Sampling period, size and duration inuence

measures of bat species richness from acoustic

surveys
Samuel L. Skalak
1
*, Richard E. Sherwin
2
and R. Mark Brigham
1
1
Department of Biology, University of Regina, Regina, SK, S4S 0A2 Canada;
2
Department of Biology, Chemistry and
Environmental Science, Christopher Newport University, Newport News, VA 23606, USA; and
3
Department of Biology,
University of Regina, Regina, SK, S4S 0A2 Canada
Summary
1. Understanding animal ecology depends on an ability to accurately inventory species. However,
there are few quantitative data available, which allow for an assessment of the eectiveness of
acoustic sampling methods for determining bat species richness.
2. We assessed inventory eciency, dened as the percentage of species detected per survey eort,
using data from 7 to 9 Anabat bat detectors deployed concurrently between June 2008 and August
2009 at xed locations. We examined sampling period and time of night to calculate the minimum
duration of sampling eort required to detect the greatest percentage of species.
3. In all cases, multiple survey nights at multiple sampling locations were necessary to detect higher
levels of species richness using acoustic detectors. Additionally, continuous sampling throughout
the night was important for detecting more species, especially during summer, fall and spring
months.
4. Species accumulation curves indicated that relatively few nights were needed to detect common
species at various sampling locations (25 nights on average); however, longer sample periods (>45
nights) were necessary to detect rare species at some sampling locations. Accumulation curves indi-
cated that the number of detector locations positively inuenced the number of species detected dur-
ing surveys periods.
5. A priori knowledge of sampling eort is fundamental for designing biologically robust invento-
ries. We make recommendations for improving the eciency of acoustic surveys using analytical
methods that are broadly applicable to a range of survey methods and taxa.
Key-words: acoustics, accumulation curves, bats, bat activity, inventory, species richness,
survey design, survey period
Introduction
A key component of understanding, and eectively managing
communities, is gaining a basic understanding of inherent
variation in their specic composition across space and time
(Morris 1990). A failure to understand or address normal
spatiotemporal variation in community structure can make
the most basic ecological data problematic (Boulinier et al.
1998). Knowledge about the presence or absence (or detection
vs. non-detection) of various species within a community over
time is necessary to elucidate spatial and temporal patterns of
ecosystems (Carroll, Zielinski & Noss 1999), especially when
using survey data collected at the same sites over extensive
sample periods (MacKenzie et al. 2002). Understanding nor-
mal levels of variation in species richness is fundamental for
conservation eorts because managers must decide whether
changes in species richness across space and time warrant con-
servation eorts. There are many spatial scales at which species
richness can be assessed, including the landscape scale where
anthropogenic change (e.g. fragmentation or restoration) is
often considered in study design (Krohne 1997; Turner 2005).
The development of passive sampling technologies to record
the acoustic calls of free-ying bats and potentially permit
species identication (OFarrell & Gannon 1999; Ochoa,
OFarrell &Miller 2000; Gannonet al. 2004) has spurredmany
*Correspondence author. E-mail: samuel_skalak@fws.gov
Ash Meadows National Wildlife Refuge, HCR-70, Box-610-Z,
Amargosa Valley, NV 89020, USA.
Correspondence site: http://www.respond2articles.com/MEE/
Methods in Ecology and Evolution 2012, 3, 490502 doi: 10.1111/j.2041-210X.2011.00177.x
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society
surveys for bats. Giventhat most insectivorous bats use echolo-
cation to detect prey and orient, acoustic detectors provide a
useful tool for measuring species richness within and across
large geographical areas and habitat types. Prior to the advent
of inexpensive acoustic detectors, our understanding of bat
species richness came fromdatageneratedby captures (i.e. harp
traps andmist nets) or visual observations (i.e. roost surveys).
Acoustic detectors are portable devices that passively record
sound frequency parameters and call patterns (duration, inten-
sity, etc.) such that individual echolocation events may be iden-
tied to the guild or species at a later time (OFarrell &
Gannon 1999; Gannon et al. 2004). Acoustic surveys typically
detect more species than active capture devices (Kalko,
Handley & Handley 1996; Murray et al. 1999; OFarrell &
Gannon 1999; Ochoa, OFarrell & Miller 2000). When com-
pared with nets and traps, acoustic detectors are: (i) a non-
invasive means of assessing activity by detecting individuals
over a greater area, (ii) not limited to surveying local resources
such as water bodies or open yways that may be necessary
when using capture devices, (iii) able to sample continuously
and (iv) operational regardless of weather and environmental
conditions.
