aquatic mating strategies of the male pacific harbor seal (phoca vitulina richardii): are males...

MARINE MAMMAL SCIENCE, 20(3):639-656 (July 2004) 0 2004 by the Society for Marine Mammalogy

AQUATIC MATING STRATEGIES OF THE MALE PACIFIC HARBOR SEAL

(PHOCA VITULINA RICHARDII): ARE MALES DEFENDING THE HOTSPOT?

SEAN A. HAYES DANIEL P. COSTA

Ecology and Evolutionary Biology Department, University of California, Santa Cruz,

100 Shaffer Road, Santa Cruz, California 95060, U.S.A. E-mail: [email protected]

JAMES T. HARVEY Moss Landing Marine Laboratories,

Moss Landing Road, Moss Landing, California 95039, U.S.A.

BURNEY J. LE BOEUF Ecology and Evolutionary Biology Department,

University of California, Santa Cruz, 100 Shaffer Road, Santa Cruz, California 95060, U.S.A.

ABSTRACT

Compared to the harem and resource defense systems of terrestrial mating pinnipeds, males of aquatic mating species appear unable to monopolize females or resources. We investigated movements, acoustics, and aquatic territorial behavior of male harbor seals, Phoca uitdina richardii, in Elkhorn Slough, California, using VHF telemetry, hydrophones, and acoustic playback experiments. During the mating season 22 males increased time spent in the water and away from haul-out locations, exhibiting activity patterns similar to Atlantic subspecies. Two acoustic display patterns were observed. At one location multiple males aggregated to display with acoustic activity peaking one month before peak estrus. At two other locations, lone males displayed primarily during peak estrus. Acoustic display areas were non-adjacent with a mean i SE size of 4,228 t 576 m2, similar to harbor seal display patterns in the Moray Firth, Scotland. Underwater playbacks of male vocalizations were used to define territorial boundaries by inducing responses from territory-holding males. Four solitary males defended adjacent territories (mean area 39,571 ? 18,818 m2) along a travel corridor, similar to observations of harbor seals at Miquelon, Newfoundland. Acoustic display stations appeared to be subcomponents of larger territories. Males exhibited site fidelity to territories for at least 2 - 4 yr. Females moved through territories freely. The establishment of male-display territories along female-traffic corridors resembles terrestrial systems described as hotspot leks.

639

640 MARINE MAMMAL SCIENCE. VOL. 20. NO. 3. 2004

Key words: aquatic mating system, breeding behavior, horspot lek, harbor seal, Phoca vitulina, pinniped.

The environmental potential for polygyny (EPP) concept presented by Emlen and Oring (1977) seeks to explain mating system evolution. The principle is that males will attempt to maximize reproductive success by copulating with as many mates as possible, and that the male’s ability to do so is influenced primarily by ecological factors and secondarily by phylogenetic factors. The mating strategies of terrestrial mating pinnipeds, such as elephant seals (Mirounga), with their highly polygynous harem and resource defense systems, have become classic examples of how mating systems evolved in response to ecological factors (Bartholomew 1970, Stirling 1983, Boness 1991, Le Boeuf 1991). In these species, males’ ability to monopolize mates results from dense female clustering on stable island habitats where seals aggregate to breed and avoid terrestrial predators.

Among the phocid seals, fifteen of the eighteen species mate solely under water. Aquatic mating has been reported as an alternative strategy for multiple otariid species as well (Boness et al. 1993). Whereas less is known about these mating systems, most investigators agree that EPP is reduced. Although size is considered an advantage to mating in the terrestrial environment, that advantage is believed to be lost in the three-dimensional aquatic environment because sexual dimorphism is reduced and often reversed in aquatic mating mammals (Reidman 1990, Le Boeuf 1991, Boness et al. 1993). Additionally, females do not cluster under water, nor do stable harems tend to form on land, as these species often favor unstable coastal or ice substrates for parturition and resting over the space-limited island rookeries preferred by terrestrial mating species (Stirling 1975, 1983). In most aquatically mating phocids, males appear to have lost the ability to monopolize mates or the resources females require in comparison to the more ancestral characteristics of the terrestrial breeding species. A variety of mating systems and strategies have been described for these species including serial monogamy, scramble competition, resource and female defense polygyny, and lek polygyny. All of these scenarios and measures of reproductive success support the hypothesis that EPP is reduced in the aquatic environment (Stirling 1983, Boness et al. 1993, Coltman et al. 1998b).

