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Genetic structure among spawning aggregations of the gulf coney Hyporthodus acanthistius


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Many large groupers form spawning aggregations, returning to the same spawning sites in consecutive spawning seasons. Connectivity between spawning aggregations is thus assured by larval dispersal. This study looks into the genetic structure and gene flow among spawning aggregations of a large grouper, the gulf coney Hyporthodus acanthistius, in the northern Gulf of California. First, using the mitochondrial control region and 11 microsatellites, we calculated FST metrics and conducted a Bayesian clustering analysis to determine structure among 5 spawning aggregations. Shallow genetic structure was found, separating the southernmost spawning aggregate from the remainder. Second, we used the results from the structure analysis and local water circulation patterns to delineate 3 distinct models of gene flow. The best-supported model, in which the southernmost spawning aggregate formed one group and all other spawning aggregates were nested into a second group, was the one that was consistent with water circulation during the species’ spawning season. Larval retention within a seasonal anticyclonic gyre that formed during the gulf coney’s spawning season may be responsible for the patterns found. This study highlights the importance of local oceanographic conditions in dictating the structure among spawning aggregations even at small geographic scales and contributes to informed management plans for this overexploited grouper.
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Mar Ecol Prog Ser
Vol. 499: 193–201, 2014
doi: 10.3354/meps10637 Published March 3
Knowledge of how genetic variation is partitioned
in the ocean is fundamental for understanding the
ecology, conservation and management of marine
resources (Mora & Sale 2002, Gell & Roberts 2003,
Cowen et al. 2007, Francis et al. 2007, Planes et
al. 2009). One of the strongest drivers of genetic struc-
ture is connectivity, i.e. the demographic linking of lo-
cal populations via the dispersal of larvae, juveniles
or adults (Sale et al. 2005), which influences almost
all ecological and evolutionary processes in meta -
populations (Hanski & Gaggiotti 2004). Genetic
connectivity has been shown across a range of geo-
graphical scales among different marine taxa, ranging
from virtually panmictic throughout considerably
large geographic ranges (Bowen et al. 2001, Lessios et
al. 2003, Klanten et al. 2007, Beldade et al. 2009, Leray
© Inter-Research 2014 ·*Corresponding author:
Genetic structure among spawning aggregations of
the gulf coney Hyporthodus acanthistius
Ricardo Beldade1, 2, 3, 4,*, Alexis M. Jackson1, Richard Cudney-Bueno5, 6,
Peter T. Raimondi1, Giacomo Bernardi1
1Department of Ecology and Evolutionary Biology, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz,
California 95060, USA
2USR 3278 CRIOBE, CNRS EPHE, CBETM de l’Université de Perpignan, 66860 Perpignan Cedex, France
3Laboratoire d’excellence ‘Corail’, USR 3278 CRIOBE CNRS-EPHE, 66860 Perpignan Cedex, France
4Universidade de Lisboa, Faculdade de Ciências, Centro de Oceanografia, Campo Grande, 1749-016 Lisboa, Portugal
5School of Natural Resources and the Environment, University of Arizona, Biological Sciences East, Room 325, Tucson,
Arizona 85721, USA
6Institute of Marine Sciences, University of California Santa Cruz, 100 Shaffer Road, Santa Cruz, California 95060, USA
ABSTRACT: Many large groupers form spawning aggregations, returning to the same spawning
sites in consecutive spawning seasons. Connectivity between spawning aggregations is thus
assured by larval dispersal. This study looks into the genetic structure and gene flow among
spawning aggregations of a large grouper, the gulf coney Hyporthodus acanthistius, in the north-
ern Gulf of California. First, using the mitochondrial control region and 11 microsatellites, we cal-
culated FST metrics and conducted a Bayesian clustering analysis to determine structure among
5 spawning aggregations. Shallow genetic structure was found, separating the southernmost
spawning aggregate from the remainder. Second, we used the results from the structure analysis
and local water circulation patterns to delineate 3 distinct models of gene flow. The best-sup-
ported model, in which the southernmost spawning aggregate formed one group and all other
spawning aggregates were nested into a second group, was the one that was consistent with
water circulation during the species’ spawning season. Larval retention within a seasonal anti -
cyclonic gyre that formed during the gulf coney’s spawning season may be responsible for the pat-
terns found. This study highlights the importance of local oceanographic conditions in dictating
the structure among spawning aggregations even at small geographic scales and contributes to
informed management plans for this overexploited grouper.
KEY WORDS: Grouper · Dispersal · Connectivity · Sea of Cortez · Oceanography · Eddies ·
Retention · Migration models · Rooster hind · Epinephelus
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 499: 193–201, 2014
et al. 2010) to clearly structured populations at very
small scales (Sotka et al. 2004, Bernardi 2005, Barber
et al. 2006, Gerlach et al. 2007, Beldade et al. 2012).
Many fish form spawning aggregations (i.e. groups
of conspecific fish that gather for the purpose of
spawning, with densities or numbers significantly
higher than those found in the area of aggregation
during non-reproductive periods; Domeier & Colin
1997), including groupers, snappers, jacks, surgeon-
fishes, damselfishes and parrotfishes (Sala et al.
2003, Erisman et al. 2007, Gladstone 2007, Sadovy
de Mitcheson et al. 2008, Gerhardinger et al. 2009).
Some groupers return to the same spawning sites in
consecutive spawning seasons (Sala et al. 2001, Starr
et al. 2007), in some cases covering large distances
to do so (Bolden 2000). If adult spawning aggrega-
tion site fidelity is indeed ubiquitous among large
groupers, then the dispersal of the pelagic larval
stages that are subjected to transport by ocean cur-
rents should be the main driver of genetic connec -
tivity. Two elements underline the importance of
oceanographic characteristics to the dispersal of
spawning aggregation offspring. First, the specific
location of spawning aggregations appears to maxi-
mize the rapid advection of eggs and larvae away
from the reef environment (e.g. Choat 2012, Colin
2012a). Second, knowledge of the onset of sensorial
and swimming abilities of pelagic larvae, which in
the case of groupers is still largely unknown, is
essential to understand how larval abilities might
steer the dispersal process (e.g. Colin 2012b, Hamner
& Largier 2012). Larval abundance and even the
magnitude of recruitment events appear to be corre-
lated with oceanographic and climatic parameters,
such as temperature, salinity and depth (but see e.g.
Aburto-Oropeza et al. 2010, Marancik et al. 2012).
The northern Gulf of California (NGC) is home to
several fishes that aggregate to spawn and is part of
one of the most productive marine ecosystems in
the world, contributing most of Mexico’s fishery re -
sources (Arvizu-Martínez 1987, Lluch-Cota et al.
2007, Erisman et al. 2012). The NGC covers a rela-
tively small area extending from the Colorado delta
in the north to Bahia de Los Angeles and Isla Tiburon
in the south (Fig. 1). In this region, in-depth know -
ledge of water circulation patterns and other geomor-
phological characteristics (Fig. 1) provide a unique
opportunity to describe genetic structure and test
models of gene flow in locally occurring species. In
the NGC, the main oceanographic features comprise
intense tidal mixing (Argote et al. 1995) and a sea-
sonally reversing gyre, anticyclonic in summer (June
to September) (Fig. 1B) and cyclonic in winter
(Fig. 1C) (Lavín et al. 1997, Marinone et al. 2008);
strong coastal currents along the eastern Sonora
coastline (Peguero-Icaza et al. 2011); and small resid-
ual currents and small eddies in the upper gulf (Mari-
none et al. 2011). These characteristics are likely to
influence the transport of larvae in the NGC (Mari-
none et al. 2004, Cudney-Bueno et al. 2009). Both
local water circulation and bottom geomorphologic
characteristics may have important implications for
the formation of spawning aggregations as well as for
the fate of eggs or larvae released there (Cherubin et
al. 2011, Karnauskas et al. 2011). In the NGC, there
are 2 deep basins, the Delfin Basin (800 m) and the
Wagner Basin (200 m), and several sills (Lavín et al.
1997) whose putative part in limiting dispersal of lar-
vae or concentrating prey for early larval stages
remains unclear (e.g. Karnauskas et al. 2011).
The gulf coney Hyporthodus acanthistius (formerly
Epinephelus acanthistius; Craig & Hastings 2007) is a
Fig. 1. Northern Gulf of California (NGC) including (A) bathymetry (depth in meters) and named sampled spawning aggrega-
tions of the gulf coney Hyporthodus acanthistius (PLI, Puerto Libertad; PLO, Puerto Lobos; STO, Santo Tomas; PPE, Puerto
Peñasco; and SLG, San Luiz Gonzaga); (B) ocean circulation in the summer (only the month of July is represented); and (C) in
the winter (only the month of January is represented). Ocean circulation reproduced from Marinone (2003) by permission of the
American Geophysical Union
Beldade et al.: Genetic structure among grouper spawning aggregations
tropical and subtropical large grouper that occurs
from southern California to Peru (Heemstra & Ran-
dall 1993), including the Gulf of California (or Sea of
Cortez) (Cudney-Bueno & Turk-Boyer 1998, Aburto-
Oropeza et al. 2008). It is found at depths greater
than ~45 m usually in silty areas adjacent to rocky
reefs (Thomson et al. 2000), and spawns in aggre -
gations on muddy bottoms during the spring and
summer months (Cudney-Bueno & Turk-Boyer 1998).
During the spawning period, artisanal fishermen
heavily target this species (Aburto-Oropeza et al.
