Landine - Etal.2024 MMS

Received: 22 September 2022 Accepted: 18 April 2024
DOI: 10.1111/mms.13146
ARTICLE
Humpback whales in the Southwest Atlantic

Ocean: investigating their breeding movements
by satellite tracking
Anne Landine 1,2 | Alexandre N. Zerbini 1,2,4,5,6 |

Daniel Danilewicz 2,3,7 | Federico Sucunza 1,2,3 |
Artur Andriolo 1,2
1
Laboratório de Ecologia Comportamental e
Bioacústica (LABEC), Instituto de Ciências Abstract
Biológicas, Universidade Federal de Juiz de Understanding animals' movements is essential to assess
Fora, Juiz de Fora, MG, Brazil
habitat use, life-history strategies, and population dynamics.
2
Instituto Aqualie, Juiz de Fora, MG, Brazil
3
Here, we investigate the movement and behavior patterns
Grupo de Estudos de Mamíferos Aquáticos
do Rio Grande do Sul (GEMARS), Torres,
of 153 humpback whales in the Southwest Atlantic Ocean
RS, Brazil (SWA) using data obtained by satellite telemetry between
4
Joint Institute for the Study of the 2003 and 2019 during the species' breeding season
Atmosphere and Ocean (JISAO), University of
(August–December) off the Brazilian coast. Switching state
Washington and Marine Mammal Laboratory,
Alaska Fisheries Science Center, National space models were applied to estimate behavior states
Marine Fisheries Service, NOAA, (bmode) classified as Area Restricted Search (ARS), Trans-
Seattle, Washington
5
iting (TRANS), or uncertain. Whales were distributed from
Cascadia Research Collective, Olympia,
Washington 4 S to 24 S, and five clusters of ARS behavior were identi-
6
Marine Ecology and Telemetry Research, fied along the Brazilian coast. Generalized linear mixed
Seabeck, Washington modeling revealed three main results: (1) a transition
7
Universidade Estadual de Santa Cruz, Ilhéus, towards more sinuous behavioral states with increasing
BA, Brazil
latitude; (2) more sinuous movement behavior around new
Correspondence moons; (3) movement behavior was temporally dynamic
Anne Landine, Rua José Lourenço, 393, Juiz
de Fora, Minas Gerais, CEP, Brazil
throughout the breeding season over the years, particularly
Email: [email protected] in 2019. The results then revealed important regions where
humpback whales cluster to engage in mating and nursing
behaviors, highlighting the influence of spatial location and
environmental cycles on their behavior. Estimated move-
ment behavior presented here improves the knowledge
about the habitat use and movement patterns of SWA
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https://doi.org/10.1111/mms.13146
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2 of 27 LANDINE ET AL.
humpback whales in their breeding ground and can be used

