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Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(4):1164-1178, October-December 2021 (Published Nov. 01, 2021)

Genetic connectivity of the metapopulation of the coral

Pocillopora verrucosa (Scleractinia: Pocilloporidae) in multi-use marine

protected areas of the Gulf of California, and management implications

Fernando Aranceta-Garza

; https://orcid.org/0000-0003-1298-1814

Pedro Cruz-Hernández

; https://orcid.org/0000-0003-2503-6643

Héctor Reyes-Bonilla

; https://orcid.org/0000-0003-2593-9631

Eduardo F. Balart

*; https://orcid.org/0000-0001-8752-1017

1. Centro de Investigaciones Biológicas del Noroeste, Consejo Nacional de Ciencia y Tecnología (CONACYT), La Paz,

Baja California Sur, México; faranceta@cibnor.mx

2. Laboratorio de Genética Acuícola, Centro de Investigaciones Biológicas del Noroeste, Sociedad Civil, La Paz, Baja

California Sur, México; pcruz@cibnor.mx

3. Laboratorio de Sistemas Arrecifales, Universidad Autónoma de Baja California Sur, La Paz, Baja California Sur,

México; hreyes@uabcs.mx

4. Laboratorio de Necton y Ecología de Arrecifes, Centro de Investigaciones Biológicas del Noroeste, Sociedad Civil,

La Paz, Baja California Sur, México; ebalart04@cibnor.mx (Correspondence*)

Received 19-IX-2021. Corrected 24-X-2021. Accepted 26-X-2021.

ABSTRACT

Introduction: Estimates of contemporary connectivity of the broadcast spawning coral Pocillopora verrucosa

between multi-use marine protected areas (MUMPAs) are required to assess MUMPA effectiveness and their

ability to enhance resilience against disturbances.

Objective: To determine the genetic structure and connectivity patterns between P. verrucosa demes inside

the Gulf of California and evaluate the role and effectiveness of established MUMPAS in their protection and

resilience.

Methods: We assessed P. verrucosa connectivity along its peninsular range (∼350 km), including five locations

and three MUMPAs in the Gulf of California using six microsatellite genetic markers.

Results: Population structure was significant (F

= 0.108***) when demes included clonal replicates; however,

when these clones were removed from the analysis, the sexual individuals comprised a metapopulation pan-

mixia (F

= 0.0007 NS). To further understand connectivity patterns, an assignment test was carried out which

identified ten recent between-deme migrants with a mean dispersal distance of 116.6 km (± 80.5 SE). No long-

distance dispersal was detected. These results highlight the ecological importance of the Bahía de La Paz region,

including Archipiélago de Espíritu Santo MUMPA. This region, located at the center of the species peninsular

range, exports larva to downstream sink demes such as the Loreto (northwardly) and Cabo Pulmo (southwardly)

MUMPAs. Of importance, inter-MUMPA spacing was larger than the mean larval dispersal by ~56 km, suggest-

ing thar the designation of intermediate ‘no-take’ zones would enhance short-distance connectivity.

Conclusion: This study contributes as a baseline for policymakers and authorities to provide robust strategies for

coral ecosystem protection and suggest that protection efforts must be increased towards peninsular intermediate

reefs to promote metapopulation resilience from natural and anthropogenic factors.

Key words: scleractinian coral; Eastern Tropical Pacific; molecular marker; connectivity; microsatellite; meta-

population; reproduction; Mexico.

Aranceta-Garza, F., Cruz-Hernández, P., Reyes-Bonilla, H.,

& Balart, E. F. (2021). Genetic connectivity of the

metapopulation of the coral Pocillopora verrucosa

(Scleractinia: Pocilloporidae) in multi-use marine

protected areas of the Gulf of California, and management

implications. Revista de Biología Tropical, 69(4), 1164-

1178. https://doi.org/10.15517/rbt.v69i4.45936

https://doi.org/10.15517/rbt.v69i4.45936

CONSERVATION

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Eastern Tropical Pacific (ETP) coral reefs

are small, dominated by few species, and with a

discontinuous distribution, presenting a typical

zonation pattern where shallow zones are most-

ly dominated by ramose monogeneric commu-

nities of Pocillopora spp., and massive species

and leafy taxa, such as Porites spp. and Pavona

spp., increases in dominance with depth (Toth

et al., 2017), whose persistence depends mainly

on the connectivity through larval dispersal

between demes (Fobert et al., 2019; Sale et al.,

2005). This connectivity determines gene flow,

coral community structure and metapopulation

dynamics (Ayre & Hughes, 2000). The extent

of connectivity by self-recruitment or long-

distance immigration, is strongly associated

to their resilience against natural and anthro-

pogenic disturbances (Almany et al., 2007;

Underwood et al., 2009). The main ETP’s

disturbances that cause bleaching events and

local to regional mass mortalities are: seasonal

sea surface temperatures (SST) with El Niño

and La Niña events (Glynn et al., 2017); solar

irradiance (LaJeunesse et al., 2010); hurricanes

(Aranceta-Garza et al., 2012); fisheries and

tourism related impacts (Cortés & Reyes-

Bonilla, 2017). The recovery of reefs has been

documented as a slow process in ETP (Guzmán

& Cortés, 2007), usually depending on recruit-

ment from distant surviving colonies.

