Content uploaded by Renata Santoro Sousa-Lima
Author content
All content in this area was uploaded by Renata Santoro Sousa-Lima on Apr 02, 2018
Content may be subject to copyright.
Notes
MARINE MAMMAL SCIENCE, **(*): ***–*** (*** 2017)
©2017 Society for Marine Mammalogy
DOI: 10.1111/mms.12382
Upcall production by southern right whale (Eubalaena australis)
mother-calf pairs may be independent of diel period in a nursery area
JULIA R. G. DOMBROSKI,
1
Laboratory of Bioacoustics, Biosciences Center, Federal University
of Rio Grande do Norte, Natal 59078-970, Rio Grande do Norte, C.P.1511, Brazil; SUSAN
E. PARKS,Department of Biology, Syracuse University, 107 College Place, Syracuse, New
York 13244, U.S.A; KARINA R. GROCH,Projeto Baleia Franca, Av. Atl^antica, Imbituba
88780-000, Santa Catarina, C.P.201, Brazil; PAULO A. C. FLORES,Centro Mamıferos
Aquaticos, Instituto Chico Mendes para Conservac
ß
~ao da Biodiversidade, Rod. Maurıcio Sir-
osky Sobrinho, km 02, Florianopolis 88.053-700, Santa Catarina, Brazil; RENATA S. SOUSA-
LIMA,Laboratory of Bioacoustics, Biosciences Center, Federal University of Rio Grande do
Norte, Natal 59078-970, Rio Grande do Norte, C.P.1511, Brazil and Bioacoustics Research
Program, Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca,
New York 14850, U.S.A.
Finding patterns in signal production may provide important insights into differ-
ent aspects of a species’ behavior (Bradbury and Vehrencamp 1998). For instance,
temporal patterns in vocal behavior of baleen whales have been reported for some
populations (e.g., humpback whales (Megaptera novaeangliae) off Maui in Au et al.
2000; minke whales (Balaenoptera acutorostrata) from the Stellwagen Bank National
Marine Sanctuary in Risch et al. 2013; and North Atlantic right whales (NARW,
Eubalaena glacialis) off the Scotian Shelf in Mellinger et al. 2007) and have provided
important clues to determine the factors influencing the evolution of communicative
behavior of whale species.
Right whales (RW, Eubalaena spp.) are known for using low-frequency vocaliza-
tions (usually under 1,000 Hz) for communication (Clark 1983, Parks and Tyack
2005). Within the collection of vocal sounds produced by RW, there is a stereotyped
upsweep, the upcall, thought to be used as contact signal (Clark 1983, Parks and
Tyack 2005). Due to its potential function as a “contact call” and because it is pro-
duced by both females and males of all age classes, upcalls are frequently used as a
detection target in passive acoustic monitoring studies (Van Parijs et al. 2009).
1
Corresponding author (e-mail: dombroski.julia@gmail.com).
1
Upcall monitoring efforts have been useful to estimate population size (Marques et al.
2011), address changes in abundance (Morano et al. 2012), and determine diel and
seasonal patterns of occurrence of right whales (Mussoline et al. 2012). Temporal pat-
terns of upcall emission have been described for different RW populations and species
(Mellinger et al. 2007, Munger et al. 2008, Morano et al. 2012, Mussoline et al.
2012, Soldevilla et al. 2014, Bort et al. 2015). However, to our knowledge, this is
the first information about the temporal pattern of calling behavior from the southern
right whale (SRW, Eubalaena australis) groups off Brazil.
From July to November, part of a population of SRW concentrates in the southern
part of Brazil, mainly off the state of Santa Catarina (Groch et al. 2005), where this
study was conducted. This wintering area provides exceptional conditions for the
study of the behavior and communication of mother-calf pairs, particularly in the last
2 mo of the “whale season.” Land-based visual surveys conducted between 2002 and
2008 in the area indicate that 95% and 99% of the overall sightings in October and
November respectively, are of mother-calf pairs (Seyboth et al. 2015). Additionally,
aerial surveys conducted in October and November from 2002 to 2015, using the
same methodology as described in Groch et al. (2005), resulted in only two sightings
of whale groups that were not mother-calf pairs in 14 yr (Table 1). The historical
occurrence pattern of whale groups in Santa Catarina indicate that this area can be
considered primarily a nursery ground between October and November. Therefore,
studies conducted during this period at Santa Catarina can address specific questions
about the biology and behavior of mother-calf pairs with negligible influence of juve-
niles and other adult whales.
