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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 487: 245–260, 2013
doi: 10.3354/meps10217
Published July 30
INTRODUCTION
Biological hotspots in the epipelagic zone have been
described as areas where dynamic processes in the
physical environment lead to enhanced productivity
and aggregation of consumers relative to their sur-
roundings (Palacios et al. 2006). In these areas,
upwelling, mesoscale eddies, and fronts may act in
concert with the local geomorphology to generate
conditions that greatly promote the availability of
© Inter-Research 2013 · www.int-res.com*Email: m.pardo@comunidad.unam.mx
Role of environmental seasonality in the turnover
of a cetacean community in the southwestern Gulf
of California
Mario A. Pardo
1,5,
*
, Norman Silverberg
1
, Diane Gendron
1
, Emilio Beier
2
,
Daniel M. Palacios
3,4
1
Centro Interdisciplinario de Ciencias Marinas, Instituto Politécnico Nacional, La Paz, Baja California Sur 23096, Mexico
2
Centro de Investigación Científica y de Educación Superior de Ensenada - Unidad La Paz, La Paz, Baja California Sur 23050,
Mexico
3
Cooperative Institute for Marine Ecosystems and Climate, Institute of Marine Sciences,
Division of Physical and Biological Sciences, University of California, Santa Cruz, California 95060, USA
4
NOAA, NMFS, Southwest Fisheries Science Center, Environmental Research Division, Pacific Grove, California 93950-2097,
USA
5
Present address: Posgrado en Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México,
Distrito Federal 04510, Mexico
ABSTRACT: La Paz Bay is a distinct region within the Gulf of California whose rich cetacean com-
munity exhibits an intense annual overturn. We studied the environmental conditions that could
drive this change over the course of a year. Cetacean biomass was estimated from monthly sur-
veys, with concurrent collection of water-column measurements of temperature, salinity, nutri-
ents, chlorophyll a (chl a), and biogenic matter fluxes. The water-column structure showed 3 major
conditions: deep mixing during winter, stratified isopycnal shoaling in spring and early summer,
and deep stratification during late summer and autumn. Chl a and relative fluxes of biogenic silica
and calcium carbonate indicated a seasonal succession of primary producers in response to the
observed evolution of hydrography. During the periods of mixing and isopycnal shoaling, the bay
provided suitable habitat for blue whales, bottlenose dolphins, and common dolphins, while fin
whales, Bryde’s whales, and short-finned pilot whales were numerically dominant during the
period of stratification. To provide a regional context to the observed seasonality, we fitted tempo-
ral least-squares to an 11 yr monthly time series of satellite-derived wind, sea surface temperature
(SST), and chlorophyll concentration (CHL). Within the bay, the SST followed the annual mon-
soonal shift in the wind, whereas CHL showed a bi-modal pattern, with a main peak occurring
under mixing conditions in winter and a second peak under isopycnal shoaling in spring/early
summer. The regional fitting suggested that the latter period was driven by a localized intra-
seasonal phenomenon that could be responsible for the higher biological richness of the bay
compared to the surrounding gulf.
KEY WORDS: Ecological succession · Seasonal variability · Nutrient supply · Stratification ·
Biogenic matter fluxes · Trophic levels · Marine hotspots
Resale or republication not permitted without written consent of the publisher
Contribution to the Theme Section ‘Biophysical coupling of marine hotspots’
FREEREE
ACCESSCCESS
Mar Ecol Prog Ser 487: 245–260, 2013
prey for large fauna (e.g. Wingfield et al. 2011). Al -
though these hotspots are often detectable through
remote sensing of the ocean’s surface, other areas
that appear oligotrophic and devoid of dynamic fea-
tures at the surface may also attract large feeding
predators and even influence their migration pat-
terns (e.g. Domeier et al. 2012). In such areas, the
biological production maxima may be in the subsur-
face in the presence of a deep/sharp thermocline,
underscoring the importance of measuring hydro-
graphic and biological parameters, both at the sur-
face and in the water column, for the characterization
of biological hotspots.
The most productive areas of the Gulf of California
(hereafter ‘the gulf’; Fig. 1) are located along its east-
ern (continental) side and in the northern region due
to winter upwelling and tidal mixing, respectively
(Lluch-Cota 2000). The southwestern gulf (peninsu-
lar side) is comparatively less produc tive, except for
La Paz Bay (hereafter ‘the bay’), whose photosyn-
thetic pigment concentrations remain high year-
round compared to its surroundings, constituting an
isolated spot of high phytoplankton biomass (Santa-
maria-del-Angel et al. 1994, Luch-Cota & Teniza-
Guillén 2000, Kahru et al. 2004). The bay sustains a
diverse megafauna that includes at least 16 ceta cean
species of temperate, tropical, and subtropical affini-
ties (Flores-Ramírez et al. 1996, Salvadeo et al. 2009).
It also hosts a growing colony of California sea lions
Zalophus californianus (Szteren et al. 2006) and is
visited by whale sharks Rhincodon typus and spine-
tail devil rays Mobula japanica, which arrive in win-
ter, spring, and early summer to feed on zooplankton
(Clark & Nelson 1997, Ketchum-Mejía 2003, Croll et
al. 2012). The rich cetacean community exhibits a
strong annual overturn, with migratory species such
as blue whales Balaenoptera musculus and hump-
back whales Mega ptera novaeangliae occurring
in winter and spring, whereas species with more
tropical affinities, like Bryde’s whales Balaenoptera
edeni, bottlenose dolphins Tursiops truncatus, and
short-finned pilot whales Globicephala macro rhyn -
chus, occur mostly during the summer and autumn.
