FORAGING BEHAVIOR OF LACTATING

GUADALUPE FUR SEAL FEMALES

Juan Pablo Gallo-Reynoso!, Ana-Luisa Figueroa-Carranza2 and Burney J. Le Boeuf

J Centro de Investigaci6n, en Alimentaci6ny Desarrollo, A.C. Unidad Guaymas, Carretera a Varadero Nacional km 66, Col. Las Playitas, CP 85480 Guaymas, Sonora, Mexico,

CE. jpgallo@ciadmx 2 Area de Protecci6n de Flora y Fauna, Islas del Golfo de California, CONANP, Calle Isla del Peruano

esquina Calle Isla de la Rasa, Col. Lomas de Miran/at: CP 85450 Guaymas, Sonora, Mexico, CE: afiguero@conanp,gob.mx

3 Office for Research and Institute of Marine Sciences, 29 Clark Kerr Hall, 1156 High Street, University of California, Santa Cruz. California 95064 USA, CE: leboeu./@ucsc,edu

Resumen: El objetivo de este estudio fue el conocer el comportamiento alimentario de las

hem bras de lobo fino de Guadalupe, Arctocephalus townsendi. Se obtuvo la localizaci6n en el

mar de tres hem bras adultas y el compOltamiento de buceo de una hembra adulta haciendo uso de

instrumentos registradores del tiempo de buceo con localizaci6n geognifica (GLTDRs). Las hef!1bras

se alimentaron en la Corriente de Californ ia al sur de la Isla de Guadalupe. La di stancia media del

viaje redon do fue de 2 ,375 ± 1,389 km. La distancia a la zona de alimentaci6n fue de 444 ± 15 1 km. El primer viaje de alimentaci6n fue de 10 ± 4 dfas . EI Segundo viaje de alimentaci6n fue de 19 ± 8 dias. Los viajes de alimentaci6n combinados promediaron 14 .4 ± 8.3 d ias, durante los cuales la velocidad del nado fue de 1.9 ± 0.1 m/s. El tiempo de transito comprendi6 el 47.9%, el tiempo de buceo fue de 36.2%, y el tiempo de descanso el 1 5.9%. El tiempo de alimentaci6n (tiempo ocupado en la zona de alimentaci6n , que incluye tiempos de tninsito y buceo) fue el 75% de todo el tiempo pasado en el mar. La profundidad promedio alcanzada por una hem bra fue de 17 ± 10 m. La duraci6n promedio de los buceos fue de 2.6 ± 1 .4 m in. EI intervalo en superficie entre buceos fue de 2 min. El tiempo de fondo promedio fue de 1.4 min. Los buceos estaban organizados en trenes de buceos; se registraron 23 trenes de buceos, con una duraci6n promedio por tren de buceo de 3 :04 ± 2 :30 h. El promedio de buceos por tren de buceo fue de 63 ± 60 buceos. La hembra buce6 durante la noche y transit6 durante el dia. Los buceos comenzaron tfpicamente alrededor de las 2030 h y terminaron alrededor de las 0530 h. EI patr6n de buceos y la d istancia viaj ada por las hem bras lactantes para alimentarse es similar al de otras especies de lobos finos.

Palabras clave: Arctocephalus townsendi, Comportamiento de buceo, Isla Guadalupe, Lobo frno de Guadalupe, localizaci6n en el mar, Mexico, viajes de alimentaci6n .

Abstract: The aim of this study was to elucidate the foraging behavior of female Guadalupe fur seals , Arctocephalus townsendi. The location at sea of three adult females and the diving behavior of one adult female were obtained using geographic location time-depth recorders (GLTDRs). The females fed in the California Cun'ent south of Isla de G uadalupe. Mean total

.......................................... _ ..... . Lorenzo, C., E. Espinoza y J. Ortega (eds.), 2008. Avances en el Estudio de los Aifamijeros de Mexico. Publicaciones

Espeeiales, Vol. n, Asociaci6n Mexicana de Ma5tozoologfa, A, c.. Mexico, D. F.

596 Foraging of Guadalupe fur seal

distance traveled was 2,375 ± 1,389 km. Distance to feeding grounds was 444 ± 151 km. The first feeding trip averaged 1 0 ± 4 days. The second feeding trip had a mean duration of 19 ± 8 days. Feeding trips combined averaged 14.4 ± 8.3 days during which the swimming speed was 1 .9 ± 0.1 m/s. Transit time accounted for 47.9%, diving time was 36.2%, and resting time was 15.9%. Tin1(�

spent foraging (time spent in the foraging area which inc ludes some transit and diving times) was 75% of all the time at sea. Mean dive depth of one female was 17 ± 10 m. Mean dive duration was 2.6 ± 1.4 min. Mean surface interval between dives was 2 min. Mean bottom time was 1.4 min. Dives were organized in bouts; 23 bouts were recorded with an average duration of3 :04 ± 2 : 30 h . Mean number of dives per bout was 63 ± 60 dives. This female d ived during the n ight and tran­sited during the day. Diving typically started around 2030 h and ended around 0530 h. The diving pattern and d istance traveled by nursing females to forage is similar to that of other fur seals.