to mitigate potential human-related impacts.
KEYWORDS
Brazilian coast, breeding behavior, marine mammal, movement
patterns, population structure, satellite telemetry
1 | I N T RO DU CT I O N
Movement is an essential component in the life history and habitat use of individuals (Dingle & Drake, 2007).
The movement of an organism is defined as a change in the spatial location over time and is intricately linked to fun-
damental aspects of survival, such as locating suitable breeding or feeding habitats, moving toward or away from
conspecifics, or simply relocating (Nathan et al., 2008). In breeding grounds, movement plays a crucial role in an
organism's life history, influencing various aspects of its behavior and ultimately contributing to its reproductive
success. In other words, through movement, animals move to suitable regions that provide optimal conditions for
nursing and caring for their calves, as well as finding mating partners, thereby increasing the chances of reproduction
and offspring survival (Fedak et al., 2009).
For migratory animals such as large whales, reproductive and feeding behavior are spatially and temporarily
separate (Dingle & Drake, 2007). The migration of large whales has been described as an annual movement between
high-latitude summer feeding grounds and low-latitude winter breeding grounds (Dawbin, 1956, 1966). At the
breeding site, in general, large whales are fasting, supplying energy from stores previously accumulated in the feeding
areas (Jönsson, 1997; Stephens et al., 2009). Understanding the components that drive movement reveals how
animals allocate resources for reproduction throughout their lives to maximize fitness (Nathan et al., 2008;
Stearns, 1992). The movement patterns of whales at breeding sites are functions of social structure and are fre-
quently sex-biased (Craig et al., 2014; Lawson Handley & Perrin, 2007), as female and male whales face different
energy constraints, including gamete production, gestation, lactation, and mating competition (Lockyer, 1981).
The humpback whale, Megaptera novaeangliae (Borowski, 1781), is a well-studied and extensively documented
species of large whale, known for its remarkable migration one of the longest recorded among all mammals (Palsbøll
et al., 1997; Robbins et al., 2011). Although the specific selective pressures driving this migration are not fully under-
stood, it is believed that the behavior of migrating individuals is associated with higher reproductive success com-
pared to nonmigrating individuals (Clapham, 2001; Corkeron & Connor, 1999). Within wintering grounds, most
behaviors are related to calving and mating. The humpback whales often form small, unstable social groups and
exhibit no territoriality. Males, to gain access to females, can engage in physical agonistic social behavior, escort
females with a newborn calf during the postpartum period, and display by singing long complex songs. In contrast,
females actively exercise mate choice, exhibiting a wide and unpredictable distribution pattern while frequently visit-
ing congregations of male singers (Clapham, 1996).
During the breeding season, humpback whales aggregate in specific areas, where their spatial patterns change
based on the biological requirements of their life history (Cerchio, 1998; Clapham & Zerbini, 2015; Martins et al., 2001;
Mattila et al., 1989; Trudelle et al., 2018). These aggregations may facilitate mate selection and potentially indicate a
suitable reproductive habitat in the wintering areas (Clapham, 1996; Rasmussen et al., 2007). Therefore, defining the
distribution of movements and identifying areas with continued or repetitive use is important for a better understand-
ing of the species' reproductive biology, as the spatial scale at which the breeding strategies of humpbacks could occur
is poorly known (Dulau et al., 2017; Hoenner et al., 2012; Kernohan et al., 2001; Powell, 2000).
Another crucial aspect of studying movement behavior is understanding temporal patterns at multiple scales
(Levin, 1992). Movement patterns offer valuable insights into breeding activities, such as mating, calving, and nursing.
LANDINE ET AL. 3 of 27
For example, slower and erratic movement may indicate engagement in these activities, while fast and directed
movement may suggest movement between different regions (Jonsen et al., 2005, 2013). These patterns are
dynamic and can undergo significant changes over time, influenced by factors like motivation, experience, social
interactions, and environmental conditions (Dingle et al., 1985).
Animal life is rhythmic, and environmental cycles shape the biology and interactions of many species (Häfker &
Tessmar-Raible, 2020). Within marine organisms, variation in response to the lunar cycle are recognized as adaptive
features in their life cycles (Lea et al., 2010; Naylor, 2001; Owen et al., 2019; Sousa-Lima & Clark, 2008; Sterling
et al., 2014). Moon-related behavioral cycles have been observed to influence mating behavior and sexual maturation
in many marine animals (Häfker & Tessmar-Raible, 2020; Raible et al., 2017), with hypotheses often considering the
influence of tides or moonlight (Andreatta & Tessmar-Raible, 2020; Robertson et al., 1990; Tessmar-Raible
et al., 2011). Specifically, humpback whales have been found to exhibit higher surface activity during the new moon
(Félix, 2004), and male whales sing less during brighter moon phases (Cerchio et al., 2014). Additionally, behavioral
changes related to diel periods have been observed in humpback whales (e.g., Español-Jiménez & van der
Schaar, 2018; Helweg & Herman, 2010). Diel periods corresponding to daily cycles of light and dark are associated
with the synchronization and regulation of circadian clocks that govern physiological and biochemical processes,
ultimately impacting animal behavior (Baird et al., 2008; Bloch et al., 2013).
Analyzing population movement data can reveal variation in mating strategies within and between sexes or
based on ontogenetic differences (Dahlgren & Eggleston, 2000; Gibson et al., 2002; Pasquaretta et al., 2021; Schlaff
et al., 2020; Wearmouth & Sims, 2008). The study of cetacean biology is particularly challenging due to the difficulty
of observing animals that spend most of their time underwater. However, the development of Argos Platform
Terminal Transmitter (PTT) technology for satellite telemetry has significantly contributed to movement studies
(Cohn, 1999). Through telemetry, it is now possible to track and record data on survival, reproduction, behavior, and
physiology of animals, especially the marine mammals.
Here, we explore a 13-yr satellite telemetry data set of the western South Atlantic humpback whale population
during the breeding season, to investigate areas where breeding activity is most likely to occur and factors that
could influence humpback whale movements. Our hypothesis suggests that movement patterns associated with
reproductive activities, specifically Area-Restricted Search (ARS), exhibit clustering along the Brazilian coast.
Additionally, we propose that the movement behavior of whales is influenced by their reproductive status, sex, and
environmental conditions. The information gained from this study contribute to a better understanding of factors
that contribute to the reproductive success and survival of humpback whales, as well as refine our knowledge on the
habitat use of the species in breeding grounds. In this way, the study also contributes to species conservation and
management strategies for situations of environmental disasters.
2 | METHODS
2.1 | Transmitter deployments and data processing
Deployment of satellite transmitters was conducted during the humpback whale breeding season along the Brazilian
coast (August–November) between 12 S and 20 S from 2003 to 2019 (Horton et al., 2020; Zerbini et al., 2006).
Tagging operations were undertaken during good weather conditions (Beaufort sea state ≤3) from fiberglass speed
boats and rigid hull inflatable boats ranging from 5.5 to 6.7 m in length.
Whales were instrumented with implant type C (Andrews et al., 2019) Wildlife Computer (SPOT3, SPOT4,
SPOT5, SPOT6, and MK10) satellite transmitters. Deployment was conducted using a 8-m-long, custom-made
carbon fiber pole (Heide-Jørgensen et al., 2003) until 2009, and the ARTS system (Air Rocket Transmitter System;
Heide-Jørgensen et al., 2001) in the years 2010–2019, at pressures of 10–15 bars. The programming of the trans-
mitters varied across different years, depending on the specific types/models employed, with the aim of prolonging
the longevity of the transmitters. In SPOT models, the transmissions were conducted daily for a 3-month period and
then every 2 days. The transmitters of model MK10 were programmed to transmit 24 hr per day, either every day or
every 2 days of the year.
Group composition was determined in the field using group follows (Mann, 1999), with photographic
evidence used for subsequent confirmation. The social roles of the tagged individuals were assigned based on
their positions within the group composition. Whenever possible, tagged animals were biopsied according to the
methods described by Heide-Jørgensen et al. (2006) and Zerbini et al. (2006), for determining the sex of each
tagged individual, using molecular methods as described by Bruford et al. (1992) and Berube & Palsbøll (1996).
In cases where biopsies were not performed, the sex was inferred based on the social role, with mothers classi-
fied as females and escorts classified as males. The identity as the mother was inferred by consistently observing
her in close proximity to the calf (Clapham, 1996). Escorts were identified based on their spatial association with
the mother-calf pair (Glöckner, 1983; Mobley et al., 1999). Females were classified as lactating when accompa-
nied by a calf and as nonlactating when they were not.
Radio-signals from the tags were processed by Argos satellites (Argos, 1990) using the Doppler effect on the
transmission frequency, which decoded the information from the sensors, and recorded the geographical position of
the monitored individuals (see Argos, 2016). Location estimates were classified by Argos into seven quality classes,