Fin whales Balaenoptera physalus are resident in the
gulf and, together with the common dolphins Delphi-
nus spp. occur year-round (Flores-Ramírez et al. 1996,
Salvadeo et al. 2009). The hydrographic con ditions
that support this cetacean diversity and underlie the
species’ replacement have not been studied.
In the present study, we posit that seasonal forcing
of oceanographic conditions in the bay, including
surface mixing driven by northwesterly winds in
winter (Badan-Dangon et al. 1991) and cyclonic
circulation in summer (Monreal-Gómez et al. 2001,
Sánchez-Velasco et al. 2006), lead to enhanced nutri-
ent supply to the base of the food web, attracting low
trophic level prey for planktivorous and piscivorous
cetaceans. Warmer conditions in summer would, in
turn, be favorable for the aggregation of higher
trophic level prey looking for a suitable habitat to
spawn near the coast (e.g. Staaf et al. 2008), attract-
ing teutophagous cetaceans. To assess the specific
hydrographic and biological conditions underlying
species’ replacement in the cetacean community of
the bay, we make use of water-column data collected
as part of a multidisciplinary time-series investiga-
tion, aimed at examining monthly changes in physi-
cal structure, nutrient and chlorophyll a (chl a) con-
246
Fig. 1. La Paz Bay, in the southwestern Gulf of California (in-
set). The gray star in the main panel indicates the position of
the oceanographic station and the site of the sediment trap
in the deepest part of the bay (~410 m)
Pardo et al.: Role of environmental seasonality in a cetacean community
centrations, vertical fluxes of biogenic matter, and
cetacean biomasses over the course of a year. The
results are put in a regional context (i.e. the south-
western gulf) using time series of remotely sensed
(satellite) measurements of surface wind, tempera-
ture (SST), and chlorophyll concentration (CHL).
Although direct measurements of the prey field
would have probably enhanced our understanding of
the relationships between cetaceans and the dynam-
ics of their physical habitat in the bay, collection of
such data was not possible due to logistical and
financial constraints. Indeed, quantitative and com-
prehensive assessments of the intermediate trophic
levels in the southwestern gulf are lacking. However,
considering that most cetacean species must con-
stantly search for food due to their high energetic
needs (Trites et al. 1997, Barlow et al. 2008), we inter-
pret their occurrence in the bay, at least in part, as a
response to the prey availability, which is in turn
aggregated by suitable physical and biological
mechanisms. Further, the evolutionary and ecologi-
cal adaptations of cetaceans to exploit specific types
of prey, such as zooplankton, small pelagic fish, or
squid (Pauly et al. 1998), facilitate such interpreta-
tion. This argument has been widely used to charac-
terize cetacean habitats (e.g. Au & Perryman 1985,
Hamazaki 2002, Doniol-Valcroze et al. 2007, Praca et
al. 2009) as well as to model cetacean abundance as
a function of predominant environmental conditions
(e.g. Becker et al. 2010, 2012, Gerrodette & Eguchi
2011, Forney et al. 2012), even when there is no
direct measurement of the potential prey.
MATERIALS AND METHODS
Study area
La Paz Bay is the largest and deepest embayment
in the Gulf of California (Fig. 1), with an area of
~2160 km
2
and a maximum depth of ~410 m. Water
exchange with the surrounding gulf occurs mainly
through the northern channel, called Boca Grande
(Salinas-González et al. 2003, Obeso-Nieblas et al.
2004). The bay lies within a tropical-subtropical tran-
sition zone that seasonally alternates between 2 well-
defined periods as a result of the monsoonal regime
that dominates the entire gulf. The temperate season,
from November to April (winter to spring), is domi-
nated by strong northwesterly winds that enhance
evaporation and increase the surface salinity, which
induces deep vertical convection (i.e. sinking). More
moderate southwesterly winds blow during the warm
season, from May to October (summer to autumn).
During this period, the water column receives the
influence of tropical waters, the thermocline deep-
ens, and the upper layer stratifies (Badan-Dangon et
al. 1991, Adams & Comrie 1997, Bordoni et al. 2004).
Hydrographic and biological conditions
The changes in the physical structure of the water
column and their influence on the base of the food
web, through nutrient supply, help us to identify the
predominant ecological conditions that attract differ-
ent cetacean species at different times of the year.
A number of physical, chemical, and biological vari-
ables were measured at an oceanographic station
located over the deepest part of the bay (~410 m;
Fig. 1). Between 17 February 2007 and 18 February
2008, 13 CTD profiles were taken to depths ranging
from 50 to 340 m. Temperature, salinity, and density
data were standardized to 1 m depth means. From
these values, we computed the Brunt-Väisälä fre-
quency (cycles h
−1
; also known as buoyancy fre-
quency), a measure of the degree of stratification
(Wahl & Teague 1983). The depth of maximum buoy-
ancy frequency in a profile corresponds to the depth
of the pycnocline. At the same site, 13 profiles of
Niskin-bottle samples were taken at discrete depths
according to 6 levels of light penetration (0.1, 1, 10,
33, 55, and 100%) estimated from Secchi disc meas-
urements following the Beer-Bourguer-Lambert law
(Walker 1982, Bustillos-Guzmán & Lechuga-Devéze
1989). Concentrations of dissolved silica (H
2
SiO
4
),
phosphate (PO
4
−3
), and total dissolved inorganic ni -
trogen (NO
2
−
+NO
3
−
+NH
4
−
) were measured from these
samples (Strickland & Parsons 1972), as well as the
concentration of chl a (Ritchie 2008). Since measure-
ments were taken at different times and in some
cases different depth levels, we performed an objec-
tive interpolation of these variables using a Gaussian
weighting function (Jalickee & Hamilton 1977, Boyer
et al. 2005) with 30 d horizontal and 1 m vertical
scales to represent the temporal evolution. All data
were truncated below 100 m depth since preliminary
evaluation of the results showed that most of the
variability was concentrated above that level.
