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- Materials and Methods
- Literature Cited
- Supporting Information
We contrast two methods for estimating the trends of bowhead whales (Balaena mysticetus) in West Greenland: (1) double platform visual aerial survey, corrected for missed sightings and the time the whales are available at the surface; and (2) a genetic capture-recapture approach based on a 14-yr-long biopsy sampling program in Disko Bay. The aerial survey covered 39,000 km2 and resulted in 58 sightings, yielding an abundance estimate of 744 whales (CV = 0.34, 95% CI: 357–1,461). The genetic method relied on determining sex, mitochondrial haplotypes and genotypes of nine microsatellite markers. Based on samples from a total of 427 individuals, with 11 recaptures from previous years in 2013, this resulted in an estimate of 1,538 whales (CV = 0.24, 95% CI: 827–2,249). While the aerial survey is considered a snapshot of the local spring aggregation in Disko Bay, the genetic approach estimates the abundance of the source of this aggregation. As the whales in Disko Bay primarily are adult females that do not visit the bay annually, the genetic method would presumably yield higher estimates. The studies indicate that an increase in abundance observed between 1998 and 2006 has leveled off.
Many baleen whale populations are recovering from significant declines due to past overexploitation (Best 1993, Wade et al. 2012). Nevertheless, there is a need to determine the rate of recovery to gain more detailed insight into the dynamics of the populations, which in turn provides the basis for stock management. One major problem with monitoring baleen whale populations is their ocean-wide distribution and the logistical difficulties associated with conducting informative surveys covering large areas. One approach is to monitor the abundance in restricted areas that are seasonally or periodically visited by whales. Conspicuous aggregations of whales gathered for feeding, breeding or other poorly understood activities may represent a reliable source for tracking population size and structure. One such area is Disko Bay in West Greenland with its seasonal occurrence of bowhead whales (Balaena mysticetus).
Bowhead whales are associated with polar pack ice, and inhabit waters at latitudes between about 54°N and 85°N (Moore and Reeves 1993). The International Whaling Commission (IWC) has recognized four mainly geographically defined stocks: (1) the Okhotsk Sea stock, (2) the Bering-Chukchi-Beaufort Seas (B-C-B) stock, (3) the Eastern Canada-West Greenland stock, and (4) the Spitsbergen stock (Heide-Jørgensen et al. 2006, Givens et al. 2010, IWC 2012). The Eastern Canada-West Greenland stock is estimated to consist of at least 7,000 animals, and is, like the B-C-B stock, substantially larger than the small Okhotsk Sea and Spitsbergen stocks (Reilly et al. 2012).
Bowhead whales between Greenland and Canada generally show annual migration patterns following the extent of the sea ice, with northwards movements as the ice recedes during spring and summer, and southwards migration with the expansion of seasonal ice in fall (Eschricht and Reinhardt 1861, Ferguson et al. 2010). Heide-Jørgensen et al. (2010) recently reviewed the sex and age-class segregation of Eastern Canada-West Greenland bowhead whales, and related the migration pattern of the eastern North American bowhead whales to their reproductive biology. In agreement with early whaling records (Southwell 1898), they hypothesized that primarily adult males and resting and pregnant females are found in Baffin Bay, while calves, subadults, and nursing females stay in Prince Regent Inlet, Gulf of Boothia, Foxe Basin, and northwestern Hudson Bay. Finley (2001) and Ferguson et al. (2010) argued that the main calving areas are in the Canadian High Arctic and the shallow waters of Foxe Basin, where sheltered areas may offer a refuge for young calves, minimizing the predation risk from killer whales as well as reducing the risk of ice entrapment.
Bowhead whales aggregate in Disko Bay during winter and spring (Eschricht and Reinhardt 1861) and are mainly observed in an area of about 25,000 km2 southwest of Disko Island (Heide-Jørgensen et al. 2007). Stafford et al. (2008) concluded that Disko Bay serves as a mating ground, which is supported by recordings of singing whales in the area (Tervo et al. 2009) along with observations of other sexual activity such as copulations (Eschricht and Reinhardt 1861). There are few observations of whales less than 14 m long in the area (Heide-Jørgensen et al. 2007), the length at which the bowhead whales are thought to be sexually mature (George et al. 1999). It is thus assumed that the aggregation primarily consists of adult whales. A further peculiarity of this aggregation is the skewed sex ratio, with an estimated fraction of females of 78% (Heide-Jørgensen et al. 2010).