2008). Indeed, the high commercial value and tempo-
ral and spatial predictability of their mass gatherings
make groupers a prime target for fisheries. Despite
its present ‘Least Concern’ conservation status (IUCN
2012), the abundance of the gulf coney in the NGC
has been rapidly declining over the past 2 decades
(Aburto-Oropeza et al. 2008). Elsewhere, there are
many examples of collapsed grouper spawning
aggregations because of overfishing such as the Nas-
sau grouper E. striatus (e.g. Sala et al. 2001, Aguilar-
Perera 2006) and the gulf grouper Mycteroperca jor-
dani (Sáenz-Arroyo et al. 2005). Given the threat of
overfishing to fish that form spawning aggregations
(Sadovy de Mitcheson et al. 2013), it is imperative to
provide connectivity data to devise informed man-
agement plans.
In this study, we integrate molecular evidence from
highly variable molecular markers (control region
and 11 microsatellites) to assess genetic structure
and connectivity among spawning aggregations of
the gulf coney in the NGC. Oceanographic and geo-
morphological regional characteristics are used to
delineate particular models of gene flow across the
spawning aggregation network. This study provides
essential information for the management and re -
covery of this threatened fishery in the NGC.
Sampling and DNA extraction
Fin clips of Hyporthodus acanthistius were collected
in 2003 aboard fishing boats that operated at 5 spawn-
ing locations in the NGC: Puerto Libertad, Puerto
Lobos, Santo Tomás, Puerto Peñasco, and San Luiz
Gonzaga (Fig. 1). Immediately after collection, fin
clips were placed in 95% ethanol and stored at ambi-
ent temperature in the field and then at 4°C in the lab.
Total genomic DNA was extracted from 20 mg of fin
tissue by Proteinase K digestion in lysis buffer (10 mM
Tris, 400 mM NaCl, 2 mM EDTA, 1% sodium dodecyl
sulfate) overnight at 55°C. This was followed by
purification using phenol/chloroform ex tractions and
alcohol precipitation (Sambrook et al. 1989).
mtDNA and microsatellites
We amplified the 5’ end of the hyper-variable por-
tion of the mitochondrial control region using the
universal primers CR-A and CR-E (Lee et al. 1995).
Each 100 µl reaction contained 10 to 100 ng of DNA,
10 mM Tris HCl (pH 8.3), 50 mM KCl, 1.5 mM MgCl2,
2.5 units of Taq DNA polymerase (Perkin-Elmer),
150 mM of each dNTP, and 0.3 mM of each primer
and was amplified with a cycling profile of 45 s at
94°C, 1 min at 52°C and 1 min at 72°C for 35 cycles.
After purification of amplified DNA genes following
the manufacturer’s protocol (ABI, Perkin-Elmer), we
sequenced on an ABI 3100 automated sequencer
(Applied Biosystems).
All individuals were genotyped for 13 microsatel-
lites following protocols described in Molecular Eco -
logy Resources Primer Development Consortium et
al. (2009). Each individual was genotyped using
GENE MAPPER 3.7 (Applied Biosystems). To estimate
potential genotyping errors, we re-amplified and re-
scored 21 randomly picked samples and evaluated
concordance between the first and second score.
Overall, the genotyping error rate was less than 2%,
which is reasonable for population differentiation
studies based on allele frequencies (Bonin et al. 2004),
and less than 2% of data were missing for any given
locus. Data were scanned for null alleles and stutter-
ing using MICROCHECKER 2.2.3 (van Oosterhout et
al. 2004) and for deviations from Hardy-Weinberg
equilibrium (HWE) and linkage disequilibrium after
10 000 permutations using ARLEQUIN 3.5 (Excoffier
& Lischer 2010). Two micro satellites, EAC_ A08 and
EAC_B08, were dropped from the ana lysis because of
the putative presence of null alleles.
Genetic diversity and genetic structure among
spawning aggregations
Genetic diversity measures for each population
including number of haplotypes, haplotype diver-
sity and nucleotide diversity were calculated with
DNAsp 5 (Librado & Rozas 2009). To assess popula-
tion structure, we used 2 separate approaches. In the
first, more classical approach, fixation indices (FST)
relying on allele frequencies were calculated using
ARLEQUIN 3.5 (Excoffier & Lischer 2010). We calcu-
Mar Ecol Prog Ser 499: 193–201, 2014
lated 95% confidence intervals around the FST esti-
mates using GDA 1.1 (Lewis & Zaykin 2001), rather
than just p-values, as these may not be good indica-
tors of differentiation between populations and are
dependent on sample size and variability (Jost 2008).
In the second approach, we used a Bayesian model-
based clustering method using microsatellite data im -
plemented in STRUCTURE 2.3.2 (Falush et al. 2007).
STRUCTURE assumes that there are knumber of
groups within which samples have compatible multi-
locus genotypes. Convergence of parameters (α, Fand
likelihood) in preliminary runs was used to deter-
mine the burn-in (500 000) and length (1 000 000) of
each run. For our analysis, we used an admixture
model, which allows individuals to have mixed
ancestry, and added sampling location as a weak
prior (Falush et al. 2007). Then we performed 10
replicate runs for each cluster kvarying between 1
and 6. To determine the correct number of clusters
in the sample, we followed Evanno et al. (2005), who
proposed the use of an ad hoc statistic Δkbased on
the rate of change in the log probability of data
between successive kvalues. STRUCTURE HAR-
VESTER was used to calculate Evanno’s Δkand illus-
trate the differences in likelihood and Δkfor each k
(Earl & VonHoldt 2012). A Q plot was chosen to illus-
trate differences between populations, where each
single vertical line (representing 1 individual) is par-
titioned into k-colored segments that represent that
indi vidual’s estimated membership fraction in each
of the k-inferred clusters (Pritchard et al. 2000).
Direction and magnitude of gene flow among
spawning aggregations
To determine the pervasive migration pattern in
the study area, we used MIGRATE-N 3.2.16 (Beerli
& Palczewski 2010) to contrast 3 migration models.
In all 3 models, spawning aggregates were nested
according to the genetic structure suggested by the
FST and structure analysis. Based on well-described
local oceanographic circulation, we defined the di -
rection of gene flow for each model as follows: (1) an
unrestricted full migration model, (2) a model consid-
ering 2 population sizes and unidirectional north-
ward gene flow and (3) a model considering 2 pop -
ulation sizes and unidirectional southward gene
flow. Model 2 was delineated taking into account
that Hyporthodus acanthistius spawns in the spring-
summer, during which time anticyclonic circulation
forces the water to flow northward on the eastern
side of the NGC (see Fig. 1B) (Marinone 2012). Model
3 depicts the autumn-winter cyclonic water circula-
tion pattern, which forces the water to flow south-
ward (see Fig. 1C) (Marinone 2012).
MIGRATE-N provides the ratio of the marginal
likelihoods (Bayes factors) of each model, which can
subsequently be compared to select the most sup-
ported model (Beerli & Palczewski 2010). The best-
supported model will have the highest log Bayes fac-
tors. This approach is particularly suited to our data
because local hydrodynamics allow for a clear expec-
tation of unidirectional gene flow in the study area
and the nesting of aggregates reduces the number
of parameters to be estimated from the data, thus
increasing the power of the approach. A random sub-
set of 30 samples from each of the 2 populations
identified previously was used to compare the mod-
els. The mitochondrial locus was not used to test the
models of gene flow because of its limited capability,
as it is a single locus, for distinguishing the models.
A series of preliminary runs using Model 1, the
unrestricted model, were used to determine con -
vergence of posterior probabilities for each of the
parameters. Running conditions chosen included
1 000 000 recorded steps, 10 long chains and 15
heated chains, a static heating scheme with the
inverse of the temperature regularly spaced between
0 and 1 and a tree swapping interval of one; finally,
the upper prior boundary for northward migration
was set to vary between 0 and 10 000. The natural
logarithm of Bayes factors with a Bezier approxima-
tion was calculated following Beerli & Palczewski
(2010) as well as each model’s probability by dividing
each marginal likelihood by the sum of the marginal
likelihoods of both models used. The best-supported
model will be the one with the highest probability
(Beerli & Palczewski 2010).
Genetic diversity
We obtained 232 sequences for a 361 bp frag -
ment of the mitochondrial control region (Genbank
KF425014 to KF425245). The sequences analyzed
here had 133 polymorphic sites, 54 of which were
informative. Genetic diversity was high for almost all
spawning aggregations (Table 1). Genetic diversity
was also calculated for the microsatellites from 246
individuals and included number of alleles, ratio of
homozygotes to heterozygotes per locus, as well as
HWE tests (Table S1 in the Supplement, available at
Beldade et al.: Genetic structure among grouper spawning aggregations
Genetic structure of spawning aggregations
Low pairwise FST values were found across both
genetic markers (Table 2). In spite of the significant
differences found between pairs of FST estimates
derived from microsatellites, 95% confidence inter-
vals precluded any conclusion regarding the struc-
ture between Puerto Libertad and either Santo
Tomás or Puerto Peñasco population pairs (Table 2).
Differentiation between the southernmost aggrega-
tion of Puerto Libertad and the remaining aggrega-
tions was identified through the Bayesian clustering
method (Fig. 2). Evanno’s Δkbased on the mean and
standard deviation of likelihoods, L(k), for each kwas
highest for k= 2 (Fig. 3), confirming that k= 2 is the
best representation of the genetic partitioning in the
data. Assessment of convergence examples of skyline
plots of log(α) are given in the Supplement (Fig. S1).
