Abundance of cetaceans in the southern U.S. North Atlantic Ocean during summer 1998.

Abstract--The U.S. Marine Mammal Protection Act requires that the abundance of marine mammals in U.S. waters be assessed. Because this requirement had not been met for a large portion of the North Atlantic Ocean (U.S. waters south of Maryland), a ship-based, line-transect survey was conducted with a 68 m research ship between Maryland (38.00[degrees]N) and central Florida (28.00[degrees]N) from the 10-m isobath to the boundary of the U.S. Exclusive Economic Zone. The study area (573,000 [km.sup.2]) was surveyed between 8 July and 17 August 1998. Minimum abundance estimates were based on 4163 km of effort and 217 sightings of at least 13 cetacean species and other taxonomic categories. The most commonly sighted species (number of groups) were bottlenose dolphins, Tursiops truncatus (38); sperm whales, Physeter macrocephalus (29); Atlantic spotted dolphins, Stenella frontalis (28); and Risso's dolphins, Grampus griseus (22). The most abundant species (abundance; coefficient of variation) were Atlantic spotted dolphins (14,438; 0.63); bottlenose dolphins (13,085; 0.40); pantropical spotted dolphins, S. attenuata (12,747; 0.56); striped dolphins, S. coeruleoalba (10,225; 0.91); and Risso's dolphins (9533; 0.50). The abundance estimate for the Clymene dolphin, S. clymene (6086; 0.93), is the first for the U.S. Atlantic Ocean. Sperm whales were the most abundant large whale (1181; 0.51). Abundances for other species or taxonomic categories ranged from 20 to 5109. There were an estimated 77,139 (0.23) cetaceans in the study area. Bottlenose dolphins and Atlantic spotted dolphins were encountered primarily in continental shelf (<200 m) and continental slope waters (200-2000 m). All other species were generally sighted in oceanic waters (>200 m). The distribution of some species varied north to south. Striped dolphins, Clymene dolphins, and sperm whales were sighted primarily in the northern part of the study area; whereas pantropical spotted dolphins were sighted primarily in the southern portion.

Manuscript approved for publication 11 February 2003 by Scientific Editor. Manuscript received 4 April 2003 at NMFS Scientific Publications Office.

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The U.S. Marine Mammal Protection Act (MMPA) requires that stocks of marine mammal species in U.S. waters be maintained at or above their optimum sustainable population (OSP) level, defined as the number of animals that will result in maximum productivity. The MMPA, as amended in 1994, requires that the U.S. National Marine Fisheries Service (NMFS) determine the potential biological removal (PBR) of each stock for management purposes. PBR is an estimate of the maximum number of animals that may be removed from a stock due to human activities (e.g. fisheries bycatch) while allowing the stock to reach or maintain its OSP. The PBR is calculated by using the estimated minimum abundance of a stock, half its maximum net productivity rate (theoretical; or estimated), and a recovery factor (Barlow et al., 1995).

For the U.S. Exclusive Economic Zone (EEZ) adjacent to the Atlantic coast of the continental U.S., the NMFS currently defines 27 taxa of cetaceans as stocks (Waring et al., 2001). These stocks include 24 one-stock species, bottlenose dolphins (Tursiops truncatus) that are divided into two stocks, and one mesoplodont beaked whale stock. Abundance estimates are available for most of these stocks from U.S. waters north of the Virginia-Maryland border (38.00[degrees]N). In 1998, except for three stocks, abundance estimates were not available for Atlantic cetacean stocks from U.S. waters south of Maryland (Waring et al., 1997). Abundance estimates for these three stocks were based on a small amount of effort from a 1992 winter ship survey south of Cape Hatteras (Mullin and Ford (1)). Other cetacean abundance estimates from U.S. waters south of Maryland are for portions of the continental shelf or continental slope (Blaylock and Hoggard, 1994; Blaylock, 1995; CeTAp (2); Fritts et al.(3)).

To estimate the abundance of cetaceans in U.S. Atlantic waters south of Maryland, a ship survey was conducted during summer 1998 and the results are reported in this study. Abundance estimates from this area are combined with abundance estimates from surveys of U.S. waters north of the Virginia-Maryland border conducted by the NMFS Northeast Fisheries Science Center to obtain overall abundance estimates for western North Atlantic cetacean stocks (e.g. Waring et al., 2001).

Methods

Study area and survey design

The study area (573,000 [km.sup.2]) was North Atlantic Ocean waters between central Florida (28.00[degrees]N) and Maryland (38.00[degrees]N) from the 10-m isobath to the boundary of the U.S. EEZ, generally 371 km (200 nmi) from the nearest U.S. point of land (Fig. 1). The study area has a diverse bottom topography and includes a very narrow continental shelf (<200 m) at Cape Hatteras which broadens to form the mid-Atlantic Bight to the north and the Florida-Hatteras Shelf to the south. Beyond the shelf, south of Cape Hatteras are found the following features: the Florida-Hatteras Slope, the Blake Plateau (700-1000 m deep), and the Blake Escarpment. North of the Blake Plateau, the continental slope from 200-2000 m deep is steep and most of the study area has water depths >2000 m. The Gulf Stream is the dominant oceanographic feature in the study area. From the south, the Gulf Stream Front generally follows the upper continental slope northward to Cape Hatteras, where it flows to the northeast. Seaward of the Gulf Stream are Sargasso Sea waters. North of Cape Hatteras and the Gulf Stream Front, cooler waters, which largely originate in the Labrador Sea, drift into the study area from the north and northeast.

[FIGURE 1 OMITTED]

Transects covered the study area uniformly in a saw-tooth pattern from a random start at the southernmost inshore point and were surveyed from the 68-m NOAA ship Relentless (renamed Gordon Gunter in 1999) between 8 July and 17 August 1998 from south to north, and from north to south. Transects were placed to cress the bathymetry gradient. The narrow band of U.S. waters between central Florida and Key West, Florida, were partially surveyed but were not included in the present report.

