MARINE MAMMAL SCIENCE, 27(3): 622–643 (July 2011)
C 2010 by the Society for Marine Mammalogy
DOI: 10.1111/j.1748-7692.2010.00428.x
Severe Karenia brevis red tides influence juvenile
bottlenose dolphin (Tursiops truncatus) behavior
in Sarasota Bay, Florida
KATHERINE A. MCHUGH
JASON B. ALLEN
AARON A. BARLEYCORN
RANDALL S. WELLS
Sarasota Dolphin Research Program,
Chicago Zoological Society,
c
/ o Mote Marine Laboratory,
1600 Ken Thompson Parkway,
Sarasota, Florida 34236, U.S.A.
E-mail: [email protected]
ABSTRACT
Harmful algal blooms (HABs) are natural stressors in the coastal environment
that may be increasing in frequency and severity. This study investigates whether
severe red tide blooms, caused by Karenia brevis, affect the behavior of resident coastal
bottlenose dolphins in Sarasota Bay, Florida through changes to juvenile dolphin
activity budgets, ranging patterns, and social associations. Behavioral observations
were conducted on free-ranging juvenile dolphins during the summer months of
2005–2007, and behavior during red tide blooms was compared to periods of
background K. brevis abundance. We also utilized dolphin group sighting data
from 2004 to 2007 to obtain comparison information from before the most severe
recent red tide of 2005 and incorporate social association information from adults
in the study area. We found that coastal dolphins displayed a suite of behavioral
changes associated with red tide blooms, including significantly altered activity
budgets, increased sociality, and expanded ranging behavior. At present, we do not
fully understand the mechanism behind these red tide-associated behavioral effects,
but they are most likely linked to underlying changes in resource availability
and distribution. These behavioral changes have implications for more widespread
population impacts, including increased susceptibility to disease outbreaks, which
may contribute to unusual mortality events during HABs.
Key words: red tide, bottlenose dolphin, Tursiops truncatus, harmful algal bloom,
Karenia brevis, sociality, activity budget, ranging behavior, social networks.
Periodic environmental disturbances can affect animals in a variety of ways, from
subtle changes in food abundance and distribution that may alter behavior to direct
changes in the physical environment that may result in mortality. Many species
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623
are also impacted by human disruption of natural ecosystems, which can increase
habitat fragmentation and alter the intensity of natural disturbance patterns. In the
marine environment, human disturbance, including habitat destruction, pollution,
and overfishing, is often a major focus of research and management concern. However,
natural disturbances, including harmful algal blooms (HABs), can also affect marine
species. These typically short-term events provide opportunities to explore sublethal
changes that may occur in animal populations present at the time of a disturbance
event. As such, they can serve as proxies to help predict impacts that may occur with
more widespread environmental disruption, which could result from global climate
change, large-scale coastal habitat alteration, or overfishing of prey species.
While documenting any direct population impacts of a disturbance event is a first
priority (e.g., mortality or morbidity of affected animals), indirect effects on animal
populations may also result from changes in resource availability and distribution or
habitat quality. These factors may alter the behavior and sociality of animals in disturbed habitats, and the potential consequences of these changes may be overlooked
despite the fact that they can affect fitness of individuals, which may ultimately
affect population viability in the event of long-term disturbance. For example, in a
recent review, Banks et al. (2007) found that habitat fragmentation had affected social interactions (such as home range use, territoriality, group size, and antipredator
behavior) in a number of terrestrial species, including primates and social carnivores, due mainly to changes in resource availability, interspecific interactions, mate
availability, and inbreeding risk.
For marine mammals, most of the disturbance-related research to date has focused
on the effects of humans on various marine mammal species. Studies typically either examine the effects of anthropogenic disturbance from boats and tourism (e.g.,
Nowacek et al. 2001; Constantine et al. 2004; Bejder et al. 2006a, b; Dans et al.
2008; Stockin et al. 2008) or human-generated noise in the marine environment
(e.g., Nowacek et al. 2007, Weilgart 2007, Tyack 2008). However, a growing body of
research is focusing on the effects of natural disturbance regimes such as HABs (Fire
et al. 2008b, Goldstein et al. 2008, Fire et al. 2009, Torres de la Riva et al. 2009),
periodic environmental oscillations including El Niño (Wells et al. 1990, Benson
et al. 2002, Lusseau et al. 2004, Whitehead and Rendell 2004, Keiper et al. 2005,
Ballance et al. 2006, Leaper et al. 2006, Trathan et al. 2007), and catastrophic events
such as hurricanes (Miller et al. 2010; Elliser and Herzing 2010) on marine mammal
populations.
Harmful algal blooms are fairly common natural stressors in the coastal environment in some regions that appear to be increasing in frequency and severity (Van
Dolah 2000, Hallegraeff 2003, Van Dolah 2005) and have been known to impact
marine mammal health (Gulland and Hall 2007). One type of HAB, the Florida
red tide, is caused by the toxic dinoflagellate Karenia brevis. Blooms of this species
occur periodically along the west Florida coast and have been linked to mortality of
many species including fish, seabirds, sea turtles, and marine mammals (Gunter et al.
1948, Landsberg 2002, Flewelling et al. 2005, Hinton and Ramsdell 2008, Pierce
and Henry 2008, Gannon et al. 2009, Landsberg et al. 2009).