Key Words: Arctocephalus townsendi, Guadalupe fur seal, Diving behavior, foraging trips, Guadalupe Island, location at sea, Mexico.

INTRODUCTION

Until recently, m igrations and feeding areas used by p innipeds were documented by the observa­

tion offree ranging individuals at sea. Sightings of stranded, marked or tagged ind ividuals at non­

rookery locations (Condit and Le Boeuf, 1984) were used to describe m igratory routes. Radiote­

lemetry was developed to locate animals and describe their distribution and movements while at

sea, which provided recovery informat ion (Loughlin et at., 1987). The deve lopment of micro pro­

cessor based techniques has given new insight into the movements and dispersal of marine ma­

mmals (DeLong et aI., 1992) integrating sampling protocols on sensors to register simultaneously

water temperatures, pressure and time, and storing data on electron ic m emory. Lately the use of

satel l ite -micro transmitters and sensors has given new tools for the description of individual

movements and dispersal over long distances and on water column movements. The aim of this

study was to use microprocessor based techniques to describe the track, location, duration and

diving behavior during foraging trips of lactating Guadalupe fur seals Arctocephalus townsendi.

The Guadalupe fur seal is an endemic and endangered species in Mexico, and is protected by

NOM-059-sEMARNAT-2001 (DOF, 200 I), the species was subject to heavy exploitation until its su­

pposed extinction at the beginning of the xx century, the species is making an extraordinary come

back due to conservation efforts (Gallo-Reynoso, 1994). There are only two rookeries where this

species breeds, the east side of Isla Guadalupe and the southeast coast oflsla San Benito del Este

(Marav i lla and Lowry, 1999) . Single animals, however, have been observed at various islands and

local ities along the coast of Baja Cal ifornia and Cal i fornia (Stewart et al., 1987). Guadalupe fur

seals are rarely seen at sea. Since) 967, there have been only three individuals seen and reported

in the Southern Cal ifornia Bight (Brownel l and DeLong, 1968; Bonnell et aI., 1980), four at

Southeastern Faral lon Is land (Hann i et aI., 1997) and one adult female at Point Lobos (Lander et

al., 2000). Several Guadalupe fur seals have been observed in the Channel Islands (Stewart et at.,

1987), including a newborn pup at San Miguellsiand (Melin and DeLong, 1999). Fur seal sightings

Gallo et at. 597

in Mexican waters include one seal in the open sea between Isla Guadalupe and Islas San Benito

(Rice et aI. , 1 965), several fur seals on Isla Cedros and Islas San Benito (Cruz, 1986), one juveni le

at Isla Asunci 6n (P. Pyle, pel's. comm., 1 994), and several groups of females over the continental

shelf of Baja Californ ia, near Islas San Benito and Isla Cedros in July 2004 (J.P.G., personal

observation). Som e subadult males have been observed inside the Gulf of Cal i fomi a at Los Islotes,

Baja Califomia S ur, Islas Encantadas, Baja California (Marav illa, 1997) , a fur seal stranded at

Bahia Bacochibampo, Sonora (Aurioles et aI., 1993), a juvenile female that stranded alive on a

beach near Zihuatanejo (Aurioles-Gamboa and Hernandez-Camacho, 1 999), and a subadult male

at the northern point of Isla San Pedro Nolasco. Sonora in May 2005 (lP.G., personal observa­

tion). These records show that Guadalupe fur seals are capable of swimming long distances from

their home rookery while foraging at sea, but it is not clear where lactating females go to forage

between nursing their pups on the rookery as wel l as the cost associated with nursing.

Other fur seals, l ike the northern fur seal, Calforhinus ursinus, forage from 100 km to 258 km

or more from the PribilofTslands (Gentry and Kooyman, 1986; Robson et aI., 2004). Lough lin et al. (1987) reported a round trip of 740 km by a nursing female from St. Paul Island. A distance of

over 70 km has been recorded from radiotracked northern fur seal females off San Miguel Island

(Antonelis et aI., 1990). Other northern fur seal females were observed at d istances of 80 to 1 60

km from St. Paul Island (Goebel et aI. , 1991). Australian fur seal females (A . pusillus doriferus)

were observed at 100 km from the rookery over Bass Strait (Arnould and Hinde l l , 2001) . Long

distance movements of 2 ,300 to 2,740 Ian have been reported in subantarctic fur seals, A. gazella,

in the Southern Ocean (Bester, 1 989; Goldsworthy and Shaughnessy, 1 989). A distance of more

than 500 km from the rookery has been recorded for Juan Fernandez fur seal females (Francis et

al. , 1 998). In this paper we describe the foraging location of three Guadalupe fur seal females and

their diving characteristics obtained with diving instruments and the implications that this has for

the conservation.

METHODOLOGY

We instrumented seven lactating females with time-depth-Iocation recorders or GL.TDRS (DeLong

et af., 1992; Hi l l , 1993). These females were depm1ing on their first or second feeding trip after

giving bi r1h at Isla de Guadalupe in June-July 1992 and July 1 993 .