The aim of ‘no-take’ in marine protected

areas (MPA) is to mitigate the anthropogenic

impacts by conserving biodiversity and pre-

venting overfishing, thereby acting as source

populations to seed demographic sinks 47 with-

in larval dispersal range (DOF, 2014; ey Gen-

eral del Equilibrio Ecológico y la Protección al

Ambiente, 2021; Munguia-Vega et al., 2018).

As such, the connectivity within MPA net-

works is a fundamental process that promotes

metapopulation resilience (Grimsditch & Salm,

2006). The Gulf of California (GC) has seven

multi-use marine protected areas (MUMPAs)

directly protecting the main reef builder, Pocil-

lopora verrucosa, which represents a protected

marine area of 3.64 % of the GC (CONANP,

2020). The effectiveness of these MUMPAs

on enhancing the conservation prospects of P.

verrucosa remains unknown. Nonetheless, this

network of MUMPAs may integrate a regional

network, as has been previously shown to be an

effective managing tool elsewhere, for the con-

servation of biodiversity, biological processes,

and critical habitats in developing countries

(Munguia-Vega et al., 2018).

The distribution of P. verrucosa is delim-

ited by the ETP ranges from GC to Ecuador

(Pérez-Vivar et al., 2006). In the southern GC,

they are found in ~400 km of the peninsular

coast including nearby islands (Reyes-Bonilla

et al., 2005). This species is a simultaneous

hermaphrodite with mixed modes of repro-

duction (Campos-Vázquez, 2014). They are

a sexual broadcast spawner with a reproduc-

tive period from June to September (Campos-

Vázquez, 2014) which should confer long

dispersal potential (Chávez-Romo & Reyes-

Bonilla, 2007) and also recruit locally by

asexual fragmentation (Aranceta-Garza et al.,

2012; Pinzón et al., 2012). While few stud-

ies have addressed regional connectivity in

Pocillopora species along the Mexican Pacif-

ic (MP), Chávez-Romo et al. (2008) found

restricted connectivity between GC and Gulf

of Tehuantepec regions, a pattern also seen

in other coral species (brooder Porites pana-

mensis: Paz-García et al., 2012b; broadcast

spawner Pavona gigantea: Saavedra-Sotelo et

al., 2011). Nevertheless, some of these studies

suggest an unrestricted gene flow in Pocillo-

pora type 1 species (as P. verrucosa is catego-

rized, Pinzón et al., 2012) throughout the ETP.

Previous Pocillopora connectivity studies spe-

cifically in the GC have explored few locations,

ranging from 10 to 100 km (less than ~30 %

of its peninsular range). They have found high

connectivity between demes (Chávez-Romo,

2014; Chávez-Romo et al., 2008; Paz-García

et al., 2012b; Pinzón et al., 2012), but with

contrasting local genotypic structures (asexual

vs sexual recruits), showing that demes are

strongly influenced by local factors (Aranceta-

Garza et al., 2012; Pinzón et al., 2012). This

variation in the contribution of sexual and

asexual reproductive strategies have important

consequences for Pocillopora resilience and

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disturbance recovery, with recent studies sug-

gesting that environmental conditions in the

GC favored coral sexual reproduction (Cabral-

Tena et al., 2018; Chávez-Romo, 2014).

Until recently, most connectivity studies

in the GC have use low resolution molecular

markers (Delmotte et al., 2002; Ridgway &

Gates, 2006), such as allozyme or internal tran-

scribed spacer (e.g.: Chávez-Romo et al., 2008;

Paz-García et al., 2012b; Saavedra-Sotelo et

al., 2011). Polymorphic microsatellites can

detect fine-scale connectivity by shifting from

populations to individuals at relevant ecologi-

cal scales (Gélin et al., 2018; Taninaka et al.,

2019). To date, only two studies have explored

the connectivity of P. verrucosa populations in

the GC using microsatellite markers (Pinzón &

LaJeunesse, 2011; Pinzón et al., 2012), how-

ever, their sampling locations examined were

few and geographically close.

Here we assess the connectivity patterns

of P. verrucosa in the Southern GC, by apply-

ing assignment test methods, where population

genetic statistics assign individuals to the puta-

tive natal population (Piry et al., 2004). These

assignment methods have been applied in other

corals species, to show the spatial scales of con-

nectivity, source-sink dynamics and population

resilience capabilities (e.g. Seriatopora hystrix

in Maier et al., 2009; Acropora austere and

Platygyra daedalea in Montoya-Maya et al.,

2016; Heliopora spp. in Taninaka et al., 2019).