Gene flow between spawning aggregations
Model 2 was the most supported migration model,
as demonstrated by the highest value for the natural
logarithm of the Bayes’ factors (Table 3). Estimates
of population size and number of migrants between
the defined populations as well as parameter conver-
gence are given in the Supplement (Table S2). Our
analysis aligns well with the summer anticyclonic
gyre used to delineate Model 2, which is consistent
with both magnitude and direction of the gulf coney’s
gene flow in the NGC. This
period coincides with the
pelagic phase of the Hypor -
tho dus acan thistius larvae.
The full migration model
comes second to Model 2
because of the unrestricted
mi gra tion between the pop-
ulations to the north of
Puerto Libertad. Finally,
Model 3, in which gene flow
follows the winter cyclonic
water movement patterns
described for the area,
scored the lowest in ex -
plaining larval mi gration in
the area.
Sampling site n nhhdπ
Puerto Libertad 53 18 0.839 0.0061
Puerto Lobos 62 27 0.911 0.0072
Santo Tomás 21 10 0.914 0.0068
Puerto Peñasco 55 17 0.902 0.0061
San Luiz Gonzaga 41 16 0.871 0.0065
Total 232 47 0.886 0.0066
Table 1. Collection sites, number of mitochondrial control
region sequences used (n) and molecular diversity indices
(number of haplotypes, nh; haplotype diversity, hd; and
nucleotide diversity, π) for Hyporthodus acanthistius
PLI 0.003 0.003 0.002 0.005
[0.000 to 0.007] [−0.005 to 0.009] [0.000 to 0.018] [0.002 to 0.020]
PLO 0.04254 0 0.001 0.003
[−0.001 to 0.009] [−0.003 to 0.003] [−0.001 to 0.005]
STO 0.03838 0.00049 −0.003 −0.005
[−0.005 to 0.001] [−0.008 to −0.002]
PPE 0.07154 0.00045 0.0052 −0.001
[−0.003 to 0.002]
SLG 0.00561 0.01327 0.01133 0.02289
Table 2. Population structure estimated by FST between Hyporthodus acanthistius popu-
lations calculated from the mitochondrial control region (below left) and from 11 mi-
crosatellites (above right) with 95% confidence intervals between brackets. Significant
pairwise FST (at p < 0.05) after 10 000 permutations shown in bold. PLI, Puerto Libertad;
PLO, Puerto Lobos; STO, Santo Tomás; PPE, Puerto Peñasco; SLG, San Luiz Gonzaga
Fig. 2. Q-plot of the Bayesian population assignment test based on 11 microsatellite loci. Each vertical line represents a single
Hyporthodus acanthistius individual; black/gray in each vertical line represent the likelihood of belonging to each of the
clusters. Black vertical lines separate the spawning aggregations; population acronyms are defined in Fig. 1
Mar Ecol Prog Ser 499: 193–201, 2014
Genetic structure, hydrodynamics and site fidelity
In groupers, genetic differentiation of spawning
aggregations has been observed but usually at large
geographic scales (e.g. Rhodes et al. 2003, Rivera et
al. 2004, Zatcoff et al. 2004). In this study, FST statistics
based on mtDNA and microsatellites as well as
Bayesian analysis were consistent in showing weak
structure at a much smaller scale. In scenarios of weak
genetic partitioning, FST metrics and Bayesian analysis
have limited power in asserting structure (e.g. Waples
& Gaggiotti 2006). In the present study, the inclusion
of zero within the calculated FST 95% confidence in-
tervals for 2 of the pairwise comparisons between
Puerto Libertad and the other populations, and the
limited capacity for Evanno’s Δkto distinguish be-
tween a panmictic population (k= 1) and the genetic
structure suggested (k= 2) as well as similar posterior
probabilities for the same kvalues, have to be ac-
knowledged. Nonetheless, the concordance between
markers and analysis in showing that within the NGC,
the southernmost spawning aggregation sampled,
Puerto Libertad, was slightly distinct from all others
lends support to this conclusion. Hence, we present
evidence for structure between spawning aggrega-
tions at a small geographic scale. Furthermore, while
unimportant over evolutionary time scales, weak ge-
netic structure can have important implications in
ecology and conservation biology (Jones & Wang 2012).
Given that the NGC covers such a small geo-
graphic area, it was unexpected to observe even
weak population structure among spawning aggrega-
tions that are so close geographically. The spawning
aggregation at Puerto Libertad was only 40 km from
the closest spawning aggregation at Puerto Lobos.
Hydrodynamic features of the study area during the
dispersive stage of the gulf coney’s larvae are also
consistent with our results, as the southernmost
spawning aggregation is the only one that sits just
outside of the summer anticyclonic gyre. This sea-
sonal gyre may trap the larvae originating from all
other spawning aggregations, preventing them from
travelling south. Eddies may entrap fish eggs and
larvae both in the open ocean (e.g. Holliday et al.
2011) and in enclosed seas (e.g. Contreras-Catala et
al. 2012). Simultaneously, the northward currents
described for the Puerto Libertad spawning aggrega-
tion site will transport larvae northward. The genetic
differentiation of Puerto Libertad may also be recon-
ciled with some level of site fidelity. While there are
no published accounts of site fidelity or home range
for Hyporthodus acanthistius, several grouper spe-
cies such as Epinephelus tauvina (Kaunda-Arara &
Rose 2004) have some degree of site fidelity. Other
examples have come from tagging studies of E. stria-
tus, in which distances traveled to spawning sites
ranged from 30 km (Sala et al. 2001) to upwards of
100 km (Carter et al. 1994, Bolden 2000). Movement
at even the smallest of these scales could be very rel-
evant within the NGC. The potential homogenizing
effects of dispersing larvae are best explained by the
study of gene flow.
Gulf coney’s gene flow in the NGC
The most supported model for the genetic ex -
change among spawning aggregations of gulf coney
Model No. Bezier Harmonic Choice Model
lmL lML (Bezier) probability
1 −4482.37 −4297.46 2 0.000
2 −4353.63 −4134.17 1 1.000
3 −5018.29 −4871.79 3 0.000
Table 3. Natural log Bayes factors (lmL) and log marginal
likelihoods (lML) for each gene flow model estimated by
thermodynamic integration using 11 microsatellite markers.
Model details are explained in ‘Materials and methods’
Fig. 3. Mean and standard deviation of log likelihoods, L(k)
(d); and Evanno’s Δk(j) for each kvalue estimated in 10 in-
dependent runs in STRUCTURE. The highest Δkindicates
the choice of k= 2 as the one that best describes the genetic
partitioning in the data
Beldade et al.: Genetic structure among grouper spawning aggregations
depicts the anticyclonic summer gyre, which coin-
cides with the pelagic stage of this species’ larvae. In
the NGC, using a 3-dimensional baroclinic numerical
model, Marinone et al. (2008) followed particles re -
leased in this gyre and found the same south-north
direction of dispersal. Calderon-Aguillera et al. (2003)
showed how hydrodynamics in the NGC influenced
the dispersal of blue shrimp Litopenaeus stylirostris
larvae and more recently Cudney-Bueno et al. (2009)
reported similar circulation patterns and enhanced
recruitment of rock scallop Spondyllus calcifer larvae
and black murex Hexaplex nigritus larvae coming
from the south of the NGC and settling into marine
reserves located to the north. The currents along the
eastern shore of the NGC may reach speeds of up to
0.06 m s–1 during the summer (Cudney-Bueno et al.
2009), which, considering a planktonic larval dura-
tion of approximately 30 d for the gulf coney in the
NGC (K. Rowell, Biology Department, University of
Washington, pers. comm.), would easily allow them
to disperse between adjoining spawning aggre gates
and even beyond. Within 4 wk, larvae may travel the
148 km distance that separates Puerto Libertad and
Puerto Peñasco, the southernmost and northernmost
spawning aggregations.
Management of spawning aggregations
Our study highlights the importance of detailing
the genetic structure and gene flow between spawn-
ing aggregations even at small geographic scales
where panmixia is expected. The weak genetic
structure found here can have important implications
in ecology and conservation biology of this species.
Management programs for the gulf coney in the
NGC should reinforce protection of the southernmost
spawning aggregation near Puerto Libertad. Both
shallow genetic structure and an anticyclonic direc-
tion of gene flow suggest that Puerto Libertad is a
source population, primarily exporting larvae north
into the NGC. Oceanographic data suggest that
Puerto Libertad may also play an important role as a
gateway for larvae and gene flow originating from
the middle gulf (e.g. Danell-Jiménez et al. 2009). If
this pattern proves to be true, overfishing in the mid-
dle gulf region may have dire consequences for the
populations in the NGC.
Acknowledgements. We thank the Intercultural Center for
the Study of Deserts and Oceans (CEDO), especially R.
Loiaza, I. Martinez and A. Sanchez; as well as Community
and Biodiversity, AC (COBI) especially N. Encinas, C.
Moreno and M. Rojo. We also thank 2 anonymous reviewers
who provided helpful comments on an earlier version of
the manuscript. Funding for this study was provided by the
David and Lucile Packard Foundation, grant award #2008-
32210. R.B. was also funded by the Fundação para a Ciência
e a Tecnologia (SFRH/BPD/26901/2006). Collecting permits
for this study were issued by SAGARPA under the National
Commission for Aquaculture and Fisheries, permit #2885.
This is a scientific contribution to the PANGAS project (www.
