Mating tactics and mating system of an aquatic-mating pinniped: The harbor seal, Phoca vitulina

Article (PDF Available)inBehavioral Ecology and Sociobiology 61(1):119-130 · October 2006with 689 Reads
DOI: 10.1007/s00265-006-0242-9
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Abstract
Our best understanding of marine mammal mating systems comes from land-mating pinnipeds. Logistical problems of observing behavior at sea have limited our ability to make inferences about species with aquatic-mating systems, which comprise over half the pinnipeds. The mating systems of these species likely involve different mating tactics than land-mating species. We used several methods in combination (e.g., animal-borne cameras, radio telemetry, time-depth recorders, and DNA paternity assessment) to provide a comprehensive study of the aquatic-mating tactics of harbor seal males. Males decreased time offshore (26.0 vs 14.8%) and increased time near shore (33.8 vs 43.7%) between premating and mating periods, respectively. Concomitantly, males reduced foraging effort and increased activities associated with competition for females (e.g., visual/vocal displays and threats). As females come into estrus near the end of lactation and spend more time at sea, males reduced their near-shore ranges (4.2 vs 1.0km2), which were clustered within 1–1.5km of the beach where females attended their pups. Body mass of males was not a major factor affecting their reproductive behavior. From a small number of paternity assignments to study males, it appears that females select males. These combined results are more consistent with a lek-type mating system than with the territorial or female defense systems characteristic of land-mating pinnipeds.
ORIGINAL ARTICLE
Mating tactics and mating system of an aquatic-mating
pinniped: the harbor seal, Phoca vitulina
Daryl J. Boness &W. Don Bowen &Birgit M. Buhleier &
Gregory J. Marshall
Received: 21 November 2005 /Revised: 25 May 2006 /Accepted: 17 June 2006 / Published online: 3 August 2006
#Springer-Verlag 2006
Abstract Our best understanding of marine mammal
mating systems comes from land-mating pinnipeds. Logis-
tical problems of observing behavior at sea have limited our
ability to make inferences about species with aquatic-
mating systems, which comprise over half the pinnipeds.
The mating systems of these species likely involve different
mating tactics than land-mating species. We used several
methods in combination (e.g., animal-borne cameras, radio
telemetry, time-depth recorders, and DNA paternity assess-
ment) to provide a comprehensive study of the aquatic-
mating tactics of harbor seal males. Males decreased time
offshore (26.0 vs 14.8%) and increased time near shore
(33.8 vs 43.7%) between premating and mating periods,
respectively. Concomitantly, males reduced foraging effort
and increased activities associated with competition for
females (e.g., visual/vocal displays and threats). As females
come into estrus near the end of lactation and spend more
time at sea, males reduced their near-shore ranges (4.2 vs
1.0 km
2
), which were clustered within 11.5 km of the
beach where females attended their pups. Body mass of
males was not a major factor affecting their reproductive
behavior. From a small number of paternity assignments to
study males, it appears that females select males. These
combined results are more consistent with a lek-type
mating system than with the territorial or female defense
systems characteristic of land-mating pinnipeds.
Keywords Harbor seals .Mating system .Lek .
Radio telemetry .Time-depth recorders .Paternity
Introduction
Animal mating systems are influenced by a variety of
factors, including phylogeny, distribution of resources, and
predation pressure (Wilson 1975; Emlen and Oring 1977;
Rubenstein 1986; Clutton-Brock 1989). Among polygy-
nous species, the primary resources affecting female
reproductive behavior are food and suitable environments
for rearing offspring, whereas the reproductive behavior of
males is most influenced by the temporal and spatial
distribution of females. In populations where females are
clustered and their movements limited or predictable, males
generally compete to monopolize females by controlling
access to resources used by the females (territoriality or
resource defense tactics) or attempt to monopolize females
directly (male dominance or female defense tactics).
However, when females are dispersed spatially and tempo-
Behav Ecol Sociobiol (2006) 61:119130
DOI 10.1007/s00265-006-0242-9
Communicated by F. Trillmich
D. J. Boness
Department of Conservation Biology,
Conservation and Research Center,
Smithsonians National Zoological Park,
Washington, DC 20008, USA
D. J. Boness
Department of Wildlife Ecology and School of Marine Science,
University of Maine,
Orono, ME, USA
W. D. Bowen
Marine Fish Division, Department of Fisheries and Oceans,
Bedford Institute of Oceanography,
Dartmouth, Nova Scotia B2Y 4A2, Canada
B. M. Buhleier :G. J. Marshall
Mission Programs, National Geographic Society,
Washington, DC 20036, USA
D. J. Boness (*)
41 Green Acres Road,
Hartford, ME 04220-5035, USA
e-mail: boness@megalink.net
rally, or are highly mobile, so that access to groups of
females cannot be controlled, males are more likely to use
other tactics, such as, lekking, scramble competition, or
sequential defense of single females.
Lekking is a relatively rare mating system reported in
less than 0.5% of birds and mammals (Davies 1991;
Höglund and Alatalo 1995). Although there is not complete
agreement on the critical elements that define a lek, the
common criteria are: (1) males aggregate and display to
attract females; (2) females and males visit these sites
primarily for mating; and (3) females have an opportunity
to select a mate (Bradbury 1981; Höglund and Alatalo
1995). The latter criterion is thought to be of lesser
importance by Höglund and Alatalo.
The mating systems of many terrestrially breeding
pinnipeds and the best-studied terrestrial mammals are
similarly well understood. Certain characteristics of such
pinnipeds, which are more suitably adapted to life at sea
than on land, predispose them to particular mating systems.
More specifically, their large body size, extensive subcuta-
neous blubber layer, and poor mobility on land predispose
them to systems in which males usually maximize mating
opportunities through territorial defense of resources used
by females (i.e., suitable pupping sites) or direct defense of
females by males (Bartholomew 1970; Stirling 1983;
Boness 1991; Le Boeuf 1991; Boness et al. 2002; Lidgard
et al. 2005). Extrapair or extraconsort matings may also
occur in these systems (Ambs et al. 1999; Goldsworthy et
al. 1999; Hoelzel 1999; Lidgard et al. 2004).
About half of all pinniped species mate at sea rather than
on land. The temporal and spatial pattern of females, and
hence male mating tactics, in this environment are likely to
be different than those for terrestrially mating pinnipeds
because of their greater mobility in water and dispersed
spatial distribution. Several authors have argued that these
conditions should lead to strategies such as lekking or
roving than to resource or female defense (Stirling 1983;Le
Boeuf 1991; Boness et al. 1993,2002). For example,
certain conditions that lead to lekking, (e.g., high mobility
of females, hot spotfor availability of females, relatively
low asynchrony of estrus) (Emlen and Oring 1977;
Bradbury 1981; Beehler and Fosters 1988; Davies 1991;
Wiley 1991; Höglund and Alatalo 1995; Widemo and
Owens 1995; Gjerde et al. 2000) match those of several
species of seal that mate at sea shortly after females in
colonies on ice or land wean their pups (Boness et al.
1993). However, the evidence to understand the mating
system of pinnipeds that mate at sea is much more limited
because of logistical difficulties in trying to observe and
follow individual animals. Nonetheless, the use of ad-
vanced technology and new approaches to studying marine
mammals are providing insights into the mating systems of
aquatically mating pinnipeds (Bartsh et al. 1992; Perry
1993; Hanggi and Schusterman 1994; Sjare and Stirling
1996; Coltman et al. 1997,1998a; Nicholson 2000;Van
Parijs et al. 2000a,b,2001,2003).
