Estimation of Harp Seal (Pagophilus Groenlandicus) Pup Production in the North Atlantic Completed: Results from Surveys in the Greenland Sea in 2002

ICES Journal of Marine Science, 63: 95e104 (2006) doi:10.1016/j.icesjms.2005.07.005

Estimation of harp seal (Pagophilus groenlandicus) pup production in the North Atlantic completed: results from surveys in the Greenland Sea in 2002

Tore Haug, Garry B. Stenson, Peter J. Corkeron, and Kjell T. Nilssen Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021

Haug, T., Stenson, G. B., Corkeron, P. J., and Nilssen, K. T. 2006. Estimation of harp seal (Pagophilus groenlandicus) pup production in the North Atlantic completed: results from surveys in the Greenland Sea in 2002. e ICES Journal of Marine Science, 63: 95e104.

From 14 March to 6 April 2002 aerial surveys were carried out in the Greenland Sea pack ice (referred to as the ‘‘West Ice’’), to assess the pup production of the Greenland Sea population of harp seals, Pagophilus groenlandicus. One fixed-wing twin-engined aircraft was used for reconnaissance flights and photographic strip transect surveys of the whelping patches once they had been located and identified. A helicopter assisted in the reconnaissance flights, and was used subsequently to fly visual strip transect surveys over the whelping patches. The helicopter was also used to collect data for estimating the distribution of births over time. Three harp seal breeding patches (A, B, and C) were located and surveyed either visually or photographically. Results from the staging flights suggest that the majority of harp seal females in the Greenland Sea whelped between 16 and 21 March. The calculated temporal distribution of births were used to correct the estimates obtained for Patch B. No correction was considered necessary for Patch A. No staging was performed in Patch C; the estimate obtained for this patch may, therefore, be slightly negatively biased. The total estimate of pup production, including the visual survey of Patch A, both visual and photographic surveys of Patch B, and photographic survey of Patch C, was 98 500 (s.e. Z 16 800), giving a coefficient of variation of 17.9% for the survey. Adding the obtained Greenland Sea pup production estimate to recent estimates obtained using similar methods in the Northwest Atlantic (in 1999) and in the Barents Sea/White Sea (in 2002), it appears that the entire North Atlantic harp seal pup production, as determined at the turn of the century, is at least 1.4 million animals per year. Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. Keywords: abundance, aerial surveys, birth distribution, Greenland Sea, harp seal, pup production. Received 6 July 2004; accepted 23 July 2005. T. Haug, P. J. Corkeron, and K. T. Nilssen: Institute of Marine Research, PO Box 6404, N- 9294 Tromsø, Norway. Current address for P. J. Corkeron: Bioacoustics Research Program, Cornell Laboratory of Ornithology, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA. G. B. Stenson: Science Branch, Department of Fisheries and Oceans, Northwest Atlantic Fisheries Centre, PO Box 5667, St. John’s, Newfoundland, Canada A1C 5X1. Correspondence to T. Haug: tel: C47 776 09722; fax: C47 776 09701; e-mail: [email protected].

Introduction examined using cranial measurements (Yablokov and Sergeant, 1963), underwater vocalizations (Perry and Three populations of harp seals, Pagophilus groenlandicus, Terhune, 1999), serum transferrins (Møller et al., 1966; inhabit the North Atlantic Ocean (Sergeant, 1991). Whelp- Nævdal, 1966, 1969, 1971), blood serum proteins (Borisov, ing occurs on the pack ice off eastern Newfoundland and in 1966), allozymes (Meisfjord and Nævdal, 1994), and DNA the Gulf of St. Lawrence (the Northwest Atlantic (Meisfjord and Sundt, 1996; Perry et al., 2000). These population), off the east coast of Greenland (the Greenland studies have revealed significant differences between the Sea or West Ice population), and in the White Sea (the Northwest Atlantic population on the one side and the Barents Sea/White Sea population). Relationships among Greenland Sea and Barents Sea harp seal populations on the three North Atlantic populations of harp seals have been the other, while no evidence of difference between the latter