We hypothesize that P. verrucosa con-

forms a highly connected metapopulation in

the GC and its dispersal capabilities are related

with regional oceanographic features character-

ized by a series of gyres that reverse direction

twice a year (Marinone, 2012); yet each deme

population structure will also be influenced

by local factors (e.g. hurricanes, bleaching).

We also hypothesize that due to the environ-

mental seasonal characteristics, intermediate

range MUMPAS will protect source demes

with a crucial role for regional coral recovery.

As such, the research objectives were (a) to

assess genetic diversity and variation in P. ver-

rucosa using microsatellites; b) to assess the

population structure in the GC; c) to estimate

larval migration patterns and dispersal dis-

tances between demes along the GC; d) to

determine the role and effectiveness of prees-

tablished MUMPAS in Pocillopora protection

and resilience; and e) to explore implications of

the estimated connectivity, as means of disper-

sal direction and magnitude, for the effective

management of hermatypic corals in the GC.

MATERIALS AND METHODS

Study area: The study area of P. ver-

rucosa encompasses its northernmost limit in

North America along the peninsular coast of

the Gulf of California (GC) (Fig. 1), where it

grows either as a coral reef (as in Cabo Pulmo,

Bahía San Gabriel in Isla Espíritu Santo, and

San Lorenzo Channel), or more commonly as

patch reefs (El Portugués and Loreto). Its popu-

lations are subjected to seasonal environmental

factors, such as high irradiance, cold water

upwellings, hurricanes, and oceanographic cur-

rents. The seasonal marine circulation in the

GC is dominated by temporal forcing agents,

which results in contrasting seasonal periods:

spring and summer; and fall and winter (Mari-

none, 2003). During the spring and summer,

the Western half of the Southern Gulf of Cali-

fornia (SGC) has a surface circulation domi-

nated by a cyclonic gyre directed southwardly

and creating a dominant peninsular northerly

coastal current. During fall and winter, this gyre

reverses with dominant southwardly coastal

current. The SGC gyre current velocities run at

0.25-0.50 ms

-1

(Lavín et al., 2014).

Sample collection: Coral species iden-

tification is complex and can be based on

morphological characters, molecular identi-

fication or both (Budd et al., 2012; Toller et

al., 2001) For the GC, Pinzón and Lajeunesse

(2011), using the mitochondrial open reading

frame (mtORF), found that the morphotypes

P. verrucosa, P. damicornis, P. meandrina,

P. capitata and P. eydouxi belong to a single

lineage defined as type 1, however, Flot et al.

(2008) mentioned the existence of ambiguities

in the molecular identification these species.

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Therefore, the present study considers that

all the colonies sampled should be regarded

according to Pinzón and Lajeunesse (2011) as

mtORF type 1. However, the identification of

the nominal species of P. verrucosa was based

on morphological diagnostic characters (Veron,

2000) conducted at the Laboratorio Virtual de

Sistemas Arrecifales (LAVISA) at the Uni-

versidad Autónoma de Baja California Sur by

regional coral expert Dr. Hector Reyes.

For the sampling design each colony was

established as an independent experimental

unit. Samples of Pocillopora verrucosa colo-

nies (Fig. 1) were collected in the SGC from

February 2008 to June 2009. The colonies

were selected randomly avoiding neighboring

heads (2 m minimal distance among colonies)

at a maximum depth of 7 m and were col-

lected by fragment removal (~2 cm

). Sam-

pling locations from North to South were: (a)

Fig. 1. Sampling sites (black stars) of Pocillopora verrucosa in the peninsular coast of the Gulf of California. Solid black

lines show multi-use marine protected area (MUMPA) polygons. Diagonal line fill areas show MUMPAs ‘no take’ zones.

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an exposed reef (i.e. intense wave and current

energy) in Bahía Loreto National Park (L); an

exposed reef in El Portugués (P); Archipelago

de Espíritu Santo Marine National Park with

two locations: a protected bay in Isla Espíritu

Santo (IES) and an exposed reef in San Loren-

zo Channel (SLC); and an exposed reef in Cabo

Pulmo National Park (CP). L samples were

collected at three areas: Las Palmas at Carmen

Island, La Biznaga at Danzante Island, and Islet

El Candelero. The three areas were taken as a

single location (denoted by “L”; N = 20) since

they did not show significant allelic frequency

differences previously tested by an analogous

Fisher’s exact test (Guo & Thompson, 1992);

(b) Bahía de La Paz area samples included

those from the peninsular location at P (N = 47

colonies) and IES at Bahía San Gabriel (N =

50 colonies) and SLC coral reefs (N = 50 colo-

nies); (c) the southernmost sampling location

was in CP reef (N = 50 colonies).