In Sarasota Bay, K. brevis blooms have occurred frequently over the past decade,
allowing researchers to examine red tide-associated changes in coastal ecosystems
affected by the blooms. For example, Gannon et al. (2009) recently found dramatic
changes in nearshore fish communities from two red tides occurring during 2005 and
2006. As top predators, bottlenose dolphins (Tursiops truncatus) can serve an important
function as sentinels of environmental health in coastal waters (Ross 2000, Wells
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et al. 2004, Bossart 2006, Moore 2008, O’Shea and Odell 2008, Stewart et al. 2008).
Because of this sentinel function, bottlenose dolphin responses to disturbance events,
such as red tides, can be indicators of more widespread ecosystem change. To date,
most studies on red tide and dolphins have focused on exposure pathways (Fire et al.
2008a, Hinton and Ramsdell 2008, Pierce and Henry 2008, Landsberg et al. 2009)
and brevetoxin accumulation in carcasses and live animals (e.g., Flewelling et al.
2005; Fire et al. 2007, 2008b).
This study investigates whether red tide affects the behavior of resident coastal
bottlenose dolphins through changes to juvenile dolphin activity budgets, ranging
patterns, and social associations. The primary objective of this study is to quantify
behavioral change associated with red tide disturbance to understand the various
ways in which HABs may impact coastal dolphin populations.
METHODS
Study Site/Population
Sarasota Bay is home to one of several overlapping long-term resident dolphin
communities on the central west coast of Florida that inhabit shallow waters inshore
of barrier islands as well as nearshore in the Gulf of Mexico (Scott et al. 1990).
The resident community ranges along 40 km of coastline, covering approximately
200 km2 from southern Tampa Bay to Venice Inlet (Fig. 1; Wells 2003, 2009). This
community has been intensively studied since 1970, providing much background
knowledge on the population (e.g., Wells et al. 1987, Scott et al. 1990, Wells 1991,
Barros and Wells 1998, Duffield and Wells 2002, Wells 2003). Approximately 150
individually identifiable dolphins are resident in the area, and long-term site fidelity
spanning at least five concurrent generations has been documented (Wells 2003,
2009). Based on long-term observations and periodic capture-release efforts, over
90% of the resident dolphins are of known age, sex, and/or maternal lineage, and the
fission-fusion social structure of the community is well documented (Wells 2003,
2009).
Data Collection
As part of a larger project on juvenile dolphin behavioral development, we conducted multiple 2 h behavioral observation sessions on a cross-section of male and
female juvenile dolphins in the summers of 2005 to 2007, using focal animal sampling techniques (Altmann 1974, Mann 1999). During this period, Sarasota Bay
experienced two red tide events, which were identified by high K. brevis cell densities
throughout the study area and associated fish kills (Gannon et al. 2009). A prolonged
and intense red tide occurred throughout 2005, followed by a shorter, less severe
bloom during August–December 2006. We observed the behavior of 27 individually
identifiable juvenile dolphins (Table 1) ranging in age from 2 to 13 yr during three
3 mo field seasons: July–September 2005, June–September 2006, and June–August
2007.
Focal individuals were located by daily boat-based surveys of the study area during
daylight hours. After encountering a dolphin group, we collected basic sighting
information, photographed group members, and identified known dolphins via dorsal
fin features prior to beginning behavioral observations (termed “focal follows” or
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
625
Figure 1. Map of the Sarasota Bay study area.
“follows”) on specific individuals (“focal animals”). To allow for dolphin habituation
to our presence, focal follows began only after at least 15 min had elapsed from the
initial sighting. All follows were conducted from a 7 m outboard-powered, centerconsole boat with an observation tower that permitted observers to consistently view
all dolphins within a radius of approximately 250 m. Generally, the first subject
individual encountered during the day was selected as a focal animal, and if two or
more potential focal animals were present in a group then we chose the individual
that had been followed less often or less recently.
During follows, we recorded latitude and longitude, water depth, habitat type,
activity state of the focal animal, number and identity of all dolphins within 200 m of
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Table 1. Summary characteristics of juvenile focal dolphins and number of 3 min instantaneous behavioral observations per individual.
ID
F109
F123
F125
F133
F135
F137
F151
F159
F165
F173
F177
F179
F187
F197
Mean:
Females (n = 14)
Year
Age independent Observations
10
7
7
6
5
5
5
9
6
3
3
3
2
2
5.2
1999
2008
2002
2005
2005
2008
2004
1999
2002
2006
2005
2005
2004
2007
2004
∗2
46
284
28∗ 2
295
202
267
253
274
129∗ 3
278
60∗ 1
287
262
121∗ 4
199
ID
Males (n = 13)
Year
Age independent Observations
F146
F148
F178
F188
F196
F198
F218
F220
F224
F226
F228
F230
F232
9
9
10
9
7
9
6
6
3
3
6
3
3
2001
1999
1999
2000
2002
1999
2004
2002
2005
2005
2005
2007
2006
262
243
248
279
292
254
171∗ 1
229
283
283
272
156∗ 1
281
Mean:
6.3
2003
231
∗
Note: Age given is from 2005, the beginning of the behavioral study. Indicates individuals
that were not followed in all seasons, including animals that: (1) died/disappeared, (2) had a
calf (matured beyond the juvenile period), (3) were not able to be followed, or (4) were not
yet included in the focal group during a particular season.
the focal animal, and an estimate of group size at 3 min intervals. If the focal animal
could not be located within 2 min of the time point, no data were recorded for that
interval. Groups were defined operationally as all animals sighted at one time moving
in the same general direction, engaged in similar activities, or interacting with each
other within a radius of approximately 100 m. Activity states (such as travel, rest,
forage, social, or mill; see Table 2) were recorded as the activity that occurred most
often during the 3 min interval. Changes in group membership were noted when
they occurred, and photographs of joining dolphins were taken to confirm their
identity. An onboard Global Positioning System (Garmin GPS-12) unit was used to
Table 2. Operational definitions of dolphin activity states from behavioral observations.
