additionally, three
and stubble, (2) sunflower residual crop fields and stub- species categorized by Vickery et al. as facultative we clas-
ble, and (3) planted pastures. Barley and pastures were sify as obligate: the Greater Rhea (Rhea americana), Nacunda
planted in austral winter 2004. By the time bird censuses Nighthawk (Podager nacunda), and Chocolate-vented Tyrant
were initiated (September 2004), the barley was well (Neoxolmis rufiventris). We believe these adjustments bet-
grown (height >1 m) and planted pastures were starting ter reflect these species reliance on grassland habitats in Uru-
to grow beneath the crop. Barley was harvested in late guay (Azpiroz 2001). We assigned species to four categories
October 2004. From December 2004 to March 2005, a reflecting migration patterns (following Gore and Gepp 1978
residual crop of sunflower grew on these fields. This sec- and Azpiroz 2001): residents, summer residents, summer visi-
ond crop developed from seeds that fell to the ground tors, and winter visitors. Birds were also classified according
during the sunflower harvest in early 2004, and it was to five feeding guilds that reflect the main component of their
harvested in late March 2005; afterward, the fields were diets: carnivores, granivores, herbivores, insectivores, and om-
used for cattle grazing on the planted pastures until the nivores. Information on species migratory status and diet in
end of the study (November 2005). The management the Pampas were taken from the literature (e.g., Gore and Gepp
of this cropland is typical of this part of Uruguay. For 1978, Sick 1985, Canevari et al. 1991).
some analyses the crop phase (i.e., crop A; September
2004March 2005) and the pasture phase (i.e., crop B; Grassland bird surveys
MayNovember 2005) of this habitat type were treated We conducted bird counts on eight 500-m variable-width
separately. transects on each of the four habitat types every two months
2. Planted-pasture habitat (Pasture) consisted of grasslands from September 2004 to November 2005. Thus each transect
seeded with exotic grasses. These pastures were part of was sampled eight times during the whole sampling period.
dairy farms and were used for cattle grazing. Transects were located at least 400 m apart, far from fencerows,
3. One type of native habitat (Native 1) was represented by and avoided the intersection of other nongrassland habitats (i.e.,
native grasslands grazed by livestock. On these fields, gallery forest). We selected transects randomly after consid-
cattle and sheep forage on native grasses and forbs. As a ering these constraints. In total, approximately 120 ha of each
result of grazing by sheep, vegetation diversity is lower habitat type were sampled. All bird surveys were conducted by
than that in the following habitat type (Sturm 2001). Azpiroz. Transects were walked at a pace of approximately 1
4. A second type of native habitat (Native 2) consisted of km hr1 from 0 to 3.5 hours after sunrise, and all birds seen or
fields of native grasslands grazed by cattle and Pampas heard on each side, with the exception of individuals passing by
Deer (Ozotoceros bezoarticus). The latter are thought and making no use of the surveyed area, were recorded. Swal-
to be indicative of distinct grassland habitats (Sturm lows feeding on the wing within the surveyed plots were, how-
2001). Because of the lack of sheep grazing (only about ever, counted. Coverage of transects and the direction walked
2030 sheep were maintained on these fields to supply on each were rotated systematically. Distances and angles from
the ranch), this habitat supports, in general, a more com- transects to individuals were estimated with a rangefinder and
plex and higher vegetation structure than does Native 1 a compass, to allow calculation of perpendicular distances (see
(Sturm 2001). Buckland et al. 2001). These data were used to estimate vari-
ables (species richness, composition, and density) to describe
Cultivated habitats (Crop and Pasture) and natural grass- the avian community structure on each study site.
lands (Native 1 and Native 2) differ with respect to two impor-
tant management activities: use of agrochemicals and plowing. Statistical analysis
These activities were absent from natural grasslands. Addi- Species richness. We calculated species richness in each hab-
tionally, the former habitat types were located within a matrix itat type (and for both Crop phases separately) as the total
of croplands and planted pastures. In contrast, Native 1 and number of species encountered in all transects in each habitat,
Native 2 sites were included in a matrix of activities similar to all sampling periods pooled. We also calculated an estimate
those found in Native 1. However, because the study was con- of species richness on the basis of a jackknife estimator using
ducted on large patches of each habitat type, any confounding observed abundance-distribution data by species and the pro-
effects related to matrix composition were minimized. gram SPECRICH (Hines 1996). The method, which considers
Here, with minor modifications, we have followed the eco- detection probabilities differing by species, was described by
logical definition of grassland birds by Vickery et al. (1999). Burnham and Overton (1979). To test for seasonal differences
These authors identified two groups of grassland birds, obli- in species richness and number of individuals among habitats,
gate and facultative species, on the basis of their dependence on we used repeated-measures analyses of variance (rmANOVA).
grasslands (higher and lower, respectively). A series of species Data were tested for normality and, when necessary, standard
not included in their scheme we classify as grassland-facultative transformations were applied. Analyses of variance were run
birds. These include the American Golden-Plover (Pluvialis in SPSS, version 15.0 (SPSS 2006). We compared the rates