DNA extraction and microsatellite geno-

typing: The fragments were preserved in 70

% ethanol and stored at 4 °C, pending DNA

extraction. Total genomic DNA from samples

was extracted using a commercial kit (DNEasy

kit, Qiagen, Valencia, CA) per manufacturer’s

instructions. The quality of the extraction was

verified by agarose gel electrophoresis (Sigma,

St. Louis, MO). Each DNA extraction was

quantified using a low DNA mass ladder (Invi-

trogen, Life Technologies, Carlsbad, CA) in 1

% agarose gel electrophoresis.

A polymerase chain reaction (PCR) was

carried out using six microsatellites developed

for Pocillopora spp.: PV6 and PV7 (Magalon

et al., 2004), and Pd3-002, Pd3-005, Pd2-006,

and Pd3-008 (Starger et al., 2008). PCR ampli-

fications of each microsatellite were performed

in a thermocycler (Applied Biosystems, Life

Technologies, Carlsbad, CA) with a final vol-

ume of 12.5 µL containing 50 to 100 ng DNA

template, 1 × buffer, 1.5 mM MgCl

, 0.2 mM

dNTP, 0.5 µM of each primer, and 0.625 units

µL–1 polymerase (Platinum Taq polymerase,

Invitrogen). The thermal cycling program was:

10 min at 94 °C + 30 × (45 s at 94 °C + 45 s

at 55 °C + 30 s at 72 °C) and + 8 min at 72

°C. PCR products were visualized on an acryl-

amide gel using a multi-view scanner (FMBIO

III, Hitashi, Yokohama, JP). Re-visualizations

were made to confirm allele sizes. The result-

ing bands were scored manually using 10

bp standard ladders (#10821015, Invitrogen).

Only two loci showed stuttered bands (PV6 and

Pd2-006), obscuring the allele reading, which

were correctly reamplified using the cycling

protocol of Yoshida et al. (2005):1 × (2 min at

94 °C ), 5 × (5 s at 94 °C, 60 s at 56 °C, 60 s at

72 °C), 20 × (0 s at 94 °C, 60 s at 56 °C, 60 s at

72 °C), and 1 × (60 min at 72 °C).

Genotyping: Genotypes were analyzed

using GIMLET (Valière, 2002) to identify

individuals with same multi-locus genotypes

(MLG). GIMLET also estimates the probabil-

ity of identity (P

), that is, the probability that

two individuals in the population are identified

as clone mates when in fact they are distinct

genets. The theoretical expected P

and the

unbiased P

were computed for each locus

using allele frequencies from the genotype

scores (see Waits et al. (2001) for the formu-

lation). According to Waits et al. (2001), P

scores ranging from 0.001 to 0.0001 should be

sufficiently low for forensic applications in nat-

ural populations, giving a very low probability

of misidentifying clone mates in this study.

Two datasets were then constructed for

subsequent genetic analyses: (1) full MLG

(i.e. including clonal individuals) and (2)

unique MLGs.

Identification and correction of null alleles

for all loci was made using the program

MICRO-CHECKER (Oosterhout et al., 2004).

Genetic variability was obtained per location

based on: mean allelic richness (A); effec-

tive allele number (ne); observed (H

); and

expected (H

) heterozygosities, which were

obtained using the program Arlequin 3.11

(Excoffier et al., 2005).

Microsatellite data were checked for

departures from Hardy Weinberg Equilibri-

um (HWE) and linkage equilibrium (Arlequin

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v.3.11) adjusting significance values with Bon-

ferroni corrections (Rice, 1989).

Population genetic structure was assessed

using the pairwise F-statistics (Arlequin v.3.11)

with 10 000 permutations and α = 0.05.

Migration patterns: To assess P. verru-

cosa isolation by distance patterns, we tested

for statistical significance between geographi-

cal and genetical distance (F

/ (1 - F

))

matrices using the program IBDWS Version

3.23 (Jensen et al., 2005). Significance tests

(P < 0.05) were obtained with a Mantel test

using 10 000 randomizations. Contemporary

migration patterns were assessed using Gene-

class 2.0 (Piry et al., 2004), which computes

genetic assignment criteria to include/exclude

reference populations as the origin to diploid

individuals. The five sampled populations were

analyzed using the six microsatellite loci of the

unique MLG dataset representing sexual plan-

ula connectivity. Briefly, the analysis employed

a Bayesian assignment criterion (Rannala &

Mountain, 1997) with a Monte Carlo resam-

pling (Paetkau et al., 2004) of 100 000 itera-

tions, generating the probability of likelihood

to include/exclude a colony (or individual) to a

sampled population.

We used two approaches to estimate

individual migration. First, the detection of

immigrants in the sampling populations (i.e.

first-generation migrants) was assessed using

the likelihood of individual genotypes within

the population where the individual had been

sampled (L_home). An assignment threshold

α = 0.05 was used to accept the alternative

hypothesis that the individual was an immi-

grant. Second, the possible origin of each

detected immigrants among the sampled popu-

lations was evaluated using an assignment cri-

terion with α = 0.10, where the population with

the highest probability was selected as the most

likely source population. When immigrants

resulted in a P-value < 0.1 the software assumed

they belonged to other unsampled populations.