Female capture

Females were captured early in the morning on days when the tide was low. Two people, each

one carrying a hoop-net offme mesh nylon 1 .5 m deep and 90- 1 20 cm diameter (Fuhrman Diver­

sified, Seabrook, Texas) crawled toward the chosen female keeping a low profile. One person

netted the fem ale whi le the other served as back up. Once captured, two other persons armed with

2.5 m white pine poles repelled attacks from territorial bulls. The female was taken outside the

territory to reduce disturbance.

598 Foraging of Guadalupe fur seal

Immediately after capture the seals were weighed with a 100 kg industrial spring scale (Jogua

Din, Basculas Nuevo Leon). Each animal was held on a restraining board with a detachable and

neoprene-padded neck brace to prevent the animal from backing up (Gentry and Holt, 1982).

Standard length (tip of nose to tip of tai l) and other body measurements were taken (ASM, 1967).

The general condition of the female was recorded as well as any scars or notches in the flippers

(Gallo-Reynoso and Figueroa-Carranza, 1996).

Female condition

"Pita", "Maya" and "Piri" were heavy, large and probably multiparolls females (mean weight

= 52.5 ± 1 .8). "Cata" weighed 54 kg, and was probably a multiparous female but had no pup.

"Lupe", "Atl" and "Rita", were small, slender and probably younger and less experienced than the

other females (mean weight = 4 1 .2 ± 1.3; Gal lo-Reynoso and Figueroa-Carranza, 1 996).

Instrumentation

After cleaning a section ofthe dorsal fur with acetone, an 8 cm wide plastic mold was placed

on the dorsal midl ine of each female above the shoulders. The mold was filled with marine epoxy

(Evercoat Ten-set, Fiber Glass-Evercoat Co. , Cincinnati , Ohio) and the adhesive was worked

under the hair, fol lowing the method of Le Boeuf et al. (1988) and Costa et al. (1989) . Each

female was instrumented with an Mk3e geolocation t ime-depth recorder (15 x 2.6 cm diameter,

1 36 g; Wildlife Computers, Woodinvi l le, Washington) and a very h igh frequency (VHF) 150 g

radio-transmitter (6 cm length x 2 cm diameter; 1 48-149 MHz; Advanced Telemetry Systems;

Bethel , Milmesota). Approximate total weight of the instruments was 386 g. Attachment was by

means of a stainless steel hose clamp glued into the marine epoxy. All subjects were marked with

b lack dye (N ice'n Easy, C lairol, U ltra blue) or with white cream bleach (Well ite, Wel la Corp.,

Englewood, New Jersey). While restrained, the animals were kept wet by pouring seawater over

them and by keeping wet towels underneath them. Their heads were covered with a b lue polyethy­

lene tarp to prevent injury to the eyes by the strong glare and sunl ight.

Time Depth Recorders sampling protocol was set at: depth every 30 seconds to obtain good

descriptions of the dives, and water temperature (0C) every 60 seconds. Condition: wet or dry. The

mean n umber of geolocation readings extracted was 4,102 ± 2,135. The instrument internal clock

was calibrated before and after each deployment. Software provided by Wildlife Computers was

used to download the data from the GLTDR to a lap-top computer for in itial analyses.

Recovery of instruments

Arrival and departure of females was monitored with a Telonics Inc. (Mesa, Arizona) TR-2

scanning telemetry receiver, as wel l as by dai ly visual survey� of the rookery (Costa et at., 1989).

Females were recaptured upon return from feeding trips lasting 1 5-28 days. Animals were weighed

and measured again, and the instrument and epoxy cradle removed. We applied waterproof, non­

fragrant, hypoallergenic baby sunblock lotion (spI" 29) to the exposed skin to prevent sunburn

while the females were on land (Banana Boat, Sun Pharmaceuticals, Ltd.). New fur was observed

Gallo et at. 599

growing 8 days after removal.

Two of the four females carrying GLTDRS were not relocated owing in part to the rough oceano­

graphic conditions prevailing during June to August of 1 992 an "El N ino" year. The first instru­

mented female never came back to her pupping site and her pup was lost by a combination of high

surf and h igh tide on July 4. The other female was observed on the rookery nursing her pup on 8

July. We attempted unsuccessfully to recapture her. The female went to sea for a day and returned

to nurse her pup for two more days then this female departed on 11 July for a long second feeding

trip of more than 28 days . Her pup was found dead on 9 August; the pup was emaciated with a

weight of 4.7 kg below the mean weight of 5.2 ± 0.8 kg (n= 13) of a newborn pup. The female had

not returned to the rookery when we left the island, but was observed the fol lowing breeding

season (1993) with a pup . Two of the four GLTDRS were recovered but no d ive data were logged due

to a faulty salt switch. Nevertheless, we obtained geolocation data from these two GLTDRS.