After almost a century of virtual absence from Greenlandic waters, bowhead whales started to reappear in Disko Bay around year 2000 and have appeared in increasing numbers for several years (Reeves and Heide-Jørgensen 1996, Heide-Jørgensen et al. 2007). In 2006, the abundance of bowhead whales in Disko Bay was estimated at 1,229 individuals (CV = 0.47, 95% CI: 495–2,939) based on sightings during an aerial survey (Heide-Jørgensen et al. 2007). A genetic capture-recapture estimate of 1,410 individuals (CV = 0.23, 95% CI: 783–2,038) was obtained by Wiig et al. (2011), based on samples collected locally in Disko Bay during the period 2000–2010. The estimates provided by this genetic method apply to some unknown portion of the Eastern Canada-West Greenland stock from which the bowhead whales in Disko Bay originate.
The combination of two independent approaches for estimating the abundance of bowhead whales in West Greenland provides two different estimates that can inform management decisions. The aerial surveys allow for independent but comparable estimates of the instantaneous abundance obtained at regular intervals or as frequently as needed. The capture-recapture technique requires estimation over longer sampling and/or resampling periods to avoid dependence. Because the Disko Bay aggregation mainly consist of adult females without calves, it is likely that the individual whales do not visit the bay annually (Heide-Jørgensen et al. 2010). Thus, the genetic approach provides a better representation of the fraction of the population that supplies the local spring aggregation of bowhead whales in Disko Bay over multiple years, while the aerial survey estimates the number of whales present in the surveyed area during the study.
The objectives of this study were to assess if the previously recorded increase in abundance in Disko Bay has been continued and to compare the applicability of two methods to estimate the abundance of bowhead whales in the area: (1) an aerial survey conducted along the west coast of Greenland in March–April 2012 and (2) an extended genetic capture-recapture approach utilizing data collected annually in Disko Bay between 2000 and 2013.
- Top of page
- Materials and Methods
- Literature Cited
- Supporting Information
There are only few cases where both line transect and capture-recapture techniques for estimating abundance of large whales have been conducted on the same aggregation of whales. Although ocean-wide studies of humpback whales (Megaptera novaeangliae) have been conducted using both genetic and photographic capture-recapture techniques (e.g., Palsbøll et al. 1997, Smith et al. 1999) comparisons between sighting survey and capture-recapture estimates have only been reported on smaller regional scales (e.g., Calambokidis and Barlow 2004). Calambokidis and Barlow (2004) highlighted that capture-recapture techniques estimate the population regardless if all individuals are present within the study area at a particular moment, while line transect methodology estimates the density and abundance of the animals present in the given area at the time of the study. Given that not all bowhead whales visit Disko Bay annually, the genetic capture-recapture approach in the present study estimates the size of the fraction of the total population that supplies this local spring aggregation with whales. In contrast, the aerial survey provides an instantaneous abundance estimate of the aggregation itself. Therefore, the estimates from the two methods give different kinds of information and are not directly comparable.
The 2012 aerial survey of bowhead whales along the coast of West Greenland indicated that most individuals were found within a relatively restricted area southwest of Disko Island (strata 2 and 3 of the survey scheme). This survey largely covered the same areas covered in earlier surveys in 1981 and 2006 (Heide-Jørgensen et al. 2007) and is the core area used by bowhead whales in spring as determined by satellite telemetry (Heide-Jørgensen et al. 2003, Laidre and Heide-Jørgensen 2012). For the 2012 survey the combined sighting rate for strata 1 and 2 was 0.023 (CV = 0.31), which is similar to the estimate of 0.023 in 2006 for the same area.
However, the 2006 (1,229 individuals CV = 0.47, 95% CI: 495–2,939; Heide-Jørgensen et al. 2007) and the 2012 (744 individuals; CV = 0.34, 95% CI: 357–1,461) abundance estimates rely on slightly different analysis methods. The 2012 estimate was corrected for both the time animals are available to be detected and the time the whales are in view of the observers, whereas the 2006 survey was not corrected for the latter. Accordingly, the 2006 estimate was positively biased as compared to the 2012 estimate. The 2012 data can, however, be processed following the same analytical approach used for the 2006 estimate, generating comparable estimates. Doing so yields an abundance estimate in 2012 of 829 individuals (CV = 0.35; 95% CI: 425–1,618). This is 33% lower than the 2006 abundance estimate, and the range of the 2012 estimate is largely within the confidence interval of the 2006 estimate. The 2006 data suggested a significant increase in sighting rates of bowhead whales in West Greenlandic waters as compared to surveys conducted before year 2000 (Heide-Jørgensen et al. 2007), but further increase in sighting rates could not be detected in the 2012 survey.