Despite the recent increased efforts to study aquatically
mating seals, we are still in the early stages of understand-
ing their reproductive behavior and mating system. One
species, the harbor seal, Phoca vitulina, has been given
more attention than most because of its greater accessibility
(Perry 1993; Coltman et al. 1997,1998a,b,1999; Van Parijs
et al. 2000a,b,2003; Hayes et al. 2004). Unlike most
aquatically mating seals, harbor seal females generally give
birth and care for their offspring on land rather than on ice,
although there are a few locations where harbor seals
produce pups on ice floes, too. The nature of harbor seal
pupping colonies is diverse, leading to considerable
variation in the size of colonies and the structure of the
area surrounding colonies (e.g., narrow sand or cobble
beaches, small rocky outcroppings affected by tidal cycles,
and mud flats with distinct water channels leading to them).
Regardless of colony structure or size, females do form
small clusters along the shoreline.
Mounting evidence shows that females spend time at sea
during the period of maternal care, and that this time at sea
involves regular foraging trips away from the colony
(Boness et al. 1994; Van Parijs et al. 1997). What appears
to be a commonality among studies of male behavior is the
use of underwater vocalizations (Van Parijs et al. 2003).
Male spatial patterns and movements in relation to the
colony and location of females are less clear, but vary
considerably among breeding colonies and even within a
colony (Perry 1993; Van Parijs et al. 2000a,b; Hayes et al.
2004). In some cases, defense of adjacent discrete territories
offshore from female haulout areas has been described, and
males may or may not display from such territories
(Sullivan 1981; Perry 1993; Hayes et al. 2004). In other
cases, males may display from underwater territories that
are not adjacent to one another nor near female haulout
sites, but be located in known foraging areas or along
routes to foraging areas (Van Parijs et al. 2000a,b; Hayes et
al. 2004). In still other situations, males may not form
discrete territories, but display vocally in the vicinity of
female haulouts and engage in combat when they come in
close contact with other males (Hanggi and Schusterman
1994). Inferences about the mating system from these
varying results range from territorial defense of transit
routes or feeding sites to lekking. As noted by Hayes et al.
(2004), virtually all of these studies raise the possibility of a
lek system. The difficulty with these interpretations is that
they generally are based on either a small number of males
or on a limited set of behavioral information, or both.
In this study, we used a combination of methods,
including an animal-borne video system, time-depth record-
ers, radio telemetry, and DNA paternity analyses to provide
120 Behav Ecol Sociobiol (2006) 61:119130
a more comprehensive assessment of the mating system of
the harbor seal at Sable Island, Nova Scotia. Our objectives
were to evaluate the likelihood that harbor seal males
exhibit a mating system that differs from those exhibited by
land-breeding pinnipeds and that some or all males use a
lekking-type pattern of behavior to acquire mates.
Methods
Data were collected from 17 to 56 males, depending on data
type, off Sable Island, Nova Scotia (43° 55N; 60° 00W)
between 1993 and 1996. Males in mixed-sex and all-male
groups were selected to achieve a full range of body size.
We deployed in various combinations on different males,
radio transmitters (to obtain locations), time-depth recorders
(to obtain diving frequency, depth and duration), and video
cameras (to observe behavior) by capturing males when
they were resting on land. Each year, males were followed
from the beginning of the birthing period (mid-May), about
3 weeks before receptive females became available (pre-
mating period), through mid-July when receptive females
had been present for 34 weeks (mating period) (Coltman
et al. 1997).
Spatial analyses
We affixed radio transmitters (Advanced Telemetry Sys-
tems, Isanti, MN, USA) on top of the head of seals using 5-
min epoxy so that signals could be received when the
animals surfaced at sea or were on land. Transmitters
remained attached and functioned for 10 males in 1993, 17
males in 1994, 15 males in 1995, and 14 males in 1996.
Males were followed from a minimum of 11 days to a
maximum of 39 days, with a mean number of days of 25.3,
32.6 25.3, and 24.7 from 1993 to 1996, respectively.
Markers at 0.5-km intervals provided location references
along a 31-km stretch of the north beach where most
females gave birth. Twice daily surveys of this area, one in
the morning and the other in the late afternoon, listening for
radio signals, were made throughout the breeding season to
locate males. These surveys involved driving the ATV
slowly along the beach looking and listening for radio-
tagged males, and obtaining a point sample of their
location. When males were seen on land, their locations
were recorded to the nearest 0.1 km. If a radio signal was
heard off the beach, we obtained bearings from two
locations, usually 12 km apart, to facilitate triangulation.
A 4-element antenna attached to a 4-m pole on an all-terrain
vehicle provided a probable receiving range of about 5 km.
If a male was neither seen nor heard, we assumed he was
beyond the range of our system. A more extensive search,
involving circumnavigating the island, was conducted when
a male was not heard for 3 days to be sure that the male was
not hauling out outside the study area. On only two
occasions was a male located elsewhere during the
premating period. Ninety-five percent minimum convex
polygon ranges were estimated for 32 of the 56 males that
had more than 12 near-shore locations. The number of
locations ranged from 13 to 38.
Behavior analyses
We attached to the backs of males the animal-borne video
system (Crittercam), which included a built in hydrophone
and time-depth recorder so diving data and vocalizations
could be associated with behavior (Marshall 1998; Bowen
et al. 2002). The total unit weighed about 2 kg or <2% of a
males body mass. A 3-h videotape determined the
maximum amount of observation time per 3-day deploy-
ment; a saltwater switch ensured maximum filming at sea.
The camera was programmed to run for 10 min every hour
from 0530 or 0600 to 1400 or 1500, and sampling of dive
depth every 7 s. We deployed cameras after 1500 h so they
would not begin sampling until the next morning. This
provided about 14 h for animals to adjust to the camera
before collecting data, although visual observation of
animals and video footage did not suggest males were
disturbed by the presence of the camera on its back.
In 1995, cameras were deployed on June 622, on 10
males. Data were obtained from nine of those deployments.
In 1996, deployments occurred on June 222 on each of 10
males twice (one each during premating and mating
periods). Data were obtained from 15 of these deployments,
seven during the premating period, and eight during the
mating period. The minimum interval between deployments
on a given male was 7 days. Longitudinal analyses were
conducted on the seven males for which both deployments
yielded data. However, data from all males in 1996 were
used once in the cross-sectional analyses, selected random-
ly for which time of season was used for a given male.
The videotapes were initially examined to determine the
behaviors exhibited. From this, behavior categories were
established and the tapes scored for the amount of time each
male spent in the different categories. The categories were:
Threat/fight Another male is in view and vocal growls,
starting with neck and chest inflated, chasing
or biting occurs.
Display The camera male engages in one of three
stereotypical behaviors involving visual and/
or vocal signaling and other seals are not in
view. Neck-quivering vocalization involves
emitting a broadband vocalization during
which the head and neck quiver. This is
always done underwater, usually near the
Behav Ecol Sociobiol (2006) 61:119130 121
bottom, although occasionally it is given
during a descent after breathing at the
surface. Bubble-blowing vocal display
involves the male ascending toward the
surface and slowly exhaling a stream of
bubbles as he drifts upward, giving a
vocalization that ends similarly to that used
during neck quivering (Fig. 1). This is often
preceded by several neck-quivering vocal-
izations. For one male in which a camera was
allowed to run for 3 h immediately after
deployment, neck-quivering and bubble-
blowing display occurred the entire time.