1054-3139/$32.00 Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved. 96 T. Haug et al. two was observed. Recent observations from satellite tagging production should be conducted periodically, preferably experiments suggest that Greenland Sea and Barents Sea with 5 or less years between two consecutive surveys, and harp seals overlap in their feeding range during summer and that efforts should be made to ensure comparability of autumn (JuneeOctober) in the northern Barents Sea (Folkow survey results (ICES, 1994, 2004; NAFO, 1995). et al., 2004). Also, recaptures from tagging experiments, Recent estimates of harp seal pup production are available using traditional flipper tags, suggest that mixing of for the Northwest Atlantic (997 900, s.e. Z 102 100, obtained immature animals between the West Ice and Barents Sea in 1999; Stenson et al.,2003) and Barents Sea/White Sea populations may occur, but there is no evidence of mixing on (330 000, s.e. Z 34 000, obtained in 2002; ICES, 2004) pop- the breeding grounds (Øien and Øritsland, 1995). ulations. Subsequent assessments, done by fitting population Estimating abundance and monitoring changes in models to the independent estimates of pup production (e.g. population size is critical for the management of harp Healey and Stenson, 2000; ICES, 2001, 2004), suggest that Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 seals and to understand their role in the North Atlantic the total size of these two populations combined may now be ecosystem. Harp seals are the most abundant pinniped in approximately 7.5 million animals. There are no current the North Atlantic, where they are the focus of the largest estimates of harp seal pup production in the Greenland Sea. marine mammal harvest in the world. Although the three Greenland Sea harp seals were surveyed aerially in 1991, populations have historically been exploited and managed giving a combined estimate of 55 270 (CV 0.141) pups for separately, the combined total reported harvest (conducted four detected and surveyed patches (Øritsland and Øien, by Canada, Greenland, Norway, and Russia) in 2002 was 1995). Obtaining updated information on pup production is approximately 450 000 animals (ICES, 2004). Thus, there needed to assess the status of the Greenland Sea harp seal is considerable interest in assessing the status and population. Consequently, aerial surveys were carried out monitoring changes in abundance in all three populations in 2002 during their whelping (pupping) period (Marche in order to manage the respective harvests responsibly. In April). The surveys were carried out using techniques addition, knowledge of harp seal population size is one similar to those developed and used previously to determine factor required in order to estimate the potential influence pup production for harp seals in the Northwest Atlantic of this species on other marine organisms, including (Stenson et al., 1993, 2002, 2003), in the Greenland Sea commercially important fish species. Harp seals are (Øritsland and Øien, 1995), and in the White Sea (Potelov important predators, and may also play a role in et al., 2003; ICES, 2004). Standardization of methodology structuring ecosystems, both in the Northwest (Hammill and interpretation of results were achieved by involving and Stenson, 2000; Bundy, 2001) and Northeast (Nilssen scientists from Canadian, Norwegian, and Russian institu- et al., 2000) Atlantic. For example, in Atlantic Canada tions in both fieldwork and subsequent analyses of data. waters harp seals accounted for over 80% of the estimated Although there were some small differences between surveys, 4 million tonnes of fish and zooplankton consumed by all the results from all areas are comparable and facilitate an seal species in the area (Hammill and Stenson, 2000). updated ‘‘turn-of-the-century’’ estimate of the total pup Annual consumption by Barents Sea/White Sea harp seals production of harp seals in the entire North Atlantic based on was calculated by Nilssen et al. (2000) to be of sampling over a restricted time period (1999e2002). a magnitude of 3.5 million tonnes, of which various fish species constituted well over 2 million tonnes e an amount comparable with the quantities of fish consumed Material and methods annually by cod Gadus morhua, the main upper-level predator of the Barents Sea (Bogstad et al., 2000). Reconnaissance surveys Due to uncertainties in the assumptions required when Whelping concentrations were located using fixed-wing and estimating abundance from catch-at-age data and sequential helicopter reconnaissance surveys of areas historically used population models, total abundance of a population is by harp and hooded seals in the Greenland Sea, mainly the estimated by fitting a population model using age-specific pack ice areas along the eastern coast of Greenland between reproductive rates and catches to the independent estimates 67(30#N and 74(40#N(Figure 1). Surveys were carried out of pup production (e.g. ICES, 2004). Although mark- between 14 March and 5 April 2002 at altitudes between recapture techniques have been used previously (e.g. 800 and 1000 ft. Reconnaissance flights using the fixed- Bowen and Sergeant, 1983; Øien and Øritsland, 1995), wing aircraft were generally flown as repeated systematic the use of aerial photographic and visual surveys represents eastewest transects spaced 10 nm apart, from the ice edge an alternative and industry independent approach to in the east into the dense drift ice closer to the Greenland estimate harp seal pup production that has been used shore. Due to ice drift and variation in pupping dates (mid to successfully both in the Northwest Atlantic (Stenson et al., late March, see Øritsland and Øien, 1995), most areas were 1993, 2002, 2003), in the Greenland Sea (Øritsland and surveyed repeatedly to minimize the chance of missing Øien, 1995), and in the White Sea (Potelov et al., 2003; whelping concentrations. Colour markers and VHF trans- ICES, 2004). It is recommended that the comprehensive mitters were deployed in major whelping concentrations to aerial surveys needed to provide estimates of current pup facilitate relocation and to monitor ice drift. Estimation of harp seal pup production in the Greenland Sea 97 Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021

Figure 1. Survey area in the Greenland Sea: shaded area indicates where fixed-wing reconnaissance surveys were flown from 14 March to 5 April 2002. Visual survey transects flown by helicopter over harp seal whelping Patches A (20 March 2002) and B (28 March 2002), and photographic survey transects flown by fixed-wing aircraft over harp seal whelping Patch C (6 April 2002) are indicated with parallel lines.