The EPP model still predicts that males will t ry to monopolize or acquire multiple mates. However, the strategies used by males are uncertain due to the limitations of observing underwater behavior. The harbor seal, Phoca vitulina, offers advantages for studying male strategies, and how they evolve in response to various environmental variables, because this seal is found across the largest geographic range and on the greatest diversity of substrates of any pinniped. For this reason, many investigators have recently focused their efforts on several populations of harbor seals, providing a great deal of new but sometimes conflicting results. During the mating season, males of Sable Island and the Moray Firth populations of harbor seal have been observed spending more time closet to shore near female travel corridors and haul-outs (Coltman et al. 1997; Van Parijs et al. 1997; Boness et al., in review). Mating season behaviors also include the onset or increase of underwater acoustic displays by males for mate attraction (Van Parijs et a/. 1999, 2 0 0 0 ~ ) and male competition (Hanggi and Schusterman 1994, Nicholson 2000). Territorial behavior has been observed in two forms in areas with narrow bays or travel corridors. In the Moray Firth, acoustic recordings revealed lone males stationing on non-adjacent acoustic display areas of approximately 40-1 35 m2 (Van

HAYES ET AL.: HARBOR SEAL MATING STRATEGIES 64 1

Parijs et al. 2000S). At Miquelon, observations of surface behaviors revealed males defending larger underwater territories (approximately 1,600-30,000 m2; estimated from figures) with adjacent boundaries (Perry 1993). In contrast, males at Sable Island were observed patrolling overlapping zones that were several square kilometers in surface area, just offshore of female beach haul-ours (Boness et al., in review). Whereas similar behaviors exist, differences are apparent in the strategies used by males of the various populations. Despite the different patterns observed, a lek mating system has been suggested for all populations (Perry 1993, Hanggi and Schusterman 1994, Van Parijs et al. 1997, Boness et a/., in review).

In the current study, mating season behaviors in California were observed with several objectives in mind. The first was to detect behavioral changes that coincided with the mating season in eastern Pacific harbor seals for comparison with other populations. The second was to study male territorial defense by combining acoustic, observational, and VHF radio tracking methods similar to those used by Van Parijs e t al. (2000b), Perry (1993) and Boness et al. (in review) with interactive playback techniques (Hayes 2002). In this way we were able to compare our results to those of previous studies. Finally, based upon the results of this and other studies, the suggestion that harbor seals exhibit some form of lek mating system was addressed.

METHODS

Study Site

Behaviors of male harbor seals were studied in Elkhorn Slough (36'48'N, 12 1'47 ' W) and the greater Monterey Bay, California area (Fig. 1) during the spring mating seasons of 1998 through 2001. During this time approximately 300 harbor seals were using this slough as a travel corridor to access mudflats in order to rest (haul out), give birth, and presumably mate (M. Weise, J. T. Harvey, unpub- lished data).

Elkhorn Slough is a narrow tidal body of salt water extending approximately four kilometers inland. It varies in width from 100 to 300 m, with a maximum depth of about 12 m and average depth less that five meters. The western portion of the slough has large channels extending north and south that are maintained as small harbors for fishing and recreational vessels. Low frequency noise is loud and constant in this section. However most vessels cannot pass under a bridge crossing the slough several hundred meters inland. The shallow nature of the slough attenuates low frequency noise quickly, and harbor and wave noises are barely audible past one kilometer inland where the acoustic portion of the study was conducted. There are many biological noises from fish and invertebrates in the upper section, but the 0.1-5 kHz frequency band utilized by harbor seals is relatively quiet. Harbor seal roars attenuate quickly and are difficult to detect beyond 400 m from the source in Elkhorn Slough.

Territory structure and associated seal attendance patterns were observed in three ways: (1) male movements were observed with VHF telemetry during the 1998 and 1999 mating seasons; ( 2 ) male acoustic displays were recorded during the 1998 mating season; and (3) male territory defense was studied by conducting playback experiments during the 1999, 2000, and 2001 mating seasons.

642 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3, 2004

37.0 -

36.9

g 3 6 . 8 .

5 Vocalizationsdetected ’ 36.7.

No vocalizations

.z

36.6 .

36.5 122.0 121.9 121.8 121.7

Longitude (W)

Figure I. This map of Monterey Bay includes recording station locations from 1998 acoustic survey symbolized by diamonds with squares indicating location of vocalizing harbor seals. Inset is a blow-up of the region of Elkhorn Slough where the hydrophone array was installed. Letters along the hydrophone array represent regions of concentrated vocal activity.

Movements

VHF telemetry was used to determine the proportion of time spent among three activities for male harbor seals before, during, and after the mating season. Seal activities were broken down into three categories: (1) time spent away from Elkhorn Slough; (2) time spent diving in Elkhorn Slough; and (3) time spent hauled out in Elkhorn Slough. In order to attach VHF tags, harbor seals were captured by rapid deployment of a seine net in front of a seal haul-out, followed by immediate shore retrieval Ueffries et al. 1993). Animals were temporarily placed in individual hoop nets, weighed, sexed, and measured for standard length and axillary girth. Individually numbered cattle tags were placed in the interdigital webbing of each seal’s rear flippers. Using Loctite 422 (Loctite Corp.), head-mounted VHF radio transmitters were glued to the pelage of 22 adult males. The seals subsequently shed their tags during their annual molt in July. Standard length and mass for this study averaged 145 ? 3 cm and 91.3 5 4.9 kg, respectively. Mean axillary girth was 105 ? 2 cm (standard error reported with means throughout). Two condition indexes, body mass divided by length and axillary girth divided by length, were used to look at relative changes in size throughout the mating season.