Surface slapping is done with either one
foreflipper or thrashing the rear flippers from
side to side. No discernable vocalization is
made during slapping although sometimes a
male rapidly exhales air creating a cloud of
bubbles just before it breaks the surface of the
water and slaps.
Patrolling This is inferred from activity immediately
preceding it. It involves a male swimming
slowly underwater, usually interspersing
active thrusting with the rear flippers and
gliding, and is preceded by displaying or
threats within a 10-min sampling period.
Observations of a few males from elevated
dunes near shore in shallow water showed
them swimming/gliding underwater repeat-
edly within a relatively small area.
Foraging Includes chasing schools or individual fish
and rooting in the bottom substrate whether
fish are seen in the cameras view.
Searching This behavior is also defined by the activities
preceding it (as in patrolling) and includes
swimming in a straight path at a moderate to
slow speed, preceded by foraging activity in
the 10-min sample.
Travelling This includes swimming with continuous
flipper thrusting or alternate thrustinggliding
swimming for which there are no clear
foraging or displaying activities during the
10-min sample.
Resting This includes lying on the bottom or bobbing
at the surface.
Other This includes ascending to the surface to
breathe, descending to depth, and hauling out
in the surf zone.
Paternity analysis
The paternity data for this study were a subset of data from
a broader study of paternity of harbor seals at Sable Island.
Details of analysis methods and broader results can be
found in Coltman et al. (1998b). Skin samples were
collected from as many females, pups, and males as
possible for several simultaneously ongoing studies on
Sable Island during this work. Six polymorphic micro-
satellites were used in the paternity analysis (Coltman et al.
1998b). Paternity assignment was done using a paternity
simulation program (CERVUS). The average probability of
exclusion was 0.957 and 0.940 (ranging from 0.309 to
0.999) for the 2 years from which data were available for
males in this study (Coltman et al. 1998b).
Statistical analyses
Parametric statistical analyseswereusedwhentheir
assumptions were satisfied, otherwise nonparametric tests
Fig. 1 Single frames captured
from a Crittercam tape to illus-
trate a male harbor seal engaged
in bubble blowing display and a
male with a camera and trans-
mitter attached threatening an-
other male. The radio transmitter
and netting glued to the head of
the male with the camera are
illustrated. The male blowing
bubbles is within 5 m of the
surface and nearly vertical. He
does not surface after complet-
ing the bubble blowing. The
sonogram represents the vocali-
zation associated with the bub-
ble blowing display
122 Behav Ecol Sociobiol (2006) 61:119130
were run. Analyses were conducted using either SigmaStat
(Version 2.03) or SPSS (Version 11.0). Rejection of the null
hypothesis in tests was set at 0.05.
Results
Interannual variation
As data were collected over several years, we first assessed
the impact of interannual variation on our ability to treat the
data as a whole. Although within the premating and mating
periods there were interannual differences in how often
males were either on land, near shore, or offshore during
the twice-daily surveys (premating: Chi-square=163.1,
df=6, p<0.001; mating: Chi-square=80.9, df=6, p<0.001),
the pattern of change in the percentage of sightings in each
location from premating to mating period was consistent
among years. Thus, for comparisons of the percentage of
sightings in each location category between the premating
and mating periods, we combined data from all years.
A MANOVA of arc-sine transformed percentages of
time spent in each behavioral activity (display, patrol,
threat, forage, search, travel, and rest) from cross-sectional
Crittercam data showed no difference between years in the
overall pattern of activity (F
7,8
=1.42, p=0.315). Thus, we
combined data from the 2 years for an analysis of the
difference in proportion of time in each behavior between
the premating and mating periods. Since the study design in
1996 was longitudinal, to increase the sample size for the
cross-sectional analyses, one deployment for each male
from 1996 was randomly chosen to be included in the
cross-sectional analysis. A two-way repeated measures
ANOVA of the size of near-shore ranges of 32 males to
examine differences between years and period failed both
normality and variance tests. Hence, we tested differences
among years for each season separately using a Kruskal
Wallis ANOVA on ranks and tested for differences between
premating and mating periods using a Wilcoxon test.
Ranges during the mating period did not differ among
years (H=1.170, p=0.557), but premating ranges did
(H=7.11, p=0.029), so we present the data separately by
year.
Daily locations from surveys
Males were not equally sighted onshore, heard at sea near
shore (<5 km of shore), or out of range offshore
(approximately >5 km) during either the premating or
mating periods (Chi-square goodness of fit test: p<0.0001
for both periods). Males rested on land during a similar
percentage of the surveys (about 40%) in both periods
(paired ttest: t=1.66, df=55, p=0.102). However, the
percentage of surveys during which males were offshore
decreased from the premating to mating periods (26.0 vs
14.8%; paired ttest: t=5.53, df=55, p<0.001), whereas the
percentage near shore increased (paired ttest: 33.8 vs
43.7%; t=6.35, df=55, p<0.001).
Behavior at sea
Based on footage from the animal-borne cameras, males
engaged in all recorded activities during both the premating
and mating periods. Different deployment procedures for
Crittercams in 1995 and 1996 as described in the methods
allowed comparison of both cross-sectional and longitudi-
nal data sets between the premating and mating periods.
Based on these data, males engaged in display behavior
significantly more during the mating period than during
premating (Table 1). Small sample sizes and individual
variability provided for low power to detect other
differences.
Males in this population are known to change their
diving behavior between premating and mating periods
(Coltman et al. 1997). In the earlier study, males made deep
dives (depths >20 m) more frequently during premating,
then switched to predominantly shallow (<20 m) diving
during the mating period. Deep dives were fairly uniform in
shape, having flat and long bottoms and rapid rates of
descent and ascent. Shallow dives were more variable in
shape. Rates of individual mass loss varied inversely with
time spent in deep dives, suggesting that deep diving
behavior reflected foraging activity (Coltman et al. 1997).
Therefore, using the Crittercam data, we also tested whether
behaviors differed between those same depth categories.
We found a significant difference between the pattern of
behavior exhibited during deep and shallow diving (MAN-
OVA, F
7,13
=5.688, p=0.004). Percentage of time spent
displaying, patrolling, and foraging clearly differed (i.e.,
significant in both cross-sectional and longitudinal analy-
ses) with dive depth; displaying and patrolling occurred
more during shallow dives and foraging more during deeper
dives. Traveling, searching, and threatening males may also
have differed, but these differences were significant in only
one or the other analysis (Table 2).
Near-shore spatial patterns
Near-shore ranges during the mating period were signifi-
cantly smaller, about 25% of those during the premating
period (Table 3). There was considerable variability among
males in the size of near-shore ranges during the mating
period, with variability being greatest in 1996 (Table 3;
Fig. 2). Male near-shore ranges during the mating period
overlapped substantially and in 1994 and 1995 were
concentrated in the region off the beach, where the greatest
Behav Ecol Sociobiol (2006) 61:119130 123
number of females with pups was located (Fig. 2). There
appeared to be an increase in the number of larger mating
ranges in 1996 that coincides with a dramatic reduction in
the number of females that produced pups on Sable Island.