Estimates of abundance horizon and bottom of the window, were used to maintain Visual surveys a constant position. The actual strip width was determined The number of pups present within the identified whelping once the observers had undergone extensive practice runs patches was estimated by conducting systematic visual strip and developed a consistent position. The strip widths, e transect surveys, flown using a ship-based helicopter at an originally aimed to be 30 35 m for each observer, were altitude of 30 m (100 ft). The helicopter was fitted with calibrated against known distances on the ground after the a satellite navigation system (GPS) and radar altimeter to surveys, and proved to be 30 and 34 m for the two ensure correct navigation and consistent altitude during observers, respectively. The observers counted all pups surveys. The same two observers were used in all surveys, occurring within their stripe on each side of the aircraft, one always seated in the left and the other in the right rear giving a total strip width of 64 m for the visual transects. seats. Their observational position in the helicopter was Each pup observation was recorded directly into a laptop by fixed to ensure standardization of strip widths. Each individual observers and identified with a GPS location on observer aligned marks on the window with a known the helicopter track. The transect began before a navigator, distance on the ice. Additional marks, to indicate the seated in the front, encountered seals and was terminated 98 T. Haug et al. when no seals were seen on transect and were not observed i.e. the number of pups present on a photograph agreed outside the survey area. The direction of, and spacing upon by the readers, after a comparison of multiple between, transects depended on orientation and size of the readings by the four different readers. Any pup that could concentration. Transects were carried out at right angles to not be positively identified was not included. Original the main orientation of the concentration. The subsequent counts (x) were regressed on the ‘‘best estimate’’ (y) to data analyses were the same as used for the photographic determine a correction factor for each survey and reader. surveys, assuming complete coverage along a transect (see Individual photo counts were corrected using the appropri- Stenson et al., 1993). ate regression for each reader. The measurement error associated with variation about the regression was estimated, summed over transects to estimate the total measurement

Photographic surveys Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 error for the survey, and added to the sampling variance, Fixed-wing aerial photographic surveys were flown using following Stenson et al. (2003). a PA31 Piper Navajo fitted with the gyro mounted Leica For the reader who examined Patch B, the equation was: RC 30 camera with 15.3 cm lens and AGFA PAN 200 y Z 0.9778x (s.e. Z 0.01132); and for the reader who read aerographic black-and-white film. The surveys were mainly Patch C, the equation was y Z 1.1246x (s.e. Z 0.01889). conducted at an altitude of 191 m (includes the entire Patch The different regression coefficients between the two B), but due to low ceilings most transects were carried out patches reflect differences in flying altitude, weather at lower altitudes (some as low as 138.5 m) in Patch C. To condition, ice condition, and different readers. avoid variations along transects, altitudes were monitored Measurement error associated with variation about the continuously during the entire photographic survey. The regression (V ) was estimated for each photograph images covered areas varying from 284.1 ! 284.1 m to photo using: 206.2 ! 206.2 m per photo at altitudes of 191 m and 138.5 m, respectively. Each transect was allocated coverage XZ Z ! 2 according to flying altitude. Photos were taken along each Vphotoj Vslope tjz transect at time intervals separated sufficiently to avoid zZ1 overlap. The camera was turned on when seals were where t is the uncorrected number of pups on photo z of observed on a transect line, turned off if open water transect j; j the transect number; and Z is the number of occurred for an extended period along a transect, and turned photos on the transect. on when ice was encountered again. The photography on a transect line was finished when no seals were observed. Survey analysis Correct altitude and transect spacing were maintained using radar altimeter and a satellite navigation system (GPS). Both visual and photographic surveys were based on a systematic sampling design with a single random start and a sampling unit of a transect of variable length. Data were Photographic counts analysed based on the methods outlined in Stenson et al. Positive prints were examined by two readers. Each frame (1993, 2002, 2003) and summarized here. e ! was examined using an illuminated hand-lens (7 8 The estimated number of pups for the i(th) survey is magnification). Readers examined a common series of given by photographs and compared seals identified with a reader with extensive previous experience. Once the cues used to XJi ^ Z identify seals were consistent among readers, all photos Ni ki xi jZ1 were read once. For each photograph the number and position of all pups were recorded on a clear acetate overlay. where Ji is the number of transects in the i(th) survey; ki the After all photographs were read, the readers re-read weighting factor for the i(th) survey determined by dividing a series of their photographs in sequence to determine if the transect interval by the transect width; and xj is the identifications had improved over the course of the readings number of pups on the j(th) transect. The estimates of the (i.e. the ‘‘learning curve’’). Photos were read until the number of pups along a transect could not be corrected for second readings were consistently within 1% of the first. The areas that were not surveyed. original readings were replaced with the second readings up The estimates of error variance (Vsi ), based on serial to this point. Additional photos were read subsequently to differences between transects (Kingsley et al., 1985), were ensure that the first and second readings were consistent. calculated as To correct for misidentified pups, 50 randomly selected XJi1 frames from each whelping concentration were examined kiðki 1ÞJi 2 V Z x x C1 by four readers; the two original readers intended to read si j j 2ðJi 1Þ jZ1 the entire material, plus two additional experienced readers. Individual seals identified by each reader were compared to Variance associated with the mis-identification corrections determine a ‘‘best estimate’’ of the number of pups present, (Vphotoj ) was summed over transects and multiplied by the Estimation of harp seal pup production in the Greenland Sea 99 weighting factor (ki) to estimate the total measurement where the estimates of the mean and standard deviation of error for the survey, and added to the sampling variance stage lengths were as given by Kovacs and Lavigne

