Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

Testing the effectiveness of natural and artificial substrates

for coral reef restoration at Isla Isabel National Park, Mexico

Pastora Gómez-Petersen 1,2; https://orcid.org/0000-0003-3537-8049

José de Jesús Adolfo Tortolero-Langarica 3,4*; https://orcid.org/0000-0001-8857-5789

Alma Paola Rodríguez-Troncoso 5; https://orcid.org/0000-0001-6243-7679

Amílcar Leví Cupul-Magaña 5, https://orcid.org/0000-0002-6455-1253

Marco Ortiz 6; https://orcid.org/0000-0002-1126-7216

Eduardo Ríos-Jara 1; https://orcid.org/0000-0003-3534-6362

Fabián Alejandro Rodríguez-Zaragoza 1*; https://orcid.org/0000-0002-0066-4275

1. Laboratorio de Ecología Molecular, Microbiología y Taxonomía, Departamento de Ecología, Centro Universitario de

Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara. Camino Ramón Padilla Sánchez, 2100, Nextipac,

CP 45200, Zapopan, Jalisco, México; pastoragomez@gmail.com, eduardo.rios@academicos.udg.mx,

fabian.rzaragoza@academicos.udg.mx (*Correspondence)

2. Programa de Doctorado en Ciencias en Biosistemática, Ecología y Manejo de Recursos Naturales y Agrícolas, Centro

Universitario de Ciencias Biológicas y Agropecuarias, Universidad de Guadalajara, Camino Ramón Padilla Sánchez

No. 2100, Nextipac, CP 45200, Zapopan, Jalisco, México.

3. Laboratorio de Esclerocronología de Corales Arrecifales, Unidad Académica de Sistemas Arrecifales, Instituto de

Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Prolongación Avenida Niños Héroes Sin

Número, CP 77580, Puerto Morelos, Quintana Roo, México.

4. Tecnológico Nacional de México / Instituto Tecnológico Bahía de Banderas, CP 63734, Bahía de Banderas, Nayarit,

México; adolfo.tl@bahia.tecnm.mx

5. Laboratorios de Ecología Marina, Centro de Investigaciones Costeras, Centro Universitario de la Costa, Universidad

de Guadalajara, Av. Universidad 203, Del. Ixtapa, CP 48280, Puerto Vallarta, Jalisco, México;

alma.rtroncoso@academicos.udg.mx, levi.cupul@academicos.udg.mx

6. Instituto Antofagasta, Instituto de Ciencias Naturales Alexander von Humboldt Facultad de Recursos del Mar,

Universidad de Antofagasta, Antofagasta, Chile; marco.ortiz@uantof.cl

Received 30-VIII-2022. Corrected 24-XI-2022. Accepted 07-II-2023.

ABSTRACT

Introduction: The branching coral Pocillopora is the main reef-building species in the Eastern Tropical Pacific

(ETP) region. However, their populations have been threatened due to the intense effect of thermal-stress events

in the last three decades. As a mitigating response, active restoration strategies have been developed. However,

it has not been possible to establish specific protocols along the ETP’s reefs.

Objective: To evaluate the efficiency of two different substrates (natural vs. artificial), through coral growth

comparison (extension rate and tissue area) in three Pocillopora coral morphospecies within a year.

Methods: Coral growth was estimated by two techniques: extension rate and tissue area of P. cf. verrucosa, P.

cf. capitata, and P. cf. damicornis every three months during a year.

Results: The extension rate and superficial area growth vary among the coral morphospecies P. cf. verrucosa

(16.33 mm yr-1 and 168.49 mm2 yr-1), P. cf. capitata (16.25 mm yr-1 and 176.83 mm2 yr-1), and P. cf. damicornis

(12.38 mm yr-1 and 87.62 mm2 yr-1). The data reveals that substrate type did not affect Pocillopora growth, yet

there was an effect caused by seasonal changes.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54738

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

Scleractinian corals are the main engineers

of coral reef ecosystems, due to their capac-

ity to precipitate calcium carbonate (CaCO3),

forming tridimensional structures that consti-

tute the base of the physical reef-framework

and providing ecosystem services and habitat

to associated biodiversity (Álvarez-Filip et

al., 2009; Sheppard et al., 2010). Coral reef

ecosystems have been threatened by natural

events (heatwaves, hurricanes, diseases, and

others), and human-derived activities (coastal-

development, nutrient input, overfishing, and

marine pollution), causing large coral mortal-

ity (up to 50 %) in Eastern Tropical Pacific

(ETP) over the last three decades (De’ath et al.,

2009; Rinkevich, 2015). As natural recovery

occurs slowly (decades or centuries), many

active restoration tools have emerged as an

alternative strategy to accelerate coral recovery

and mitigate the rapid coral reef degradation

(Rinkevich, 2020). Direct coral transplantation

is one of the most used techniques as it avoids

the early-stage of coral farming/nursering and

post-outplanting stress, which have resulted

in high survival and growth rates (Harriott &

Fisk, 1988; Tortolero-Langarica et al., 2014).

Also, artificial substrate (typically comprised

of ceramic, concrete, or terracotta, among oth-

ers) is most likely to aid in reef conservation

and restoration by providing nursery habitat for

target species or recruitment substrate for cor-

als and other organisms (Hylkema et al., 2021;

Conclusions: This study demonstrates that coral restoration can be implemented using both natural and artifi-

cial substrata, with no differences in coral growth. We recommend the implementation of coral reef restoration

programs, highlighting the importance of initiate during the warm season due to optimal growth performance

of P. cf. verrucosa and P. cf capitata species, which improves the effectiveness of management actions in Isla

Isabel National Park.

Key words: Isabel Island; hermatypic coral; Central Mexican Pacific; reef restoration.

RESUMEN

Evaluación del sustrato natural y artificial en la restauración de arrecifes de coral

en el Parque Nacional Isla Isabel, México.

