Exodus! Large-scale displacement and social adjustments of resident Atlantic spotted dolphins (Stenella frontalis) in the Bahamas
Exodus! Large-scale displacement and social adjustments of resident Atlantic spotted dolphins (Stenella frontalis) in the Bahamas
Denise L. Herzing 0 1
Bethany N. Augliere 0 1
Cindy R. Elliser 0 1
Michelle L. Green 0 1
Adam A. Pack 1 2
0 Wild Dolphin Project, Jupiter, Florida, United States of America, 2 Department of Biological Sciences, Florida Atlantic University , Boca Raton , Florida, United States of America, 3 Pacific Mammal Research, Anacortes, Washington, United States of America, 4 Department of Animal Science and Illinois Natural History Survey, University of Illinois at Urbana-Champaign , Urbana, Illinois , United States of America
1 Editor: Ulrike Gertrud Munderloh, University of Minnesota , UNITED STATES
2 Departments of Psychology and Biology, University of Hawaii at Hilo, Hilo, Hawaii, United States of America, 6 The Dolphin Institute , Hilo, Hawaii , United States of America
Over the last 20 years, significant habitat shifts have been documented in some populations of cetaceans. On Little Bahama Bank (LBB) there are sympatric communities of resident Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus), monitored since 1985. The size and social structure (three clusters: Northern, Central, Southern) have been stable among the spotted dolphin community with little immigration/ emigration, even after large demographic losses (36%) following two major hurricanes in 2004. In 2013 an unprecedented exodus of over 50% (52 individuals) of the spotted dolphin community was documented. The entire Central cluster and a few Northern and Southern individuals relocated 161 km south to Great Bahama Bank (GBB), also home to two sympatric resident communities of spotted dolphins and bottlenose dolphins. During the late summer of 2013 and the summers of 2014 and 2015 both sites were regularly monitored but no former LBB dolphins returned to LBB. Uncharacteristic matriline splits were observed. Social analyses revealed random associations for those spotted dolphins and very little integration between spotted dolphins that moved to GBB (MGBB) and those dolphin resident to GBB (RGBB). Male alliances among spotted dolphins were present, with some altered patterns. On LBB, the operational sex ratio (OSR) was reduced (.40 to .25). OSR for MGBB and RGBB dolphins were similar (.45 and .43). A significant steady decrease in sea surface temperature and chlorophyll a (a proxy for plankton production) occurred on LBB leading up to this exodus. Similar trends were not present over the same period on GBB. The sudden large-scale shift of spotted dolphins from LBB to GBB in association with the gradual decline in certain environmental factors suggests that a possible ªtipping pointº was reached in prey availability. This study provides a unique view into social and genetic implications of largescale displacement of stable dolphin communities.
Data Availability Statement: All relevant data are
within the paper and its Supporting Information
Funding: All the funding received during this
specific study include: The Marisla Foundation, The
Coypu Foundation, and The W. Bradford Ingalls
Foundation. The funders had no role in study
design, data collection and analysis, decision to
publish, or preparation of the manuscript. No
authors received a salary from any of these
Emigration and immigration patterns can greatly influence the origin and structure of social
groups [1±2] as well as effect changes to previously stable groups, e.g. [
]. Very little is known
about the effects of large-scale emigration events in social animals involving stable social
clusters of individuals, where researchers have knowledge and long-term tracking of both the
population from which immigrants arise and the population into which they join. Usually
immigration events are at the individual, or small group level, where the association choices
made by resident individuals can strongly affect the acceptance of immigrants into the
], ultimately affecting the grouping patterns and social structure . Research on
immigration events, whether large- or small-scale can be challenging due to the logistics involved
in following individuals [
] and the fact that even for well-studied species immigration events
are often rare [
]. This is particularly true for many cetacean species in which individuals
typically spend most of their time underwater making them often difficult to track, and where
some individuals (usually males) from distinct communities may pay occasional short-term
visits to adjacent communities for purposes of mating and not immigration. Here, we describe
the large scale and relatively rapid emigration of more than 50% of the community of
longterm resident Atlantic spotted dolphins (Stenella frontalis) from Little Bahama Bank (LBB) to
Great Bahama Bank (GBB) where another community of Atlantic spotted dolphins is resident.
The Wild Dolphin Project (WDP) has a unique long-term dataset with over 30 years of data
for two sympatric communities of Atlantic spotted dolphins (Stenella frontalis) and bottlenose
dolphins (Tursiops truncatus) on the northwestern edge of LBB. Data on Atlantic spotted
dolphins includes life history and reproduction [
], correlations with sound and behavior [7±9],
ultrasonic vocalizations [
], long-term community and social structure [11±12] nocturnal
], changes in social structure [
] and genetics [15±16]. The social structure of
the resident community of bottlenose dolphins has also been documented over the decades
Since 1991, annual immigration rates into the community of Atlantic spotted dolphins on
LBB were low, with new births accounting for the majority of increases in the population [
The community was comprised of roughly 100 individuals in any given year prior to 2004,
when two hurricanes struck the study area. Thirty six percent of the community was lost after
these strong (category two and three) hurricanes [
] and these individuals have not been
resighted to date. Following the hurricanes, approximately 67 community members remained.
The population increased steadily thereafter and by late 2012 had nearly recovered to 85
individuals. Immigration after the hurricanes remained low (2005±2007: 2 noncalf individuals per
year), consistent with pre-hurricane immigration (pre-hurricane 2002±2004: 2.3 noncalf
]. This remained consistent in the following years (see results), indicating that the
increase back to near normal numbers by 2012 was mainly due to births, not immigration into
Following demographic upheaval after hurricane disturbance in 2004, differing social
structure changes also occurred on LBB between the two closely related sympatric species of
resident Atlantic spotted dolphins and bottlenose dolphins [
]. The long-term interspecies
interactions of these two stable communities of dolphins have been documented [19±21],
along with changes following the hurricanes .
Over the decades, and through the demographic upheaval of the two hurricanes mentioned
earlier, three distinct and stable clusters (Northern, Central, and Southern) have been
documented in the spotted dolphin community on LBB through genetics [
], social association
data [11±12,14], and GIS distribution and home range analysis [
]. From 1985±2012 (28
2 / 32
years) both the communities of sympatric spotted and bottlenose dolphins on LBB have been
resident to the area, showing strong site fidelity.
Data have also been collected in both winter (1998 through the winter of 2004) and summer
months, on the resident communities of Atlantic spotted and bottlenose dolphins on GBB
located approximately 50 km south of LBB. During this time, no photo identification matches
were made between LBB and GBB spotted dolphins. Although consistent yearly data is
unavailable for GBB, photographic evidence of site fidelity exists (see results).
Sometime between Sept 12, 2012 and May 28, 2013 (between summer field seasons), a
major shift in the distribution of spotted dolphins occurred on LBB. The Central cluster of
LBB spotted dolphins (45 dolphins) and 5 individuals from the Northern and 2 from the
Southern clusters were found on GBB, and have remained there through the 2015 field season. In
theory, this unprecedented shift can have large implications on the social and genetic structure
of the larger population.
The large scale emigration/immigration that occurred between the two dolphin
communities in this study provides a unique view into the social and genetic implications of a long-term
stable social cluster from one community moving into an established community on another
sandbank, and how the original community fairs after their exodus (with no subsequent
immigration into that community). This paper discusses the preliminary observations, the social
and genetic implications of this unprecedented emigration on these two sympatric
communities, and the possible factors that may have contributed to the large-scale movement.
Materials and methods
Little Bahama Bank (LBB). LBB is north of Grand Bahama Island and 64 km from the
east coast of Florida (Fig 1). The sandbank is shallow, between 6±16 m deep and surrounded
by deep water (steep drop off to over 500m into the Gulf Stream), and encompasses 480km2
(spanning 60 km north to south and 8km east to west).
Great Bahama Bank (GBB). GBB is south of LBB from the southern end of Grand
Bahama Island across deep water approximately 50 km to the beginning of the northern
sandbank of GBB. This sandbank is larger than LBB, and encompassed twice the search area,
960km2 (Fig 1). The western edge of this sandbank is similar to LBB, with depths between
616m deep with deep water and a steep drop off to over 500m into the Gulf Stream on the
Data have been collected on the community of dolphins on LBB since 1985; the dolphins are
habituated to the presence of boats and people in the water. Data were collected from May to
September each year (average 80±100 d/yr) in all but rough weather conditions (over Beaufort
3 and/or intense rain squalls) from 0700 to 2000 in shifts of one person/one hour or 2 persons/
two hours. Observers scanned an arc of 180Ê while underway and 360Ê while anchored. Past
field effort on LBB (including number of days at sea, encounters, days with encounters, total
hours and percent of time underway/anchored) for 1991±2002 can be found in [
], and for
2002±2007 in [
Data have also been collected (following the same protocol stated above for LBB) on the
community of dolphins on GBB prior to the exodus (summer of 1998: 13 encounters, and the
winters of 1999: 13 encounters, 2000: 18 encounters, 2001: 13 encounters, 2002: 4 encounters,
and 2003: 13 encounters). Adjusted effort between LBB and GBB occurred since the summer
of 2013 when over 50% of the long-term resident spotted dolphins on LBB were noted as
3 / 32
Fig 1. Map of the study area in the northern Bahamas. Little Bahama Bank (LBB) and Great Bahama
Bank (GBB) in the northern Bahamas. Land masses (Grand Bahama Island±LBB) and Bimini±GBB) are in
solid colors and are south of shaded areas. Oceanographic data was collected from dark shaded boxes that
represent areas on the sandbank (shallow water), and lightly shaded boxes represent areas off the sandbank
(adjacent deep water) for both LBB and GBB.
missing from LBB. After surveys on LBB and the adjacent GBB, it was determined that these
previously resident LBB individuals (primarily the Central cluster) moved to GBB. Survey time
was split between these two sandbanks for the years of 2013±2015 summer field seasons.