RESULTS

A total of 217 P. verrucosa colonies were

sampled along 350 km in the Gulf of Cali-

fornia. Only 99 (45.6 %) of these had unique

MLG. The rest (N = 118,54.4 % of the sampled

colonies) were clones of one of the unique

MLGs. Clonal individuals were observed at

all the sampling sites and ranged from ∼40 %

of the sampled individuals in Cabo Pulmo, El

Portugués and Loreto to ∼95 % in San Lorenzo

Channel and Isla Espíritu Santo. No MLG were

share among localities.

The probability of identity (P

) for the full

MLG was 4.12 × 10

–05

(biased approach) and

3.67 × 10

-05

(unbiased approach); the results

for the unique MLG was 2.00 × 10

–05

(biased

approach) and 1.50 × 10

–05

(unbiased approach).

Genetic diversity: The allelic diversity

(A) for the full MLG dataset ranged from 4-10

alleles with a maximal mean of 6.33 alleles (

2.58 SE, N = 6) in Cabo Pulmo and minimal of

4.00 alleles ( 0.89 SE, N = 6) in San Lorenzo

Channel (Table 1).

Linkage disequilibrium was not statisti-

cally significant for the unique MLG dataset.

Null alleles were observed in the locus Pd3-002

(P < 0.001) for Loreto resulting in an excess of

homozygotes.

The tests of HWE assumptions was ana-

lyzed in the unique MLG dataset (i.e. no clone

individuals) all loci were in equilibrium, except

for the locus (Pd3-200) in Loreto with an het-

erozygote excess. Cabo Pulmo was the only

location in HWE in both datasets.

Genetic Structure: Pairwise F

analyses

(Table 2) were contrasting between full and

unique MLG datasets where the F-statistics

over all loci were statistically significant for

the former with a F

= 0.108 *** and non-

significant for the latter with a F

= 0.0007

NS. Pairwise F

analysis in the unique MLG

showed only one significant genetic differenti-

ation between population extremes, Loreto and

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TABLE 1

Pocillopora verrucosa allele richness (A), effective alleles (ne) and observed (H

) and expected (H

) heterozygosity per

locus in the five populations sampled in the Gulf of California using the unique multi-locus genotypes

Unique Multilocus Genotypes (UMLG)

CP SLC IES P L

N 37 6 5 35 16

PV6

A 10 5 6 10 5

ne 6.86 3.13 4.17 6.43 3.91

0.92 0.67 1.00 0.77 0.88

0.87 0.74 0.84 0.86 0.77

PV7

A 8 5 5 8 6

ne 3.22 2.57 3.85 3.04 3.76

0.73 0.67 1.00 0.71 0.69

0.70 0.67 0.82 0.68 0.76

Pd3-005

A 7 4 4 5 5

ne 1.87 2.06 2.38 1.79 2.18

0.51 0.50 0.60 0.43 0.69

0.47 0.56 0.64 0.45 0.56

Pd3-002

A 6 3 4 5 4

ne 2.24 1.95 2.94 2.77 3.66

0.51 0.67 0.80 0.49

0.31*

0.56 0.53 0.73 0.65

0.75*

Pd3-008

A 4 4 3 4 4

ne 1.49 2.06 1.85 1.94 1.48

0.32 0.50 0.40 0.46 0.31

0.33 0.56 0.51 0.49 0.33

Pd2-006

A 3 3 3 5 4

ne 2.95 2.88 2.94 3.27 2.93

0.70 1.00 0.80 0.74 0.75

0.67 0.71 0.73 0.70 0.68

± SD

6.3 ± 2.58 4.0 ± 0.89 4.2 ± 1.17 6.2 ± 2.32 4.7 ± 0.82

± SD

3.1 ± 1.95 2.4 ± 0.49 3 ± 0.87 3.2 ± 1.69 3.0 ± 0.98

± SD

0.62 ± 0.21 0.67 ± 0.18 0.77 ± 0.23 0.6 ± 0.16 0.6 ± 0.24

± SD

0.6 ± 0.19 0.63 ± 0.09 0.71 ± 0.12 0.64 ± 0.15 0.64 ± 0.17

*Significant at P < 0.05 for Hardy-Weinberg departure using a sequential Bonferroni correction; CP: Cabo Pulmo; SLC: San

Lorenzo Channel; IES: Isla Espíritu Santo; P: El Portugués; L: Loreto.

TABLE 2

Pairwise multi-locus estimates of F

between populations of Pocillopora verrucosa in the Gulf of California.

Populations labelled from South to North

Unique Multi-locus Genotype (UMLG)

CP SLC IES P L

CP –

SLC -0.017 –

IES -0.012 -0.028 –

P 0.001 -0.013 -0.029 –

L 0.021* -0.010 -0.017 0.011 –

Significant * at P < 0.05; ** at P < 0.01; *** at P < 0.001; CP: Cabo Pulmo; SLC: San Lorenzo Channel; IES: Isla Espíritu

Santo; P: El Portugués; L: Loreto.