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24 Adrin B. Azpiroz and John G. Blake

of species accumulation across habitats through rarefaction Population densities. We used program DISTANCE ver-
analyses based on Monte Carlo simulations run 1000 times in sion 5.0 (Thomas et al. 2005) to estimate densities of grassland
EcoSim 7 (Gotelli and Entsminger 2006). The analyses were birds from census data obtained on transects. We constructed
based on a sample of 503 individuals, the lowest number of detection functions for all species with at least 60 observations.
birds recorded for any habitat (Crop A). For each species, data from all habitats were pooled except
Community composition. We used species presence/ab- when vegetation structure was thought to influence detection
sence over all sampling periods in each habitat to calculate probability. For example, census data from fields of barley and
BrayCurtis similarity coefficients among habitat types. Data sunflower were used separately from data from other habitats
from the similarity matrix were also used to test for differences where vegetation was significantly lower (unpubl. data). Addi-
in species composition among habitats through an analysis of tionally, in a few cases, species similar morphologically and be-
similarity (ANOSIM; Clarke and Warwick 2001). ANOSIM haviorally were grouped together in order to increase sample
determines whether samples (i.e., transects) within each habi- sizes to allow for construction of detection functions (see Buck-
tat type are more similar to each other than to samples taken at land et al. 2001:302). The probability of detecting each species
random from the whole sample pool (i.e., 32 transects). Thus as a function of perpendicular distance from the transects was
ANOSIM compares the level of similarity among transects of determined by means of the following robust models presented
a given habitat to that among transects of all habitats and de- by Buckland et al. (2001): uniform key function with cosine and
termines if the former is greater than expected by chance. Re- simple polynomial expansion series, the half-normal key func-
sults from ANOSIM were tested for significance with a Monte tion with cosine and hermite polynomial expansion series, and
Carlo randomization procedure. ANOSIM also estimates the hazard-rate key function with cosine and simple polynomial
pairwise comparisons, so used it to determine species turn- expansion series. We evaluated each of these models consider-
over at a spatial scale (comparisons among habitats) and at a ing the complete data set (i.e., all observations) or subsets with
temporal scale (comparisons among sampling periods within 5 and 10% truncation of detections at largest distances to re-
each habitat). Afterward, we used nonmetric multidimen- duce errors incurred by outliers, as recommended by Buckland
sional scaling (MDS) to compare species composition among et al. (2001). Model suitability was evaluated through Akaikes
transects and habitats. This analysis graphically portrays sim- information criterion (AIC). Density estimates are presented
ilarities and differences among samples based on species with standard errors and 95% confidence intervals; estimates
presence/absence; thus, points that are closer are more simi- for values with non-overlapping intervals were considered sig-
lar in terms of species composition. ANOSIM and MDS were nificantly different.
done with PRIMER version 5.2.9 (Clarke and Gorley 2002)
and PC-ORD version 4 (McCune and Mefford 1999), respec- RESULTS
tively. These analyses do not account for differences in de-
tectability, but because they were used to analyze data from Species richness
habitats with similar structural characteristics (i.e., grassland Throughout the whole 14-month sampling period, 4968 in-
and grassland-like habitats), we believe results are still infor- dividuals of 50 grassland bird species were recorded, all
mative despite this limitation. Across-habitat differences in transects combined (Appendix 1). Total observed species
the proportions of species included in categories of habitat richness varied from 24 on Native 2 to 34 on Native 1 (Table 1,
specialization, migration, and feeding guild were tested with Fig. 1), and results corrected through rarefaction analysis
G-tests. In order to identify characteristic species of each hab- yielded similar patterns (Table 1). Species richness estimated
itat type, we used an indicator-species analysis (Dufrne and with SPECRICH ranged from 26 2.0 for Native 2 to 43
Legendre 1997). This analysis, which we did in PC-ORD ver- 7.8 for Crop A, indicating that more species could still be re-
sion 4 (McCune and Mefford 1999), calculates an indicator corded in all habitats, especially in Crop A (Table 1).
value for species based on its relative frequency and relative The mean number of species per habitat varied signifi-
abundance in all treatment categories (i.e., habitat types). In- cantly through the sampling period (Fig. 2A) and responded to
dicator values can range from 0 (no indication) to 100 (per- the effects of time (rmANOVA, F7,196 = 7.46, P < 0.001), habitat
fect indication). A perfect indication for a given habitat means (rmANOVA, F3,28 = 10.66, P < 0.001), and time habitat in-
that the species was recorded in all samples (i.e., transects) teraction (rmANOVA, F21,196 = 2.99, P < 0.001). Mean number
within that habitat and was not observed in any of the samples of individuals per habitat (Fig. 2B) varied as an effect of time
of other habitats. Indicator values were tested for significance (rmANOVA, F7,196 = 2.09, P = 0.045) and time habitat inter-
with a Monte Carlo randomization procedure which com- action (rmANOVA, F21,196 = 2.09, P = 0.005); in this case, the
pares the observed indicator values to alternative values cal- effect of habitat was not significant (rmANOVA, F3,28 = 1.12,
culated from the same data and randomly assigned to habitat P = 0.36). During May 2005, a few large flocks (i.e., 38 indi-
type. Only species with indicator values that were significant viduals, the largest flocks recorded during the whole sampling
(P 0.01) and >25% are reported. period) of the Eared Dove (Zenaida auriculata) and Shiny