Behavior
Code
Definition
Forage
Mill
FO
MI
Other
OT
Rest
Social
RE
SO
Travel
TR
Dolphin displaying feeding behaviors or actively catching fish.
Nondirectional movement, often in conjunction with other
activities, such as searching for food.
Less frequently observed behaviors including interactions with
boats and object play.
Slow, quiescent activity in absence of other identifiable activities.
All active interactions with other dolphins, including contact,
chasing/following, sexual interactions, and aggression.
Directed movement, including zig-zag movement.
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
627
track the focal dolphin’s location because the boat typically remained within 20 m
of the focal individual during follows.
This study also made use of a long-term sighting database for Sarasota Bay containing records of over 37,000 dolphin groups encountered from 1970 to 2008.
Records include the date, time, location, number and identifications of animals of
different age classes, environmental conditions, and activity states. These data were
used for more comprehensive analyses of association and ranging patterns as well as
to provide baseline data from 2004, before the severe red tide event and behavioral
data collection for this project began.
Data Analysis
Behavioral data from summer focal follows were designated as coming from one
of two sampling periods: (1) red tide (RT; all 2005, August–September 2006)
or (2) nondisturbance (non-RT; June–July 2006, all 2007). Red tide events were
defined after Gannon et al. (2009) based on K. brevis cell counts high enough to
result in fish kills in the study area during observations (>105 cells/L). Behavioral
differences between RT and non-RT periods were determined using paired t-tests or
Wilcoxon signed-ranks tests if data did not meet assumptions of parametric tests.
We stratified the survey data for focal individuals annually for 4 yr surrounding
and including the most severe recent red tide period: 2004 (baseline, pre-RT), 2005
(severe RT), 2006 (recovery/moderate RT), 2007 (recovery/non-RT). To ensure at least
10 sightings per individual for analysis of association patterns and ranging behavior,
we included survey data from the entire calendar year. Nonparametric Friedman
repeated measures analysis of variance (ANOVA) on ranks was used to determine
significant differences in behavior patterns among years, and where appropriate,
post hoc pairwise comparisons between years were conducted using Tukey’s test.
Significance was assigned at the P < 0.05 level throughout, and tests were conducted
in SigmaStat 3.5 unless otherwise noted.
Activity Budgets
Overall activity budgets from focal follows were calculated for each individual by
summing time spent engaged in major activities (i.e., travel, mill, forage, social and
other) across all observation sessions, standardizing for amount of time observed.
Comparisons of overall activity budgets between time periods were made using Gtests of independence in PopTools 3.1.1 (Hood 2009), and disturbance-associated
differences in the proportion of time spent engaged in specific behaviors were determined using paired t-tests.
In order to account for the potential confounding factor of diurnal variation in
behavior, we compared the overall distribution of observation points across different
parts of the day in RT vs. non-RT periods using G-tests. We divided the typical
daily observation period (0900–1700) into four 2 h blocks of time and summed the
number of observation points collected during each block. Very few observations
took place earlier or later than this period.
Sociality
Three measures of sociality were calculated for each focal individual and compared
across RT and non-RT periods: (1) proportion of time spent alone, (2) average group
size, and (3) number of associates. Proportion of time spent alone was calculated by
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Table 3. Social network metrics calculated for the Sarasota Bay community (after Croft
et al. 2008, Whitehead 2008).
Metric
Strength
Reach
Density
Distance
Diameter
Description
Measure of direct connections or gregariousness. Calculated as the sum
of association indices of an individual with all other individuals.
Measure of indirect connectedness in the network or overall strength of
network neighbors.
The proportion of possible connections between individuals that are
actually connected or how linked the associates of individuals are.
Measure of how far away others are in the network or the number of
connections needed in the shortest path between individuals in a
network.
Measure of the network as a whole rather than of individual nodes. The
number of connections needed in the shortest path between the two
most distant individuals in the network.
summing the time that each individual was solitary (i.e., without any other group
members within ∼100 m) during behavioral observation sessions, standardizing for
observation time. Group size measures were calculated from both types of available
data: average group size was calculated from behavioral observations during RT and
non-RT time periods separately, and annual average group size by individual was
calculated from sighting records. This was done not only to allow for a pre-RT
measure from 2004 but also because we suspected that measures of group size from
focal follows may be negatively biased due to difficulties associated with following
specific individuals as group size increases. The raw number of associates for each
individual was calculated annually from sighting records by summing the total
number of unique individuals observed interacting with each focal juvenile that year.
In order to account for yearly differences in effort, we also calculated a standardized
measure using only sighting data collected from monthly population monitoring
photographic identification surveys, which take place on 10 d each month throughout
the year. The annual number of associates seen interacting with focal individuals
during these standardized surveys was summed and divided by the total number
of times each individual was seen during these surveys to account for differences in
sighting frequency among individuals.
Group Stability
As a measure of fine-scale group stability, we calculated the fission-fusion rate for
each individual from behavioral observations made during red tide and nondisturbance seasons. Fission-fusion rates for focal individuals were calculated by dividing
the number of group composition changes (individuals either leaving or joining
our focal animal’s group) during observation sessions by the number of observation
hours.