Data collectionÐIndividual, group, and community identification
Atlantic spotted dolphins have four developmental color phases described by [
] for the
pantropical spotted dolphin (Stenella attenuata) and adapted for Atlantic spotted dolphins by [
The four age classes include: two-tones (calves, 4 yr), speckled (juveniles, 4±9 yr), mottled
(young adult, 10±16 yr) and fused (adult, 16 yr). Every individual was assigned to an age
class and these data were updated each year. Individual identification was accomplished using
4 / 32
LBB Total #encounters
LBB Total duration
GBB Total #encounters
GBB total duration
spotting patterns along with additional marks such as nicks and scars on the dorsal fin, flukes,
pectoral fins and marks or scars on the body. Males were sexed by a gap between the genital
slit and the anus, or observation of an erection. Females were sexed by observation of
mammary slits or observation of nursing by a calf. Sex was determined for 98.5% of the LBB
community, and 83.6% for GBB, and verified multiple times for all individuals seen more than
A group was defined as all dolphins in sight, moving in the same direction and typically
involved in the same activity [
]. An encounter was defined as a group of dolphin observable
underwater for more than 2±3 min [
]. The final group size/identified individuals were a
product of in-water identification and photo-identification afterwards. Encounter methods
including group size and individual ID followed the same methods described in [11±12].
For basic group analysis Atlantic spotted dolphins were categorized according not only to
their location (LBB or GBB) but according to their Community ID as follows: LBB dolphins
found on LBB, LBB dolphins found on GBB, GBB dolphins on GBB, LBB/GBB dolphins
together on GBB. Bottlenose dolphins were categorized as single species in two locations (BN
on LBB, BN on GBB) or as a bottlenose/spotted mixed group in the two locations (Mixed on
LBB, Mixed on GBB).
For social analyses individual spotted dolphins were labeled as those resident/remaining on
LBB after the displacement (RLBB), those resident to GBB (RGBB), and those that moved
from LBB to GBB (MGBB).
This research was done under a permit issued by the Department of Fisheries in Nassau
Bahamas. All research was observational and no samples were collected or experimental
manipulation occurred during this study.
Social structure analysis
Coefficients of association (CoAs) were calculated using the half-weight index [
] with the
software program SOCPROG 2.5 . Data were pooled into 3 year groupings: 1. 2007±2009
(a follow up after the before/after hurricanes analyses [
] to determine whether any further
changes occurred, or remained stable), 2. 2010±2012 (three years prior to the displacement
event and 3. 2013±2015 (3 years after the displacement event). An individual spotted dolphin
was placed in the age class category that they were in for the majority of the pooled time frame
(i.e. two or more years).
CoAs were determined for pairs of noncalf individuals of known sex sighted at least six
times per pooled period (this is consistent with previous work [
]). Calves were not included
due to their associations being dependent on their mother. Strong associations were defined as
greater than twice the average CoA of the study group [29±30].
To test the null hypothesis that individuals associate at random, permutation tests were
conducted in SOCPROG by permuting individuals into groups, using 100 flips per iteration,
5 / 32
within sampling periods of one day . We tested for between-sampling period association
preference/avoidance by comparing the Standard Deviation (SD) of the observed half-weight
index matrix with the SD expected by chance, i.e. calculated for a total of 10,000 permuted
matrices (which was enough permutation to stabilize the P-value). The P-value was calculated
as the number of times the SD from the permuted data was less than the observed SD. We
rejected the null hypothesis when the SD of the observed half-weight indices were higher than
the permuted SD. This means there was more variation in the real indices than expected by
chance, i.e. higher and lower CoAs which can be interpreted as preferred and avoided
associations, respectively . For nonrandom associations, Mantel tests were conducted to examine
whether differences in association occur between classes (e.g. sex, age class, cluster, residency,
The correlation coefficient (CC) between the true and calculated association indices [30±
31] was used to infer on the reliability of the results and if the data was a reliable representation
of the social system. The statistical power of the permutation test was estimated with the Social
differentiation (S, a measure of the variability of the associations where 0 is homogenous and
over 1 indicates considerable diversity) and the mean number of observed associations per
individual (H), giving that S2xH>5 suggests sufficient power . The precision (Standard
Errors, SE) of the estimate of the Social Differentiation and CC was estimated with bootstrap
techniques (100 replications).
Non-parametric multidimensional scaling (nMDS) and hierarchical agglomerative cluster
analyses were used to investigate cluster stability/changes on LBB and GBB. In nMDS plots
individuals strongly associated will be plotted together, and weakly associated farther apart
. The stress of the nMDS indicates how representative the 2D plot is of the data, with lower
stress values indicating a better representation. The number of dimensions was increased until
the stress fell below 0.10, and the starting position was set to random. A network diagram was
drawn based on this nMDS plot arrangement in which nodes representing individuals are
connected by links, whose thickness indicate their CoA values. The average-linkage method was
used for the hierarchical cluster analysis and produced a dendogram where individuals are on
one axis and their CoA on another  and a cophenetic correlation coefficient (which is a
measure of how well the dendogram matches the matrix of association indices) of > 0.80
indicates a good match to the association matrix .
Breeding population size. To calculate breeding population size of the original LBB
community, we estimated the age of animals during each of the three time periods used for social
structure analysis (2007±2009, 2010±2012, 2013±2015). Ages were estimated through a
combination of observational data and generalized age-class ranges. Because Atlantic spotted
dolphins gain spots as they age, age estimates can be made based on the spotting and color
patterns of individuals. In this study, age ranges were based on identified age class at the time
they were first observed in the field.
Females typically achieve first parturition during the mottled age class [
]. The exact age
at which males reach sexual maturity is unknown in this species, therefore, we first assumed
that males reach sexual maturity at the same age as females. We considered all animals in the
mottled and fused age classes as contributors to the breeding population, regardless of other
factors (i.e., sex or proof of reproductive success). We considered the estimate including all
mottled animals to be non-conservative because it may include more animals, specifically
males, that have not actually contributed offspring to the population and may result in an
overestimate of the breeding population. Previous paternity analysis indicated that males may not
successfully breed until they reach the fused age class [
]. Therefore, we used a more
conservative approach that was less likely to overestimate the breeding population size by excluding
mottled males as contributors to the breeding population. The operational sex ratio (OSR) was
6 / 32
calculated as the proportion of breeding males out of all breeding males and females. We tested
whether the OSR was different from an expectation of equal sexes using chi-square analysis.
The exodus of such a large proportion of a breeding group may have serious implications for
the genetic health of the remaining population. To better understand whether the remaining
individuals were at an increased risk of inbreeding, we determined whether the mean
relatedness among the remaining individuals decreased with the loss of animals to another location
and compared it to the mean relatedness of the original group and the animals that relocated.
We used microsatellite genotypes generated from previous work [
] to determine
coefficients of relatedness (r-values) among pairs of individuals using RELATEDNESS v. 5.0.8
]. Values range from -1±1 with negative values indicating that relatedness between two
individuals is less than expected between individuals chosen at random and positive values
indicate some degree of relatedness. When generating relatedness values prior to the move, the
known maternal relatives were removed to reduce bias and estimates were jackknifed over loci
to generate standard errors. After the move we generated relatedness values both with and
without maternal relatives in the analysis to assess the impact of the reduction in sample size.
Allele frequencies were generated using residency groupings for the three different time
periods. Pairwise r-values were estimated for all pairs of individuals with genotype data.
Average r-values within families, clusters and resident groups were estimated including all
individuals except in cases of known maternal relatives that were excluded from the calculation.
Habitat and oceanographic dataÐInterannual trends
To examine and compare trends in sea surface temperatures (ÊC), productivity as estimated
with surface chlorophyll a concentrations (mg m-3), and surface scalar wind speeds (m s-1)
between LBB and GBB in the northern Bahamas, we used data and time-series analytical
tools from the Interactive Time-series Explorer toolkit of the Coastal and Oceanic Plankton
Ecology, Production and Observation Database, COPEPOD http://www.st.nmfs.noaa.gov/
] (Fig 2). COPEPOD is a global database of plankton survey data, supporting data
products, and time series data extraction and exploration tools [35±36] hosted by the National
Marine Fisheries Service of the U.S. National Oceanic and Atmospheric Administration.
Because contiguous phytoplankton, zooplankton, and in situ chlorophyll data were not
available for either LBB or GBB, we used satellite surface chlorophyll a concentrations at LBB
and GBB as a proxy for lower tropic level food availability in these areas. Chlorophyll is a
rough indicator of phytoplankton concentration, and thus food available to the zooplankton
and upper trophic levels (e.g., fish, sea birds, and marine mammals).
Using the geographic coordinates for the LBB and GBB sub-areas (Fig 1), we used
COPEPOD's time series toolkit (http://www.st.nmfs.noaa.gov/copepodite/toolkit) to extract and
generate spatially-averaged time series of sea surface temperature (from NOAA's Optimum
Interpolation Sea Surface Temperature data set, OISST version 2, https://www.ncdc.noaa.gov/
oisst), satellite-based surface chlorophyll a concentration (from NASA's SeaWiFS/MODIS-A
data set, https://oceandata.sci.gsfc.nasa.gov), and surface wind speed (from the International
Comprehensive Ocean-Atmosphere Data Set, ICOADS release 2.5, https://rda.ucar.edu/
datasets/ds540.0). All of the time-series in our analysis were truncated to start in 1998, as this
is the first year that SeaWiFS satellite chlorophyll data were available for LBB and GBB.
Seasonally corrected annual anomalies of sea surface temperature and chlorophyll data
from 1998±2015, and of surface wind speed from 1998±2014 (the last year data were available)
were calculated for the LBB and GBB areas using the COPEPOD toolkit. This calculation
7 / 32
Fig 2. COPEPOD data for the Bahamas. Data includes Satellite Chlorophyll, Sea Surface Temperature, and Scalar Surface winds on Little Bahama Bank
(LBB)±left panels) and Great Bahama Bank (GBB- right panels).
method is described in [
], with additional documentation also available online at http://
Interannual seasonally corrected annual anomalies in sea surface temperature, chlorophyll
data and surface wind speed were analyzed from 1998±2012, to examine trends through the
final year the 52 spotted dolphins involved in the move to GBB were sighted on LBB.