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Grassland Bird Diversity in Northern Uruguay 25

Phase A and Native 1 were the most different in species com-

position (R = 0.99, P = 0.001) (Table 2). In the assessment of
temporal turnover within each habitat, the results of ANOSIM
indicated that in all habitats differences in species composition
by sampling period were small (Fig. 3). Crop was the habitat
most different (global R = 0.43, P = 0.001) from the other three
habitats (Pasture global R = 0.30, P = 0.001; Native 1 global R =
0.15, P = 0.001; Native 2 global R = 0.34, P = 0.001).
The indicator-species analysis identified 11 species with
significant indicator values; four were associated with Crop,
three with Native 1, and four with Native 2 (Table 3). It iden-
tified no indicator species for Pasture. Except for the Great
Pampa-Finch (Embernagra platensis), Crop indicator species
were all facultative grassland birds. Conversely, all Native 2
indicator species were obligate grassland birds. Notably, all
three species of pipit showed indicator signals.
FIGURE 1. Species-accumulation curves for each of the four habi- Species differed in terms of habitat specialization, mi-
tats studied, based on visual and aural detections from September
2004 to November 2005. For Crop, two curves corresponding to each
gration status, and diet (Appendix 1). The total 50-species
of the two phases of this habitat type are presented (Crop A = crop pool included 23 obligate and 27 facultative grassland spe-
phase; Crop B = pasture phase; see Methods for more details). cies (sensu Vickery et al. 1999), respectively. Crop harbored
the highest proportion of facultative species and the lowest
Cowbird (Molothrus bonariensis) were observed in Crop of obligate species; the opposite pattern prevailed in Native
(Fig. 2B). When these flocks were excluded from the anal- 2. Bird assemblages were dominated by resident species,
ysis, the effect of time (rmANOVA, F7,196 = 1.75, P = 0.099) which represented between 71% and 85% of all species in the
was not significant and the effect of time habitat interaction four habitat types. Among migrants, only summer residents
(rmANOVA, F21,196 = 1.58, P = 0.058) was only marginally so. (present mainly from September to March) were well repre-
sented, accounting for 12 to 14% of all species found in each
Species composition habitat. In terms of feeding guilds, insectivores were the best
The mean number of habitat types used per species was 2.4 represented in all habitats, accounting for 42 to 66% of spe-
0.2. Eleven species were recorded in all four habitats, and 14 cies recorded. Proportion of granivores was highest in Crop
were seen in only a single habitat (Appendix 1). In terms of (30%) and lowest in Native 2 (8%). Despite these trends,
species composition, the analysis of similarity indicated that overall proportions of obligate/facultative species (G = 3.20,
overall differences in species composition by habitat were sig- df = 3, 0.50 > P > 0.25) and of species in different migration
nificant (global R = 0.68, P = 0.001), and such differences are (G = 6.76, df = 9, 0.75 > P > 0.50) and feeding-guild (G = 9.23,
highlighted in the MDS graphical representation (Fig. 3). In df = 12, 0.75 > P > 0.50) categories did not differ significantly
terms of spatial turnover, the two phases of Crop were the least by habitat.
different in species composition (R = 0.41, P = 0.001), followed Species of conservation concern were recorded in all hab-
by Native 1 and Native 2 (R = 0.42, P = 0.001), whereas Crop itat types. The Greater Rhea was the only one found in all

TABLE 1. Observed numbers of individuals and species and expected number of species in each of four
habitat types in the Northern Campos of Uruguay (RSR = rarefied species richness; ESR = estimated species
richness). Values for Crop distinguish between the crop phase (Crop A) and the pasture phase (Crop B;
see Methods for more details).


Crop A Crop B Pasture Native 1 Native 2

Total number transects 8 8 8 8 8
Total survey periods 4 4 8 8 8
Individuals observed 503 1052 1150 1225 1038
Observed species richness 26 28 30 34 24
RSR (95% CI) 26.0 25.9 26.4 28.8 24.0
(26.0) (24.028.0) (23.029.0) (25.032.0) (20.024.0)
ESR ( SE) 43 7.8 30 2.0 33 2.5 38 2.8 26 2.0

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26 Adrin B. Azpiroz and John G. Blake

FIGURE 2. Temporal variation in mean species richness (A) and mean number of individuals (B) for each habitat type from September
2004 to November 2005 in the Northern Campos of Uruguay.

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Grassland Bird Diversity in Northern Uruguay 27

TABLE 3. Indicator values (as percentage of perfect indication) and

values of Monte Carlo test of significance of observed maximum indi-
cator values. Only values significant at least at P < 0.01 are shown.