Social Network Measures
In addition to individually based measures of sociality for focal juveniles, we
calculated annual community-wide social metrics (Table 3) using SOCPROG 2.3
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
629
(Whitehead 2009) and UCINET 6.0 (Analytic Technologies, Harvard, MA). These
analyses allowed us to explore changes in the overall social environment during disturbance events and examine consistency between the social changes exhibited by
juveniles during disturbance to those shown by adults in the community. Annual
pairwise association matrices were calculated in SOCPROG for all individuals seen
≥10 times per year in Sarasota Bay during 2004–2007 by applying the half-weight
index (HWI) to sighting data using a daily sampling period. These association matrices were then quantitatively analyzed in the network statistics module of SOCPROG
to calculate weighted social network measures for both direct connectedness (strength)
and indirect connectedness (reach) of all individuals and for adults and juveniles separately each year based on associations greater than zero. Standard errors for these
network measures were calculated using the bootstrap method with 1,000 replicates, allowing for comparison between age classes and years. The annual association
matrices were also visualized as social networks using NetDraw for all associations
with HWI ≥ 0.2. For each visualized network, we used Ucinet to calculate the total
number of network ties (associations) present, the network diameter, as well as the
average density, and average distance for individuals in the community that year.
Ranging Behavior
Average travel distance during behavioral observations was calculated for GPS
track lines recorded from individual focal follows using XTools Pro version 1.0.1
in ArcGIS 9.2 (Environmental Systems Research Institute, Redlands, CA). Distance
traveled was standardized for observation time (km/h) and stratified into red tide and
nondisturbance seasons for analysis.
Overall ranging areas (95% utilization distribution, UD) for each focal individual
were determined by applying the fixed-kernel method (Seaman and Powell 1996,
Seaman et al. 1999, Powell 2000) to location data from sighting records using
the Animal Movements extension in ArcView GIS 3.3 (Hooge and Eichenlaub
1997). Land was clipped from these ranges in ArcGIS 9.2 before overall areas were
calculated in square kilometers using XTools Pro version 1.0.1. Annual home ranges
were determined for each focal individual for all 4 yr of interest: 2004, 2005, 2006,
and 2007. Because of known reductions in home range size coincident with calves’
life history transition to independence (McHugh 2010), individuals who were not
yet independent of their mothers in 2004 (before the behavioral study began) were
excluded until the year they became independent.
RESULTS
Activity Budgets
In all seasons, juvenile dolphins spent the majority of their time traveling, with less
time devoted to milling, foraging, and socializing (Fig. 2). Other activities accounted
for less than 5% of the overall activity budget in any season. Overall juvenile dolphin
activity budgets differed significantly between red tide and nondisturbance time
periods (G-test: G = 297.78, df = 4, P < 0.0001).
Paired t-tests between red tide and nondisturbance periods (all df = 21) showed
that the proportion of time juvenile dolphins spent engaged in specific behaviors
differed based on disturbance, with juvenile dolphins spending more time milling
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Figure 2. Juvenile dolphin activity budgets during red tide and nondisturbance time
periods.
(x ± SD = 25.4 ± 9.9% vs. 18.4 ± 4.6%; t = 2.338, P = 0.03) and socializing (x ±
SD = 13.0 ± 13.3% vs. 5.8 ± 3.9%; t = 2.661, P = 0.02) and less time foraging
(x ± SD = 8.9 ± 8.3% vs. 18.5 ± 10.3%; t = −4.211, P < 0.001) during red tide
events. Time spent traveling (x ± SD = 54.4 ± 9.3% non-RT vs. 51.2 ± 15.2%
RT, t = −1.057, P = 0.30) and engaged in other activities (x ± SD = 2.9 ± 2.6%
non-RT vs. 1.5 ± 1.9% RT, t = −1.633, P = 0.12) did not differ significantly based
on disturbance events.
There was no difference in the distribution of observation points throughout the
day (G-test: G = 2.25, df = 4, P = 0.69) that might account for the observed
differences in activity budgets between RT and non-RT periods.
Sociality: Time Alone
Juvenile dolphins on average spent approximately 50% less time alone during red
tide events (x ± SD = 14.4 ± 14.6%; Median = 10.9%) than during nondisturbance
times (x ± SD = 27.7 ± 23.1%; Median = 19.9%; Wilcoxon signed-rank test:
W = 163, Z = 2.646, P = 0.009, n = 22), and they displayed reduced variability in
proportion of time alone during disturbance events (range: 0%–43% RT vs. 0%–93%
non-RT).
Sociality: Group Size
Average juvenile group sizes from follows were larger during disturbance events
(x ± SD = 4.79 ± 1.88 individuals/group) than non-RT periods (x ± SD = 3.22 ±
1.02 individuals/group; paired t-test: t = 3.83, df = 21, P < 0.001), with an
additional 1.5 individuals per group on average during red tide.