In 1998 animals were tracked manually with an Advanced Telemetry Systems (ATS) hand-held receiver at multiple locations around Monterey Bay from 17 April to 13 June. A null-peak direction finding system with a pair of yagi H antennae mounted on a 5-m tower was used to detect animal presence and determine animal location along the slough corridor during 1998 and 1999. In 1999 an ATS Data Collection Computer I1 (DCC), connected to a VHF Receiver/Scannet, was placed along the slough corridor to monitor the ptesence/absence and activity of male harbor seals. The DCC was set to scan for each seal and record the total number of

HAYES ETAL.: HARBOR SEAL MATING STRATEGIES 64 3

pulses counted over one-minute intervals. Each tag frequency was scanned approximately four times per hour from 29 March through 1 July 1999.

For both years, data collection for an animal commenced on the day after tag deployment. If the DCC stopped detecting the tag, it was assumed that loss of the signal meant the tag had failed or fallen off, or the seal was no longer present. In 1999 data collected on or after the last day the tag was detected by the DCC were excluded from analysis.

The data were scored for three behaviors: Hauled out (H), Diving in the slough (D), and Absent (A). These behaviors were readily apparent in the 1998 data set that had been collected manually. In order to compare the percentage of time spent for each behavior, the data were sorted by time of day, and the ratio of time spent for each behavior was calculated for each seal at half-hour intervals. This was done in order to remove sampling biases where more data had been collected for certain times of day than others, or when there were more data for some seals than others.

During 1999 the DCC sometimes failed to count the maximum expected number of pulses when seals were hauled out. This was due to combinations of fluctuating receiver sensitivity, seal range, and animal position relative to the VHF receiver station. To distinguish between incomplete pulse counts for seals on land and shorter pulse sequences of diving seals, it was necessary to estimate a rhreshold value for the maximum number of pulses the DCC would typically count for a seal diving in the slough versus a seal that was hauled out. Dive and surface interval (SI) data manually recorded in Elkhorn Slough were used to determine mean -+ standard deviation duration of dive and SI times, 95 -+ 68 sec and 19 2 12 sec, respectively. The typical time for one dive/SI cycle was still less than two minutes and a DCC scan was conducted for one minute. As indicated by the large standard deviation, SI duration was highly variable. Therefore the threshold number of pulses per surface interval (TSI) was set high enough to incorporate 95% of all surface interval durations observed (36 sec) and used to determine an expected number of pulses that would be detected:

(pzllse ra.) (Mean S I ) sec (100 pzllse/min) (36 sec) TSI = - - = 60 puEses/scan.

As the receiver starts or finishes a scan it can trigger false pulse detection by the DCC. The manufacturer suggests esrablishing a user-defined threshold value for ignoring false pulse detections (TFP) below a certain number (Advanced- Telemetry-Systems 1998). The DCC data were sorted into columns by seal and arranged into 15-min bins. Data were transformed to a 0, 1, or 2 depending on whether the pulse rate was less than the TFP, between the TFP and TSI, or greater than the TSI, respectively. In order to better distinguish between seals that were hauled out and diving in the slough, and between seals that were diving in or absent from the slough, a second transformation was done, comparing the cell in question to the cell before and after it to determine the seals behavior (A, D, or H) (see Hayes 2002 for details).

Seasonal changes in male behavior were interpreted by breaking the season into three parts: premating, mating, and postmating. The premating/mating season split was defined by Walker and Bowen (1993), as the point when females presumably enter estrus after a mean lactation period of 24 d (Bigg 1969, Boulva and McLaren 1979). In 1999, the first pups in Elkhorn Slough appeared on 31 March (Greig 2002). Therefore, the date for transition from premating to mating was set at 24

60 sec 60 sec

644 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3 , 2004

April. Pup numbers peaked on 11 May 1999, six weeks after pupping began. By mid-May, most pups were larger than newborn size and no newborn pups were observed after this time. Estimates show that the last female entered estrus during the first week of June (Greig 2002). To be conservative, the estrous period was extended by two weeks and the beginning of the postmating period was defined as 21 June.

Acozcstics

On 18 March 1998 a bottom-mounted hydrophone array (1,000-m, 12-element, variably spaced, sensitivity -170 dB re 1 VIpPa) was positioned between two major seal haul-out sites (Fig. 1). Up to eight channels were recorded at any given time by one of two systems: a Tascam DA-38 Digital Audio Tape recorder (0.02-48.0 kHz) connected to the array through a Spirit Protracker mixedamplifier, or a TEAC XR- 7000 multichannel analog recorder (tape speed 9.5 cm/sec frequency range 0.01- 2.5 kHz). Channels were selected to ensure acoustic coverage of the greatest region. The array was monitored for 24-h periods approximately every 5 d throughout the mating season. During the daylight periods of recording sessions, seal counts at the major haul-out site were conducted on an hourly basis using a 1,300-mm Questar telescope.