During the breeding season of 1993, three females were instrumented with GLTDRS, only one

of which was recovered. The first instrumented female did not return while we were present. Her

pup was still alive and in good shape after 33 days of fasting. The second instrumented female

returned after 1 4 days at sea. Th is GLTDR was successfully recovered. The third instrumented fe­

mal e returned after 1 6 days at sea. Her behavior was erratic, coming and going from telTitory to

territory, but never coming back to the ten'itory in wh i ch she had given birth . She was last heard on

the radio on 14 August to the south ofthe study area in a deep cave; we were not able to locate her.

Migratory path and travel s peed

Light level data provided estimates of the time of dawn and dusk from which an algorithm

calculated position to within ± 1 degree in latitude and longitude (DeLong et at., 1992 ; Hill ,

1993 ). Ambiguities in latitude were adjusted by matching sea surface temperatures (SST) recorded

by the diving instrument to mean SST of the area compiled semi-monthly from satellites by the

National Meteorological Weather Service (Ashvi lle, North Carol ina; Le Boeuf el aI., 1 993) . At­

sea locations were filtered, removing any unrealistic fixes of Latitude and Longitude in terms of

the approximated rate of travel speed (2 m/s) for a seal of similar size and weight than a Guadalupe

fur seal female. Position was plotted at daily intervals to calculate the mean daily distance tra­

veled. Minimum travel speed was calculated as the distance in kilometers between two points, one

at the beginn ing and one at the end of a segment of the track where the seal was traveling. Min i­

mum travel speed, mean daily distance traveled and total distance traveled by Guadalupe fur seal

females were calcu lated by us ing marine chmts of the area (Secretaria de Marina, SM 010, Ensenada

to Mazati<in). "In trans it" was defmed as moving in a straight line covering long d istances at a

steady rate . "Foraging area" was defmed as a geographical location where the seal reduced its

horizontal speed substantially and was relatively stationary in its migration (Le Boeuf el at., 1993) .

Diving behavior

Dive bout duration was defined following Gentry and Kooyman (1 986). Bouts were defined

as diving sequences having no interdive intervals greater than 40 minutes and consisting offive or

600 Foraging of Guadalupe fur seal

more d ives (a requ i s ite that was necessary for calculating d ives per hour). Trans i t t imes were

measured from departure to the onset of the first dive bout, and from the end of the last bout to

return onto the rookery (Gentry et aI., 1986a).

RESULTS

Location at sea

During the first feeding trip, females showed a tendency to move to the northwest of Isla de

Guadalupe (Fig. 1). In the second feeding trip, females traveled to the south-southeast (Fig. 1).

Mean maximum distance to feeding grounds was up to 444 ± 151 km (range: 222-589 km) from

Isla Guadalupe. Mean total distance traveled was 2 ,375 ± 1,389 km (n = 4 of 3 females; one

female made two trips , range: 704-4,092 km). Mean daily distance traveled was 171 ± 10 km/day

(n = 4 of 3 females; one female m ade two trips, range: 157-179 km/day; Table I). This suggests

that intensive feeding took place between Latitude 24°00 to 28°00, and Longitude 114°00 to

120°00. This corresponds to a foraging area of about 86,400 square nautical miles ( 1 60, 121 square

km; Fig . 1 ). Sea surface temperature (SST) in these waters was in the range of 17.6°C to 22.7°C.

Feeding trip duration and nursing duration

The first feeding trip of instrumented females had a mean duration of I 0 ± 4 days for females

(n = 4, range: 4-14 days). The second feedillg trip had a mean duration of 19 ± 8 days (n = 4,

range: 8-28 days). The difference in the mean values of the two trips was not statistically signifi­

cant (t-test, t = -1.266, d.f. = 4, P = 0.274). Larger females took shorter trips (mean = 13 ± 8 days,

n = 4) than small females (mean = 28 ± 15 days, n = 4 of 3 females; Table 2). The difference in

foraging trip duration of instrumented females (mean= 14.4 ± 8. 3 days, n = 7) versus non-instru­

mented females (mean = 11 ± 6 days, n = 46) was not stat i stically s ignificant (t = 1.517, d .f. = 52,

P> 0.05). There was no s ignificant difference in the nursing duration of large females (mean = 4

± 1 days, n = 4) and small females (mean = 4 ± 2 days, n = 4 of3 females; t = -0.166, d .f. = 7, P>

0.05).

There was n o stati stical d ifference in fasting duration of pups of large instrumented females

(mean = 13 ± 8 days, n = 5 of 3 females) and small i nstrumented females (mean = 28 ± 15, n = 4

of 3 females) whi le the mother was away (t = -1.944, d .f. = 7, P > 0.05). Similarly days spent

attending pups for large i nstrumented females (mean= 4 ± 1, n = 5 of 3 females) and small instru­

mented females (mean = 4 ± 2, n = 4 of3 females) was not significantly different (t = -0.166, d.f.

= 7, P = 0.873).

Travel Speed

Mean travel or swimm ing speed of these females was 1.9 ± 0.1 mis, based on the mean daily

distance traveled of 171 ± 10 km .