Paternity in relation to near-shore range
Paternity analyses were conducted during the same time
period as this study, but were published separately
(Coltman et al. 1998b,1999). Each year the entire cohort
of pups (and most of the mothers) was sampled. The
potential pool of males was estimated to be about 180, 90
of which were sampled (Coltman et al. 1998b). During 1993
and 1994, 12 of 27 males from our study that had radio
transmitters attached were assigned one or more paternities:
eight sired one pup, two sired two pups, one sired three,
and one sired four. In the larger paternity analysis by
Coltman, the maximum number of pups sired for a given
male was five, and most males sired only one pup or none.
As it has been suggested that harbor seal males hold
territories offshore to control travel routes and gain access
to estrous females moving from land (Perry 1993), we
conducted an analysis to evaluate whether this might be
happening at Sable Island. The analysis used the 11
Table 1 Behavior of male harbor seals at sea
Cross-sectional data Longitudinal data
Premating (n=9) Mating (n=9) Premating (n=7) Mating (n=7)
Mean Standard error Mean Standard error T-value
(p-value)
a
Mean Standard error Mean Standard error T-value
(p-value)
b
Threat 0.9 0.51 1.0 0.43 0.552
(0.589)
0.4 0.23 0.3 0.23 1.323
(0.234)
Display 2.5 0.84 9.4 2.42 2.506
(0.023)
3.6 1.38 11.1 4.29 3.692
(0.010)
Patrol 13.1 4.69 25.8 4.70 2.027
(0.060)
20.1 4.99 22.7 5.72 0.269
(0.797)
Forage 8.2 2.78 5.0 1.53 1.017
(0.324)
3.4 1.11 5.9 1.92 1.133
(0.300)
Search 16.4 3.91 12.6 3.14 0.821
(0.424)
15.6 3.48 15.9 5.01 0.252
(0.809)
Travel 18.8 3.67 10.8 2.74 1.591
(0.131)
19.0 3.87 8.8 2.20 2.897
(0.027)
Rest 19.0 2.37 21.3 2.88 0.628
(0.539)
18.8 2.53 15.1 1.86 1.261
(0.254)
Mean percentages of time spent in each activity at sea during the premating and mating periods for two data sets, one based on cross-sectional
data for 18 males and the other on longitudinal data for seven males. Othercategory is not included so the total is less than 100%
a
ttests using arcsine square-root transformation
b
Paired ttests using arcsine square-root transformation
Table 2 Behavior of male harbor seals during diving
Cross-sectional data Longitudinal data (n=7)
<20 m (n=9) >20 m (n=9) P-value
a
<20 m >20 m P-value
b
Mean Standard error Mean Standard error Mean Standard error Mean Standard error
Threat 1.2 0.47 0.3 0.20 0.049 0.5 0.53 0.8 0.56 0.449
Display 9.0 2.65 3.0 1.91 0.023 4.7 1.26 0.2 0.14 0.006
Patrol 29.9 2.92 6.1 3.11 0.001 21.7 4.25 1.6 0.81 0.001
Forage 1.7 0.43 14.1 2.83 0.001 3.0 1.38 13.4 3.51 0.028
Search 9.8 2.39 24.8 4.11 0.004 13.9 3.12 23.4 4.63 0.196
Travel 15.3 3.1 7.1 2.47 0.059 22.0 4.07 8.65 2.85 0.002
Rest 19.2 2.60 19.4 2.32 0.856 16.8 2.18 26.6 6.59 0.235
Mean percentages of time spent in each activity at sea during dives >20 and <20 m for two data sets, one based on cross-sectional data for 18
males and the other on longitudinal data for seven males. Othercategory is not included so the total is less than 100%
a
ttests using arcsine square-root transformation
b
Paired ttests using arcsine square-root transformation
124 Behav Ecol Sociobiol (2006) 61:119130
paternities that could be assigned to one of the males with
attached radio transmitters, for which we knew the location
of their near-shore ranges. We then asked whether the
probability of the female being fertilized by a male adjacent
to her location on land was commensurate with the amount
of time the male spent in his near-shore range, assuming
positioning nearby off the beach gave a male primacy
access. We operationally defined adjacent to a females
location on landby determining whether all or part of a
males range fell within lines perpendicular to the shore one
half kilometer on either side of the females beach location
at the end of lactation. The proportion of surveys males
were at their near-shore site was used to calculate the
expected frequency of fertilization for an adjacent male.
The actual frequency of fertilizations by males that were
adjacent to females was compared to this expected
frequency. The results showed that females were fertilized
less often than expected by a study male that was adjacent
to her beach location (G
adj
=4.66; p<0.05); only one of the
11 females was fertilized by an adjacent study male. The
average minimum linear distance between a line perpen-
dicular to the closest part of the near-shore range of the
male assigned paternity and a line perpendicular to where
the female was last located on the beach before weaning
was 4.6±3.05 km.
Influence of body mass on male behavior
Previous studies have shown body mass to be a factor in
male mating behavior in many polygynous mammals,
including some pinniped species. However, body mass
may be less important in determining male reproductive
behavior of harbor seals (Coltman et al. 1998a,b). To
examine the relationship between body mass and behavior
of males, we conducted several analyses using male survey,
near-shore range, and Crittercam behavioral data. A
MANOVA with the percentage (Arcsine Square Root
transformed) of surveys observed near shore during the
premating period and offshore during the mating period,
and near-shore range size during the mating period as
dependent variables, and dividing the range of initial body
mass into two groups based on the median mass (106 kg),
failed to find an effect of mass on these behaviors
(F
3,28
=0.695, p=0.563). Consistent with this pattern, a
Table 3 Near-shore range size of male harbor seals
Year NPremating period Mating period
Median Range Median Range
1994 9 1.5 0.412.5 0.7 0.26.9
1995 10 3.2 0.55.3 0.8 0.35.6
1996 13 11.3 0.719.4 2.2 0.115.7
19941996 32 4.2 1.0
Ranges are given in km
2
. A Wilcoxon sign rank test of the median between the premating and mating periods for all years combined is significant
(p<0.001)
Fig. 2 Schematic of near-shore ranges of male harbor seals during the
mating period. Each polygon represents a different male, 17 harbor
seal males in 1994, 15 in 1995, and 14 in 1996. The filled circles in
the beach area represent relative numbers of females with pups on
shore between kilometer marker. The largest filled circle represents 35
females and the smallest one female. There were 130 females in 1994,
116 in 1995, and 39 in 1996
Behav Ecol Sociobiol (2006) 61:119130 125
regression analysis of Crittercam behavioral data found a
significant negative relationship between percent time spent
foraging during the mating period and initial body mass for
those Crittercam males for which we had a body mass at the
beginning of the breeding season (R
2
=0.545, p=0.015,
n=10). We failed to find a statistically significant relation-
ship between initial body mass and percent time spent
displaying (R
2
=0.208, p=0.185).
Discussion
Male tactics and mating system
The combination of systematic behavioral, spatial, and
paternity data used in our study provides the most
comprehensive study of an aquatic-mating system of a
pinniped population. Yet, even with these more compre-
hensive data than in previous studies of this species, or
any other aquatic-mating pinniped, we are not able to
unequivocally describe the mating system in terms of
categories used in mating system theory. Nonetheless, our
data are more supportive of some male tactics than others.
Consistent with several other studies of harbor seals
(Walker and Bowen 1993;HanggiandSchusterman
1994; Van Parijs et al. 1997,1999,2000a,b; Coltman et
al. 1999; Nicholson 2000; Hayes et al. 2004) and with
discussions of alternative mating tactics and plasticity in
mating systems (Emlen and Oring 1977; Davies 1991; Lott
1991), our data support the idea that more than one tactic
may be used by males to acquire females, and that there
may have been a shift in primary tactic in 1996 from 1994
and 1995.