Separately, interannual seasonally corrected annual anomalies in sea surface temperature and
chlorophyll data were analyzed from 2013 to 2015 to examine for trends from the first year the 52
spotted dolphins involved in the move to GBB were sighted on GBB. However, a similar
analysis on annual anomalies in wind speed was not conducted as these data were only available
Inasmuch as many spotted dolphins feed both on the sandbank and also off the deep water
(300m) edge of the bank (in evening hours), we also conducted a microanalysis of seasonally
corrected annual anomalies of sea surface temperature, chlorophyll data and surface wind
speed both on the shallow sandbank and off adjacent deep waters of the sandbank (see Fig 2)
for both LBB and GBB for those factors found to have significant overall trends in LBB and
Between Fall 2012 and Spring 2013, a total of 52 spotted dolphins (25 males = 15 adults 5
juveniles, 5 calves and 27 females = 16 adults, 8 juveniles, 3 calves) that had been resident (in three
8 / 32
SP = spotted dolphins; BN = bottlenose dolphins; Mixed = bottlenose and spotted dolphins.
LBB = Little Bahama Bank; GBB = Great Bahama Bank.
distinct clusters) on LBB up to the Fall of 2012, moved to GBB. We compared changes in their
group size and describe the interactions between the displaced dolphins and resident dolphins
Encounters and group size on LBB and GBB
The number of encounters varied across years and locations of both Atlantic spotted dolphins
and bottlenose dolphins (Table 2). Effort to survey in both study sites over the years was
successful, although the number of encounters varied between location and species.
Mean group size changed over the years in the different locations by different Community
ID (Table 3). Mean group size of LBB dolphins on LBB remained similar over the three-year
period (Kruskal-Wallis H = 0.21675, df = 2, p = 0.89729). Although mean group size for LBB
dolphins on GBB decreased over the three-year period the decrease was not significant
(Kruskal-Wallis H = 4.48571, df = 2, p = 0.10615). Mean group size for LBB/GBB dolphins on GBB
was also not significantly different across the three-year period (Kruskal-Wallis H = 0.39125,
df = 2, p = 0.82232). There was no significant difference in group size for Community ID across
2013 (Kruskal-Wallis H = 2.5, df = 2, p = 0.28650) or across 2015 (Kruskal-Wallis H = 3.8044,
df = 2, p = 0.14924) but there was a significant in 2014 across Community IDs (Kruskal-Wallis
H- 6.69082, df = 2, p = 0.03525).
Site fidelity on GBB
Site fidelity was documented on GBB with at least two dolphins over at least a four-year period,
Salinger (adult male±observed 1998±2003) and Picard (juvenile female± 2000±2003) both
resighted in the summer of 2013 by WDP on GBB. This suggests that there is site fidelity and
residency of at least some (and likely more) spotted dolphins on GBB over the decades (Fig 3).
Cluster changes on LBB
After the 2015 season, tallies of displaced dolphins included not only the entire Central cluster
(45 individuals) but also 5 individuals from the Northern and 2 from the Southern cluster. A
Mean (SD) group size for spotted dolphins by location (Little Bahama Bank±LBB, Great Bahama Bank±GBB) and Community ID (LBB dolphins on LBB,
GBB, or LBB/GBB mixed species on GBB).
9 / 32
Fig 3. Identification of two spotted dolphins on GBB over a decade. Top: Female Atlantic spotted
dolphin Picard with a distinct insignia mark, in 2000 as a juvenile on Great Bahama Bank (GBB) and again in
2013 as a young adult mottled on GBB. Black arrows denote dorsal fin mark and nick in tip of fin. Bottom: Male
adult fused Atlantic spotted dolphin, Salinger, with distinctive fluke, taken on GBB in 1998 and again in 2013
on GBB. Photo credit: Wild Dolphin Project.
few unusual disruptions to matrilineal relationships from the Northern and Southern clusters
were also noted.
Northern cluster±A total of 5 individuals moved to GBB from LBB. One young adult female
(Burgundy) moved to GBB while her mother and multiple siblings remained on LBB (Brush/
Palette, Brat) and one adult female (Tyler) moved to Bimini leaving her female juvenile
offspring (Tristan). One adult male (Liney) and 2 young adult males (Picasso and Sunami) also
moved to GBB. Central clusterÐall 45 individuals (37 non-calves, 8 calves) moved to GBB
from LBB. Southern clusterÐOne juvenile male (Infinite) moved to GBB while her mother
remained on LBB, and one juvenile female (Marble-matriline unknown) moved to GBB from
Reproduction and health
Of the LBB spotted dolphins that migrated to GBB, average pregnancy rates and calving rates
have remained within normal ranges (1±10 calves/yr, [
]) and are as follows: (2013:11 calves,
2014: 8 calves 2015: 1 calf). Based on our observations of body characteristics, the physical
health of the dolphins appeared uncompromised (e.g., no dolphin appeared emaciated).
Social structure results
The total number of encounters, spotted dolphin individuals (male/females) and CoA statistics
(including mean, SD, CV, S, CC, H, S2xH and P value) for all pooled years are given in Tables
4 and 5. Due to the different locations after the displacement, the 2013±2015 data are split
into two datasets (GBB vs. LBB). For all these datasets the statistical power to reject the null
10 / 32
Social differentiation (S) + Standard Error (SE), Number of associations per individual (H), Correlation Coefficient (CC) +SE. S>0.50 high social
differentiation, CC>0.80 good representation, S2xH >5 good ability to reject null hypothesis of no preferred companions.
* Data from post-hurricane years (2005±2007) is given for reference from [
hypothesis of no preferred companions was good with S2xH > 5. The correlation coefficient
(CC) was close to or above the 0.80 criterion of a good representation. This indicates the data
are reliable and a good representation of the true social system (Table 4).
Social structure 2007±2009. The annual immigration rate remained low at 4.3 noncalf
individuals per year. Permutation tests revealed nonrandom associations (SD and CV Table 5
p <0.001). The results were consistent with the post-hurricane years [
]: the mean CoA was
similar as well as the social differentiation remaining lower (Tables 4 and 5) and Mantel tests
(Table 6) found within class CoA to be higher than between class CoA for cluster (t = 5.05,
r = 0.36, p < 0.001) and sex (t = 6.68, r = 0.16, p< 0.001). Within class CoA for age class were
found to be higher than between (Table 6, t = 2.63, r = 0.12, p = 0.01) which was not found
post-hurricane (although when broken down by sex, there were still some differences in CoAs
in relation to age [
]). Social differentiation by cluster was low (Central, 38 individuals: S =
0.29 ± 0.05; Southern, 6 individuals: S = 0.00 ± 0.16; Northern, 7 individuals: S = 0.22 ± 0.09)
Social structure 2010±2012. The annual immigration rate remained low at 1 non-calf
individual per year. Permutation tests revealed nonrandom associations (SD and CV Table 5
p = 0.0001). The mean CoA was similar to 2007±2009, however social differentiation
increased, edging closer to what was seen pre-hurricane [
]. Mantel tests (Table 6) found within
class CoA to be higher than between class CoA for cluster (t = 10.85, r = 0.56, p = 0.0), sex
(t = 3.36, r = 0.10, p = 0.01), and slightly significantly higher for age class (t = 1.93, r = 0.09,
p = 0.04). Social differentiation by cluster was low (Central, 37 individuals: S = 0.30 ± 0.05;
Southern, 13 individuals: S = 0.34 ± 0.13; Northern, 7 individuals: S = 0.14 ± 0.10).
Social structure 2013±2015 on LBB. Annual immigration rates remained low at 1.3
noncalf individuals per year. Permutation tests revealed random associations (SD and CV Table 5
p >0.35). The mean CoA increased compared to previous years (Table 5) and social
differentiation remained near 2010±2012 levels (Table 4).
Number of encounters (Enc), number of individuals (M = male, F = female), CoA statistics: Mean, Standard Deviation (SD) and Coefficient of Variation (CV)
from permutation tests. SD and CV (real) significantly higher than random = nonrandom associations (in bold).
* Data from post-hurricane years (2005±2007) is given for reference from [
11 / 32
Social structure 2013±2015 on GBB. Annual immigration rates are unknown for GBB
location. Permutation tests revealed nonrandom associations (SD and CV Table 5 p <0.001).
The mean CoA was lowest and social differentiation was highest and closest to that seen in
long-term pre-hurricane analyses on LBB [
]. Social differentiation for just MGBB dolphins
(there was no difference between clusters, CoA 0.34 vs. 0.29 t = 1.33, r = 0.10, p = 0.11) revealed
homogenous associations (S = 0.00 ± 0.14), whereas RGBB dolphins had low differentiation
(S = 0.27 ± 0.12). For all dolphins on GBB Table 6 shows Mantel tests found within class CoA
to be higher than between class CoA for residency (MGBB vs. RGBB) (t = 29.80, r = 0.67, P =
0.00), sex (t = 2.39, r = 0.05, p = 0.03), and age (t = 4.34, r = 0.10, p = 0.002). Fig 4 (S1 Fig) and
Fig 5 (S2 Fig) show a cluster dendogram and network diagram (based on nMDS plot)
respectively, that support the Mantel results concerning residency and the extreme separation
between the MGBB dolphins and those RGBB dolphins. In the network diagram there seem to
be three individuals (Zion (female), Lord and Duke (males)) that appear to link the two
clusters, and in the cluster dendogram, two of these RGBB animals (Lord and Duke) are actually
clustered with the MGBB animals.
Social structure male alliances. The presence of adult (mottled or fused) male spotted
dolphins remaining on LBB after 2012 was greatly reduced from 28 to only five; 15 moved
Fig 4. Cluster dendogram for GBB 2013±2015. Average linkage method, CCC = 0.83, modularity 0.34.
RGBB (resident to GBB), MGBB (moved to GBB). *Lord and Duke are RGBB animals that have been
grouped with the MGBB in the cluster diagram, but are grouped with RGBB animals in the network diagram.
12 / 32
Fig 5. Network diagram for GBB 2013±2015. Based on nMDS plot (4 dimensions, stress = 0.097). Legend
indicates CoA values for line strength: 0.17 overall mean, 0.34 twice the overall mean (strong associations),
0.51 (three times the overall mean). * indicates two RGBB animals that are grouped with RGBB here
(although on edge of cluster), but have a lot of links to MGBB cluster, and were grouped with MGBB in cluster
to GBB and eight have been lost (not seen anywhere since 2012). It should be noted that the
number of males remaining in the alliance analysis is less than the actual number of males
physically remaining in the respective communities because of the requirement of 6
sightings per individual. Most males in the area (Central cluster) moved to GBB. Very few males
were left on LBB, and only two of these males had enough sightings to be included in analyses.