Biogenic matter fluxes
The sinking particulate matter is indicative of the
nature of biogenic components and thus the ecologi-
cal succession taking place in the upper layers
247
Mar Ecol Prog Ser 487: 245–260, 2013
248
(Bishop 1988, Silver & Gowing 1991, Silverberg et al.
2006), which could trigger the incursion of different
cetacean species according to their feeding require-
ments. We analyzed samples from a Technicap
®
PPS
3/3 trap of 0.125 m
2
aperture, which was anchored
and suspended at ~310 m depth at the same site as
the oceanographic measurements (Fig. 1). The sink-
ing matter was collected in separate bottles during 7
to 15 d periods each and then fixed with a preser -
vative solution of 4% buffered formaldehyde satu-
rated with sodium tetra borate. The total mass flux, in
g m
−2
d
−1
, was estimated from 4 sub-samples, which
were centrifuged for 25 min at 3000 rpm (~1600 × g),
decanted, and washed with distilled water. The col-
lected material was weighed after a 72 h drying
period at ~50°C. The lithogenic fraction of the total
flux was subtracted since our interest was only
related to the biological processes. From the total
biogenic fractions, we analyzed the proportions of
biogenic silica, or opal (SiO
2
·nH
2
O), and calcium car-
bonate (CaCO
3
).
Local and regional seasonality
Because of their great mobility, the incursions of dif-
ferent cetacean species into the bay could be the
result of both local and/or regional conditions. There-
fore, it was important to address the larger spatial
context in which the hydrographic and biological con-
ditions within the bay occur. Also, since
the small sample sizes yielded by the
present study (14 monthly data points)
prevented us from quanti ta tively corre-
lating cetacean densities to the monthly
evolution of the water column within
the bay, it was important to compare
those conditions to longer time series of
surface variables and put them in the
spatial context of the southwestern gulf.
We therefore characterized the season-
ality of the entire region, from north of
Loreto Bay to south of La Paz Bay (Fig.
2), using an 11 yr time series of remotely
sensed SST and CHL as proxies for the
physical and biological en vironment.
The monthly CHL data came from the
Sea-viewing Wide Field-of-view Sensor
(SeaWiFS) aboard the satellite Orb-
view-2 (O’Reilly et al. 1998, 2000,
Hooker & McClain 2000), with a pixel
resolution of 1.39 km. The monthly SST
data came from the Advanced Very
High Resolution Radio meter (AVHRR)
aboard NOAA satellites (Program
Pathfinder 5.0; Walton et al. 1998, Casey
& Cornillon 1999, Kilpatrick et al. 2001),
with a spatial resolution of 4.89 km. Ad-
ditionally, we used the monthly wind
velocity data from the SeaWinds sensor
aboard the NASA satellite QuikSCAT
(Freilich 2000). Due to the coarser
spatial resolution of this product (13.9
km), only the measurement point closest
to the bay was used to compute the local
seasonality since the other available
nearby points were on land or too far
from the bay. All re motely sensed vari-
Fig. 2. Spatial representation of the 11 yr seasonal least-squares fits of sea sur-
face temperature (SST; upper panels; in a variable color scale to highlight spa-
tial gradients) and chlorophyll concentration (CHL; lower panels; same color
scale among panels) for the southwestern Gulf of California. The periods
shown were chosen following the maximum and minimum CHL values of the
sea sonal least-squares fit within La Paz Bay, which are denoted here and in
Fig. 7 as I, II, III, and IV
Pardo et al.: Role of environmental seasonality in a cetacean community
ables were obtained through the Environmental Re-
search Division’s Data Access Program of NOAA,
NMFS, Southwest Fisheries Science Center (http://
coastwatch. pfeg. noaa. gov/ erddap/ index. html). A spa-
tially explicit characterization of the seasonal cycle of
the southwestern gulf (Fig. 2) was done by fitting tem-
poral least-squares with annual and semi-annual har-
monics (Emery & Thomson 1998, Ripa 2002) to the re-
motely sensed variables. Within the polygon of the
bay (see map in Fig. 3), the temporal behavior of each
variable was calculated using the same analyses, ap-
plied to the mean of all monthly values. The periods of
maxima and minima resulting from the local (i.e.
within the bay) CHL seasonal analysis were chosen to
portray the results of the regional (i.e. southwestern
gulf) analysis of SST and CHL (Fig. 2).
Cetacean population density
We conducted monthly visual surveys within the
bay over a systematic zig-zag arrangement of tran-
sects (Fig. 3) aboard the 28 ft (8.5 m) RV ‘CICIMAR
XV’ at ~18 km h
−1
between 6 February 2007 and 23
March 2008. Two trained observers simultaneously
searched for cetaceans with the aid of 7 × 50 hand-
held binoculars (Fujinon
®
FMTRC-SX) equipped with
compass and vertical reticles, independently cover-
ing both sides of the transect line, from the front of
the vessel to an angle of 90°. A team of 4 observers
rotated every 40 min. Observations were made from
a platform at 5.09 m effective visual height. The per-
pendicular distance (x) from the transect line to the
sighting was calculated following Lerczak & Hobbs
(1998). The animals were approached to confirm
species identification only when they were within
~1.5 km of the transect line (i.e. closing mode tech-
nique; Dawson et al. 2008). Most of the large species
were easily identified beyond this distance, whereas
some dolphin schools remained unidentified as well
as some whales recorded too far from the transect
line. Search effort was suspended during the ap -
proach and the time spent with the animals as well
as when the Beaufort sea-state was higher than 3.