designated as 3, 2, 1 0, A, B, and Z, in order of precision (Argos, 2016). Positions classified as Z are invalid locations
and were then removed from the database, as well as locations on land. The other locations were filtered using the
speed-distance-angle filter (SDA filter; Freitas et al., 2008), at a conservative maximum whale displacement speed of
18 km/hr (Zerbini et al., 2015) to remove only highly erroneous and unrealistic locations.
2.2 | Switching state-space model analysis
A Bayesian switching state-space model (SSSM) was applied to Argos-derived telemetry data to assess the
movement and behavior of humpback whales (Jonsen et al., 2006, 2013). An SSSM estimates animal's current
state (locations and behavioral) via a process model and uses that to predict its future state, and an observation
model that links the unobserved location states predicted by the process model to the observed data. To model
movement dynamics, we employed a first-difference correlated random walk model (DCRW) that accommodates
switching movement parameters between two distinct behavioral states: Transiting (TRANS) and Area
Restricted Search (ARS) (Jonsen et al., 2005). This was achieved by incorporating a separate DCRW for each
state, which varies in terms of their mean turning angle (θ) and move persistence (γ; autocorrelation in speed
and direction). A TRANS behavior is defined as a persistent and highly directional movement with low turning
angles (near 0 ), while an ARS behavior relates to animals moving at relatively slow speeds and displaying
sinuous paths (with turning angles around 180 ) as a result of a spatially restricted activity (e.g., interacting with
conspecifics or feeding; Barraquand & Benhamou, 2008). The SSSM ran two parallel Markov chain Monte Carlo
simulations (MCMC), producing a total of 50,000 MCMC samples for each chain. The first 20,000 samples were
discarded as burn-in, and the remaining iterations were thinned by retaining every 15th sample to reduce
autocorrelation. The posterior distribution of the model parameter estimates was computed with the remaining
2,000 samples (de Castro et al., 2014).
Markov chain models were used to describe the behavioral states through time by estimating the probability of
an individual switching states from TRANS at time t to ARS at time t + 1, or vice-versa (Jonsen et al., 2013). As in
previous studies (e.g., Andrews-Goff et al., 2018; Bailey et al., 2009; de Castro et al., 2014; Riekkola et al., 2019;
Weinstein et al., 2017), we have adopted conservative cut-off values for behavioral modes. Values closer to 1 (bmode
<1.25) were considered an indicative of TRANS behavior and values closer to 2 (bmode >1.75) indicative of ARS
behavior. Locations with behavioral mode values estimated between 1.25 and 1.75 were considered as “uncertain”
or without sufficient information to clearly distinguish behaviors (Jonsen et al., 2005).
An SSSM was fitted to all filtered locations for each humpback whale track separately, using the
software R (R Core Team, 2020) and WinBUGS software through the R package “R2WinBUGS”
(Lunn et al., 2000; Sturtz et al., 2005). A time interval of 6 hr was used to provide detailed data on the
movement of the whales (e.g., Andriolo et al., 2014; de Castro et al., 2014; Riekkola et al., 2019).
2.3 | Data organization and explanatory variables
Although an SSSM was fitted to each individual's throughout its route, only the positions located in the breeding
ground were retained for the analysis, adopting a region that comprises the limits of the continental shelf along the
Brazilian coast, with a depth of <200 m (Andriolo et al., 2010a, b; Zerbini et al., 2006, 2011). The trajectory positions
outside the continental shelf limits, but with a return to the 200 m isobaths, were also analyzed. Locations beyond
continental shelf boundaries (depth > 200 m) with a continuous transit behavioral state (>3 TRANS locations) were
recorded as a departure from wintering grounds and were removed from the analysis.
The influence of the variables diel period, day of the year, year, moon phase, longitude, latitude, and animal sex
on the behavioral modes estimates by SSSM was explored through linear models. The date of the locations was
converted to Julian days, using the R package “lubridate” (Grolemund & Wickham, 2011) and was used to evaluate
the moon phases using the R package “lunar” (Lazaridis, 2014). Phases were categorized as new, waxing crescent,
first quarter, waxing gibbous, full, waning gibbous, last quarter, and waning crescent. Diel period was classified into
four categories according to solar elevation, using the R package “oce” (Kelley & Richards, 2016). The day period
was defined with a solar elevation greater than +6 ; solar elevation from 12 to +6 of the horizon, including
sunrise was classified as dawn; For the twilight period, the solar elevation was +6 to 12 , including sunset, and
when the solar elevation was below 12 , the period was night (Falcone et al., 2017).
2.4 | Area-restricted-search patches
ARS patches were identified for each individual to describe habitat use and to identify important areas for
interspecific interaction. ARS patches were defined as three or more successive locations with behavioral
estimated state >1.75 and ending with three or more consecutive locations assigned a behavioral estimated state
<1.75 (Bailey et al., 2009; Lesage et al., 2017; Lydersen et al., 2020). The number of positions and time spent
for each patch were determined, and the total range of ARS patches with more than five locations combined was
estimated using the “Minimum Convex Polygons” package in R (MCP km2; Lydersen et al., 2020).
The hierarchical density-based spatial clustering of applications with noise (HBSCAN) method was applied to the
ARS patches using the R package “dbscan” (Hahsler et al., 2019). This method is a clustering algorithm that groups
together nearby data points based on their density, where points that are closer together have a higher density than
those that are farther apart. The algorithm also identifies areas of low density, called noise, where points do not
belong to any cluster. A minimum of 30 points per cluster (minPts = 30) was established by visual analysis, striking a
balance between avoiding noise points being assigned to clusters and preventing clusters from being divided into
subclusters (McInnes & Healy, 2017). After identifying the clusters, the number of locations and range of each cluster
site were also computed using MCP (Lydersen et al., 2020).
2.5 | Analyses of movement behavior
Generalized linear mixed models (GLMMs) were fitted to assess the influence of the explanatory variables on the
SSSM estimated behavioral modes, by maximum likelihood (ML) using the R package “nlme” (Pinheiro et al., 2019).
The behavior mode variable was logit transformed (Cerchio et al., 2016; O'Toole et al., 2015; Riekkola et al., 2019)
after being adjusted to range between 0 (TRANS) and 1 (ARS) as a continuous variable (Warton & Hui, 2011).
Tagged individuals were included as a random effect and an autoregressive moving average (ARMA) autocorrelation
structure (3,1) was added to model temporal autocorrelation in the telemetry data for each whale. Variables were
tested for collinearity using variance inflation factors (VIF) in the R package “car” (Fox & Weisberg, 2019). A thresh-
old value of 3 was used to remove collinear variables (Zuur et al., 2009). All predictors were scaled and centered to
zero mean and unit variance.
An automated model selection was conducted (function dredge in the R package “MuMIn”; Bartoń, 2018) to
check for all possible model combinations. Second-order Akaike information criterion (AICc) tests were
conducted, and models with a ΔAICc <4 were considered for selection of the best model (Burnham et al., 2011).
The best model was refitted using restricted maximum likelihood (REML) to obtain the final parameter estimates
(Zuur et al., 2009). The normality and homogeneity of the residues were checked graphically. Post hoc analyses
were run using the R package “emmeans” (Lenth, 2020) to assess pairwise differences between categorical
variables. All figures were produced using the R package “ggplot2” (Wickham, 2016). Analyses were completed
in R (R Core Team, 2020). The values were reported as mean ± standard deviation (SD). A significance level of
0.05 was used for statistical analyses.
3 | RESULTS
3.1 | Data collected
A total of 158 humpback whales were tagged on the Brazilian coast from 2003 until 2019 (no tagging operations
occurred in 2013, 2014, and 2015). Five individuals were not included in the analysis because they had less than
three locations available, resulting in a total of 153 individuals investigated (Table S1). Sex identification was
determined for 54 individuals, and inferred for the remaining 99 individuals, with 35 males, 97 females, and
21 indeterminate identified (Table S1). After processing the tracking data obtained in the breeding area, a total of
11,712 locations were obtained from all individuals combined (Table 1), with whales occupying regions over the
continental shelf spanning from 4 S to 24 S (Figure 1). The mean tracking duration ranged between 1.25 and
77.25 days (22.34 ± 16.15 days). The mean distance traveled, based on model-derived positions for all individuals
in the breeding area, ranged from 18.66 to 4,530.83 km (1,166.41 ± 821.37 km).
The departure positions from the wintering grounds, referring to when the whales moved beyond the continental
shelf limits (depth > 200 m) and did not return to the breeding area, were recorded for a total of 121 whales.
Departures occurred between August 8 and December 26. One mother departed from the breeding ground at 10 S in
September 2009, while all other individuals began their migration between 19 S and 24 S. An individual tagged in
2012 had its transmission recorded until the following year's breeding season, and was tracked returning to the
Brazilian coast on August 20, 2013.
T A B L E 1 Summary of SSSM estimated locations based on sex and reproductive class of tagged animals. Mean
location per individual.
Sex Reproductive class n Number of locations Mean number of locations (± SD)