Data collected with the Tascam were transferred digitally to a PC and filtered to make 8-channel 8-kHz AIFF format sound files. All multichannel files were then analyzed using Cornell’s Canary 1.5 bioacoustics analysis software with a custom “Beluga” DSP board (Charif et af. 1995). Files were scored for vocalization activity. Real time scrolling of 8 channels enabled simultaneous comparison of the entire area covered by the bottom-mounted hydrophone array. Canary’s localization function was used to assign position to the vocalizing seal based upon time-of-arrival differences and sensor locations with a hyperbolic least-squares fixing algorithm (Clark and Ellison 2000).

Acoustic surveys of the foraging areas were conducted at 5-km intervals between Santa Cruz and Monterey (Fig. 1). These surveys were performed at distances of approximately 1 and 6 km from shore on 2, 5 , and 24 June 1998. Recordings were analyzed to determine the relative distribution of vocalizing harbor seals offshore. Logistic constraints of weather and time limited the recordings to early morning hours on certain dates.

Territorial Behavior

Data from playback experiments were collected to determine the size and locations of territories, and the stability of territories during and between mating seasons. Complete details of the playback apparatus and methods used are provided in Hayes et af. (in press).

From 24 March to 1 September 2000, male responses to playbacks of male harbor seal roars were used to map the boundaries of male territories. This was done at locations where an identifiable animal was regularly observed. Calls were broadcast continuously until an individual responded. Once the animal responded, the playback was halted, the research skiff was allowed to drift with the tidal current to a new location, and playback resumed. This continued until the animal no longer stayed with the boat but remained at what appeared to be a territory boundary, performing surface displays, or the animal disappeared. The boat was then returned

HAYES ET AL.: HARBOR SEAL MATING STRATEGIES 645

to the point where the animal was displaying or last seen and playbacks resumed. If the animal resurfaced or attacked the playback apparatus, drifting was resumed. If the animal remained at the same point as before or again disappeared, the point was marked as a boundary and retested at later dates. The locations of all male responses were logged with a GARMIN 45 XL GPS set to record position at 1 minute intervals. A GARMIN differential receiver was employed during the first part of the study until the U.S. government granted civilian access to military-quality GPS signals on 1 May 2000. Photographs were taken of responding harbor seals for identification purposes with a 35-mm camera (Nikon N-90 with 80-300-mm lens).

Minimum convex polygon (MCP) analysis was used to determine territory boundaries and surface areas using data from the playback experiments and acoustic observations. Data were converted to UTM coordinates and loaded into CALHOME, a home range analysis package produced by and available from the US Forest Service Pacific Southwest Research Station and the California Department of Fish and Game (http://nhsbig.inhs.uiuc.edulweslhome_range.html). MCP analysis was conducted with all points included within the contours for playback experiments and 95% of points included within contours for the acoustic localizations. The remaining five percent of the acoustic localizations were excluded to compensate for localization errors associated with shallow hyperbolic intersection angles.

Results were analyzed using SYSTAT 8.0. Unless otherwise stated, the prob- ability of significance was set at ~1 = 0.05. All means are presented as mean 2 standard error (SE). Proportional values of behavioral data were arcsine transformed before conducting ANOVA analyses.

RESULTS

M ouements

Males were tracked for a mean of 31.5 2 3.2 d (Table 1). Males tagged later in the season (after 10 May, peak breeding season) carried their tags longer (Fisher exact test: P = 0.026). The data for all males that were tracked using a DCC in 1999 were pooled to determine daily ratios of time spent in the three behaviors: H, D, or A (Fig. 2). The daily proportion of time spent at the three behaviors changed with season. Pre- and postmating season levels were very similar. Males spent less time hauled out (ANOVA; F2,90 = 70.34, P < 0.000) and more time diving or absent during the mating season (Fig. 2). Regression analysis did not reveal a relationship between male size and the percentage of time spent in any of the three activities: H, D, or A.

During the pre- and postmating seasons, most tagged males were hauled out from 1200 to 2000, which exceeded time spent diving in the slough or absent (Fig. 3). During the mating season, male haul-out behavior was uniformly low throughout the day (Fig. 3a). Males still entered the slough during this time, but tended to remain in the water (diving) (Fig. 3b). Males were typically absent from the slough from approximately 2100 to 1100 (Fig. 3c) during all seasons. The 1998 radio tracking surveys revealed that when seals (n = 7) were detected away from Elkhorn Slough, they were rarely hauled out at other locations (2% of the time), indicating that when males were absent from Elkhorn Slough, they were at sea the majority of the time.

Male body condition declined over the mating season. Two recaptured males lost mass between captures at respective rates of 1.4 and 1.6 kg per day during the 1999


Table 1. Summary statistics of study males. 1999 animals with T designations did not carry VHF tags.

