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2010 SOUTHEASTERN NATURALIST 9(1):95–104
River-based Surveys for Assessing Riparian Bird
Populations: Cerulean Warbler as a Test Case
Mark B. Robbins1,*, Árpád S. Nyári1, Monica Papeş1, Brett W. Benz1,
and Brian R. Barber1,2
Abstract - Birds concentrated in riparian habitats are poorly sampled by traditional
survey methods because of the difficulties associated with accessing these habitats.
Our objectives were to test the effectiveness of river-based surveys to determine the
status, distribution, and relative abundance for riparian bird species in Missouri and
northern Arkansas, with special emphasis on Dendroica cerulea (Cerulean Warbler).
Our canoe-based surveys revealed an average of 2.3 and 0.8 singing male Cerulean
Warblers/river km along the Current River (128 river km surveyed), MO, and the
Buffalo National River (96 river km), AR. Nonparametric estimates for repeated
surveys of the same river stretches indicate that 69–79% of singing male Cerulean
Warblers were detected. However, the bias associated with the estimate methodology
and independent song rate data suggest those are conservative estimates. In
comparison with land-based point-counts, this river-based protocol offers a quick
and efficient assessment of Cerulean Warblers in riparian areas.
Riparian birds are among the most under-sampled category of birds in
North America due to the difficulty in accessing the habitat (Fletcher and
Hutto 2006, Peterjohn 1994). The most comprehensive data set for assessing
North American avian population trends, the United States Geological Survey
(USGS) Breeding Bird Survey (BBS), is limited to road-based surveys
and therefore samples only a small proportion of riparian habitats. Studies
using BBS data to assess population estimates, trends, conservation priorities,
or depict distributions with relative abundance isoclines (James et al.
1992, Panjabi et al. 2005, Price et al. 1995, Rich et al. 2004, Rosenberg and
Blancher 2005) of riparian species have suffered from limited sample sizes
as well as other biases (Confer et al. 2008, Link and Sauer 2002, Thogmartin
et al. 2006). One approach to solving this problem has been to lump data
from multiple habitats into single estimates (e.g., Sauer and Droege 1992),
but trends for better-sampled habitats mask trends for less-sampled riparian
habitats (Robbins et al. 1986).
Link and Sauer (2002) underscored that species like Dendroica cerulea
Wilson (Cerulean Warbler) are poorly sampled using BBS protocol since
relatively few individuals are encountered because the roadside surveys
transverse only a limited portion of the species’ habitats. Across much of
1The University of Kansas Natural History Museum and Biodiversity Research
Center, 1345 Jayhawk Boulevard, Lawrence, KS 66045. 2Department of Biology,
Brigham Young University, Central 401 WIDB, Provo, UT 84602. *Corresponding
author - firstname.lastname@example.org.
96 Southeastern Naturalist Vol. 9, No. 1
its distribution, the Cerulean Warbler breeds in riparian habitat, and in some
regions, such as Missouri and Arkansas, a large proportion of its populations
are in riparian forest, which have been poorly sampled using conventional
survey methods (Jacobs and Wilson 1997, Robbins et al. 1998; data presented
herein). To address this issue, we conducted river-based surveys for
15–19 species, depending on species composition, across 16 river systems
(760 km) in Missouri and northern Arkansas. As a test case for using this
method to assess riparian bird populations, we present results for Cerulean
Warblers, a species that has been reported as having suffered the most significant decline of any passerine in North America during the 40-year history
of the BBS (Hamel 2000a, b; Hamel et al. 2004; Robbins et al. 1992).
Methods and Study Areas
From 1992 through 2006 we conducted surveys of 15–19 species of
riparian-inhabiting avian species across 16 rivers systems (760 river km)
in Missouri and northern Arkansas (Robbins 2003; M.B. Robbins, unpubl.