Female Lactating 90 7,603 84.47 ± 57.05
Nonlactating 7 338 48.28 ± 33.56
Male 35 2,327 66.48 ± 44.56
Indeterminate 21 1,444 68.71 ± 56.38
3.2 | Movement behavior
In the breeding area (depth < 200 m), the SSSM-predicted locations were classified into three behavioral states
(Figure 2), with ARS accounting for 39% of the total, followed by uncertain locations (37%), and TRANS (23%). The
mean number of behavioral modes per individual was 41.7 ± 44.8 for ARS, 33.4 ± 36 for TRANS, and 28.9 ± 32.2 for
uncertain states. The frequency of behavior modes among all 153 whales in the data set did not show a significant
F I G U R E 1 Switching state-space model derived from Argos System locations and inferred behavioral modes for
153 humpback whales instrumented with satellite tags 2003 (n = 11), 2005 (n = 13), 2006 (n = 10), 2007 (n = 11),
2008 (n = 17), 2009 (n = 12), 2010 (n = 11), 2011 (n = 8), 2012 (n = 15), 2016 (n = 2), 2017 (n = 25), 2018
(n = 14), and 2019 (n = 4). The track of 2013 was from individual 121196.12 tagged in 2012, in which the
transmitter's duration reached the year following the tagging. ARS = Area Restricted Search, TRANS = Transiting.
Isobath of 200 m shown in blue line.
F I G U R E 2 Switching state-space model (SSSM)-derived locations of animals tagged in a breeding season (2011)
to show in detail the behavioral states estimated by SSSM. Isobath of 200 m shown in blue line.
difference between males, lactating females, and nonlactating females (approximative K-sample Fisher-Pitman
permutation test χ2 = 2.97, p = .22; Table 2). In all months except for December, ARS had the highest observed
frequency among the behavioral states (Figure 3a). ARS behavior was most prevalent during the dawn and day
periods, while uncertain behavior remained consistent across all periods, and TRANS behavior had lower occurrence
compared to ARS and uncertain behaviors in all periods but dawn (Figure 3b).
Thirty-seven whales (28 lactating females, three nonlactating females, and six males) exhibited a
total of 598 model predicted locations off the continental shelf and then returned to isobaths <200 m.
T A B L E 2 Mean frequency of behavior states per individual (mean ± SD) estimated by SSSM based on sex and
reproductive class. ARS = Area Restricted Search, TRANS = transiting.
Behavior states Sex Reproductive class Number of locations Frequency (%)