Average group size per year calculated from monthly photographic identification
surveys showed a similar trend of increased group size with disturbance (Fig. 3), and
the Friedman repeated measures ANOVA indicated significant differences in median
group size among years (␹ 2 = 45.13, df = 3, P < 0.001). Group size during the
severe red tide of 2005 (x ± SD = 9.88 ± 2.46 individuals/group, median = 10.41)
was significantly higher than all other years as determined by the post hoc Tukey test
(all P < 0.05), with half again as many individuals per group on average as compared
to other years. No significant differences were found in comparisons of the moderate
disturbance year of 2006 (x ± SD = 6.75 ± 1.05 individuals/group, median = 6.33)
to the two nondisturbance years of 2004 (x ± SD = 5.88 ± 1.13 individuals/group,
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
631
Figure 3. Box plot of juvenile dolphin group size by year from monthly photographic
identification survey data. Boxes range from the 25th to 75th percentiles. Solid line is the
median value. White circles represent 5th and 95th percentile outliers.
median = 5.61) and 2007 (x ± SD = 5.89 ± 1.01 individuals/group, median =
5.71).
Group size values from behavioral observations appear to be skewed toward smaller
dolphin groups than those from general survey data, especially during disturbance
periods, where average group size from sightings (x ± SD = 9.88 ± 2.47 individuals/group) was nearly double that from behavioral data during the same time period
(x ± SD = 4.79 ± 1.88 individuals/group; paired t-test: t = 11.61, df = 25, P <
0.001). This trend continued for nondisturbance periods, with paired t-tests (t =
12.47, df = 22, P < 0.001) again indicating significantly larger mean group sizes for
focal juvenile dolphins from survey data (x ± SD = 5.90 ± 1.01 individuals/group)
as compared to behavioral observations (x ± SD = 3.19 ± 1.01 individuals/group).
Sociality: Number of Associates
Juveniles interacted with more unique associates during the severe red tide of 2005
than in any other year (Table 4), nearly doubling the number of different individuals
they had associated with during the preceding baseline year of 2004. Raw numbers
of associates from 2006 and 2007 fell between the values for the baseline and severe
disturbance years. A nonparametric Friedman repeated measures ANOVA indicated
a significant difference in median number of associates among years (␹ 2 = 42.07,
df = 3, P < 0.001), and post hoc tests determined that the number of associates in
the baseline year of 2004 was significantly smaller than any other year and that the
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Table 4. Average number of different associates of juvenile dolphins by year.
Year
n
2004
2005
2006
2007
27
27
25
25
Raw number of associates
Mean ± SD
Median
56.74 ± 13.22
95.93 ± 23.08
74.92 ± 15.53
83.44 ± 15.65
56
96
78
80
Standard number of associates
Mean ± SD
Median
2.53 ± 0.59
3.78 ± 1.15
2.62 ± 0.84
2.00 ± 0.60
2.5
4.0
2.44
1.95
Note: Raw values correspond to the total number of distinct individuals observed associating
with focal juveniles each year. Standardized values are raw numbers divided by the number of
sightings of each individual per year, utilizing data from systematic monthly photographic
identification population monitoring surveys only.
raw number of associates during the severe red tide year of 2005 was also larger than
the moderate year of 2006 (all P < 0.05).
However, because the raw total number of different associates may be affected by
effort differences, we repeated this analysis using a standardized number of associates
derived only from sightings during systematic monthly photographic identification
population surveys (Table 4). The Friedman repeated measures ANOVA on these
standardized values determined that median number of associates still differed significantly among years (␹ 2 = 27.86, df = 3, P < 0.001). Post hoc tests revealed that
when effort was properly accounted for, juvenile dolphins had a greater number of
associates during the severe red tide year of 2005 than during any other year (Fig. 4,
all P < 0.05).
Group Stability
Juvenile dolphin groups were significantly less stable during disturbance periods
(paired t-test: t = 2.31, df = 21, P = 0.03), with average fission-fusion rates over
40% higher during red tides (x ± SD = 4.04 ± 1.76 group composition changes
per hour) than during nondisturbance periods (x ± SD = 2.88 ± 1.64 changes/h).
However, this relationship may be a side effect of increased group size, because
fission-fusion rates during focal follows were also found to have a significant positive
correlation with group size (r = 0.47, P < 0.001, n = 205 follows).
Social Network Measures
The social network structure of resident dolphins in Sarasota Bay changed substantially during the severe red tide disturbance of 2005 (Fig. 5). The overall community
network in 2005 was significantly more connected, both in the number of direct ties
between individuals and in average density, than any other year. There were almost
four times as many direct connections between individuals in 2005 (1,252 ties) as
compared to the baseline year of 2004 (320 ties), and over twice as many ties as in
2006 (492 ties) or 2007 (528 ties). Similarly, the average density was nearly twice
as high in 2005 as any other year. In addition, the diameter and average distance
of the community network were both smaller in 2005 as compared to any other
year, meaning that there were fewer steps necessary both in the longest shortest path
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
633
Figure 4. Box plot of standardized number of different associates by year from monthly
photographic identification survey data. Boxes range from the 25th to 75th percentiles. Solid
line is the median value. White circles represent 5th and 95th percentile outliers.
between two nodes in the network and in the average shortest paths to get from one
individual to another in the community during the severe red tide.
Finally, in both direct (strength) and indirect (reach) connectedness (Table 5), average
measures were significantly higher during the severe red tide of 2005 than any other
year (P < 0.05; determined because the difference in mean values between years
was greater than twice the sum of the bootstrapped standard errors calculated in
SOCPROG). Juveniles and adults displayed similar patterns, and values did not
differ substantially between age classes in any year.
Ranging Behavior: Short-term Travel Distance
Overall, juvenile dolphins traveled greater distances per hour during red tide
seasons (x ± SD = 4.0 ± 0.54 km/h) than nondisturbance seasons (x ± SD nonRT = 3.7 ± 0.47 km/h; paired t-test: t = 2.614, df = 21, P = 0.02). This translates
to total travel distances of 96 km/d during disturbance periods vs. 88.8 km/d in
nonbloom periods, or additional 7.2 km traveled per day on average during red
tides.