Monthly population densities (individuals km
−2
)
were estimated using distance sampling line-transect
techniques (Buckland et al. 2001) by modeling a
detection probability function g (x), based on the dis-
tribution of all perpendicular distances from the tran-
sect line to the groups sighted of each species. Since
the cetacean surveys have continued within and out-
side the bay after the completion of the present study,
we used all of the perpendicular distances available
through April 2012 to improve the modeling of the
detection functions (Fig. 4). We established a priori
truncation points (w) based on the frequency distri-
bution of distances. The effective half-strip width (μ)
was estimated from the detection function to convert
the linear effort into an effectively sampled area
(Thomas et al. 2002). Several mathematical functions
(uniform, half-normal, and hazard-rate) and expan-
sion series (cosine, sine, simple polynomial, and her-
mit polynomial) were tested, and Akaike’s informa-
tion criterion (Burnham & Anderson 2002) was used
to choose the best fit (Table 1). This function, evalu-
ated at zero perpendicular distance, represents the
detection probability
ˆ
f(0). Mean group sizes
ˆ
E(s)
were estimated for the odontocetes and the fin
whale, whereas for the blue and the Bryde’s whale,
the few sightings of >1 animal were split into individ-
ual detections to avoid the increase of the variance
due to the indeterminacy of the expected group size.
For all species, we assumed that all animals located
directly on the track-line were detected and counted
(i.e. g (0) = 1). Finally,
ˆ
f(0) was used, together with the
number of counted groups (n) and the total transect
249
Fig. 3. Total survey effort by month (bars) and the average length of transects in each month (dotted line with circles). Map
shows the polygon of La Paz Bay (red line) and the transect track lines (dark grey lines)
Mar Ecol Prog Ser 487: 245–260, 2013
length (L), to estimate a point density value (
ˆ
D) for
each month (Thomas et al. 2002). The variance
(D) and the lower and upper limits of the 95%
confidence intervals (D/C, D · C) were estimated by
a 999 iteration bootstrap analysis of samples (i.e.
transects) at each stratum (i.e. month). For the less-
frequent species, we only calculated the encounter
rate of groups as the number of sightings recorded in
the total linear effort in each survey. Although both
the short-beaked common dolphin Delphinus delphis
and the long-beaked common dolphin Delphinus
capensis occur in the Gulf of California, we treated
them at the genus level, given the difficulty in identi-
fying them to species level in most sightings.
Cetacean biomass
The population density estimates (individuals km
−2
)
were converted into values of biomass (t km
−2
) to
make the species comparable. This was
done by multiplying the estimated density
by the mean species-specific body mass
values previously reported for the Califor-
nia Current (Barlow et al. 2008 and refer-
ences therein). These values come from
both direct measurements and regression
models of body mass as a function of the
mean body length (Table 2).
RESULTS
Hydrographic and biological conditions
Temperature dominated the density
structure in the water column (Fig. 5). Cold
water (<18°C) occurred throughout the first
100 m during the winter (February 2007
and January to February 2008). During
March 2007, the upper 75 m were above
20°C. From April to July, a doming of the
isotherms took place, and water below
17°C penetrated the surface layer up to
10 m. From June to November, the upper
25 m warmed above 25°C. December was a
transition period in which the temperature
in the upper 55 m cooled below 21°C. The
Brunt-Väisälä frequency (Fig. 6a) showed
3 major conditions over the year, defined
by the depth and degree of stratification.
High values indicate a strong stratification,
whereas low values mean strong mixing.
The low buoyancy contours in February to March
2007 and January to February 2008 indicated deep
mixing in the upper water column. During these win-
ter periods, the pycnocline (i.e. the maximum buoy-
ancy frequency along the profile) deepened to at least
100 m. Then, during the spring and early summer, the
buoyancies in the upper 25 m marked a period of
isopycnal shoaling, when the pycno cline almost
reached the surface. This doming of isopycnals lasted
4 mo, until early August, and it was followed by a
thickening of the stratified upper layer in the late
summer and autumn, marking conditions of deep
stratification, with the pycnocline around 40 m depth.
These conditions prevailed until December 2007,
when a mixed period developed again.
For nutrients, we only show the concentration (µM)
of the sum of all components (Fig. 6b) since concen-
trations of dissolved silica, phosphate, and total dis-
solved in organic nitrogen followed similar patterns
over the course of the year. Relatively high concen-
var
250
Fig. 4. Detection probability function (g(x); black line), estimated from the
distribution of per pendicular sighting distances (gray bars). The estimated
effective half-strip width (μ) is shown as a dashed vertical line. The total
number of distances used (n) is presented, specifying the number of dis-
tances from the study period and area (first value within parentheses) and
the distances taken from subsequent years and/or areas aboard the same
platform (second value within the parentheses)
Pardo et al.: Role of environmental seasonality in a cetacean community
trations of nutrients were found in the water column
during the mixing conditions in the winter, but there
was an evident depletion in the upper 50 m during
February and March 2007. The pycnocline shoaling
of the spring and early summer brought higher sub-
surface concentrations of nutrients to just below the
thermocline, reaching up to 50 μM in the top 100 m.
The surface and sub-surface concentration of nutri-
ents decreased in the late summer and autumn.