Genetic Capture-recapture Approach
The genetic capture-recapture approach was used earlier for the Disko Bay spring aggregation in 2010 by Wiig et al. (2011), who estimated the source population size as 1,410 bowhead whales (CV = 0.23, 95% CI: 783–2,038) and 999 (CV = 0.23, 95% CI: 546–1,452) when analyzing the females only. As the confidence ranges of these estimates are largely overlapping with the estimates obtained in this study, we have not detected any change in source population size during the period 2009–2013 based on the genetic capture-recapture result alone (Table 4). This was not statistically tested due to possible dependence between the estimates (Fig. 3).
One of the major assumptions of the Chapman capture-recapture method is a closed population, i.e., that the effects of mortality, recruitment and migration are insignificant, and that N thus remains constant over the sampling period (Seber 1973). The longevity of bowhead whales of over 100 yr (George et al. 1999) makes an impact of mortality effects on the estimated size of the source population likely to be negligible, and as long as the marked and unmarked individuals have the same average probability of surviving until the second sampling occasion, the population size estimate is unaffected (Seber 1973). Earlier sighting rates of bowhead whales in the area indicated an increasing population (Heide-Jørgensen et al. 2007), and accordingly, N cannot be considered constant. In an increasing source population the proportion of marked individuals at the time of the second sampling will be lowered. Even though the initial population size thus would be overestimated, will be applicable to the stock at the time of the second sampling (Seber 1973). However, there might be a significant effect of migration, as discussed below.
A further assumption of the capture-recapture analysis is that all individuals have the same probability of being sampled and resampled. As the resampling was conducted in one year only, a possible multi-year cyclical pattern linked to female reproductive biology, in which the females may not visit the bay annually (Heide-Jørgensen et al. 2010, Wiig et al. 2011), must be considered. The analysis can be modified to overcome this bias to include the females’ cyclic returns, i.e., letting the resampling interval cover four years, while excluding within-period recaptures. Using the years between 2000 and 2009 as the initial sampling period and treating the sampling years of 2010–2013 as the resampling period, a similar yet more precise abundance estimate was obtained (for both sexes: 1,274 (CV = 0.12, 95% CI: 967–1,581), for females only: 1,012 (CV = 0.14, 95% CI: 738–1,286)). This approach maintains large sample sizes (>150) for both sampling and resampling. These estimates are within the range of the 2013 genetic abundance estimates, and the consistency of the results may indicate that the estimates of the population size of the source of the Disko Bay aggregation are reliable.
Temporal Changes in the Disko Bay Bowhead Aggregation
While the aerial surveys offer a temporary snapshot of the local spring aggregation in West Greenland, the genetic capture-recapture approach relates to the size of the source population based on a 14 yr sampling period. If not all individuals of the source population visit Disko Bay annually, the genetic estimate of the source population is expected to be higher than the aerial survey abundance estimate, which is valid only for the surveyed area in a single year. This fits well with our findings; the genetic capture-recapture estimate ( = 1,538) was about two-fold of the aerial survey estimate ( = 744).