Data collection

Data were collected by two teams of three observers from the ship's flying bridge, located 14.5 m above the surface of the water, during daylight hours, weather permitting (i.e. no rain, Beaufort sea state <6). Observers used standard line-transect survey methods for cetaceans that were similar to those used from ships in the Pacific Ocean and Gulf of Mexico (e.g., Barlow, 1995; Hansen et al. (4)). Each team had at least two members experienced in shipboard line-transect methods and in the identification of tropical and temperate cetaceans. Two observers searched for cetaceans using 25x binoculars and another observer searched using unaided eye or 7x hand-held binoculars and recorded data. These three observers constituted the "primary team." From 18 July to 17 August, a fourth observer was added to one team to act as a conditionally independent observer (CIO, see below). The area from 90[degrees] left and right of the ship's bow to the horizon was searched by the primary team. Observers changed position (including the CIO position) every 30-40 minutes, and each team alternated two-hour watches throughout daylight hours. The survey speed was usually 18 km/h but varied with sea conditions.

Data were recorded on a computer interfaced with a global positioning system (GPS) by a data acquisition program. Data collected for each cetacean sighting included time, position, bearing, and reticle (a measure of radial distance) of the sighting, species, group-size, behavior, bottom depth, sea surface temperature, and associated animals (e.g. seabirds, fish). The bearing and radial distance for sightings that were close to the ship were estimated. Survey effort data were automatically recorded every two minutes and included position, heading, effort status, observer position, and environmental conditions that could affect the observers' ability to sight animals (e.g. Beaufort sea state, position of the sun).

Typically, if a sighting was within a 5.5-km strip on either side of the ship, the ship was diverted from the transect line and approached the group so that observers could identify species and obtain group-size estimates. For each sighting, the final group-size was estimated by a consensus of the primary team. Mixed-species groups were uncommon (five of 217 sightings) and group-size estimates were made separately for each species.

Species identification

Cetaceans were identified to the lowest taxonomic level possible from descriptions in field guides and scientific literature (e.g. Leatherwood and Reeves, 1983; Jefferson et al., 1993; Carwardine, 1995) (Table 1). An observer's ability to make identifications depended on weather and animal behavior. The study area was potentially inhabited by short-finned pilot whales (Globicephala macrorhynchus), which are thought to occur within the study area from about Virginia south, and long-finned pilot whales (G. melas), thought to occur from near Cape Hatteras north (Payne and Heinemann, 1993). Because the two species cannot be reliably distinguished at sea, they were recorded simply as pilot whales. Two forms of the Atlantic spotted dolphin (Stenella frontalis) were tentatively identified: the larger, more coastal form, and the smaller offshore form (Perrin et al., 1994). Abundances were estimated for each form and for all Atlantic spotted dolphins combined because only one stock is currently designated for U.S. Atlantic waters. Coastal and offshore forms of bottlenose dolphins (Hersh and Duffield, 1990), which constitute the two stocks, were recorded, but most sightings could not be clearly categorized; therefore, all bottlenose dolphin sightings were pooled for one overall abundance estimate. Bottlenose and Atlantic spotted dolphins could not always be distinguished at large distances and a separate estimate was made for animals that could not be approached and were identified as "Tursiops or S. frontalis." Overall abundances for the genus Kogia and the genus Mesoplodon were estimated. Dwarf sperm whales (K. sima) and pygmy sperm whales (K. breviceps) were difficult to distinguish and stranding records of both species are numerous from U.S. Atlantic shores (Schmidly (5)). Based on stranding records of mesoplodont whales from U.S. Atlantic shores, sightings of Mesoplodon were probably True's (M. mirus), Gervais's (M. europaeus) or Blainville's (M. densirostris) beaked whales (Mead, 1989). In some cases cetaceans could only be identified as large whales (>7 m long), small whales (nondolphin, <7 m), dolphins, or odontocetes.

Analytical techniques

For each species or taxonomic category, abundance estimates (N) were made with line-transect methods by using the software program DISTANCE (Colorado Coop. Fish and Wildlife Research Unit, Colorado State Univ., Fort Collins, CO) (Bucldand et al., 1993) with the equation

N = A n S f(O) / 2 L g(O),

where A = size of the study area;

n = number of on-effort group sightings;

S = mean group-size estimate;

f(0) = sighting probability density function at perpendicular distance zero;

L = total length of transect line; and

g(0) = probability of seeing a group on the transect line.

The log-normal 95% confidence interval was computed for each abundance estimate because it was a product of estimates and tends to have a skewed distribution. The variance of N was estimated as

var(N) = [N.sup.2][var(n)/[n.sup.2]+var(S)/[S.sup.2]+var[f(f0)] /f[(0).sup.2]=var[g(0)/f[(0).sup.2]]

and the coefficient of variation (CV) was estimated as

CV(N) = [square root of (var(N))/N].

The sampling unit was the length of the transect completed on-effort each day when the Beaufort sea state was <5. The formula used to estimate each component of the variance is given in Buckland et al. (1993).Var(n) was length-weighted and based on the variation in the number of on-effort group sightings between sampling units that ranged in length from 39 to 229 km/day.

Estimation of/(0)

The perpendicular distance,y, was estimated by using bearing and reticle measurements. The reticle readings were converted to radial sighting distances (R) by the method of Lerczak and Hobbs (1998), and the formula y = R sin(b), where b = angle between the sighting and the transect line. Estimates of f(0) were made by using a hazard-rate, uniform, or half-normal model with exact perpendicular sighting distances. For each species group, outlying values ofy were truncated to improve the fit of the model (Table 2). Model selection was determined by using Akaike's information criterion (AIC; Buckland et al., 1993).

The number of groups sighted of most species was insufficient to obtain an estimate off(0). Therefore, sightings of species with similar sighting characteristics (i.e. body size, group-size, surface behavior, blow visibility) were pooled to estimate f(0) for five categories (Table 1). The abundance for each species was estimated by using the pooled f(0) and var[f(0)] for its category. The var[f(0)] was assumed to be zero for the strip-transect estimates explained below. If the individual detection functions of all species within a category are indeed very similar, by pooling, the variance, CV, and confidence interval of each abundance estimate was probably underestimated because the variance off(0) was based on an artificially high sample size. On the other hand, if the true detection functions of the species within a category are highly variable, the variance of f(0) for an individual species may be overestimated.

During the study, effort was sometimes maintained while in transit to and from ports or along the border of the study area, but it usually occurred in a small range of water depths (e.g. parallel to shore) and was excluded because it could have biased abundance estimates. However, due to the small number of sightings for the survey, y from the "transit" sightings were pooled with the on-effort sightings for estimates off(0) (Table 2).