Two different types of chl a concentration peaks
occurred (Fig. 6c): during the winters of 2007 and
2008, high concentrations (~1.5 mg m
−3
) were re -
corded above the pycnocline in the upper 40 m and
upper 70 m, respectively, whereas under conditions
of shallow stratification, higher values (~2.5 mg m
−3
)
occurred as 2 sub-surface maxima in May and Au -
gust, just below the pycnocline. Low chl a concentra-
tions (<0.5 mg m
−3
) in the upper 100 m characterized
the deep stratified conditions of the late summer
(September to November). Biogenic silica contri -
buted strongly to the total biogenic flux from winter
to early summer, reaching a maximum of 60% in
April 2007, whereas carbonate (CaCO
3
) components
dominated during the late summer and autumn,
reaching 48% in October 2007 (Fig. 6d). The 2 com-
ponents showed completely opposite seasonal pat-
terns. A Pearson’s test resulted in a correlation of
−0.7032 (p = 0.002, 95% CI = [−0.8324, −0.5016], n =
40, effective degrees of freedom (N
eff
) = 17 following
Davis 1978).
Local and regional seasonality
The seasonal cycle of surface wind, SST, and CHL
showed different patterns within the bay. The wind
followed the monsoonal cycle (Fig. 7a). The annual
pattern of the temperature was unimodal, with a
251
Species Mean
ˆ
D Mean
ˆ
N %CV Group size %CV
ˆ
f(0) %CV Function Expansion
μ
(km) %CV w
(ind. km
−2
) (ind.)
ˆ
D,
ˆ
N
ˆ
E(s)
ˆ
E(s)
ˆ
f(0) series
μ
(km)
Bryde’s whale 0.0007 (0.0003, 0.0016) 1 (1, 4) 45.0 − − 0.77 (0.48, 1.23) 22.4 Half-normal Hermite 1.30 (0.81, 2.07) 22.4 −
polynomial
Fin whale 0.0022 (0.0012, 0.0034) 4.7 (3, 7) 32.2 1.3 (1.1, 1.6) 9.51 0.75 (0.56, 1.05) 23.1 Hazard rate Cosine 1.42 (1.08, 1.86) 13.5 4
Blue whale 0.0034 (0.0019, 0.0058) 7 (4, 13) 38.9 − − 0.98 (0.80, 1.19) 9.7 Uniform Cosine 1.02 (0.84, 1.24) 9.7 3
Bottlenose dolphin 0.1911 (0.0950, 0.3842) 412 (205, 828) 36.3 18 (13.6, 24) 14.52 1.76 (1.18, 2.62) 20.3 Hazard rate Hermite 0.57 (0.38, 0.84) 20.3 2
polynomial
Common dolphin 0.3943 (0.2140, 0.7263) 850 (461, 1566) 31.6 85.1 (60.4, 119.9) 17.41 1.18 (0.98, 1.41) 9.3 Half-normal Cosine 0.85 (0.71, 1.02) 9.3 2.4
Short-finned pilot 0.0154 (0.0044, 0.0454) 33.2 (9, 98) 70.3 27.7 (15.8, 48.8) 27.32 0.53 (0.35, 0.90) 30.1 Uniform Cosine 1.86 (1.32, 2.64) 16.6 −
whale
Table 1. Parameter results from the distance sampling analyses. Point estimates are provided, followed by the 95% confidence interval in parentheses and the percent-
age of the coefficient of variation (%CV) in a separate column to the right. From left to right: the mean population density (
ˆ
D), the mean total abundance (
ˆ
N), the esti-
mated group size (
ˆ
E(s)), the detection probability (
ˆ
f(0)), the effective half-strip width (μ), the mathematical function and the expansion series used in the model chosen,
and the a priori truncation point (w). (–) not available
Species Common name Mean body
mass (t)
Mysticetes
Balaenoptera edeni Bryde’s whale 16.477
Balaenoptera physalus Fin whale 42.150
Balaenoptera musculus Blue whale 57. 230
Odontocetes
Tursiops truncatus Bottlenose dolphin 0.188
(offshore)
Delphinus spp. Common dolphins 0.080
Globicephala Short-finned pilot 0.608
macrorhynchus whale
Table 2. Values of body mass used to standardize the density
estimates of the dominant species (after Barlow et al. 2008)
Mar Ecol Prog Ser 487: 245–260, 2013
maximum in September and a minimum in January
(Fig. 7b). In contrast, the CHL pattern was bimodal,
with a maximum in January (I in Fig. 7c), a decrease
in March (II in Fig. 7c), a secondary peak at the end
of May (III in Fig. 7c), and the main minimum in Sep-
tember (IV in Fig. 7c). Note that, except for the very
warm September period when CHL values were low-
est throughout the region (IV in Fig. 2), the values
within the bay tended to be higher than in the gulf
waters offshore. These values were similar to adja-
cent coastal areas in January (I in Fig. 2), lower than
offshore and coastal areas in March (II in Fig. 2), and
significantly higher than anywhere else in June (III in
Fig. 2). The least-squares SST values within the bay
were slightly warmer than elsewhere in January and
cooler the rest of the year, considerably so in June.
Cetacean population density
Altogether, the effective search effort within the
bay during the 14 mo totaled 3937 km (mean ± SD =
281 ± 137 km; Fig. 3). Four mysticete and 6 odon -
tocete species were identified from 276 sightings. The
blue whale, fin whale, Bryde’s whale, common dol-
phin, bottlenose dolphin, and short-finned pilot whale
were the most frequent species observed (Table 1,
Fig. 8). The humpback whale, sperm whale Physeter
macrocephalus, dwarf sperm whale Kogia sima, and
killer whale Orcinus orca were only sporadically
recorded (Fig. 8). Differences in the estimated effec-
tive half-strip widths (μ in Fig. 4) between species
typically suggest interspecific variations that deter-
mine their detectability, such as their body sizes,
grouping behavior, and/or level of surface activity
(e.g. Barlow & Forney 2007, Williams & Thomas 2007).