These two were adult immigrants (in 2009) and had a CoA of 0.95, much higher than twice
the 0.33 overall mean; however the overall associations were found to be random, so care
should be taken in assigning this as an alliance. No alliances that were on LBB prior to the
move remained on LBB.
After the immigration event, alliances between male spotted dolphins on GBB were
observed, but there were no strong associations between MGBB and RGBB males. Indeed,
there was little observed integration between the MGBB and RGBB spotted dolphins.
Therefore, CoA levels for male alliances were not based on the overall male-male mean, as it would
have been artificially low due to their low interaction, not actually preferred avoidance of
specific males. Thus an alliance was defined as twice the mean for each cluster (MGBB male-male
mean = 0.37, RGBB male-male mean = 0.28). Using this modified metric, MGBB had four
alliances and RGBB had three alliances.
Two of the four MGBB alliances were previously known LBB alliances that survived the
move, with slight changes. Linus, Kai and Lhasa were a speckled trio that formed after the
2004 hurricanes on LBB, with Kai and Lhasa the primary pair. On GBB, Kai and Malibu (who
was previously in a different alliance and whose partner was subsequently lost), were now the
primary pair (CoA = 0.82). Linus, Kai and Lhasa had a very strong association with each other
(CoA 0.74±0.76) and Linus and Lhasa have less strong associations with Malibu (CoA 0.60±
0.67), making it difficult to determine the exact structure of their alliance. They are now all
mottled/fused individuals. Sunami and Picasso were another pair that formed on LBB after the
13 / 32
hurricanes (both speckled at the time). On GBB Picasso and Finesse (no known previous
alliance) are now the primary pair (CoA = 0.73, just below the 0.74 cut off) with Sunami a possible
third member (CoA = 0.62±0.67), now all mottled/fused individuals. Interestingly both of
these alliances formed after the hurricanes between speckled individuals, which was the first
documentation of juvenile alliance level associations in that community [
A third MGBB alliance formed between speckled individuals: Leucadia and Achilles
(CoA = 0.82) with both Bonito (speckled) and Zen (mottled) as strong partners (CoA = 0.67±
0.78 with the primary pair Leucadia and Achilles, and 0.50 between Bonito and Zen), again
making it difficult to determine the exact structure. The final fourth MGBB alliance is a pair of
fused individuals: Navel and Geo (CoA = 0.86, the strongest CoA observed). Both of these
individuals where not strongly associated with any particular males prior to the move. It is
interesting to note that two of the four alliances of MGBB involve four individuals instead of
the normal two or three.
There were three RGBB male alliances. Evren and Atlas (both speckled, CoA = 0.78) was
the primary pair, with Benjo as the odd male (speckled, CoA = 0.56±0.63) and a possible fourth
member Doc (mottled, CoA = 0.53±0.59). Another alliance was Montana and Manny as the
primary pair (CoA = 0.75) with Salinger as the odd male (CoA = 0.53±0.71), all fused
individuals. The last alliance is Toad and Pulsar (CoA = 0.75) with Baelish as the odd male (CoA =
0.59±0.67), all mottled individuals.
Breeding population estimates
The breeding population (mottled and fused males included) on LBB was reduced from 45
potential breeding contributors (2010±2012) to 24 (2013±2015) as a result of the move of
animals to GBB (Table 7). If only fused males are considered contributors with mottled and fused
females, the breeding group was reduced from 34 individuals to 23. The Northern cluster lost
three males, which was a substantial proportion of the males in the cluster (75%) given its
small size. The Central social cluster was reduced to zero total animals. The Southern cluster
actually increased from 4 breeding males in the pre-move period (2010±2012) to 5 males (1
mottled and 4 fused) in the post-move period (2013±2015; Table 7). We have observed 57 total
resident animals on GBB. Therefore, the total group of animals on GBB consists of at least 112
animals following the move, including new calves that have been born into the groups.
Prior to the move, the operational sex ratio was skewed towards females among resident
animals on LBB at 0.40 but it was not statistically different from a 1:1 ratio (X2 = 1.8, p = 0.18,
Table 7). The skew towards females was significant when mottled males were not considered
(0.32 proportion of males; X2 = 6.7, p < 0.01). Operational sex ratios ranged from 0.24 in the
Southern cluster to 0.37 in the Central cluster.
Following the move, the operational sex ratio dropped to 0.25 (0.22 fused males only)
among the animals that remained on LBB. The skew in sex ratio was different than the
expected 1:1 ratio both when mottled and fused males were included (X2 = 6.0, p < 0.05) and
when mottled males were excluded (X2 = 7.4, p < 0.01). The OSR was reduced to 0.50 in the
Northern cluster and 0.25 (0.22 fused males only) in the Southern cluster.
The OSR among animals that moved from LBB to GBB was 0.45 (0.37 fused males only)
that was slightly less than the OSR of the Central cluster prior to the move (0.50, 0.37 fused
males only). The OSR was not different from 1:1 (mottled and fused males X2 = 0.3, p = 0.59;
fused males only X2 = 1.8, p = 0.18). The resident animals on GBB consisted of 57 total
animals, with an OSR of 0.43 (0.28 fused males only), which were not different from 1:1 (mottled
and fused males X2 = 0.4, p = 0.50; fused males only X2 = 3.6, p = 0.06). If mottled and fused
males are contributors, the OSR is 0.44, which is not different than 1:1 (X2 = 0.7, p = 0.41).
14 / 32
TBmf M:Fmf (M:Ff)
Individual residency and age may change between time periods. TA = total number of animals, TB = total number breeding animals, OSR = operational sex
ratio, M = male, F = female, mf = using mottled and fused males, f = using fused males only
§ Operational sex ratio reported as the proportion of males.
³ Combined MGBB and RGBB.
However, if only fused males are considered, then the OSR is 0.33, which is statistically skewed
towards females (X2 = 5.0, p < 0.05).
We used genotypes from 84 individual Atlantic spotted dolphins that originated from LBB.
Prior to the move, the average r-value was 0.0920 (SE ± 0.0443, 95% CV = 0.1002). The Central
cluster had the largest r-value indicating the more genetic relatedness than either the Northern
or Southern clusters.
Following the move, only 40 animals with genotypes remained active. Of those, 29 moved
to GBB and 11 remained on LBB. The animals that moved had a larger r-value than those that
stayed. Following the move, the combination of a reduced sample size and the removal of
maternal relatives produced lower relatedness values (Table 8). For example, prior to the
move, the baseline relatedness within the Central cluster was 0.108. The relatedness of 29
animals that moved to GBB was reduced to 0.051 if the maternal relatives were removed.
However, if the maternal relatives remain in the analysis, the relatedness was 0.101 that is closer to
the pre-move estimate within the Central cluster. The same pattern was observed among the
animals that remained on LBB with prior r-values of 0.075 (Northern) and 0.044 (Southern)
compared to 0.021 of those than remain (regardless of social cluster) if maternal relatives are
removed and 0.092 if they remain in the analysis.
Habitat and oceanographic trends
Interannual trends in sea surface temperature. From 1998±2012, there was significant
negative trend in annual sea surface temperature anomalies on LBB, which showed a cooling
effect (Pearson correlation: r15 = -0.54, p = 0.040) (Fig 6). A linear regression analysis revealed
that year accounted for a significant proportion of the variance in annual sea surface
temperature anomalies during this period (R2 = 0.29, F1,13 = 5.22, p = 0.040). No similar trend occurred
in annual sea surface temperature anomalies on GBB (Pearson correlations: r15 = -0.33, p =
0.233) (Fig 6) (S3 Fig). The cooling trend on LBB from 1998±2012 could be traced to
15 / 32
N is total number of animals in the group, R is the relatedness coefficient, SE is standard error, and CV is confidence interval. Dolphins on LBB after the
displacement (RLBB), those resident to GBB (RGBB), and those that moved from LBB to GBB (MGBB). Values range from -1±1 with negative values
indicating that relatedness between two individuals is less than the expected between individuals chosen at random, where positive values indicate some
degree of relatedness.
significant cooling on the shallow bank (vs. adjacent deep water) of LBB (Pearson correlation:
r15 = -0.63, p = 0.012) with year accounting for a significant proportion of the variance in
annual sea surface temperature anomalies during this period (R2 = 0.40, F1,13 = 8.61, p = 0.012)
(Fig 7) (S4 Fig).
From 2013±2015, the annual sea surface temperature anomalies revealed some warming on
both LBB and GBB. However, the trend over the three-year period was not statistically
significant in either of these locations (on LBB, Pearson correlation: r3 = 0.996, p = 0.060; on GBB,
Pearson correlations: r3 = 0.995, p = 0.064).
Interannual trends in chlorophyll. From 1998±2012, there was a significant negative
linear correlation in year vs. annual anomalies of chlorophyll on LBB (Pearson on: r15 = -0.77,
p = 0.001), with year accounting for a significant proportion of the variance in annual
chlorophyll anomalies (R2 = 0.59, F1,13 = 18.54, p = 0.001) (Fig 8, S5 Fig). This trend in annual
anomalies of chlorophyll was associated with a reduction in chlorophyll production both on LBB
(Pearson correlation: r15 = -0.73, p = 0.002) and off LBB (Pearson correlation: r15 = -0.57,
p = 0.026) (Fig 9) (S6 Fig). In both cases, year accounted for a significant proportion of
variance in annual anomalies of chlorophyll (On LBB, R2 = 0.53, F1,13 = 14.74, p = 0.002; Off LBB,
R2 = 0.33, F1,13 = 6.35, p = 0.026). In contrast, over the same period there was no significant
relationship between year and annual anomalies in chlorophyll on GBB (Pearson correlation:
r15 = 0.44, p = 0.098) (Fig 8) (S5 Fig).
From 2013±2015, there was no significant trend in annual anomalies of chlorophyll on
either LBB (Pearson correlation: r3 = 0.89, p = 0.304) or GBB (Pearson correlation: r3 = -0.19,
p = 0.877).