# days Mass Standard Axillary Male ID Date range tracked tracked (Kg) length (cm) girth (crn)

1998 341 840" 643 663 603 304 624

1999 T407 T710 "709 T717 T716 477 1 4978 4616** T745 4856 4595 4736 4819 4877 4877** 4754 4896 4796** 4717 4040 4109 5693 5915 T832 T370 T843

411 8/98 4/29/98 5/13/98 511 3/98 5/13/98 5/22/98 5/22/98

111 1/99 111 1/99 111 1/99 111 1/99 111 1/99 3130199 3130199 4120199 4/26/99 5/3/99 513199 5/3/99 5/3/99 5/3/99 5/12/99 5/18/99 51 18/99 51 18/99 5/18/99 5/25/99 6/3/99 6/3/99 6/3/99 6/2/99 6/2/99 6/2/99

5/26/98 6/13/98 5/25/98 5/26/98 61 13/98 61 13/98 6/13/98

4120199 5/12/99 5/3/99

5/3/99 51 10199 5/25/99 7/1/99 6/8/99

6/28/99 7/1/99 7/1/99 7/1/99 7/1/99 7/1/99 7/1/99 7/1/99

38 45 12 13 31 22 22

22 44

13(59)

1 8

23 60 37

42 45

46459) 45 38 29 29 29

68.4 104.2 109.4 97.4 89 83.2 71.6

55.8 85.6 77.4 97.6

146.2 120.6 90.8

145 64.2

100.2 137 74.0 94.4 63.1 55.8 86.2 92.4

105.6 104.4 63.0 82.4

109.9 90.6 72.1 83.2 76

127 98 153 113 153 145 140 137 118 94

127 99 135 115 137 116 150 107 163 119 159 149 159 135 94 144 106 166 130 138 101 143 98 123 96 120 93 142 93 147 98 149 116 153 107 129 89 158 103 158 117 166 105 136 102 138 109 149 108

* Animal 840 was matched through molecular techniques to a territory male. ** Recaptured animals. Animals 4616 lost all tags, was recaptured and tagged as 4796

on 511 7/99 and later reidenrified through molecular techniques.

mating season (Table 1). An index of axillary girth-length yielded a significant negative slope (ANOVA: F1,24 = 6.304 P = 0.020, Y' = 0.231) indicating that seals were becoming thinner as the mating season progressed.

Acoastics

Recordings were made in Elkhorn Slough at biweekly intervals from 9 April through 7 June 1998. There was a bimodal distribution of vocalization activity


Figwe 2. Mean 2 SE proportion of time spent either hauled out, diving in Elkhorn Slough or absent from the slough for male seals radio tagged in 1999 during the premating (n = 3), mating (n = 13) and postmating season (n = 9).

throughout the day before and during the mating season, with major peaks occurring between 0400 and 0600 and between 2000 and 2300 (Fig. 4). Harbor seal sounds were concentrated in three locations along the hydrophone array. At areas B and C (Fig. l ) , it appeared that only one seal was vocalizing at any given time with no overlap of calls. Vocalization rates at these locations peaked on 22 May during the peak mating season and dropped off sharply after that. The vocalization pattern at area A was different. It was apparent from the many overlapping calls that many seals were gathered in this area and displaying simultaneously. This was confirmed visually during daylight hours when 10-20 seals were often seen at the surface in this area. Vocalizations at area A were more frequent and activity peaked a month earlier on 24 April at the onset of the mating season (Fig. 5).

The acoustic survey of Monterey Bay revealed little acoustic activity in the offshore recording sites. A few distant vocalizations were detected at three of the northern stations (Fig. 1). Nighttime operations along a coast with strong surf conditions inhibited our ability to conduct recordings within 1 km of shore.

Territorial Behavior

Vocalizations from two 24-h recording sessions, 25 April 1998 and 9 May 1998, were localized in two-dimensional space. The vocalizations were clustered at three locations: areas A, B, and C. Each location or acoustic display station was separated from the next by 100-300 m and varied in area from 1,173 to 6,493 m2 (Table 2 , Fig. 6). Recordings from the bottom mounted hydrophone array were only made during the 1998 season.

Playbacks were used to identify territorial males along the slough corridor during 1999, 2000, and 2001. The territories of four male harbor seals (WB, DG, DJ, and #840) were extensively mapped out during the 2000 mating season (Table 2, Fig. 6). Male WB was found in the harbor area during the 1999, 2000, and 2001 mating season. The second male was biopsied during a playback in 2000 and

648 MARINE MAMMAL SCIENCE, VOL. 20, NO. 3 , 2004

.. .. . Pre-mating (n=3) - Mating (n=13) _ _ _ Post-mating (n=9)

I .o Hauled out a.