Gallo et al. 60]

30

25

• MAYA <> OnJdlOleI'lhi., b(",ksi • PITA o Sympleet(}fcuthi,t lumirw,'o"a .to. PIRI o ])(J,�itJicu:;: gig(t'f

20�--------���---------L----------�--J 10 J25 120 1J5 110

Figure I. Location at sea of females "Pita" (so l id square), first and second foraging trip (28 June to 31 July,

1992). "Maya" (solid circle) first foraging trip (30 June to 18 July, 1992). And "Piri" (solid triangle) second

foraging trip (18 July to 2 August, I 993), in relation to squid fishing areas in the Cal ifornia Current of Baja

California.

Table 1. Total distance traveled by adult Guadalupe fur seal females. Calculated by plotting the geolocation

positions in a marine chart of the area (Secretaria de Marina, SM 010, Ensenada to Mazatlan).

Female Days at sea Total distance traveled Daily distance traveled Estimated travel velocity

(Ion) (Ion/day) (m/s)

Pita • 4 704.2 176.1 2.0 24 4,092.0 170.5 1.97

Maya 14 2,508.6 179.2 2.1 Piri 14 2,196.5 156.9 1.8

Mean � 14 2,375.3 170.7 1.97 SD� 8.2 1,389.2 9.9 0.1

'Values of first and second trip.

602 Foraging of Guadalupe fur seal

Table 2. Trip duration and duration of attendance to pups of large and small females. Second row per female

other trip duration or attendance duration while instrumented with GLTDRS.

Large females Trip duration

(days)

Pita 4 24

Maya 14

Piri 14

Cata 16 .,

Mean = 12.8 SD= 7.6

Attendance (days) Small females

3 Lupe

4 All

6 3 Rita

3 2

3.5 1.4

Mean = SD=

• Values as "non-present" during the length of stay on the study area . • • Value of the probable third feeding trip of this non-nursing female.

Not used to estimate the averages.

Diving behavior

Trip duration

(days)

42' 7

28' 33'

27.5' 14.8·

Attendance (days)

2 4

5

3.7 1.5

Diving behavior was recorded for one female ("Piri") during a foraging trip (July 19-2 Au­

gust, 1993). Time at sea was 3 47 h or approximately 14 days (Table 3). This provided a sample of

1,465 dives :::3 m, between 18 July and 2 August (Fig. 2). Mean dive depth was 17 ± 10 m (range :

3-82 m), modal dive depth was 3 .1 m (Fig. 3A). Mean dive duration was 2 .6 ± 1.4 min (range: 0.5-

18 min); modal dive duration was 0.6 min (Fig . 38) . Dive duration tended to increase as dive

depth increased showing a slight but significant correlation (r = 0.48, d.f. = 1, P < 0.05) .

Shorter and shal lower dives occurred at the beginning of the record as the animal traveled

south to the foraging area, the frequency of dives greater than 20 m increased rapidly. The distri­

bution of dive depth was negatively skewed . Dives less than 20 m tended to be within the mixed

Table 3. Activity patterns during a trip to sea of a Guadalupe fur seal female in 14.5 days or 347 h (expressed

in hours (h) and percentage of time), in a total of 1,465 dives.

Mean Mean Total diving Total rest time Total transit Transit times dives per dives time time

day per hour outbound inbound

h % h % h % h % h % 101.3 4.2 125.5 36.2 55.2 15.9 166.3 47.9 98.3 59 68.3 41

n 23 11 29 14 15

Gallo et al.

,.

:g"D

t � Q ..

'"'

100

HOllK Of' 1l1\ Y 11 U Il (t 12 (J 11 (I 12 U It (t 11 ., U • U Jl a II

_'-_lInn _

603

Figure 2. Plot of 1,465 dives made on one trip to sea by female "Piri" over a period of 14 days (18 July to 2 August). Sunrise was at -0611 and sunset at -2002. Times are local (8 h earlier than Greenwich Mean

Time). Minimum dive depth plotted was 3 m. 81.

A

� 6 .C-0

� 0 I-!r: '" '-' � 2 ""

0

201

II

� 15 ;;. Q -' <: l-e 10 I-� '" '-' '" '" ..

j u

10

X= 16.9

26

'\""r

J

30 llEl'Tli (.n)

ADL�J.8

Ill)RAT10N (mia)

46 �5t)

7 �u

Figure 3. (A) dive depth frequency analysis for female "Piri" (x= 16.9 ± 10.3 m. n= 1,465 dives). Mode 3.1 m. (B) dive duration frequency (x= 2.6 ± 1.4 min, n= 1,465 dives). Mode 3.6 min. ADL= Aerobic Dive Limit .

604 Foraging of Guadalupe fur seal

layer near the surface (0-30 m), whereas deeper dives broke through the mixed layer into subsur­

face water (>30 m; Fig. 4A, 4B, 4C).

The record during the foraging trip showed a strong daily cycl e of diving activity, with a mean

of 92 ± 49 dives per day (range: 6-168). This female increased the number of dives towards the

end of the foraging trip (Fig. 2), reaching an average of 6 ± 3 dives per hour. Most dives occurred

from dusk to dawn . Diving typically started around 2030 h and ended around 0530 h . Deep dives

started abruptly, increasing in depth towards midnight. The deepest dives occurred at midnight,

with d ive depth declining after dawn (Fig. 4A, 4B, 4C.; Fig. 5).