Estimation of mean group-size

The group-sizes for most species tended to be related to y, because in many cases larger groups are easier to see than small groups with increasing y. In general, the arithmetic mean of group-size may be an overestimate of the true mean group-size and could lead to positively biased abundance estimates. Therefore, a regression of group-size by y was used to estimate an "expected mean group-size" (program DISTANCE). The expected mean group-size was used in the abundance estimate if it was smaller than the arithmetic mean group-size. For estimates based on a small number of sightings, the expected mean group-size was sometimes greater than the arithmetic mean. Because group-size estimates were usually made after the ship approached the group, this was assumed to be an artifact of the small sample size, and the arithmetic mean was used in these cases. Var(S) was the analytical variance for mean group-sizes based on arithmetic means or was estimated as in Buckland et al. (1993:79) for expected mean group-sizes.

Strip-transect estimates

One requirement for unbiased line-transect estimates of abundance is that the cetacean group should not move in response to the ship before it is sighted (Buckland et al., 1993). If cetaceans are not sighted before they respond to the ship, in cases of attraction to the ship, f(0) and abundance will be overestimated. In the Gulf of Mexico, five species appear to be consistently attracted to ships to ride the bow waves (i.e. bottlenose, Atlantic spotted, spinner [S. longirostris], Clymene [S. clymene], and pantropical spotted dolphins IS. attenuata]) (Wursig et al., 1998). All sightings made with 25x binoculars had radial distances >665 m and were assumed to be made before these species were attracted to the ship. If sightings of these species were made at radial distances <665 m, because of the possibility of attraction, they were not included in the line-transect abundance estimate, and a separate strip-transect abundance estimate was made with these sightings. For each species, the width of the strip for strip-transect estimates was set at the line-transect strip width (1/2f(0)) for that species (Tables 1 and 2). This procedure yields the same result as the formula given above with f(0) for the species-group category. However, f(O) for small dolphins and for small whales and large dolphins combined was not positively biased by including sightings of groups that were probably attracted to the transect line. For each species, the line- and strip-transect estimates were summed for one overall abundance estimate.

Conditionally independent observer

The central assumption for estimating abundance with line-transect methods is that cetacean groups on the transect line are detected with certainty (i.e. g(0) = 1; Buckland et al., 1993). However, this assumption is usually not met during cetacean surveys because of availability and perception bias (i.e. g(0) < 1) (Marsh and Sinclair, 1989). Some groups on the transect line are missed because they may not be at the surface during the time the ship is in the area and are not available to be seen, whereas other groups at the surface are missed by observers (i.e. not perceived) because of factors such as observer experience, sea state, and animal behavior, among others.

An attempt was made to estimate g(0) due to perception bias with a conditionally independent observer (CIO) by using methods based on Barlow (1995). The CIO was used when the 4-observer team was on duty and was stationed at 25x binoculars located on a bridge-wing 2.7 m below the primary team. One individual switched teams each day; therefore all seven observers on the ship acted as the CIO at different times. The CIO searched for cetaceans near the transect line (from 30[degrees] left to 30[degrees] right of the bow) when the primary observers were on-effort. The CIO and the primary team could not see or hear each other. Whenever the primary team made a sighting, the data recorder relayed its bearing and reticle to the CIO. When the CIO made a sighting, the time, bearing and reticle were noted by the CIO, and the sighting was monitored until it was sighted by the primary team or, theoretically, passed abeam, at which time the CIO was to notify the primary team to divert the ship to identify the species and estimate group-size.

Results

Abundance estimates were based on 4163 km of effort in Beaufort sea states [less than or equal to] 4 and 217 on-effort sightings of cetacean species or other taxonomic categories (Fig. 1 and Table 1). At least 13 cetacean species were sighted. The most commonly sighted species (number of sightings) were bottlenose dolphins (38), sperm whales (Physeter macrocephalus) (29), Atlantic spotted dolphins (28), and Risso's dolphins (Grampus griseus) (22). Thirty sightings occurred during transit in Beaufort sea states [less than or equal to] 4 (861 km) and were used to estimate f(0). Estimates of f(0) ranged from 0.300/kin for large whales to 0.561/km for cryptic whales (Table 2).

Conditionally independent observer

The CIO achieved 1775 km of effort (35% of effort, including transit, with Beaufort sea state [less than or equal to] 4) and sighted 21 cetacean groups. Of these, six groups ranging in size from 1 to 10 animals were missed by the primary team and included three unidentified dolphin groups, two unidentified odontocete groups, and one Mesoplodon sp. Each of these sightings was observed briefly by the CIO but could not be tracked until they passed the beam of the ship; however, in each of the six cases no sightings were made by the primary team during the time frame it would have been possible to sight them. To estimate g(0) following the analytical methods described by Barlow (1995), a separate estimate of f(0) is therefore required for CIO sightings missed by the primary team. Because there were only six of these, g(O) could not be estimated for any f(0) category, and g(0) = 1 and var[g(0)] = 0 was used in each abundance estimate.

Abundance

The following were the most abundant species (abundance coefficient of variation) observed in our study: Atlantic spotted dolphins (14,438; 0.63); bottlenose dolphins (13,085; 0.40); pantropical spotted dolphins (12,747; 0.56) and striped dolphins (S. coeruleoalba) (10,225; 0.91); and Risso's dolphins (9533; 0.50). Sperm whales were the most abundant large whale (1181; 0.51). Abundances for other species or taxonomic categories ranged from 20 to 6086 There were an estimated 77,139 (0.23) cetaceans in the study area.

Group sizes

Mean group sizes for balaenopterids, physeterids, and ziphiids were less than three animals per group. Bottlenose dolphins, pilot whales, Risso's dolphins, and "coastal' Atlantic spotted dolphins were in groups that averaged 12-18 animals. The average group sizes of pantropical spotted, Clymene, and striped dolphins ranged from 75 to 110 individuals (Table 3).

Distribution

Cetaceans were distributed throughout the study area but few sightings occurred on the eastern Blake Plateau (Fig. 1). The distribution of species varied regionally an by water depth (Fig. 2-4, Table 4). Bottlenose dolphins an( "coastal" Atlantic spotted dolphins were sighted throughout the study area but primarily in or near continental shelf waters. Pilot whales and Risso's dolphins were widely distributed seaward of the continental shelf. Sperm whales unidentified large whales, "offshore" Atlantic spotted dolphins, striped dolphins, and Clymene dolphins occurred almost exclusively in oceanic waters (>200 m) from Cap Hatteras northward. Most pantropical spotted dolphin sightings were in the southern part of the study area.