The substantially greater mobility and dispersion of
pinniped females at sea compared to on land, should favor
male tactics that involve displaying to attract females or
those in which males search out or follow individual
females than those that involve defense of females or
resources that are used by females (Bradbury 1981; Stirling
1983; Clutton-Brock 1989; Boness 1991; Davies 1991;Le
Boeuf 1991; Boness et al. 1993,2002). Moreover, female
harbor seals are clustered on land before dispersing at sea,
conditions ideal to create a hotspotbasis for aggregation
of males to engage in display competition over females
(Beehler and Fosters 1988; Balmford et al. 1993b; Widemo
and Owens 1995). We believe our evidence from 1994 and
1995, especially, point to a lek-like tactic as the primary
one for harbor seals at Sable Island. The criteria most often
used to describe leks include males aggregating and
displaying to attract females, both males and females
visiting these sites primarily for mating, and females having
an opportunity to select males (Bradbury 1981; Höglund
and Alatalo 1995). Early descriptions of classical lek
systems in birds also usually reported extremely high levels
of mating skew (Wiley 1991; Höglund and Alatalo 1995).
Höglund and Alatalo, however, prefer not to use this
characteristic in defining a lek system, arguing that mating
skew is difficult to define because of variation in
determining the number of males in a population, and that
other systems also produce high levels of skew. Moreover,
the degree of skew appears to be related to the size of the
lek, with lower skew found in larger leks (Höglund and
Alatalo 1995).
Our spatial analysis shows that harbor seal males increased
the amount of time spent near shore during the mating period.
Males fitted with radio transmitters aggregated near where
females were most abundant on land about the time the
females become receptive, which could be considered a
hotspot. While near shore males did not appear to defend
exclusive areas, most maintained relatively small ranges
within which they engaged in competitive encounters with
other males. Males did not spend their entire time during the
mating period on these near shore ranges. They still spent
about 40% of their time on land and smaller amounts of time
out of range of detection. That male near-shore ranges likely
serve a mating function is suggested by changes in behavior
from the premating period to the mating period, including the
reduction in range size, the increased time spent near shore,
and the increased time spent displaying at the expense of time
spent foraging.
We were unable to track the pelagic movements of
females simultaneously with our observation of males.
However, from previous studies of lactation strategies
(Boness et al. 1994; Bowen et al. 2001), we know that
later in lactation, females make regular foraging trips to
sea with typical diving bouts in the range of 1530 m
deep, mixed with time spent in shallower waters of 5
10 m, but return to land daily. The diving and haulout
pattern of females changes dramatically soon after wean-
ing their pup. At this time, females begin making dive
bouts greater than 45 m in depth continuously for multiple
days without returning to shallower water or land. This
pattern of behavior before and after weaning provides
females with increasing opportunities to sample the
quality of males at their near-shore ranges before or
immediately after weaning, when females are thought to
become receptive. As Höglund and Alatalo (1995)
suggest, mating with males that become established at an
arena (i.e., location of the aggregation of males) in itself
may convey a level of selection by females. In addition,
the fact that females at Sable Island were not fertilized by
study males in positions opposite to where the female was
on land at the end of lactation supports the hypothesis that
females are exercising choice among males within the
near-shore area, although it is not conclusive evidence of
choice.
126 Behav Ecol Sociobiol (2006) 61:119130
These results are all consistent with the criteria often
used to judge a system as a lek system. Though mating
skew in this population was not extreme, it did exist at a
low to moderate level (Coltman et al. 1998b), which is
consistent with the findings of a negative relationship
between level of skew and lek size (Höglund and Alatalo
1995). The area over which male near shore ranges were
distributed off the beach at Sable Island stretched along
30 km of beach.
We do not believe our results on behavior in near shore
ranges are supportive of either resource defense or female
defense systems. Resource defense systems involve defense
of discrete territories containing resources used by females.
The spatial analysis in this study clearly shows a lack of
exclusiveness of the areas used by males. While there may be
occasional foraging at the depth of these near-shore ranges,
most foraging off Sable Island occurs at deeper depths
(Boness et al. 1994; Coltman et al. 1997). We cannot,
however, rule out the possibility that some males might have
defended exclusive resource territories near foraging areas
used by females outside the range of our ability to detect
them with radio telemetry (Van Parijs et al. 2000a).
Despite a small sample size, the paternity analysis shows
that it is also unlikely that males in their near-shore ranges
were simply defending travel lanes of females, where they
could control females by capturing them and forcing
copulations (Perry 1993; Hayes et al. 2004). Females were
not fertilized by males on ranges adjacent to the females
location on the beach, but in addition, the average linear
distance between where a female was on the beach and the
male that fertilized her was more than 4 km.
If males were defending females directly, we would have
expected the video footage to provide relatively frequent
views of females in range of the lens, as we saw encounters
between males. Yet, we rarely saw females in the videotape
analysis. Additionally, from our earlier studies of female
diving activity at sea, their daily patterns of movement were to
and from the beach and to deeper waters for foraging. It seems
unlikely that this pattern of behavior would provide the spatial
clustering of females for female defense to be effective.
We cannot so readily rule out male tactics involving
roving or scramble competition. Some males in each year
had relatively large near-shore ranges during the mating
period in contrast to the typical small range. This may
reflect the existence of alternative tactics, such as following
or searching for departing females in an effort to copulate
with them. Such variability in male tactics has been
described in terrestrial species that have lek systems
(Clutton-Brock et al. 1988; Apollonio et al. 1992; Balmford
et al. 1993a; Widemo and Owens 1999) and shifts in
reproductive behavior and mating systems associated with
changes in female density and distribution are well
documented for terrestrial species (Lott 1991). The fact
that there appears to be an increase in the occurrence in
large mating ranges in 1996 suggests there might have been
a shift away from a primary lekking-type tactic and toward
an alternative tactic such as roving. This might not be
surprising because the female population at Sable Island,
especially in the study area, was dramatically reduced in
1996 compared to the previous 2 years (Bowen et al. 2003),
and as a result there was no clear hotspot of females.
Plasticity in mating tactics by a few males has also been
shown in bearded seals (Van Parijs et al. 2003). It may be
that there is a greater degree of flexibility in behavior of
aquatic-mating seals than in terrestrially mating species so
we may not as yet have adequate descriptions for all mating
systems of aquatic-mating species.
Unfortunately, some shortcomings with our study pre-
vent us from understanding the system and potential
variation in male tactics within and between years further.
As mentioned earlier, we cannot directly link the behavior
and location of females with that of males. Nor were we
able to collect all data sets on the same individual males
because repeated captures necessary for this could have
affected the malesbehavior. Despite using an animal-borne
camera to observe behavior at sea, the view is limited and
the total duration of sampling per individual is small.
Body mass and male behavior
The fact that initial body mass of males does not seem to be
a major factor affecting the behavior and spatial pattern of
harbor seal males is consistent with earlier work at Sable
Island that failed to find a clear relationship between large
body mass and reproductive behavior or success (Coltman
et al. 1998a,b). Indeed Coltman et al. found that the most
successful males were the moderate-sized males not the
largest ones. Body size was also not related to various
behavioral measures of males during the mating period at
Elkhorn Slough in California (Hayes et al. 2004). Body size
may play a role in extending the length of time engaged in
direct sexual activity for male harbor seals (i.e., needing to
spend less time foraging during breeding), but it does not
appear to confer an advantage through contest or displaying
competition (Andersson 1994).
