Part of the funding for this study was provided by Shell. This company had no input in any stage of this study or in the decision to submit this manuscript for publication. This does not alter our adherence to PLOS ONE policies on sharing data and materials
The western South Atlantic (WSA) humpback whale population inhabits the coast of Brazil during the breeding and calving season in winter and spring. This population was depleted to near extinction by whaling in the mid-twentieth century. Despite recent signs of recovery, increasing coastal and offshore development pose potential threats to these animals. Therefore, continuous monitoring is needed to assess population status and support conservation strategies. The aim of this work was to present ship-based line-transect estimates of abundance for humpback whales in their WSA breeding ground and to investigate potential changes in population size. Two cruises surveyed the coast of Brazil during August-September in 2008 and 2012. The area surveyed in 2008 corresponded to the currently recognized population breeding area; effort in 2012 was limited due to unfavorable weather conditions. WSA humpback whale population size in 2008 was estimated at 16,410 (CV = 0.228, 95% CI = 10,563–25,495) animals. In order to compare abundance between 2008 and 2012, estimates for the area between Salvador and Cabo Frio, which were consistently covered in the two years, were computed at 15,332 (CV = 0.243, 95% CI = 9,595–24,500) and 19,429 (CV = 0.101, 95% CI = 15,958–23,654) whales, respectively. The difference in the two estimates represents an increase of 26.7% in whale numbers in a 4-year period. The estimated abundance for 2008 is considered the most robust for the WSA humpback whale population because the ship survey conducted in that year minimized bias from various sources. Results presented here indicate that in 2008, the WSA humpback whale population was at least around 60% of its estimated pre-modern whaling abundance and that it may recover to its pre-exploitation size sooner than previously estimated.
The humpback whale
The IWC recognizes seven humpback whale breeding stocks in the Southern Hemisphere [
Most humpback whales along the coast of Brazil concentrate on the Abrolhos Bank (16°40’S–19°30’S), where about 80% of the animals are expected to be found every year during the breeding season [
Such a recovery and expansion of the WSA humpback whale population may result in increased conflicts with anthropogenic activities, including ship strikes [
Multiple studies have provided abundance estimates for humpback whales off the Brazilian coast (e.g. [
Two research cruises were conducted aboard the R/V Atlântico Sul (Universidade Federal do Rio Grande, FURG) in 2008 and 2012. Surveys were designed to search for humpback whales using line transect methods [
This study was conducted under permits issued by the Brazilian National Council for Scientific and Technological Development (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq; grant #CMC 026/02-028/03) and the Brazilian Institute of the Environment and Renewable Natural Resources (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis, IBAMA, permit #009/02/CMA/IBAMA; process #02001.000085/02-27; ICMBio #11523–1).