Data; Robbins et al. 1998). Here we present results from surveys conducted
in 2003 and 2004 on the Current River and 2006 on the Buffalo River. In
an attempt to estimate the number of individuals detected by this protocol,
we conducted repeat surveys of three sections of two of these rivers. Locations
and dates of repeat surveys were: upper Current River Pulltite access
(37º20.0'N, 91º28.5'W) to Round Spring access (37º16.8'N, 91º24.2'W)
(15.4 river km), 25–26 May 2004 and Round Spring access to Jerktail
Landing (37º13.7'N, 91º18.5'W) (19.8 river km), 27–28 May 2004; Buffalo
National River: Maumee North access (36º02.11'N, 92º37.70'W) to Highway
14 access (36º04.03'N, 92º34.73'W) (15.7 river km), 2 and 4 June 2006.
Each repeated river section was subdivided into three subsections so withinsection
variability could be analyzed.
All surveys were initiated at 05:00 hrs (CST), from a canoe with little to
no paddling and at average fl ow rates (± SD) of 4.0 ± 0.5 km/hr (4.1 ± 0.4
for repeat surveys only). No surveys were done under river fl ow extremes,
i.e., after heavy rains which increased fl ow and noise, or during low water
levels, and only under conditions of no precipitation and no or very light
wind. A global positioning system unit (Garmin 12, Map Datum WGS 84)
was continually used to monitor canoe fl ow rate during all surveys. In areas
of relatively fast fl ow, e.g., short, narrow stretches with associated riffl es
at a sharp bend in the river, we either stopped prior to or immediately after
such areas for 3–5 min to increase the likelihood that singing males would
be detected. We surveyed river sections that did not exceed 20 km (with one
exception) in length each day to ensure that surveys were completed by ca.
10:00 hrs. River width was generally <50 m (maximum 90 m), so birds on
both sides of the river could be heard. We estimate, based on monitoring
singing behavior of Cerulean Warblers, that we sampled riparian corriders
ca. 100 m in width on each side of the river bank (Robbins et al. 2009).
Although we recorded the number of detected individuals of 15–19 ripar2010
M.B. Robbins, Á.S. Nyári, M. Papeş, B.W. Benz, and B.R. Barber 97
ian species during all surveys, including repeat surveys of the same routes,
because of logistics associated with recording coordinates for literally
hundreds of individuals, coordinates were taken for only Cerulean Warbler.
Thus, we used this species as a test case to estimate the number of individuals
that might be detected during river-based surveys.
To ensure that Cerulean Warbler songs were not confused with Type B
(= Song Type II, (Moldenhauer and Regelski 1996) of Parula americana L.
(Northern Parula), each Cerulean Warbler was heard singing at least twice
before being tallied. GPS coordinates and the side of the river from which
the bird sang were recorded for each male; GPS readings were taken at the
point when the canoe-based observer was closest to a singing male (i.e.,
shortest perpendicular distance of male to stream). Because of vegetation
density, time, and effort constraints, distances between the canoe-based
observer and the eye-level base of the tree from which the bird sang could
not be recorded reliably to estimate detection probabilities (Buckland et al.
2001). However, we took distance measurements with a laser range finder
from the observer to the singing bird, typically in the crown of emergent
sycamores, to obtain approximate distance estimation. All surveys followed
BBS weather protocol and were conducted when human volume on the river
was either non-existent or very low. A single observer recorded bird detections
to eliminate multiple surveyor bias (Sauer et al. 1994).
To estimate the number of Cerulean Warblers not detected on single
surveys, repeat surveys were conducted on three river sections: two on the
upper Current and one on the lower Buffalo National (details above). All
repeat surveys were conducted within two days of the original survey.
In ArcGIS 8.3 (ESRI 1999–2002), we created a 100-m radius buffer
around each Cerulean Warbler male GPS location as an approximation to
individual territory size. We chose the 100-m radius based on a combination
of male territory size and error associated with how GPS readings of male
locations were obtained. Average (± SD) male Cerulean Warbler territory
size was 0.9 ± 0.1 ha, with a maximum width by length of 112 (± 18) x 87
(± 33) m (n = 20 males that were monitored for a minimum of four consecutive
hrs, 05:00–09:00; Robbins et al. 2009). GPS readings of singing males
were taken from the river (ca. midpoint of the river, river width ranged from
ca. 30 to 90 m), and buffer location was placed entirely on land from where
the bird sang. Although the 100-m radius buffer is larger than our mean territory
measurements of densely packed Cerulean Warblers, the position of
the male’s singing post in relation to the territory as a whole was unknown.