(Vsi ) to obtain the variance of a given survey (Vi): (1985). From these resampled estimates of birth date, all random draws born prior to midday of the day the survey XJi (visual and/or photographic) was performed, were V ZV Ck V i si i photoj counted. For each survey of each patch, counts were Z j 1 made of the number of random draws ‘‘born’’ both before P ^Z I and after this date. A correction factor was derived by The total populationP was estimated as N iZ1 Ni and ^Z I dividing the total number of randomized dates of birth by its error variance V iZ1 Vi, where I is the number of surveys. the number of randomized dates of birth that were estimated to have taken place prior to the survey. The Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 original estimated number of pups from a survey was then Temporal distribution of births multiplied by this proportion to give a corrected estimate To correct the estimates of abundance for pups that had left of all pups born in each patch. An approximate estimate the ice or were not yet born at the time of the survey (Myers of variance for multipliers was obtained by estimating the and Bowen, 1989; Stenson et al., 1993, 2002, 2003), it was range of birth estimates that occurred during the course of necessary to estimate the distribution of births over the the survey (taken as 4 h). This variance estimator was pupping season. This was done using information on the incorporated into the overall variance following Stenson proportion of pups in each of seven distinct age-dependent et al. (2003). stages. These arbitrary, but easily recognizable age categories were based on pelage colour and condition, overall appearance, and muscular coordination, as de- Results scribed for Northwest Atlantic harp seals by Stewart and Lavigne (1980): Identification of whelping areas Two harp seal whelping concentrations, one small and one (i) Newborn: Pup still wet, bright yellow colour often large, apparently in the very beginning of formation, were present. Often associated with wet placentas and observed during a fixed-wing reconnaissance flight on 15 blood-stained snow. March in the area between 72(37#Ne72(43#N and (ii) Yellowcoat: Pup dry, yellow amniotic stain still 10(03#We12(22#W. Both patches were subsequently persistent on pelt. The pup is lean and moving relocated during helicopter reconnaissance flights. A small awkwardly. patch (Patch A, Figure 1) was found on 17 March at an (iii) Thin whitecoat: Amniotic stain faded, pup with approximate mean position of 72(14#N/12(43#W and visible neck and often conical in shape, pelage white. a VHF transmitter was deployed in the patch to monitor (iv) Fat whitecoat: Visibly fatter, neck not visible, movements which were generally in a southwesterly cylindrical in shape, pelage still white. direction. On 30 March, this patch was relocated at (v) Greycoat: Darker juvenile pelt begin to grow in under 70(52#N/14(11#W. A larger harp seal concentration the white lanugo giving a grey cast to the pelt; ‘‘salt- (Patch B, Figure 1) was located on 20 March near position and-pepper’’-look in later stages. of 72(10#N/13(10#W. This patch also drifted to the (vi) Ragged-jackets: Lanugo shed in patches, at least southwest. On 5 April, a third harp seal whelping a handful from torso (nose, tail, and flippers do not concentration (Patch C, Figure 1) was located during count). a fixed-wing reconnaissance flight between 69(00#N/ (vii) Beaters: Fully moulted, weaned pups (a handful of 19(52#W and 69(11#N/19(35#W. The known movement lanugo may remain). of the ice and other patches indicated that this group was separate from the previously identified patches. Very few Prior to the survey, classifications of pup stages were harp seals were observed outside the whelping concen- standardized among observers to ensure consistency. To trations. determine the proportion of pups in each stage on a given day, random samples of pups were obtained by flying a series of transects over the patch. Pups were classified Temporal distribution of births from the helicopter hovering just above the animals. The Estimates of the proportion of pups in each developmen- spacing between transects depended on the size of the tal stage were obtained from Patches A and B. Systematic actual patch. Repeated classifications were obtained from eastewest staging transects (spaced 1e3 nautical miles each patch several days apart. apart) were flown over Patch A on 17, 19, 21, and 30 For each pup observed on staging flights, a set of March, and over Patch B on 22, 24, 27, and 29 March randomized dates of birth were generated for each pup, and on 2 April (Table 1). Prior to the visual and taking 100 random draws from a normal distribution photographic surveys, newborns (stage 1) were absent 100 T. Haug et al.