,rf -A\ 0.8

00 04 08 12 16 20 00 1 .o

Diving b. 0.8 1

00 04 08 12 16 20 00 I .o

0.8

0.6

0.4

0.2

0.0

C.

w 04 08 I2 16 20 00

Time of Day

Figure 3 . Proportion of time males spent either (a) hauled out, (b) diving in, or (c) absent from Elkhorn Slough as a function of time-of-day during the premating, mating, and postmating season.

identified through genetic techniques (Hayes 2002) as a male tagged in 1998 with VHF tag #840. He was regularly detected through VHF tracking in the same region of the slough in 1998 as observed with playback techniques in 1999, 2000, and 2001. The third male, SG, was observed in 1999 and 2000. However, a new male occupied SG’s territory in 2001. The fourth male, DJ, was not photographed with sufficient quality to confirm markings between seasons. The seal that occupied DJ’s territory in 1999 and 2000 had similar pelage pattern-light spots on dark coat-and displayed similar behavioral patterns (e.g., this animal was more reclusive than the other three animals). He rarely surfaced and generally performed underwater displays including speaker attacks and “jaw claps.” This seal’s territory was in close proximity to a large breeding haul-out. Potential disturbance issues inhibited identification and mapping efforts at this location and this territory size was underestimated.


+ Vocalizations + Seals hauled out

50 100 0 P - r;j

40 80 Z

R 'T E .- B g ; B

VI

30 60

.- w 20 40

3 10 20 8 B

> a

z 0 0

00 04 08 12 16 20 00

Time of day

Figare 4. Mean 2 SE number of vocalizations detected from 5-min samples recorded on an hourly basis across the region of the slough covered by the bottom-mounted hydrophone array. Data are taken from five recording sessions conducted between 9 April and 7 June 1998. The second y-axis (right side) is the number of seals hauled out at the primary haul- out (west of area C , Fig. 11, during daylight hours.

DISCUSSION

During the mating season, we observed changes in display behavior, activity patterns and body condition in the male Pacific harbor seal. Male body condition declined as the mating season progressed. At the same time, males spent less time hauled out and more time in the water. The timing of these changes in behavior is consistent with the estrous cycle of females from this population (Greig 2002). These observations, in conjunction with observed increases in male vocal behavior, indicated that males were investing more time performing aquatic mate attraction and searching behaviors and less time foraging. Similar behaviors have been reported in other harbor seal populations. Harbor seal males at Sable Island reduced foraging activities in deep water to invest more time in mating displays or mate- searching activities in shallow water (Coltman et al. 1997; Coltman et al. 1998~; Boness et ul., in review). During the mating season in the Moray Firth and at Sable Island, males switched from foraging dives to display dives, but did not spend more time at sea. These males also restricted their movement patterns and contracted their home ranges (Van Parijs et al. 1997; Boness et al., in review). These observations indicated that reproductive success of male harbor seals for all populations studied was contingent upon some aquatic behavior performed by the males.

Acoustic behavior of male harbor seals in Elkhorn Slough peaked during the mating season in this study. Two different vocalization patterns were observed, suggesting two different functions for the male call. Approximately 20 males were observed vocalizing together in one location (area A, Fig. 5, 6). Vocal activity at area A was high in April, prior to the onset of the mating season and declined in May as the majority of females entered estrus. It is possible that the males had clustered to compete for a vacant territory. The apparent winner of this competition, male #840, retained the territory in the following years and the tight clustering of males was not observed again. The timing of this clustering is similar to that reported by Nicholson (2000), who observed adult and subadult


vr .g 20

f l 5

a

2 9 c 10

8

.Q

g 5

0

A B C A B C A B C A B C A B C

4/9/98 4/25/98 5/9/98 5/22/98 6/1/98

Figure 5 . Mean ? SE number of vocalizations recorded per 5-min sampling period during 19 h from 1900 to 1300. The x-axis gives the area of the array on which the vocalizations were detected (A, B, C; see Fig. l), and the date recorded.

males socializing and vocalizing together. These observations indicate that male vocalizations play a role in male-male competition. This is supported by the results of Hayes et al. (in press), where males were observed responding aggressively to playbacks simulating intruders in their territories.

Vocalizations likely play a role in mate attraction as well. The second vocalization pattern observed consisted of lone males displaying at the onset of estrus with vocal activity peaking in May and declining in early June (areas B and C, Fig. 5, 6). This behavior was similar to that described for seals in the Moray Firth (Van Parijs et al. 1999, Van Parijs et al. 20006) and presumably represented adult males displaying from their territories. The diurnal pattern of vocalizations in the slough corresponded with the haul-out patterns for the area. The greatest number of seals observed resting at the main haul-out occurred in late afternoon, corresponding to the point of minimum acoustic activity. Vocalization activity increased with the number of females transiting along the slough corridor. This agreed with observations by Van Parijs et al. (1999) that males in Scotland regulate their behavioral patterns to maximize encounters with estrous females.