Comparison with other populations
The picture that emerges from the various studies of harbor
seal mating behavior at sea is complex. It undoubtedly reflects
some real differences, but some apparent differences might be
a result of the use of different methodologies. For example,
we used signals from radio transmitters when males surfaced
to triangulate locations at sea. Others used direct observation,
triangulation of vocalizations using a hydrophone array
underwater, playback responses to vocalizations to determine
Behav Ecol Sociobiol (2006) 61:119130 127
boundaries, or some combination of these methods. Two
commonalities that emerge from most studies is an increase in
male vocal behavior with the onset of the mating season and a
reduction in range size (Hanggi and Schusterman 1994;Van
Parijs et al. 1997,1999,2000a,b;Nicholson2000;Hayeset
al. 2004). However, in Scotland, range estimates incorporat-
ed sampling a much larger area than we could on Sable
Island. As a result, the Scottish study found some males
frequently located in positions at the feeding grounds used by
females during and after lactation, as much as 50 km from the
pupping grounds (Van Parijs et al. 1997). As noted above, if
we had been able to locate males offshore (i.e., >5 km from
the colony), our results might similarly show males defending
areas at frequently used feeding sites, if there are distinct and
predictable feeding sites around Sable Island. Studies at other
colonies, like ours, only followed males close to female
puppingsitesonland(Perry1993; Hanggi and Schusterman
1994; Nicholson 2000; Hayes et al. 2004).
We found considerable overlap in the ranges of
individual males near Sable Island, whereas most other
studies reported at least some males occupying exclusive
territories, with clearly defined boundaries, some being
adjacent territories (Perry 1993) and others being separated
by some distance (Van Parijs et al. 2000b). In California,
Hayes et al. (2004) reported some males with large adjacent
territories but with smaller nonadjacent display areas within
their territories. They also reported males that were highly
aggregated and vocalizing from a small area, but do not
provide precise data on individual males in such aggrega-
tions. While it is possible that our triangulation on radio
signals from males at the surface produces a level of error
that could spuriously increase the apparent overlap in
ranges, it seems unlikely that the error would be great
enough to account for the level of overlap we found. The
degree of overlap is substantial in many cases (Fig. 2) and
we were only defining space use for up to 20 males in a
given season. There may have been as many as 150 males
engaging in similar mating behavior to those of the males
with transmitters we were following off Sable Island in a
given season. The size of our ranges and those of males
holding clear territories in California were an order of
magnitude different, although the territory size of males in
Scotland were similar to the ranges at Sable Island.
The apparent differences in exclusive or overlapping
areas of use by males from different populations, whether
real or artifacts of methodological differences, do not
preclude drawing similar inferences about the use of a
lek-type tactic. Whether males defend exclusive areas or
overlap in space use does not define lekking (Höglund and
Alatalo 1995). The order of magnitude of difference in the
size of area used by males and difference in location
relative to females and female resources is more likely to
suggest differences in tactics within or among colonies.
While there is no conclusive evidence from a single
study or population of alternative male tactics or annual
variation in tactics, the accumulation of circumstantial
evidence from our study and those of others supports this
hypothesis. Within years, we had males near shore that had
ranges differing by an order of magnitude. Moreover, in the
last year of our study, when the female population declined
dramatically, there was an increase in the number of males
exhibiting the pattern of a large near-shore range. In
Scotland, those males observed tens of kilometers from
pupping sites, stationed at feeding sites are likely engaging
in a resource defense tactic (Van Parijs et al. 1997). At
Miquelon Island (Perry 1993) some males were observed
defending large, adjacent territories in channels off the sand
flats where females were hauled out suggesting defense of
transit routes of females leaving the beach. Yet, DNA
analysis failed to assign paternities to any of these males,
suggesting the possibility that males engaged in alternative
tactics were likely siring the offspring.
We have provided evidence consistent with an expecta-
tion that aquatic-mating seals should exhibit a primary male
tactic and a mating system different than those typical of
land-mating pinniped species. Our findings add consider-
ably to an accumulating body of evidence that suggests
harbor seals may exhibit a lek-type primary mating tactic
under certain conditions, but also that this species may
show variability in tactics of males within colonies, among
colonies, and interannually. To advance our understanding
of the mating tactics of harbor seals, and other aquatic-
mating pinnipeds, it will be necessary to incorporate
measures of mating success along with spatial and
behavioral data on both males and females over spatial
scales that encompass foraging areas as well as areas near
breeding sites.
Acknowledgements We thank the following people for assistance
in the field: Brian Beck, Dave Coltman, Sarah Ellis, Sara Iverson,
Jim McMillan, and Monica Muelbert. Gerry Forbes of the
Department of Environment, Canada provided logistical assistance
on Sable Island. Dave Coltman conducted the DNA paternity
analysis and kindly provided the data. Sara Iverson, Martha
Leonard, Chris Wemmer, Sophie van Parijs, and an anonymous
reviewer provided helpful feedback on drafts of the manuscript.
The project was supported by the Smithsonian Institution, Friends
of the National Zoo, Department of Fisheries and Oceans of
Canada, Natural Sciences and Engineering Research Council of
Canada, and National Geographic Society.
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    • Gisela Heckel
      Gisela Heckel
    The Pacific harbor seal (Phoca vitulina richardii) can be found from Japan to Baja California Sur, Mexico. In Mexico, harbor seals are found on nine islands and along part of the Baja California Peninsula coast. Information on their abundance in Mexico is scarce, although it is recognized to be low in contrast to their northern distribution. This study's objectives were to determine the distribu-tion of harbor seals in Mexico and to estimate their minimum abundance during the pupping (winter) and molting (spring) seasons. During winter and spring 2009, we visited the islands west of the Baja California peninsula (from Asunción to Coronado, including Guadalupe Island) to pho-tograph the harbor seal's haul-out sites from a boat. In addition, during the pupping season, we carried out one aerial survey along the coast from Ensenada, Baja California, to Asunción Bay, Baja California Sur, with the same purpose. Harbor seals in the photographs taken at the haul-out sites were counted by three independent counters; results were compared, and repeatability values > 0.95 were obtained, which represent the propor-tion of similarity between counters. There were harbor seal colonies from Asunción to Coronado Islands, and they were found along the coast almost continuously from Ensenada southward to 29° 32' N. Pups were found on all these islands, and we report for the first time that San Roque Island is a breeding colony. The colonies with the highest counts were San Roque, Natividad, San Jerónimo, and Cedros. During the molting season, we counted more individuals on the islands (3,785) than during the pupping season (3,138). However, the highest abundance of harbor seals was during the pupping season (4,862) when we included all the colonies on nine islands and along the coast of the Baja California Peninsula-the complete distribution in Mexico. The only previ-ous extensive survey in Mexico was carried out from winter to spring between 1982 and 1986 on seven islands, with a total of 1,715 harbor seals reported. On the same islands, we counted 2,326 individuals in 2009, so we suggest there has been an increase in the abundance since then.