[FIGURES 2-4 OMITTED]

Discussion

Abundance

Cetacean abundances for the entire study area have no been estimated previously. Based on stranding record and previous surveys within or near the study area, all the species encountered were expected to be sighted. Previous abundance estimates for the western North Atlantic stocks of short-finned pilot whales and of dwarf and pygmy sperm whales, 749 (0.64) and 420 (0.60), respectively, were based on a winter 1992 ship survey in U.S. oceanic water (>200 m) south of Cape Hatteras (Waring et al., 1997). The 1992 dwarf and pygmy sperm whale estimate is similar t our estimate (580; 0.57); although the 1998 study area was much larger and many sightings occurred north of Cape Hatteras (Fig.4).

Abundances have also been estimated for small portions of the study area, but direct comparisons to our estimates are difficult. Seasonal abundances were estimated for about 26 cetacean species or genera encountered in U.S. continental shelf and slope waters between Cape Hatteras and Canada during aerial surveys conducted from 1978 to 1982 (CeTAp (2)), including at least 11 species or genera sighted during our survey. Fritts et al. (3) sighted 12 cetacean species during seasonal aerial surveys of the continental shelf and southern Blake Plateau off central Florida from 1980 to 1981; eight of these were sighted during our survey.

The abundance estimate reported in the present study for the Clymene dolphin represents the first for this species in any portion of the U.S. Atlantic EEZ. However, the estimate was based on only three sightings and has a large 95% confidence interval (1293-28,652 dolphins). The Clymene dolphin was recognized as a valid species in 1981 and is sympatric with the spinner dolphin in the tropical Atlantic (Perrin et al., 1981). The two species have similar color patterns, and in previous studies both were possibly recognized as S. longirostris and were not distinguished (CeTAp (2); Fritts et al. (3)). The identifications of Clymene dolphins were made by observers with experience from the Gulf of Mexico where both species are relatively common (Hansen et al.4; Hansen et al. (6)). There is currently no stock designation for the Clymene dolphin in U.S. Atlantic waters (Waling et al., 2001).

Our estimate of bottlenose dolphins is for waters >10 m in depth; however, this estimate does not include their entire water depth range in U.S. Atlantic waters south of Maryland. Bottlenose dolphins occur year-round in coastal waters <10 m in depth (the inshore boundary of the study area) and in some bays and estuaries from Cape Hatteras south. North of the Cape they have been found close to shore in waters <25 m in depth only during warm months and are assumed to have migrated along-shore from the south (Mead, 1975; Kenney, 1990). Aerial surveys of bottlenose dolphins conducted in the past along the U.S. Atlantic included waters from the shore to 10 m in depth. For waters typically <75 m deep south of Cape Hatteras, the winter 1992 abundance from an aerial survey was 12,435 (0.18) (Blaylock and Hoggard, 1994). For waters <25 m deep from Cape Hatteras to northern New Jersey, the abundance from a summer 1994 aerial survey was 26,809 (0.40) (Blaylock, 1995). The frequency of bottlenose dolphin sightings during these surveys increased substantially inshore of the 10-m isobath boundary of the ship study area and, compared with the estimate from the ship, may account for the generally larger aerial survey estimates even though they are for smaller study areas.

There are currently two genetically distinguishable bottlenose dolphin stocks designated in the U.S. Atlantic: the coastal stock and the offshore stock (LeDuc and Curry, 1998; Waring et al., 2001). Using mitochondrial DNA from skin biopsy samples obtained during the summer 1998 study and other sampling efforts, Torres et al. (in press) reported no offshore form was sampled within 6 km of shore and no coastal from was sampled beyond 39 km from shore or in waters >34 m deep. Therefore an area of overlap of the two forms occurs within the 1998 study area but the fraction of each stock in our estimate (13,085; 0.40) is unknown because the number of biopsy samples between the two boundaries was very small in the Torres et al. (in press) study. However, 20 of the 38 bottlenose groups we used to estimate abundance were found in waters >50 m deep.

Abundances were estimated for ten species and three other genera of cetaceans, but other species are known or expected to occur in the study area. Three of these species, right whales (Eubalaena glacialis), humpback whales (Megaptera novaeangliae), and harbor porpoises (Phocoena phocoena), occur in the study area seasonally, primarily in months other than summer months, and abundances have been estimated from studies of their primary summer ranges north of the study area (e.g. Knowlton et al., 1994; Palka, 1995; Smith et al., 1999).

Additional species expected in at least part of the study area include Bryde's whale (B. edeni), Cuvier's beaked whale (Ziphius cavirostris), pygmy killer whale (Feresa attenuata), false killer whale (Pseudorca crassidens), melon-headed whale (Peponocephala electra), killer whale (Orcinus orca), common dolphin (Delphinus delphis), spinner dolphin, and Fraser's dolphin (Lagenodelphis hosei). Each of these species is thought to have a tropical to subtropical or broader distribution worldwide (Jefferson et al., 1993), and except for the common dolphin, an abundance estimate for each species is available for the adjacent northern Gulf of Mexico (Hansen et al. (6)). However, except for the spinner dolphin, each of these species is relatively uncommon in the northern Gulf of Mexico and was not encountered every year during four annual spring surveys with effort similar to that in our survey (Hansen et al. (6)). Therefore, many of these species may also be uncommon in the Atlantic study area and were simply not encountered during the 1998 survey. During a late summer 1999 ship survey of the inner half of the southern Atlantic study area that targeted bottlenose dolphins, a group of Fraser's dolphins and melon-headed whales was sighted in water 3000 m deep east of Cape Hatteras (Roden (7)).

Some species may also inhabit the study area seasonally. During the 1992 winter ship survey south of Cape Hatteras (Mullin and Ford (1)), five groups of balaenopterid whales were recorded, three of which were classified as unidentified Bryde's or sei whales. Also during the winter 1992 survey, groups of false killer whales and Cuvier's beaked whales were sighted twice, and pygmy killer whales once. Common dolphins were sighted between Cape Hatteras and Maryland in all seasons, except summer, during the CeTAP (2) study but were sighted once in this area during the late summer 1999 survey (Roden (7)). Common dolphins are expected to occur throughout the area surveyed in 1998 but they may not. Although there are stranding records south of Cape Hatteras (Schmidly (5)), there are no valid stranding or sighting records of common dolphins in the adjacent Gulf of Mexico despite extensive seasonal surveys of the northern Gulf (Jefferson, 1995; Hansen et al. (4)).