Data from the acoustic detection of bats have been used to
document activity patterns (Hayes 1997; Tibbels & Kurta
2003), resource use (Vaughan, Jones & Harris 1997; Williams,
OFarrell & Riddle 2006; Zukal & Rehak 2006), species rich-
ness (Wickramasinghe et al. 2003) and species distribution
(Jaberg & Guisan 2001). However, explicit evaluations of the
survey eort necessary to acoustically detect dierent species
are generally lacking (Hayes 1997; Milne et al. 2004). Greater
a priori knowledge about spatial and temporal variation in spe-
cies detection rates should improve the design of future studies.
Acoustic survey eort inuences the likelihood that various
species are detected during survey events (Gorresen et al. 2008;
Weller 2008). By not accounting for spatiotemporal variation
in bat activity, researchers may fail to detect certain species at
dierent locations (Moreno & Halter 2000; Broders 2003;
Milne et al. 2005) because it is dicult to predict the time
needed to acoustically detect inconspicuous species. Typically,
multiple surveys and methods are required to detect all species
in an area (Krebs 1989; Hayes 1997; Moreno &Halter 2001),
and yet wildlife managers may be constrained by limited
resources. While ecological attributes of bat communities (i.e.
diversity and richness) typically vary across spatiotemporal
scales, basic elements of general study design (i.e. survey inten-
sity, duration and detector orientation) are applicable across
locations and communities (Duchamp et al. 2006). To design
studies intending to assess species richness, it is necessary to be
familiar with the spatiotemporal variation inherent in bat
assemblages so that variation in community structure across
space and through time can be assessed (Sherwin, Gannon &
Haymond 2000; Gannon &Sherwin 2004). For example, ques-
tions regarding seasonal variation in community structure or
non-random distribution of species across the landscape of
interest likely require dierent sampling strategies.
While understanding inherent spatiotemporal variation in
community structure has proven critical in understanding
long-termecological attributes of wildlife communities (Morris
1990), there has been little formal evaluation of this variation
in species richness of bat communities using acoustic detectors.
To date, there have been no studies that have investigated
nightly patterns of species richness of bat communities using
long-term (>1 year) continuous acoustic survey data concur-
rently collected at multiple permanent sampling locations. Our
objective was to assess the sampling eort required to detect
xed levels of bat species acoustically. Our broad expectation
was that increased sampling would yield more precise estimates
of richness, and that there would be dierences across nights
and detector sites during dierent seasons. We further expected
that given the extensive nature of our data set, richness esti-
mates would plateau at each site. Our second objective was to
then develop specic recommendations for the design of acous-
tic monitoring studies intended to assess species richness.
Materials and methods
STUDY SI TE
Our study was conducted at Ash Meadows National Wildlife Refuge
in southern Nevada (36 25 N, 116 19 W), a 95-km
2
region of the
Mojave Desert managed by the U.S. Fish and Wildlife Service. The
location receives roughly 70 mm annual rainfall; however, it is a
major discharge point for two underground aquifer systems. The area
is one of the fewplaces in the Mojave Desert with reliable year-round
surface water and supports the highest concentration of endemic spe-
cies in the United States per unit land area (Stevens & Bailowitz
2008). The Refuge is located between limestone mountains to the east
and west and is characterised by a variety of dierent habitats.
Approximately half of the total land area in the study area is com-
posed of alkali shrub scrub and creosote shrub land. Alkali mead-
ows, wet meadows, invasive weed patches and riparian woodlands
comprise roughly 25% of the total land area. The remainder of the
Refuge is a mixture of vegetation types including mesquite bosque,
alkali playas, seasonally ooded woodlands, dunes, open water and
mixed Mojave scrub habitats.
Locations of Anabat detectors were chosen using a randomised
block design that considered habitat types and current and historical
restoration eorts. Each detector was deployed in a dierent habitat
and or vegetative structure. However, while habitat dierences likely
contributed to the variability in species richness across sampling loca-
tions, we did not assess habitat use by bats. Each detector was located
between 2 and 6 km from other detectors, and the location of each
detector was maintained (permanently) throughout the study. Seven
detectors were deployed in June of 2008, and an additional two detec-
tors were added the following February and June of 2009.
ECHOLOCATI ON RECORDI NG
We used frequency-division systems (i.e. Anabat II detectors; Titley
Electronics, Balina, NSW, Australia) because they are best suited to
record echolocation calls passively at remote sampling locations for
extended periods of time (Corben 2000; Limpens & McCracken
2004). We collected data between June 2008 and August 2009. Each
detector systemwas powered by a 12-Vbattery connected to a 5-watt
solar panel and mounted on a pole 2530 m above the ground.