Indicator values based on habitats

Species Crop Pasture Native 1 Native 2 P
Gallinago paraguaiae 0 6 9 61 0.002
Columba maculosa 63 0 0 0 0.003
Zenaida auriculata 87 13 0 0 0.001
Geositta cunicularia 0 0 63 0 0.001
Xolmis cinerea 68 0 1 0 0.001
Alopochelidon fucata 1 0 56 0 0.002
Anthus furcatus 0 19 47 30 0.003
Anthus hellmayri 2 0 19 55 0.006
Anthus nattereri 0 0 1 83 0.001
Sicalis luteola 3 2 10 75 0.007
FIGURE 3. Nonmetric multidimensional scaling based on spe- Embernagra platensis 54 2 0 0 0.003
cies presence/absence per transect for each sampling period. Sym-
bols represent individual transects during a given sampling period:
Crop transects during crop phase (open circles) and pasture each habitat, the Spotted Nothura and Grassland Yellow-Finch
phase (filled circles); Pasture (squares), Native 1 (triangles), and Na- (Sicalis luteola) were the only ones shared by all. Additionally,
tive 2 (diamonds) habitats. The closer the symbols the more similar
the Southern Lapwing (Vanellus chilensis), White-rumped
they are in terms of species composition.
Swallow (Tachycineta leucorrhoa), and Short-billed Pipit were
included in the top ranks of all habitats except Crop. Unlike
four habitats; the Ochre-breasted Pipit (Anthus nattereri) and most species, density estimates of the White-rumped Swallow
Pampas Meadowlark (Sturnella defilippii) were recorded in and Brown-chested Martin (Progne tapera) were similar for
both Native 1 and Native 2, whereas the Dark-throated Seed- all four habitats (Table 4). In terms of individuals, the five most
eater (Sporophila ruficollis) was found in Crop and Pas- abundant species accounted for 67.6% of all birds recorded in
ture. The Buff-breasted Sandpiper (Tryngites subruficollis), Crop, 78% of those in Pasture, 62.5% of those in Native 1, and
Bearded Tachuri (Polystictus pectoralis) and Black-and-white 73.0% of those in Native 2 (Appendix 1).
Monjita (Heteroxolmis dominicana) were recorded only in
Native 1, Pasture, and Crop, respectively. DISCUSSION

Population densities Species richness

Patterns of species densities differed by habitat type. Of species The highest number of species was recorded in Native 1, the
with enough observations for detection functions to be built for lowest in Native 2; the former has a lower vegetation struc-
density estimation (Table 4, Appendix 2), five had higher den- ture that reflects the effects of sheep grazing (Sturm 2001, un-
sities in Native 1, four species had higher densities in Crop, publ. data). In the West Pampa (region defined and mapped by
and three species had higher densities in Native 2 and Pasture, Soriano 1992), Isacch et al. (2003) found that ungrazed natu-
respectively (Table 4). Species with the highest densities in- ral grasslands supported fewer species than did those under
cluded the White-browed Blackbird (Sturnella superciliaris) grazing regimes. They hypothesized that the greater struc-
and Eared Dove in Crop, Spotted Nothura (Nothura maculosa) tural heterogeneity promoted by grazing was responsible for
and White-browed Blackbird in Pasture, and Short-billed Pipit differences in species richness (Isacch et al. 2003). In con-
(Anthus furcatus) and Spotted Nothura in both Native 1 and trast, in his study of five North American grassland habitats,
Native 2. Among the 10 species with the highest densities for Wiens (1974) found it especially intriguing that habitats with
higher structural development did not support more species
TABLE 2. Pairwise comparisons in species composition than those with less.
among habitats based on presence/absence. Values are pairwise Undoubtedly, the relatively high number of species we
R from ANOSIM based on BrayCurtis similarity. All the com- found in Crop is explained, at least in part, by this habitat
parisons were significant (P < 0.05). categorys including several management phases with differ-
ing vegetation structures. Just as spatial habitat heterogeneity
Crop A Crop B Pasture Native 1
in agricultural landscapes is known to facilitate the co-oc-
Crop B 0.41 currence of species with diverse habitat requirements (e.g.,
Pasture 0.56 0.51 Verhulst et al. 2004), temporal habitat heterogeneity in Crop
Native 1 0.99 0.80 0.67 probably has a similar effect by allowing species with differ-
Native 2 0.95 0.81 0.70 0.42
ing ecological needs to exploit these areas whenever suitable

02_MS080111.indd 27 2/13/09 4:49:22 PM

28 Adrin B. Azpiroz and John G. Blake

TABLE 4. Density (individuals per 100 ha), SE, and 95% CI calculated with program
DISTANCE for species with at least 60 observations. The highest density value for each
species is shown in bold.