Precision

The precision of the abundance estimates was generally poor. For species or genera abundances, only the estimate for bottlenose dolphins (the most commonly sighted species), Risso's dolphins, and pilot whales had a CV [less than or equal to] 0.50 (Table 3). The abundance estimate for the Atlantic spotted dolphin, the most abundant species, had a CV = 0.63. In cases where there is human-caused mortality in a cetacean stock, abundance estimates with a CV < 0.50 are generally required to avoid incorrectly classifying a cetacean stock as "strategic" under the U.S. MMPA (i.e. annual human-caused mortality > annual PBR) less than 10% of the time (Wade and DeMaster, 1999). For most species, the variance in the encounter rate, var(n), accounted for more than 70% of the var(N). The distribution of most species was not uniform in the study area and precision might be improved by stratifying estimates by water depth (e.g. shelf and nonshelf) and by area (e.g. north and south of Cape Hatteras).

Biases in abundance estimates

The survey was designed to meet the assumptions of line-transect theory (Buckland et al., 1993). However, the abundance estimates are negatively biased to varying degrees because the central assumption, that cetacean groups on the transect line are detected with certainty (i.e. g(0)=1), was not met, and data were not available to correct estimates for perception and availability bias. By using the CIO methods described by Barlow (1995), we attempted to estimate the fraction of groups missed on the transect line by the primary observers due to perception bias. However, there were too few sightings to make g(0) estimates because the overall group encounter rate was lower than anticipated and the CIO was only used for 35% of the total survey effort. In the future, a CIO should be used whenever the primary team is on-effort and the CIO should search an area larger than 30[degrees] left and right of the bow. Although the data in proximity of the transect line are most critical for estimating g(0), it is also necessary to have enough data to estimate f(0) for groups missed by the primary team.

More work is needed to develop methods for estimating g(0) in relation to perception bias in the southern U.S. Atlantic. Completely independent observers cannot be used because the ship has to be diverted from the transect line to identify species and make group-size estimates. Because many groups can easily be lost once sighted, the ship must be diverted well before the group passes abeam. Barlow (1995) used a CIO that searched the same area as the primary team with unaided eye or 7x binoculars. The 25x binoculars were used in our study to increase the number of CIO sightings and avoid attraction bias in f(0). Previous experience in the Gulf of Mexico has indicated that many unaided-eye sightings would be of small groups of species that are attracted to the ship to ride the bow waves. Conversely, small groups are the most difficult for an independent observer to track with 25x binoculars because the ship is not diverted and the bearing to the group is constantly changing.

Similar to Barlow's (1995) findings on perception bias, the majority of groups missed by the primary team were apparently small groups, although the group-sizes were not estimated at close range. Barlow (1995) estimated g(0) ranging from 0.73 and 0.79 for small groups of delphinids (<21) and cryptic species (which usually occur in small groups), and g(0) = 1 for groups of >20 delphinids. In addition to group-size, the magnitude of perception bias is dependent on behavior, weather (e.g. Beaufort sea state), and the observer: active groups are less likely to be missed than resting groups or species whose behavior does not produce pronounced cues (e.g. blows, splashes).

Availability bias varies by species because of differences in individual dive cycles, group diving behavior, and groupsizes. Long-diving sperm whales and beaked whales will be at the surface for much less time than will many small delphinids, which have much shorter dive cycles. Diving synchrony among members of a group also affects availability bias; if dives are asynchronous, the probability that at least one animal will be at the surface increases with group size.

Barlow (1999) estimated both availability and perception bias for long-diving whales during ship surveys using 25x binoculars in a simulation study and estimated that for dwarf and pygmy sperm whales, Cuvier's beaked whales, and Mesoplodon spp., abundance estimates need to be increased 2 to 4 times (i.e. g(0)=0.50 to g(0)=0.25) to account for these biases. Barlow's (1999) estimates of g(0) for perception or availability bias (or both) are probably representative of the bias in the southern Atlantic survey because similar ship survey methods were used. However, it may not be valid to apply them directly to our abundance estimates because cetacean diving behavior and group sizes may be temporally and geographically specific, and survey conditions and observers may vary among surveys.

For the strip-transect estimates (Table 2), use of the line-transect strip width [2xl/f(0)] from the 25x binocular sightings as the strip width was assumed to be conservative and somewhat negatively biased. The distance from which animals will come to the ship to ride the bow is unknown, and variable, depending on factors such as the animals' previous behavior, number of opportunities for riding bow waves, and the type of ship. If the strip width was too narrow, the strip-transect estimates would overestimate abundance.

The geographical bathymetric range of the bottlenose dolphin was not covered during the survey. Because bottlenose dolphins undertake seasonal movements in the study area, in order to estimate the entire population size, ship survey estimates need to be combined with same-season abundance estimates from coastal waters <10 m and inshore waters (bays, sounds, and estuaries).

Distribution

Water-depth distributions of cetacean species were for the most part similar to those in the Gulf of Mexico (Mullin et al., 1994; Davis et al., 1998). Bottlenose dolphins and Atlantic spotted dolphins inhabit the continental shelf and shelf-edge region, whereas most other species have primarily oceanic distributions. The offshore form of the Atlantic spotted dolphin has not been identified in the northern Gulf of Mexico. The sightings of some species were highly regional (e.g. sperm whales, striped dolphins, Clymene dolphins, pantropical spotted dolphins) were probably heavily influenced by oceanographic features such as the Gulf Stream. Much more survey effort is needed in summer and other seasons before conclusions can be drawn about each species' distribution.