  • Preprint
    • Joseph M Korpela
    • Hirokazu Suzuki
    • Sakiko Matsumoto
    • Ken Yoda
    Animal-borne data loggers, i.e., biologgers, allow researchers to record a variety of sensor data from animals in their natural environments. This data allows biologists to observe many aspects of the animals' lives, including their behavior, physiology, social interactions, and external environment. However, the need to limit the size of these devices to a small fraction of the animal's size imposes strict limits on the devices' hardware and battery capacities. Here we show how AI can be leveraged on board these devices to intelligently control their activation of costly sensors, e.g., video cameras, allowing them to make the most of their limited resources during long deployment periods. Our method goes beyond previous works that have proposed controlling such costly sensors using simple threshold-based triggers, e.g., depth-based and acceleration-based triggers. Using AI-assisted biologgers, biologists can focus their data collection on specific complex target behaviors such as foraging activities, allowing them to automatically record video that captures only the moments they want to see. By doing so, the biologger can reserve its battery power for recording only those target activities. We anticipate our work will provide motivation for more widespread adoption of AI techniques on biologgers, both for intelligent sensor control and intelligent onboard data processing. Such techniques can not only be used to control what is collected by such devices, but also what is transmitted off the devices, such as is done by satellite relay tags.
  • Article
    Full-text available
    • Peter D. Shaughnessy
      Peter D. Shaughnessy
    • Colin Southwell
    Crabeater seals Lobodon carcinophaga breed on Antarctic pack-ice in spring, primarily in October. They are widely dispersed as triads: an adult female, her pup and an adult male. Mean weights were 257 kg for ten males and 228 kg for eight females. Mean standard lengths (nose to tail in a straight line) were 2.19 m (18 males) and 2.18 m (12 females). For a species that mates on pack-ice with dispersed females, it is likely to be advantageous for crabeater males to be fast and agile to maximise matings, consistent with the apparent absence of sexual dimorphism.
  • Article
    Full-text available
    • Dietmar Schwarz
      Dietmar Schwarz
    • Sara M. Spitzer
    • Austen C Thomas
      Austen C Thomas
    • Alejandro Acevedo-Gutierrez
      Alejandro Acevedo-Gutierrez
    Sex‐specific diet information is important in the determination of predator impacts on prey populations. Unfortunately, the diet of males and females can be difficult to describe, particularly when they are marine predators. We combined two molecular techniques to describe haul‐out use and prey preferences of male and female harbor seals (Phoca vitulina) from Comox and Cowichan Bay (Canada) during 2012–2013. DNA metabarcoding quantified the diet proportions comprised of prey species in harbor seal scat, and qPCR determined the sex of the individual that deposited each scat. Using 287 female and 260 male samples, we compared the monthly sex ratio with GLMs and analyzed prey consumption relative to sex, season, site, and year with PERMANOVA. The sex ratio between monthly samples differed widely in both years (range = 12%–79% males) and showed different patterns at each haul‐out site. Male and female diet differed across both years and sites: Females consumed a high proportion of demersal fish species while males consumed more salmonid species. Diet composition was related to both sex and season (PERMANOVA: R² = 27%, p < 0.001; R² = 24%, p < 0.001, respectively) and their interaction (PERMANOVA: R² = 11%, p < 0.001). Diet differences between males and females were consistent across site and year, suggesting fundamental foraging differences, including that males may have a larger impact on salmonids than females. Our novel combination of techniques allowed for both prey taxonomic and spatiotemporal resolution unprecedented in marine predators.
  • Article
    Full-text available
    • Andrea Ravignani
      Andrea Ravignani
    • Christopher T. Kello
      Christopher T. Kello
    • Koen de Reus
      Koen de Reus
    • Bart de Boer
      Bart de Boer
    Puppyhood is a very active social and vocal period in a harbour seal's life Phoca vitulina. An important feature of vocalizations is their temporal and rhythmic structure, and understanding vocal timing and rhythms in harbour seals is critical to a cross-species hypothesis in evolutionary neuroscience that links vocal learning, rhythm perception, and synchronisation. The current study utilised analytical techniques that may best capture rhythmic structure in pup vocalisations with the goal of examining whether (i) harbour seal pups show rhythmic structure in their calls and (ii) rhythms evolve over time. Calls of three wild-born seal pups were recorded daily over the course of 1-3 weeks; three temporal features were analysed using three complementary techniques. We identified temporal and rhythmic structure in pup calls across different time windows. The calls of harbour seal pups exhibit some degree of temporal and rhythmic organisation, which evolves over puppyhood and resembles that of other species' interactive communication. We suggest next steps for investigating call structure in harbour seal pups and propose comparative hypotheses to test in other pinniped species.
  • Article
    Full-text available
    • Andrea Ravignani
      Andrea Ravignani
    • Christopher T. Kello
      Christopher T. Kello
    • Koen de Reus
      Koen de Reus
    • Bart de Boer
      Bart de Boer
    Puppyhood is a very active social and vocal period in a harbour seal’s life Phoca vitulina. An important feature of vocalizations is their temporal and rhythmic structure, and understanding vocal timing and rhythms in harbour seals is critical to a cross-species hypothesis in evolutionary neuroscience that links vocal learning, rhythm perception, and synchronisation. The current study utilised analytical techniques that may best capture rhythmic structure in pup vocalisations with the goal of examining whether (i) harbour seal pups show rhythmic structure in their calls and (ii) rhythms evolve over time. Calls of three wild-born seal pups were recorded daily over the course of 1–3 weeks; three temporal features were analysed using three complementary techniques. We identified temporal and rhythmic structure in pup calls across different time windows. The calls of harbour seal pups exhibit some degree of temporal and rhythmic organisation, which evolves over puppyhood and resembles that of other species’ interactive communication. We suggest next steps for investigating call structure in harbour seal pups and propose comparative hypotheses to test in other pinniped species.
  • Article
    • Mario Fernando Garcés-Restrepo
      Mario Fernando Garcés-Restrepo
    While polygyny is the dominant mating system in mammals, it is increasingly recognized that promiscuity occurs in most species. Using a long-term genetic and space-use data set, we documented the mating system for 2 sedentary and uniparous species of tree sloths, brown-throated three-toed (Bradypus variegatus) and Hoffmann’s two-toed (Choloepus hoffmanni) sloths. We predicted that the life history of these species facilitates female strategies that promote mating with multiple males across breeding seasons, and shape central features of the mating system in tree sloths. We found that many female sloths mated with different males during our study: 70% of female B. variegatus and 50% of female C. hoffmanni switched mates among years at least once during our study. Our observations of individual movements suggested that females employed 2 strategies that appeared to influence mate switching across breeding seasons: 1) selecting a male from a pool of males in their activity center, and 2) mating with different males by shifting their home ranges during estrus. Collectively, our findings suggest that individual variation in female reproductive strategies contributes to shaping the mating systems for a sedentary mammal like sloths, and highlights the need for long-term studies to effectively capture the mating systems of mammals with slow life histories. Aunque la poligamia es el sistema de apareamiento dominante en los mamíferos, es cada vez más reconocido que las hembras en la mayoría de las especies de mamíferos se aparean con múltiples machos. Usando un set de datos genéticos y de uso de hábitat a largo plazo, se documentó el sistema de apareamiento de dos especies sedentarias y uníparas, el perezoso grisáceo (Bradypus variegatus) y el perico ligero (Choloepus hoffmanni). Se predijo que las características de estas especies, facilitan que las hembras presenten estrategias que promuevan el apareamiento con múltiples machos, determinando finalmente el sistema de apareamiento en estas especies. Se encontró que muchas hembras se aparearon con múltiples machos: 70% de las hembras de B. variegatus y el 50% de las de C. hoffmanni presentaron múltiples parejas por lo menos una vez durante esta investigación. Nuestras observaciones sobre movimientos individuales revelaron que las hembras cambian de pareja bajo diferentes escenarios: (1) apareamiento con machos diferentes en cada estro, de los que se superponen en su ámbito hogareño (2), apareamiento con machos diferentes al cambiar su ámbito hogareño durante el estro. Estas evidencias sugieren que las estrategias reproductivas individuales de las hembras ayudan a modelar el sistema reproductivo de especies sedentarias como los perezosos; finalmente, es importante destacar la necesidad de investigaciones a largo plazo para poder entender los sistemas de apareamiento de especies con lenta historia de vida.