Table 1. Number of harp seal pups in individual age-dependent stages in two whelping patches (A and B) in the Greenland Sea during March/April 2002.

Stage

Thin Fat Grey Ragged Date Patch New Yellow whitecoat whitecoat coat jacket Beater Total

March 17 A 0 18 73 0 0 0 0 91 19 0 3 144 0 0 0 0 147 21 0 2 256 23 0 0 0 281 30 00 4 24600088Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 March 22 B 54 303 1 513 0 0 0 0 1 870 24 1 81 879 7 0 1 0 969 27 4 28 424 1 135 111 2 0 1 704 29 0 4 122 810 32 1 0 969 April 2 0 0 1 38 711 3 0 753

while yellowcoats (stage 2) occurred in low numbers in No staging was carried out in Patch C and therefore no the patches. No newborns were observed after the surveys correction could be attempted. were flown. The majority of pups present during and immediately after the estimation survey periods were thin whitecoats (stage 3) in Patch A and fat whitecoats (stage Visual surveys 4) in Patch B. Systematic visual strip transect surveys were flown over The 100 random draws for each sighted pup resulted in Patch A on 20 March (Figure 1). The whelping concentra- 60 700 estimates for dates of pup births in Patch A and tion occupied an area between approximately 625 800 estimates for Patch B. From these estimates of 71(41#Ne71(50#N and 11(40#We12(50#W. Eighteen birth date, all random draws born prior to midday on the eastewest transects were flown spaced 0.5 nautical mile days the surveys were run were counted. The number of apart. A total of 277 harp seal pups was counted on random draws ‘‘born’’ just after midday on the day of the transects within a 64-m-wide strip (Table 2). This gave survey was counted also, and the midpoint of these used a total estimated number of 4008 (s.e. Z 706). Including as the time when the visual survey occurred. This resulted the correction for the temporal distribution of births, the in a correction of an additional 16.9% (Patch A) and 0.8% number of pups in Patch A estimated from the visual survey (Patch B) of the pups being born after the visual survey. was 4686 (s.e. Z 707) during the survey. No correction was necessary on the day of the Patch B was surveyed on 28 March when the patch photographic survey of Patch B. An approximate estimate occupied an area between approximately 71(13#Ne71( of variance for multipliers was obtained by estimating the 43#N and 14(38#We16( 30#W(Figure 1). Sixteen east- range of birth estimates that occurred during the course of ewest transects were flown spaced 2 nautical miles apart. In the survey (taken as 4 h). This variance estimator was total, 1416 pups were counted on the 64-m-wide transect strip incorporated into the overall variance following Stenson (Table 3). The estimated number of pups in Patch B was et al. (2003). 81 955 (s.e. Z 16 711). Including the correction for the The applied method only looks at the possibility of temporal distribution of births, the number of pups in Patch B births after the survey, and does not account for the estimated from the visual survey was 82 615 (s.e. Z possibility that pups have left. Pups do not appear to 16 711). leave the area before they get to the ragged jacket and Visual surveys were not flown over harp seal Patch C. beater stage. Younger pups appear to be on the ice most of the time e some may move among ice pans, but they tend to travel on the surface where they are seen by the Photographic surveys visual and photographic readers. A small number of Harp seal whelping Patch A was not surveyed photograph- ragged jackets were observed in Patch B, which suggests ically. A survey of Patch B (occupying an area between that a few could have gone into the water. However, the 70(52#Ne71(25#N and 14(44#We16(38#W) was suc- shape of the birth curve, given the timing of harp seal cessfully completed on 29 March (Figure 1). Twenty pups’ moulting, suggested that if any pups left the transects were flown in an eastewest direction, spaced whelping patch prior to either survey, the number would 2 nautical miles apart (Table 4). A total of 5220 pups was be minor. counted on the 521 exposures obtained. Correcting for Estimation of harp seal pup production in the Greenland Sea 101

Table 2. Number of harp seal pups counted on eastewest transects 69(01#Ne69(14#N and 19(06#We19(51#W. A total of obtained during a helicopter ﬂown visual survey of the Patch A 321 exposures was taken, and 1282 pups were counted whelping concentration in the Greenland Sea on 20 March 2002. (Table 5). Including the correction for reader errors, but not for pups born outside of photographs along a transect, Longitude Longitude Pups a total of 11 166 (s.e. Z 1202) was estimated to have been Transect Latitude start ﬁnish counted born.