Table 1

Number of on-effort cetacean group sightings of each species
or other taxonomic category during 4163 km of survey effort in the
southern U.S. Atlantic study area during summer 1998. Species are
listed in categories pooled to estimate f(0) (see Table 2). The number
of sightings used for line-transect and strip-transect abundance
estimates are indicated for each species.

f(0) groupings and species               Line-transect   Strip-transect

Large whales
  Fin whale (Balaenoptera physalus)            1               0
  Minke whale (B. acutorostrata)               1               0
  Sperm whale (Physeter macrocephalus)        29               0
  Unidentified large whale                     6               0
Cryptic whales
  Dwarf and pygmy sperm whale (Kogia
    spp.)                                      9               0
  Mesoplodon spp.                              4               0
  Unidentified Ziphiidae                       3               0
  Unidentified small whale                     4               0
  Unidentified odontocete                     12               0
Small whales and large dolphins
  Pilot whale (Globicephala spp.)             10               0
  Bottlenose dolphin (Tursiops
    truncatus)                                35               3
  Risso's dolphin (Grampus griseus)           22               0
  "Coastal" Atlantic spotted dolphin
    (Stenella frontalis)                      24               3
  Unidentified T truncatus or S.
    frontalis                                  7               1
  Rough-toothed dolphin (Steno
    bredanensis)                               1               0
Small dolphins
  Pantropical spotted dolphin
    (Stenella attenuata)                       6               0
  Striped dolphin (Stenella
    coeruleoalba)                              5               0
  Clymene dolphin (Stenella clymene)           2               1
  "Offshore" Atlantic spotted dolphin
    (Stenella frontalis)                       1               0
Unidentified dolphins
  Unidentified dolphins                       26               0
  Stenella spp.                                1               0
Total                                         209              8

Table 2

Estimate of f(0) for each species group (see Table 1). n =
number of sightings used for the estimate of f(0) before truncation
(included in n is the number of sightings in parentheses
that occurred while the ship was in transit in or near the study
area). Truncation = the perpendicular distance, y, at which groups
with a greater y were excluded from the analysis. ESW = effective
strip width.

                                     f(0)      CV     Truncation   ESW

Species group                n       (/km)   [f(0)]      (m)       (m)

Large whales              38  (1)    0.300    0.12       5500      6666
Cryptic whales            33  (1)    0.561    0.13       3000      3565
Small whales and
  large dolphins         121 (22)    0.498    0.10       4000      4016
Small dolphins            20  (6)    0.398    0.11       4500      5025
Unidentified dolphin      27  (0)    0.496    0.10       4000      4032
Total                    239 (30)

Table 3

Group size, density and abundance estimates of cetaceans
in the southern U.S. Atlantic Ocean during summer 1998 (n = number
of on-effort group sightings after truncation, S = mean group-size
estimate, D = animals/100 [km.sup.2], N = abundance estimate, CV =
coefficient of variation, LCI and UCI = lower and upper limits
of a log-normal 95% confidence interval).

Species                        n     S       CV(S)         D        N

Fin whale                      1     2.0      --        0.007       41
Minke whale                    1     1.0      --        0.004       20
Sperm whale                   28     2.1     0.12       0.206     1181
Dwarf/pygmy sperm whale        8     1.9     0.16       0.101      580
Mesoplodon spp.                4     2.3     0.28       0.061      348
Unidentified Ziphiidae         3     1.7     0.40       0.034      193
Pilot whale                    9    16.6     0.19       0.892     5109
Bottlenose dolphin
    line-transect             31    11.8     0.29       2.194   12,571
    strip-transect             3     5.0     0.12       0.090      514
    sum                                                 2.284   13,085
Risso's dolphin               18    15.4     0.26       1.664     9533
Atlantic spotted dolphin
    "coastal"
      line-transect           21    17.6     0.25       2.211   12,670
      strip-transect           3     7.3     0.39       0.132      754
      sum                                               2.343
    "offshore"
      line-transect            1    37.0      --        0.177     1014
      strip-transect           0
      sum (coastal and
        offshore)                                       2.520   14,438
Unid. T. truncatus or S.
  frontalis
    line-transect              7     3.9     0.27       0.162      926
    strip-transect             1     1.0      --        0.006       34
    sum                                                 0.168      960
Rough-toothed dolphin          1     8.0      --        0.048      274
Pantropicalspotted dolphin     6    77.5     0.25       2.225   12,747
Striped dolphin                5    74.6     0.21       1.785   10,225
Clymene dolphin
    line-transect              2   110.0     0.37       1.053     6031
    strip-transect             1     2.0      --        0.010       55
    sum                                                 1.063     6086
Stenella spp.                  1    15.0      --        0.089      512
Unidentified large whale       6     1.2     0.14       0.025      143
Unidentified small whale       3     2.7     0.63       0.054      309
Unidentified odontocete       11     1.4     0.14       0.101      580
Unidentified dolphin          20     1.2     0.13       0.113      775
Sum (all cetaceans)                                    13.462   77,139

Species                              CV(N)      LCI       UCI

Fin whale                            1.15         6       270
Minke whale                          1.29         3       156
Sperm whale                          0.51       445      3136
Dwarf/pygmy sperm whale              0.57       197      1708
Mesoplodon spp.                      0.76        88      1376
Unidentified Ziphiidae               0.71        49       755
Pilot whale                          0.41      2302    11,341
Bottlenose dolphin
    line-transect                    0.42      5600    28,222
    strip-transect                   0.82       118      2249
    sum                              0.40      6098    28,077
Risso's dolphin                      0.50      3684    24,671
Atlantic spotted dolphin
    "coastal"
      line-transect                  0.71      3471    46,244
      strip-transect                 0.64       211      2696
      sum
    "offshore"
      line-transect                  0.85       223      4618
      strip-transect
      sum (coastal and
        offshore)                    0.63      4672    44,618
Unid. T. truncatus or S.
  frontalis
    line-transect                    0.73       246      3480
    strip-transect                   0.99         6       189
    sum                              0.71       276      3334
Rough-toothed dolphin                1.03        47      1584
Pantropicalspotted dolphin           0.56      4420    36,763
Striped dolphin                      0.91      2072    50,449
Clymene dolphin
    line-transect                    0.94      1138    31,963
    strip-transect                   1.15         8       361
    sum                              0.93      1293    28,652
Stenella spp.                        1.15        77      3392
Unidentified large whale             0.58        48       426
Unidentified small whale             0.86        53      1796
Unidentified odontocete              0.36       284      1181
Unidentified dolphin                 0.51       291      2066
Sum (all cetaceans)                  0.23    49,649   119,850

Table 4

Mean water depth and sea surface temperature of cetacean
species sighted in the southern U.S. Atlantic Ocean during summer
1998 (n=number of groups sighted on-effort; SE =standard error).