Polyvinyl chloride (PVC) hoods protected microphones from the
elements, and a 15 15 cm acrylic glass plate mounted below each
Eective acoustic monitoring 491
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
microphone reected sound upwards into the microphone. The fre-
quency-division setting was set to eight to provide the greatest call res-
olution (Corben 2000), and sensitivity levels were set to about 65 on
all detectors to minimise background noise (i.e. wind, insects) while
enabling the detection of most echolocation calls. Detectors were pro-
grammed to switch on automatically 90 min before sunset, and o
90 min after sunrise each day. Detectors remained switched oduring
day-time hours to recharge batteries. Data were saved internally to
compact ash cards and later transferred to a computer.
Detector malfunction was prevalent during some periods (speci-
cally spring); therefore, we only used data for any given unit when
>20 nights per season were recorded. We made no attempt to com-
pare detection rates among detectors.
ECHOLOCATI ON ANALYSI S
Recordings were analysed to identify species using Analook software
version 37f (Titley Electronics, Balina, NSW, Australia). We used a
reference library of >8000 echolocation calls from various species
captured and recorded in the western U.S. (many within 500 km of
the study area) and made the assumption that the identication of
calls in the library was accurate. Twenty-one of Nevadas 23 species
of bat are reported to occur in the southern part of the state (Bradley
et al. 2006).
Fragmentary call sequences consisting of 2 discernable call notes
from an individual (OFarrell & Gannon 1999) were classied as
unknown because of high levels of inter- and intraspecic call varia-
tion. Acall was dened as one note in a sequence of call notes, and a
call le as a sequence of call notes from one or more individuals dur-
ing a single recorded sequence (Corben & OFarrell 1999). Single call
les could contain multiple call notes from multiple individuals. To
account for multiple species recorded within single les, each call le
was independently viewed to ensure that all detected species were
recognised and identied.
Calls were identied qualitatively following the methods of
OFarrell, Miller & Gannon (1999) and Milne et al. (2002). All calls
were identied by SLS to prevent interobserver bias. Calls that could
only be identied to the level of bat because of the fragmentary nat-
ure of the call were classied as unknown. Identication accuracy
was vetted using discriminant function analysis (Parsons & Jones
2000; Russo &Jones 2002; Fukia, Agetsuma &Hill 2004) and tests of
interobserver agreement. Tests of interobserver agreement were
conducted by sending batches of randomly selected les to a third
party for identication. Pearsons r was used to ascertain whether dif-
ferent analyses (discriminant function analysis, third part individuals
and SLS) produced statistically similar results.
Subsamples of identied call les were randomly chosen (including
unknowns) and checked for species identication accuracy and
consistency across nights. Subsample sizes were chosen using power
analysis, and resulting call-le batches were selected randomly. By
selecting subsample sizes using the total number of les identied for
each species, we assumed that species classications were fairly accu-
rate. For tests of interobserver agreement, information about species,
date, and time information were extracted from each subsample call
le and then removed so that call les contained no information
about initial identications. Neither observer had any prior knowl-
edge about the numbers or kinds of species contained in the selected
les, and analyses were performed independently.
Discriminant function analysis was conducted using systat 11 for
Windows (Systat Software Inc., Chicago IL, USA). Nine parameters
were extracted fromreference calls automatically using Analook soft-
ware: minimum frequency (F
min
), maximum frequency (F
max
), char-
acteristic frequency (F
c
), the frequency of the knee or inection
point of each call (F
k
), the duration in time of each call (Dur), the time
from the start of the call to F
c
(T
c
), the time from the start of the call
to F
k
(T
k
) and the slope of the call at the F
c
(S
c
) (for denitions, see:
Corben & OFarrell 1999; Corben 2000; Milne 2002). We chose these
parameters because they are representative of call structures across
species. Species were set as the grouping variable, and call parameters
were used as the predictive variables. All groups were weighted
evenly.
Our verication tests indicated a high level of agreement in the total
number of species detected, total number of echolocation call les
detected, and the numbers of species detected among and across
nights for most species. Identication accuracy and consistency was
>90%for most species. There were minor issues identifying between
Eptesicus fuscus and Lasionycteris noctivigans and discerning Lasiurus
blossevilli from Parastellus hesperus. Both issues are not surprising,
however, as these species pairs have calls that are similar in frequency,
structure and pattern. Despite issues parsing between these species,
identication accuracy remained >75%.
ANALYSI S OF VARI ABI LI TY I N SPECI ES RI CHNESS
For simplicity, we used 3-month blocks of the annual 12-month cal-
endar to dene the four seasons in temperate North America: spring
(MarchMay), summer (JuneAugust), fall (SeptemberNovember)
and winter (DecemberFebruary). We treat seasons independently
with the exception of summers 2008 and 2009, where data were
combined for some analyses. Because detector malfunction occurred
during some periods (specically spring), we only used data where
20 nights per season were recorded by individual detectors in tests
that required longer sample periods (i.e. species accumulation curves).