Interannual trends in scalar surface wind speed. From 1998±2012, there was an overall
positive linear correlation in year vs. annual anomalies of surface wind speed both on LBB
(Pearson correlation: r15 = 0.79, p = 0.001) and on GBB (Pearson correlation: r15 = 0.76,
p = 0.001) (Fig 10) (S7 Fig), with year accounting for a significant proportion of the variance
in annual anomalies in surface wind speed in both areas (In LBB, R2 = 0.62, F1,13 = 20.99,
p = 0.001; in GBB, R2 = 0.58, F1,13 = 17.60, p = 0.001). The microanalysis revealed that the
overall increasing trend in annual anomalies in surface winds on LBB was associated with a
significant positive linear correlation between annual surface wind speed anomalies and year both
on LBB (Pearson correlation: r15 = 0.75, p = 0.001) and off LBB (Pearson correlation: r15 =
0.84, p < 0.001), with year accounting for a significant proportion of the variance in annual
anomalies in surface winds in both areas (on LBB, R2 = 0.56, F1,13 = 16.48, p = 0.001; off LBB,
16 / 32
Fig 6. Sea surface temperature anomalies on LBB and GBB. Scatter plot of year vs. annual anomalies in sea surface temperature for the combined
shallow and adjacent deep-water areas on LBB and also for GBB from 1998±2012.
R2 = 0.70, F1,13 = 30.53, p < 0.001) (Fig 11) (S8 Fig). The microanalysis also revealed that the
overall increasing trend in annual anomalies in surface winds on GBB was associated with a
significant positive linear correlation between annual surface wind anomalies and year both
on GBB (Pearson correlation: r15 = 0.79, p < 0.001) and off GBB (Pearson correlation: r15 =
0.64, p = 0.010), with year accounting for a significant proportion of the variance in annual
anomalies in surface winds in both areas (on GBB, R2 = 0.62, F1,13 = 21.19, p < 0.001; off the
GBB sandbank, R2 = 0.42, F1,13 = 9.23, p = 0.010) (Fig 12) (S9 Fig).
Dispersal can have profound effects on the structure and stability of a population [
subsequent demographic and/or environmental factors can help shape the future social structure
17 / 32
Fig 7. Sea surface temperature anomalies on vs. off LBB. Scatter plot of year vs. annual anomalies in sea surface temperature on LBB vs. off LBB from
[3,14,37±43]. For 28 years the resident community of Atlantic spotted dolphins suggested a
stable association scenario with long-term social clusters, high social differentiation and
preferred companions [
] until sometime between fall 2012 and spring 2013 when a major
distribution shift of 50% of the stable spotted dolphin community occurred, throwing both the
remnant community, and the shifted community, into new situations. Responses to
demographic changes may differ between populations, with varying degrees of alterations in
population and/or social structure as they adapt to changing conditions [
], which can profoundly
affect the survival of the individual, and structure at the community and population levels. We
discuss the social and genetic implications of the unprecedented emigration event described
here and the possible factors that may have contributed to the move.
18 / 32
Fig 8. Satellite chlorophyll anomalies on LBB and GBB. Scatter plot of year vs. annual anomalies in chlorophyll production for the combined
shallow and adjacent deep-water areas on LBB and also for GBB from 1998±2012. Trend lines, R2 and linear regression equations are shown for
The movement of individuals affects and is affected by the environment and other individuals
]. An individual's movements, through its own situation with regard to sex, age,
ontogenetic status and social surroundings, may affect or be affected by others [
]. The splitting of
the LBB spotted dolphin community resulted in two different communities with varying social
structures that are distinctly different from their previous long-term structure. In many social
species it has been shown that demographic changes can result in altered behavior and social
structure [3,14,39±46]. In sperm whales it has been suggested that the stark differences in
social structure between whales in the Pacific vs. Atlantic may be attributed to the
anthropogenic destruction of genetic lineages [
] where the devastation of social units due to intense
19 / 32
Fig 9. Satellite chlorophyll anomalies on vs. off LBB. Scatter plot of year vs. annual anomalies in chlorophyll production on LBB vs. off LBB from
1998±2012. Trend lines, R2 and linear regression equations are shown for significant trends.
whaling in the Pacific may have led to larger, less matrilineal and more socially homogenous
units . The results of this study indicate that the movement of such a large socially cohesive
cluster altered the social patterns of the remnant and shifted communities. This could have
profound impacts on the future social structure and survival of the two spotted dolphin
communities (and affect the sympatric bottlenose dolphin communities with whom they regularly
interact) on LBB and GBB, which are likely part of a larger genetic population.
For the RLBB dolphins after the emigration event, social differentiation remained
moderate/high (likely due to differences in associations between the Northern and Southern
individuals), but their overall associations were random with no preferred or avoided companions,
strikingly different from their nonrandom associations documented since 1991 [
communities of dolphins and primates have been shown to have increased cohesiveness and
20 / 32
Fig 10. Scalar surface wind anomalies on LBB and GBB. Scatter plot of year vs. annual anomalies in surface winds for the combined shallow and
adjacent deep-water areas on LBB and also for GBB from 1998±2012. Trend lines, R2 and linear regression equations are shown for significant trends.
less fission/fusion dynamics, with more time spent with all other members of the population
]. Smaller social groups may need more individuals to maintain normal social and
behavioral functions, thus making recruitment of individuals easier [
] and/or necessary.
This did not occur between the clusters on LBB after the hurricanes and loss of over 30% of the
] nor after the mass emigration event. This provides further support to the
finding of [
] that the clusters are an integral part of the community structure, remaining in some
capacity regardless of demographic changes. It may also take longer than three years for the
individuals to adapt to the new conditions; in this study site it took more than five years for
`normal' aggressive behaviors during interspecies encounters to re-occur following hurricanes
and social restructuring [
], thus future research may reveal nonrandom associations and a
similar or different social structure. Regardless of time frame however, the changes observed
will have important implications regarding survivability of individuals, social clusters/social
21 / 32
Fig 11. Scalar surface wind anomalies on vs. off LBB. Scatter plot of year vs. annual anomalies in surface winds on LBB vs. off LBB from 1998±2012.
Trend lines, R2 and linear regression equations are shown for significant trends.
structure, and community as a whole if outside individuals and genes are not integrated (see
genetic section below).
The low social differentiation observed within each social cluster on LBB prior to the
emigration event indicates that there was some complexity in the associations between individuals
within in each cluster. For each cluster the levels remained relatively consistent between 2007±
2009 and 2010±2012 (the drop for the Southern cluster was likely an artifact because fewer
individuals were included in the analysis based on number of sightings). Interestingly the
social differentiation for the MGBB dolphins was 0, indicating relationships between members
were completely homogenous. This is a large change from the ~0.30 social differentiation of
the Central cluster prior to the move and also indicates (along with the Mantel test showing no
difference within/between clusters) that the Northern and Southern individuals became fully
integrated into the new MGBB cluster. Immigration carries costs (e.g., increased aggression,
22 / 32
Fig 12. Scalar surface wind anomalies on vs. off GBB. Scatter plot of year vs. annual anomalies in surface winds on GBB vs. off GBB from 1998±
2012. Trend lines, R2 and linear regression equations are shown for significant trends.
decreased foraging and energetic travel costs) which can be high [
], with such a large group
moving as one, there may have been more incentive to increase cohesiveness to maintain
normal behaviors in an unknown situation. Although we do not have information on social
differentiation or associations for RGBB dolphins prior to the event, the current ~0.29 social
differentiation indicates a similar diversity of association as seen in the LBB social clusters
prior to the move. Associations between MGBB and RGBB dolphins were extremely low
indicating that MGBB dolphins did not integrate into the resident community, but maintained
themselves as a distinctly different social cluster.
Interestingly there were three male individuals that seemed to link the very thin connection
between the two clusters on GBB. There is often a sex bias in acceptance of female vs. male
immigrants, and in many cases female immigrants may find more resistance and male
immigrants find less from residents [
]. In many dolphin populations males tend to have larger
23 / 32
home ranges [17,49±50]. Thus it may not be uncommon for residents to interact with various
unknown males, which may make it easier for immigrant males, like these three, to integrate
]. These individuals may begin to cement relationships between the immigrants and
residents possibly becoming ªcentralized brokersº, who in some social scenarios, may play a more
important role in the connectivity within a network [
]. The future structure of this
community will depend greatly on the amount of interaction and ultimate integration of these two
clusters with varied social structures.
In these spotted dolphins, females generally remain in their natal cluster [
there were matriline splits where one dolphin stayed on LBB and the other moved to GBB.
Interestingly this type of split did not occur after losing over 30% of the community following
the hurricanes [
]. A similar event occurred in killer whales following demographic losses
related to the Exxon Valdez oil spill, where a subpod split from the original matrilineal pod
and began consistently associating with another pod [
] and may have been due to the loss of
related females tying the pod together. In both cases, these splits are unprecedented and
unexplained. This could indicate that for some individuals strong social familiarity with other
conspecifics (vs. matrilineal relationships) may have a stronger influence on associations and
behavior. This may be more important for females than males, as social familiarity is an
important component of female associations [
Male alliances were observed in both MGBB and RGBB dolphins, though with some altered
patterns. The most interesting is three of the four MGBB alliances were formed when the
individuals were juveniles and two of these are individuals that remained intact (although with
some changes) since the hurricanes and through the move. One of the three RGBB alliances
was also between speckled individuals. Alliance level associations between juvenile spotted
dolphins had not been documented until after the hurricanes [
], as relationships like this
usually crystallize during sexual maturity [
]. Factors that alter social behavior may affect
young animals to a greater degree [
], and the loss of individuals after the hurricanes may
have effectively sped up the development of alliance formation [
]. This idea is supported by
the results presented here, and further support that environmental and demographic changes
can influence current and future alliance formation.