Mysticetes in general had the widest effective half-
strip widths due to their larger body sizes and taller
blows. Among the odontocetes, the short-finned pilot
whales had the largest effective half-strip width,
probably because of the combination of large groups
and large body sizes. They were followed by the com-
mon dolphins, whose high level of surface activity
and tendency to aggregate in very large groups make
them detectable at large distances. Bottlenose dol-
phins had the shortest distance range, which could be
attributed to their tendency to approach the vessel
and to the small group sizes recorded within the bay.
252
Fig. 5. Monthly progression of hydrographic variables in La Paz Bay (from objective interpolations using a Gaussian weighting
function). Each cast is shown as a vertical gray line
Pardo et al.: Role of environmental seasonality in a cetacean community
Cetacean biomass
Overall cetacean biomass was dominated by the
mysticetes and displayed 3 major peaks (Figs. 6e & 8).
The first occurred in spring, from May to June 2007,
the second covered late summer and autumn (Sep-
tember to December), and the third and highest was
in February 2008 (Fig. 6e). The odontocetes showed
an opposite pattern from the mysticetes (Fig. 6e):
They in creased in biomass when mysticetes de -
creased, showing 2 main peaks during July to August
2007 and in Jan uary 2008. The first mysticete peak of
the spring (0.62 t km
−2
) resulted from the co-occur-
rence of the 3 most frequent species but was domi-
nated by the blue whale (Fig. 8). In contrast, the
peaks of the late summer and autumn (0.73 and 0.63 t
km
−2
, respectively) were dominated by the fin whale
in the absence of the blue whale and the occurrence
of the Bryde’s whale, the latter always in low bio-
masses. Finally, the highest peak of mysticete bio-
253
Fig. 6. Physical and biological context underlying variations in cetacean biomass in La Paz Bay. (a) Buoyancy frequency, with
the dashed white line representing the depth of the pycnocline (i.e. maximum buoyancy frequency at each profile). Gray dots
show the depth of the Niskin-bottle samples for (b) nutrients and (c) chl a. (d) The contributions of biogenic silica (SiO
2
·nH
2
O)
and calcium carbonate (CaCO
3
) to the total biogenic sinking matter, shown as 7 to 15 d absolute values. (e) Monthly cetacean
biomass
Mar Ecol Prog Ser 487: 245–260, 2013
mass (1.87 t km
−2
) occurred during February 2008
and was also dominated by blue whales but in the
presence of fin and Bryde’s whales (Fig. 8). The first
peak of odontocetes biomass (0.30 to 0.27 t km
−2
, July
to August 2007) resulted from the increase in bottle-
nose dolphins and from the incursion of short-finned
pilot whales, whereas the second peak (0.35 t km
−2
)
was dominated by the common dolphins, with a mod-
erate increase of bottlenose dolphins, which domi-
nated the odontocete biomass during the rest of the
year (Fig. 8).
DISCUSSION
The strong mixing in winter and the isopycnal
shoaling in spring and early summer produced peaks
in surface and subsurface chl a concentrations,
respectively (Fig. 6c). The high proportion of opal in
the biogenic sinking matter (Fig. 6d) suggests that
these peaks were dominated by diatoms and sili-
coflagellates, whose blooms result from the input of
new nutrients into the euphotic zone (Egge & Aksnes
1992) and typically favor the aggregation of krill and
planktivorous fish (Kudela et al. 2008). Silicoflagel-
lates and diatoms have been previously found as
dominant among the micro- and nano-phytoplankton
within the bay (Verdugo-Díaz 2003). The former
have been associated with peaks of primary produc-
tion in winter and early summer (Villegas-Aguilera
2009, Martínez-López et al. 2012) and are abundant
in the siliceous fraction of the sediment trap samples
(Álvarez-Gómez 2010). These 2 chl a peaks observed
in the water column are in agreement with the
remotely sensed CHL peaks of the seasonal analysis
derived from the 11 yr least-squares regression
(Fig. 7). This constitutes evidence that the isopycnal
shoaling within the bay and its influence on phyto-
plankton is not a phenomenon particular only to the
sampled year cycle but a recurring intraseasonal
event of local nature. While the first CHL peak within
the bay corresponds to a general pattern of high CHL
values along the entire region of the southwestern
gulf (I in Fig. 2), especially near the coast, the second
corresponds to a local phenomenon, in which the bay
gets colder and CHL-richer than the surrounding
254
Fig. 7. Seasonal pattern of wind, sea surface temperature (SST), and chlorophyll concentration (CHL) in La Paz Bay. The black ar-
rows (a) and circles (b,c) represent the original monthly values. The seasonal fits of wind, SST, and CHL are drawn as blue arrows
and red and green lines, respectively. The seasonally adjusted maxima and minima of CHL are labeled as I, II, III, and IV, which
are the periods chosen to portrait the regional (i.e. the entire southwestern gulf) spatial-temporal fit of SST and CHL in Fig. 2
Pardo et al.: Role of environmental seasonality in a cetacean community
255
Fig. 8. Monthly estimates of cetacean biomass (±95% confidence intervals) for the dominant species and encounter rates (ER)
for the less-frequent species (bottom panel)
Mar Ecol Prog Ser 487: 245–260, 2013
gulf (III in Fig. 2). Note that even when the cold water
is at subsurface during the period of isopycnal shoal-
ing (Fig. 5), its influence on SST is also noticeable,
with the surface remaining ~1.5°C cooler than the
surrounding gulf.