When comparing two consecutive (repeat) surveys of the same river section,
we treated birds as unique if the 100-m radius buffers representing male territories
did not overlap. In those situations where males had contiguous or
nearly contiguous territories and not all of these abutting males sang during
at least one of the repeat surveys, use of the 100-m buffer may result in underestimates
of males present. For example, if during the initial survey, we
recorded a male singing at the extremity of his territory where it interfaced
98 Southeastern Naturalist Vol. 9, No. 1
with an adjacent male’s territory, and a repeat survey failed to detect this bird
singing, but its adjacent male was singing at the interface of their territories,
then our buffer would represent them as a single male. Obviously, if both
were singing on either survey or if the males were spaced farther apart, then
the buffer would not introduce bias.
We then used resulting numbers of unique and repeated observations
of individual Cerulean Warblers to calculate expected total numbers of individuals
for each river section by employing the nonparametric estimator
developed by Chao (1984) for assessing number of classes in a population
when class equality is not assumed. Specifically, from two surveys, it is possible
to count individuals twice (both surveys) or once only (one survey or
the other); the Chao estimator uses the comparative frequencies of individuals
detected twice and individuals detected once to estimate the frequency of
individuals likely not to have been detected on either of the surveys. Given
that repeat surveys were all conducted within two days of the original count,
we treat this as a closed system, i.e., no turnover in males or territory size
was assumed to have occurred within that time span. The expected number
of individuals (Sexp) is estimated as
Sexp = Sobs + (a2/2b),
where Sobs is the total number of individuals observed in either survey, a is
the number of individuals observed in only one survey, and b is the number
observed in both surveys. A 95% confidence interval of Sexp was calculated
following Chao (1988).
We recorded an average of 2.3 and 0.8 singing Cerulean males/river km
along 128 km of the Current River in 2003 (Robbins 2003) and 96 river km of
the Buffalo National River in 2006, respectively. The upper and middle stretches
of the Buffalo lacked the extensive forested fl oodplain found in the lower
portions, and this was refl ected in the number of Cerulean Warblers. An average
of 0.3 males/river km were recorded along the middle Buffalo section (64.5
km), whereas the lower section (31.6 km) had 2.1 males/river km. Ninety-five
percent (n = 231) of the Cerulean Warblers detected were estimated (see Methods)
to be ≤100 m from the canoe-based observer . The Chao estimator allowed
estimation of the completeness of our surveys for which we conducted repeat
surveys. For example, for the Pulltite section, 22 males were detected during
both surveys, while 8 and 5 individuals were detected only during the first or
second survey, respectively. As such, for this river section, a = 13, b = 22, and
Sobs = 35, which leads to an estimate of Sexp = 38.8 ± 6.5 SD males expected
along this river section (Table 1). Hence, we estimate that a minimum of 8–9
males were missed on the first survey, and 11–12 were missed on the second
survey, and that 69–77% of males were detected on the two surveys. Calculations
for males detected on Round Spring were 76–79% (70.5–79.0, 95% CI)
and 72–74% (47.3–56.5, 95% CI) on Maumee.