Introducción: Los corales ramificados del género Pocillopora son los constructores arrecifales más importantes

del Pacífico Tropical Oriental (PTO). Sin embargo, sus poblaciones han disminuido por efectos de eventos de

estrés térmico ocurridos las últimas décadas. Por ello, se han desarrollado estrategias de restauración activa como

respuesta de mitigación, pero no ha sido posible establecer protocolos específicos para estas especies en el PTO.

Objetivo: Evaluar la eficiencia de dos tipos de sustrato (natural vs. artificial) con base en la comparación del

crecimiento de coral (tasa de extensión y área de tejido) en tres morfoespecies de Pocillopora a lo largo de un año.

Métodos: Las estimaciones del crecimiento coralino se hicieron con dos técnicas (extensión lineal y área super-

ficial) en P. cf. verrucosa, P. cf. capitata and P. cf. damicornis cada tres meses durante un año.

Resultados: Las tasa de extensión y crecimiento del área superficial variaron entre las morfoespecies de P. cf.

verrucosa (16.33 mm año-1 y 168.49 mm2 año-1), P. cf. capitata (16.25 mm año -1 y 176.83 mm2 año-1), y P. cf.

damicornis (12.38 mm año-1 y 87.62 mm2 año-1). Los resultados mostraron que los tipos de sustratos no afectaron

el crecimiento de los corales Pocillopora, aunque existió un efecto causado por el cambio de la estación climática,

donde la estación cálida promueve un incremento su crecimiento.

Conclusiones: Este estudio demuestra que la restauración de corales puede ser implementada con sustrato artifi-

cial o natural, sin diferencias en el crecimiento de corales entre ellos. Nosotros recomendamos continuar con la

implementación de los programas de restauración de arrecifes de coral, resaltando, la importancia de iniciarlos

en la estación cálida cuando existe un desempeño más óptimo en el crecimiento, particularmente de las especies

P. cf. verrucosa y P. cf. capitata, lo cual ayudará a mejorar la efectividad de las acciones de manejo en el Parque

Nacional Isla Isabel.

Palabras clave: Isla Isabel; coral hermatípico; Pacífico Central Mexicano Central; restauración arrecifal.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

Monchanin et al., 2021). A coral reef restored

not only leads to an increase in coral coverage

but also improves the increase of structural

heterogeneity and calcium carbonate produc-

tion, facilitating the recovery/maintenance of

coral reef habitats (Lindahl, 2003; Tortolero-

Langarica et al., 2014).

Branching coral species are commonly

used for testing the efficiency of coral restora-

tion techniques due to their fast-growth and

3-D properties (Rinkevich, 2019; Rinkevich,

2020), and also allows to determine the long-

term potential success of restoration initiatives

(Tortolero-Langarica et al., 2019). However,

branching corals are considered one of the

most sensitive species to abrupt environmen-

tal changes such as temperature anomalies,

light irradiance, including extreme hydrody-

namic conditions (tropical storms and swells),

causing negative effects on coral calcification

(Allemand et al., 2011; Prachett et al., 2015).

Hence, coral growth assessment provides

insights to understand the species’ response

to environmental fluctuations of seasonal sea-

water temperature, thermal-stress events, and

substrate availability during and after the res-

toration (Grigg, 2006; Lough & Cooper, 2011;

Rinkevich, 2019).

Along the ETP, pocilloporid corals com-

prise the most abundant coral genera in shallow

reef areas (Glynn & Ault, 2000), but also has

been the most affected by heatwaves events

causing massive bleaching and high mortali-

ties (> 90 %) (Carriquiry et al., 2001; Glynn,

2000; Glynn, 2001), with different recovery

trajectories among ETP’s coral reef locations

(Cruz-García et al., 2020; Romero-Torres et

al., 2020). Coral reef recovery has been quicker

after a bleaching event in some sites because

of its oceanographic conditions (Cruz-García

et al., 2020). For example, Marietas islands are

in a place with seasonal upwellings and inter-

nal waves, so seawater temperature does not

rise as much as Isabel island, which is on the

continental shelf with shallow water and higher

positive thermal anomalies (Godínez et al.,

2010). Therefore, the total live coral cover on

Isabel island is lower than on Marietas islands

(Hernández-Zulueta et al., 2017). Despite these

differences in coral recovery, few attempts of

coral restoration actions have been tested along

the region (Liñán-Cabello et al., 2011; Muñiz-

Anguiano et al., 2017; Nava & Figueroa-Cama-

cho, 2017; Tortolero-Langarica et al., 2014;

Tortolero-Langarica et al., 2019; Tortolero-

Langarica et al., 2020). In particular, in the

Central Mexican Pacific (CMP), there is still

insufficient information on the effectiveness of

different restoration techniques, based on coral

growth and survival data (Tortolero-Langarica

et al., 2019). This study presents the first resto-

ration approach at the Isla Isabel National Park,

Mexico, using two different substrates (natural

and artificial) and the comparisons of three

pocilloporid morpho-species (P. cf. damicornis,

P. cf. capitata, and P. cf. verrucosa) through lin-

ear extension and tridimensional (3D) growth

(live tissue area) during a one-year period of

restoration. Due to the different characteristics

of both substrates, three morpho-species, and

the environmental condition variation along the

year, we expected coral growth differences in

all these factors.

MATERIALS AND METHODS

Study area: Isla Isabel National Park

(IINP) (21°50’50’’ N - 05°53’10” W) is a

volcanic island with a surface area of 82.1 ha,

located within the CMP (Fig. 1). The study

site is located in a transitional oceanographic

region, seasonally influenced by the California

Current, the North Equatorial Current, and the

Gulf of California water mass (Badan, 1997).