Ranging Behavior: Home Range Size
Annual home range sizes for individual juvenile dolphins were significantly larger
during years in which red tide events took place than years in which there was
no disturbance (Fig. 6), with individuals ranging the farthest during the most
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Figure 5. Sarasota Bay social networks 2004–2007. Annual networks include all individuals
in the community seen ≥10 times that year, and connections displayed are all associations
with HWI ≥ 0.2. Sex classes: black = female; white = male, gray = unknown. Age classes:
circles = dependent calves, triangles = independent juveniles, squares = adults, diamonds =
unknown.
severe disturbance period in 2005 (x ± SD = 113.66 ± 82.6 km2 , median =
88.69 km2 ), followed by the moderate disturbance year of 2006 (x ± SD = 98.64 ±
80.53 km2 , median = 69.91 km2 ), then the baseline and recovery years of 2004
(x ± SD = 76.56 ± 54.17 km2 , median = 59.61 km2 ) and 2007 (x ± SD =
72.52 ± 67.42 km2 , median = 54.97 km2 ). Friedman repeated measures ANOVA
determined a significant difference in home range size among years (␹ 2 = 13.80,
df = 3, P = 0.003), with post hoc comparisons showing that median home range size
for juvenile dolphins was larger in both years in which red tide was present (2005
and 2006) as compared to the baseline year of 2004 (both P < 0.05).
DISCUSSION
Juvenile dolphins displayed a suite of behavioral changes associated with red
tide disturbances in Sarasota Bay, Florida, including significantly altered activity
budgets, sociality, and ranging patterns. At present, we do not fully understand the
mechanism behind these red tide-associated behavioral effects. While it is possible
that individuals present during red tides may have responded to and even avoided
the blooms directly, or that some other environmental variable may have played a
role, it is likely that many of these behavioral effects are linked to underlying changes
in resource availability and distribution that in turn influenced individual space use,
activity, and social interaction patterns. A concurrent study of nearshore prey fish
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MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
Table 5. Social network measures for the entire Sarasota Bay resident dolphin community,
juveniles, and adults separately. Values are presented as Mean ± SD [bootstrapped standard
error].
Overall
2004
2005
2006
2007
Juveniles
2004
2005
2006
2007
Adults
2004
2005
2006
2007
n
Strength
129
130
127
174
3.84 ± 1.43 [0.21]
8.47 ± 3.25 [0.68]
4.64 ± 1.98 [0.33]
4.24 ± 1.84 [0.19]
16.76 ± 7.76 [1.95]
82.19 ± 36.90 [13.97]
25.38 ± 12.93 [3.85]
21.35 ± 13.31 [2.04]
34
32
35
39
3.83 ± 1.31 [0.28]
9.14 ± 3.10 [0.90]
4.91 ± 1.55 [0.59]
4.80 ± 1.80 [0.31]
16.65 ± 6.64 [2.34]
90.63 ± 36.55 [17.29]
27.30 ± 9.86 [4.23]
24.89 ± 11.13 [3.19]
60
64
61
86
3.46 ± 1.49 [0.17]
7.95 ± 3.38 [0.63]
4.21 ± 2.10 [0.33]
3.79 ± 1.77 [0.15]
14.70 ± 8.02 [1.57]
75.89 ± 37.18 [12.59]
22.43± 13.30 [3.61]
18.30 ± 12.74 [1.55]
Reach
communities in Sarasota Bay found that abundances of most dolphin prey fish guilds
were reduced by 57% to 88% during the red tides of 2005 and 2006, and in some
habitats top prey were reduced by more than 90% (Gannon et al. 2009). Many of the
changes seen in dolphin behavior during red tide blooms, such as increased ranging
and reduced foraging and group stability, are consistent with the idea that red tides
may primarily affect dolphin behavior through such changes in prey availability
or distribution, which could increase competition for remaining resources among
resident animals in the area during disturbance.
Reduced availability of typical sea grass-associated demersal prey (Barros and
Wells 1998, Gannon et al. 2009) could be a driving force behind the basic changes
we observed in juvenile dolphin activity and ranging patterns during red tides.
Individuals present during these disturbance events ranged farther on both short
(daily) and longer (annual home range) time scales during red tide blooms, indicating
that coastal dolphins may need to expend extra energy looking for resources such as
relatively undisturbed habitats or areas with locally higher prey densities during red
tide events. While individuals may have traveled farther to avoid areas of relatively
poor habitat quality due to high toxin levels, associated changes in activity patterns
highlight that reduced food availability probably played at least some role in their
altered behavior.
Dolphins spent significantly less time actively foraging during red tides, indicating
that reductions in available prey were apparently large enough to change their daily
activity budgets. In addition, dolphins spent significantly more time milling, which
may reflect increased time devoted to searching for rather than catching prey. Previous
studies in Sarasota Bay utilizing an overhead video system have shown that some
observations of milling may actually include foraging behavior, including “search
time,” that boat-based observers cannot detect (Nowacek 2002). Thus, available
surface behavioral indications of foraging are typically more closely related to prey
capture, or “successful” foraging effort by dolphins. Because of this, the reductions
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MARINE MAMMAL SCIENCE, VOL. 27, NO. 3, 2011
Figure 6. Example of home range size expansion associated with HAB disturbance. Annual
95% UD, fixed-kernel home ranges for one focal juvenile female in the study.
in time spent foraging exhibited by dolphins during red tides most likely reflect
decreased ability to find and successfully capture food during these blooms rather
than a true reduction in overall foraging effort. In fact, if the proportion of time spent
milling is added to that spent foraging, juvenile dolphins may have actually increased
their overall foraging effort during red tides to compensate for declines in typical
prey species. More detailed observations of dolphin foraging behavior during K. brevis
blooms, perhaps utilizing techniques such as overhead video, will be necessary to
gain a better understanding of exactly how feeding success is affected by red tides.