The objective of the present study was to investigate diel trends in SWR mother-
calf calling behavior at Santa Catarina’s nursery ground. Based on previously
described behavior of SRW mother-calf pairs in wintering areas and on the potential
function of upcalls as contact calls, our initial hypothesis predicted invariable
Table 1. Summary of aerial survey sightings of whale groups (mother-calf pairs and others)
in October and November by year, from 2002 to 2015. Note that historically the occurrence
of other whale groups in the area is very rare in the presented months. Other whale groups
were sighted only twice: once in October 2007 and once in November 2002. Both sightings
were identified as adult whales unaccompanied by calves.
Year
Mother-calf pair Other
October November October November
2015 0 —0—
2014 —70—
2013 —7—0
2012 —2—0
2011 —14 —0
2010 —9—0
2009 —9—0
2008 15 0 0 0
2007 28 7 1 0
2006 11 —0—
2005 9 —0—
2004 12 0 0 0
2003 19 0 0 0
2002 —1—1
2MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
upcalling activity of pairs. Calves and their respective mothers tend to actively main-
tain closeness as they near the departure date from the wintering grounds (Taber and
Thomas 1982, Thomas and Taber 1984). Actually, in this phase of imminent migra-
tion, physical closeness between mother and calf may be greater than in any other
phase of the calf’s development (Taber and Thomas 1982, Thomas and Taber 1984).
Thus, as upcalls are thought to be used for contact maintenance (Clark 1983, Parks
and Tyack 2005), we could expect the individuals within pairs to be emitting upcalls
with no regard to light regime during the final months of the whale season when
sounds were recorded for this study.
Gamboa beach (27°570S, 48°370W) (Fig. 1) was chosen as a recording site because
the area is considered relatively pristine (with low commercial ship traffic due to its
distance from the Imbituba harbor) and because it had adequate conditions for the
Figure 1. Map of the study area. Due to the importance of the Santa Catarina’s coastal
waters for SRW, the Brazilian government created the Right Whale Environment Protection
Area (Right Whale EPA, Brasil 2000). The Imbituba harbor, located within the Right Whale
EPA, concentrates commercial shipping traffic in the area. Archival recording devices were
deployed at Gamboa beach, a location considered pristine in terms of underwater noise.
NOTES 3
recorder’s operation and deployment. One fixed archival autonomous recording unit
(DSG Ocean, Loggerhead Instruments, Sarasota, FL) was deployed on 14 October and
replaced by a second identical device on 21 October. The second unit remained
recording until 28 October, totaling 14 d of recordings in 2011.
Devices were set to continuously sample at a rate of 8 kHz and 16-bit resolution.
Each DSG unit was equipped with HTI-96 MIN hydrophones with typical sensitiv-
ity of –201 dBV lPa
–1
between 2 Hz and 30 kHz. Gain level was set to 33 dB (~168
dB re 1lPa clip level). As sampling was interrupted, data from days on which devices
were manipulated (deployed, substituted, and/or recovered: 3 d) were excluded from
analysis.
In order to elect the most effective method to detect upcalls, trial data consisting
of 43 h of recordings were subjected to different detection methods: (1) manual
inspection; (2) an automated detection tool developed for NARW upcalls
(Urazghildiiev and Clark 2006, Urazghildiiev et al. 2009); and (3) a combined tech-
nique using the NARW automated tool associated with manual browsing of 1 min
segments before and after each detection event using XBAT (Figueroa 2007) as
described in Rocha et al. 2015.