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Cabo Pulmo (F

= 0.021*). This observation

was also supported by a significant Mantel test

(P < 0.05) using the unique MLG dataset.

Contemporary migration patterns: The

ecological time scale migration patterns sug-

gested 10 individuals identified as putative

immigrants between sampling locations (P <

0.05, Table 3). All the locations showed immi-

grants: Cabo Pulmo had the most (N = 3), Isla

Espíritu Santo had the least (N = 1) (Table 3,

see letter A, Fig. 2). Three unassigned immi-

grants (two in El Portugués and one in Cabo

Pulmo) originated in an unsampled locality.

The mean distance range traveled by the seven

planulae was of 116.6 km (± 80.5 SE) (Table 3,

see letter B). The spacing between the Archip-

iélago de Espíritu Santo Marine National Park

with respect to Bahía Loreto and Cabo Pulmo

National Parks was 180 km and 165 km,

respectively, exceeding the mean planulae dis-

persal distance in 64 and 49 km, accordingly

(Table 3, see letter B).

DISCUSSION

This study examines for the first time,

the ecological connectivity patterns of the

main coral reef builder in the Gulf of Califor-

nia, Pocillopora verrucosa. At a local scale,

P. verrucosa deme maintenance showed a

mixed mode reproductive strategy. Some loca-

tions almost exclusively made of clones (Isla

Espíritu Santo and San Lorenzo Channel);

some showed intermediate levels of clon-

ality and sexual recruitment (El Portugués

and Loreto), while others were dominated by

TABLE 3

Number of individuals (immigrants) excluded from their sampling site and their most probably deme of origin (assigned

deme) (A) and observed dispersal distance matrix and multi-use marine protected area (MUMPA) interspace (B)

(A) Assigned deme

Immigrants (n) Immigrants unassigned (n)

Sampling deme L P SLC IES CP

L * 2 2

P * 2 2

SLC 1 * 1 2

IES 1 * 1

CP 1 1 * 3 1

Total 0 3 0 4 0 10 3

(B) Distance matriz (km)

MUMPAs Interspace (km)

Sampling deme L P SLC IES CP

L * 180 AES→CPNP 165

AES→LBNP 180

P *

SLC 49 * 7

IES 42 *

CP 200 158 *

Mean dispersal distance

(116.571 ± 80.473)

Mean MUMPA interspace

(172.5 ± 10.60)

Individuals were excluded from their sampling site at a P-value < 0.05; individuals were assigned to their putative deme of

origin with the highest probability of occurrence; excluded individuals with P-value < 0.1 were assumed to have originated

from a deme not sampled in the study. L: Loreto; P: El Portugués; SLC: San Lorenzo Channel; IES: Isla Espíritu Santo; CP:

Cabo Pulmo; AES = Archipiélago de Espíritu Santo Marine National Park; LBNP = Bahía de Loreto National Park; CPNP

= Cabo Pulmo National Park.

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Fig. 2. Connectivity patterns of the seven assigned immigrants (n) for the Pocillopora verrucosa planulae in the Gulf of

California. Black stars show the demes; black solid arrow shows the planula dispersal direction, where brackets indicate

the immigrant source deme. Light and heavy gray solid arrows show the summer coastal and oceanic current direction,

respectively; they inverse during the fall-winter seasons (in Marinone, 2003).

sexual planula recruitment (Cabo Pulmo). On a

regional scale, all the demes were in panmixia,

acting as a metapopulation with differential

migrant contributions allowing to differenti-

ate between source and sink demes. However,

significant genetic differentiation was observed

between the most distant demes, Loreto and

Cabo Pulmo National Parks. This emphasizes

the importance of the mid-range Bahía de la

Paz area (i.e. Archipiélago de Espíritu Santo

National Park and El Portugués deme), which

appears to act as a stepping stone for connect-

ing distant sink demes and maintaining meta-

population resilience.

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Genetic diversity and structure: The

genetic diversity found in the GC (A = 5.07 ±

0.68) was similar to other studies of subtropi-

cal populations of Pocillopora: Africa: A = 5.0

± 1.4 in Ridgway et al. (2008); Australia: A =

6.3 ± 3.23 in Thomas et al. (2014); and Pan-

amá A = 7 ± 2.4 in Combosch and Vollmer

(2011), and contrasts with the higher diversity

seen at low latitudes: Polynesia A = 9 ± 5.2

in Magalon et al. (2004). This difference may

reflect the effects of isolation and low effective

population size on genetic diversity (Ayre &

Hughes, 2004).