In summer, seawater temperature ranges from

23.5 to 32.7 ºC, while in winter ranges from

18.6 to 29.7 ºC (CONANP, 2005). The IINP har-

bors an important coral community, with small

fringing and rocky reefs with a high coverage

of hermatypic corals (10.7 %) of the genera

Pocillopora, Pavona, and Porites (Galván-Villa

et al., 2010; Hernández-Zulueta et al., 2017;

Ríos-Jara et al., 2008; Tortolero-Langarica et

al., 2016). These coral ecosystems are char-

acterised by a high associated biodiversity

(Galván-Villa et al., 2010; Hermosillo-Núñez

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

et al., 2015; Rodríguez-Zaragoza et al., 2011),

and act as a “stepping stone” that contributes

to the connectivity of marine species along the

CMP (Briggs & Bowen, 2013; Galván-Villa et

al., 2010; Glynn & Ault, 2000).

Coral samples: The coral restoration was

conducted from August 2010 to August 2011

using two substrata types: 1) steel-stacks sta-

bilized into the natural substrate, and 2) semi-

spherical concrete modules (Ø = ~1 m) with

steel-stacks, considered as artificial substrate.

Both treatments were installed at 2–4 m depth

with a distance of 2–3 m between them (Fig. 2).

Coral fragments of opportunity (~10 cm) were

hand collected with SCUBA from the nearby

area. Each fragment was visually examined

and selected to avoid those with partial dead

or bleaching but also the invasion of algae and

sponges (i.e., Cliona spp. and Thoosa spp.)

(Nava & Carballo, 2008).

Every three-months (August 2010, Novem-

ber 2010, February 2011, and May 2011), 72

coral fragments were installed and then stained

with alizarin red at a concentration of 0.02 gl

l-1 (Sigma®) for 15 hours and fixed with plastic

ties in both natural and artificial substrata (P. cf.

damicornis n = 12, P. cf. capitata n = 12 and P.

cf. verrucosa n = 12, for each substrate; These

species were chosen because they have the

highest coverage and frequency in the CMP).

After each growth period (three-monthly =

quaternary-1), coral fragments were extracted

and bleached with 10 % sodium hypochlo-

rite for 12 hours for further growth analyses.

Coral surface area growth was estimated by

evaluating the surface area increase (mm2)

using the aluminium foil technique described

by Marsh (1970), and the extension growth

(mm) fragments were cut into slices (~30 x

20 x 10 mm) using a tipped diamond saw

blade (Qep®). Each coral slice was individually

photo-documented with a Panasonic DMC-FS7

camera with a high resolution (300 dpi) using

a common rule as standard reference (precision

of 0.1mm); growth was determined as apical

Fig. 1. Study area in Isla Isabel National Park (IINP) at Mexican Pacific Coast. Red star: coral restoration area.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

height measured from the alizarin mark to the

top of each coral sample with ImageJ (v.1.41)

software (Rasband, 2012).

The seawater temperature (SWT) was

recorded using Onset HOBO® (precision of ±

0.5 °C) thermographs installed in situ with a set

record of 20 minute intervals. Data were pooled

during the warm season (July-November 2010),

and cold season (December 2010-June 2011),

and used to relate to coral growth parameters.

Data analysis: To determine the effect

of time, substrate and temperature into the

growth parameters, extension rate and surface

area were analysed using a three-way crossed

analyses of variance based on permutations

(ANOVA), which was built with an Euclid-

ean distance matrix following Anderson et al.

(2008). These unrestricted analyses were used

as data were not parametric. Differences among

species, between substrates and across to peri-

odicity were tested for each technique based on

the next model:

Fig. 2. Coral restoration of Pocillopora species using A. artificial and B. natural substrata at Isla Isabel National Park.

where Y is the analyzed variable (i.e., linear

extensions and surface area), μ is the variable’s

average, Spi is coral Morphospecies factor

(P. cf. damicornis, P. cf. capitata and P. cf.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

verrucosa), STj is Substrata Type (artificial or

natural), Pk is sampling periodicity (four sam-

pling periods) and εijk is the accumulated error.

All factors were fixed (model type I). Sta-

tistical significance was tested using a sum of

squares type III (partial) and 10 000 permuta-

tions of residuals under a reduced model and

a sum of squares type III (partial). Pairwise

comparisons (permutational t-tests) were used

when significant differences were found in

the factors or their interaction. The analyses

were performed using PRIMER 7.0.21 soft-

ware (Anderson et al., 2008). Finally, simple

linear regressions were performed to deter-

mine the relationship between temperature,

extension rate, using a coefficient of deter-

mination (r2). For all regression models, 95%

confidence intervals were estimated and global

test was evaluated using a least-squares pro-

cedure in SigmaPlot Ver. 11 software (Systat

Software, Inc.).

RESULTS

Extension growth rate: The factors of

Morphospecies and Periods, and the triple

interaction explained most of the variation

observed in coral growth rates (Table 1). Those

differences were attributed to the Period fac-

tor (Appendix 1), where temperature influ-

enced most of these differences in warmer

seasons (min. 23.5 °C, max. 32.7 °C) rates

varied between 2.45 to 7.49 mm quarterly-1,

meanwhile in cold seasons (min. 18.6 °C,

max. 29.7 °C) varied between 1.28 to 6.20 mm

quarterly-1 (Table 2, Fig. 3, Fig. 4). Morphospe-

cies factor showed that P. cf. damicornis has

the lowest growth rate in all periods (3.39 ±

1.8 mm quarterly-1), meanwhile P. cf. capitata

(4.33 ± 2.3 mm quarterly-1) and P. cf. verrucosa

(4.24 ± 2.0 mm quarterly-1) resulted with the

highest growth rate (Table 2, Fig. 4, Appendix

2). The accumulated annual growth rates were

of 12.38 mm/yr-1 for P. cf. damicornis, 16.25

mm yr-1 for P. cf. capitata, and 16.33 mm yr-1

for P. cf. verrucosa (Fig. 5). Substrata Type did

not influence differences in coral growth (Fig.