The survey area was defined as the coast of Brazil, from Cabo de São Roque (~5°S), Rio Grande do Norte State, to Cabo Frio (~23°S), Rio de Janeiro State, covering the continental shelf from shore to the shelf break, defined in this study as the 500 m isobath limit (
Transect lines were zigzag-designed and allocated in 15 strata (i.e. survey blocks;
Tracklines allocation on the 2012 cruise was different from the 2008, because this survey’s focus was deploying tags throughout the study area while still surveying lines in all blocks. Therefore the survey design in 2012 did not follow that of 2008. Additionally, due to unfavorable weather conditions, the survey in 2012 was restricted to the area between Salvador (13°S), in Bahia State, and Cabo Frio, corresponding to the original blocks 8 to 15 (
Tracklines were surveyed in passing mode [
When detections were made, observers provided sighting information (reticle reading, radial angle, species identification and group size) to the data recorder using hand-held VHF radios. Data were immediately logged in a laptop computer equipped with the Wincruz software (R. Holland, SWFSC, NOAA, U.S.A.). Radial distances
Analyses were performed using the beta version of software Distance 7.0 and followed the guidelines suggested in Thomas et al. [
Covariate | Factor/Numeric | Levels |
---|---|---|
Sea condition | Factor | calm (Beaufort 0–3) and moderate (Beaufort 4–6) |
Cue | Factor | splash, body, blow and aerial behavior |
Method of detection | Factor | binoculars and naked eye |
Group size | Numeric | 1–7 |
Because of the relatively high numbers of unidentified whale sightings in both years, their abundances were also estimated. These estimates were assumed to correspond to humpback whales because sightings of other confirmed large whale species represented less than 1% of all large whale sightings in both cruises. Estimates were summed with those for confirmed humpback whale sightings and combined confidence intervals were computed with the log-based method [
Because the area surveyed in 2012 was smaller than that of 2008 (blocks 8 to 15,
Completed search effort was 2,337 km in 2008 and 1,683 km in 2012. In total, 416 humpback and 77 unidentified whale groups were sighted in 2008, and 557 humpback and 180 unidentified whale groups in 2012. These numbers were slightly reduced after truncation and are summarized in
2008 | 2012 | ||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Block | Area (km2 | k | L (km) | n HW | n/L HW(CV) | s HW(CV) | n UW | n/L UW(CV) | k | L (km) | n HW | n/L HW(CV) | s HW(CV) | n UW | n/L UW(CV) | ||||||
1 | 2,360 | 5 | 96.5 | 1 | 0.010 | (0.931) | 1.00 | — | 0 | 0 | — | — | — | — | — | — | — | — | — | — | — |
2 | 2,756 | 2 | 47.5 | 2 | 0.042 | (0.313) | 1.00 | — | 0 | 0 | — | — | — | — | — | — | — | — | — | — | — |
3 | 5,348 | 2 | 43.5 | 3 | 0.069 | (0.123) | 1.67 | (0.400) | 1 | 0.023 | (0.543) | — | — | — | — | — | — | — | — | — | — |
4 | 3,713 | 6 | 242.7 | 13 | 0.054 | (0.203) | 1.46 | (0.166) | 2 | 0.008 | (0.597) | — | — | — | — | — | — | — | — | — | — |
5 | 3,802 | 12 | 307.1 | 43 | 0.140 | (0.185) | 1.56 | (0.074) | 8 | 0.026 | (0.581) | — | — | — | — | — | — | — | — | — | — |
6 | 5,145 | 5 | 99.6 | 3 | 0.030 | (0.400) | 2.67 | (0.250) | 2 | 0.020 | (0.717) | — | — | — | — | — | — | — | — | — | — |
7 | 5,681 | 6 | 111.6 | 12 | 0.108 | (0.337) | 1.42 | (0.136) | 2 | 0.018 | (0.682) | — | — | — | — | — | — | — | — | — | — |