Two different patterns of male spatial distribution were observed along the slough corridor. In 1998 small spatially discrete acoustic display areas occupied by lone males were observed. Playback mapping experiments conducted along the slough corridor in 1999, 2000, and 2001 revealed that lone individuals were defending large adjacent territories centered at the locations where male vocalizations were detected in 1998. Previous studies on harbor seals reported different behaviors in the strategies used by males of the different populations. In the Moray Firth harbor seals established small acoustic display areas that were non- adjacent and spatially discrete (Van Parijs et al. 20006). Miquelon harbor seals established large adjacent territories near haul-out sites and along travel corridors (Perry 1993). The results of this study indicate that the previously described divergence in strategies between subspecies may not exist. Individual male harbor seals in Elkhorn Slough hold large adjacent territories within which they maintain small acoustic display areas. The present study suggests all of these strategies may


Table 2. Polygons.

Area Area (m2) Date Number of vocalizations

Size of acoustic display areas and male territories based on Minimum Convex

A

B

C

4,375 4/25/98 3,289 5/9/98 4,021 4/25/98 5,860 5/9/98 1,327 4/25/98 6,493 5/9/98

195 141 16 17 23 54

~

Animal Area (m2) Date range observed ID method

DJ 5608

SG 13145

#840 864 12

WB 53839

511 5/00-8/28/00 6/1/99-7/ 12/99 5/4/00-9/2/00

5/14/99-6/17/99 41 110 1-4/2710 1

3/29/00-8/20/00 717199-7/14/99

4128198-611 3/98 4/1/01-4/27101

5/10/00-9/2/00 6125199-7/11/99

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be pursued by the two Atlantic populations of harbor seals; confirmation of this could be obtained by repeating this multiapproach technique on those populations. Finally, in comparison to the behaviors of seals breeding along travel corridors and narrow bays, male seals along the open coast of Sable Island established large overlapping “patrol areas” (Boness et al. in review). From these comparisons we conclude that the environment in which they breed influences the strategies which male harbor seals pursue.

The reason males defend territories in Elkhorn Slough is not clear. The only observed potential value of male territories is proximity to the haul-out sites and position along travel corridors. Perry (1993) suggested that males used the territories’ proximity to the haul-out as a resource and that the males try to harass females or restrict their access. Although it may be possible for males in Elkhorn Slough to periodically intercept females, it would seem impossible for them to regulate passage along the corridor due to the width of the corridor and the number of animals that travel through it. It is likely these territories are only valuable in terms of intrasexual competition among males and maximizing exposure to females, but not as a resource relevant to female needs.

Aquatic territorial behavior in phocid seals has been documented in several polar species, including Weddell seals, Leptonychotes weddellii (Hill 1987, Morrice et ul. 1994), bearded seals, Erignathus barbatas, (Cleator et a/. 1989, Cleator and Stirling 1990, Van Parijs et al. 2003) and has been suggested for leopard seals, Hydwrga leptonyx (Stirling and Sinniff 1979). The Weddell seal, which mates on fast ice, establishes a territory under a breathing hole, which is clearly an example of resource defense. However, the other pack-ice breeding species may be limited to establishing acoustic display stations similar in function to that observed for harbor seals in this and other studies.


> \ Breeding haul-out

/ \

H 200 m I /

Figure 6. Upper map gives locations and MCP-based boundaries where territorial males responded to playbacks during the spring 2000 mapping sessions. Lower map provides MCP-based boundaries of vocalizations recorded at each of three areas along hydrophone array in 1998 on 25 April and 9 May.

This study, along with work by Perry (1993) and Van Parijs et al. (20006), demonstrated interannual site fidelity to territories in pinnipeds. The present study indicates that animals can maintain a territory for at least four years, the longest territory tenure observed in a breeding male for an aquatic species. During the year 2000, playback experiments were continued into September. While the intensity of male responses had decreased, there was no indication that seals had stopped defending their territories. Possibly, these animals maintained or defended their territories year round; confirmation requires further study. Mating tenure is especially important when considering lifetime reproductive success for males, because they have much lower annual polygyny levels when compared to terrestrial mating pinnipeds (Coltman et a/. 19986, Hayes 2002).

Several researchers have suggested a high potential for lek mating systems to evolve among the aquatic mating phocids (Stirling 1983, Boness 1991, Le Boeuf 1991). In harbor seals males gather to display. Whether this display serves to attract females or repel males is unclear. However, it probably serves both functions and suggests lekking (Hanggi and Schusterman 1994; Van Parijs et al. 1999; Nicholson 2000; Boness et al., in review). The definition of gathering and the size of the area are open to interpretation; however, the spacing of males in this study is within the ranges observed for avian and ungulate lek systems (Clutton-Brock et al. 1993, Hoglund and Alatalo 1995). The only apparent resource in harbor seal territories is advertising space for performing acoustic displays. In Elkhorn Slough males establish


territories along a female traffic corridor. Along the open coast of Sable Island males patrol offshore of female pupping beaches. In both cases this phenomenon is best described as a hotspot lek and has been observed in several terrestrial species, including ochre-bellied fly catchers (Westcott 1997), sage grouse (Centrocercus uropbasianus) (Gibson 1996), and fallow deer ( D a m dama) (Apollonio et al. 1998).