5, Appendix 3).

Surface area: The results showed that

double interactions “Morphospecies x Period”

and “Period x Substrata Type” explained the

surface area variation (Table 1). The morpho-

species x period interaction showed differences

in coral growth rates during the warm period

and among morphospecies varied between

79.17 ± 33.27 mm2 quarterly-1 to 411.31 ±

120.23 mm2 quarterly-1, and during the cold

period, growth rates varied from 23.78 ± 15.35

mm2 quarterly-1 to 226.48 ± 227.24 mm2

quarterly-1 (Table 2, Fig. 3, Fig. 4, Appendix

4). Regarding morphospecies factor, P. cf.

damicornis showed the lowest annual tissue

area increase (34.14 mm2 yr-1) compared with

P. cf. capitata (70.73 mm2 yr-1) and P. cf. ver-

rucosa (65.67 mm2 yr-1) (Table 2, Fig. 3, Fig. 4,

TABLE 1

Results of three-way PERMANOVA with crossed and fixed factors.

Source of variation ER SAG

Pseudo-F P(perm) Perms Pseudo-F P(perm) Perms

Spp 2.65 0.0001 9 955 4.82 0.0001 9 950

P 61.77 0.0001 9 948 18.9 0.0001 9 956

ST 13.15 0.5111 9 844 0.23 0.2680 9 938

Spp x P 7.09 0.0001 9 935 8.05 0.0001 9 936

P x ST 3.61 0.4061 9 955 0.55 0.0184 9 952

Spp x ST 0.78 0.198 9 949 1.5 0.4780 9 957

Spp x P x ST 4.39 0.0078 9 938 2.19 0.3679 9 931

Codes: Spp = species (P. cf. damicornis, P. cf. capitata, P. cf. verrucosa), P = period, ST = substrate type (natural and

artificial), ER = extension rates, SAG = surface area growth. Bold numbers correspond to P ≤ 0.05.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

Appendix 5). Substrata Type x Period interac-

tion showed the same pattern tissue growth was

higher during the warm season (158.0 mm2

yr-1 in natural substrate and 158.2 mm2 yr-1 in

artificial substrate) than cold season (108.63

mm2 yr-1 in natural substrate and 146.69 mm2

yr-1 in artificial substrate) (Table 2, Fig. 3, Fig.

4, Appendix 6). Nevertheless, substrata type

factor exhibited non-significant influences in

the live coral tissue area (P > 0.05).

Linear regression models showed that

extension rate and tissue area growth were

positively related to SST in both substrate types

(Fig. 6). The corals P. cf. damicornis and P. cf.

capitata showed a significant relation with SST

in both methods, while P. cf. verrucosa were

significant only with extension rate (Fig. 6).

DISCUSSION

Direct transplantation is one of the most

successful methods used for the coral restora-

tion of damaged coral reefs (Boch & Morse,

2012; Boström-Einarsson et al., 2020; Edwards,

2010; Edwards & Gomez, 2007; Rinkevich,

2014; Rinkevich, 2019; Young et al., 2012),

along both coastal and insular areas. (Ishida-

Castañeda et al., 2019; Tortolero-Langarica et

al., 2020). The direct outplanting of fragments

of opportunity in IINP resulted as efficient in

terms of coral growth, regardless of the sub-

strate, confirming the feasible and potential of

using Pocillopora coral species fixed to natural

or artificial substrata as a technique for coral

restoration along the CMP (Nava & Figueroa-

Camacho, 2017; Tortolero-Langarica et al.,

2014; Tortolero-Langarica et al., 2019).

During 2010-2011, a period of negative

thermal stress (La Niña event) influenced the

study area, with temperatures < 1.3 °C for a

period of eight months (NOAA, 2022). Ther-

mal stress conditions elicit the expulsion of

the algae-symbiont, which provides 90 % of

the energetic budget used for the coral growth

and reproduction process (Van Oppen & Black-

all, 2019). The optimal temperature for coral

growth rates in the ETP region is ranged from

26-29 °C during a neutral ENSO period, yet

TABLE 2

Coral growth rates per period, substrata type, and species.

Aug-Nov (cold season) Nov-Feb (cold season) Feb-May (warm season) May-Aug (warm season)

Natural substrate Artificial substrate Natural substrate Artificial substrate Natural substrate Artificial substrate Natural substrate Artificial substrate

Linear extension mm mm mm mm mm mm mm mm

P. cf. damicornis 4.10 ± 0.70 4.74 ± 0.96 1.28 ± 0.39 1.98 ± 1.89 2.52 ± 0.86 2.45 ± 0.74 5.16 ± 2.07 4.35 ± 1.56

P. cf. capitata 4.53 ± 1.13 4.69 ± 1.61 2.95 ± 2.0 2.18 ± 0.82 2.99 ± 1.46 2.43 ± 0.97 6.82 ± 1.20 7.49 ± 1.51

P. cf. verrucosa 4.81 ± 1.01 6.20 ± 1.87 2.60 ± 0.81 1.95 ± 0.74 3.39 ± 1.81 3.97 ± 0.66 4.65 ± 2.40 5.79 ± 1.93

Surface area mm2mm2mm2mm2mm2mm2mm2mm2

P. cf. damicornis 93.65 ± 36.02 138.57 ± 73.94 23.78 ± 15.35 60.71 ± 81.80 97.23 ± 51.16 79.79 ± 33.27 128.06 ± 71.84 79.17 ± 63.27

P. cf. capitata 92.44 ± 55.25 223.89 ± 166.0 90.27 ± 58.98 64.94 ± 37.91 105.29 ± 137.7 98.2 ± 76.36 328.32 ± 145.24 411.31 ± 120.23

P. cf. verrucosa 248.27 ± 224.23 299.95 ± 232.82 151.92 ± 104.18 65.54 ± 26.94 143.66 ± 100.88 120.68 ± 58.79 138.11 ± 107.67 179.79 ± 97.12

Mean ± standard deviation. Codes: Aug = August, Nov = November, Feb = February, May = May, NS = Natural substrate, AS = Artificial substrate.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

at La Niña event, there are sub-optimal tem-

peratures that could promote coral growth rate

decay from 20-50 % (Tortolero-Langarica et

al., 2016). Nevertheless, coral growth may vary

among reef locations due to different local and

temporal environmental conditions (Tortolero-

Langarica et al., 2017). In this study, Pocil-

lopora species increased two times compared

with their initial size (rising from 178 to 442

%), which agrees with Tortolero-Langarica et

al. (2017), whose study site is near our study

site and has similar environmental conditions.