Species Crop Pasture Native 1 Native 2
Rhea americana
Mean 5.5 0.3 10.7 7.0
SE 2.1 0.3 3.1 2.3
95% CI 2.611.6 <0.11.6 6.218.7 3.713.2
Nothura maculosa
Mean 20.7 126.7 98.3 93.1
SE 9.6 41.2 32.5 29.4
95% CI 8.649.5 67.8236.8 52.0185.7 50.6171.2
Vanellus chilensis
Mean 5.6 28.1 49.3 31.7
SE 2.1 6.9 5.9 4.2
95% CI 2.711.5 17.345.6 39.062.4 24.441.1
Pluvialis dominica
Mean 0.0 0.0 4.8 1.1
SE 1.9 0.8
95% CI 2.210.4 0.34.2
Bartramia longicauda
Mean 1.3 4.0 3.0 1.3
SE 1.0 1.7 1.2 0.8
95% CI 0.35.3 1.79.1 1.46.3 0.44.1
Zenaida auriculataa
Mean 134.4
SE 43.7
95% CI 70.8255.3 N/A N/A N/A
Zenaida auriculatab
Mean 25.4 66.1 0.0 0.0
SE 15.0 29.0
95% CI 8.575.6 29.0151.2
Tachycineta leucorrhoa
Mean 18.4 14.1 11.7 4.9
SE 5.3 3.8 3.4 1.9
95% CI 10.432.4 8.323.9 6.620.7 2.310.4
Progne tapera
Mean 7.7 5.1 2.6 3.1
SE 2.1 2.1 1.7 1.2
95% CI 4.513.2 2.311.5 0.88.6 1.46.7
Anthus furcatus
Mean 0.0 94.3 321.2 219.2
SE 32.7 78.5 56.9
95% CI 48.5183.3 200.0515.6 132.7362.0
Anthus hellmayri
Mean 1.5 0.0 5.8 11.8
SE 0.7 1.7 3.2
95% CI 0.73.5 3.210.4 6.920.1
Anthus nattereri
Mean 0.0 0.0 1.1 21.1
SE 0.8 4.2
95% CI 0.34.3 14.231.1
Ammodramus humeralis
Mean 20.2 27.3 9.7 2.6
SE 6.9 14.0 4.3 2.1
95% CI 10.539.0 10.471.1 4.222.3 0.710.5

02_MS080111.indd 28 2/13/09 4:49:23 PM

Grassland Bird Diversity in Northern Uruguay 29

TABLE 4. (Continued)

Species Crop Pasture Native 1 Native 2
Sicalis luteola
Mean 3.2 3.2 5.0 47.9
SE 1.5 2.0 1.7 10.4
95% CI 1.37.7 1.09.9 2.69.6 31.273.5
Sturnella defilippii
Mean 0.0 0.0 13.6 1.5
SE 6.7 1.1
95% CI 5.434.3 0.45.8
Sturnella superciliarisa
Mean 242.4 N/A N/A N/A
SE 83.7
95% CI 124.8470.8
Sturnella superciliaris b
Mean 91.7 95.1 11.3
SE 27.0 21.4 4.1
95% CI 51.3164.1 61.2147.7 0.0 5.622.6
Detection function built exclusively with data from September 2004 to March 2005, corre-
sponding to the crop phase (barley and sunflower fields) of Crop habitat.
Detection function built with data from May to November 2005, corresponding to the crop
phase (barley and sunflower fields) of crop habitat, as well as with data from other habitats for
the total sampling period.

conditions become available (i.e., feeding and/or breeding albifrons), Great Pampa-Finch, and Dark-throated Seed-
opportunities). eater, place their nests in tall grass or shrubs, which also
In general, more species were present during the austral suggests that nest-site availability plays an important role in
spring and summer than during fall and winter. Similar tem- determining bird communities in this habitat type. This fac-
poral patterns have been reported for the West and Flood- tor is thought to be key in shaping bird assemblages in agri-
ing Pampas (Isacch and Martnez 2001, Isacch et al. 2003), cultural areas in general (Sderstrm et al. 2003).
where seasonal variation in species numbers stems, at least Cultivated and natural grasslands sites differed not only
in part, from more migratory birds reaching the study area in terms of agricultural management (local characteristics)
during the summer than during the winter (Isacch and Mar- but also in terms of the composition of the matrix in which
tnez 2001). This same pattern also applied to our study area the different types of grasslands were embedded (regional
in the Northern Campos, where the number of summer mi- characteristics). Cultivated grasslands were located within a
grants (11) was substantially higher than that of their winter similar matrix of crops and planted pastures, whereas natu-
counterparts (2). ral grasslands were located within a matrix characterized
by conditions resembling Native 1 habitat. This pattern re-
Species composition flected a logistic constraint, since there is currently no region
A relatively low proportion (22%) of all species in the study in Uruguay that contains habitat patches with the characteris-
area was present in all habitat types; most species were re- tics of those studied here within a single type of matrix. Be-
stricted to certain subsets of habitats (50%) or to single cause of this mismatch in matrix characteristics, differences
habitats (28%). The absence of several tyrant-flycatcher spe- in the bird community between habitats in cultivated and
cies from Native 2 is probably related to the lack of suitable natural grasslands may be influenced by this variable. But a
perches, a key feature of these species foraging strategies. substantial proportion of species being restricted to a single
Species absent from Crop suggest that this habitat type pro- habitat within each matrix type indicates that management
vides limited opportunities for ground-nesting birdsnot practices (i.e., local conditions) do play an important role in
surprising since operations in agricultural fields, especially determining species richness in the region. Information from
crop harvesting, can have detrimental effects on nesting suc- the southern Pampas supports this conclusion; the presence
cess (see Mller et al. 2005). Alternatively, many species of breeding Pampas Meadowlarks could be predicted by local
absent from Native 1, such as the Bearded Tachuri, Black- variables (e.g., local habitat-specific characteristics) but not
and-white Monjita, Long-tailed Reed-finch (Donacospiza by landscape variables (Fernndez et al. 2003).