Some detectors came online later in the study, and malfunctions elim-
inated usable data from some detectors during some seasons. There-
fore, our results do not represent comparisons between seasons.
Species richness was assumed to be zero at the start of each season.
ANALYSI S OF SPECI ES DETECTI ON PATTERNS
To measure bat activity, we quantied the number of echolocation
events recorded over specic time periods. We found it dicult to dis-
cern detection patterns using le size (e.g. bytes: Broders 2003) or
counts of the number of les recorded (Kalcounis et al. 1999) because
multiple species were frequently encountered within individual les at
some sampling locations. Therefore, we used the activity index (AI;
Miller 2001) to calculate the magnitude of species presence across
individual time blocks. Modied to include sampling eort, AI is
dened as:
AI
X
n
e
P
The AI is calculated by summing the number (n) of time blocks for
which a species was present (P*) and dividing by sampling eort
(e: time period over which the data were collected).
AI allows for comparison of the relative time contribution of each
species compared with other species detected. For example, a species
was recorded present during the time blocks; it was detected regard-
less of the number of call notes (2) or sequences present in the given
le. As the AI is applicable regardless of the number of individuals,
species or call notes in a recorded le, it reduces the inuence of an
individual repeatedly circling within the range of the detector micro-
phone. By plotting the amount of time that dierent species were
detected during hour time blocks across detectors, we plotted
492 S. L. Skalak, R. E. Sherwin & R. M. Brigham
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
species-specic patterns of activity by time of night. This allowed us
to assess whether sampling all night inuenced species richness
measures. Sunset and sunrise data were gathered using Moonrise
software version 35 (Sidell 2002; Moonrise, Grande Rapids, MN,
USA).
We used the program presence (Proteus Research & Consulting
Ltd., Dunedin, New Zealand) to test whether all-night sampling was
eective for detecting previously undetected (i.e. unique) species dur-
ing nightly sampling events. presence is frequently employed to
produce occupancy models fromdata on detection vs. non-detection,
where detection probabilities are <1 (MacKenzie et al. 2002). Detec-
tion probabilities were weighted according to temporal distributions
of detections. For example, a species detected only on the rst ve
and last ve nights of a 100-night survey would have a lower detection
probability than a species detected every 10th night because the latter
detection rate is more consistent. Missing observations (i.e. detector
malfunction) provided no data about detection vs. non-detection and
were therefore not used in the analysis.
Estimates of species occupancy were calculated for hour time
blocks during each night beginning at sunset. Occupancy estimates
were a function of the probability that an individual species was
detected present during each time block at each detector location,
and the probability that each species had previously been detected at
each site. Final estimates for each time block were averaged across
species and detector locations for each season. The analysis assumed
that species richness at the start of the sampling night was zero and
that detections at each site were independent of other sites.
ANALYSI S OF SAMPLI NG PERI OD AND SI ZE
We evaluated sampling ecacy and completeness across time and
among detectors using species accumulation curves (Moreno &
Halter 2000). Species accumulation curves are a class of linear
dependence models, which assume the number of new species
detected will decrease with increasing sampling eort, and are useful
in situations where an assessment of the amount of eort necessary
to detect X% of species is the objective (Sobero n & Llorente 1993).
Curves were calculated using ecosim ver. 7.72 (Gotelli & Entsminger
2001). Numbers of nights (n nights) and number of detectors
(n detectors) were used as measures of sampling eort, which made
it possible to predict the likelihood that greater species would be
detected through time based on sampling eort. Accumulation
curves reached an asymptote when the probability of detecting a
new species approaches zero.
Sample nights were repeatedly randomly reordered 1000 times by
Ecosimto produce smoothed curves. Reaching 100%species richness
within models is unlikely because of the chance that some species
remain undetected during the survey period. Therefore, the propor-
tion of species detected during simulated sampling periods is typically
used to assess sampling completeness. We selected 80% and 90% of
total species richness detected during each season as conservative
levels of survey completeness to allow for comparison of species rich-
ness within and among locations (Moreno & Halter 2000; Shiu &
Lee 2003). Per cent species richness values were derived from Ecosim
calculations. We then used the species accumulation curves to calcu-
late the mean number of nights needed to attain these values follow-
ing Lamas, Robbins & Harvey (1991) as reviewed by Sobero n &
Llorente (1993) and applied by Moreno &Halter (2000).