Even various authors report similar growth

rates for Pocillopora corals in several stud-

ied years throughout the ETP (Glynn, 1977;

Guzmán & Cortés, 1989; Jiménez & Cortés,

2003; Manzello, 2010; Medellin-Maldonado

et al., 2016). These comparisons indicate that

the growth of the three coral species studied

in our study was not affected by La Niña, per-

haps because they are acclimated to changes

in temperature.

The overall tissue growth area among

pocilloporid morphospecies was different, P. cf.

capitata and P. cf. verrucosa had the highest

superficial growth compared with P. cf. dami-

cornis (Appendix 5). These results evidenced

that P. cf. capitata and P. cf. verrucosa could

have a greater competitive advantage than P.

cf. damicornis in terms of live tissue growth,

and perhaps, it can be more considerable to

increase live coral cover (Tortolero-Langarica

et al., 2017). It is known that the coral growth

is sometimes moderated by the need to increase

skeletal density mass to withstand hydrody-

namic forces and recovery rates (Chindapol et

al., 2013; Hughes, 1987; Lirman et al., 2010).

The latter is relevant because the water motion

and wave exposure effect strongly influences

the Isla Isabel area, so P. cf. capitata and P. cf.

verrucosa would have greater recovery, and

possibly better substrate colonization. Thus,

the coral morphology may be an important

factor influencing growth rates during coral

Fig. 3. Monthly seawater temperature (mean ± SD) of Isla Isabel National Park, Mexico.

Red dash and dotted lines represent mean annual ± SD temperatures, respectively.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

restoration, depending on physical environ-

mental factors to efficient metabolic pathways

(Wild et al., 2005). For example, P. damicornis

has more branching and three-dimensional

growth shape, while P. capitata and P. verru-

cosa keep all their energy growing vertically,

so this different morphology could affect their

growth rates. In other words, some corals grow

vertically to find the sun faster, and other

corals expand their branches to increase their

volume and surface to capture more solar ener-

gy. However, depending on the hydrodynamic

conditions, the coral colonies also modify their

shape; Thus, Pocillopora species could change

their morphology in months under different

flow regimes (Paz-García et al., 2015).

Similar coral growth was found between

natural and artificial substrata types through

using three coral morphospecies; However,

coral self-attachment was different (personal

authors’ observation) may be due to biofilms

and crustose coralline algae (CCA) that could

induce better coral self-attachment in natu-

ral substrate. This pattern coincides with the

Fig. 4. Comparison of coral growth rates between natural and artificial substrata. Black circles are natural substrates; white

circles are artificial substrates. Codes: Pd = Pocillopora cf. damicornis, Pc = Pocillopora cf. capitata, Pv = Pocillopora cf.

verrucosa.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

reported in other restoration studies where nat-

ural substrate promotes higher attachment rates

over any other substrate (Forrester et al., 2011;

Schlancher et al., 2007; Tortolero-Langarica

et al., 2014; Yap, 2004). However, the artifi-

cial substrate could be an alternative option

to incrementing habitat structural complexity,

promoting shelter, and improving biodiversity

(Schuhmacher et al., 2000; Tortolero-Langarica

et al., 2014). In this study, we used artificial

hollow hemispheres made with holes on the

sides with corals attached to steel-stacks, which

enhanced the habitat heterogeneity and favored

the coral growth and the coral-associated fauna.

The current context of coral reefs declin-

ing worldwide and the use of active coral

restoration strategies can mitigate the potential

coral ecosystem degradation (Manzello, 2010;

Fig. 5. Cumulative coral extension growth (mean ± SD) of Pocillopora species over one-year restoration using two different

substrates. Black circles = natural, and white triangles = artificial substrate.

Fig. 6. Relationship of annual coral growth parameters and sea surface temperature. Only significant regression models are

shown. Black circles are natural substrates; white circles are artificial substrates.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

Rinkevich, 2015). This work has shown that

developing coral reef restoration efforts using

Pocillopora coral fragments could be feasible

in CMP and potentially effective everywhere

in the ETP region. Our results correspond to

and support what was found by other studies

carried out in many sites in this region. In the

CMP, the transplanted Pocillopora fragments’

growth rates are similar to our estimates (Liñán-

Cabello et al., 2011; Tortolero-Langarica et al.,

2014) in natural (Liñán-Cabello et al., 2011)

and artificial substrata (Tortolero-Langarica et

al., 2014), as such as under ENSO conditions

(Tortolero-Langarica et al., 2017). Therefore,

the results of this work, and other studies that

have previously been done in many sites of the

ETP, allow recommending: i) to start the resto-

ration in the summer season because there were

the highest coral growth rates; ii) to use P. cf.

capitata and P. cf. verrucosa because these spe-

cies are more resistant to heat-waves exposure.

This information can increase yield and effec-

tiveness during coral restoration programs.

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.

ACKNOWLEDGMENTS

We thank J.A. Castrejón-Pineda, G. Pérez-

Lozano, and C. Robles-Carrillo for their help

and assistance during fieldwork at Isla Isabel.

We also thank J.P. Carricart-Ganivet, anony-

mous reviewers, and RBT editorial staff for

providing comments that improved this work.