02_MS080111.indd 29 2/13/09 4:49:24 PM

30 Adrin B. Azpiroz and John G. Blake

Population densities species from occupying what seem to be adequate nesting

In general, species with higher densities in cultivated habitat sites (Fernndez et al. 2003).
types are common and widespread throughout the Pampas,
while all species of conservation concern for which density es-
timates are available occurred exclusively or in higher densi- Contrary to expectations, natural grasslands did not support
ties in natural grasslands (Greater Rhea, Ochre-breasted Pipit, more grassland-obligate species than did cultivated grass-
Pampas Meadowlark). Although detailed information on the lands, although all but one of the species restricted to natu-
diet of grassland birds in the Pampas is limited, data from the ral grasslands were grassland obligates. The latter, however,
five most abundant species in each habitat type suggest that bird did attain higher densities in less modified habitats. The value
assemblages in cultivated grasslands are dominated by species of natural grasslands for grassland obligates is further high-
that rely heavily on seeds, while those in natural grasslands are lighted by the fact that most facultative indicator species were
dominated largely by species that regularly take insects. tied to Crop whereas most obligate indicator species were as-
The Short-billed Pipit was the most abundant species in sociated with either Native 1 or Native 2. Because of the fairly
natural grasslands. Additionally, differences in pipit densities pristine condition of Native 2, bird assemblages there probably
between cultivated and natural grasslands were very marked. resemble those typical of pre-settlement times in the Northern
Pipits are also important elements in natural grasslands of Campos of Uruguay more closely. On the basis of our results,
other subregions of the Pampas (Comparatore et al. 1996, other alternative land-use practices seem to have caused both
Isacch et al. 2003) and also in some North American grass- an increase in species richness and substantial shifts in spe-
lands (Owens and Myers 1973). cies composition in the Northern Campos.
In the case of the Greater Rhea, density estimates were During the last two decades (especially since 2000) land
significantly higher for Native 1 than for Pasture. In contrast, use in Uruguay has shifted toward an expansion of agriculture
in Crdoba province, Argentina, Bellis et al. (2004) reported and planted pastures, reducing native grasslands traditionally
the rhea to prefer planted pastures over natural grasslands. used for cattle ranching (Martino and Methol 2008). If this
This difference may reflect the effects of poaching, which af- trend continues it could trigger changes in bird distribution and
fects natural populations of the Greater Rhea severely (Bellis abundance patterns. The patterns we identify suggest that an
et al. 2004 and references therein). We noted poaching in our expansion of croplands will probably benefit a few common
Pasture sites, whereas it was infrequent in the Argentine study species (e.g., the Eared Dove and White-browed Blackbird) but
area (Bellis et al. 2004). will be detrimental to several other common and threatened
Density estimates of the Ochre-breasted Pipit for Native 2 birds. More land devoted to planted pastures will benefit several
were significantly higher than those for Native 1, suggest- common species (e.g., the Southern Lapwing and Short-billed
ing that the species population trends will be affected by the Pipit) that do not attain high densities in cropland but will nega-
availability of areas with characteristics similar to those found tively affect birds that are restricted to native grasslands (e.g.,
in Native 2. In other parts of its range, the Ochre-breasted the Pampas Meadowlark). Although a substantial increase of
Pipit has been reported to inhabit burnt areas with regener- land devoted to the Pampas Deer (where sheep are excluded) is
ating short grass and lightly grazed grasslands (Tyler 2004). unlikely, at a local scale an expansion of this habitat type would
It is worth noting that a few individuals were recorded in also benefit both common (e.g., the Grassland Yellow-finch)
Pasture from early October to early November 2005 (i.e., be- and threatened (Ochre-breasted Pipit) birds.
tween sampling periods). Attempts at breeding were not suc- Ours is the first characterization of grassland bird com-
cessful (nests were depredated or abandoned; unpubl. data). munities inhabiting an agricultural landscape in the Northern
On the basis of available information, which suggests Campos of Uruguay. We found that cultivated grasslands
high sensitivity to habitat change (Fernndez et al. 2003), a seem to provide suitable habitat for a substantial proportion
tight association of the Pampas Meadowlark with Native 2 of grassland birds, including some of the species of conserva-
was expected, but this was not the case. It is intriguing that the tion concern in the Pampas. Threatened species, however, at-
Pampas Meadowlark was largely confined to a specific area tained relatively high densities only in natural grasslands. The
of Native 1 and mostly absent from Native 2, even though, in availability of opportunities for feeding and breeding seem to
terms of grazing pressure and vegetation cover, the latter hab- have been an important factor shaping the bird communitys
itat better resembles the species preferences in southern Bue- structure in this region, something that has also been reported
nos Aires province, where the largest remaining population for avian communities in other farmland ecosystems (e.g.,
is located (Fernndez et al. 2003, R. Snchez pers. comm., Sderstrm et al. 2003, Whittingham et al. 2006). Because
Azpiroz unpubl. data). Interestingly, in Buenos Aires many these patterns are based solely on presence/absence data and
fields with adequate vegetation characteristics remained density estimates by species, the question of whether each
unused, and it has been suggested that factors such as lim- habitat supports viable populations of the species recorded
ited food resources and presence of predators may deter the in it has not been fully addressed. To do so, information on