  • Article
    Full-text available
    • Eva M Fernández-Martín
      Eva M Fernández-Martín
    • Gisela Heckel
      Gisela Heckel
    • Yolanda Schramm
      Yolanda Schramm
    • Maria García-Aguilar
      Maria García-Aguilar
    Pupping and molting of Phoca vitulina are processes that occur each year with high precision, although their timing varies according to location. Knowledge about the timing of these events allows us to determine when the highest numbers of individuals are hauled out, which is important to achieve a good abundance estimation. In this study we determined the timing of pupping and molting of P. v. richardii at Punta Banda Estuary, Baja California (Mexico), previously unknown at this site or along its entire distribution in Mexico. Observations were carried out during the 2011 and 2012 pupping seasons, as well as the 2012 molting season. We determined that the pupping season starts in mid- February and ends in mid-April, and that the maximum number of pups occurs in mid-March. The late premolt stage was observed from the end of March to the beginning of July, with the peak proportion of individuals in this stage at the beginning of May. The molting period extends from the end of April to mid-July, with the peak proportion of individuals molting at the beginning of June. The reverse molt pattern (starting on the torso and ending on the head and flippers) was the most common. The highest number of adult and subadult individuals on land was observed during the molting season; therefore, the best time to carry out counts to estimate seal abundance in this area is from the beginning of May to the beginning of June.
  • Article
    Full-text available
    • Ivar Gjerde
      Ivar Gjerde
    • Per Wegge
      Per Wegge
    • Jørund Rolstad
    The evolutionary processes behind the polygynous mating system known as leks are difficult to document. One approach is to study the behaviour that drives the formation of new leks today. Several hypotheses have been put forward to explain the formation of leks, and they can roughly be divided into two groups; one which advocates that the males are the driving force and one which argues that the females are the driving force. In this study we use data from a long-term study (1979-1998) of a capercaillie population at Varaldskogen in southeast Norway to develop a model describing how new leks are formed in this species. By using data on spacing pattern and behaviour of radio-marked young and adult birds of both sexes we demonstrate how the situation develops from winter towards mating in spring. Furthermore, we report on a few cases of new leks that have arisen in the area during the 20 years of study. We argue that both female mate choice, male territoriality and male attraction to locations with high densities of females are involved in a dynamic process of lek formation. We present results which indicate that new leks are mainly founded by young birds. Finally, we show that when new leks are formed the spacing patterns of the individuals involved change. This questions the method of using comparisons between the position of female home ranges and established leks to infer how leks are formed.
  • Article
    • Burney Le Boeuf
      Burney Le Boeuf
  • Article
    • Daryl J Boness
      Daryl J Boness
    Substantial advances have been made in the past two decades toward a theory of mating systems (Orians, 1969; Selander, 1972; Trivers, 1972; Jarman, 1974; Emlen and Oring, 1977; Bradbury and Vehrencamp, 1977; Kleiman, 1977; Wittenberger, 1979; Thornhill and Alcock, 1983; Rubenstein and Wrangham, 1986). These recent efforts have focused on the interplay between sexual selection and environmental factors that determine temporal and spatial dispersion of males and females (e.g. resource distribution, predation pressure). Increased information on behavioural reproductive strategies has led to examination of theory both within and between taxa to assess the breadth of its applicability (see Bradbury and Vehrencamp, 1977; Ostfeld, 1985; Rubenstein and Wrangham, 1986 for reviews of different taxa). A comparison between antelope and emballonurid bats has shown that the form of mating systems in both groups is set within the bounds of female dispersion, which is strongly related to food distribution (Bradbury and Vehrencamp, 1977). On the other hand, factors such as habitat type and body size are good predictors of social dispersion and mating strategies in antelopes but not bats.
  • Article
    Full-text available
    • Daniel I Rubenstein
      Daniel I Rubenstein
  • Article
    • G.J. Marshall
    CRITTERCAM is an animal-borne integrated video, audio and TDR data logging system designed for studying the behavior and ecology of large marine vertebrates at sea where systematic human observation is impossible. Harnessed to free-ranging animals, CRITTERCAM enables study of animal behavior free of potentially disturbing human presence. 169 CRITTERCAM deployments have been made on 22 species. Most work has been done with harbor seals and Hawaiian monk seals, and to a lesser extent sperm whales (65, 25 and 25 deployments, respectively). Deployments revealed information and insights on habitat use, diving, foraging, reproductive and social behavior, territoriality, vocalization, and interspecific contact.
  • Article
    • George A. Bartholomew
    It is proposed (1) that the evolution of pinniped polygyny can profitably be examined as an integral part of a complex adaptive suite including physiology, morphology, ecology, and distribution which has involved in relation to an amphibious mode of life, and (2) that the selective factors evolved in this behavioral evolution can be identified by analysis of the processes by which the breeding structure is annually re-established and maintained in the rookeries. Terrestrial parturition and offshore marine feeding appear to have been key determinants of the major adaptive features of pinnipeds, and also to have interacted with characteristics common to most mammals in such a way as to favor both polygyny and sexual dimorphism. A model is presented that starts with terrestrial parturition and offshore marine feeding, which together are unique to pinnipeds, derives from them a series of functions typical of polygynous pinnipeds, relates these to characteristics common to most mammals, and indicates the major feedback loops which have given selective impetus to the evolution of the polygynous breeding system. Key roles are assigned to gregariousness, and male exclusion. The roles of large size, fat deposits, sexual dimorphism, female reproductive patterns, and ontogenetic development are evaluated.
  • Article
    • Sofie Van Parijs
      Sofie Van Parijs
    • Christian Lydersen
      Christian Lydersen
    • Kit M. Kovacs
      Kit M. Kovacs
    We combined observations of individual male bearded seal, Erignathus barbabus, behaviour at sea with acoustic localization techniques to investigate their reproductive strategies. Data on trill vocalizations and dive behaviour were collected over consecutive years during the seals' mating season in Svalbard, Norway. Males showed stereotypical dive and vocal displays, with clear individual variation. Acoustic localization provided at-sea locations for 17 males based on variation in trill parameters. Kernel home range analyses showed that 12 individuals displayed at set locations (95% kernels=0.27-1.93 km2) and five other males displayed within considerably larger geographical areas (95% kernels=5.31-12.5 km2). Males that used the set locations maintained single discrete core areas (50% kernels), while males with large areas moved between multiple core areas. Movement patterns of males suggest that those with small areas patrolled aquatic territories, while those that used larger areas appeared to 'roam'. Territorial males showed little spatial overlap, while roaming males overlapped substantially with both territorial and other males' areas. Territorial males had significantly longer trills than roamers. We suggest that trill duration may be a useful indicator of male 'quality'. Territorial male bearded seals may be 'successful' individuals while roaming males may be younger animals or males in poorer condition that are unable to maintain an aquatic territory. Our data on underwater vocalizations and movements of male bearded seals thus provide evidence for the use of alternative mating tactics in this species. © 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.