This research was supported by Universidad de

Guadalajara (P3E-08634) and the Mexican gov-

ernment’s PRODEP program (103.5/08/2919).

This research was conducted by UDG-CA-888

and UDG-CA-942 academic groups of Univer-

sidad de Guadalajara.

Ver apéndice digital / See digital appendix

- a10v71s1-A1

REFERENCES

Allemand, D., Tambutté, É., Zoccola, D., & Tambutté, S.

(2011). Coral calcification, Cells to reefs. In Z. Dub-

insky, & N. Stambler (Eds.), Coral reefs: an ecosys-

tem in transition (pp. 119–150). Springer.

Álvarez-Filip, L., Dulvy, N. K., Gill, J. A., Côté, I. M., &

Watkinson, A. R. (2009). Flattening of Caribbean

coral reefs: region-wide declines in architectu-

ral complexity. Proceedings of the Royal Society,

276(1669), 3019–3025.

Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008).

PERMANOVA + for PRIMER: Guide to Software

and Statistical Methods. PRIMER-E: Plymouth, UK.

http://updates.primer-e.com/primer7/manuals/PER-

MANOVA+_manual.pdf

Badan, A. (1997). La corriente costera de Costa Rica en el

Pacífico mexicano. In M. F. Lavín (Ed.), Contribucio-

nes a la oceanografía física en México (pp. 141–171).

Unión Geofísica Mexicana.

Boch, C. A., & Morse, A. N. C. (2012). Testing the effec-

tiveness of direct propagation techniques for coral

restoration of Acropora spp. Ecological Engeneering,

40, 11–17.

Boström-Einarsson, L., Babcock, R. C., Bayraktarov, E.,

Ceccarelli, D., Cook, N., Ferse, S. C., Hancock, B.,

Harrison, P., Hein, M., Shaver, E., Smith, A., Suggett,

D., Stewart-Sinclair, P. J., Vardi, T., & McLeod, I. M.

(2020). Coral restoration- A systematic review of

current methods, successes, failures and future direc-

tions. PLoS ONE, 15 (1), e0226631.

Briggs, J. C., & Bowen, B. W. (2013). Marine shelf habitat:

biogeography and evolution. Journal of Biogeogra-

phy, 40(6), 1023–1035.

Carriquiry, J. D., Cupul-Magaña, A. L., Rodríguez-Zara-

goza, F. A. & Medina-Rosas, P. (2001). Coral blea-

ching and mortality in the Mexican Pacific during

the 1997-98 El Niño and prediction from a remote

sensing approach. Bulletin of Marine Science, 69(1),

237–249.

Chindapol, N., Kaandorp, J. A., Cronemberger, C., Mass,

T., & Genin, A. (2013). Modelling Growth and Form

of the Scleractinian Coral Pocillopora verrucosa and

the Influence of Hydrodynamics. PLoS Computatio-

nal Biology, 9(1) e1002849.

Comisión de Áreas Naturales Protegidas. (2005). Progra-

ma de Conservación y Manejo del Parque Nacional

Isla Isabel, México. Comisión de Áreas Naturales

Protegidas.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

Cruz-García, R., Rodríguez-Troncoso, A. P., Rodríguez-

Zaragoza, F. A., Mayfield, A., & Cupul-Magaña, A.

L. (2020). Ephemeral effects of El Niño Southern

Oscillation events on an eastern tropical Pacific

coral community. Marine and Freshwater Research,

71(10), 1259–1268.

Cupul-Magaña, A., & Calderón-Aguilera, L. (2008). Cold

water bleaching at Islas Marietas National Park,

Nayarit, México. In L. López & H. Bustos (Eds.),

Memoria XV Congreso Nacional de Oceanografía,

Veracruz, México.

De’ath, G., Lough, J. M., & Fabricius, K. E. (2009). Decli-

ning Coral Calcification on the Great Barrier Reef.

Science, 323(5910), 116–119.

Edwards, A. J. (2010). Reef rehabilitation manual. The

Coral Reef Targeted Research and capacity building

for management program.

Edwards, A. J., & Gomez, E. D. (2007). Reef restoration

concepts and guidelines: marking sensible manage-

ment choices in the face of uncertainty. Coral Reef

Targeted Research and Capacity Building for Mana-

gement Program.

Forrester, G. E., O’Connell-Rodwell, C., Baily, P., Forres-

ter, L. M., Giovannini, S., Harmon, L., Karis, R.,

Krumhols, J., Rodwell, T., & Jarecki, L. (2011).

Evaluating Methods for Transplanting Endangered

Elkhorn Corals in the Virgin Islands. Restoration

Ecology, 19(3), 299–306.

Galván-Villa, C. M., Arreola-Robles, J. L., Ríos-Jara, E.,

& Rodríguez-Zaragoza, F. A. (2010). Ensamblaje de

peces arrecifales y su relación con el hábitat bentó-

nico de la Isla Isabel, Nayarit, México. Revista de

Biología Marina y Oceanografía, 45(2), 311–324.

Glynn, P. W. (1977). Coral growth in upwelling and non-

upwelling areas of the Pacific coast of Panama. Jour-

nal of Marine Research, 35(3), 567–585.

Glynn, P. W. (2000). Effects of the 1997-98 El Niño

Southern-oscillation on Eastern Pacific corals and

coral reefs: an overview. In M. K. Moosa, S. Soemo-

dihardjo, A. Soegiarto, K. Romimohtarto, A. Non-

tji, Soekarno & Suharsono (Eds.), Proceedings of

the 9th International Coral Reefs Symposium, Bali,

Indonesia.

Glynn, P. W. (2001). Eastern Pacific coral reef ecosys-

tems. In U. Seeliger, & B. Kjerfve (Eds.), Coastal

Marine Ecosystems of Latin America (pp. 281–305).

Springer-Verlag.