02_MS080111.indd 30 2/13/09 4:49:24 PM

Grassland Bird Diversity in Northern Uruguay 31

demographic parameters, such as survival rates and breeding Canevari, M., P. Canevari, G. R. Carrizo, G. Harris, J. Rodrguez
success in each habitat, need to be considered. M ata, and R. J. Straneck. 1991. Nueva gua de las aves argenti-
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Clarke, K. R., and R. N. Gorley. 2002. PRIMER 5 for Windows,
ACKNOWLEDGMENTS version 5.2.9. PRIMER-E, Ltd., Plymouth, UK.
Clarke, K. R., and R. M. Warwick. 2001. Change in marine com-
We are indebted to J. P. Castro and family, G. Constantin, M. Berretta,
munities: an approach to statistical analysis and interpretation.
A. Menndez, E. Muguerza, J. Oviague, and L. Baranov for grant-
2nd ed. PRIMER-E, Ltd., Plymouth, UK.
ing permission to work on their lands. We thank field assistants and
Collar, N. J., L. P. Gonzaga, N. K rabbe, A. M adroo Nieto, L. G.
volunteers for their time and effort in data collection: G. Corts, A.
Naranjo, T. A. Parker III, and D. C. Wege. 1992. Threatened
Ocampo, E. Mndez, A. P. Blazina, C. A. Balbusso, K. Alexander,
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R. Snchez, G. Barrenechea, L. Liguori, C. Abud, A. Lafranconi, P.
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mida, F. Encinas, G. Veiga, F. Garca Olaso, and P. Arbiza. For logis-
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colorada) manejados con fuego (Prov. de Buenos Aires, Argen-
Bisio, M. Toucon, E. Mena, N. Rodrguez, R. Nuez, Familia San
tina). Interciencia 21:228237.
Martn, and P. Larrosa. Financial support for this research was pro-
Dufrne, M., and P. Legendre. 1997. Species assemblages and
vided by the Wildlife Conservation Society, Rufford Maurice Laing
indicator species: the need for a flexible asymmetrical approach.
Foundation, Cleveland Metroparks Zoo and Cleveland Zoological
Ecological Monographs 67:345366.
Society, Neotropical Grassland Conservancy, and Sigma XiThe
Fernndez, G. J., G. Posse, V. Ferretti, and F. M. Gabelli. 2003.
Scientific Research Society. Idea Wild and Neotropical Grassland
Birdhabitat relationship for the declining Pampas Meadowlark
Conservancy provided additional grants for field equipment. The
populations in the southern Pampas grasslands. Biological Con-
University of Missouri-St. Louis Institutional Animal Care and
servation 115:139148.
Use Committee approved all survey methods, and the Direccin de
Gore, M. E. J., and A. R. M. Gepp. 1978. Las aves del Uruguay.
Recursos Naturales, Ministerio de Agricultura, Ganadera y Pesca
Mosca Hnos. S.A., Montevideo, Uruguay.
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Grassland Bird Diversity in Northern Uruguay 33

APPENDIX 1. Number of individuals and species found in four grassland habitats, Crop (CR), Pastures (PA), Native 1 (N1), and Native
2 (N2). For the Crop column superscripts denote species recorded during one management phase only. Each species is also classified (+) by
habitat specialization, migration status, and feeding guild. Habitat specialization: obligate, OB; facultative, FA, sensu Vickery et al. (1999).
Migration status: year-round resident, RE; summer resident, SR; nearctic migrant, NM; winter migrant, WM. Feeding guild: carnivore, CA;
granivore, GR; herbivore, HE; insectivore, IN; omnivore, OM.

Habitat specialization Migration Feeding guild
Family/species CR PA N1 N2 OB FA RE SR NM WM CA GR HE IN OM
Greater Rhea Rhea americana 41 4 69 50 + + +
Red-winged Tinamou Rhynchotus 15 9 0 0 + + +
Spotted Nothura Nothura maculosa 38 143 142 116 + + +
Whistling Heron Syrigma sibilatrix 2c 4 1 0 + + +
Maguari Stork Ciconia maguari 0 0 0 3 + + +
White-tailed Kite Elanus leucurus 1 0 0 0 + + +
Cinereous Harrier Circus cinereus 0 1 0 2 + + + +
Southern Lapwing Vanellus chilensis 29c 146 278 186 + + +
American Golden-Plover Pluvialis 0 0 130 16 + + +
Tawny-throated Dotterel 0 0 1 0 + + +
Oreopholus ruficollis
Upland Sandpiper Bartramia 6c 20 27 15 + + +
South American Snipe Gallinago 0 6 9 34 + + +
Buff-breasted Sandpiper Tryngites 0 0 4 0 + + +
Spot-winged Pigeon Columba 19 0 0 0 + + +
Picazuro Pigeon Columba picazuro 23c 10 2 0 + + +
Eared Dove Zenaida auriculata 481 74 0 0 + + +
Monk Parakeet Myiopsitta monachus 61c 12 0 0 + + +
Burrowing Owl Athene cunicularia 0 5 3 4 + + +
Nacunda Nighthawk Podager 0 0 2 0 + + +
Field Flicker Colaptes campestris 1c 25 20 1 + + +
Common Miner Geositta cunicularia 0 0 18 0 + + +
Rufous Hornero Furnarius rufus 2 0 0 0 + + +
Firewood-Gatherer Anumbius 0 5 5 4 + + +
Bearded Tachuri Polystictus 0 3 0 0 + + +
Grey Monjita Xolmis cinerea 29 1 2 0 + + +
White Monjita Xolmis irupero 3c 2 1 0 + + +
Black-and-white Monjita 20 0 0 0 + + +
Heteroxolmis dominicana