2010 M.B. Robbins, Á.S. Nyári, M. Papeş, B.W. Benz, and B.R. Barber 99
The river-based protocol is appropriate for a wide range of water courses
that do not have rapid or noisy water fl ow. For the period 1966–2000, using
counts (n = 8585 total counts; 50 counts/route) of BBS routes where at least
one warbler was recorded, 75.9% had zero, 12.2% had one, and 3.3% had
≥5 individuals (Link and Sauer 2002). These results are indicative of the
relatively few Cerulean Warblers that are recorded on BBS routes. In the
physiogeographic region of our study (Ozark-Ouachita Plateau BBS region),
Cerulean Warblers are a very low-density species along road-based routes
in the Missouri and Arkansas Ozarks. During 2003–2007, this species was
recorded on only 4 of 43 routes, with an average of 0.12 birds on those four
routes (Sauer et al. 2008). In contrast, we documented previously unknown
Cerulean Warbler populations that had among the highest densities recorded
with an average of >2.0 birds/river km for some Missouri Ozark rivers (Robbins
2003, Robbins et al. 1998) and the lower Buffalo National River in
While a canoe-based approach is clearly more effective than road-side
surveys in assessing riparian-inhabiting species, how does it compare to
other survey techniques that might be employed? In effect, our river-based
protocol is a line transect, and as has been underscored by others, linetransect
methodology has advantages over point counts (Buckland et al.
2001, Diefenbach et al. 2007). In particular, we consider our river-based,
line-transect protocol better suited than riparian-based point counts because
of river-associated logistics: i.e., point counts would require additional time
associated with canoe pullout and put-in/survey point, and entire sections
of rivers can be surveyed increasing the number of observations, and hence
accuracy, and avoiding undersampling micro-habitats. An example of a
microhabitat that is not randomly distributed along Ozark streams and rivers
are stands of Arundinaria gigantea Walter Muhl. (Giant Cane). Ozark
Table 1. Chao’s estimator calculations for male Cerulean Warblers on repeat surveys of three
river sections of the Current (2003) and Buffalo (2006) rivers.
Upper Current River Buffalo River
Pulltite Round Spring Maumee
Males counted only on the first day 8 12 9
Males counted only on the repeat day 5 10 8
Males recorded on both days 22 46 28
Sobs 35 68 45
Chao Sexp 38.8 ± 6.5 73.3 ± 7.7 50.2 ± 8.9
95% CI 36.6–44.4 70.5–79.0 47.3–56.5
Males missed on first day 8.8 15.3 13.2
Males missed on repeat day 11.8 17.3 14.2
% detected on first day 77.2 79.2 73.8
% detected on repeat day 69.5 76.4 71.8
100 Southeastern Naturalist Vol. 9, No. 1
Limnothlypis swainsonii Audubon (Swainson’s Warbler) distribution is
closely associated with this habitat (Robbins and Easterla 1992). Moreover,
this protocol requires minimal effort and costs when compared to labor-intensive
protocols such as double-sampling and double-observer. With repeat
surveys using the same experienced observer and using the Chao estimator
for birds present but missed, one can eliminate among-observer bias and
assumptions concerning multiple observer independence associated with
double-observer methods (Fletcher and Hutto 2006, Nichols et al. 2000).
During our canoe-based surveys, we often detected continuously singing
males at >100 m (maximum distance was 250 m), before fl oating by the
same male at <40 m. Based on consistently singing males, our exposure to
each male ranged from 3–10 min, with estimated average exposure of <5
min. Singing rate and river topology, i.e., whether the stretch was straight vs.
highly convoluted, both affected exposure time (see below). Despite efforts
in attempting to standardize canoe fl ow rate, we undoubtedly had varying
time exposures to territorial males. Thus, one advantage of land-based point
counts over the river-based transect is consistency in sampling period.
Comparison of observed totals/subsection (simple tallies of males encountered,
without using any estimators) for all repeated surveys combined
indicated that we missed an average of 7.3% (± 6.9 SD ; range = 0–18%) of
the male Cerulean Warblers. We underscore that each one of our subsections
consisted of several river km; thus, more finely divided subsections, perhaps
1 km increments, would have revealed that some of the individuals were not
the same between the two repeat surveys. The most extreme difference between
absolute value of repeat surveys and the 100-m buffer estimate was for
one 16-km stretch of the Buffalo River where we recorded the same number
of males for each subsection (n = 3 subsections with 37 total males) for two
consecutive surveys. Based on that absolute count, one might conclude that
each male was recorded on both surveys, when, in fact, based on the 100-m
buffer estimates, we believe that a minimum of 17 males (9 uniques first
day, 8 second day) were missed during repeated surveys (Table 1). Based on
our repeat river surveys using the 100 m buffered GPS readings, the Chao
estimator suggests that a minimum of between 21 and 31% of the birds were
missed during our river surveys. For repeat BBS counts, the percentage estimates
for variability in individuals recorded for the parulid clade (n = 21
species; Cerulean Warbler was not represented because of small sample size)
was 42% (Link et al. 1994).