The combined technique resulted in 635 upcall detections in the trial data set. It
had the best performance among the methods tested and the resulting number of
detections was considered the number of true positives (635 =100%). Manual
inspection resulted in 464 upcall detections (73%). The automated NARW detection
tool detected 505 events and included 386 (61%) true positives and 119 false posi-
tives, which were manually verified. False positives were identified as noise, fish
sounds, and duplicated detections of the same upcall. The automated detection tool
failed to detect all calls in a sequence of closely spaced upcalls (<10 s between calls).
However, it was more effective in detecting masked upcalls in comparison to the
manual method. Thus, the entire data set was subjected to the combined detection
method.
Days with uninterrupted 24 h sampling were divided into four diel periods accord-
ing to the sun altitude angle in relation to the horizon: Dawn, Day, Dusk, and Night
(Munger et al. 2008). Dawn was defined by sun altitude between –12°and 0°,which
corresponds to the beginning of nautical twilight until sunrise. Day was the period
between sunrise and sunset when sun altitude was >0°. Dusk was defined by the per-
iod where sun altitude was between –12°and 0°followed by sunset. Night periods
were defined as hours of darkness in which sun altitude was <–12°to the horizon.
Hourly altitude angle of the sun for Gamboa (27°570S, 48°370W) was obtained at
the United States Naval Observatory website (http://aa.usno.navy.mil/data). Calling
rates (upcalls/h) were calculated within diel periods by dividing the total number of
detected calls in a given period by the period duration, as described in Munger et al.
(2008).
To correct for variation in the number of detected calls in each day, mean-adjusted
calling rates were computed by subtracting the daily calling rate from the calling rate
of each diel period of that same day (Munger et al. 2008). As data were divided into
heteroscedastic groups (Levene’s test =11.6, df1 =3, df2 =40, P<0.001), the Krus-
kal-Wallis test was used to verify if the mean ranks of adjusted calling rates across
periods were the same. Statistical tests were done using SPSS software (IBM
Statistics).
Overall, 3,712 SWR upcalls were detected in 264 h of continuous recordings made
off Santa Catarina’s nursery area in Brazil. We found no significant variability in
adjusted calling rates in relation to diel periods (Kruskal-Wallis test chi-square =
4MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
5.8, df =3, P=0.1). Mean rank of adjusted calling rates for Dawn, Day, Dusk, and
Night were 14.5, 23.9, 26.5, and 25.0, respectively. Median and mean values for
adjusted calling rates in each diel period are shown in Table 2. Distribution of calling
rates by diel period is shown in Figure 2.
To test the influence of outliers on our analysis, the same statistical tests were con-
ducted on our data set after the exclusion of outliers in adjusted calling rates. This
additional analysis also did not detect differences of calling rate throughout diel peri-
ods (P>0.05). Thus, as we believe that all calling rates accurately correspond to the
vocal behavior of whales, we reported here results considering the complete data set,
including outliers.
Our study provides evidence which suggests that the upcall emission by SRW
mother-calf pairs may be independent of diel period in the nursery area off Brazil,
whereas previous studies reported significant trends in upcalling behavior of the
North Atlantic right whale. Mellinger et al. (2007) and Mussoline et al. (2012) con-
ducted research in NARW foraging grounds and reported higher calling rates during
daytime and twilight periods. In contrast, Morano et al.(2012)andBortet al.
(2015) reported greater calling activity at night. Soldevilla et al. (2014) also found
higher calling activity during the night on NARW winter nursery grounds. For
North Pacific right whales (Eubalaena japonica), Munger et al. (2008) reported a sig-
nificant diel trend with increased calling rates at night. Finally, in SRW wintering
grounds off Argentina, Clark (1983) suggested greater calling activity during the
night.
As behavior varies between feeding and wintering areas, differences in temporal
patterns in calling behavior may be expected. In feeding areas, calling patterns may
be explained by a complex series of factors including the correlation between foraging
behavior and vocal activity (Parks et al. 2011, Morano et al. 2012, Matthews et al.
2014). In winter nursery areas, foraging behavior is infrequent making it unlikely
that diel trends are linked to feeding behavior in such areas. A more reasonable expla-
nation for increased calling rates during dark periods would be the greater use of
acoustic communicative signals when visual cues are less effective (Soldevilla et al.