8 | 1,400 | 4 | 114.5 | 22 | 0.192 | (0.159) | 2.05 | (0.113) | 2 | 0.017 | (0.750) | 2 | 97.1 | 9 | 0.093 | (0.405) | 1.67 | (0.141) | 12 | 0.124 | (0.427) |
9 | 2,737 | 5 | 89.4 | 14 | 0.157 | (0.282) | 1.93 | (0.065) | 2 | 0.022 | (0.446) | 3 | 131.9 | 15 | 0.114 | (0.180) | 1.33 | (0.094) | 11 | 0.083 | (0.629) |
10 | 6,906 | 3 | 125.8 | 12 | 0.095 | (0.331) | 1.92 | (0.077) | 7 | 0.056 | (0.279) | 3 | 219.2 | 32 | 0.146 | (0.261) | 1.41 | (0.070) | 10 | 0.046 | (0.248) |
11 | 3,533 | 4 | 134.8 | 14 | 0.104 | (0.318) | 2.29 | (0.191) | 5 | 0.037 | (0.298) | 3 | 124.9 | 20 | 0.160 | (0.146) | 1.75 | (0.100) | 15 | 0.120 | (0.184) |
12 | 49,317 | 7 | 605.2 | 249 | 0.411 | (0.285) | 1.96 | (0.029) | 36 | 0.059 | (0.270) | 5 | 645.0 | 397 | 0.616 | (0.100) | 2.06 | (0.029) | 96 | 0.149 | (0.052) |
13 | 7,492 | 3 | 133.5 | 5 | 0.037 | (0.958) | 1.40 | (0.175) | 1 | 0.007 | (0.958) | 2 | 180.8 | 37 | 0.205 | (0.084) | 1.68 | (0.073) | 11 | 0.061 | (0.195) |
14 | 5,379 | 3 | 103.1 | 2 | 0.019 | (0.899) | 2.00 | (0) | 0 | 0 | (0) | 2 | 89.2 | 10 | 0.112 | (0.411) | 1.40 | (0.157) | 0 | 0 | (0) |
15 | 17,531 | 2 | 82.4 | 5 | 0.061 | (0.486) | 2.40 | (0.166) | 2 | 0.024 | (0.486) | 2 | 195.0 | 9 | 0.046 | (0.508) | 1.44 | (0.121) | 5 | 0.026 | (0.775) |
k, number of transects; L, realized effort; n, number of sighted groups; HW, humpback whales; CV, coefficient of variation; UW, unidentified whales; n/L, group encounter rate; s, average group size.
A half-normal model with one cosine adjustment term and a hazard rate model with no extra terms or covariates were chosen, respectively, as the detection probability models for confirmed humpback whale sightings in the 2008 and 2012 cruises. In the case of unidentified whales, models for both 2008 and 2012 were half-normal functions without adjustment terms or covariates. The most supported detection functions for each data type are presented in
Year | Species | Key function | Covariate/adjustment | Delta AIC | Par | ESW (km) | P (CV) | GOF–K-S p | |
---|---|---|---|---|---|---|---|---|---|
HW | Half-normal | Cosine | 0 | 2 | 1.59 | 0.40 | (0.05) | 0.9990 | |
HW | Hazard Rate | — | 1.20 | 2 | 1.57 | 0.40 | (0.08) | 0.9487 | |
HW | Hazard Rate | Group size | 1.80 | 3 | 1.61 | 0.40 | (0.04) | 0.9963 | |
UW | Half-normal | — | 0 | 1 | 3.54 | 0.64 | (0.10) | 0.7892 | |
UW | Hazard Rate | — | 0.72 | 2 | 3.08 | 0.56 | (0.22) | 0.9769 | |
UW | Half-normal | Sea conditions | 1.20 | 2 | 3.52 | 0.64 | (0.07) | 0.8370 | |
HW | Half-normal | Cosine | 0 | 3 | 2.04 | 0.51 | (0.07) | 0.9985 | |
HW | Hazard Rate | Cosine | 0.24 | 3 | 1.96 | 0.49 | (0.08) | 0.9595 | |
HW | Hazard Rate | Sea conditions | 1.37 | 3 | 2.01 | 0.50 | (0.03) | 0.8470 | |
HW | Hazard Rate | — | 1.47 | 2 | 2.06 | 0.51 | (0.06) | 0.8648 | |
UW | Hazard Rate | — | 0 | 2 | 2.34 | 0.58 | (0.13) | 0.5932 | |
UW | Hazard Rate | Sea conditions | 0.45 | 3 | 2.27 | 0.57 | (0.06) | 0.4468 | |
UW | Half-normal | — | 0.90 | 1 | 2.54 | 0.64 | (0.06) | 0.5603 | |
UW | Half-normal | Method | 1.67 | 2 | 2.53 | 0.63 | (0.05) | 0.7104 | |
UW | Hazard Rate | Method | 1.69 | 3 | 2.38 | 0.59 | (0.05) | 0.7692 |
Chosen models are highlighted in grey. Par, number of parameters; ESW, effective half-strip width; P, probability of detection; CV, coefficient of variation; GOF–K-S p, goodness-of-fit Kolmogorov-Smirnov test probability.