Glynn, P. W., & Ault, J. S. (2000). A biogeographic analy-

sis and review of the far Eastern Pacific coral reef

region. Coral Reefs, 19, 1–23.

Godínez, V. M., Beier, E., Laven, M. F., & Kurczyn, J. A.

(2010). Circulation at the entrance of the Gulf of

California from satellite altimeter and hydrographic

observations. Journal of Geophysical Research, 115,

C04007.

Grigg, R. W. (2006). Depth limit for reef building corals

in the Au’au Channel, S.E. Hawaii. Coral Reefs, 25,

77–84.

Guzmán, H. M., & Cortés, J. (1989). Growth rates of eight

species of scleractinian corals in the eastern Pacific

(Costa Rica). Bulletin of Marine Science, 44(3),

1186–1194.

Harriot, V. J., & Fisk, D. A. (1988). Recruitment patterns of

scleractinians corals: a study of three reefs. Marine

and Freshwater Research, 39(4), 409–416.

Hermosillo-Nuñez, B., Rodríguez-Zaragoza, F., Ortiz, M.,

Galván-Villa, C., Cupul-Magaña, A., & Ríos-Jara,

E. (2015). Effect of habitat structure on the most

frequent echinoderm species inhabiting coral reef

communities at Isla Isabel National Park (Mexico).

Community Ecology, 16(1), 125–134.

Hernández-Zulueta, J., Rodríguez-Zaragoza, F. A., Araya,

R., Vargas-Ponce, O., Rodríguez-Troncoso, A. P.,

Cupul-Magaña, A. L., Díaz-Pérez, L., Ríos-Jara, E.,

& Ortiz, M. (2017). Multi-scale analysis of herma-

typic coral assemblages at Mexican Central Pacific.

Scientia Marina, 81(1), 91–102,

Hughes, T. P. (1987). Skeletal density and growth form of

corals. Marine Ecology Progress Series, 35, 259–266.

Hylkema, A., Hakkaart, Q. C. A., Reid, C. R., Osinga, A. J.,

Murk, A. J., & Debrot, A. O. (2021). Artificial reefs

in the Caribbean: a need for comprehensive monito-

ring and integration into marine management plans.

Ocean & Coast Management, 209, 105672.

Ishida-Castañeda, J., Pizarro, V., López-Victoria, M., &

Zapata, F. A. (2019). Coral reef restoration in the Eas-

tern Tropical Pacific: Feasibility of the coral nursery

approach. Restoration Ecology, 28(1), 22–28.

Jiménez, C., & Cortés, J. (2003). Growth of seven species

of scleractinian coral in an upwelling environment of

the eastern Pacific (Golfo de Papagayo, Costa Rica).

Bulletin of Marine Science, 72(1), 187–198.

Lindahl, U. (2003). Coral reef rehabilitation through

transplantation of staghorn corals effects of artificial

stabilisation and mechanical damages. Coral Reefs,

22, 217–223.

Liñán-Cabello, M. A., Flores-Ramírez, L. A., Laurel-

Sandoval, M. A., Mendoza, E., García, S., Olinda,

S., & Delgadillo-Nuño, M. A. (2011). Acclimation in

Pocillopora spp. during a coral restoration program

in Carrizales Bay, Colima, Mexico. Marine and

Freshwater Behavior and Physiology, 44 (1), 61–72.

Lirman, D., Thyberg, T., Herlan, J., Hill, C., Young-Lahiff,

C., Schopmeyer, S., Huntington, B., Santos, R., &

Drury, C. (2010). Propagation of the threatened

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

staghorn coral Acropora cervicornis: methods to

minimise the impacts of fragment collection and

maximise production. Coral Reefs, 29(3), 729–735.

Lough, J. M., & Cooper, T. F. (2011). New insights form

coral growth band studies in an era of rapid envi-

ronmental change. Earth Science Review, 108(3-4),

170–184.

Manzello, D. P. (2010). Coral growth with thermal stress

and ocean acidification: lessons from the eastern

tropical Pacific. Coral Reefs, 29, 749–758.

Marsh, J. A. (1970). Primary productivity of reef-building

calcareous red algae. Ecology, 51(2), 255–263.

Medellin-Maldonado, F., Cabral-Tena, R. A., López-Pérez,

A., Calderón-Aguilera, L. E., Norzagaray-López,

C. O., Chapa-Balcorta, C., & Zepeta-Vilchis, R.

C. (2016). Calcification of the reef-building coral

species on the Pacific coast of southern Mexico.

Ciencias Marinas, 42(3), 209–225.

Muñiz-Anguiano, D., Versuzco-Zapata, M., & Liñán-Cabe-

llo, M. A. (2017). Factors associated with response

Pocillopora spp. (Anthozoa: Scleractinia) during res-

toration process on the Mexican Pacific coast. Revista

de Biología Marina y Ocenografía, 52(2), 299–310.

Monchanin, C., Mehrotra, R., Haskin, E., Scott, C. M.,

Plaza P. U., Allchurch, A., Arnold, S., Magson, K., &

Hoedsema, B.W. (2021). Contrasting coral communi-

ty structures between natural and artificial substrates

at Koh Tao, Gulf of Thailand. Marine Environmental

Research, 172, 105505.

Nava, H., & Carballo, J. L. (2008). Chemical and mechani-

cal bioerosion of boring sponges from Mexican Paci-

fic coral reefs. The Journal of Experimental Biology,

211(17), 2827–2831.

Nava, H., & Figueroa-Camacho, A. G. (2017). Rehabilita-

tion of damaged reefs: Outcome of the use of recently

broken coral fragments and healed coral fragments of

pocilloporid corals on rocky boulders. Marine Ecolo-

gy, 38(5), 1–10.

NOAA (2022). El Niño/Southern Oscillation (ENSO).