Aburto-Oropeza O, Erisman B, Valdez-Ornelas V, Dane-
mann G (2008) Commercially important serranid fishes
from the Gulf of California: ecology, fisheries and conser-
vation. Pronatura, Ciencia y Conservation: 1−44
Aburto-Oropeza O, Paredes G, Mascareñas-Osorio I, Sala E
(2010) Climatic influence on reef fish recruitment and
fisheries. Mar Ecol Prog Ser 410: 283−287
Aguilar-Perera A (2006) Disappearance of a Nassau grouper
spawning aggregation off the southern Mexican Carib -
bean coast. Mar Ecol Prog Ser 327: 289−296
Argote ML, Amador A, Lavín MF, Hunter JR (1995) Tidal
dissipation and stratification in the Gulf of California.
J Geophys Res 100: 16103−16118
Arvizu-Martínez J (1987) Fisheries activities in the Gulf of
California. CalCOFI Report, XXVIII
Barber PH, Erdmann MV, Palumbi SR (2006) Comparative
phylogeography of three codistributed stomatopods: ori-
gins and timing of regional lineage diversification in the
coral triangle. Evolution 60: 1825−1839
Beerli P, Palczewski M (2010) Unified framework to evaluate
panmixia and migration direction among multiple sam-
pling locations. Genetics 185: 313−326
Beldade R, Heiser JB, Robertson R, Gasparini JL, Floeter SR,
Bernardi G (2009) Historical biogeography and specia-
tion in the Creole wrasses (Labridae, Clepticus). Mar Biol
156: 679−687
Beldade R, Holbrook SJ, Schmitt RJ, Planes S, Malone D,
Bernardi G (2012) Larger female fish contribute dispro-
portionately more to self-replenishment. Proc R Soc Lond
B Biol Sci 279: 2116−2121
Bernardi G (2005) Phylogeography and demography of sym-
patric sister surfperch species, Embiotoca jacksoni and
E. lateralis along the California coast: historical and eco-
logical factors. Evolution 59: 386−394
Bolden S (2000) Long-distance movement of a Nassau
grouper (Epinephelus striatus) to a spawning aggrega-
tion in the central Bahamas. Fish Bull 98: 642−645
Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F,
Brochmann C, Taberlet P (2004) How to track and assess
genotyping errors in population genetics studies. Mol
Ecol 13: 3261−3273
Bowen W, Bass AL, Rocha LA, Grant WS, Robertson DR
(2001) Phylogeography of the trumpetfishes (Aulosto-
mus): ring species complex on a global scale. Evolution
55: 1029−1039
Calderon-Aguilera L, Marinone SG, Arago EA (2003) Influ-
ence of oceanographic processes on the early life stages
of the blue shrimp (Litopenaeus stylirostris) in the upper
Gulf of California. J Mar Sci 39: 117−128
Carter J, Marrow G, Pryor V (1994) Aspects of the ecology
and reproduction of Nassau grouper, Epinephelus stria-
Mar Ecol Prog Ser 499: 193–201, 2014
tus, off the coast of Belize, Central America. Annu Proc
Gulf Caribb Fish Inst 43: 65−111
Cherubin LM, Nemeth RS, Idrisi N (2011) Flow and trans-
port characteristics at an Epinephelus guttatus (red hind
grouper) spawning aggregation site in St. Thomas (US
Virgin Islands). Ecol Model 222: 3132−3148
Choat JH (2012) Spawning aggregations in reef fishes; eco-
logical and evolutionary processes. In: Sadovy de Mitch-
eson Y, Colin PL (eds) Reef fish spawning aggregations:
biology, research and management. Springer Nether-
lands, Dordrecht, p 85−116
Colin PL (2012a) Timing and location of aggregation and
spawning in reef fishes. In: Sadovy de Mitcheson Y,
Colin PL (eds) Reef fish spawning aggregations: bio l-
ogy, research and management. Springer Netherlands,
Dordrecht, p 117−158
Colin PL (2012b) Aggregation spawning: biological aspects
of the early life history. In: Sadovy de Mitcheson Y, Colin
PL (eds) Reef fish spawning aggregations: biology,
research and management. Springer Netherlands, Dor-
drecht, p 191−224
Contreras-Catala F, Sanchez-Velasco L, Lavín MF, Godinez
VM (2012) Three-dimensional distribution of larval fish
assemblages in an anticyclonic eddy in a semi-enclosed
sea (Gulf of California). J Plankton Res 34: 548−562
Cowen RK, Gawarkiewicz G, Pineda J, Thorrold SR, Werner
FE (2007) Population connectivity in marine systems.
Oceanography 20: 14−21
Craig MT, Hastings PA (2007) A molecular phylogeny of the
groupers of the subfamily Epinephelinae (Serranidae)
with a revised classification of the Epinephelini. Ichthyol
Res 54: 1−17
Cudney-Bueno R, Turk-Boyer PJ (1998) Pescando entre
mareas del Alto Golfo de California: una guia sobre la
pesca artesanal, su gente y sus propuestas de manejo.
Centro Intercultural des Estudios de Desiertos y Oce -
anos, Puerto Penasco, Sonora
Cudney-Bueno R, Lavín MF, Marinone SG, Raimondi PT,
Shaw WW (2009) Rapid effects of marine reserves via
larval dispersal. PLoS ONE 4: e4140
Danell-Jiménez A, Sánchez-Velasco L, Lavín MF, Marinone
SG (2009) Three-dimensional distribution of larval fish
assemblages across a surface thermal / chlorophyll
front in a semienclosed sea. Estuar Coast Shelf Sci 85:
Domeier ML, Colin PL (1997) Tropical reef fish spawning
aggregations: defined and reviewed. Bull Mar Sci 60:
Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a
website and program for visualizing STRUCTURE output
and implementing the Evanno method. Conserv Genet
Resour 4: 359−361
Erisman BE, Buckhorn ML, Hastings PA (2007) Spawning
patterns in the Leopard grouper, Mycteroperca rosacea,
in comparison with other aggregating groupers. Mar Biol
151: 1849−1861
Erisman B, Aburto-Oropeza O, Gonzalez-Abraham C, Mas-
careñas-Osorio I, Moreno-Báez M, Hastings PA (2012)
Spatio-temporal dynamics of a fish spawning aggrega-
tion and its fishery in the Gulf of California. Sci Rep 2: 284
Evanno G, Regnaut S, Goudet J (2005) Detecting the num-
ber of clusters of individuals using the software STRUC-
TURE: a simulation study. Mol Ecol 14: 2611−2620
Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new
series of programs to perform population genetics ana -
lyses under Linux and Windows. Mol Ecol Resour 10:
Falush D, Stephens M, Pritchard JK (2007) Inference of pop-
ulation structure using multilocus genotype data: domi-
nant markers and null alleles. Mol Ecol Notes 7: 574−578
Francis RC, Hixon MA, Clarke ME, Murawski SA, Ralston S
(2007) Ten commandments for ecosystem-based fisheries
scientists. Fisheries 32: 217−233
Gell FR, Roberts CM (2003) Benefits beyond boundaries: the
fishery effects of marine reserves. Trends Ecol Evol 18:
Gerhardinger LC, Hostim-Silva M, Medeiros RP, Matarezi J,
Bertoncini ÁA, Freitas MO, Ferreira BP (2009) Fishers’
resource mapping and goliath grouper Epinephelus ita-
jara (Serranidae) conservation in Brazil. Neotrop Ichthyol
7: 93−102
Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V
(2007) Smelling home can prevent dispersal of reef fish
larvae. Proc Natl Acad Sci USA 104: 858−863
Gladstone W (2007) Selection of a spawning aggregation
site by Chromis hypsilepis (Pisces: Pomacentridae): habi-
tat structure, transport potential, and food availability.
Mar Ecol Prog Ser 351: 235−247
Hamner WM, Largier JL (2012) Oceanography of the plank-
tonic stages of aggregation spawning reef fishes. In:
Sadovy de Mitcheson Y, Colin PL (eds) Reef fish spawn-
ing aggregations: biology, research and management.
Springer Netherlands, Dordrecht, p 159−190
Hanski I, Gaggiotti O (2004) Metapopulation biology: past,
present and future. In: Hanski I, Gaggiotti O (eds) Eco -
logy, genetics and evolution of metapopulations. Elsevier
Academic Press, London, p 3−22
Heemstra PC, Randall JE (1993) FAO species catalogue, Vol
16: Groupers of the world (family Serranidae, subfamily
Epinephelinae). FAO Fish Synop 125: 102−103
Holliday D, Beckley LE, Olivar MP (2011) Incorporation of
larval fishes into a developing anti-cyclonic eddy of the
Leeuwin Current off south-western Australia. J Plankton
Res 33: 1696−1708
Jones OR, Wang J (2012) A comparison of four methods for
detecting weak genetic structure from marker data. Ecol
Evol 2: 1048−55
Jost L (2008) GST and its relatives do not measure differenti-
ation. Mol Ecol 17: 4015−4026
Karnauskas M, Chérubin LM, Paris CB (2011) Adaptive sig-
nificance of the formation of multi-species fish spawning
aggregations near submerged capes. PLoS ONE 6:
Kaunda-Arara B, Rose GA (2004) Homing and site fidelity in
the greasy grouper Epinephelus tauvina (Serranidae)
within a marine protected area in coastal Kenya. Mar
Ecol Prog Ser 277: 245−251
Klanten OS, Choat JH, Herwerden L (2007) Extreme genetic
diversity and temporal rather than spatial partitioning in
a widely distributed coral reef fish. Mar Biol 150: 659−670
Lavín MF, Durazo R, Palacios E, Argote ML, Carrillo L (1997)
Lagrangian observations of the circulation in the north-
ern Gulf of California. J Phys Oceanogr 27: 2298−2305
Lee WJ, Conroy J, Howell WH, Kocher T (1995) Structure
and evolution of teleost mitochondrial control regions.