2014). Visual monitoring of whale groups in periods of darkness is impossible.
Therefore, increased calling rates at night could be a result of an increased number of
vocally active but visually undetectable whales under the hydrophones’ detection
range, in both wintering and feeding areas (Mellinger et al. 2007, Munger et al.
2008).
Temporal patterns in calling behavior may be related to site-specific characteristics
(Mellinger et al. 2007). Thus, our results differ from Clark’s study (1983), conducted
in a SRW wintering area off Argentina, and from other research conducted in
NARW wintering areas (Soldevilla et al. 2014 and Bort et al. 2015), possibly due to
the unique demographic conditions of our study site when this study was conducted:
the area is utilized nearly exclusively by mother-calf pairs (see Table 1). In contrast,
Table 2. Mean (xSD) and median of adjusted calling rates (upcall/h) for each diel period.
Diel period Mean Median
Dawn (n=11) 7.4 12.6 –7.8
Day (n=11) 0.6 4.5 –1.3
Dusk (n=11) 16.0 31.2 9.9
Night (n=11) 0.02 6.5 1.4
NOTES 5
in other RW wintering areas, the occurrence of lone animals and SAGs were observed
(e.g., Clark 1983). Therefore, the temporal pattern reported here—invariable calling
rate throughout a 24 h period—may likely refer to the mother-calf pair’s vocal
dynamics alone while at other wintering grounds, vocalizations of other whale groups
present during recordings could have affected the reported temporal pattern of calling
behavior.
Greater variability in calling rates as observed in the dusk period in Santa Catarina
may indicate encounter events between pairs or other unknown situations that may
favor greater or lower vocal activity of pairs. Variable upcall detection might also
indicate changes in the number of vocally active animals within the detection range
of our recording system, lower vocal activity of animals within the detection range,
or changes in detection conditions (Mellinger et al. 2007, Munger et al. 2008, Sold-
evilla et al. 2014).
Although statistical results support our initial hypothesis of invariable contact sig-
naling during final weeks of the wintering season at the Santa Catarina nursery area,
given the short duration of our recorders deployment, the present study was not able
to provide evidence about variations in the temporal pattern of calling behavior dur-
ing early and mid-season, when different spatial relations between mother and calf
are expected (Thomas and Talber 1984). Therefore, increasing the sample size may
change the homogeneous vocal communication pattern of mother-calf pairs detected
in this study. This caveat warrants the collection of longer recordings to further
explore the hypothesis that increased acoustic activity occurs shortly before departure
from the wintering grounds and an increased sample size to provide further evidence
of the presence or absence of a diel pattern throughout the entire season.
Conversely, statistical results reported here may indeed reflect the calling behavior
of mother-calf pairs in this wintering ground throughout the season. In this scenario,
one can speculate that constant need of contact maintenance between mother-calf
could be related to parental care and calf dependence on lactation to acquire energy to
Figure 2. Adjusted calling rate (upcall/h) was not statistically different throughout diel
periods. Color bar corresponds to light regime within each diel period: Dawn and Dusk (gray),
Day (white), and Night (black).
6MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
migrate to feeding areas (Whitehead and Mann 2000). Furthermore, McCordic et al.
(2016) suggested that upcalls contain cues for individual identification. If vocal
recognition is important for mother right whales and their calves, constant vocal
activity could be associated with the individuals’ process of learning how to recognize
each other by using properties of upcalls before migration (Charrier et al. 2009).
Our results suggest that the vocal activity of southern right whale mother-calf
pairs may not vary significantly in 24 h in the nursery area off Brazil, and we hypoth-
esize that mother-calf pairs may require constant vocal communication in wintering
grounds in the last weeks before migration. Other environmental influences such as
tidal variation, moon phase, and boat traffic noise are among factors that may influ-
ence vocal activity of whales (Sousa-Lima and Clark 2008), and could be related to
temporal patterns of calling behavior of RW off Santa Catarina. Long-term monitor-
ing of the wintering area off Brazil is required to determine whether calling rates
change throughout the season and to comprehend the influence of such uninvesti-
gated factors on the vocal behavior of the species. Additionally, it is advisable to
investigate the spatial behavior and acoustic communication of RW mother-calf pairs
at wintering grounds, taking into consideration the ontogeny of acoustic signals and
behavior to expand knowledge about the mother-calf group that is key to the sur-
vivorship of all right whale populations.