Results
We analysed patterns of species richness based on data col-
lected by 79 detectors on 2645 total sample nights between
June 2008 and August 2009. We recorded data during 437
detector nights (seven detectors) during the summer of 2008,
637 detector nights (seven detectors) during fall, 610 nights
(eight detectors) during winter, 337 nights (9) detectors during
spring and 624 nights (nine detectors) during the summer of
2009. We identied 12 dierent species froma potential 14 spe-
cies that are presumed to occur at our study site (unpublished
data; U.S. Fish and Wildlife Service survey records on-le at
Ash Meadows National Wildlife Refuge) and recorded
353 371 individual call les (Table 1). For 186%of the echolo-
cation events, we classied the species as unknown. A review
of the unknowns by an independent observer and discriminant
function analysis suggested that the majority (85%) were the
most commonly detected species: Myotis californicus, Myotis
yumanensis and Parastrellus hesperus. However, unknowns
Table 1. Summary of identied echolocation events by season
Summer 08 Fall 08 Winter 0809 Spring 09 Summer 09
Total Sp.
Detections
Antrozous pallidus 274 33 1 442 562 1312
Corynorinus townsendii 522 195 15 175 180 1087
Eptesicus fuscus 3 2 3 4 12
Lasiurus blossevilli 181 62 5 21 269
Lasiurus cinereus 5 16 70 3 94
Lasionycteris noctivigans 9 51 12 3 75
Lasiurus xanthinus 4057 704 152 2188 7101
Myotis californicus 21625 7421 890 8545 22632 61113
Myotis ciliolabrum 3 12 3 18
Myotis yumanensis 5033 1838 71 604 2634 10180
Parastrellus hesperus 63865 11593 155 11839 105868 193320
Tadarida brasiliensis 1015 895 1 6870 4225 13006
Unknown 23505 10071 348 6819 24996 65739
Grand Total 120098 32934 1480 35542 163316 353371
No. Species 12 12 5 12 11 12
Summer 2008 (n nights = 437, n detectors = 7), fall (n nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7), spring
(n nights = 293, n detectors = 6) and summer 2009 (n nights = 624, n detectors = 9).
Eective acoustic monitoring 493
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
were too indistinct to condently identify, and we left them as
undiagnosed for our analysis.
ANALYSI S OF SPECI ES DETECTI ON PATTERNS
The mean SD number of species detected per night across
each detector was highest during the summer of 2008
(36 18) and 2009 (30 16), and lowest in winter
(03 06; Fig. 1). The number of species detected per night
across detectors during fall and spring averaged 26 20 and
28 21, respectively. Several species were detected at all
detectors within and across seasons, but some species were
only recorded at some detectors within and across seasons
(Table 2). Additionally, the percentage of survey nights that
various species were detected varied (Table 3).
We found a range of 512 species recorded across individual
detectors during summers 2008 and 2009, 412 species in fall,
05 in winter and 211 in spring. On average, four species were
detectedevery05 hper detector during summer, fall andspring
between sunset and sunrise (Fig. 2). During winter, <1 species
was detectedevery05 h. Species were more or less active during
dierent parts of the night (Figs 36). More species were
detected earlier in the evening during fall and spring compared
with summer. Some species exhibited crepuscular patterns of
detection (e.g. P. hesperus), whereas some species exhibited
more nocturnal patterns of detection (e.g. T. brasiliensis). The
probability of detecting previously undetected species during
the current night varied with time of night (Fig. 7), but was
highest inthe rst 2 hafter sunset inall seasons.
ANALYSI S OF SAMPLI NG PERI OD AND SI ZE
Species accumulation curves approached an asymptote at dif-
ferent rates within and among seasons (Fig. 8). The number of
nights needed to detect 80 and 90% of the possible species at
each detector varied with season (Fig. 9). It took a
mean SDof 225 179 nights to detect 80%of the known
species during summer, 155 74 nights in fall, 206 99 in
winter and 97 53 in spring. To detect 90% of species at
each detector in summer, 464 292 sampling nights were
needed, 300 151 nights in fall, 308 154 in winter and
212 96 in spring.
The probability of detecting species increased with an
increasing number of detectors (Fig. 10). The number of detec-
tors necessary to detect 80% and 90% of species varied with
season (Fig. 11). Detecting 80% required a mean SD of
3 31 detectors in summer, 4 58 in fall, 5 16 in winter
and 5 38 in spring. To detect 90%, it took a mean
of 6 13 detectors in summer, 75 35 in fall, 7 19 in
winter and 8 18 in spring.
Discussion
The objective of many acoustic bat surveys is to determine
which species occur in an area (Walsh, Barclay & McCracken
2004). Such surveys often strive to assess the relative
Fig. 1. Box-and-whisker plot showing mean (bold), median and 25th
and 75th percentiles of the number of species detected per night from
June 2008August 2009. Vertical lines represent range from1090%.
Data are cumulative averages of data from detectors that operated
largely continuously between June 2008 and August 2009 (detectors
17, n nights = 2395).