Mean surface interval between dives was 2 min (range : 0.5-38.5m in) with a modal surface

interval of 0.6 min. Surface intervals were skewed, with most of them lasting greater than 5 min.

Mean bottom dive time was 1 min (range: 0-15.5 min); modal bottom time was 0.1 min. Bottom

time showed a tendency to increase as d ive depth increased (r = 0.25, d .f. = I, P < 0.05), although

th is re lat ionship is non-significant. Dive was organized in bouts; 23 bouts were recorded with an

average dw'ation of3:04 ± 2:30 h (range: 36'-6:26' h). Mean number of dives per bout was 63 ± 60

(range: 7- 1 73). The time between departure and the first dive bout was 35.05 h (10.1% of total

time at sea), that is at 249 km from the island. The time between the last dive bout and return to

shore was 1 1 .18 h (3.2% of total time at sea), at 79 km (Table 4).

20 0

20

40

60 20

! 0

:c 20 t w Q 40

60

0

20

4()

60

Houn OF DAY

21 22 o 4 5 'M-llrrNNN--�--N""'·I"'-'r�W'�""�'rrv�� ,

�/- ___ ,- --�-��-l - - ----- ---------- ---------- --- - - - ---�� A

21 22 23

c

o

I /

3

------------------

23 22 21 20 19 18 17 U

23 "-

22 � :>: ;;> 21

� 20 '" "-I'} :;: 18 � ;-17 I

I 23 22 21 20 19 18 17

Figure 4. Exampl.es of different days on the dive record. Sunrise was at -0611 and sunset -2002 h. (A) crepuscular diving while transiting to the foraging area. (8) crepuscular and night diving at the middle of the foraging trip, the seal has reached the foraging area and starts its way back. (C) crepuscular, night and deep

diving prior to the last two days foraging in a full moon night.

Gal lo et af. 605

N=J"(65

80 o 80

60 0 60 0

�<9 l o

t 0 tg0 � 40

o� 00 0

20

o 4 8 12 16 20 24

LOC,\L TIMf, (HOUR OF DAY)

Figure 5. Cumulative distribution of dives by hour of day by female "Piri" over a period of 14 days. Condi­

tions are s imi lar to Figure 2.

Table 4. Dive bout characteristics ora Guadalupe fur seal female in 23 dive bouts (J ,439 dives).

Dives Dives per Bout Dives! h Time of bout Depth per Surface lnterbout

excluded bout duration in bout underwater bout interval per interval

(%) (h) (%) bout (min) (min)

Mean Mean Mean Mean Mean Mean Mean

(±SD) (±SD) (±SD) (±SD) (±SD) (±SD) (±SD)

range range range range range range range

26 62.7 5.05 10.5 38 15 2.08 9.42 (\.8) (60.1) (4.05) (4.04) (26.9) (6.32) (4.5) (7.19)

7-173 0.6- 6.26 6-27 4-86.4 4.3-27.1 0.5-38.5 0.42-20.40

Note: includes all bouts that fit the dual criterion of including no interdive intervals >40 min, and including at

least five dives. Note that bout duration does not equate with percentage of time spent diving.

Effect of instrument

There was no difference in the duration of the first trip (t = -0.632, df = 2 , P> 0.05, n = 4) and

the second trip (t = - 1 . 1 85, d.f. = 7, P> 0.05, n = 9) of instrumented and non in strumented females .

This was also the case for the second trip duration of instrumented and non instrumented females

during the summer of 1993 (t = -0.241, d.f. = 14 , P> 0 .05 , n = 16).

606 Foraging of Guadalupe fur seal ....................... ...................................................................................................................... _ .............................................. _ ..... .

DISCUSSION

Location at sea

During the first feeding trip, females showed a tendency to move northwest ofIsla de Guadalupe

against the flow of the California Current (Fig. 1). In the second part of the feeding trip, females

traveled south-southeast (Fig. 1). They were probably taking advantage of the California Current,

swimming south in a parallel direction to the Baja Cal ifornia Peninsula (Fig. 1), indicating a

probable use of currents on their way south. Evidence of the utilization of oceanic CUlTents and

gyres in A. gazella and A. tropicalis has been reported by Rodriguez et al. (1993). The distance to

feeding grounds for this female in a straight line was approximately 444 ± 151 km from Isla de

Guadalupe, greater than the distance traveled by two other fur seals species: 160-200 km with a

round trip of 400 km for C. ursinus (Loughlin et aI., 1987), and A. gazella that travel about 200

km to feed (Croxall et aI. , 1985), but similar to those of Juan Fernandez fur seals of about 500 km

(Franc is et aI., 1998).

At a certain point these females started moving back, apparently taking more time and diving

more often than on the way out from the island, suggesting that these females foraged against the

flow of the Cal ifornia Current. Even though th is is a single case, the return of one female was

probably tTiggered by the full moon of August 2, 1993, as suggested by Tri l lmich and Mohren

(1981), who found that Galapagos fur seals peaked with about twice as many animals on land near

full moon, than near the new moon with a minimal number of seals.