National Centers for Environmental Information,

National Oceanic and Atmospheric Administration.

https://www.ncei.noaa.gov/access/monitoring/enso/

sst

Paz-García, D. A., Hellberg, M. E., García-de-León, F. J.,

& Balart, E. F. (2015). Switch between morphospe-

cies of Pocillopora corals. The American Naturalist,

186(3), 434–440.

Prachett, M. S., Anderson, K. D., Hoogenboom, M. O.,

Widman, E., Baird, A. H., Pandolfi, J. M., Edmunds,

P. J., & Lough, J. M. (2015). Spatial, temporal and

taxonomic variation in coral growth – Implica-

tions for the structure and function of coral reef

ecosystems. Oceanography and Marine Biology: An

Annual Review, 53, 215–295.

Rasband, W. S. (2012). Image J: Image processing and

analysis in Java. Astrophysics Source Code Library

[Computer Software]. Ascl-1206. https://imagej.nih.

gov/ij/

Rinkevich, B. (2014). Rebuilding coral reefs: Does active

reef restoration lead to sustainable reefs? Current

Opinion in Environmental Sustainability, 7, 28–36.

Rinkevich, B. (2015). Climate Change and Active Reef

Restoration –Ways of Constructing the “Reefs of

Tomorrow”. Journal of Marine Science and Enginee-

ring, 3(1), 111–127.

Rinkevich, B. (2019). The active reef restoration toolbox

is a vehicle for coral resilience and adaptation in

a changing world. Journal of Marine Science and

Engineering, 7(7), 201.

Rinkevich, B. (2020). Ecological engineering approaches

in coral reef restoration. ICES Journal of Marine

Science, 78(1), 410–420.

Ríos-Jara, E., Galván-Villa, C. M., & Solís-Marín, F. A.

(2008). Equinodermos del Parque Nacional Isla Isa-

bel, Nayarit, México. Revista Mexicana de Biodiver-

sidad, 79(1), 131–141.

Rodríguez-Zaragoza, F. A., Cupul-Magaña, A. L., Galván-

Villa, C. M., Ríos-Jara, E., Ortíz, M., Robles-Jarero,

E. G., López-Uriarte, E., & Arias-González, J. E.

(2011). Additive partitioning of reef fish diversity

variation: a promising marine biodiversity mana-

gement tool. Biodiversity Conservation, 20(8),

1655–1675.

Romero-Torres, M., Acosta, A., Palacio-Castro, A. M.,

Treml, E. A., Zapata, F. A., Paz-García, D. A., &

Porter, J. W. (2020). Coral reef resilience to thermal

stress in the Eastern Tropical Pacific. Global Change

Biology, 26(7), 3880–3890.

Schlancher, T. A., Stark, J., & Fischer, A. B. P. (2007).

Evaluation of artificial light regimes and substrate

types for aquaria propagation of the staghorn coral

Acropora solitaryensis. Aquaculture, 269, 278–289.

Schuhmacher, H., van Treeck, P., Eisinger, M., & Paster,

M. (2000). Transplantation of coral fragments from

ship groundings on electrochemically formed reef

structures. In M. K. Moosa, S. Soemodihardjo, A.

Soegiarto, K. Romimohtarto, A. Nontji, Soekarno &

Suharsono (Eds.), Proceedings of the 9th International

Coral Reefs Symposium, Bali, Indonesia.

Sheppard, C. R. C., Davy, S. K., & Pilling, M. (2010). The

biology of coral reefs. Oxford University Press.

Tortolero-Langarica, J. J. A., Cupul-Magaña, A. L., &

Rodríguez-Troncoso, A. P. (2014). Restoration of

a degraded coral reef using a natural remediation

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54738, abril 2023 (Publicado Abr. 30, 2023)

process: A case study from a Central Mexican Pacific

National Park. Ocean & Coastal Management, 96,

12–19.

Tortolero-Langarica, J. J. A., Rodríguez-Troncoso, A. P.,

Carricart-Ganivet, J. P., & Cupul-Magaña, A. L.

(2016). Skeletal extension, density and calcification

rates of massive free-living coral Porites lobata Dana,

1846. Journal of Experimental Marine Biology and

Ecology, 478, 68–76.

Tortolero-Langarica, J. A., Rodríguez-Troncoso, A. P.,

Cupul-Magaña, A. L., Alarcón-Ortega, L. C., &

Santiago-Valentín, J. D. (2019). Accelerated recovery

of calcium carbonate production in coral reefs using

low-tech ecological restoration. Ecological Enginee-

ring, 128, 89–97.

Tortolero-Langarica, J. J. A., Rodríguez-Troncoso, A. P.,

Cupul-Magaña, A. L., & Carricart-Ganivet, J. P.

(2017). Calcification and growth rate recovery of

the reef-building Pocillopora species in the northeast

tropical Pacific following an ENSO disturbance.

PeerJ, 5, e3191.

Tortolero-Langarica, J. A., Rodríguez-Troncoso, A. P.,

Cupul-Magaña, A. L., & Rinkevich, B. (2020).

Micro-Fragmentation as an Effective and Applied

Tool to Restore Remote Reefs in the Eastern Tropi-

cal Pacific. International Journal of Environmental

Research and Public Health, 17(18), 6574.

Van Oppen, M. J. H., & Blackall, L. L. (2019). Coral

microbiome dynamics, functions and design in a

changing world. Nature Reviews Microbiology, 17(9),

557–567.

Wild, C., Woyt, H., & Huttel, M. (2005). Influence of coral

mucus on nutrient fluxes in carbonate sands. Marine

Ecology Progress Series, 287, 87–98.

Yap, H. T. (2004). Differential survival of coral transplants

on various substrates under elevated water temperatu-

res. Science Direct, 49(4), 306–312.

Young, C. N., Schopmeyer, S. A., & Lirman, D. (2012). A

review of reef restoration and coral propagation using

the threatened genus Acropora in the Caribbean and

Western Atlantic. Bulletin of Marine Science, 88(4),

1075–1098.