While the above changes observed in ranging and activity patterns are consistent
with the possibility of increased competition due to reduced prey availability during
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
637
red tides, many of the social changes observed, such as increased time in groups, larger
group sizes and numbers of associates, and more time spent actively socializing during
disturbance events, seem counter to predictions based on increased competition.
Fission-fusion social systems, such as that exhibited by coastal bottlenose dolphins
in Sarasota Bay, are often thought to allow animals to balance the costs and benefits
of grouping in flexible ways as local conditions change (Lehmann et al. 2007). For
example, when food is abundant or predation risk is high, animals can aggregate
to gain benefits of group living without suffering from the constraints of intragroup competition. However, when resources are scarce, groups may separate to
reduce feeding competition among group members. For example, Lusseau et al.
(2004) found reduced group size in killer whales in the north Pacific and bottlenose
dolphins in the north Atlantic with declines in prey related to climatic oscillations.
In a seeming paradox, we found that dolphin group size and overall gregariousness in
Sarasota Bay significantly increased during severe red tide events, which dramatically
reduced prey availability.
While this result appears counterintuitive at first, a closer look at changes in prey
availability and distribution in Sarasota Bay points toward a possible explanation.
Although severe declines of most common prey species occurred during red tides,
Gannon et al. (2009) found that the abundance of one group of fishes, the clupeids
(a guild of pelagic filter feeders), did not decline in our study area during the bloom
periods, and they suggested that clupeids may become an important component
of the diet of local piscivores, including bottlenose dolphins, during disturbance
events. In contrast to the shallow, predictably dispersed sea grass beds where most
inshore dolphin prey species are found (Barros and Wells 1998), clupeids tend to be
found in larger, more unpredictably located schools in the open, deeper waters of our
study area, and some of the behavioral changes we observed are consistent with the
possibility of a dietary shift towards this guild as other prey species declined.
For example, a shift towards pelagic schooling prey fish could help to explain the
increases in dolphin group size we observed in Sarasota Bay during severe red tide
blooms because more individuals can feed at once on large schools of fish than would
be able to feed together on sea grass-associated species. Dolphins present during
disturbance events may aggregate on these relatively rich, but spatially and temporally less predictable patches of food as would be predicted by socioecological theory
(Wells et al. 1980, Gowans et al. 2008). It is also possible that dolphins present
during red tide disturbances may even gain direct benefits from associating in larger
groups if they can cooperatively herd and catch these schooling prey fish more successfully in large groups than smaller ones. However, more foraging observations
during red tide events are necessary to determine whether cooperative herding becomes a more important component of the foraging repertoire of individuals during
red tides or whether larger groups are more successful at foraging on schooling prey
than smaller ones. Stomach contents from stranded Sarasota Bay resident dolphins
were not available from 2005 to directly assess possible shifts in diets.
Interestingly, a community-wide analysis found that overall dolphin distribution
in Sarasota Bay was both shifted spatially and more tightly concentrated during the
summer of 2005 than surrounding years,1 indicating a possible reduction in the
overall amount of suitable habitat for the resident dolphin community in the study
area or shift in the location of profitable habitats during the most severe red tide
1
Personal communication from Janet Gannon, Department of Biology, Bowdoin College, 6500
College Station, Brunswick, ME 04011, June 2010.
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MARINE MAMMAL SCIENCE, VOL. 27, NO. 3, 2011
event. The only habitat type selected for by dolphins during the severe red tide event
of 2005 was the more open Gulf of Mexico, a habitat-type more likely to contain
schooling clupeids. This finding, coupled with the distributional shifts noted above,
may further indicate the possibility of a dietary shift away from decimated demersal
species and toward the still abundant schooling pelagic prey that was suggested by
Gannon et al. (2009).
Dolphins aggregating on remaining schooling prey patches could also provide an
explanation for the overall tighter, more connected social network seen in Sarasota
Bay during the severe red tide of 2005. Individuals who might not normally come in
contact with each other during non-red tide periods, when dolphins typically forage
alone or in small groups in shallow sea grass beds and sand flats, would be more
likely to encounter one another in larger groups foraging on large schools of clupeids
in deeper waters, increasing the number of connections between individuals in the
community. Thus, as changes in prey availability and distribution likely altered
dolphin grouping patterns, this shift could also have been responsible for the other
changes in sociality that we observed during red tide, including decreased time spent
alone, increased numbers of associates, and increased direct and indirect connectivity
amongst the entire Sarasota Bay dolphin community.