Comparing with a rehabi l itated non-pregnant Guadalupe fur seal adult female (Lander et aI., 2000) that was instrumented with a satellite Time Depth Recorder (SLTDI�) on January 1998 (post

El Nifio year), the trip of this female was irregular, the female swam to Bahia San Quintin, Isla de

Guadalupe and further north to the Latitude of Mendocino County, a 2,890 km, longer than the

mean total distance of2,375 km of the three nursing females from Guadalupe. Due that this was a

non-pregnant or nursing female its track during winter might give us some idea of where Guadalupe

fur seals females forage in EI Nino conditions wh ile they are not breeding.

Prel iminary analysis of24 scats and vomits show that Guadalupe fur seals feeds on vertically

migrati ng squid (Onychoteuthis banksi, 0. boreal-japonica, Eucleoteuthis luminosa, Dosidicus

gigas, Stenoteuthis ovalensis, Histioteuthis heteropsis, Symplecoteuthis luminosa, Pterygioteuthis

giardi and Loligo opalescens), unidentified myctoph id fishes found in shallow depths at night,

and of epipelagic Pacific mackerel (Scomber japonicus) and frigate mackerel (Auxis thazard;

Gallo-Reynoso, 1994; Gallo-Reynoso et al., 2000). These squ ids and fishes are all found in the

California Current about Isla Guadalupe, Islas San Benitos and Isla Cedros, and the continental

shelf of Baja California in the area were these females feed. The species found in their diet has

been repOlted by oceanographic research cruises and fishing records (Young, 1972; Okutani,

1980; Allen et al. , 1995; Roper et aI., 1995).

Feeding trip duration and nursing duration Feeding trips of instrumented females versus non i nstrumented females show that female trip

Gallo et at. 607

duration was not affected by the instrument, as was affected by the female condition in which

larger females did shorter trips than smaller females, even though larger females spent the same

time attending their pups as smaller females, th is suggest a more efficient energy al location by the

larger females than the smaller ones. Foraging trips were s imi lar or longer in duration than those

of Juan Fernandez fur seal females described by Francis et al. ( 1 998).

The mean foraging trip duration of Guadalupe fur seal non-instrumented females during the

1992 EI Nino was 9 ± 6.4 days (n = 55 trips of 1 8 females; Figueroa-CatTanza, 1 994). In post EI

Nino 1 993, when oceanographic conditions were approaching nornlal, non-instrumented female 's

foraging trips were longer, mean= 13.5 ± 7 days (n = 3 1 trips of 29 females; Figueroa-Carranza,

1994). ln other otariids El Niiio conditions increase the duration of foraging trips (A . australis, A.

galapagoensis, C . ursinus at San Miguel Is land, and Zalophus californianus; L imberger et aI. , 1983; Trillmich et aI., 1986; Tri llmich, 1986; Costa et aI. , 1991; DeLong and Antonelis , 199 1 ;

Feldkamp et aI. , 199 1; Heath et aI., 1991; Majluf, 199 1 ; Trillmich, 199 1). Our data shows that

during EI N iilo conditions the trips were not affected during the breed ing season, while in the post

El Nino conditions the trips were longer. Our data might be related to the northward shift on the

distribution of food either geographically or in the water column wh ich can explain the difference

in foraging effort by these females.

Travel speed

The mean travel speed of 2 mls found in these three females is sim ilar to that reported for

northern fur seals of 2.06 mls (combining outbound and inbound travel speed from Loughlin et aI., 1987) and only marginally faster than Galapagos fur seals of 0.6- 1.9 mls measured with velo­

city meters (Ponganis el a1. , 1990). Guadalupe fur seal females trave l speed is well within the

minimum cost of transport (MeT) of2.1 mls (Gentry et aI. , 1986b; Feldkatnp, 1987), for an otariid

seal with a mean weight of 52.5 ± 1.8 kg. Mean travel speed of2 ml sec i s not only similar to other

otariids but also to phocids like elephant seals (Le Boeuf et aI. , 1993).

Diving behavior

The diving characterist ics of the female are broadly sim ilar to those described for female

Antarcti c fur seals, A. gazella (Croxall et al. , 1985; Kooyman and Tri l lmich, 1986; Boyd and

Croxal l , 1992), for female Galapagos fur seal s, A. galapagoensis (Kooyman and Trillmich, 1986),

female South American fur seals , A. australis during lactation (Tri l lmich et aI. , 1 986), to seasonal

div ing shown by female New Zealand fur seal, A. Jorsteri (Mattl in, 1 993), and female Juan

Fernandez fur seals (Francis el aI. , 1998). But they are different from those of northern fur seals,

C. ursinus that show ind ividual specialization on shallow and deep dives (Gentry et aI., 1 986b;

Goebel el aI., 1991).