Estimates of density, abundance, CVs and 95% confidence intervals of confirmed humpback whales and unidentified large whales in 2008 are presented in
Humpback whales | Unidentified whales | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Block | D | N | %CV | N 95% CI | D | N | %CV | N 95% CI | ||
0.003 | 8 | 93.3 | 1 | 69 | — | — | — | — | — | |
0.013 | 37 | 31.8 | 1 | 1,136 | — | — | — | — | — | |
0.036 | 194 | 42.2 | 44 | 847 | 0.004 | 22 | 55.4 | 0 | 5,180 | |
0.025 | 92 | 26.9 | 52 | 162 | 0.001 | 5 | 60.8 | 1 | 23 | |
0.069 | 262 | 20.7 | 170 | 403 | 0.005 | 18 | 59.2 | 5 | 59 | |
0.025 | 130 | 47.5 | 43 | 392 | 0.004 | 19 | 72.6 | 3 | 109 | |
0.048 | 273 | 36.8 | 118 | 634 | 0.003 | 18 | 69.2 | 4 | 89 | |
0.124 | 174 | 20.3 | 109 | 277 | 0.003 | 4 | 75.8 | 1 | 36 | |
0.095 | 261 | 29.5 | 123 | 555 | 0.004 | 11 | 46.0 | 3 | 35 | |
0.058 | 398 | 34.4 | 113 | 1,399 | 0.010 | 69 | 30.1 | 25 | 187 | |
0.075 | 265 | 37.6 | 107 | 653 | 0.007 | 24 | 31.8 | 10 | 56 | |
0.254 | 12,519 | 29.2 | 6,303 | 24,867 | 0.011 | 526 | 29.3 | 272 | 1,017 | |
0.017 | 124 | 97.5 | 5 | 3,347 | 0.001 | 10 | 96.5 | 0 | 302 | |
0.012 | 66 | 90.1 | 2 | 1,778 | 0 | 0 | — | — | — | |
0.046 | 805 | 51.7 | 18 | 35,565 | 0.004 | 76 | 49.9 | 1 | 9,003 | |
D, density of animals; N, abundance of animals; CV, coefficient of variation; CI, confidence interval.
Humpback whales | Unidentified whales | |||||||||
---|---|---|---|---|---|---|---|---|---|---|
Block | D | N | %CV | N 95% CI | D | N | %CV | N 95% CI | ||
0.038 | 53 | 43.4 | 2 | 1,130 | 0.032 | 44 | 43.5 | 0 | 4,194 | |
0.037 | 101 | 21.4 | 56 | 183 | 0.021 | 58 | 63.5 | 5 | 665 | |
0.050 | 344 | 27.8 | 132 | 898 | 0.012 | 81 | 26.1 | 31 | 206 | |
0.068 | 241 | 18.9 | 150 | 385 | 0.031 | 109 | 20.0 | 56 | 210 | |
0.308 | 15,177 | 12.9 | 11,509 | 20,013 | 0.038 | 1,877 | 9.4 | 1,551 | 2,272 | |
0.083 | 624 | 12.9 | 451 | 864 | 0.016 | 117 | 21.0 | 27 | 507 | |
0.038 | 205 | 44.5 | 11 | 3,832 | — | — | — | — | — | |
0.016 | 284 | 52.7 | 3 | 29,323 | 0.007 | 115 | 77.9 | 0 | 486,360 | |
See
Pooled estimate | D | N | %CV | N 95% CI | |
---|---|---|---|---|---|
0.133 | 16,410 | 22.8 | 10,563 | 25,495 | |
0.163 | 15,332 | 24.3 | 9,595 | 24,500 | |
0.206 | 19,429 | 10.1 | 15,958 | 23,654 |
See
Block-specific estimates show that humpback whales distribution was not uniform across the surveyed area. Block 12 comprised Abrolhos Bank and had the highest density, including 85% and 88% of the total estimated abundance for 2008 and 2012, respectively. Some other regions also had relatively higher concentration of whales, such as the central coast of Bahia (blocks 8 and 9) in 2008, while areas further north (blocks 1 and 2) had very low densities. In 2012, the highest concentrations outside the Abrolhos Bank were found in adjacent areas, in blocks 10, 11 and 13.