Regardless of survey protocol used, it is widely recognized that to
obtain better estimates of the number of birds present, detection probabilities
must be incorporated through distance sampling (Buckland 2006,
Thogmartin et al. 2006), and where aural clues are used, song availability
data must be incorporated (Confer et al. 2008, Diefenbach et al. 2007).
Although we explored density estimates with the program DISTANCE
(Buckland et al. 2001), our river-based protocol did not provide an integral
measurement: accurate horizontal, perpendicular distance estimates from
2010 M.B. Robbins, Á.S. Nyári, M. Papeş, B.W. Benz, and B.R. Barber 101
the canoe-based observer to trees where the canopy-dwelling male Cerulean
Warblers sang. Such estimates were impossible given the vegetation
structure (i.e., dbh height tree trunks from where birds sang were rarely
visible); indeed, an inordinate amount of time and effort would have been
needed to clear vegetation for obtaining accurate distance measurements
for most individuals regardless of survey methodology. Moreover, we recognize
that the fundamental assumption in distance sampling, that 100%
of the survey targets are detected at the point of the count, is consistently
violated when aural clues are used in detection. Intensive avian studies using
aural cues for detection, ranging from grassland to forest-inhabiting
species, have demonstrated that a large proportion of the population is not
available (singing) at any given point in time (Confer et al. 2008, Diefenbach
et al. 2007, Robbins et al. 2009, Staicer et al. 2006).
When aural clues are used, song availability is integral for obtaining
less-biased detection probabilities, i.e., estimating the number of individuals
that may be available during any count period (Diefenbach et al. 2007).
To obtain an estimate of the number of males that might be detectable based
solely on song availability, we monitored, during the same time frame and
location (Current River only) that the river surveys were conducted, the
singing rates of 24 male Cerulean Warblers for a minimum of four consecutive
hours, 05:00–09:00 (Robbins et al. 2009). The mean number (± SD) of
5-min periods (n = 48) over the course of 4 hrs during which male Cerulean
Warblers did not sing was 33% (± 21). Thus, availability, i.e., whether males
sang during any given period, may explain a large portion of the variability
in males detected not only among our repeat river-based counts, but in all
survey protocols where vocalizations are used for detection (Confer et al.
2008, Diefenbach et al. 2007, Robbins et al. 2009, Staicer et al. 2006).
Whether one uses the Chao estimator for repeat surveys or only song
availability estimates, the average number of Cerulean males within ca.
100 m of each side of the 128 Current River km that we surveyed was
likely >3.0 males/river km (2.8–3.1 Chao estimator, 3.1 song availability
estimate). In order to obtain less-biased detection probabilities to estimate
density, a large amount of resources and labor must be invested in obtaining
song availability data and distance measurements (the latter would require
clearing extensive understory in study areas such as ours) for each species
at the time of surveys (Diefenbach et al. 2007). In lieu of those nontrivial
investments, we recommend the following river-based protocol for obtaining
relative abundance indexes of poorly sampled avian riparian-inhabiting
species. Instead of using the laborious method of recording coordinates for
each individual during each survey to estimate the number of birds present,
we recommend subdividing each river section into 1-km increments and
surveying each section twice, preferably on consecutive days to assume that
it is a closed system. The Chao estimator can then be used to provide a better
estimate of the number of birds present.
102 Southeastern Naturalist Vol. 9, No. 1
Brad Jacobs and Victoria Grant helped with support and/or logistics. Funding was
provided by the Ozark National Scenic Riverways and the Wildlife Division of the
Missouri Department of Conservation. Paul McKenzie has provided invaluable help
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