Not all males in this population of harbor seals participated in the lek, and instead appeared to pursue other strategies. None of the animals instrumented with VHF tags during the 1999 mating season were observed responding during playback sessions. These males spent significantly more time away from Elkhorn Slough, and less time hauled out during the mating season, indicating that these tagged seals did not hold territories in the slough. It is possible they were pursuing females on the foraging grounds. Alternatively they might have been defending territories outside Elkhorn Slough or patrolling the coast similar to seals off Sable Island.

The acoustic survey of Monterey Bay, although conducted after the peak in vocalization activity for the slough, indicated that males did not display much, if at all, in open water. VHF telemetry and TDR studies of harbor seal movements in Monterey Bay show that the survey points were within the region of normal harbor seal foraging grounds (Eguchi 1998). A few distant harbor seal calls were heard at some of the northern survey points and i t is possible that harbor seals were displaying closer to shore. However, it appears Monterey Bay males do not establish territories in open water. Van Parijs et al. (1997) conducted an open water survey of the Moray Firth and found males calling throughout the region near female haul- outs and travel corridors, as well as on foraging grounds. At Sable Island most of the males were observed reducing foraging and increasing time spent patrolling near shore at the onset of the mating season (Coltman et al. 1997; Boness et al., in review). However, diving and energy data indicated that a few males continued foraging throughout the mating season. Interestingly, these were the males who achieved the highest level of reproductive success in the Sable Island population (Coltman et al. 1999). It is not clear why males from Elkhorn Slough do not display on the foraging grounds in Monterey Bay, but one possible explanation is bathymetry. In Montetey Bay the continental shelf drops off rapidly to depths exceeding hundreds of meters within one to two kilometers west of Elkhorn Slough. However, many of the survey points for this study were conducted in water depths comparable to the Moray Firth and Sable Island sites. Lack of male display effort on the foraging grounds may also be a function of low female density or the presence of large predators such as great white sharks (Carcbarodon carcbarias) and killer whales (Orcinus orca).

Several other strategies have been suggested for male harbor seals besides territory defense. These include satellite males without territories attempting to intercept females on their way to sea. In the case of areas where territory formation may be inhibited by a lack of topographic landmarks, a scramble/searching strategy may be employed (Stirling 1983; Perry 1993; Coltman et al. 1999; Boness et al., in review). The observations of multiple male strategies within one population are unsurprising. Similar behaviors have been observed in other species where some males have been shown to lek, while others maintain solitary territories, appear to be floaters, or act as satellites to territorial males (Westcott and Smith 1994, Van Patijs et al. 2003).

The role of female choice in harbor seal mating systems is unclear but likely to be important. Coltman et al. (1999) showed low levels of polygyny for an island breeding population of harbor seals. Perry (1993) also observed low levels of


reproductive success in a population breeding in a habitat similar to Elkhorn Slough. However, this study utilized DNA fingerprinting techniques and small sample sizes; paternities were confirmed for only a few cases. One might predict that the establishment of territories along travel corridors might increase the polygyny levels beyond that observed by Coltman et al. (1999) in the Sable Island population where males appeared to have large overlapping patrol areas. Boness et al. (in review) observed that females were fertilized by males several kilometers from the females’ known haul-out site. Because males that were actively patrolling the female haul-out sites were no more likely to sire the pups of local females, Boness et al. (in review) concluded males were not able to force copulations and female choice was playing a role in mating decisions.

It is rare that a species’ mating system will fit a discrete definition; rather it often falls along a continuum of subtypes. This study, along with the work of others, places harbor seals in the category of lek type systems. The evolution of a lek mating system in an aquatically mating pinniped demonstrates the influence of the environment on mating system evolution and reflects changes in response to mating in an aquatic three-dimensional environment. Specifically, this has led to the loss of mating harems and the underwater clumping of males to display. Associated with this has been a decrease in polygyny levels, and subsequent reduction in sexual selection pressure. Finally, female choice appears to be playing a strong role in this system.

ACKNOWLEDGMENTS

This study encompassed several years and could not have been completed without the help of many people. We would like to extend special thanks to Jennifer Burns, Don Canestro, DJ, John Douglas, Tomo Eguchi, Jennifer Gafney, Denise Greig, Tracey Goldstein, Nancy Gong, Scott Hansen, Anu Kumar, Michelle Lander, Brett Long, Stori Oates, and Brandon Southall. We would also like to thank two anonymous reviewers for their helpful comments. Funding was provided by the Animal Behaviour Society, Theodore Roosevelt, American Cetacean Society, Sigma Xi, Friends of Long Marine lab, The Meyers Trust, and GAANN research funds. S. Hayes was supported by a GAANN fellowship during 1998 and 2001 and TA-ships from UCSC during 1999-2000. Koshrow Lashkari and Dave Mellinger of MBARI provided acoustic equipment and logistical support. Animal studies were approved by NMFS permit #974 to J. T. Harvey, and by the UCSC Animal Use Committee using NIH guidelines.

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Received: 12 September 2003 Accepted: 3 February 2004

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