ARS Female Lactating 3,349 42.5 ± 40.8
Nonlactating 73 17 ± 8.3
Male 631 32.6 ± 32.3
TRANS Female Lactating 1,822 33 ± 32.9
Nonlactating 112 52.3 ± 63
Male 497 30 ± 31.8
Uncertain Female Lactating 2,432 24.3 ± 26.1
Nonlactating 154 30 ± 31.8
Male 1,199 37.2 ± 35.7
F I G U R E 3 Frequency distribution of behavioral states rates of western South Atlantic humpback whale
population tagged in Brazilian coast over the months (a), and diel periods (b). ARS = Area Restricted Search,
TRANS = Transiting.
Among individuals that engaged in movements outside the continental shelf, the TRANS behavioral mode
showed the highest frequency offshore (45.6%), followed by uncertain (27.7%) and ARS (26.6%). These
individuals reached regions up to 3,824 m deep. Between September and December, 17 tagged whales
(12 lactating females, one nonlactating female, and four males) presented positions near Vitória-Trindade
Seamount Chain (Besnard Chain) at 19 S, 38 W in the years 2003, 2006, 2008, 2010–2012, and 2017–2019,
before later returning to the continental shelf (Figure 2).
ARS was only performed up to two times for 56 animals (30 lactating females, one nonlactating female, 17 males,
and eight indeterminate) tagged between August and October. Among animals without ARS behavior, 35 individuals
(17 lactating females, eight indeterminate, and 10 males) had a tracking duration between 1.25 and 18.5 days. The
remaining 21 animals, consisting of 13 lactating females, one nonlactating female, and seven males were tracked for
20.2–77.5 days. This group of whales included animals tagged in various years, including 2003 (one lactating female),
2008 (one lactating female and one male), 2009 (one nonlactating female), 2017 (six lactating females and four
males), and 2018 (five lactating females and two males). Whales tagged in 2008 and 2009 reached latitudes between
F I G U R E 4 Maps showing the tracks of the humpback whales instrumented with satellite transmitters on the
Brazilian coast when presenting Area Restricted Search (ARS) movement behavior per sex (a) and per cluster regions
with high densities of ARS patches (b) Cluster 1: n = 1, Cluster 2: n = 5, Cluster 3: n = 6, Cluster 4: n = 71, Cluster
5: n = 8. IND = indetermined sex. Isobath of 200 m shown in blue line.
10 S and 9 S and migrated south to leave their wintering grounds. The whales tagged in 2017 and 2018 moved to
the southern region, reaching regions between 16.3 S and 23.7S .
3.3 | Area restricted search patches
Among the 98 whales that showed ARS behavior, 89 (55 lactating females, five nonlactating females, 16 males,
and 13 indeterminate) were identified with three or more consecutive ARS modes (Figure 4a). The other nine
whales exhibited ARS behavior but not with a sequence of three or more consecutive ARS states. A total of
145 ARS patches were identified (4,305 locations), with a maximum of five patches per individual and a mean of
1.62 (± 1.02). Time spent in patches varied between 1.25 and 43.5 days (10.6 ± 9.7 days). On average, males
(12.3 ± 13.7 days) spent more time in the ARS patches than females (10.5 ± 8.8 days) (approximative two-sample
Fisher-Pitman permutation test z = 0.63, p < .05). ARS patches occurred most often in October (45%), followed
by September and November, with 24% and 26% of ARS patches, respectively. August (4%) and December
(2%) had the lower frequency of ARS patches (approximative K-sample Fisher-Pitman permutation test, χ2 = 17.5,
p = .05). Time spent per ARS patch (days) did not vary significantly with year (approximative K-sample Fisher-
Pitman permutation test χ2 = 17.5, p > .05).
The patch track sizes ranged from 35.6 km to 6,129.3 km, with a mean of 578.9 ± 850.4 km. We found no
significant difference in patch track size between males and females (approximative two-sample Fisher-Pitman
permutation test z = 1.3, p > 0.05). The calculation of patches resulted in 110 patches, each with more than
5 recorded locations. These patches varied in size from 24.5 km2 to 39,267.6 km2 (5,486.06 ± 7,707.2 km2). Males
(6,701.6 ± 7,127 km2) and females (5,337 ± 8,003.1 km2) failed to show significant differences in patch area. The
travel speed in ARS patches ranged from 0.23 km/hr to 5.37 km/hr (1.9 ± 1.87 km/hr). The mean individuals' speed
was significantly higher in patches located further south, (between 17 S and 22 S; 5.37 km/hr) in comparison to the
north portion of the study area (2.16 km/hr) (approximative K-sample Fisher-Pitman permutation test χ2 = 177,
p < .05). A significant positive correlation was found between the time spent in an ARS patch and the size of the
patch area (Spearman's rank correlation rho S = 48,388, p < .05, rho = 0.78).
3.4 | ARS patch clustering
Five ARS patch clusters were identified (Figure 4b). Cluster 1 has a size of 8,569 km2 and was localized in northern
Brazil between 4.7 S and 6 S and their 56 positions came from a unique mother whale (PTT 87768.08) in September
and October of 2008. Individuals used Cluster 1 for 19.5 days, moving with a mean speed of 2.48 ± 1.7 km/hr.
Cluster 2 has a size of 9,707 km2 and was formed by positions (n = 120) of five individuals (three females and two
indeterminate) that together occupied the area from August to October in 2008, and October in 2009 and 2011,
between 8 S and 11 S, moving with a mean speed of 2.18 ± 1.48 km/hr, during a period of 6.75 ± 5.34 days.
Cluster 3 has a size of 1,179 km2 and was occupied by six whales (four females and two males) between
September and October from 2009 to 2011, moving at a slower mean speed of 1.28 ± 1.32 km/hr compared to
other cluster regions, during a period of 2.08 ± 1.99 days. Cluster 4 covering 102,802 km2 and located between
15 S and 22 S, comprised 71 individuals (49 females, 11 males, and 11 of indeterminate) moving at a mean speed of
1.84 ± 1.83 km/hr. It had the highest number of positions (n = 3,896) recorded between August and December in all
years studied, with individuals spending a period of 16.16 ± 14.02 days in the region. Cluster 5 was comprised of
eight female whales that were tracked for 4.09 ± 1.96 days between September and November over seven years
(2003, 2005, 2007, 2008, 2011, 2017, and 2018). These whales exhibited the highest mean speed (2.65 ± 2.48 km/hr)
among all the clusters studied, and their movements occurred in a region spanning 10,061 km2 between latitudes
22 S and 23 S.
3.5 | Linear models
Model selection indicated that the full model had the best fit, including the effects of the variables sex, dial phase,
year, day of the year, and lunar phase as important predictors on the behavioral state of humpback whales within
their Southwest Atlantic Ocean (SWA) breeding grounds (Table 3), and presented 22% of deviance explained.
Latitude and longitude were maintained as fixed variables in dredge selection to control spatial effects, therefore all
models presented these variables and their interaction.
In the best fit model (Table 4), latitude had a significant effect on bmode values, revealing that animals
exhibited more erratic movements when localized in high latitudes. Although latitude had a greater impact on
the bmode, its interaction with the day of the year was not statistically significant, suggesting that the relation-
ship between latitude and bmode values does not vary significantly depending on the specific day of the year.
T A B L E 3 Model selection results for the nine more plausible models (ΔAICc <4). Akaike's information criterion
(AIC), changes in AIC (ΔAIC) are reported for each candidate model compared to the best model.
Variables Model no. K logLik AICc ΔAICc Weight