Acknowledgments
We are grateful to Artur Andriolo, Christopher Clark, and all reviewers who provided valu-
able comments to improve this manuscript. We would like to acknowledge Ildar R.
Urazghildiiev for providing the NARW upcall detection tool, Fulvio A. M. Freire for sugges-
tions on statistical methods, and Renan Paitach for making the study area map. Scientific
Expedition authorization was provided by the Brazilian National Council for Scientific and
Technological Development (CNPq) to SEP, KRG, and RSSL. JRGD received a Master’s
scholarship from CNPq through the Graduate Program in Psychobiology at the Federal
University if Rio Grande do Norte. The Office of Naval Research provided SEP with funding
for fieldwork (grant number N00014-08-1-0967). License for data collection at the Right
Whale EPA was granted to KRG (SISBIO number 29774-1). Logistical support at the study
site was provided by APA Baleia Franca and Base Cangulo.
Literature Cited
Au, W. W. L., J. Mobley, W. C. Burguess, M. O. Lammers and P. E. Nachtigall. 2000.
Seasonal and diurnal trends of chorusing humpback whales wintering in waters off
western Maui. Marine Mammal Science 16:530–544.
Bort, J., S. M. Van Parijs, P. T. Stevick, E. Summers and S. Todd. 2015. North Atlantic right
whale Eubalaena glacialis vocalization patterns in the central Gulf of Maine from October
2009 through October 2010. Endangered Species Research 26:271–280.
Bradbury, J. W., and S. L. Vehrencamp. 1998. Principles of animal communication. Sinauer
Associates, Sunderland, MA.
Brasil. 2000. Decreto de 14 de Sembro de 2000. Disp~oe sobre a criac
ß
~ao da
Area de Protec
ß
~ao
Ambiental da Baleia Franca, no estado de Santa Catarina, e daoutrasprovid^encias
[Decree of 14 September 2000. Provides for the creation of the Right Whale
Environment Protected Area in the State of Santa Catarina, and other measures]. Diario
Oficial da Uni~ao, Brasılia, Brazil. 2 pp.
NOTES 7
Charrier, I., B. Pitcher and R. Harcourt. 2009. Vocal recognition of mothers by Australian sea
lion pups: Individual signature and envirmental constraints. Animal Behaviour
78:1127–1134.
Clark, C. W. 1983. Acoustic communication and behavior of the Southern right whale
(Eubalaena australis). Pages 163–198 in R. Payne, ed. Communication and behavior of
right whales. Westview Press for the American Association for the Advancement of
Science, Boulder, CO.
Figueroa, H. 2007. XBAT Extensible BioAcoustic Tool. Cornell Bioacoustic Research
Program, Ithaca, NY.
Groch, K. R., J. T. Palazzo, P. A. C. Flores, F. R. Adler and M. E. Fabian. 2005. Recent rapid
increase in the right whale (Eubalaena australis) population off southern Brazil. Latin
American Journal of Aquatic Mammals 4:41–47.
Marques, T. A., L. Munger, L. Thomas, S. Wiggins and J. A. Hildebrand. 2011. Estimating
North Pacific right whale Eubalaena japonica density using passive acoustic cue counting.
Endangered Species Research 13:163–172.
McCordic, J. A., H. Root-Gutteridge, D. A. Cusano and S. E. Parks. 2016. Calls of North
Atlantic right whales Eubalaena glacialis contain information on individual identity and
age class. Endangered Species Research 30:157–169.
Mellinger, D. K., S. L. Nieukirk, H. Matsumoto, et al. 2007. Seasonal occurrence of North
Atlantic right whale (Eubalaena glacialis) vocalizations at two sites on the Scotian Shelf.
Marine Mammal Science 23:856–867.
Morano, J. L., A. N. Rice, J. T. Tielens, B. J. Estabrook, A. Murray, B. L. Roberts and C. W.