The heterogenous frequency of clones

presented in all the locations emphasize the

important role of asexual reproduction for

local maintenance (e.g. by storm fragmenta-

tion). This suggests a coral’s adaptive strategy

towards local factors where a few specialized

clonal genotypes redirected resources towards

repair and growth (Aranceta-Garza et al.,

2012). Recently, this process could have been

mechanically enhanced by documented anthro-

pogenic impacts, such as shipwrecks and rec-

reational activities such as anchoring, scuba

diving and also fishing nets (Aranceta-Garza

et al., 2012; López-Espinosa de los Monteros,

2002). The observed frequencies of sexual

colonies over the locations was explained pre-

viously in Aranceta et al. (2012), suggesting a

relation with external factors such as type of

substrate and coral density, where higher hard

substrata and less coral density could be pro-

moting sexual recruitment (e.g. Cabo Pulmo,

Loreto and El Portugés).

The connectivity by sexual migrants

between demes showed a P. verrucosa meta-

population in panmixia on the peninsular GC.

However, extreme demes such as Loreto and

Cabo Pulmo, showed low levels of connectiv-

ity (Table 2), suggesting that most of the dis-

persal occurs between neighboring demes and

long-distance events may be rare. Moreover,

Loreto is the Northern limit of P. verrucosa’s

ETP range and often experiences severe dis-

turbances, which may explain the few and

isolated standing colonies surrounded by dead

coral heads. This results in a sink population,

dependent from Southern larvae, showing low

genetic diversity whilst observing and excess in

heterozygote (Balloux, 2004). Contrary to local

asexual maintenance, sexual larvae dispersal

is an important process for coral resilience in

GC (Chávez-Romo, 2014), ensuring demes

replenishment and recovery in areas impacted

by natural or anthropogenic factors (McLeod

et al., 2009).

Pocillopora verrucosa contemporary

connectivity: The assignment test results sug-

gested that most larvae dispersing out of their

region (70 %) originated in the Bahía de La

Paz area, mainly from both Archipiélago de

Espiritu Santo National Park and the unprotect-

ed deme El Portugués. However, there was no

long-distance dispersal between extreme demes

(~330 km between Cabo Pulmo and Loreto),

which could be attributed to physical factors

such as oceanographic GC retention features:

gyres, fronts, bays and islands. Moreover,

mean dispersal distance was 116.6 km (± 80.5

SE) and the observed source-sink dynamics

revealed that Bahía de La Paz is a key source

area, supplying larvae to North (Loreto) and

South sink demes (Cabo Pulmo) and depend

on the seasonal direction of oceanographic

currents and gyres (Marinone, 2003) during P.

verrucosa reproductive period. These results

further demonstrate the importance of conserv-

ing central demes for coral replenishment and

recovery, enhancing regional metapopulation

resilience. One recent example was Loreto,

presenting 90 % loss of coral cover which has

been slowly recolonized by Southern larvae

(Hernández et al. 2010; LaJeunesse et al.,

2010; Paz-García et al., 2012a), probably from

Bahía de La Paz. Furthermore, these newly

recruited individuals probably will be geneti-

cally and physiologically more adapted (i.e.

thermal tolerant zooxanthellas) to conditions of

very high/low temperature and light intensity

(Iglesias-Prieto et al., 2004; LaJeunesse et al.,

2007; Paz-García et al., 2012a; Reyes-Bonilla,

2001). This adaptive process may have already

been demonstrated after the 2015 ENSO distur-

bance, where no Pocillopora colony mortality

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was reported in Loreto (Reyes-Bonilla, per-

sonal communication, 2021).

Management implications: The incor-

poration of connectivity among demes in the

P. verrucosa metapopulation, including the

existing MUMPA network in the Southern GC,

combines with other considerations for their

conservation prospects. The coral reefs are

fragile ecosystems whose resilience depends

not only on their biology, but on other species,

especially herbivorous fish and invertebrates

(Grimsditch & Salm, 2006). Current manage-

ment schemes in the GC-MUMPAs permit

fishing activities over large areas, leaving just

a few small areas as ‘no-take’ zones, reducing

the MUMPA conservation value by decreas-

ing fish species, functional richness, and their

ecosystems processes over time (Ramirez-Ortiz

et al., 2020), affecting reef resilience. If the

expansion of these ‘no-take’ is not possible,

another recommended conservation tool for

the protection of coral reefs in the GC is the

establishment of critical habitats, as defined in

the General Wildlife Law (Ley General de Vida

Silvestre, 2018).