In this study, abundance estimates were computed for 2008 and 2012 using line transect ship surveys data. The estimate obtained from the 2008 cruise data represents the best estimate for the size of the humpback whale population wintering off Brazil, because that survey covered the majority of the species range in their breeding grounds. That estimate suggests that there were nearly 16,400 whales off the Brazilian coast in 2008. The 2012 estimate, while higher, did not cover the total population range and therefore does not reflect its size in the wintering ground off Brazil.
Over the past 20 years, multiple surveys have been conducted in this wintering ground to estimate abundance of the western South Atlantic humpback whales (see a summary in
Survey | Platform | Region | Area (km2) | Year | N (%CV) | N 95% CI | GS (%CV) | Method | Reference |
---|---|---|---|---|---|---|---|---|---|
Vessel | Abrolhos bank | — | 1995 | 1,634 (9.5) | 1,379–1,887 | — | Mark-recapture | [ |
|
Vessel | Northern portion of the Abrolhos bank | — | 2000 | 3,871 | 2,795–5,542 | — | Mark-recapture | [ |
|
Vessel | Rio Grande do Norte to Sergipe | 20,040 | 2000 | 628 (33.5) | 327–1,157 | 1.95 (8.8) | Line transect | [ |
|
Airplane | Bahia and Espirito Santo | 86,225 | 2001 | 2,229 (31.3) | 1,201–4,137 | 1.52 (4.6) | Line transect | [ |
|
Airplane | Bahia and Espirito Santo | 81,103 | 2002 | 3,396 (14.2) | 2,562–4,501 | 1.52 | Line transect | [ |
|
Airplane | Bahia and Espirito Santo | 81,103 | 2003 | 3,661 (13.1) | 2,819–4,756 | 1.79 | Line transect | [ |
|
Airplane | Bahia and Espirito Santo | 81,103 | 2004 | 5,353 (12.8) | 4,146–6,913 | 1.57 | Line transect | [ |
|
Airplane | Rio Grande do Norte to Rio de Janeiro |
160,004 | 2005 | 6,404 (11.6) | 5,084–8,068 | 1.63 (1.7) | Line transect | [ |
|
Airplane | Rio Grande do Norte to Rio de Janeiro |
160,004 | 2008 | 9,330 (28.1) | 4,857–20,300 | 1.59 (6.9) | Line transect | [ |
|
Vessel | Rio Grande do Norte to Rio de Janeiro |
123,101 | 2008 | 16,410 (22.8) | 10,563–25,495 | 1.89 (2.5) | Line transect | Present study | |
Airplane | Sergipe to Rio de Janeiro | 130,546 | 2011 | 14,315 (28.7) | 8,257–24,818 | 1.679 (2.2) | Line transect | [ |
|
Vessel | Bahia and Espirito Santo(coastal shipping route) | 7,207 | 2011 | 382 (10.4) | 303–454 | 1.81 (3.4) | Line transect | [ |
|
Vessel | Bahia to Rio de Janeiro | 94,295 | 2012 | 19,429 (10.1) | 15,958–23,654 | 1.93 (2.5) | Line transect | Present study |
N = abundance; CV = coefficient of variation; CI = confidence interval; GS = mean group size.
aHumpback whales breeding range off the Brazilian coast. The larger survey area in studies 8 and 9 is explained by the inclusion of regions beyond the shelf-break in the southern portion of the area.