diel + lat + lon + lunar + sex + year + 1 59 10,546 21,210.32 0 0.28
yday + diel:sex + lat:lon + lat:yday + lunar:
yday + year:yday
diel + lat + lon + lunar + sex + year + 2 58 10,547.21 21,211.09 0.77 0.19
yday + diel:sex + lat:lon + lunar:yday +
year:yday
lat + lon + lunar + year + yday + lat:lon + 3 52 10,553.46 21,211.46 1.14 0.16
lat:yday + lunar:yday + year:yday
lat + lon + lunar + year + yday + lat:lon + 4 51 10,555 21,212.4 2.08 0.1
lunar:yday + year:yday
lat + lon + lunar + sex + year + yday + 5 53 10,553.22 21,213 2.68 0.07
lat:lon + lat:yday + lunar:yday + year:yday
diel + lat + lon + lunar + sex + year + yday + 6 46 10,560.69 21,213.81 3.5 0.05
diel:sex + lat:lon + lat:yday + lunar:yday
lat + lon + lunar + year + yday + lat:lon + 7 39 10,568 21,213.84 3.52 0.05
lat:yday + lunar:yday
lat + lon + lunar + sex + year + yday + 8 52 10,554.67 21,213.87 3.56 0.05
lat:lon + lunar:yday + yr:yday
diel + lat + lon + lunar + year + yday + 9 55 10,552 21,214.3 3.98 0.04
lat:lon + lat:yday + lunar:yday + year:yday
Note: K = number of parameters; Yday = day of the year; lunar = lunar phase; Diel = diel phase; lat = latitude;
lon = longitude. The individual whale was included as a random effect in all models. Model with best fit in bold.
Additionally, the effect of the lunar phase was noticeable. The post hoc analysis showed that the new moon had
a different effect compared to the waning crescent, waxing gibbous, last quarter, and waning gibbous phases
(Figure 5a). Such analysis also indicated that the interaction between the day of the year and moon phases had a
significant effect on bmode values. This finding suggests that moon phases play a significant role in influencing
bmode values, and the magnitude of this influence varies depending on the specific day of the year.
The day of the year alone did not show a significant effect on the behavior of the whales, nor did the variable sex.
Therefore, despite their inclusion in the selected model, the contribution of these variables to explaining the variability in
whale behavior was not significant based on the analyzed data. However, when in interaction with the year, the day of
the year caused a significant decrease in the bmode value, mainly in 2019 (Figure 5c). This year showed a distinct pattern
compared to others, marked by a sharp decrease in bmode values towards the end of September and the beginning of
October, resulting in a reduction of approximately 1.18 units of bmode. This substantial decline indicates an abrupt transi-
tion to TRANS movement behavior, possibly reflecting the onset of animal migration or other relevant seasonal events. In
contrast, in other years, the transition to TRANS behavior was more gradual and occurred later in the season, typically
near December (Figure 5c). With respect to the year factor, bmode values were found to be smaller in the years 2016,
2017, 2018, and 2019 compared to the other years analyzed. The bmode values were significantly higher in the years
2005 and 2007 compared to the years 2017 and 2009, as well as in 2007 compared to the year 2018 (Figure 5b).
4 | DISCUSSION
This study contributes to a better understanding of movement behavior and habitat use by humpback whales
in wintering areas, exploring their movements in the SWA through a long-term satellite telemetry study.
T A B L E 4 Results of the best linear mixed-effect model, with logit transformed behavioral state (b) as a response
variable and individual whales as a random effect. Variables with a significant parameter estimate (<.05) are in bold.
Predictors Estimates SE t p
Intercept 0.72 0.58 1.24 .21
Diel phase
Day 0 0.04 0.04 .97
Dusk 0.02 0.04 0.37 .71
Night 0.03 0.05 0.65 .52
Waxing crescent 0.04 0.06 0.71 .48
First quarter 0.17 0.08 2.24 <.05
Waxing gibbous 0.26 0.08 3.10 <.05
Full 0.24 0.09 2.67 <.05
Waning gibbous 0.31 0.09 3.54 <.05
Last quarter 0.28 0.08 3.45 <.05
Waning crescent 0.20 0.06 3.14 <.05
Sex
Male 0.05 0.32 0.15 .88
Year
2005 1.02 0.72 1.41 .16
2006 0.42 0.95 0.45 .66
2007 1.96 0.83 2.36 <.05
2008 0.31 0.80 0.39 .70
2009 1.86 0.88 2.10 <.05
2010 0.70 0.90 0.78 .44
2011 0.16 0.77 0.21 .83
2012 0.23 0.81 0.28 .78
2013 21.14 12.39 1.71 .09
2016 0.85 2.43 0.35 .73
2017 1.44 0.63 2.27 <.05
2018 0.82 0.66 1.24 .22
2019 1.09 1.17 0.93 .36
Yearday 0.14 0.14 0.45 0.32 .75
Latitude 0.29 0.29 0.08 3.52 <.05
Longitude 0.06 0.06 0.04 1.39 .16
Diel phase * Sex
Day * Male 0.14 0.08 1.68 .09
Dusk * Male 0.20 0.08 2.47 <.05
Night * Male 0.19 0.08 2.20 <.05
Yearday * Latitude 0.13 0.13 0.08 1.64 .10
Lunar phase * Yearday
Waxing crescent 0.16 0.06 2.72 <.05
First quarter 0.25 0.08 3.11 <.05
Waxing gibbous 0.35 0.09 3.93 <.05
(Continues)
TABLE 4 (Continued)
Predictors Estimates SE t p
Full 0.20 0.09 2.10 <.05
Waning gibbous 0.15 0.09 1.63 .10
Last quarter 0.13 0.09 1.53 .13
Waning crescent 0.06 0.06 0.95 .34
Year * Yearday
2005 0.71 0.70 1.02 .31
2006 1.49 1.30 1.15 .25
2007 0.59 0.61 0.97 .33
2008 0.58 0.59 0.97 .33
2009 1.06 0.74 1.42 .16
2010 1.14 0.95 1.20 .23
2011 0.89 0.75 1.19 .23
2012 0.8 0.66 1.22 .22
2013 7.13 4.60 1.55 .12
2016 0.07 2.92 0.02 .98
2017 0.37 0.48 0.76 .44
2018 0.37 0.50 0.74 .46
2019 3.63 1.79 2.03 <.05
Latitude * Longitude 0.05 0.05 0.03 1.79 .07
Marginal R2: 0.22; Conditional R2: 0.37
F I G U R E 5 The relationship between the least square mean of logit transformed behavioral mode (bmode) and
significant explanatory variables lunar phase (a), year (b), and year and year day interaction (c). Higher predicted
logit(bmode) values indicate an increased likelihood of whales exhibiting Area Restricted Search (ARS) behavior.
Different lower-case letters indicate statistically significant differences between the categories (p < .05) (multiple
comparison procedure using Tukey contrasts; insets: generalized linear mixed-effects model output). Full line
represents a significant effect (p < .05). Models were fitted with scaled predictors.
Since the latest telemetry-based studies of the SWA humpback whale population (e.g., Andriolo et al., 2014;
de Castro et al., 2014; Zerbini et al., 2006, 2011), there has been a significant increase in the number of tagged
individuals, as well as variation in the locations and periods of tagging operations. With the increased number
of tagged animals in the years following the publication of previous telemetry studies, our findings confirm
their widespread distribution along the Brazilian coast, extending from 4 S to 24 S (Andriolo et al., 2010a;
Zerbini et al., 2006). This study provides a more detailed and comprehensive description of movement and
habitat use in the breeding area of this reproductive stock, revealing additional aspects of the species' move-
ment behavior and habitat use in Brazil.
Although humpback whales primarily utilize the continental shelf as their calving and mating area, observations of
whales exceeding the 200 m depth threshold but later returning to lower depths within the wintering area, predomi-
nantly in TRANS behavior, suggest that whales can move beyond the continental shelf for the purpose of transitioning
between different areas. Furthermore, the occurrence of ARS behavior near the Vitória-Trindade Chain, indicates
potential breeding activities due to the proximity of these seamounts to the breeding ground (Derville et al., 2020;
Dulau et al., 2017), supporting previous studies on the winter distribution near oceanic islands off Brazil (Lodi, 1994;
Siciliano et al., 2012; Wedekin et al., 2014; Zerbini et al., 2011). The observation of ARS behavior near seamounts
suggests that they may serve as habitats for sporadic foraging by humpback whales (Pitcher et al., 2008), which has
been observed along the Brazilian coast (Alves et al., 2009; Bortolotto et al., 2016b; Danilewicz et al., 2009). However,
further studies in these areas are recommended to provide additional support for this hypothesis.
4.1 | Movement behavior
Intensive searches correspond to periods of slow movement with high turning rates, where animals thoroughly
explore a small area, classified as ARS, potentially indicating reproductive behavior (Bailey et al., 2009; Knell &
Codling, 2012). While there is variation in energy expenditure among males and females of humpback whales, with
lactating females engaged in nursing behaviors and males displaying courtship behaviors to attract potential mates
and compete for breeding opportunities, the results suggest that they exhibit similar frequencies for each behavioral
state. In the model, we found that the variable “sex” did not exhibit a statistically significant impact on whale
behavior, despite its inclusion in the selected model. This implies that there is no statistically significant difference
in “bmode” values between male and female humpback whales. However, its inclusion in the model may serve to
control for potential effects or covariates. This indicates that, despite their distinct objectives in the breeding ground,
all whales alternate between more tortuous and linear movement patterns, with a predominance of ARS behavior
throughout the whole season.
Despite variation in the behavioral state of humpback whales throughout the day, the prevalence of the ARS
state remains consistently high across different diel periods. These results suggest that SWA humpback whales might
not exhibit specific preferences for particular times of the day when it comes to displaying breeding behaviors in
the breeding grounds. This idea is supported by the findings from the model analysis, which also revealed a lack of
significant temporal influence on the longitudinal behavior of the whales. However, it is crucial to acknowledge the
limitations imposed by the data resolution, which may impact the interpretation of behavioral differences within diel
periods. To gain a more comprehensive understanding of humpback whale behavior during specific times of the day,
future studies utilizing higher-resolution data are recommended.
In contrast, it was observed that humpback whale movement behavior is influenced by latitude and lunar phase.
Latitude and lunar phase are directly related to gravity, with variation in the strength of the gravitational field
contributing to additional topographical cues (Keeton, 1979). Horton et al. (2017) suggested that exogenous