The blue whale specializes on krill and dominated
the cetacean biomass during these 2 periods of sur-
face and subsurface chl a peaks, suggesting those
were suitable conditions for low trophic level prey. It
is also the only migratory cetacean among all of the
species recorded that feeds actively during its win-
tering period in the gulf (Del-Ángel-Rodríguez 1997,
Gendron 2002, Bailey et al. 2009). Variations of its
seasonal migration may be responses to a larger
scale of interannual oceanic conditions in a manner
that is still unstudied. At the seasonal and intra -
seasonal scales, however, it seems that the distribu-
tion of the species within the gulf is guided by the
persistence of local pulses of biological production
(Pardo et al. 2011) that aggregate krill (Gendron
1992). In one of its major feeding grounds off Califor-
nia, the blue whale abundance also increases in
response to the aggregation of krill resulting from the
upwelling pulses of the California Current (Croll et
al. 2005). In contrast, the migratory humpback whale
has been recorded only sporadically feeding on krill
within the gulf (Gendron & Urbán 1993), and its
occurrence is more associated with breeding activi-
ties during winter. Although krill may also serve as
prey for fin and Bryde’s whales during the winter and
spring within the bay, these species can also exploit
juvenile stages of Pacific sardine that aggregate
along the western coast of the gulf during this period
(Hammann et al. 1988, Tershy 1992, Tershy et al.
1993, Gendron et al. 2001, Jaume-Schinkel 2004)
and thus reduce com petition with blue whales. Small
pelagic fish are also the most likely prey for common
dolphins (Gallo-Reynoso 1991, Niño-Torres et al.
2006), which exploit the bay in large numbers during
winter. The higher biomasses of bottlenose dolphins
over the entire iso pycnal shoaling period (May to
August) may reflect the availability of mesopelagic
fish and/or squid, which are likely prey for this op -
portunistic species (Pauly et al. 1998, Díaz-Gamboa
2009).
In contrast, the deep stratification of the late sum-
mer and autumn was not conducive to high near-
surface nutrient or chl a concentrations. The increase
in the proportion of calcareous content in the settling
biogenic particles (Fig. 6d) suggests the presence
of coccolithophorids, foraminifera, and/or pteropods
(Romero et al. 2002). Coccolithophorids are better
adapted than silicoflagellates and diatoms to growth
at limiting nutrient levels and tend to dominate under
oligotrophic conditions (Iglesias-Rodríguez et al. 2002).
Nevertheless, despite their dominance, the total flux
of coccolithophorids does not increase at all during
the late summer in the bay (Rochín-Bañaga 2012),
and values of primary production drop (Reyes-Salinas
et al. 2003, Cervantes-Duarte et al. 2005). How then
might one explain the high peaks of fin and Bryde’s
whales at this time? The period of high surface water
temperatures near the coast frequently marks the
spawning season for several pelagic fish species in
the southwestern gulf (Moser et al. 1973), including a
‘warm stock’ of Pacific sardine that enters the gulf
(Félix-Uraga et al. 2004). These are likely the main
prey for rorqual whales during the deep stratification
period, as has been suggested from the δ
15
N ratios
between fin whales and sardines (Jaume-Schinkel
2004). Similarly, the short-finned pilot whale, along
with the other teutophagous odontocetes, such as the
dwarf sperm whale and the sperm whale (Clarke
1996, Pauly et al. 1998), were in the bay predomi-
nately during summer. The maximum biomass peaks
of the short-finned pilot whale (August and October
2007; Fig. 8) occurred just when the surface temper-
ature within the bay was the warmest (Fig. 5). Squid
searching for warm waters near the coast to spawn
typically aggregate under such conditions (Staaf et
al. 2008). Thus, we surmise that spawning prey, at
least the squid and the Pacific sardine, could sustain
the biomass of teutophagous odontocetes and fin
whales, respectively, during the deeply stratified
summer conditions.
The physical origin of some of the observed water-
column conditions in the bay is still not fully under-
stood. During winter, Ekman upwelling occurs along
the eastern coast of the gulf (Lluch-Cota 2000, Lavín
& Marinone 2003), but most blue whale sightings
(Gendron 2002) and large krill aggregations (Brinton
& Townsend 1980) occur on the western side during
this period. It is not clear if the series of eddies that
form regularly along the gulf (Pegau et al. 2002)
could be responsible for cross-gulf transport of nutri-
ents and plankton from east to west, where the mate-
rial could be retained. Nevertheless, since blooms of
siliceous phytoplankton typically occur in response
to new nutrient input, it is more likely that the phyto-
plankton biomass of the southwestern gulf is gener-
ated locally due to the strong vertical mixing (Fig. 6a)
produced by the northwesterly winds blowing during
winter (Fig. 7a). The high surface salinity (>35) ob -
served during this period (Fig. 5) reinforces the
hypothesis that strong northwesterly winds lead to a
high rate of evaporation, which in turn enhances
256
Pardo et al.: Role of environmental seasonality in a cetacean community
vertical mixing. The causes of the intraseasonal iso -
pycnal shoaling, associated with the second peak in
CHL within the bay, are also poorly known. Previous
studies have described cyclonic circulation (Mon-
real-Gómez et al. 2001, Sánchez-Velasco et al. 2006)
and proposed that it could be related to the wind
curl and the overall seasonal circulation of the
gulf (Beier 1997). This CHL peak occurs at a time
when the southwesterly wind maximum takes place
(Fig. 7a), which could also force the cyclonic circula-
tion and resulting Ekman pumping, but the subject
has not been investigated in detail due to the lack of
high-resolution data.