Clark. 2012. Acoustically detected year-round presence of right whales in an urbanized
migration corridor. Conservation Biology 26:698–707.
Munger, L. M., S. M. Wiggins, S. E. Moore and J. A. Hildebrand. 2008. North Pacific right
whale (Eubalaena japonica) seasonal and diel calling patterns from long-term acoustic
recordings in the southeastern Bering Sea, 2000–2006. Marine Mammal Science
24:795–814.
Mussoline, S. E., D. Risch, C. W. Clark, et al. 2012. Seasonal and diel variation in North
Atlantic right whale up-calls: Implications for management and conservation in the
northwestern Atlantic Ocean. Endangered Species Research 17:17–26.
Parks, S. E., and P. Tyack. 2005. Sound production by North Atlantic right whales (Eubalaena
glacialis) in surface active groups. Journal of the Acoustical Society of America
117:3297–3306.
Parks, S. E., A. Searby, A. Celerier, M. P. Johnson, D. P. Nowacek and P. L. Tyack. 2011.
Sound production behavior of individual North Atlantic right whales: Implications for
passive acoustic monitoring. Endangered Species Research 15:63–76.
Risch, D., C. W. Clark, P. J. Dugan, M. Popescu, U. Siebert and S. M. V. Parijs. 2013. Minke
whale acoustic behavior and multi-year seasonal and diel vocalization patterns in
Massachusetts Bay, USA. Marine Ecology Progress Series 489:279–295.
Rocha, L. H. S., L. S. Ferreira, B. C. Paula, F. H. G. Rodrigues and R. S. Sousa-Lima. 2015.
An evaluation of manual and automated methods for detecting sounds of maned wolves
(Chrysocyon brachyurus Illiger 1815). Bioacoustics 24:185–198.
Seyboth, E., K. R. Groch, E. R. Secchi and L. Dalla Rosa. 2015. Habitat use by southern right
whales, Eubalaena australis (Desmoulins, 1822), in their main northernmost calving area
in the western South Atlantic. Marine Mammal Science 31:1521–
1537.
Soldevilla, M. S., A. N. Rice, C. W. Clark and L. P. Garrison. 2014. Passive acoustic
monitoring on the North Atlantic right whale calving grounds. Endangered Species
Research 25:115–140.
Sousa-Lima, R. S., and C. W. Clark. 2008. Modeling the effect of boat traffic on the
fluctuation of humpback whale singing activity in the Abrolhos National Marine Park,
Brazil. Canadian Acoustics 36:174–181.
Taber, S., and P. Thomas. 1982. Calf development and mother-calf spatial relationships in
Southern right whales. Animal Behaviour 30:1072–1083.
8MARINE MAMMAL SCIENCE, VOL. **, NO. **, 2017
Thomas, P. O., and S. M. Taber. 1984. Mother-infant interaction and behavioral development
in southern right whales, Eubalaena australis. Behaviour 88:42–60.
Urazghildiiev, I. R., and C. W. Clark. 2006. Acoustic detection of North Atlantic right whale
contact calls using the generalized likelihood ratio test. Journal of Acoustical Society of
America 120:1956–1960.
Urazghildiiev, I., C. W. Clark, T. P. Krein and S. E. Parks. 2009. Detection and recognition
of North Atlantic right whale contact calls in the presence of ambient noise. IEEE
Journal of Oceanic Engineering 34:358–368.
Van Parijs, S. M., C. W. Clark, R. S. Sousa-Lima, S. E. Parks, S. Rankin, D. Risch and I. C.
Van Opzeeland. 2009. Management and research applications of real-time and archival
passive acoustic sensors over varying temporal and spatial scales. Marine Ecology
Progress Series 395:21–36.
Whitehead, H., and J. Mann. 2000. Female reproductive strategies of cetaceans. Pages 219–
246 in J. Mann, R. C. Connor, P. L. Tyack and H. Whitehead, eds. Cetacean societies:
Field studies of dolphins and whales. The University of Chicago Press, Chicago, IL.
Received: 7 September 2015
Accepted: 4 November 2016
NOTES 9