J Mol Evol 41: 54−66
Leray M, Beldade R, Holbrook SJ, Schmitt RJ, Planes S,
Bernardi G (2010) Allopatric divergence and speciation
in coral reef fish: the three-spot dascyllus, Dascyllus tri-
maculatus, species complex. Evolution 64: 1218−1230
Beldade et al.: Genetic structure among grouper spawning aggregations
Lessios HA, Kane J, Robertson DR (2003) Phylogeography of
the pantropical sea urchin Tripneustes: contrasting pat-
terns of population structure between oceans. Evolution
57: 2026−2036
Lewis PO, Zaykin D 2001. Genetic data analysis: computer
program for the analysis of allelic data. Version 1.1. Avail-
able at http: // software.
Librado P, Rozas J (2009) DnaSP v5: a software for com -
prehensive analysis of DNA polymorphism data. Bio -
informatics 25: 1451−1452
Lluch-Cota SE, Aragón-Noriega EA, Arreguín-Sánchez F,
Aurioles-Gamboa D and others (2007) The Gulf of Cali-
fornia: review of ecosystem status and sustainability
challenges. Prog Oceanogr 73: 1−26
Marancik K, Richardson D, Lyczkowski-Shultz J, Cowen R,
Konieczna M (2012) Spatial and temporal distribution of
grouper larvae (Serranidae: Epinephelinae: Epineph-
elini) in the Gulf of Mexico and Straits of Florida. Fish
Bull 110: 1−20
Marinone SG (2003) A three-dimensional model of the mean
and seasonal circulation of the Gulf of California. J Geo-
phys Res 108:3325, doi: 10.1029/2002JC001720
Marinone SG (2012) Seasonal surface connectivity in the
Gulf of California. Estuar Coast Shelf Sci 100: 133−141
Marinone SG, Gutierrez OQ, Parés-Sierra A (2004) Numeri-
cal simulation of California, larval shrimp dispersion in
the northern region of the Gulf of California. Estuar
Coast Shelf Sci 60: 611−617
Marinone SG, Ulloa MJ, Parés-Sierra A, Lavin M, Cudney-
bueno R (2008) Connectivity in the northern Gulf of Cal-
ifornia from particle tracking in a three-dimensional
numerical model. J Mar Syst 71: 149−158
Marinone SG, Lavin M, Parés-Sierra A (2011) A quantitative
characterization of the seasonal Lagrangian circulation
of the Gulf of California from a three-dimensional
numerical model. Cont Shelf Res 31: 1420−1426
Molecular Ecology Resources Primer Development Consor-
tium, Abercrombie LG, Anderson CM, Baldwin BG and
others (2009) Permanent genetic resources added to
molecular ecology resources database 1 January 2009−
30 April 2009. Mol Ecol Resour 9: 1375−1379
Mora C, Sale PF (2002) Are populations of coral reef fish
open or closed? Trends Ecol Evol 17: 422−428
Peguero-Icaza M, Sanchez-Velasco L, Lavín MF, Marinone
SG, Beier E (2011) Seasonal changes in connectivity
routes among larval fish assemblages in a semi-enclosed
sea (Gulf of California). J Plankton Res 33: 517−533
Planes S, Jones GP, Thorrold SR (2009) Larval dispersal con-
nects fish populations in a network of marine protected
areas. Proc Natl Acad Sci USA 106:56935697
Pritchard JK, Stephens M, Donnelly P (2000) Inference of
population structure using multilocus genotype data.
Genetics 155: 945−959
Rhodes KL, Lewis RW, Chapman RI, Sadovy Y (2003) Genetic
structure of camouflage grouper, Epinephelus polyphe -
ka dion (Pisces: Serranidae), in the western central
Pacific. Mar Biol 142: 771−776
Rivera MAJ, Kelley CD, Roderick GK (2004) Subtle popula-
tion genetic structure in the Hawaiian grouper, Epine -
phelus quernus (Serranidae), as revealed by mitochondr-
ial DNA analyses. Biol J Linn Soc 81: 449−468
Sadovy de Mitcheson Y, Cornish A, Domeier M, Colin PL,
Russell M, Lindeman KC (2008) A global baseline for
spawning aggregations of reef fishes. Conserv Biol 22:
Sadovy de Mitcheson Y, Craig MT, Bertoncini AA, Carpen-
ter KE and others (2013) Fishing groupers towards
extinction: a global assessment of threats and extinction
risks in a billion dollar fishery. Fish Fish 14: 119−136
Sáenz-Arroyo A, Roberts CM, Torre J, Cariño-Olvera M,
Enríquez-Andrade RR (2005) Rapidly shifting environ-
mental baselines among fishers of the Gulf of California.
Proc R Soc Lond B Biol Sci 272: 1957−1962
Sala E, Ballesteros E, Starr RM (2001) Rapid decline of
Nassau grouper spawning aggregations in Belize: fish-
ery management and conservation needs. Fisheries 26:
Sala E, Aburto-Oropeza O, Paredes G, Thompson G (2003)
Spawning aggregations and reproductive behavior of
reef fishes in the Gulf of California. Bull Mar Sci 72:
Sale PF, Cowen RK, Danilowicz BS, Jones GP and others
(2005) Critical science gaps impede use of no-take fish-
ery reserves. Trends Ecol Evol 20: 74−80
Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning:
a laboratory manual, 2nd edn. Cold Spring Harbor Labo-
ratory, Cold Spring Harbor, NY
Sotka EE, Wares JP, Barth JA, Grosberg RK, Palumbi SR
(2004) Strong genetic clines and geographical variation
in gene flow in the rocky intertidal barnacle Balanus
glandula. Mol Ecol 13: 2143−2156
Starr RM, Sala E, Ballesteros E, Zabala M (2007) Spatial
dynamics of the Nassau grouper Epinephelus striatus in
a Caribbean atoll. Mar Ecol Prog Ser 343: 239−249
Thomson D, Findley L, Kerstitch A (2000) Reef fishes of
the Sea of Cortez, the rocky shore fishes of the Gulf of
California. University of Texas Press, Austin, TX
van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P
(2004) MICRO-CHECKER: software for identifying and
correcting genotyping errors in microsatellite data. Mol
Ecol Notes 4:535– 538
Waples RS, Gaggiotti O (2006) What is a population? An
empirical evaluation of some genetic methods for identi-
fying the number of gene pools and their degree of con-
nectivity. Mol Ecol 15: 1419−1439
Zatcoff MS, Ball O, Sedberry GR (2004) Population genetic
analysis of red grouper, Epinephelus morio, and scamp,
Mycteroperca phenax, from the southeastern U.S. Atlantic
and Gulf of Mexico. Mar Biol 144: 769−777
Editorial responsibility: Per Palsbøll,
Groningen, The Netherlands
Submitted: January 24, 2013; Accepted: November 3, 2013
Proofs received from author(s): February 15, 2014
... The use of molecular techniques to investigate genetic diversity, population structure and connec- tivity in marine ecosystems has increased substan- tially over the last 2 decades (Shulman & Bermingham 1995, Palumbi 2004, Cowen et al. 2006, Craig & Hastings 2007, Harrison et al. 2012, Beldade et al. 2014, Jackson et al. 2015). Molecular methods are now being applied in the assessments of population structure and genetic diversity (Silva-Oliveira et al. 2008), investigating evolutionary processes and local adaptation to natural or anthropogenic stressors ( Paris et al. 2015), exploring genes controlling or reg- ulating diseases ( Teng et al. 2008), understanding sexual development ( Luo et al. 2010), informing con- servation management plans ( Reiss et al. 2009) and in predicting the impacts of climate change (Nielsen et al. 2009, Davey et al. 2011, Horreo et al. 2011, Narum et al. 2013, Hemmer-Hansen et al. 2014). ...
... Although evidence of population structuring has been documented in coral reef fish (e.g. Shulman & Bermingham 1995, Bay et al. 2008, only a few studies have assessed population structure in Epi- nephelinae groupers ( Rivera et al. 2004, Zatcoff et al. 2004, Maggio et al. 2006, Silva-Oliveira et al. 2008, Beldade et al. 2014, Jackson et al. 2014, 2015 and there is a paucity of information regarding genotypic variation within and among spawning aggregations generally. ...
... Although evidence of population structuring has been documented in coral reef fish (e.g. Shulman & Bermingham 1995, Bay et al. 2008, only a few studies have assessed population structure in Epi- nephelinae groupers ( Rivera et al. 2004, Zatcoff et al. 2004, Maggio et al. 2006, Silva-Oliveira et al. 2008, Beldade et al. 2014, Jackson et al. 2014, 2015 and there is a paucity of information regarding genotypic variation within and among spawning aggregations generally. ...