1 71(41.0#N12(9.98#W12(46.76#W1 ( # ( # ( # 2 71 41.5 N1210.48 W1246.13 W6Estimate of total pup production for 2002 3 71(42.0#N12(10.62#W12(43.412#W6 4 71(42.5#N12(43.44#W12(10.94#W7Although a photographic estimate was available for Patch 5 71(43.0#N12(43.74#W12(9.92#W10B, it was incomplete since it did not account for pups born Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 6 71(43.5#N12(10.74#W12(36.55#W32between the photographs along the transect and therefore 7 71(44.0#N12(40.30#W12(8.28#W22was negatively biased. Therefore, combining visual survey ( # ( # ( # 8 71 44.5 N128.29 W1233.44 W18estimates of Patches A and B and the photographic estimate ( # ( # ( # 9 71 45.0 N1231.50 W127.06 W25of Patch C resulted in a total estimate of pup production of 10 71(45.5#N12(7.68#W12(26.77#W6 98 467 (s.e. Z 16 769, CV Z 17.0%, Table 6). 11 71(46.0#N12(28.84#W12(6.74#W2 12 71(46.5#N11(46.26#W12(18.00#W56 13 71(47.0#N12(16.53#W11(45.38#W46 14 71(47.5#N11(45.93#W12(17.87#W23Discussion 15 71(48.0#N12(16.26#W11(45.87#W9 16 71(48.5#N11(42.59#W12(17.10#W6The survey used methods comparable with those applied in 17 71(49.0#N12(16.24#W11(45.90#W2previous surveys performed for harp seal assessments in the 18 71(49.5#N11(47.56#W12(18.79#W0Northwest Atlantic in 1990, 1994, and 1999 (Stenson et al., 1993, 2002, 2003), in the Greenland Sea in 1991 (Øritsland and Øien, 1995), and in the White Sea in 1998, 2000, and reader errors, but not for pups born outside the photographs 2002 (Potelov et al., 2003; ICES, 2004). Additionally, the along a transect, pup production was estimated to be 66 545 survey and analysis methods were standardized with (s.e. Z 13 534). researchers who have carried out previous harp seal surveys The harp seal whelping Patch C was surveyed with to ensure that the results were comparable. The estimate photographic strip transects on 6 April in relatively difficult presented here (98 467, s.e. Z 16 769) is slightly negatively weather conditions (Figure 1). However, 14 eastewest biased owing to the lack of correcting for non-overlapping transects, spaced 1 nautical mile apart, were flown over photographs and areas where the camera was turned off the whelping patch, which covered an area between during the photographic survey of Patch C. Along transects, the camera was turned off in areas with open waters, i.e. Table 3. Number of harp seal pups counted on eastewest transects where there was no habitat (ice) and, therefore, no seals. obtained during a helicopter flown visual survey of the Patch B Unfortunately, the exact areas where the camera was turned whelping concentration in the Greenland Sea on 28 March 2002. off were not properly recorded, so the estimate could not be corrected for pups present on ice between photographs Longitude Longitude Pups while the camera was still on. However, given the relatively Transect Latitude start finish counted small number of seals present in this whelping patch, this correction is not likely to change the total estimate ( # ( # ( # 1 71 15 N1629.71 W167.00 W64significantly. Similarly, although the late date of the survey 2 71(13#N16(1.21#W16(10.82#W34 suggests that most of the pups had been born before the 3 71(17#N16(30.74#W15(53.40#W 108 4 71(19#N15(32.56#W16(26.24#W9survey of Patch C, where no staging was performed, it is 5 71(21#N16(18.59#W15(14.10#W34possible that some pups had left the ice. Therefore, the 6 71(23#N15(19.66#W16(6.31#W 134 estimate from Patch C may be further underestimated 7 71(25#N16(5.08#W15(16.31#W40slightly. 8 71(27#N15(14.33#W15(58.33#W 322 The photographic survey of Patch B was also negatively 9 71(29#N15(56.30#W15(9.22#W 343 biased for the same reasons as Patch C. Since a complete 10 71(31#N15(5.76#W15(49.37#W 142 visual survey was available, the photographic survey was ( # ( # ( # 11 71 33 N1549.70 W1438.43 W 118 not used. However, applying a range of reasonable ( # ( # ( # 12 71 35 N1439.52 W1523.48 W51correction factors to the photographic estimate resulted in 13 71(37#N15(17.91#W14(35.02#W15 estimates that were consistent with the visual survey 14 71(39#N14(39.46#W15(14.68#W0 15 71(41#N15(10.94#W14(38.15#W2results. 16 71(43#N15(10.94#W14(38.15#W0In general, surveys of ice-breeding seals are designed to obtain a minimum of one good estimate for each whelping 102 T. Haug et al.

Table 4. Number of photographs obtained during eastewest transects during a complete ﬁxed-wing survey of the harp seal Patch B whelping concentration in the Greenland Sea on 29 March 2002. A total of 521 exposures was taken. Estimates were not corrected for pups present on the ice between photographs along the transect.