                                     Water depth (m)

Species                       n    Mean   SE        Range

Fin whale                      1     48    --        --
Minke whale                    1   3475    --        --
Sperm whale                   29   3252   122     2195-4389
Dwarf and pygmy sperm whale    9   2586   493      766-4079
Mesoplodon spp.                4   2699   735      774-4353
Unidentified Ziphiidae         3   1817   832      878-3475
Pilot whale                   10   1527   387      251-4280
Bottlenose dolphin            38    371    89       12-2561
Risso's dolphin               22   1300   285       44-4755
"coastal" Atlantic spotted
  dolphin                     27    216   117       13-2524
"offshore" Atlantic
  spotted dolphin              1   4298    --         --
Rough-toothed dolphin          1   4353    --         --
Pantropical spotted dolphin    6   1498   708      598-5030
Striped dolphin                5   2736   237     2012-3475
Clymene dolphin                3    756   538      139-1829

                               Sea surface temperature ([degrees]C)

Species                        Mean       SE             Range

Fin whale                      25.1       --              --
Minke whale                    29.5       --              --
Sperm whale                    29.0      0.28          22.8-29.9
Dwarf and pygmy sperm whale    29.6      0.37          26.9-30.9
Mesoplodon spp.                27.2      1.65          24.0-31.1
Unidentified Ziphiidae         29.8      0.15          29.6-30.1
Pilot whale                    28.5      0.73          23.2-31.5
Bottlenose dolphin             29.3      0.27          23.2-31.3
Risso's dolphin                28.4      0.62          22.9-31.3
"coastal" Atlantic spotted
  dolphin                      29.1      0.26          25.1-31.3
"offshore" Atlantic
  spotted dolphin              27.9       --               --
Rough-toothed dolphin          27.3       --               --
Pantropical spotted dolphin    30.5      0.61          27.6-31.6
Striped dolphin                23.9      0.37          22.9-25.1
Clymene dolphin                27.9      0.59          26.8-28.8

Acknowledgments

Many people made significant contributions to the success of this survey including the officers and crew of NOAA ship Relentless and C. Roden, the Field Party Chief. The Relentless was configured for marine mammal surveys through the dedicated efforts of W. Hoggard. The marine mammal observers were C. Brown, C. Burks, C. Cates, W. Hoggard, C. Hubard, T. Martinez, K. Maze-Foley, M. Newcomer, S. Swartz, J. Tobias, and K. Touhey. Environmental and ichthyoplankton data were collected by L. Bero, P. Brown, W. Fambrough, D. Fertl, A. Hamilton, A. Hohn, R. Holmes, E. Keith, E. LaBrecque, J. Litz, and J. Taylor. W. Irvin and T. Pusser were seabird observers. The survey was designed with the help of S. Swartz and the late R. Blaylock. Comments by C. Hubard, K. Maze-Foley, and three anonymous reviewers were very helpful in completing the manuscript.

(1) Mullin, K. D., and R. Ford. 1992. Report of NOAA ship Oregon II cruise 92-01 (198) (a cetacean survey of U.S. Atlantic waters south of Cape Hatteras, winter 1992). Southeast Fisheries Science Center, P.O. Drawer 1207, Pascagoula, Mississippi 39568.

(2) CeTAP (Cetacean and Turtle Assessment Program). 1982. A characterization of marine mammals and turtles in the midand north-Atlantic areas of the U.S. outer continental shelf. Final Report of the Cetacean and Turtle Assessment Program Bureau of Land Management, contract no. AA551-CT8-48, 450 p. U.S. Dep. Interior, Washington D.C.

(3) Fritts, T. H., A. B. Irvine, R. D. Jennings, L. A. Collum, W. Hoffman, and M. A. McGehee. 1983. Turtles, birds, and mararnals in the northern Gulf of Mexico and nearby Atlantic waters. Rep. FWS/ OBS-82/65, 455 p. U.S. Fish and Wildlife Service, Office of Biological Services, Washington, D.C.

(4) Hansen, L. J., K. D. Mullin, T. A. Jefferson, and G. P. Scott. 1996. Visual surveys aboard ships and aircraft. In Distribution and abundance of marine mammals in the northcentral and western Gulf of Mexico: final report; vol. II: technical report (R.W, Davis and G. S. Fargion, eds.), p. 55-132. Outer Continental Shelf (OCS) Study MMS 96-0027. U.S. Dep. Interior, Minerals Mgmt. Service, Gulf of Mexico OCS Region, New Orleans, LA.

(5) Schmidly, D.J. 1981. Marine mammals of the southeastern United States and the Gulf of Mexico. U.S. Dep. Interior, U.S. Fish and Wildlife Service Biological Services Program FWS/ OBS-80/41, 165 p.

(6) Hansen, L. J., K. D. Mullin, and C. L. Roden. 1995. Estimates of cetacean abundance in the northern Gulf of Mexico from vessel surveys, 9 p. Southeast Fisheries Science Center, P.O. Drawer 1207, Pascagoula, Mississippi 39568.

(7) Roden, C.L. 1999. Report of NOAA ship Oregon H cruise 99-05 (236) (a cetacean survey of U.S. Atlantic continental shelf and slope waters between New Jersey and central Florida, August-September 1999), 32 p. Southeast Fisheries Science Center, P.O. Drawer 1207, Pascagoula, Mississippi 39568.

Literature cited

Barlow, J. 1995. The abundance of cetaceans in California waters. Part I: Ship surveys in summer and fall of 1991. Fish. Bull. 93: 1-14. 1999. Trackline detection probability for long-diving whales. In Marine mammal survey and assessment methods (G. W. Garner et al., eds.), p. 209-221. A.A. Balkema, Rotterdam.

Barlow, J., S. L. Swartz, T. C. Eagle, and P. R. Wade. 1995. U.S. marine mammal stock assessments: guidelines for preparation, background, and a summary of the 1995 assessments. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-OPR-6, 73 p.

Blaylock, R. A. 1995. A pilot study to estimate abundance of the U.S. Atlantic coastal migratory bottlenose dolphin. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-SEFSC-362, 9 p.

Blaylock, R. A., and W. Hoggard. 1994. Preliminary estimates of bottlenose dolphin abundance in the southern U.S. Atlantic and Gulf of Mexico continental shelf waters. U.S. Dep. Commer., NOAATech. Memo. NMFS-SEFSC-356, 10 p.

Buckland, S. T., D. R. Anderson, K. P. Burnham, and J. L. Laake. 1993. Distance sampling: estimating abundance of biological populations, 446 p. Chapman and Hall, London.