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Groupers are a phylogenetically diverse group and include many ecologically and economically valuable predatory marine fishes that have experienced drastic population declines. Reproduction via spawning aggregations increases the vulnerability of grouper species such as Nassau grouper Epinephelus striatus to overfishing, and this is likely to be a major contributing factor to population declines. However, the lack of information pertaining to population structure and dynamics of Nassau grouper spawning aggregations has impeded effective ecosystem-based fisheries management for remaining stocks. Worldwide, The Bahamas has the largest number of known Nassau grouper spawning aggregations, yet very little is known about the overall status of groupers in the region. Landings of Nassau grouper in The Bahamas have declined by 86% in the last 20 years from a peak of 514 t in 1997. Available data suggest that existing management measures are failing in their attempts to prevent further declines. Effective management strategies are urgently needed that balance ecological and socioeconomic considerations to enable a sustainable Nassau grouper fishery. This review provides an analysis of the reproductive and population biology of Nassau grouper and a suggested framework to direct future research efforts for enhancing conservation management of this endangered marine fish species.
... One of the strongest drivers of genetic structure within a species is connectivity, the demographic linking of local populations via larval dispersal or movement of juveniles or adults. For instance, connectivity influences almost all ecological and evolutionary processes in metapopulations (Beldade et al. 2014). In a metapopulation, subpopulations are linked through dispersal as sources or sinks at one or more points during the species' life cycle (Kritzer and Sale 2006). ...
... Adults are found on shallow rocky reefs (20 m) and seamounts (30 m), and moderate fidelity to their home reef has been reported, with movements on the scale of~3 km (Tinhan et al. 2014;Green et al. 2015). L. argentiventris habitat is not distributed homogenously in the SGC, and the species is likely to survive only within networks of patches that are sufficiently connected by larval dispersal (Kindlmann and Burel 2008) or adult migration (Beldade et al. 2014). ...
We analysed the genetic connectivity and larval transport routes of Lutjanus argentiventris to test if eddies could transport coastal-demersal fish larvae between the peninsular and mainland coasts of the Southern Gulf of California. Larval transport was estimated using the ROMS oceanographic model during the main spawning period (July–August). We used 12 microsatellite loci to assess genetic diversity, population structure and gene flow estimates in 233 L. argentiventris samples from nine sites. The oceanographic model suggested the existence of a stream flow and eddies that maintain connectivity in the Southern Gulf of California. The global AMOVA and paired FST showed no significant genetic differentiation among the sites, and the estimations of the number of migrants indicated moderate to high gene flow among locations. However, after testing five demographic scenarios of connectivity with a coalescent sampler, our results supported the presence of a metapopulation structure with source-sink dynamics. We discuss the challenges to reconcile our results considering the assumptions of the different analyses and the characteristics of marine metapopulations. Connectivity of L. argentiventris could be representative of other costal-demersal species with a similar life history and spawning season. Link to read the article (free):
... First, a coupled biological oceanographic model (CBOM) that re-creates the circulation of the NGC and allows the inclusion of biological traits was developed to predict larval dispersal patterns between sites and local retention processes within sites (Marinone 2003(Marinone , 2012aMarinone et al. 2008). Second, connectivity hypotheses from the model output were validated in the field by density counts of recently settled juveniles ), deployment of drifters and acoustic doppler current profilers (ADCPs) to track currents Soria et al. 2014b), larval collectors (Soria 2010;Soria et al. 2008Soria et al. , 2010Soria et al. , 2013Soria et al. , 2014a, and population genetics (Soria 2010;Munguía-Vega et al. 2014;Beldade et al. 2014). We employed molecular markers to measure the rates of larval exchange between sites and retention within sites using tissue samples from target species taken in the field for a set of empirical sites that replicate those included in the oceanographic model outputs (Soria et al. 2012;Munguía-Vega et al. 2014). ...
... Our oceanographic models for the summer months suggest larval dispersal via cyclonic (counterclockwise) currents, from the Midriff Islands region toward southern Sonora and continuing along the coast to northern Sonora and the upper GC. This cyclonic gyre has been validated via gene flow estimates in several species that spawn during summer, including the rock scallop (Soria et al. 2012), the blue crab (Munguía-Vega et al. unpublished), the Gulf coney (Beldade et al. 2014), and the leopard grouper Jackson et al. 2015). As expected, because the gyre in the NGC reverses its direction twice a year, species reproducing during the winter phase of the gyre (i.e., anticyclonic or clockwise direction) show similar patterns but in completely opposite direction. ...
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This paper is dedicated to the memory of Miguel Fernando Lavín (1951–2014), a pioneer of the PANGAS initiative who dedicated his life to advance the field of oceanography in Mexico. He was a visionary who connected oceanographers, marine conservationists, and fisheries managers. Small-scale fisheries contribute about half of global fish catches, or two-thirds when considering catches destined for direct human consumption (FAO 2014). Small-scale fisheries play an important role in food security and nutrition, poverty alleviation, equitable development, and sustainable use of natural resources, providing nutritious food for local, national, and international markets. More than 90% of the world’s fishers and fish workers (those who work in pre-harvest, harvest, and post-harvest activities, including trade) are employed by small-scale endeavors that underpin local economies in coastal, lakeshore, and riparian ecosystems. This, in turn, generates multiplier economic effects in other sectors (FAO 2014). These activities may be a recurrent sideline undertaking or become especially important in times of financial difficulty. Small-scale fisheries represent a diverse and dynamic sector, often characterized by seasonal migration. They are strongly anchored in local communities and reflect historic links to fishery resources and traditions. Many small-scale fishers and fish workers are self-employed and are direct food providers for their household and communities. Most small-scale fisheries lack formal assessment, and the development of the sector over the past four decades has led to overexploitation of resources in several places across the globe. Recent studies estimate unsupervised small-scale fisheries are in substantially worse condition than fisheries where stocks have been assessed (Costello et al. 2012). Furthermore, the health of marine ecosystems and associated biodiversity are a foundation for the livelihoods and well-being of small-scale fishers. Figure 1. Pangas in the Gulf of California. Photo by Adrian Munguía-Vega. View full resolution In 2005, the PANGAS project was created with funding from the David and Lucile Packard Foundation as part of the Foundation’s initiative to support ecosystem-based management (EBM) for sustainable coastal and marine systems in various parts of the world (mainly the Western Pacific, U.S. West Coast, and the Gulf of California, Mexico). PANGAS is an acronym in Spanish that stands for Pesca Artesanal del Norte del Golfo de California: Ambiente y Sociedad (Small-Scale Fisheries of the Northern Gulf of California: Environment and Society). “Pangas” also refers to the small skiffs (6–8 m in length), made of fiberglass, with 55- to 150-horsepower outboard motors. These are versatile boats that can use multiple types of fishing gear, hold two to three fishers, and are the primary vessel used by small-scale fishers in the northern Gulf of California (NGC), México (Cudney-Bueno and Turk-Boyer 1998) (figure 1). From its inception in 2004 as a “fuzzy”—yet ambitious—idea of ultimately coupling biophysical and human processes for management of small-scale fisheries at a regional scale (the NGC), the idea quickly transitioned to the assembly of individuals who could bring a broad, multidisciplinary perspective for research and management of small-scale fisheries. PANGAS was structured as a multidisciplinary and bi-national initiative with the goal of developing and testing an interdisciplinary framework for ecosystem-based research and management of small-scale fisheries in the NGC ecosystem and increasing capacity for ecosystem-based research in the Gulf of California. PANGAS grew as a consortium of six leading academic institutions and nonprofit organizations with experience in the NGC, with the direct involvement of 50+ researchers, students, fishers, and management practitioners. Partners in the project have included two leading academic institutions from the Southwest United States (University of Arizona’s School of Natural Resources and the Environment [UA-SNRE] and University of California Santa Cruz [UCSC]) and one from northwest Mexico (Centro de Investigación Científica y Educación Superior de Ensenada, Baja California [CICESE]). It also included three leading Mexican nonprofit organizations with decades of experience working in the NGC (Comunidad y Biodiversidad, A.C. [COBI], and Pronatura Noroeste A.C. [PNO]) and in both sides of the U.S.-Mexico border (Intercultural Center for the Study of Deserts and Oceans [CEDO, Inc. and CEDO...
... Besides the gaps in habitat, other studies have found that at scales <1,000 km the larval dispersal and recruitment were the main processes affecting genetic structure (Berkström et al., 2020;Dalongeville et al., 2018;Pascual et al., 2017;Schunter et al., 2019).The general lack of genetic structure in the GC could be related to seasonally-reversing surface currents and mesoscale eddies (Lavín and Marinone, 2003). that transport fish larvae, creating different patterns of metapopulation structure that tend to homogenize allele frequencies (Beldade et al., 2014;Cisneros-Mata et al., 2018;Lodeiros et al., 2016;Munguia-Vega et al., 2014, 2018aReguera-Rouzaud et al., 2020;Soria et al., 2012). However, swimming behaviour, different settlement success and topography, like the narrow continental shelf or very steep slopes, could also contribute to genetic differences (Sefc et al., 2020). ...
The tropical Eastern Pacific (TEP) is a highly dynamic region and a model system to study how habitat discontinuities affect the distribution of shorefishes, particularly for species that display ontogenetic habitat shifts, including snappers (Lutjanidae). To evaluate the genetic structure of the Pacific red snapper (Lutjanus peru) and the yellow snapper (Lutjanus argentiventris) throughout their distribution range along the TEP, 13 and 11 microsatellite loci were analyzed, respectively. The genetic diversity of L. peru (N = 446) and L. argentiventris (N = 170) was evaluated in 10 and five localities, respectively, showing slightly higher but non‐significant values in the Gulf of California for both species. The genetic structure analysis identified the presence of significant genetic structure in both species, but the locations of the identified barriers for the gene flow differed between species. The principal driver for the genetic structure at large scales >2500 km was isolation by distance. At smaller scales (<250 km) the habitat discontinuity for juveniles and adults and the environmental differences throughout the distribution range represented potential barriers to gene flow between populations for both species. This article is protected by copyright. All rights reserved.