As juvenile dolphins associated in larger groups, bringing them into contact with a
wide variety of individuals and presumably some novel associates, they increased their
amount of time spent actively socializing relative to nondisturbance periods. Increases
in time spent socializing or playing are typically noted during times of plenty rather
than scarcity, as has been documented in semi-provisioned baboons (Papio cynocephalus)
(Altmann and Muruthi 1988) and lemurs (Trachypithecus leucocephalus) in high quality
habitats (Li and Rogers 2004). However, a disturbance-related dietary shift toward
schooling prey that may have brought individuals together in larger numbers would
also be likely to promote indirectly the socialization of young animals that are
recently independent of their mothers and still learning about other community
members and developing relationships. Because behavioral observations were only
conducted on juvenile animals during this time period, we do not know whether
adults also spent more time socializing during red tide blooms, but it is likely that
this effect would be stronger for young animals that typically socialize at higher rates
than adults (McHugh 2010).
Most other changes in sociality appear to be widespread across the Sarasota Bay
community. Increases in average group size found for juveniles mirror what has been
seen in the overall Sarasota Bay community. This finding coupled with the changes
we found in the Sarasota Bay dolphin social network during red tides appear to be
indicative of a pervasive effect of red tides on the resident dolphin community, rather
than an impact specific to young animals.
On a methodological note, we found that the type of data collection (focal follows
vs. photographic identification surveys) affected measures of group size, such that
group size measures from follows were smaller than those from survey data. While
this finding makes sense due to the difficulty of focusing on an individual’s behavior
as group size increases, it highlights the importance of accounting for the method
of data collection in interpreting findings and comparing across time periods and
study sites. Thus, it may be important to use information from different sources to
get a complete picture of the behavioral changes that accompany disturbance and
keep in mind which sources are being used if results are applied to management
efforts.
MCHUGH ET AL.: RED TIDE INFLUENCES DOLPHIN BEHAVIOR
639
Conclusions
In summary, dolphins during red tide events were more gregarious, spending
less time alone, associating in larger, less stable groups, and interacting with more
associates than nondisturbance periods. This shift in sociality meant that juveniles
interacted with significantly more individuals during the severe red tide than during
other periods, a pattern that was consistent for the entire Sarasota Bay community as
seen from social network metrics. These changes in sociality are particularly striking
given that the individuals present during the disturbance events appear to have
had more difficulty locating and capturing food than during nondisturbance events,
which would presumably increase competition for the few prey resources remaining
in the area. Because of this, we feel that some underlying change in resource use
to compensate for reductions in typical prey species, such as a possible dietary shift
towards remaining schooling prey fish, may be a logical driving factor behind the
altered behavior patterns observed during red tides. However, we have not yet been
able to directly test this idea, or had an opportunity to observe whether or not similar
behavioral changes may occur during milder disturbances where prey availability is
not as severely impacted.
Importantly, these changes in sociality also have implications for potential synergistic effects during similar disturbances in the future. While there was no evidence
that any resident dolphins died from brevetoxicosis during the severe red tide of
2005, mortality and morbidity of resident dolphins is a potential concern during
disturbance events. For example, increased connections among greater numbers of
individuals may make coastal dolphins more susceptible to disease outbreaks during
red tide events, as transmission both through the resident community and from individuals of neighboring communities would be more likely. Brevetoxins are known
to impact immune function (Pierce and Henry 2008), and exposure to these toxins
both through respiratory inhalation and via food web transfer when individuals may
already be nutritionally compromised could also make them more susceptible to
disease during red tide blooms. Also, new and more frequent social interactions and
reduced prey may increase stress, which also could affect immune function during
K. brevis blooms. Thus, behavioral changes associated with red tide may compound
physiological changes associated with brevetoxin exposure and lead to dramatically
increased chances of widespread disease outbreaks among dolphin populations during
red tide blooms, which would have the potential to contribute to unusual mortality
events during HABs.
Despite increasing evidence that bottlenose dolphins in Sarasota Bay are impacted
by red tides occurring periodically in their coastal habitat, resident individuals have
not abandoned the community range during even the most severe events. This
suggests that they are currently either able to cope with these disturbances by
altering their behavior to compensate for changes in local conditions or that they are
restricted to the area in and around Sarasota Bay, perhaps by social factors relating to
long-established neighboring communities of dolphins that may prevent them from
moving elsewhere. We have documented that short-term (weeks to months) changes
in local conditions associated with red tide disturbances have significant effects on
behavior patterns and social dynamics of resident coastal dolphins in terms of altered
ranging, activity, and social behavior, perhaps as individuals try to compensate for
changes in resource availability and habitat quality within their multi-generational
range. Whether these behavioral shifts would be sufficient to allow resident dolphins
to cope with disturbance across a larger temporal or spatial scale, or if natural
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MARINE MAMMAL SCIENCE, VOL. 27, NO. 3, 2011
disturbance regimes were to be altered by climate change or human activities, is
yet to be seen. However, it is likely that changes in social dynamics during red tide
blooms could exacerbate long-term disturbance to coastal dolphin populations by
increasing exposure and susceptibility to novel or invading pathogens.
ACKNOWLEDGMENTS
We would like to thank Lynne Isbell, Pete Klimley, and three anonymous reviewers for
helpful comments on this manuscript as well as our field assistants and Sarasota Dolphin
Research Program lab members whose assistance has been invaluable. Funding for this work
was provided by the Animal Behavior Society’s Cetacean Behavior and Conservation Award,
NOAA Fisheries, the Chicago Zoological Society, an NSF Graduate Research Fellowship, and
UC Davis. The research was conducted under NMFS Scientific Research Permit No. 522-1785
issued to RSW and approved by the Institutional Animal Care and Use Committees of the
University of California Davis and Mote Marine Laboratory.
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Received: 5 April 2010
Accepted: 17 July 2010