Carwardine, M. 1995. Whales, dolphins and porpoises, 256 p. Dorling Kindersley, New York. NY.

Davis, R. W., G. S. Fargion, N. May, T. D. Leming, M. Baumgartner, W. E. Evans, L. J. Hansen, and K. D. Mullin. 1998. Physical habitat of cetaceans along the continental slope in the north-central and western Gulf of Mexico. Mar. Mamm. Sci. 14:490-507.

Hersh, S. L., and D. A. Duffield. 1990. Distinction between northwest Atlantic offshore and coastal bottlenose dolphins based on hemoglobin profile and morphometry. In The bottlenose dolphin (S. Leatherwood and R. R. Reeves (eds.), p. 129-142. Academic Press, San Diego, CA.

Jefferson, T.A. 1995. Distribution, abundance, and some aspects of the biology of cetaceans in the offshore Gulf of Mexico. Ph.D. diss., 232 p. Texas A&M University, College Station, TX.

Jefferson, T. A., S. Leatherwood, and M. A. Webber. 1993. Marine mammals of the world--FAO species identification guide, 320 p. FAO, Rome.

Kenney, R. D. 1990. Bottlenose dolphins off the northeastern United States. In The bottlenose dolphin (S. Leatherwood and R. R. Reeves, eds.) p. 369-386. Academic Press, San Diego, CA.

Knowlton, A. R., S. D. Kraus, and R. D. Kenney. 1994. Reproduction in North Atlantic right whales (Eubalaenag lacialis). Can. J. Zoo.72:1297-1305.

Leatherwood, S., and R. R. Reeves. 1983. The Sierra Club handbook of whales and dolphins, 302 p. Sierra Club Books, San Francisco, CA.

LeDuc, R. G., and B. E. Curry. 1998. Mitochondrial DNA sequence analysis indicates need for revision of the genus Tursiops. Rep. Int. Whaling Comm. 47:393.

Lerczak, J. A., and R. C. Hobbs. 1998. Calculating sighting distances from angular readings during shipboard, aerial, and shore-based marine mammal surveys. Mar. Mature. Sci. 14:590-599.

Marsh, H., and D. F. Sinclair. 1989. Correcting for visibility bias in strip transect aerial surveys of aquatic fauna. J. Wildl. Manage. 53:1017-1024.

Mead, J. G. 1975. A preliminary report on the former net fishery for Tursiops truncatus in the western North Atlantic. J. Fish. Res. Board Can. 32:1155-1162 1989. Beaked whale of the genus Mesoplodon. In Handbook of marine mammals. Volume 4: River dolphins and the larger toothed whales (S. H. Ridgway and R. Harrison (eds.), p. 349-430. Academic Press, San Diego, CA.

Mullin, K. D., W. Hoggard, C. L. Roden, R. R. Lohoefener, C. M. Rogers, and B. Taggart. 1994. Cetaceans on the upper continental slope in the north-central Gulf of Mexico. Fish. Bull. 92:773-786.

Palka, D. 1995. Abundance estimate of the Gulf of Maine harbor porpoise. In Biology of the phocoenids (A. Bjorge and G.P. Donovan, eds.), p. 27-50. Rep. Int. Whaling Comm. (special issue 16).

Payne, P. M., and D. W. Heinemann. 1993. The distribution of pilot whales (Globicephala spp.) in the shelf]shelf-edge and slope waters of the northeastern United States, 1978-1988. In Biology of northern hemisphere pilot whales (G. P. Donovan, C. H. Lockyer and A. R. Martin, eds.), p. 51-68. Rep. Int. Whaling Comm. (special issue 14).

Perrin, W. F., D. K. Caldwell, and M. C. Caldwell. 1994. Atlantic spotted dolphin--Stenella frontalis. In Handbook of marine mammals. Volume 5: The first book of dolphins (S.H. Ridgway and R. Harrison, eds.) p. 173-190. Academic Press, San Diego, CA.

Perrin, W. F., E. D. Mitchell, J. G. Mead, D. K. Caldwen and P. J. H. van Bree. 1981. Stenella clymene, a rediscovered tropical dolphin of the Atlantic. J. Mamm. 62:583-598.

Smith, T. D., J. Allen, P. J. Clapman, P. S. Hammond, S. Katona, F. Larsen, J. Lien, D. Mattila, P. J. Palsboll, J. Sigurjonsson, P. T. Stevick, and N. 0ien. 1999. An ocean-basin-wide mark-recapture study of the North Atlantic humpback whale (Megaptera novaeangliae). Mar. Mature. Sci. 15:1-32.

Torres, L. G., P. E. Rosel, C. D'Agrosa, and A. J. Read. In press. Improving management of overlapping bottlenose dolphin ecotypes through spatial analysis and genetics. Mar. Mamm. Sci.

Wade, P. R., and D. P. DeMaster. 1999. Determining the optimum interval for abundance surveys. In Marine mammal survey and assessment methods (G. W. Garner, S. C. Amstrup, J. L. Laake, B. F. J. Manly, L. L. McDonald, and D. G. Robertson, eds.), p. 53-66. A.A. Balkema, Rotterdam.

Waring, G. T., D. L. Palka, K. D. Mullin, J. W. Hain, L. J. Hansen, and K. D. Bisack. 1997. U.S. Atlantic and Gulf of Mexico marine mammal stock assessments--1996. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-NE-114, 245 p.

Waring, G. T., J. M. Quintal, and S. L. Swartz (eds). 2001. U.S. Atlantic and Gulf of Mexico marine mammal stock assessments--20Ol. U.S. Dep. Commer., NOAA Tech. Memo. NMFS-NE-168, 310 p.

Wursig, B., S. K. Lynn, T. A. Jefferson, and K. D. Mulliu. 1998. Behavior of cetaceans in the northern Gulf of Mexico relative to survey ships and aircraft. Aquat. Mamm. 24: 41-50.

Manuscript approved for publication 11 February 2003 by Scientific Editor.

Manuscript recieved 4 April 2003 at NMFS Scientific Publications office.

Fish Bull. 101:603-613 (2003).

keith D. Mullin

gregory L. Fulling

Southeast Fisheries Science Center

national marine fisheries Service, NOAA

3209 Frederic Street

Pascagoula, Mississippi 39567

E-mail (for K. D. Mullin): [e-mail]