... Spawning in the Gulf of California occurs in the spring and summer months with a peak in July when fish form spawning aggregations on muddy bottoms (Cudney-Bueno and Turk-Boyer 1998, Aburto-Oropeza et al. 2008, Beldade et al. 2014. Spawning peaks occur in Colombia in July and February (Acevedo 1996). ...
... Advances in molecular biology and population genetics have proven to be extremely valuable in generating information on population status, genetic diversity and connectivity of a variety of fish species (Carvalho and Hauser, 1998;Silva-Oliveira et al., 2008;Davey et al., 2011;Adams et al., 2016;Garcia-Mayoral et al., 2016); in turn, these data have been applied to support population management and conservation efforts Beldade et al., 2014;Selkoe et al., 2016). In particular, the application of genetics for stock identification (Carvalho and Hauser, 1994) and estimates of effective population size, N e (Wright, 1931), combined with traditional fisheries stock assessment models (Hilborn and Walters, 1992) are emerging approaches for advancing conservation management of at-risk species (Luikart et al., 2010;Hare et al., 2011;Ovenden et al., 2016). ...
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Severe declines of endangered Nassau grouper (Epinephelus striatus) across The Bahamas and Caribbean have spurred efforts to improve their fisheries management and population conservation. The Bahamas is reported to hold the majority of fish spawning aggregations for Nassau grouper, however, the status and genetic population structure of fish within the country is largely unknown, presenting a major knowledge gap for their sustainable management. Between August 2014–February 2017, 464 individual Nassau grouper sampled from The Bahamas were genotyped using 15 polymorphic microsatellite loci to establish measures of population structure, genetic diversity and effective population size (Ne). Nassau grouper were characterized by mostly high levels of genetic diversity, but we found no evidence for geographic population structure. Microsatellite analyses revealed weak, but significant genetic differentiation of Nassau grouper throughout the Bahamian archipelago (Global FST 0.00236, p = 0.0001). Temporal analyses of changes in Ne over the last 1,000 generations provide evidence in support of a pronounced historic decline in Bahamian Nassau grouper that appears to pre-date anthropogenic fishing activities. M-ratio results corroborate significant reductions in Ne throughout The Bahamas, with evidence for population bottlenecks in three islands and an active fish spawning aggregation along with apparent signs of inbreeding at two islands. Current estimates of Ne for Nassau grouper are considerably lower compared with historic levels. These findings represent important new contributions to our understanding of the evolutionary history, demographics and genetic connectivity of this endangered species, which are of critical importance for advancing their sustainable management.
... In the GC, multiple seasonal oceanic gyres present within each of the main deep (1-3 km) basins shift direction at the beginning of the spring (March) and fall (October) seasons (Marinone et al. 2011;Marinone 2012). These gyres create a unique model system, where strongly asymmetric oceanic currents define a metapopulation structure, where upstream larval sources export larvae towards specific downstream locations, according to the spawning time and the direction of the predominant flow (Soria et al. 2012;Beldade et al. 2014;Munguia-Vega et al. 2015;Lodeiros et al. 2016). ...
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The dispersal during the planktonic larval period is a key feature to understand the metapopulation structure of marine fishes, and is commonly described by four general models: 1) lack of population structure due to extensive larval dispersal, 2) isolation by geographic distance where larval connectivity decreases with increasing distance between sites in all directions (isotropy), 3) population structure without any clear geographic trend (chaotic), 4) population structure explained by seascape approaches that explicitly incorporate the spatial and temporal variation in the direction and strength of oceanic currents via oceanographic modeling. We tested the four models in the Pacific red snapper Lutjanus peru, a key commercial species in the Gulf of California (GC), Mexico. We genotyped 15 microsatellite loci in 225 samples collected during 2015-2016 from 8 sites, and contrasted the observed empirical genetic patterns against predictions from each model. We found low but significant levels of population structure among sites. Only the seascape approach was able to significantly explain levels of genetic structure and diversity, but exclusively within spring and summer, suggesting this period represents the spawning season for L. peru. We showed that in the GC the strong asymmetry in the oceanic currents cause larval connectivity to show different values when measured in distinct directions (anisotropy). Management tools, including marine reserves, could be more effective if placed upstream of the predominant flow. Managers should consider that oceanographic distances describing the direction and intensity of currents during the spawning period are significant predictors of larval connectivity between sites, as opposed to geographic distances. The manuscript is available free to view here:
... Though the sites included in our study are small and isolated, these eddies may serve to enhance self-recruitment, especially for species with short PLDs, and therefore increase genetic structure among sites. Oceanographic features such as seasonal eddies have been shown to drive genetic connectivity of reef fishes elsewhere (e.g., Beldade et al. 2014). The eddies in the narrowest part of the Mozambique Channel near Juan de Nova may increase retention rates of larvae with short durations, such as A. akallopisos. ...
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The Western Indian Ocean harbors one of the world’s most diverse marine biota yet is threatened by exploitation with few conservation measures in place. Primary candidates for conservation in the region are the Scattered Islands (Îles Éparses), a group of relatively pristine and uninhabited islands in the Mozambique Channel. However, while optimal conservation strategies depend on the degree of population connectivity among spatially isolated habitats, very few studies have been conducted in the area. Here, we use highly variable microsatellite markers from two damselfishes (Amphiprion akallopisos and Dascyllus trimaculatus) with differing life history traits [pelagic larval duration (PLD), adult habitat] to compare genetic structure and connectivity among these islands using classic population structure indices as well as Bayesian clustering methods. All classical fixation indexes FST, RST, G′ST, and Jost’s D show stronger genetic differentiation among islands for A. akallopisos compared to D. trimaculatus, consistent with the former species’ shorter PLD and stronger adult site attachment, which may restrict larval dispersal potential. In agreement with these results, the Bayesian analysis revealed clear genetic differentiation among the islands in A. akallopisos, separating the southern group (Bassas da India and Europa) from the center (Juan de Nova) and northern (Îles Glorieuses) islands, but not for D. trimaculatus. Local oceanographic patterns such as eddies that occur along the Mozambique Channel appear to parallel the results reported for A. akallopisos, but such features seem to have little effect on the genetic differentiation of D. trimaculatus. The contrasting patterns of genetic differentiation between species within the same family highlight the importance of accounting for diverse life history traits when assessing community-wide connectivity, an increasingly common consideration in conservation planning.
... Pearse and Crandall 2004;Hedgecock et al. 2007), or the degree to which gene flow affects evolutionary processes within populations (Lowe and Allendorf 2010), as well as historical and contemporary mechanisms driving divergence when connectivity is limited (Cowen and Sponaugle 2009). The extent of connectivity among established reserves, and the extent of genetic differentiation among organisms within them, may be influenced by a number of mechanisms including vicariance events (Bernardi et al. 2003;Riginos 2005), environmental differences (Riginos and Nachman 2001), oceanography (Soria et al. 2012;Beldade et al. 2014), and limited dispersal ability (Hurtado et al. 2010). ...
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Effective design of marine reserves for use in fisheries management and conservation requires a clear understanding of patterns of larval transport and sink- source dynamics between populations, as well as a clear understanding of population demography. Mitochondrial and nuclear markers were analyzed to investigate potential mechanisms impacting connectivity among and the de- mographic history of subpopulations of a commercially important species in the Gulf of California, the leopard grouper (Mycteroperca rosacea). Demographic history and connectivity analyses included a coalescent analysis, esti- mating neutrality indices, estimating global and pairwise F’ST, UST, or G’’ST, and a priori methodologies to identify genetically distinct units and barriers to dispersal. Average, long-term connectivity between geographic regions in the Gulf was also estimated. Divergence of mitochondrial lineages of leopard grouper dated to the late Pleistocene, with deep-water islands serving as demographically stable populations that may have acted as sources for new populations during periods of climate variability. Addi- tionally, we observed genetically distinct units of leopard grouper in the Gulf, particularly between peninsular and mainland sites, as well as asymmetrical migration between the northern and central Gulf. Observed patterns of genetic differentiation are likely attributed to complex asymmet- rical oceanographic currents and local larval retention. Based on our genetic findings and current fishing pressure in certain regions, we recommend implementing small, upstream no-take zones in the areas east of Isla A ́ ngel de la Guarda, around Isla San Lorenzo and Isla San Esteban, and north of Isla Tiburo ́n, that would enhance connectivity among subpopulations, preserve sites with high genetic diversity, and benefit fisheries downstream of these sites.
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What factors have been important in the evolution of reef fish spawning aggregations? Surprisingly, basic biological features such as size, trophic ecology and anatomy are more predictive than life history features. As long as the different groups (Resident and Transient aggregators) shared basic properties of body size, nutritional ecology and anatomy they manifest similar spawning behaviours regardless of whether they are protogynous or gonochoristic, exhibit short or long generation times or have slow or fast population turnover rates. A critical element in the evolution of spawning aggregations is proposed to be the rapid advection of eggs and larvae away from the reef environment. In addition the timing of spawning episodes may be linked to specific seasonal and climatic features of the ocean environment, a variant of the match/mismatch hypothesis developed to explain spawning patterns in clupeoid fishes. Neither larval retention nor broad dispersal are seen as critical elements in the evolution of spawning aggregations. It is hypothesized that differences in aggregate spawning patterns and their underlying processes will occur in the Pacific and Atlantic oceans, a reflection of the different histories, oceanic environments and habitat structures of these two ocean basins.