magnetic and gravitational cues play a role in the orientation system of marine mammals. Our results support this
hypothesis, indicating a link between humpback whale movement behavior and gravity. However, further analysis is
needed to explore the influence of gravity on animal movement at breeding grounds.
In analyzing the influence of moon phases on the behavioral movement of humpback whales, the findings
indicate a significant association between moon phases and bmode values throughout the year. Specifically, higher
bmode values were consistently observed during the new moon phase, while lower values were associated with the
waning gibbous phase. This suggests that the cyclic phenomena associated with different moon phases, such as light,
gravitational, and magnetic cycles, may play distinct roles throughout the year (Bulla et al., 2017; Tessmar-Raible
et al., 2011). The stable ecological conditions provided by the lunar cycle can potentially serve as cues for synchronizing
physiology and behavior across the whale population, either through direct responses to cyclic environmental changes
or via internal biological mechanisms referred to as “clocks” (de la Iglesia & Johnson, 2013; Tessmar-Raible et al.,
2011). However, despite the significance of lunar cycles, the specific mechanisms underlying the impact of lunar cycles
on whale behavior remain unclear. Further research is necessary to investigate the underlying mechanisms driving this
influence and to identify the specific behavioral and ecological factors associated with different moon phases and their
effects on bmode values.
Despite being in the breeding area, some tagged whales did not exhibit ARS behavior, possibly due to shorter
tracking periods (<20 days). Conversely, whales without ARS behavior and longer tracking periods moved southward
and departed from the continental shelf shortly after tagging, indicating their migration initiation to feeding grounds.
The GLMM results revealed that movement behaviors were influenced by the whale's location, with more erratic
behaviors observed at higher latitudes. These findings align with the known departure location from the wintering
grounds, which occurs along the southeastern coast of Brazil between 20 S and 25 S (Zerbini et al., 2011). There-
fore, at lower latitudes, whales reduce their engagement in reproductive behaviors to initiate their migration, during
which they travel along a relatively straight and linear path (Horton et al., 2011; Zerbini et al., 2006).
Most of the records without ARS behavior occurred in 2017 and 2018, specifically between September and October.
This period coincided with the occurrence of a La Niña event, which is known to lower sea surface temperatures and alter
oceanic circulation dynamics (Kessler, 2006; Páez-Rosas et al., 2018). Such events can lead to variability in the distribution
patterns of tropical species or the migration of relatively cold-water species to warmer areas (Ballance et al., 2006). Envi-
ronmental fluctuations have been shown to impact the movement behavior and ecological interactions of humpback
whales (Benson et al., 2002; Chavez, 1996; Lenarz et al., 1995; McGowan et al., 1998). Denkinger et al. (2023) observed
humpback whales migrating further north during a La Niña event, supporting the hypothesis that these observations
could be related to the whales' adaptive response to environmental fluctuations, highlighting the importance of consider-
ing such events in understanding the movement patterns and ecological dynamics of humpback whales.
The model reveals a more pronounced variation in bmode values in 2019, characterized by a sharp decrease
between the end of September and the beginning of October, indicating a transition to TRANS behavior. Several
hypotheses can be raised to explain this behavioral change, such as the influence of seasonal events like El Niño or La
Niña, the timing of the year, the location of tagging operations, or anthropogenic actions. However, since the study
spanned multiple years, these factors were not unique to 2019. Nevertheless, in the same year, on August 30, an oil
spill occurred along the Brazilian coast, contaminating 4,334 km of coastline in 11 states in the northeast and southeast
(Escobar, 2019; Lourenço et al., 2020; Magris & Giarrizzo, 2020; Soares et al., 2020). The spill affected 31 coastal
municipalities in Bahia state, including the area where the tagging operations took place in 2019, on the southern coast
of Bahia (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, 2020a,b). The harmful effects of
oil impregnation and contamination have impacted endangered, vulnerable, and migratory species, escalating the possi-
bility of bioaccumulation and resulting in various ecological, social, and economic issues (Soares et al., 2020). The first
oil spots near Abrolhos, a site used by the tagged whales, were recorded at the end of October (Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renováveis, 2020b). However, to support the hypothesis that the oil spill
influenced humpback behavior, more thorough analyses must be conducted to explore the observed behavioral change
and the regions affected by oil spills, such as determining whether there was overlap or if the whales had already left
the area when the oil spill occurred. Hence, additional research is necessary to thoroughly analyze this finding.
Tagging operations conducted in October 2019 coincided with the period of the highest frequency of ARS
behaviors. However, in that particular year, the whales exhibited a propensity for displaying more uncertain
behaviors. Furthermore, despite the limited data available for that particular year, it was observed that two
individuals departed from the wintering ground in October. Studies following the 1989 Exxon Valdez oil spill in the
United States showed whales avoid oil-affected areas (Dahlheim & Matkin, 1994; Loughlin, 1994). This behavior can
be attributed to oil's adverse effects, including appendage fouling, fur adherence, and body orifice clogging, which
cause discomfort and lead animals to avoid contaminated areas (Fair & Becker, 2000). Understanding the habitat
preferences and movement patterns of humpback whales along the Brazilian coast can guide the development of
effective management strategies to mitigate the impacts related to human activities.
4.2 | Spatial distribution of localized behavior – ARS patches
Despite the population increase of humpback whales in the SWA (Bortolotto et al., 2016a; Pavanato et al., 2018)
and their reoccupation of previously utilized areas during the whaling period (Rossi-Santos et al., 2008), tagged
whales in recent years (2016–2019) exhibited localized movements primarily restricted to areas near Abrolhos
Bank, which serves as the main breeding area for humpback whales in Brazil (Andriolo et al., 2010a), reinforcing
the importance of the region for humpback whales. Abrolhos Bank includes three Marine Protected Areas
(MPAs), one of which is designated as an integral protection zone: the Abrolhos Marine National Park (de Castro
et al., 2014). However, these areas do not cover the southern portion of the Bank, where many anthropogenic
activities occur (de Castro et al. 2014; Martins et al. 2013). Moreover, the oil and gas industry is increasingly
keen on conducting exploration activities in the Abrolhos Bank region, and in an effort to protect marine species
in the area, previous management initiatives have entailed the suspension of oil and gas exploration operations
during the humpback whale breeding season (Engel et al. 2004, Marchioro et al. 2005). With the intensive use of
this region by the humpback whale population for reproductive activities, expanding the protected areas could
reduce the risk of anthropogenic impact, especially for calves, which are more vulnerable to disturbances
(Bortolotto et al., 2017).
The extended duration of humpback whales in ARS patches (averaging 10 days) suggests their tendency to
stay in suitable sites for extended periods to maximize fitness. These regions likely offer suitable environmental
factors, which could provide energetic advantages, such as seabed topography with shallowest waters, and low
sea surface temperature variability, increasing the chances of encountering mating partners and providing optimal
conditions for offspring care, thus enhancing their reproductive success (Clapham, 1996; Derville et al., 2019;
Rasmussen et al., 2007). Additionally, male patches were observed to be approximately 2 days longer on average
compared to female patches and covered a larger area. This aligns with the humpback mating system, where males
form aggregations and females disperse over greater distances to increase exposure to potential mates
(Clapham, 1996). Therefore, males spend more time in specific regions to display reproductive behaviors, resulting
in larger areas covered during ARS behavior.
Even so, the duration in the patches is relatively high for females as well. It is important to note that the majority
of tagged females were lactating, and for this class, energy expenditure is of particular importance. Lactating females
metabolize their stored energy reserves to sustain themselves and produce milk (Chittleborough, 1964). Therefore,
the motivation for lactating females to leave the patch must be influenced by factors that favor calf survival or
minimize additional energy expenditure. Such factors may include avoiding turbulent waters, predators, and male
harassment (Craig et al., 2014; Ersts & Rosenbaum, 2003).
Higher frequency of ARS patches was observed during the middle to the end of the breeding season, specifically
from September to November. This pattern coincides with the typical breeding season for humpback whales in
Brazil, which occurs from April to December (Andriolo et al., 2010a; Danilewicz et al., 2009; Martins et al., 2001;
Morete et al., 2003; Rossi-Santos et al., 2008; Zerbini et al., 2004). The higher likelihood of encountering potential
mating partners during this time, as most individuals have reached the wintering grounds, may explain the prevalence
of ARS behavior during these months, potentially contributing to enhanced reproductive success.
4.3 | Clusterings of ARS patch locations
Clustering of humpback whales in the breeding grounds may facilitate mate selection for both males and females