The other notable difference is that two of the four MGBB alliances and one of the three
RGBB alliances may have as many as four alliance partners. Although it is difficult to
determine the exact nature of these alliances from their CoAs at this point, it is clear that there may
be a more complicated structure than has previously been seen. Long-term stable dolphin
male alliances are generally formed between pairs or trios of individuals [
also have second order alliances of strong associations between members of different alliances
that can vary in level of stability over years [12,14,55±56] Alliance size and formation are
affected by the number of competing males and the factors that impact this including density
of females, operational sex ratio, and encounter rate of females . It has also been shown
that environmental disturbance/large demographic changes can affect alliance formation, as
seen with the juvenile alliances formed after the hurricanes on LBB . The combination of
normal alliance formation factors and the unprecedented emigration event may have created
the possibility of an alliance with four members (vs. two pair alliances with strong associations)
to be viable and possibly necessary. Further research into the stability of these associations
over time will provide insight into whether this is a stable scenario, or a temporary status
during times of change.
Social behavior and dispersal may be connected by feedback loops so that dispersal patterns
may change social behavior, which in turn may modify dispersal patterns [
]. There is
behavioral flexibility between delphinid populations indicating that social variability is a
common response to environmental variability [
], but may also be important in surviving
24 / 32
environmental or demographic changes that can affect social structure and sociality [
This is evident in this study as well, and further supports the suggestion that responses to
demographic upheaval differ between populations and/or species, with varying degrees of
social structure changes as the individuals adapt to new conditions [
Genetic and population implications
The change in community groups has major implications for genetic diversity. Male
reproductive success and female strategies may change depending on sex ratio and/or resource
availability and these factors may influence the overall mating system of the community [
If we consider the animals that relocated separate from those that remained on LBB, there
are differing potential outcomes. For those animals that relocated to GBB, the outcome is likely
positive. It is not surprising that the average relatedness among the animals that moved to
GBB was similar to the Central cluster, because the entire Central cluster moved to GBB with a
few additional animals. Previous research indicates that the Central cluster, being the largest,
could function as a self-contained social and reproductive unit [
]. The number of males and
females could support mating within the cluster even though mating between clusters was
indicated through genetic paternity assignments. Therefore, when moving to a new location,
the cluster will likely remain relatively constant. The group that dispersed may face integration
issues with the existing spotted and bottlenose dolphins on GBB but we expect mating to
occur between members of the RGBB group and the relocated MGBB group, even if they do
not fully integrate socially. With the addition of new mating opportunities through the
resident group on GBB, the gene pool will likely expand and provide increased genetic diversity
over time. The same reciprocal benefit is expected for the resident animals of GBB.
On the other hand, given the reduced number of spotted dolphins in the remnant
community on LBB, especially males, mating opportunities are greatly reduced. The animals that
moved to GBB had a greater r-value than those that stayed indicating that the animals left on
LBB are less closely related than those that moved. However, given the small number of
genotyped animals from the Northern and Southern clusters, the data should be interpreted
cautiously. The level of relatedness may be underestimated as a result of missing genotypes from
close relatives to those that were genotyped. With a low level of genetic diversity and closely
related individuals, the remnant animals may experience at least some level of inbreeding over
time. Without an influx of new genes, this could result in decreasing levels of genetic diversity
and potential mating between closely related animals. Such negative outcomes are expected
among the remaining animals on LBB unless new mates become available. It remains to be
seen whether new spotted dolphins will enter the area. However, the previous low immigration
rates may make an influx in immigration an unlikely scenario. This is especially true if the
exodus was a result of limited resources. In that case, we do not expect large numbers of new
animals to immigrate into the area simply because the habitat is resource limited.
It is possible that rather than new spotted dolphins immigrating into the area, new
bottlenose dolphins will enter the area. Although resource limits could still be a limiting factor for
new immigration of any species, bottlenose and spotted dolphin food resources do not overlap
]. Because we have observed increased immigration of bottlenose dolphins in to
the LBB study area following the hurricanes [
], it is reasonable to expect bottlenose dolphins
to fill the niche if resources are available. With increasing numbers of bottlenose dolphins and
smaller numbers of spotted, the possibility for hybridization increases. For decades we have
observed mating behaviors on LBB between spotted and bottlenose dolphins [
]. There are at least 15 anomalous bottlenose dolphins on LBB that exhibit varying
degrees of uncharacteristic ventral spotting [
]. Furthermore, a suspected bottlenoseÐ
25 / 32
spotted hybrid calf was observed on GBB; the suspicion of hybridization was based on
intermediate morphology between the two species [
]. Although the hybrid was not genetically
confirmed observations of anomalous individuals lends strong support to the idea that
hybridization already occurs between these species and it is reasonable to expect hybridization given
the relatively common hybridization of bottlenose dolphins with other species [62±65]. In the
short term, if hybridization occurs, it opens up new mating opportunities to the remnant
population of spotted dolphins and provides a mechanism to bolster their population size.
Furthermore, hybridization may open the possibility of speciation mechanisms. Although in the
short term it may be positive to increase hybridization, the long-term effects may be
challenging. For instance, if the majority of mates are bottlenose, an imbalanced species ratio may
cause mates to become a limited resource for spotted dolphins and it may be difficult for the
spotted community to rebuild its numbers on LBB. In the case of an imbalanced species ratio,
it is not known whether the remaining spotted dolphins will eventually relocate in order to
access additional mates or if they will travel longer distances to temporarily access mates
similar to long-finned pilot (Globicephala melas) or killer whales (Orcinus orca). Long-finned pilot
whales and killer whales live in matrifocal groups where males may remain with their natal
group and social groups, at times, aggregate and provide temporary opportunities to breed
with non-related individuals [66±67]. In the event that hybridization between species increases
on LBB, there are fitness risks to consider for the hybrid offspring. In many instances, hybrids
are not viable although the observation of a suspected hybrid calf in good health [
this may not be a concern for Tursiops—Stenella hybrids. Even though a hybrid calf survives,
there are higher instances of sterility, especially in the heterogametic sex [
]. Such sterility
would reduce the number of breeding males on LBB even further and over time it is possible
that spotted dolphins would decrease further in numbers, especially if new spotted dolphins
do not immigrate to LBB.
Habitat and survival implications
Major dramatic shifts of habitat in several cetacean species have been associated with changes in
prey field [
]. For example,  reported a gradual departure of humpback whales (Megaptera
novaeangliae) from Stellwagen Bank in the Southern Gulf of Maine, a major feeding ground in
the mid-1970s through mid-1980s. From 1990 to 1994 the number of identified humpbacks
decreased from 258 to 7 and from 1988±1994, the mean number of humpbacks identified per
day dropped from 17.7 to 0.9 respectively. The major prey item of humpback whales off
Stellwagen Bank in the 1970s and 1980s was sand lance (Ammodytes spp.). Echo-sounder surveys in
1990 and 1992 showed a dramatic decline in prey trace levels from 19.1% of the vertical water
column to 2.8% respectively. Data from Jeffrey's Ledge, 22 km north of Stellwagen Bank revealed
a sudden increase in humpbacks in 1992 with 64% individuals that had previously been
identified off Stellwagen Bank in the late 1980s. The population shift in humpbacks from Stellwagen
Bank to Jeffery's Ledge appeared to be associated with recovering herring populations.
The dramatic shift of over 50% of the historically stable Atlantic spotted dolphin
community from LBB to GBB between fall 2012 and spring 2013 appeared to be associated with
changes in several oceanographic factors that may likely have influenced availability of prey.
From 1998 through 2012 (the final year in which the LBB Atlantic spotted dolphin community
was still intact), LBB showed a significant cooling trend that could be traced to the LBB
sandbank vs. the adjacent deep waters. Over this same period, LBB also witnessed a significant
decrease in chlorophyll production, which could be traced to reductions both on and off the
LBB sandbank. No significant changes in either of these factors were witnessed for the same
period on GBB. The contrast between these gradual oceanographic trends on LBB from 1998±
26 / 32
2012 and the dolphin community's sudden dramatic shift between 2012 and 2013 suggests that
the community may have been under an increasing stress that eventually reached a tipping
point. Given the environmental factors involved (sea surface temperature and chlorophyll),
and the current complexity of physical oceanographic features [71±73] the most likely
candidate is a lack of sufficient food resources. Historically, only the Central cluster was documented
feeding off the deep-water edge at night on flying fish and squid [
], suggesting that this
offshore food source may have been compromised for this specific group of dolphins.
In terms of trends from 2013 onward, there were no significant changes in annual
anomalies in either sea surface temperature or chlorophyll on either LBB or GBB although there may
have been an emerging warming trend on both locations. With regard to scalar surface wind
speeds, an examination of annual anomalies revealed a significant trend towards greater
surface wind speeds from 1998±2012 both on LBB and GBB, which in each area was associated
with increasing surface wind speeds across years both on and off the sandbanks. Surface
winds, including increased speeds and changing predominate wind directions, can have an
effect on nutrient replacement and production [
]. However, because greater surface wind
speeds were observed on both LBB and GBB during the period leading up to the dolphin
relocation event, other factors are likely to have contributed to the sea surface temperature cooling
trend and collapse in chlorophyll production on LBB but not on GBB.
Because the exodus occurred between September 2012 and May 2013 we do not know if the
dolphins moved gradually or as a group. The unprecedented shift in residency of LBB dolphins
suggests a complex response to potential environmental changes, and may have profound
effects on the social and genetic structure, including hybridization of both species, of both
communities on LBB and GBB. Ecological forces, sometimes linked with changes in prey
density, have been shown to act strongly on the social behavior of cetaceans [52,75±78] and
the genetic composition of mammal populations [
]. Considerable behavioral plasticity in
response to stressors like these has been documented in many marine mammal species,
however the limits of this plasticity are unknown [
]. Because of our findings it seems likely that
changing environmental variables on LBB may have led to a crash in the food chain, causing
an unprecedented move of resident animals to a new location. It remains unknown whether
this is a permanent exodus of the displaced dolphins, or a temporary shift in location due to
resources. Oceanographic factors should be monitored in the future to assess these changing
habitat features on the social and location adjustments of this dolphin community.
S1 Fig. Association matrix for hierarchical cluster. Analysis and nMDS for 2013 to 2015 on
Great Bahama Bank (GBB).
S2 Fig. Supplemental file for hierarchical cluster. Analysis and nMDS for 2013 to 2015 on
Great Bahama Bank (GBB).