Table 2. Per cent of detector locations various species were detected at by season
Summer
08 (%)
Fall
08 (%)
Winter
0809 (%)
Spring
09 (%)
Summer
09 (%)
Antrozous pallidus 1000 714 143 778 1000
Corynorinus townsendii 571 429 143 444 667
Eptesicus fuscus 286 143 00 111 222
Lasiurus blossevilli 571 429 00 111 444
Lasiurus cinereus 429 143 00 444 333
Lasionycteris noctivigans 286 143 00 222 333
Lasiurus xanthinus 429 286 00 333 333
Myotis californicus 1000 1000 286 889 1000
Myotis ciliolabrum 143 143 00 111 00
Myotis yumanensis 1000 1000 286 556 1000
Parastrellus hesperus 1000 1000 714 889 1000
Tadarida brasiliensis 857 1000 143 778 1000
Summer 2008 (n nights = 437, n detectors = 7), fall (n nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7), spring
(n nights = 293, n detectors = 6) and summer 2009 (n nights = 624, n detectors = 9).
494 S. L. Skalak, R. E. Sherwin & R. M. Brigham
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
importance of various habitat types based on the known distri-
bution of species within the landscape (Sherwin, Gannon &
Haymond 2000; Miller, Arnett &Lacki 2003). Despite the use-
fulness of acoustic detector data for monitoring bat communi-
ties, there is growing recognition that much of the data that
result fromacoustic surveys do not adequately account for var-
iation in species activity across space and time (Hayes 1997,
2000; Gannon, Sherwin & Haymond 2003 & Miller, Arnett &
Lacki 2003; OShea, Bogan & Ellison 2003; Milne et al. 2005;
Fischer et al. 2009). An a priori understanding of the survey
eort necessary will help to ensure statistically powerful
sampling designs, clearer data interpretation and likely more
successful management and conservation actions.
WHEN SHOULD SURVEYS BE CONDUCTED?
The duration of sampling within nights varies across studies
(Gannon, Sherwin & Haymond 2003). For example, some
authors sample continuously from dusk until dawn (e.g.
Kuenzi & Morrison 1998; Williams, OFarrell & Riddle 2006;
Dzal et al. 2009), while others sample for only parts of the
night (e.g. Wickramasinghe et al. 2003; Gehrt & Chelsvig
2004; Ford et al. 2005; Flaquer, Torre & Arrizabalaga 2007).
A principal objective of all of these studies was to quantify
species richness. Varying approaches to answering similar
questions can lead to confusion about which method is best,
diering interpretations fromthe data and can make it dicult
to directly compare studies. We found that the probability of
detecting a new species during a sample night generally
declined 34 h after sunset after which most acoustically com-
mon species had been detected. However, bat detections did
not appear to decrease linearly with time of night, and during
summer and spring exhibited a bimodal peak where detection
probability increased slightly in the 34 h before sunrise. This
suggests that sampling all night is important to record less
frequently detected species. In all but the winter, some acousti-
cally rare species were only detected late at night or in the early
morning. These species may not have been detected had sur-
veys not lasted the entire night.
HOW MANY SURVEYS WERE NEEDED TO DETECT X%
OF POSSI BLE SPECI ES?
We found that 25 survey nights were necessary to detect the
57 species (between 40%and 60%of the possible species rich-
ness) that were commonly recorded at most detectors during
spring, summer and fall. Many more nights of sampling were
required to yield increased richness estimates beyond this level.
For example, in summer, it took on average >20 nights to
detect 80% of possible species and >45 nights to detect 90%
of possible species at some detectors. In spring, the number of
nights needed to detect 80%and 90%of species was about half
of that for summer. This may be due in part to seasonal vari-
ability in species richness among detector locations, and possi-
bly lower detection probabilities of acoustically rare species in
Table 3. Per cent of survey nights that species were detected by season
Summer
08 (%)
Fall
08 (%)
Winter
0809 (%)
Spring
09 (%)
Summer
09 (%)
Antrozous pallidus 248 24 02 184 227
Corynorinus townsendii 178 83 12 125 114
Eptesicus fuscus 07 02 00 031 05
Lasiurus blossevilli 131 43 00 06 10
Lasiurus cinereus 09 13 00 42 03
Lasionycteris noctivigans 13 24 00 12 03
Lasiurus xanthinus 115 74 00 36 64
Myotis californicus 696 454 38 427 800
Myotis ciliolabrum 02 16 00 06 00
Myotis yumanensis 528 265 23 249 460
Parastrellus hesperus 841 567 72 413 965
Tadarida brasiliensis 217 220 02 306 254
Summer 2008 (n nights = 437, n detectors = 7), fall (n nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7), spring
(n nights = 293, n detectors = 6) and summer 2009 (n nights = 624, n detectors = 9).