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34 Adrin B. Azpiroz and John G. Blake

APPENDIX 1. (Continued)

Habitat specialization Migration Feeding guild
Family/species CR PA N1 N2 OB FA RE SR NM WM CA GR HE IN OM
Chocolate-vented Tyrant Neoxolmis 0 0 2 1 + + +
Cattle Tyrant Machetornis rixosus 4 1 5 0 + + +
Fork-tailed Flycatcher Tyrannus 14 12 5 0 + + +
White-rumped Swallow Tachycineta 43 45 21 13 + + +
Gray-breasted Martin Progne 4a 3 0 6 + + +
Brown-chested Martin Progne 22 22 7 6 + + +
Blue-and-white Swallow 0 0 2 0 + + +
Notiochelidon cyanoleuca
Tawny-headed Swallow 1a 0 8 0 + + +
Alopochelidon fucata
Rough-winged Swallow 0 0 2 0 + + +
Stelgidopteryx ruficollis
Short-billed Pipit Anthus furcatus 0 118 292 216 + + +
Hellmayrs Pipit Anthus hellmayri 5 0 23 48 + + +
Ochre-breasted Pipit Anthus 0 0 5 92 + + +
Rufous-collared Sparrow Zonotrichia 6b 0 1 0 + + +
Grassland Sparrow Ammodramus 29 43 32 13 + + +
Long-tailed Reed-Finch 1b 0 0 0 + + +
Donacospiza albifrons
Grassland Yellow-Finch Sicalis 15 9 26 148 + + +
Great Pampa-Finch Embernagra 12 2 0 0 + + +
Dark-throated Seedeater Sporophila 3 4 0 0 + + +
Pampas Meadowlark Sturnella 0 0 33 4 + + +
White-browed Blackbird Sturnella 460 416 0 55 + + +
Brown-and-Yellow Marshbird 23 2 43 3 + + +
Pseudoleistes virescens
Bay-winged Cowbird Agelaioides 15 0 0 0 + + +
Shiny Cowbird Molothrus 127c 3 4 2 + + +
Total individuals 1555 1150 1225 1038
Total species 33 30 34 24 23 27 37 8 3 2 5 10 1 28 6
Recorded only when field grown to barley.
Recorded only when field grown to sunflower.
Recorded only when field used as pasture.

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Grassland Bird Diversity in Northern Uruguay 35

APPENDIX 2. Number of observations and model selection of

detection functions of grassland birds in four habitats in northern
Uruguay. Pluvialis dominica, Bartramia longicauda, Progne chaly-
bea, and Sturnella defilippii had fewer than 60 observations each,
so detection functions for these species included additional obser-
vations of species of similar characteristics and behavior (Vanellus
chilensis for P. dominica and B. longicauda, Tachycineta leucorrhoa
for P. tapera, and Sturnella superciliaris for S. defilippii).

Species na Model selectedb mc

Rhea americana 81 HR + cosine 2
Nothura maculosa 131 HR + cosine 2
Vanellus chilensis 351 HN + cosine 3
Pluvialis dominica 367 HN + cosine 3
Bartramia longicauda 377 HN + cosine 3
Zenaida auriculatad 71 HN + cosine 2
Zenaida auriculatae 62 HR + cosine 2
Tachycineta leucorrhoa 80 HN + cosine 1
Progne tapera 116 HN + cosine 1
Anthus furcatus 498 HR + cosine 5
Anthus hellmayri 63 UN + polynomial 1
Anthus nattereri 83 HN + cosine 1
Ammodramus humeralis 68 HR + cosine 3
Sicalis luteola 131 UN + cosine 1
Sturnella defilippii 266 HR + polynomial 5
Sturnella superciliarisd 89 HR + cosine 4
Sturnella superciliarise 264 UN + cosine 4
Number of observations.
HR, hazard-rate base function; HN, half-normal base function;
UN, uniform base.
Number of parameters in detection function.
Detection function built exclusively with data collected from
September 2004 to March 2005, corresponding to the crop phase
(barley and sunflower fields) of crop habitat.
Detection function built with data collected from May to November
2005, corresponding to the pasture phase of crop habitat, as well
as with data from other habitats for the total sampling period.

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