S3 Fig. Scatter plot of year versus annual anomalies in sea surface temperature (ÊC) for the
combined shallow and adjacent deep-water areas on Little Bahama Bank and Great
Bahama Bank from 1998±2012.
S4 Fig. Scatter plot of year versus annual anomalies in sea surface temperature (ÊC) on and
off Little Bahama Bank from 1998±2012.
27 / 32
S5 Fig. Scatter plot of year versus annual anomalies in surface chlorophyll A production
for the combined shallow and adjacent deep-water areas on Little Bahama Bank (LBB) and
on Great Bahama Bank (GBB) from 1998±2012.
S6 Fig. Scatter plot of year versus annual anomalies in surface chlorophyll A production
on and off Little Bahama Bank from 1998±2012.
S7 Fig. Scatter plot of year versus annual anomalies in surface winds for the combined
shallow and adjacent deep-water areas of Little Bahama Bank and of Great Bahama Bank
S8 Fig. Scatter plot of year versus annual anomalies in surface winds on and off Little
Bahama Bank from 1998±2012.
S9 Fig. Scatter plot of year versus annual anomalies in surface winds on and off Great
Bahama Bank from 1998±2012.
We thank the Wild Dolphin Project and all crew and volunteers involved during the time
frame of this study. Special thanks to Todd O'Brien and COPEPOD for extracting and helping
with the oceanographic data, Jay Baldwin for assistance in running relatedness analysis, and
Marguerite Koch for ocean ecology discussions. All research was conducted under a permit
from the Bahamian Department of Fisheries.
Conceptualization: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L.
Green, Adam A. Pack.
Data curation: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser.
Formal analysis: Denise L. Herzing, Cindy R. Elliser, Michelle L. Green, Adam A. Pack.
Funding acquisition: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L.
Investigation: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L. Green,
Adam A. Pack.
Methodology: Denise L. Herzing, Cindy R. Elliser, Michelle L. Green.
Project administration: Denise L. Herzing, Cindy R. Elliser, Michelle L. Green.
Resources: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L. Green, Adam
Supervision: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L. Green.
Validation: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L. Green,
Adam A. Pack.
28 / 32
Visualization: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle L. Green,
Adam A. Pack.
Writing ± original draft: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser, Michelle
L. Green, Adam A. Pack.
Writing ± review & editing: Denise L. Herzing, Bethany N. Augliere, Cindy R. Elliser,
Michelle L. Green, Adam A. Pack.
29 / 32
Whitehead H. Analyzing animal societies: Quantitative Methods for vertebrate social analysis. Chicago:
The University of Chicago Press; 2008.
Whitehead H. Precision and power in the analysis of social structure using associations. Anim Behav.
2008; 75: 1093±1099.
32. Green ML, Herzing DL, Baldwin JD. Noninvasive methodology for the sampling and extraction of DNA
from free-ranging Atlantic spotted dolphins (Stenella frontalis). Mol Ecol Notes 2007; 7: 1287±1292.
30 / 32
62. Dohl TP, Norris KS, Kang I. A porpoise hybrid: Tursiops x Steno. J Mammal. 1974; 55: 217±221. PMID:
31 / 32
1. Baker AJ , Dietz JM . Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia) . Am J Primatol . 1996 ; 38 : 47 ± 56 .
2. Brockelman WY , Reichard U , Treesucon U , Raemaekers JJ . Dispersal, pair and social structure in gibbons (Hylobates lar) . Behav Ecol Sociobiol . 1998 ; 42 : 329 ± 339 .
3. Elliser CR , Herzing DL . Replacement Dolphins? Social restructuring of a resident pod of Atlantic Bottlenose Dolphins, Tursiops truncatus, after two major hurricanes . Mar Mamm Sci . 2011 ; 27 : 39 ± 59 .
4. Kahlenberg SM , Thompson ME , Muller MN and Wrangham RW . Immigration costs for female chimpanzees and male protection as an immigrant counter strategy to intrasexual aggression . Anim Behav . 2008 ; 76 : 1497 ± 1509 .
5. Bowler DE , Benton TG . Causes and consequences of animal dispersal strategies: Relating individual behaviour to spatial dynamics . Biol Rev . 2005 ; 80 : 205 ± 225 . PMID: 15921049
6. Herzing DL . The natural history of free-ranging Atlantic spotted dolphins (Stenella frontalis): Age classes, color phases, and female reproduction . Mar Mamm Sci 1997 ; 13 : 576 ± 595 .
7. Herzing DL . Vocalizations and associated underwater behavior of free-ranging Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus . Aquat Mamm . 1996 ; 22 : 61 ± 79 .
8. Herzing DL . Acoustics and Social Behavior of Wild Dolphins: Implications for a sound society . In Au WWL , Popper AN , Fay RR , editors. Hearing in whales. New York: Springer-Verlag; 2000 . pp. 225 ± 272 .
9. Herzing DL . Social and nonsocial uses of echolocation in free-ranging Stenella frontalis and Tursiops truncatus . In Thomas JA , Moss CF , Vater M , editors. Advances in the study of echolocation in bats and dolphins . Chicago: University of Chicago Press; 2004 . pp. 404 ± 410 .
10. Lammers MO , Au WWL , Herzing DL . The broadband social acoustic signaling behavior of spinner and spotted dolphins . J Acoust. Soc Am . 2003 ; 114 : 1629 ±1639 PMID: 14514216
11. Elliser CR , Herzing DL . Community structure and cluster definition of Atlantic spotted dolphins, Stenella frontalis, in the Bahamas . Mar Mamm Sci . 2012 ; 28 : E486± E502 .
12. Elliser CR , Herzing DL . Long-term social structure of a resident community of Atlantic spotted dolphins, Stenella frontalis , in the Bahamas , 1991 ± 2002 . Mar Mamm Sci. 2014 ; 30 : 308 ± 328 .
13. Herzing DL , Elliser CR . Nocturnal feeding of Atlantic spotted dolphins (Stenella frontalis) in the Bahamas . Mar Mamm Sci . 2014 ; 30 : 367 ± 373 .
14. Elliser CR , Herzing DL . Social structure of Atlantic spotted dolphins, Stenella frontalis, following environmental disturbance and demographic changes . Mar Mamm Sci . 2014 ; 30 : 329 ± 347 .
15. Green ML , Herzing DL , Baldwin JD . Reproductive success of male Atlantic spotted dolphins (Stenella frontalis) revealed by noninvasive genetic analysis of paternity . Can J Zoolog . 2011 ; 89 : 239 ± 253 .
16. Green ML , Herzing DL , Baldwin JD . Molecular assessment of mating strategies in a population of Atlantic spotted dolphins . PloS ONE . 2015 ; 10 : e0118227. https://doi.org/10.1371/journal.pone. 0118227 PMID: 25692972
17. Rogers CA , Brunnick BJ , Herzing DL , Baldwin JD . The social structure of bottlenose dolphins, Tursiops truncatus, in the Bahamas . Mar Mamm Sci . 2004 ; 20 : 688 ± 708 .
18. Rossbach KA , Herzing DL . Inshore and offshore bottlenose dolphin (Tursiops truncatus) communities distinguished by association patterns near Grand Bahama Island, Bahamas . Can J Zool. 1999 ; 77 : 581 ± 592 .
19. Herzing DL , Johnson CM . Interspecific interactions between Atlantic spotted dolphins (Stenella frontalis) and bottlenose dolphins (Tursiops truncatus ) in the Bahamas , 1985 ± 1995 . Aquat Mamm . 1997 ; 23 : 85 ± 99 .
20. Herzing DL , Elliser CR . Directionality of sexual activities during mixed-species encounters between Atlantic Spotted Dolphins (Stenella frontalis) and Bottlenose Dolphins (Tursiops truncatus) . Int J Comp Psychol . 2013 ; 26 : 124 ± 134 .
21. Elliser CR , Herzing DL . Long-term interspecies association patterns of Atlantic bottlenose dolphins, Tursiops truncatus, and Atlantic spotted dolphins, Stenella frontalis, in the Bahamas . Mar Mamm Sci . 2016 ; 32 ( 1 ): 38 ± 56 .
22. Elliser CR , Herzing DL . Changes in interspecies association patterns of Atlantic bottlenose dolphins, Tursiops truncatus, and Atlantic spotted dolphins, Stenella frontalis, after demographic changes related to environmental disturbance . Mar Mamm Sci . 2016 ; DOI: https://doi.org/10.1111/mms.12289
23. Green ML . Assessment of genetic population structure, promiscuity, and paternity in free-ranging Atlantic spotted dolphins, Stenella frontalis, in the Bahamas . Ph.D. Dissertation , Florida Atlantic University. 2008 .
24. Augliere B. Home on the range: Spatial ecology of Atlantic spotted dolphins (Stenella frontalis) in the Bahamas . M.Sc. Thesis , Florida Atlantic University. 2012 .
25. Perrin WF . Color pattern of the eastern pacific spotted porpoise Stenella graffmani Lonnberg (Cetacea, Delphinidae) . Zoologica 1970 ; 54 : 135 ± 149 .
26. Shane S. Behavior and ecology of the bottlenose dolphin at Sanibel Island, Florida . In Leatherwood S, Reeves RR , editors. The bottlenose dolphin . San Diego: Academic Press; 1990 . pp. 245 ± 265 .
27. Cairns SJ , Schwager, SJ. A comparison of association indices . Anim Behav . 1987 ; 35 : 1454 ± 1469 .
Whitehead H. SOCPROG programs: Analyzing animal social structures . Behav Ecol Sociobiol . 2009 ; 63 : 765 ± 778 .
29. Gero S , Bejder L , Whitehead H , Mann J , Connor RC . Behaviourally specific preferred associations in bottlenose dolphins, Tursiops sp . Can J Zoolog . 2005 ; 83 : 1566 ± 1573 .
33. Queller DC , Goodnight KF . Estimating relatedness using genetic markers . Evolution 1989 ; 43 : 258 ± 275 . https://doi.org/10.1111/j.1558- 5646 . 1989 .tb04226. x PMID: 28568555
34. O 'Brien T. COPEPOD : The Global Plankton Database; 2014 . Accessed October 12, 2016 . http://www. st.nmfs.noaa.gov/copepod.