Fig. 2. Mean species richness in relation to time after sunset during
summer (solid circles), fall (open circles), winter (solid triangles) and
spring (open triangles). Summers (2008: n nights = 437, n detec-
tors = 7; 2009: n nights = 624, n detectors = 9), fall (n
nights = 637, n detectors = 7), winter (n nights = 606, n detec-
tors = 7) and spring (n nights = 293, n detectors = 6) months from
June 2008 to August 2009.
Eective acoustic monitoring 495
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
summer (i.e. migratory species like Lasiurus cinereus) vs. other
seasons.
Longer survey periods will produce more precise survey
results (Krebs 1989). Samplingshouldoccur for as longas possi-
ble, especially giventhat the cost does not increase substantially
when using passively operated detectors. However, extensive
long-termdatasets are more costlyinterms of analysis.
HOW MANY SAMPLI NG LOCATI ONS WERE NECESSARY
TO DETECT THE MOST SPECI ES?
Studies that have measured bat activity at multiple sites often
report variation in species richness among detector locations
(e.g. Milne et al. 2005; Williams, OFarrell &Riddle 2006; Cie-
chanowski et al. 2007). Providing recommendations about the
number of detectors needed to detect the most species for study
areas other than our own is dicult because there are environ-
mental, technological, nancial and logistical factors that inu-
ence study objectives and the applicability of ndings (Miller,
Arnett &Lacki 2003). However, our general recommendations
are broadly applicable to all geographical regions. We found
that the probability of detecting more species increased with
the number of detectors used. While there exists the statistical
possibility of detecting all species using as few as one detector
during the summer and fall seasons, and two detectors during
the winter and spring seasons, we calculated there was a low
probability of this actually occurring. Most importantly, a lim-
ited number of detectors make it dicult to assess spatial varia-
tion in species richness, which precludes extrapolation to
broader spatial scales.
We found a range of 612 and a mean SD of 89 23
species recorded at each detector location over a relatively long
(>12 months) period of survey eort. In instances where the
number of detectors for use is not limited, our data suggest that
sampling 6 locations for approximately 30 nights each should
detect most acoustically detectable species in a relatively small
landscape similar to ours. Additionally, because we found that
the detection of acoustically rare species varied both tempo-
rally and spatially, we recommend that researchers rst assess
local variation via concurrent acoustic sampling and then
modify the sampling design to best reect local community
dynamics.
CONCLUSI ONS AND RECOMMENDATI ONS FOR FUTURE
RESEARCH
Many of the species we detected are broadly distributed
throughout the south-western United States and northern
Fig. 3. Species-specic activity patterns relative to sunset during summer. Data are cumulative from all detectors during summer (2008: n
nights = 437, n detectors = 7; 2009: n nights = 624, n detectors = 9). Figures 36 are arranged by activity levels, with the most active species
in the top left and least active species in the bottomright. Values are multiplied by a factor of 100 to convert smaller values to whole numbers. We
note, however, that for rarely detected species, these gures may be biased reections of the actual activity patterns.
496 S. L. Skalak, R. E. Sherwin & R. M. Brigham
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
Mexico. Despite their broad distributions, many of these spe-
cies are considered to be at risk in all, or portions of their range.
We focused on acoustic bat detectors as their use has increased
exponentially (Hayes 2000; Fenton 2003; Gannon, Sherwin &
Haymond 2003; Miller, Arnett & Lacki 2003). Understanding
patterns of activity by various species may help future survey
eorts, especially for rare or threatened species. However,
given the diversity of bats, thorough surveys will require
Fig. 4. Species-specic activity patterns relative to sunset during fall. Data are cumulative from all fall detectors (n detectors = 7; n detector
nights = 637).
Fig. 5. Species-specic activity patterns relative to sunset during winter. Data are cumulative from all detectors in winter (n detectors = 8; n
detector nights = 610).
Eective acoustic monitoring 497
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
Fig. 6. Species-specic activity patterns relative to sunset during spring. Data are cumulative fromall spring detectors (n detectors = 9; n detec-
tor nights = 337).
(a) (b)
(c) (d)
Fig. 7. Probability of detecting a previously undetected species (within a single sampling night) by time of night. Values (lled circles) are cumula-
tive from detectors that operated during summers (2008: n nights = 437, n detectors = 7; 2009: n nights = 624, n detectors = 9), fall
(n nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7) and spring (n nights = 293, n detectors = 6).
498 S. L. Skalak, R. E. Sherwin & R. M. Brigham
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
multiple sampling techniques. For example, we only detected
12 species out of a projected 14 (Myotis thysanodes and Eum-
ops perotis californicus have been documented on Refuge lands
previously), and only 12 species out of a potential 21 species
known to occur in southern Nevada (Bradley et al. 2006).