Nevertheless, it is clear that the isopycnal shoaling
enhances subsurface phytoplankton aggregations
within the bay at a time when the rest of the south-
western gulf remains oligotrophic. Therefore, it may
also be responsible for the higher annual values of
CHL previously described for the bay (Santamaria-
del-Angel et al. 1994, Luch-Cota & Teniza-Guillén
2000, Kahru et al. 2004). This phenomenon extends
the period of phytoplankton blooms that normally
would be associated only with the winter mixing.
Recent results of a long-term analysis of blue whale
density, comparing La Paz Bay to Loreto Bay, showed
that blue whales leave Loreto in April, earlier than
their departure from La Paz, where they can be seen
as late as June (Pardo et al. 2011). This pattern sug-
gests the importance of the intraseasonal isopycnal
shoaling within the bay as a potential driver of
krill aggregation in the southwestern gulf at a time
when the surroundings are comparatively warmer
and oligotrophic (III in Fig. 2).
The presence of cetaceans with different require-
ments over the course of the year in the bay suggests
a sustained availability of prey, aggregated by high
biological production or suitable physical conditions.
Recent measurements of the proportion of particulate
organic carbon in the sinking matter and the monthly
fluxes (export production) in the bay (Silverberg
2009, Silverberg et al. 2009) show that these do not
vary much seasonally, indicating that biological pro-
duction extends throughout the year regardless of
the type of physical forcing. The export production of
the bay is more than double that of Guaymas Basin,
often considered a particularly high production area
in the gulf (García-Pámanes et al. 2011). All of these
characteristics lead us to propose that La Paz Bay
constitutes a biological hotspot in the southwestern
Gulf of California, driven by the seasonal evolution of
regional surface mixing conditions in winter, local
isopycnal shoaling in spring and early summer, and
deep stratification in late summer and autumn. This
physical contrast attracts a wide variety of cetaceans
foraging at different trophic levels at different times
of the year and probably also favors the incursion of
other species of marine megafauna.
Future work should focus on addressing the infer-
ences drawn in the present study regarding the phys-
ical and biological mechanisms that drive cetacean
occurrence in the bay. Such work would require a
sampling grid aimed at resolving spatial patterns in
environmental variables concurrently with measure-
ments of the low, mid, and high trophic levels. Test-
ing these mechanistic linkages would require a
numerical modeling approach. Two species that
would be particularly amenable for such work are
the blue whale and the short-finned pilot whale
because of their specialist diet and because they
showed the most evident relationships with the envi-
ronment, with blue whales using the bay during peri-
ods of cool temperature, high CHL, and a primary
producer community dominated by siliceous phyto-
plankton, while short-finned pilot whales occurred
during warm, oligotrophic periods dominated by
calcareous phytoplankton. The physical mechanisms
driving isopycnal shoaling in the bay during spring
and early summer, which make this area biologically
richer than the surrounding gulf, should be investi-
gated through a study of the effects of the wind
field in combination with the local physiography (as
shown by Wingfield et al. 2011). The role of the
northwesterly winds in the evaporation and subse-
quent mixing of the surface layer during winter
should be studied to understand the reasons for the
aggregation of krill and blue whales along the west-
ern coast of the gulf rather than along the upwelling-
influenced eastern coast.
Acknowledgements. The present study received financial
support from the Consejo Nacional de Ciencia y Tecnología
(CONACyT) through the projects Monitoreo ecológico con-
tínuo de la Bahía de La Paz: Serie de tiempo (47310-F;
PI: N.S.) and Investigaciones Oceanográficas del Sistema
Frontal de Baja California (SEP-2008-103898; PI: E.B.), as
well as MSc and PhD scholarships to M.A.P. The Instituto
Politécnico Nacional (IPN) funded part of the field work
through the projects Monitoreo Ecológico Continuo en
Bahía de La Paz (SIP 20040095, 2005-0274, 20060199,
20070664, 20080650, 20090523; PI: N.S.) and Estructura
poblacional y movimiento de algunos cetáceos del Golfo de
California (SIP 20070803; PI: D.G.). D.M.P. was supported by
funding from the NASA Applied Sciences Program, Earth
Science Division, through a grant provided by Research
Announcement NNH07ZDA001N, Research Opportunities
in Space and Earth Sciences (ROSES-2007), Program
Element A.20: Decision Support through Earth Science
Research Results. M.A.P. also received funding from the IPN
(PIFI grant), Centro Interdisciplinario de Ciencias Marinas
(CICIMAR-IPN; M.Sc. Recovery Funds), The Society for
257
Mar Ecol Prog Ser 487: 245–260, 2013
Marine Mammalogy (Grants in Aid of Research 2009),
Cetacean Society International, American Cetacean Society
(Monterey Bay Grant 2008), and The Ocean Foundation. We
are grateful to all of the personnel from Laboratorio de
Ecología de Cetáceos y Quelonios and Departamento de
Oceanología at CICIMAR-IPN for their support during en -
vironmental and cetacean sampling. We also thank NOAA
CoastWatch Program, NASA’s Goddard Space Flight Center,
and GeoEye for making the satellite data products readily
available. Valuable comments during the study were pro-
vided by R. Palomares, G. De-La-Cruz-Agüero, O. Victori -
vich, R. Díaz-Gamboa, G. Busquets-Vass, and A. Martínez-
López from CICIMAR-IPN.
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Submitted: July 9, 2012; Accepted: December 6, 2012 Proofs received from author(s): April 1, 2013
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