35. O 'Brien TD . Time series data analysis and visualization . In: O' Brien TD , Wiebe PH , Falkenhaug T , editors. ICES Zooplankton Status Report 2010/2011, ICES Cooperative Research Report 318; 2013 . pp. 6 ± 19 .
36. O 'Brien TD . Methods and Visualization . In: O'Brien T , Lorenzoni L , Isensee K , Valdes L , editors. What are Marine Ecological Time Series telling us about the ocean? A status report , IOC-UNESCO, IOC Technical Series 129 ; 2016 . pp 304 .
37. Morales JM , Moorcroft PR , Matthiopoulos J , Frair JL , Kie JG , Powell RA , et al. Building the bridge between animal movement and population dynamics . Philos T R Soc B . 2010 ; 365 : 2289 ± 2301 .
38. Brandt CA. Social factors in immigration and emigration . In: Stenseth NC , Lidicker Jr . WZ, editors. Animal dispersal: Small mammals as a model . New York: Chapman & Hall; 1992 . pp. 96 ± 141 .
39. Lazaro-Perea C , Castro CSS , Harrison R , Araujo A , Arruda MF , Snowdon CT . Behavioral and demographic changes following the loss of the breeding female in cooperatively breeding marmosets . Behav Ecol Sociobiol . 2000 ; 48 : 137 ± 146 .
40. Lehmann J , Boesch C . To fission or to fusion: Effects of community size on wild chimpanzee (Pan troglodytes verus) social organization . Behav Ecol Sociobio . 2004 ; 56 : 207 ± 216 .
41. Lusseau D , Newman MEJ . Identifying the role that animals play in their social networks . Proc R Soc Lond B Biol Sci . 2004 ; 271 : S477± S481 .
42. Matkin CO , Saulitis EL , Ellis GM , Olesiuk P and Rice SD . Ongoing population-level impacts on killer whales Orcinus orca following the `Exxon Valdez' oil spill in Prince William Sound , Alaska. Mar Ecol Prog Ser . 2008 ; 356 : 269 ± 281 .
43. Sapolsky RM , Share LJ . A Pacific Culture among Wild Baboons: Its Emergence and Transmission . Plos Biol . 2004 ; 2 ( 4 ): 0534 ± 0541 .
44. Gero S , Gordon J , Whitehead H . Individualized social preferences and long-term social fidelity between social units of sperm whales . Anim Behav 2015 ; 102 : 15 ± 23 .
Whitehead H , Antunes R , Gero S , Wong S , Engelhaupt D , Rendell L. Multilevel societies of female sperm whales (Physeter macrocephalus) in the Atlantic and Pacific: why are they so different? Int J Primatol . 2012 ; 33 : 1142 ± 1164 .
46. Cantor M , Whitehead H , Gero S , Rendell L . Cultural turnover among Galapagos sperm whales . Roy. Soc. Open Sci . 2017 ; 3 : 160615 .
47. Lusseau D , Schneider K , Boisseau OJ , Haase P , Slooten E , Dawson SM . The bottlenose dolphin community of Doubtful Sound features a large proportion of long lasting associations . Behav Ecol Sociobiol . 2003 ; 54 : 396 ± 405 .
48. Schaffner CM , French JA . Group size and aggression: `Recruitment incentives' in a cooperatively breeding primate . Anim Behav . 1997 ; 54 : 171 ± 180 . PMID: 9268447 49 .
Wells RS , Scott MD , Irvine AB . The social structure of free-ranging bottlenose dolphins . In Genoways H, editor. Current mammalogy . New York: Plenum Press; 1987 . pp. 247 ± 305 .
50. Gubbins CM . Use of home ranges by resident bottlenose dolphins (Turisops truncatus) in a South Carolina estuary . J Mammal . 2002 ; 83 : 25 ± 34 .
51. Moller LM , Harcourt RG . Shared reproductive state enhances female associations in dolphins . Res Lett Ecol . 2008 ; https://doi.org/10.1155/ 2008 /498390 52.
Wells RS , Hansen LJ , Baldridge A , Dohl TP , Kelly DL , Defran RH . Northward extension of the range of bottlenose dolphins along the California coast . In Leatherwood S, Reeves RR , editors. The bottlenose dolphin . San Diego: Academic Press Inc.; 1990 . pp. 421 ± 431 .
53. McHugh KA , Allen JB , Barleycorn AA , Wells RS . Severe Karenia brevis red tides influence juvenile bottlenose dolphins (Tursiops truncatus) behavior in Sarasota Bay, FL . Mar Mamm Sci . 2010 ; 27 : 622 ± 643 .
54. Connor RC , Smolker RA , Richards AF . Two levels of alliance formation among bottlenose dolphins (Tursiops sp .). P Natl Acad Sci USA . 1992 ; 89 : 987 ± 990 .
55. Connor RC . Dolphin social intelligence: Complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals . Philos T R Soc B . 2007 ; 362 : 587 ± 602 .
56. Connor RC . Cooperation beyond the dyad: On simple models and a complex society . Philos T R Soc B . 2010 ; 365 : 2687 ± 2697 .
Whitehead H , Connor R. Alliances I. How large should alliances be? Anim Behav . 2005 ; 69 : 117 ± 226 .
58. Karczmarski L , WuÈrsig B , Gailey G , Larson KW , Vanderlip C . Spinner dolphins in a remote Hawaiian atoll: Social grouping and population structure . Behav Ecol . 2005 . 16 ; 675 ± 685 .
59. Sugg D , Chesser R . Effective population sizes with multiple paternity . Genet . 1994 ; 137 : 1147 ± 1155 .
60. Malinowski CR , Herzing DL . Prey use and nutritional differences between reproductive states and age classes in Atlantic spotted dolphins (Stenella frontalis) in the Bahamas . Mar Mamm Sci . 2015 ; 31 ( 4 ): 1471 ± 1493 .
61. Herzing DL , Moewe K , Brunnick BJ . Interspecies interactions between Atlantic spotted dolphins, Stenella frontalis and bottlenose dolphins, Tursiops truncatus , on Great Bahama Bank, Bahamas. Aquat Mamm . 2003 ; 29 : 335 ± 341 .
63. Nishiwaki M , Tobayama T . Morphological study on the hybrid between Tursiops and Pseudorca . Sci Rep Whales Research Institute Tokyo. 1982 ; 34 : 109 ± 121 .
64. Zornetzer HR , Duffield DA . Captive-born bottlenose dolphin x common dolphin (Tursiops truncatus x Delphinus capensis) . Can J Zool . 2003 ; 81 : 1755 ± 1762 .
65. Caballero S , Baker CS . Captive-born intergeneric hybrid of a Guiana and bottlenose dolphin: Sotalia guianensis x Tursiops truncatus . Zoo Biol . 2010 ; 5 : 647 ± 657 .
66. Amos B , Barrett J , Dover GA . Breeding behavior revealed by DNA fingerprinting . Heredity . 1991 ; 67 : 49 ± 55 . PMID: 1917551
67. Hoelzel AR , Hey J , Dahlheim ME , Nicholson C , Burkanov V , Black N. Evolution of population structure in a highly social top predator, the killer whale . Mol Biol Evol . 2007 ; 24 : 1407 ± 1415 . https://doi.org/10. 1093/molbev/msm063 PMID: 17400573
68. Haldane JBS . Sex ratio and unisexual sterility in hybrid animals . Journal of Genet . 1922 ; 12 : 101 ± 109 .
69. Payne PM , Wiley D , Young S , Pittman S , Clapham PJ , Jossi JW . Recent fluctuations in the abundance of baleen whales in the southern Gulf of Maine in relation to changes in selected prey . Fish Bull . 1990 ; 88 : 687 ± 696 .
Weinrich M , Martin M , Griffiths R , Bove J , Schilling M. A shift in distribution of humpback whales, Megaptera novaeangliae, in response to prey in the southern Gulf of Maine . Fish Bull . 1997 ; 95 : 826 ± 836 .
71. Barton A , Lozier MS , Williams RG . Physical controls of variability in North Atlantic phytoplankton communities . Limnol.Oceanogr . 2014 ; 60 : 181 ± 197 .
72. Behrenfeld MJ , O'Malley RT , Boss ES , Westberry TK , Graff JR , Halsey KH , Milligan AJ , Siegel DA , Brown MB . Revaluating ocean warming impacts on global phytophankton . Nature Climate Change . 2015 ; https://doi.org/10.1038/NCLIMATE2838
73. Park JY , Kug JS , Park J , Yeh SW , Jang CJ . Variability of chlorophyll associated with El Nino-Southern Oscillation and its possible biological feedback in the equatorial Pacific . J Geophy Res . 2011 ; 116 : https://doi.org/10.1029/2011JCoo7056
74. Kahru M , Gille ST , Murtugudde R , Strutton PG , Manzano-Sarabia M , Wang H , Mitchel BG . Global correlations between winds and ocean chlorophyll . J Geophy Res . 2010 ; 115 : https://doi.org/10.1029/ 2010JC006500
Wells RS , Irvine AB , Scott MD . The social ecology of inshore odontocetes . In Herman LM, editor. Cetacean behavior: Mechanisms and functions . New York: Wiley Interscience; 1980 . pp. 263 ± 318 .
76. Lusseau D , Williams R , Wilson B , Grellier K , Barton TR , Hammond PS et al. Parallel influence of climate on the behavior of Pacific killer whales and Atlantic bottlenose dolphins . Ecol Lett 2004 ; 7 : 1068 ± 1076 .
77. MacLeod CD , Bannon SM , Pearce GJ , Schweder C , Learmonth JA , Herman JS et al. Climate change and the cetacean community of northwest Scotland . Biol Conserv . 2005 ; 124 : 477 ± 483 .
78. Learmonth JA , Macleod CD , Santos MB , Pierce GJ , Crick HQP , Robinson RA . Potential effects of climate change on marine mammals . Oceanogr Mar Biol . 2006 ; 44 : 431 ± 464 .
79. ReÂale D , McAdam AG , Boutin S , Berteaux D . Genetic and plastic responses of a northern mammal to climate change . Proc Biol Sci . 2003 ; 270 : 591 ± 596 . https://doi.org/10.1098/rspb. 2002 .2224 PMID: 12769458