Gentry et af. ( l 986b) calculated the aerobic dive l imit (ADL ) for fur seals of different body

sizes and, us ing their prediction equation for the ADL based on body mass, the predicted ADL for the

53 kg female in th is study was 3.8 minutes. The predicted ADL was exceeded by thi s female in 1 5%

of al l dives (Fig . 3B), sug-gest i ng that lactic acid (LA) may accumulate during diving. One dive of

608 Foraging of Guadal upe fur seal

1 8 min was recorded, which was 4 . 7 times the predicted ADL . It is not unusual for a certain percen­

tages of dive duration to exceed ADL ; this has been noted in many species (Feldkamp et aI. , 1 98 9 ;

Pongan i s e t al. , 1 990; Boyd and Croxal 1 996; Costa e t al. , 1 996; C osta and Gales, 2000).

Theoretically thi s female was capabl e of diving deeper than the deepest dive shown on the

record (82 m) . A s s uming th at she dived vertically during deep dives, swimming speed did not

normal ly exceed 1 . 5 m/s. Based on this swimm i ng speed and a theoretical ADL of3 . 8 min (G entry

et aI. , 1 986b; Boyd and Croxal l , 1 992), the m aximum depth for aerobic dives by Guadalupe fur

seals would be 1 74 m .

The diving record suggests that dives occurred i n bouts separated by extended periods spent

at the surface, poss ib ly in transit . This has been suggested for other species of the genu s

Arc/ocephalus (Gentry et aI. , 1 986b; B oyd and Croxall , 1 992). The geolocation method suggests

that this particu lar seal, instead of spending time resting at the surface (or physiological "reco­

very" periods), was transiting to foraging areas. Wil liam s et al. ( 1 992) hypothes ized a simi lar

strategy for the gentoo penguin, Pygoscelis papua. Transit to foraging areas showed repeated

short dives from surface to one or two m eters during the daily long surface intervals, suggesting

that th is fem ale was clearing LA concentration w ith repeated short dives with in the ADI.. Castel l ini

et al. ( 1 9 8 8) reported a s imi lar result for Weddell seals in which LA decl ined rapidly as i f the seal

were at the surface .

Effect of instrument

Attached instruments may affect the overal l performance of seal s . N early 1 7% reduction in

swim speed of California sea lions, Z. californianus, was found by Feldkamp ( 1 987), and Feldkamp

et al. ( 1 989). Foraging trip metabolic rate increased by 1 9% in northern fur seals harnessed with

TORS (Costa and Gentry, 1 986) . However, these studies used TORS with twice the cross-sectional

area and three times the mass of the instruments used in this study; furthernlOre they were attached

with harnesses, which increased drag. This suggests that our instruments had m in imal effects on

div ing behavior and or distance traveled.

During the summer of 1 992, there was no difference between the first and second trip dura­

tion of instrumented and n on i nstrumented fem ales of s i m i lar wei ght. S im i l arly, during the sum ­

mer of 1 993, there was no d ifference in tri p duration of instrumented and n on i n strum ented fe­

males during the second tri p (Fig. 6) . S i m i l arly, Boyd et al. ( 1 99 1 ) found no sign ificant difference

in foraging trip durati on and time spent ashore between Antarctic fur seal s with and w ithout TOR S .

Studies in other diving species have shown none or l ittle effect (Wilson et aI. , 1 986). Croxall et al.

( 1 988) , Gales et al. ( 1 990) and Kooyman et al. ( 1 992) found no s ignificant difference in foraging

trip duration or mass of prey brought ashore between instrumented and non-instrumented pen­

gu ins us ing s imilar or greater devices (cross sectional area and mass) to the TORS used in th is study.

Results show that instru mented Guadalupe fur seals with geolocation t ime depth recorders

can render high quality data on the diving behavior and foraging trips at sea. The traveling d is­

tan ce, the foraging area and its in situ characteristics give a w i der v i ew of the b iogeographic

impl ications for the conservat ion of a vulnerable and h i gh ly dispers ing species, pointing to new

Gal lo et at. 609

Figure 6. Tim e Depth Recorder attached to the back of a Guadalupe fur seal female. The female is n ursing

her pup upon arrival from a foraging trip; note the territorial male to the left.

directions on the effective conservation of a species and the location and characteristics of their

foraging area, which should have some level of management to protect the food and the feeding

habits of Guadalupe fur seals in their oceanic habitat over the California Current to warrant their

survival.

ACKNOWLEDGMENTS

We are indebted to Direccion General de Intercambio Academico-UNAM, to Education Abroad

Program, University of California, The National Geographic Society, the Institute of Marine Sci­

ences, Univers ity of California Santa Cruz, and uc-Mexus for funding the different expeditions .

Thanks are given to P. Thorson for helping in the field in 1992, and to D . Costa for lending us the

capture nets and a VHF radio-receiver. We are grateful to R. Hill from Wildlife Computers for

lending us 2 TORS for this study. We also thank A . Delgado, M. Peralta and A . Sanchez for their

help in the field. We are grateful to Secretaria de Marina and to fishermen of "Cooperativa de

Langosteros y Abuloneros de Ensenada" wh ich provided logistic support on the i sland. These

field studies were conducted under permits No. 0561 of Secretarfa de Pesca, and Nos. 2538, 4933

and 2025 of Secretaria de Desarrollo Urbano y Ecologia, (now SEMARNAT) Mexico.

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