Transect Latitude Longitude (W) start Longitude (W) ﬁnish Pups counted No. of photographs

1 70(49#N16(38#W16(30#W010 2 70(51#N16(35#W16(46#W 270 14 3 70(53#N16(38#W16(20#W 182 22 4 70(55#N16(24#W16(37#W3615 5 70(57#N16(34#W16(02#W 184 37 6 70(59#N15(58#W16(30#W7518Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 7 71(01#N16(33#W16(02#W 156 29 8 71(03#N15(47#W16(12#W4124 9 71(05#N16(01#W15(30#W 250 39 10 71(07#N15(37#W16(16#W 636 44 11 71(09#N16(03#W15(08#W 569 57 12 71(11#N15(12#W15(51#W 586 30 13 71(13#N15(49#W15(06#W 1 379 49 14 71(15#N15(10#W15(48#W 267 37 15 71(17#N15(25#W14(52#W 185 28 16 71(19#N14(58#W15(17#W7918 17 71(21#N15(11#W14(54#W 260 19 18 71(23#N14(42#W15(07#W5723 19 71(25#N14(56#W14(44#W88 20 71(27#N14(54#W15(08#W00 patch. In this study, good visual coverage was obtained for conditions in a particular year (see Stenson et al., 1993, two patches (A and B) and a photographic survey of Patch 2002, 2003). Given the uncertain and extremely variable C. Which technique is the most useful is not known until conditions (such as unpredictable weather and ice drift) the survey is actually done. When more than one survey is usually encountered when harp seal pups are to be available for a patch, and there is no obvious reason to surveyed, preparations must always be made to carry out reject one, a combined estimate is obtained from the both methods wherever possible. Results will subsequently average, weighted inversely by their variance. This determine which has the most inﬂuence in a given survey. approach is similar to harp seal surveys in the Northwest The Greenland Sea stocks of harp seals have been subject Atlantic where visual and photographic methods have to commercial exploitation for centuries (Iversen, 1927; contributed diﬀerently, depending upon the logistics and Nakken, 1988; Sergeant, 1991). Knowledge of the Greenland

Table 5. Number of photographs taken on eastewest transects during a complete ﬁxed-wing survey of the harp seal Patch C whelping concentration in the Greenland Sea on 6 April 2002. A total of 321 exposures was taken. Estimates were not corrected for pups present on the ice between photographs along the transect.

Transect Latitude Longitude (W) start Longitude (W) ﬁnish Pups counted No. of photographs

1 69(14#N19(07#W19(23#W5618 2 69(13#N19(06#W19(20#W6216 3 69(12#N19(15#W19(32#W4714 4 69(11#N19(11#W19(36#W 118 33 5 69(10#N19(14#W19(36#W7225 6 69(09#N19(12#W19(36#W 111 26 7 69(08#N19(16#W19(40#W4623 8 69(07#N19(15#W19(40#W4519 9 69(06#N19(15#W19(42#W9233 10 69(05#N19(17#W19(37#W 123 24 11 69(04#N19(25#W19(39#W 168 20 12 69(03#N19(22#W19(49#W 128 25 13 69(02#N19(34#W19(51#W 172 28 14 69(01#N19(27#W19(42#W6 17 Estimation of harp seal pup production in the Greenland Sea 103