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The timing, sources and pathways for incorporation of larval fishes into a developing anti-cyclonic eddy off south-western Australia were investigated. Larval fish assemblages within the study region were structured by location (shelf, eddy and oceanic) and water mass. The larval fish assemblage within the eddy was significantly distinct from that characterizing the surrounding oceanic water. The eddy assemblage, which was comprised largely of larvae of oceanic meso-pelagic fishes (especially Diaphus spp. and Vinciguerria spp.) and less abundant neritic taxa, reflected its Leeuwin Current (LC), shelf and oceanic source waters. The occurrence of neritic taxa in the eddy confirmed the hypothesis that these larvae were incorporated as it developed in proximity to the shelf break. The significantly larger larval size of temperate neritic taxa (e.g. Sardinops sagax, Engraulis australis) in the eddy compared with the shelf suggests that these larvae were transported from the shelf adjacent to the developing eddy. The occurrence of tropical neritic taxa (e.g. Acanthuridae, Lutjanidae, Pomacentridae) highlighted the LC as an important transport route to higher latitudes. Coupling the sampling of larval fishes with the trajectories of Lagrangian drifters provided insight into how larval fish assemblages changed during development of the eddy.
Aggregation spawning reef fi sh have planktonic (pre-fl exion) and nektonic (post-fl exion) larval phases. Pelagic eggs hatch in about 24 h into non-motile, yolk-sac larvae and several days later into pre-fl exion larvae which feed actively and control depth despite incomplete fi n development and limited motility. Thus, eggs, yolk-sac and pre-fl exion larvae are all passive, planktonic drifters, yet they are not necessarily fl ushed away by coastal currents into the open sea. Here we investigate how the physics of near-shore fl ow features, such as diffusion of the initial spawning cloud, tidal advection in coastal boundary currents and entrainment into tidal eddies, interact with the complexities of reef topography to reduce offshore dispersion. We use scale modelling to estimate dispersal via turbulence of gamete clouds for the fi rst few days post-spawning. Thereafter, we emphasize empirical information from tracked drifters released at spawning sites to evaluate alongshore tidal advection and entrainment into tidal eddies. Larval behaviour is of great importance not only to trajectories, but also because subtle depth adjustments by planktonic pre-fl exion larvae permit contact with concentrated foods on density discontinuities or at convergent fronts. This food source is critical for transformation from pre-fl exion plankton into post-fl exion nektonic larvae.
Fishes that engage in aggregation spawning do so at specific sites and times and have a wide diversity of spawning strategies. There are some clear distinctions in locations and timing between transient aggregations (TA) and resident aggregations (RA). TAs have larger predatory fishes, occur infrequently, but seasonally largely on or near shelf edge areas. RAs have herbivores and omnivores, are more numerous and occur in both shelf edge areas and inshore regions. Aggregations differ between the Indo-west Pacific (IWP) and tropical western Atlantic (TWA); probably due to current dominated regimes in the IWP due to the higher tidal amplitudes and barrier reef/channel geomorphology. Migration patterns are related to the frequency of spawning. Nearly all TA (and some RA) sites are used by multiple species, either sequentially or simultaneously. Many aggregation sites are stable in location over decades with only slight variation. Spawning at some TAs is now known to occur during periods of low current speed. The entrainment of TA propagules into oceanic circulation after spawning is uncertain with tendencies at some TA sites for retention of propagules. Spawn from RAs is less likely to become entrained into oceanic circulation. Water temperature regimes may be an important determinant of seasonality of spawning and early life history success. Most aggregations occur over a limited temperature range. The daily and lunar timing of aggregation spawning may be related to needs of pelagic life history. Predation on spawning adults is rare while predation of released eggs is common, but neither factor is believed to limit or structure aggregations.
We review commonly used population definitions under both the ecological paradigm (which emphasizes demographic cohesion) and the evolutionary paradigm (which emphasizes reproductive cohesion) and find that none are truly operational. We suggest several quantitative criteria that might be used to determine when groups of individuals are different enough to be considered ‘populations'. Units for these criteria are migration rate ( m ) for the ecological paradigm and migrants per generation ( Nm ) for the evolutionary paradigm. These criteria are then evaluated by applying analytical methods to simulated genetic data for a finite island model. Under the standard parameter set that includes L = 20 High mutation (microsatellitelike) loci and samples of S = 50 individuals from each of n = 4 subpopulations, power to detect departures from panmixia was very high (∼ 100%; P < 0.001) even with high gene flow ( Nm = 25). A new method, comparing the number of correct population assignments with the random expectation, performed as well as a multilocus contingency test and warrants further consideration. Use of Low mutation (allozyme-like) markers reduced power more than did halving S or L . Under the standard parameter set, power to detect restricted gene flow below a certain level X (H 0 : Nm < X ) can also be high, provided that true Nm ≤ 0.5 X . Developing the appropriate test criterion, however, requires assumptions about several key parameters that are difficult to estimate in most natural populations. Methods that cluster individuals without using a priori sampling information detected the true number of populations only under conditions of moderate or low gene flow ( Nm ≤ 5), and power dropped sharply with smaller samples of loci and individuals. A simple algorithm based on a multilocus contingency test of allele frequencies in pairs of samples has high power to detect the true number of populations even with Nm = 25 but requires more rigorous statistical evaluation. The ecological paradigm remains challenging for evaluations using genetic markers, because the transition from demographic dependence to independence occurs in a region of high migration where genetic methods have relatively little power. Some recent theoretical developments and continued advances in computational power provide hope that this situation may change in the future.
Little is known about the seasonality and distribution of grouper larvae (Serranidae: Epinephelini) in the Gulf of Mexico and Atlantic Ocean off the coast of the southeast United States. Grouper larvae were collected from a transect across the Straits of Florida in 2003 and 2004 and during the Southeast Area Monitoring and Assessment Program spring and fall surveys from 1982 through 2005. Analysis of these larval data provided information on location and timing of spawning, larval distribution patterns, and interannual occurrence for a group of species not easily studied as adults. Our analyses indicated that shelf-edge habitat is important for spawning of many species of grouper-some species for which data were not previously available. Spawning for some species may occur year-round, but two peak seasons are evident: late winter and late summer through early fall. Interannual variability in the use of three important subregions by species or groups of species was partially explained by environmental factors (surface temperature, surface salinity, and water depth). A shift in species dominance over the last three decades from spring-spawned species (most of the commercial species) to fall-spawned species also was documented. The results of these analyses expand our understanding of the basic distribution and spawning patterns of northwest Atlantic grouper species and indicate a need for further examination of the changing population structure of individual species and species dominance in the region.
Most reef fishes have bipartite life histories, separate pelagic-oceanic (egg/larvae) and benthic (juvenile/adult) periods. The several-week pelagic period has early planktonic (egg, yolk sac and preflexion larva) and later nektonic components (post-flexion larva to settlement); the plankton-nekton transition timing is variable. For aggregating species, larvae are weak swimmers early in life, but late stages are often strong swimmers able to perhaps influence their settlement locations. No obvious differences were found between larval stages of aggregating and non-aggregating species and both types of spawning are found within single families, and even within a species. There are no egg types, morphologies, feeding strategies or special structures exclusive to aggregating species. Initial dispersal is determined by location and time of spawning. Pelagic eggs are buoyant, keeping them in near-surface waters and away from benthic predators. The larvae go through a series of stages (egg, yolk sac larvae, pre- and post-flexion larvae, pelagic juvenile), becoming larger and more capable over time. Critical periods occur and can cause major mortality of a cohort. Ocean conditions during the early egg and yolk sac stage are critical to survival followed by initiation of feeding as a second critical event. During pelagic life larvae must survive in open water, find appropriate food as larvae and avoid predators. Cohorts from aggregations can recruit as a large pulse, but other fishes may also have such pulses. The mass spawnings of reef invertebrates, such as stony corals, are generally not comparable to those of fishes, while crustaceans (spiny lobsters, marine crabs, terrestrial crabs) have some similarities. There is a need for fisheries oceanography research on aggregation spawning, as well as more work on laboratory culture. The question of potential maternal benefits to larvae needs careful attention.
Transects of CTD (to 1000 m) and zooplankton stations (to 200 m in 50 m strata) were made across an anticyclonic eddy in the southern Gulf of California during October 2007 to determine its influence upon the three-dimensional distribution of larval fish assemblages. The eddy was ∼90 km in diameter and ∼70 m deep. A larval fish assemblage, representing a mix of oceanic and coastal species, was defined mainly in the eddy from 200 m depth to the surface. Mesopelagic species, such as Vinciguerria lucetia, were dominant. Coastal reef (Diplectrum sp.) and pelagic (Auxis spp.) species were found mainly in the surface layer. This suggests that, because of the Gulf's relative narrowness, the eddy trapped coastal fish larvae during its formation and trajectory southward, retaining larvae of different adult habits. Another larval fish assemblage was defined off the eastern coast; its high larval abundance and specific richness was probably associated with coastal upwelling. Mesopelagic species (e.g. Triphoturus mexicanus) dominated this assemblage, and coastal demersal species that were absent from the eddy (e.g. Symphurus williamsi) were recorded in the surface layer, suggesting that the thermocline was a vertical boundary in this assemblage. The 3D differentiation of planktonic habitats was the result of the mesoscale hydrodynamics in the area sampled, in particular that associated to the eddy life history and characteristics (radius, depth and velocity), and to coastal upwelling, promoting larval retention of a mix of species of different adult habits.