The mean dispersal distance in P. verru-

cosa (116.6 km) was longer than the individ-

ual length of the multi-used marine protected

areas, but shorter than mean spacing between

installed MUMPAs (172.5 km). Given these

estimates, we suggest the designation of two

new ‘no-take’ zones to be integrated with

existing Southern GC-MUMPAs. This man-

agement measure would reduce the separation

between Archipiélago Espíritu Santo and Cabo

Pulmo (to the South) and Loreto (to the North)

MUMPAs to ~50 km each, which agrees with

the minimum spacing recommended for coral

connectivity (50-200 km in Munguia-Vega et

al. (2018), although 10-20 km in McLeod et

al. (2009). Moreover, the resulting MUMPA

network would also cover a variety of tem-

perature regimes (tropical and subtropical) to

increase the survival rate in bleaching events

(Iglesias-Prieto et al., 2004). Finally, including

the El Portugués source deme under a ‘no-take’

regimen would build up ecological redundancy

into the network against large scale distur-

bances (Munguia-Vega et al., 2018). All the

above measures will promote the preservation

of regional coral connectivity, mainly by step-

ping-stone recolonization events coming from

central and South demes, which are valuable

for short term recovery in continuous reef sys-

tems (Underwood et al., 2009) and may apply

for GC reefs and patch systems.

The genetic assignment methods we

applied here contributed to the identification

of the dispersal patterns and level of connectiv-

ity in the P. verrucosa metapopulation within

an installed MUMPA network in the GC. This

study determined that the central peninsular

area functions as a key source of larvae to other

locations, promoting metapopulation resilience

by enhancing recovery of damaged reefs with

Southern thermal tolerant larvae, especially

to higher latitude areas. Moreover, anthropo-

genic disturbances should be removed from

coral habitats by changing current management

schemes to ‘no-take’ zones to protect connec-

tivity, reproduction and ecosystem functional

diversity. The inclusion of intermediate ‘no-

take’ zones in the MUMPA network, as well as

adding redundant source areas (El Portugués),

would provide a stepping-stone refuge and hab-

itat replication in case of severe damaged. This

study provides as a baseline for policymakers

and authorities to establish robust strategies

for coral ecosystem protection and to promote

metapopulation resilience from natural and

anthropogenic factors.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

1175

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ACKNOWLEDGMENTS

The authors would like to thank Alejandra

Aranceta-Garza from the University of Dundee,

Scotland for her constructive criticism of the

manuscript. We thank Juan J. Ramírez-Rosas,

Mario Cota-Castro, Horacio Bervera-León,

Rafael Cabral-Tena, Luis. F. Drew-Morales,

Jeb Rabadan-Sotelo and Daniel Vazquez-Arce

for their assistance in the field work and D.

Fischer for the editorial services. The sampling

permit number was DGOPA.08546.050809.-

2596 SAGARPA-CONAPESCA. The CONA-

CYT granted a graduate fellowship to FAG.

This study was funded by CONABIO (grant

number GD001) entitled “Variabilidad genética

y probable origen de las poblaciónes coloniza-

doras en el área afectada por el buque tanque

Lárazo Cárdenas II, Baja Califorina Sur”; and

by CONACYT (grant number 37528-B).

RESUMEN

Conectividad genética de la metapoblación del coral

Pocillopora verrucosa (Scleractinia: Pocilloporidae)

en áreas protegidas multipropósito del Golfo de

California, e implicaciones de manejo

Introducción: La estimación de la conectividad en corales

escleractinios, como P. verrucosa, dentro de una red de

áreas marinas protegidas (MPA) preestablecidas es funda-

mental para garantizar la efectividad en su conservación e

incrementar su resiliencia.

Objetivo: Determinar la estructura genética y la conec-

tividad entre los demes de P. verrucosa dentro del Golfo

de California, y evaluar el papel y efectividad de la red

preestablecida de áreas marinas protegidas.

Métodos: Se evaluó la conectividad de P. verrucosa en

cinco locaciones a lo largo del golfo incluyendo tres MPA

usando seis marcadores microsatélites.

Resultados: Se demostró que existe estructura poblacional

adjudicada a la presencia local y heterogénea de individuos

clones (F

= 0.108***); pero al removerlos del análisis,

los individuos de origen sexual conformaron una meta-

población en panmixia (F

= 0.0007 NS). Así mismo, se

identificaron 10 potenciales migrantes en la región con

una dispersión promedio de 116.57 km (± 80.47 SE) y sin

conexión entre localidades extremas. De relevancia, se

identificó la importancia ecológica del área central o Bahía

de La Paz y MPA Archipiélago Espíritu Santo, como fuente

larvaria de corales a toda la región. Además, se determinó

que el espacio inter-MPA fue mayor que la distancia de

dispersión promedio larvaria mencionada, por lo que sería

de importancia ecológica el establecimiento de MPAs inter-

medias que favorezcan la conectividad a distancias cortas.

Conclusiones: Los resultados encontrados en el estudio

son pertinentes y contribuyen como línea base para los

tomadores de decisiones y autoridades, proporcionando la

conectividad de la región para establecer las estrategias de

protección apropiadas, sugiriendo aumentar la conserva-

ción de las subpoblaciones centrales, la cuales promueven

la resiliencia metapoblacional de P. verrucosa ante factores

ambientales y/o antropogénicos.

Palabras clave: coral escleractinio; Pacífico Tropical del

Este; marcador molecular; conectividad; microsatélite;

metapoblación; reproducción; México.

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