Table 6. Estimates, standard errors, and coefficients of variation of suggest that pup production is higher than the 1991 harp seal pup production in the Greenland Sea during MarcheApril estimates, although it is important to remember that caution in 2002. The Patch A and Patch B estimates are corrected for the should be taken when comparing estimates made by temporal distribution of births. All estimates are rounded to the different methods, as they are subject to different biases. nearest hundreds. Interestingly, the point estimate we obtained (98 500) is within the confidence intervals of the estimate of pup Patch Method Date Estimate s.e. CV (%) production for 2000 (76 700; 95% CI 48 000e105 000) derived from a population model, tuned to the previous pup A Visual 20 March 4 700 700 15.1 B Visual 28 March 82 600 16 700 20.2 production estimates based on mark-recapture data (ICES, C Photographic 6 April 11 200 1 200 10.8 2001). Using preliminary results from the 2002 survey, the Joint Downloaded from https://academic.oup.com/icesjms/article/63/1/95/625803 by guest on 27 September 2021 Total 98 500 16 800 17.0 ICES/NAFO Working Group on Harp and Hooded Seals (WGHARP) estimated the total stock size and assessed the impact of various levels of annual harvest on future Sea catches in the 18th and the first two-thirds of the 19th population size (ICES, 2004). They estimated a current centuries, performed by Dutch, British, German, and Danish population of 349 000 (95% CI 319 000e379 000) one year ships, is poor. Norwegian sealers appeared for the first time in of age and older, and they also predict that the population the Greenland Sea in 1846, and have subsequently will continue to increase under the current harvest regime participated with increased effort. Exploitation levels of very small annual removals. Confirming these results reached a historical maximum in the 1870s and 1880s when will have implications both for future management of the annual catches of harp seals (pups and adults) varied between stock and for the understanding of its role in the Greenland 50 000 and 120 000 (Iversen, 1927). This overexploitation Sea and Barents Sea ecosystems. appears to have driven the stock to an all time low, and the Assuming that the estimates of the mean and standard competition for a limited supply of seals in the 1870s resulted deviation of pup stage length were as given by Kovacs and in the disappearance of all non-Norwegian fleets (Sergeant, Lavigne (1985), results from the staging flights over 1991). It was evident that the catch levels in the 1870s were Patches A and B suggest that the majority of harp seal higher than the stock could sustain, and some regulatory females in the Greenland Sea whelped between 16 and 21 measures (mainly designed to protect adult females) were March in 2002. This is in accordance with observations introduced in 1876 (Iversen, 1927). In the first decades of the made in the Greenland Sea in 1991, whereas in 1990 it 20th century, the annual harp seal catches varied between appears that the breeding may have peaked 5e7 days later 10 000 and 20 000 animals. An increase to around 40 000 (Øritsland and Øien, 1995). Variations from year to year in seals per year occurred in the 1930s (Iversen, 1927; Sergeant, peak pupping has been observed also for harp seals in the 1991). After a 5-year pause in the sealing operations during Northwest Atlantic, where pupping generally peaks earlier World War II, total annual catches quickly rose to a post-war than in the Greenland Sea (see Stenson et al., 2003). Earlier maximum of about 70 000 in 1948, but then followed pupping than in the Greenland Sea is also observed for the a decreasing trend until quotas were imposed in 1971 White Sea stock of harp seals (Potelov et al., 2003). (Sergeant, 1991; ICES, 2004). From 1955 to 1994 a minor By combining this estimate with those obtained for other part of the catches was taken by the Soviet Union/Russia, and populations in recent years (1999e2002) provides the first the total annual catches have varied between a few hundreds estimate of total pup production for North Atlantic harp to about 17 000 from 1971 to present (ICES, 2004). seals. The most recent (1999) estimate of harp seal pup Available knowledge of both previous and more recent production from the Northwest Atlantic was 997 900 abundance of Greenland Sea harp seals has been rather (s.e. Z 102 100, Stenson et al., 2003), while an estimate restricted. Based on catch per unit effort analyses and mark- of 330 000 (s.e. Z 34 000) pups was obtained in 2002 for recapture pup production estimates, it has been assumed the Barents Sea/White Sea (ICES, 2004). The present 2002 that the population may have increased since the early estimate from the Greenland Sea (98 500, s.e. Z 16 800) 1960s, although direct evidence is limited (Ulltang and shows that this population is the smallest, and that the Øien, 1988; Øien and Øritsland, 1995). From 1977 to 1991, North Atlantic harp seal pup production, as determined at about 17 000 harp seal pups were tagged in a comprehensive the turn of the century, is in the order of 1.4 million animals mark-recapture experiment in the Greenland Sea (Øien and per year (1.426 million with an s.e. of 109 500). Øritsland, 1995). Based on this experiment, pup production was estimated to be 40 000e50 000 in 1980. Updates of the Acknowledgements mark-recapture estimates indicated pup production in 1991 of 67 300 (95% CI 56 400e78 113) (NAFO, 1995). Aerial The authors thank I. Ahlqvist, B. Bergflødt, L. Lindblom, surveys performed in 1991 suggested a minimum pup N. E. Skavberg, pilots, engineers, and camera operators, production of 55 000 (cv 0.14) in this year (Øritsland and and the crew on board RV ‘‘Lance’’ e without their Øien, 1995). The present estimate, obtained 11 years later, assistance and enthusiasm during fieldwork the surveys 104 T. Haug et al. would not have been completed. We are especially grateful Myers, R. A., and Bowen, W. D. 1989. Estimating bias in aerial to A. K. Frie, L. Lindblom, D. Wakeham, and A. P. surveys of harp seal pup production. Journal of Wildlife e Golikov for reading the photos, and to J. Lawson who Management, 53: 361 372. Nævdal, G. 1966. Protein polymorphism used for identification of provided the map. Participation in surveys as well as harp seal populations. A˚ rbok for Universitetet i Bergen subsequent analyses and publication of results by G. B. (Matematisk Naturvitenskapelig Serie), 9: 1e20. Stenson was secured by funding by the Norwegian Council Nævdal, G. 1969. Blood protein polymorphism in harp seals off of Research, project no. 146573/120. eastern Canada. Journal of the Fisheries Research Board of Canada, 26: 1397e1399. Nævdal, G. 1971. Serological studies on marine mammals. Rapports et Proce`s-Verbaux des Reúnions de Conseil Interna- tional pour l’Exploration de la Mer, 161: 136e138.

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