A comparison of ship and aerial surveys shows that the estimates of abundance computed from different survey platforms are substantially different, when equivalent time periods are considered. For example, the point estimate for the abundance from the 2008 ship survey in this study (16,410 whales) is 76% greater than that of the aerial survey conducted in the same year and approximately in the same area (9,330 whales; [
Assuming that the ship-based estimate presented here is accurate, the aerial is then biased low, which can be explained by a number of reasons. First, aerial surveys conducted using passing mode tend to underestimate group size. This is clearly visible in
For the aerial survey conducted off Brazil in 2008 (study 9,
The correction factor for availability bias computed by Andriolo et al. [
Another possibility to consider is that the aerial survey estimate is accurate and the 2008 ship survey is biased high. Overestimation of abundance could result from a number of reasons, but all are thought not to be a significant problem in the ship survey reported here. First, if sightings of unidentified whales, which estimates were combined with those of confirmed humpback whales, were in fact from other species, the estimate provided here would be biased high. However, no other large whales have been observed in large numbers in the survey area. For example, sightings of southern right whales (
Other sources of positive bias include the potential for double counting, which could occur in areas of high density where distinguishing new groups from those that had already been recorded could be difficult [
Although the differences between the WSA humpback whale abundance estimates in 2008 from the aerial and the ship surveys (
Even though we consider the abundance estimate computed from the 2008 shipboard survey the most representative for humpback whales wintering along the coast of Brazil, this estimate probably does not correspond the total population size. This occurs because areas along the northern coast of Brazil, north and/or west of 5°S, are used by an unknown, possibly small, number of humpback whales [
Regarding the approach of combining the estimated abundances for humpback whales and unidentified large whales adopted here, an alternative would be to consider the sightings from both as being of humpback whales and estimate the distance sampling parameters (i.e. detection probability, group size etc.) from combined detections. However, the present approach aims to clearly separate the contributions of abundance and variance estimates of humpback and unidentified whale sightings on the final (combined) abundance estimates, because of known biases on the unidentified whale data. For example, mean group sizes of unidentified whales are expected to be biased low because the same factors that prevented species identification may be responsible for inaccuracy on group size estimates (e.g. distance to detection and visibility conditions).
Abundance estimates provided here for comparable areas indicate that the number of humpback whales wintering off Brazil increased nearly 27% between 2008 and 2012. Because these estimates represent the majority of the population (i.e. abundance in blocks 8 to 15 in 2008 corresponded to 93% of the overall abundance) it is possible that the increase observed between these two years corresponds to the growth of the whole population from 2008 to 2012. Such an increase implies an average annual population growth rate of 6.1%, which is consistent with the point estimate of the rate of increase of 7.4%/year computed from sightings data for WSA humpback whales in the 1990s [
The estimates provided above also suggest that the recovery of this population is more optimistic than previously thought. Zerbini et al. [
The conservation status of WSA humpback whales is relatively optimistic when compared to other baleen whale populations around the world [
The authors wish to thank Universidade Federal de Rio Grande–FURG and the N/Pq Atlântico Sul crew for the support in field work. During the major development of this work, GA Bortolotto was a master’s degree student at the Universidade Estadual de Santa Cruz. The Research Group Ecologia e Conservação da Megafauna Marinha (EcoMega/CNPq) contributed to this study. Franciele Castro, Igor Morais, Jonatas Prado, Federico Sucunza, Marco Aurélio Crespo, Natália Mamede, Daniela Godoy, Suzana Stutz, Ygor Maia, Paulo Ott, Juliana Di Tullio and Janaína Wickert helped with data collection. The authors also thank the Brazilian Inter-Ministerial Commission for the Resources of the Sea (CIRM) for supplying the diesel for the ship for both surveys. Eric Rexstad provided valuable advices regarding data analysis. This manuscript was greatly improved thanks to the comments of Professor Philip Hammond and from two anonymous reviewers.