(Clapham, 1996). Along the Brazilian coast, ARS patches were consistently observed in five specific regions over the years,
indicating a strong preference for these areas (Figure 4b). The Abrolhos Bank region, in particular, has been extensively stud-
ied and shown to be favored by humpback whales (Andriolo et al., 2010a; Bortolotto et al., 2017; Martins et al., 2013).
However, two clusters (Cluster 2 and Cluster 3) in less-explored regions near Salvador (13oS) and off the coasts of Sergipe
and Alagoas States have previously been predicted to have a high density of humpback whales (Baracho-Neto et al., 2012;
Bortolotto et al., 2017; Zerbini et al., 2004). These findings suggest that the recognized areas crucial for humpback whale
mating and nursing behavior in the western South Atlantic may be more extensive than currently recognized.
The patches of lactating females exhibited a wide distribution along the Brazilian coast and comprised both the
northernmost and southernmost cluster locations. Conversely, the patches of males were confined to regions where
females also displayed ARS patches (Figure 4a). In mammalian males, reproductive success is primarily determined by
the availability of females, thus suggesting that male group patterns are influenced by female distribution
(Poole, 1994). Trudelle et al. (2016) demonstrated that in Madagascar, the movement of female humpback whales
was influenced by environmental factors, while male movement was influenced by social factors such as female
presence, which may also be occurring along the Brazilian coast.
Clusters 1 and 2 were located along the northeastern coast of Brazil, corresponding to historical areas where
humpback whales were hunted in the 20th century. These regions were predominantly occupied by females with
calves, underscoring their significance as crucial areas for nursing and caring for calves. These findings highlight the
reoccupation of important historical areas by humpback whales as they recover from the impacts of commercial
whaling. The presence of a land station in Paraíba State (6 S, 34 W) during that period suggests a relatively high
density of humpback whales in the region, which is consistent with the whaling data (Donovan, 1991;
Williamson, 1975). Furthermore, these observations align with previous studies documenting the regular presence of
humpback whales in coastal waters as far north as 5 S along the northeastern coast of Brazil, with a notable proportion
of calves observed in groups off NE Brazil (Andriolo et al., 2010a; Zerbini et al., 2004).
The smallest cluster area (Cluster 3) was observed between Morro de São Paulo and Serra Grande in the state
of Bahia. This region is characterized by a shelf break that is closer to the shore, resulting in abrupt changes in depth
(Gonçalves et al., 2018). This geographical feature may explain the limited area utilized by humpback whales for their
ARS movements in this area. It is worth noting that the average daily residence time for ARS behavior was relatively
low, around two days, which aligns with the overall low rates of occupation observed in the northern part of
Bahia state (Baracho-Neto et al., 2012; Rossi-Santos et al., 2008). However, despite the relatively short stays, the
consistent and prolonged presence of ARS behavior in this region over a span of 3 years highlights its significance
for humpback whale mating or nursing activities.
The cluster exhibiting the highest density of ARS patches and occupying the largest area is located between the
southern region of the State of Bahia and the northern region of the State of Espírito Santo. This region encom-
passes significant features such as Royal Charlotte Bank, Abrolhos Bank, and Besnard, one of the volcanic mounts
forming the Vitória-Trindade Chain. Among these, Abrolhos Bank emerges as the most crucial breeding site for
humpback whales in the western South Atlantic population (Andriolo et al., 2006; Engel, 1996). The unique charac-
teristics of Abrolhos Bank, including its sheltered conditions from prevailing winds and reduced water movement
dynamics, create an environment favorable for calf suckling and enable the mother-calf pair to remain in close
proximity with less effort (Martins et al., 2001).
ARS patches of nonlactating females were limited to the boundaries of Cluster 4, contrasting with the expected
behavior based on their movement in the breeding area, where they cover long distances to encounter a higher num-
ber of males and assess potential reproductive partners (Cerchio et al., 2005; Clapham, 1996, 2000; Herman &
Tavolga, 1980). The absence of nonlactating females in other clusters may be due to the relatively small sample size
of this specific group. Notably, the cluster where non-lactating females displayed ARS behavior overlaps with one of the
clusters where male ARS patches were observed. Humpback whales do not form stable groups, and mature females are
known to associate with different individuals during a single winter season (Clapham, 1996; Mobley & Herman, 1985).
These observations, along with molecular analysis supporting the promiscuous nature of females (Clapham &
Palsbøll, 1997), suggest a dynamic reproductive strategy influenced by mate choice and potential breeding opportunities.
The southernmost region of the breeding area consistently showed a higher concentration of ARS behavior from
September to November over 7 years. However, humpback whales had a relatively short stay in this region, typically
around 4 days. This particular region, spanning from the southern portion of Abrolhos Bank to the southeastern
coast of Brazil between 20 S and 25 S, is recognized as the departure zone for humpback whales as they transition
from their wintering grounds (Zerbini et al., 2006, 2011). The findings suggest that the whales in this cluster may
have been actively engaged in nursing their calves before initiating their migration to the feeding grounds, as the
majority of observed tracks in the area belonged to lactating whales. This highlights the significance of this area for
mother-calf pairs after their departure from the wintering grounds.
4.4 | Conclusions
This study fills an important gap in knowledge regarding humpback whale movement behavior in breeding/calving
grounds. The movement records during the breeding season indicate that their distribution along the Brazilian coast is
clustered; their movement patterns are influenced by environmental cycles, particularly lunar phases. The nature of hump-
back whale movement behavior is dynamic, both spatially and temporally, highlighting the complexity of their interactions
within the breeding grounds. This expanded knowledge base on species' movement patterns within the SWA provides
invaluable insights for future research into the degree to which humpback whales depend on environmental factors, such
as lunar phases, for navigation, and how changes in these cues impact their movement patterns. Additionally, it sheds
light on how the dynamic behavior of humpback whales influences conservation efforts, including the establishment of
protected areas, management of human activities in critical habitats, and mitigation of anthropogenic threats.
ACKNOWLEDGMENTS
This study was funded by the Exploration and Production Division of Shell Brasil SA from 2001 to 2012, and CGG from
2016 to 2019. Logistical and administrative support were provided by Instituto Aqualie, the National Marine Mammal
Laboratory/NOAA, and Programa de Pós-Graduação em Biodiversidade e Conservação da Natureza, Universidade Federal
de Juiz de Fora, Brazil. We thank the PMBS field teams for their support during the work. A.E.L. was supported by the
Coordenação de Aperfeiçoamento Pessoal de Nível Superior (CAPES), Brazil. This study was conducted under permits
issued by SISBIO 55354-4 e ABIO 857/2017, CNPq (Grant #CMC 026/02-028/03) and the Brazilian Environmental
Agency (IBAMA, permit #009/02/CMA/ IBAMA, process #02001.000085/02-27, ICMBio #11523-1).
AUTHOR CONTRIBUTIONS
Anne Landine: Conceptualization; formal analysis; investigation; writing – original draft; writing – review and editing.
Alex Zerbini: Funding acquisition; investigation; project administration; supervision; writing – review and editing.
Daniel Danilewicz: Methodology; project administration; writing – review and editing. Federico Sucunza Sucunza:
Methodology; writing – review and editing. Artur Andriolo: Funding acquisition; supervision; writing – review and editing.
ORCID
Anne Landine https://orcid.org/0000-0002-1402-6709
Alexandre N. Zerbini https://orcid.org/0000-0002-9776-6605
Daniel Danilewicz https://orcid.org/0000-0002-2164-5989
Federico Sucunza https://orcid.org/0000-0001-9418-5541
Artur Andriolo https://orcid.org/0000-0002-5582-0183
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SUPPORTING INFORMATION
Additional supporting information can be found online in the Supporting Information section at the end of this
article.
How to cite this article: Landine, A., Zerbini, A. N., Danilewicz, D., Sucunza, F., & Andriolo, A. (2024).
Humpback whales in the Southwest Atlantic Ocean: investigating their breeding movements by satellite
tracking. Marine Mammal Science, e13146. https://doi.org/10.1111/mms.13146

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Received: 22 September 2022 Accepted: 18 April 2024

Humpback whales in the Southwest Atlantic

Anne Landine 1,2 | Alexandre N. Zerbini 1,2,4,5,6 |

humpback whales in their breeding ground and can be used

2.1 | Transmitter deployments and data processing

2.2 | Switching state-space model analysis

2.3 | Data organization and explanatory variables

2.4 | Area-restricted-search patches

2.5 | Analyses of movement behavior

3.1 | Data collected

Sex Reproductive class n Number of locations Mean number of locations (± SD)

3.2 | Movement behavior

Behavior states Sex Reproductive class Number of locations Frequency (%)

3.3 | Area restricted search patches

3.4 | ARS patch clustering

3.5 | Linear models

Variables Model no. K logLik AICc ΔAICc Weight

4.1 | Movement behavior

4.2 | Spatial distribution of localized behavior – ARS patches

4.3 | Clusterings of ARS patch locations

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