While our levels of species richness may reect our sampling
methodology, for example the sensitivity of Anabat detectors
(Larson & Hayes 2000), they clearly show that even long-term
acoustic data sets can be inconclusive for some species.
Our results support our original predictions that greater
sampling eort would yield more accurate species richness esti-
mates. On average, 2030 sampling nights were needed to
detect 8090% of the species that occurred at each sampling
location, and dierent species were detected with dierent
Fig. 8. Species accumulation curves by season. Symbols and lines represent dierent detector locations.
(a) (b)
Fig. 9. Mean (dot) number of sample nights for all detectors required to detect 80% and 90% of the bat species detected during each season.
Vertical lines represent 95% condence intervals. Values (lled circles) are cumulative from detectors that operated during summers (2008:
n nights = 437, n detectors = 7; 2009: n nights = 624, n detectors = 9), fall (n nights = 637, n detectors = 7), winter (n nights = 606,
n detectors = 7) and spring (n nights = 293, n detectors = 6).
Eective acoustic monitoring 499
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
frequencies across locations. Additionally, species richness var-
ied at dierent sampling locations as did the rate at which spe-
cies were detected. If only one detector is available, our
analyses suggest that moving the detector between locations
for 25 nights at each location would eectively detect the
acoustically common species at our study site. This method is
likely the best option where an inventory needs to be done
quickly, and a general species list from across the landscape is
the main objective. However, when a comparison of commu-
nity structure, species richness, habitat associations and activ-
ity patterns among species is the focus of the study, longer
periods of sampling eort with larger numbers of detectors will
be required. Overall, we recommend sampling at 6 dierent
locations for approximately 30 nights per location to detect less
common species (Table 4), but acknowledge that our results
may have diered slightly had we access to more detectors or
sampled in a dierent geographic location.
Our results lead to the following three cautionary sugges-
tions about sampling design for future acoustic monitoring
studies: (i) sample continuously throughout the night (dusk
dawn); (ii) sampling for repeated numbers of nights at the same
locations increases chances of detecting acoustically rare spe-
cies and developing more accurate estimates of species richness
and (iii) sampling at multiple locations may not (statistically)
be necessary to detect the acoustically common species, but will
increase the rate at which species are detected and are necessary
for robust comparisons of species richness between sampling
locations.
(a) (b)
(c) (d)
Fig. 10. Accumulation curves with 95%condence intervals showing the number of bat species detected during each season as a function of the
number of detectors units sampling continuously. Smoothed curves were produced by randomly reordering data 1000 times. Data are cumulative
from detectors that operated during summers (2008: n nights = 437, n detectors = 7; 2009: n nights = 624, n detectors = 9), fall (n
nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7) and spring (n nights = 293, n detectors = 6).
(a) (b)
Fig. 11. Number of detectors calculated to detect 80%and 90%of the acoustically detected species richness within the study area across seasons.
Bars represent variance. Data are from detectors that operated during summers (2008: n nights = 437, n detectors = 7; 2009: n nights = 624,
n detectors = 9), fall (n nights = 637, n detectors = 7), winter (n nights = 606, n detectors = 7) and spring (n nights = 293, n detectors = 6).
500 S. L. Skalak, R. E. Sherwin & R. M. Brigham
2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502
Acknowledgements
This study would not have been possible without the help, guidance and sup-
port of many individuals. We thank C. Baldino & S. McKelvey and the sta at
Ash Meadows National Wildlife Refuge for making this study possible. S.L.S.
would like to thank K. Taylor for valuable help with data management, M.J.
OFarrell for help with species identication, R. Fisher for statistical assistance
and C. Somers and R. Poulin for valuable comments that helped guide the
direction of this analysis. This research was funded through a research grant to
CNU from the U.S. Fish & Wildlife Service, facilitated through Biowest, Inc.
R.E.S. wishes to thank D. Olsen of Biowest for his support and assistance with
administration of the grant throughout the project. M.B. Fenton and three
anonymous reviewers provided comments that improved an earlier draft of the
manuscript.
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Season
Minimum Sample Period Found
Survey period
n nights n locations
80% S 90% S 80% S 90% S
Summer SunsetSunrise 22 46 3 6
Fall SunsetSunrise 16 30 4 8
Winter Sunset + 5 h after 21 31 5 7
Spring SunsetSunrise 10 21 5 8
Average 17 32 4 7
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Received 25 July 2011; accepted 11 November 2011
Handling Editor: Robert Freckleton
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2012 The Authors. Methods in Ecology and Evolution 2012 British Ecological Society, Methods in Ecology and Evolution, 3, 490502