Both approaches, however, provide information on only a fraction of the entire stock in the waters between eastern Canada and West Greenland. Calves are rarely seen in Disko Bay. The first confirmed observation of a bowhead whale calf in Disko Bay since the 1840s (Eschricht and Reinhardt 1861) occurred in Disko Bay on 20 April 2012 during the aerial survey. Given the absence of calves and a strongly skewed sex ratio, the aggregation presumably consists primarily of pregnant or postlactating females (Heide-Jørgensen et al. 2007). Applying the sex ratio to the aerial abundance estimate (744 × 0.789), we roughly estimated 590 of the whales in the 2012 Disko Bay spring aggregation were females. This corresponds to ~50% of the adult female part of the source population, based on the genetic abundance estimate (1,212 females (CV = 0.27, 95% CI: 574–1,851)). If the occurrence in the bay is tied to the reproductive cycle of the females, cyclic returns of the females may be expected (Heide-Jørgensen et al. 2010, Wiig et al. 2011). Assuming a 3 or 4 yr reproductive cycle (Koski et al. 1993), this pattern may arise if adult female bowhead whales visit the bay in resting and gestation years, while giving birth and spending the lactation period elsewhere. Some of the mature females in the area are indeed reproductively active as newly pregnant females and a near-term pregnancy were found among the animals taken during the subsistence hunt in Disko Bay since 2009 (Heide-Jørgensen et al. 2012a). During the aerial survey in March–April 2012, six possible mating events with three or more closely interacting whales were observed (Fig. S1). Because Disko Bay is a region of high productivity (Laidre et al. 2007), it is likely that the area is used both as a mating and as a feeding ground (Heide-Jørgensen et al. 2010).
It is generally accepted that commercial whaling prior to 1815 greatly reduced the bowhead whale stock, and that termination of industrial whaling enabled restoration of prewhaling stock sizes (Zeh et al. 1993, Finley 2001). Even though ecosystem shifts could pose limitations on the exploited bowhead whale stocks and may lead to a time lag in the recovery (Hacquebord 1999, Clapham et al. 2008), the estimated population size implies that the stock has expanded from the assumed low abundance in the 20th century. The abundance estimates obtained since year 2000 are in sharp contrast to those obtained in earlier attempts to estimate abundance of bowhead whales in West Greenland. Reeves et al. (1983) and Zeh et al. (1993) indicated that the former Baffin Bay-Davis Strait stock consisted of only “a few hundred” whales. However, we now assume that bowhead whales in eastern Canada and West Greenland belong to one stock, with an estimate of over 7,000 whales (Reilly et al. 2012). The predicted population growth rates for the species (i.e., 3.4%; George et al. 2004) are too low to explain the increase observed in Disko Bay at the turn of this century, which may also be caused by immigration. A persistent retreat of sea ice could facilitate an influx of individuals to Disko Bay from the expanding B-C-B stock through the opening of the Northwest Passage (George et al. 2004, Heide-Jørgensen et al. 2012b). Whether site-fidelity (Reeves et al. 1983; Finley 1990, 2001) or a “cultural memory” (see Clapham et al. 2008) could prevent such movements is not known, but improved access to Arctic straits would likely lead to increased migration between the stocks.
Because all estimates of population size are based on geographically restricted sampling, they are sensitive to changes in migration patterns of the stock. Reduced sea ice and thus extended access to coastal foraging areas and changes in the primary production could be alternative reasons for the increased sightings of bowhead whales in certain areas since the turn of this century (Heide-Jørgensen et al. 2007). Plasticity in the migration of bowhead whales (Heide-Jørgensen et al. 2006) may thus be responsible for the sudden increase in abundance in Disko Bay.
The result of the capture-recapture study compared to the stock size in 2002–2004 (i.e., over 7,000 bowhead whales (Reilly et al. 2012)) indicates that the size of the Eastern Canada-West Greenland stock of bowhead whales has been high during the whole period 2002–2013. The latest estimate from the aerial surveys in West Greenland indicates that the abundance of bowhead whales has stabilized in Disko Bay after the dramatic increase in numbers documented in the early 2000s (Heide-Jørgensen et al. 2007). The cause for the sudden appearance of large numbers of bowhead whales by the turn of the century remains unknown. One reason may be the availability of prey. Laidre et al. (2007) concluded that the total biomass of zooplankton in the upper 50 m of the water column in Disko Bay theoretically could support the predation level of bowhead whales in the area. However, bowhead whales leave the Disko Bay area before the peak in the zooplankton bloom, and we therefore believe that limited food availability is not the main explanation for variability in abundance. Future monitoring of bowhead whales in West Greenland may help answer this question.
The present study is one of few studies of large whales with two independent abundance estimates for the same population. The two abundance estimates are complementary as the aerial survey provides snapshots that are useful for examining local trends without dependence between years, whereas the genetic capture-recapture approach allows for estimating the size of the actual source population. However, it is less suited for time series estimates as it requires samples over many years in both the marked and recaptured samples. The two approaches have different merits and do not necessarily lead to identical estimates, but when used in combination give valuable insight into trends affecting abundance and the fraction of the population that is present within the surveyed area.