Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54850, abril 2023 (Publicado Abr. 30, 2023)

Spatio-temporal variation in the growth of coral fragments of opportunity

in the Eastern Tropical Pacific: implications for coral reef restoration

Alma Paola Rodríguez-Troncoso1*; https://orcid.org/0000-0001-6243-7679

J. J. Adolfo Tortolero-Langarica2,3; https://orcid.org/0000-0001-8857-5789

Raúl Padilla-Guzmán1; https://orcid.org/0000-0002-6946-7798

Liza Danielle Kelly-Gutiérrez 4; https://orcid.org/0000-0002-1437-7517

Amílcar Leví Cupul-Magaña1; https://orcid.org/0000-0002-6455-1253

1. Laboratorio de Ecología Marina, Centro Universitario de la Costa, Universidad de Guadalajara, Puerto Vallarta,

Jalisco, Mexico; alma.rtroncoso@academicos.udg.mx (*Correspondence), raul.padilla.794@gmail.com,

amilcar.cupul@gmail.com

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

Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, Puerto Morelos, Mexico;

adolfo.tl@bahia.tecnm.mx

3. Tecnológico Nacional de México, Bahía de Banderas, Nayarit, México.

4. Departamento de Ciencias Biológicas, Centro Universitario de la Costa, Universidad de Guadalajara, Puerto Vallarta,

Mexico; lizadke@cuc.udg.mx

Received 22-VIII-2022. Corrected 09-XII-2022. Accepted 26-I-2023.

ABSTRACT

Introduction: Coral-reef communities are considered one of the most biodiverse, but also most threatened,

marine ecosystems, and the accelerating loss of habitat over the past decades warrants active intervention.

Objective: The present study demonstrates the successful implementation of a low-impact restoration technique

in three Central Mexican Pacific degraded coral communities, using a protocol based on natural fragmentation

(“fragments of opportunity”) of the branching coral Pocillopora spp., considered the most abundant and primary

carbonate-producing coral species of the Eastern Tropical Pacific.

Methods: The restoration program was implemented in two offshore and one inshore coraline areas. The rela-

tionships between seawater temperature and coral survival, growth, and attachment rate were assessed over one

year, with 183 fragments monitored each month.

Results: The mean coral growth rate was 3.3 ± 0.1 mm mo-1, with annual growth rates in length and width of

39.9 ± 14.2 and 36.5 ± 19.5 mm yr-1, respectively. Self-attachment efficiency was 78 % and the survival rate was

high (84 %). The growth rate differed significantly among reefs.

Conclusions: Upon monitoring directly fragmented corals over a year, growth rates were deemed high enough

to merit active restoration in the region. However, our data show that structural and abiotic differences and

seasonal variability must be considered overall in successful long-term coral community restoration initiatives

in the eastern Pacific region.

Key words: coral reef restoration; eastern tropical Pacific; fragments of opportunity; growth rate; marine ecol-

ogy; Pocillopora.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54850

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54850, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

Coral reefs are considered one of the

world’s most productive and biodiverse eco-

systems and provide important human services

(Spalding et al., 2001). Their high biodiversity

is related to the physical complexity of the reef

structure, benthic groups heterogeneity, and

architectural three-dimensionality, all depen-

dent upon coral accretion (Álvarez-Filip et al.,

2009). Unfortunately, coral communities are

also among the most threatened ecosystems

due to the cumulative effects of multiple natu-

ral and anthropogenic stressors that have led to

massive bleaching and mortality events world-

wide (Brainard et al. 2018; Spalding & Brown,

2015; Vargas-Ángel et al., 2019); over the past

20 years alone, at least 50 % of the coral reefs

have been lost, and the remaining 70-90 % are

considered to be highly threatened, becoming

urgent and an international priority for their

conservation (Souter et al., 2020)

Active restoration programs are now

frequently employed (Boström-Einarsoon et

al., 2020) as a tool to mitigate the loss of

coral cover by “outplanting” corals to where

ecosystem assemblage and function are re-

established (Bayraktarov et al., 2016; Edwards,

2010); complete reef rehabilitation is the long-

term goal of most such initiatives (Boström-

Einarsoon et al., 2020; Montoya-Maya et al.,

2016; Shackelford et al., 2013). However, fac-

tors such as community life history, historical

shifts in the local biota, spatio-temporal varia-

tion in regional- and local-scale environmental

conditions (particularly seawater quality), and

the physiology of the target restoration species

must all be considered prior to active restora-

tion efforts (Combilet et al., 2022; Montoya-

Maya et al., 2016; Suding, 2011).

Monitoring of outplants is imperative

(Guest et al., 2011; Shaish et al., 2008), as

the success of any restoration program does

not only depend on the technique initially

employed but also on the local response of the

coral species (Bayraktarov et al., 2016; Sund-

ing, 2011). Since coral growth and survival are

influenced by temperature, light, wave energy,

sedimentation, nutrients, pH, and aragonite sat-

uration state (Lough & Cooper, 2011; Manzello

et al., 2017), it is critical to demonstrate that the

RESUMEN

Variación espacio-temporal en el crecimiento de fragmentos de coral de oportunidad en el Pacífico

Tropical Oriental: implicaciones para la restauración de arrecifes de coral

Introducción: Las comunidades de arrecifes de coral se consideran uno de los ecosistemas marinos con mayor

biodiversidad, pero también los más amenazados, y la pérdida acelerada de hábitat en las últimas décadas justi-

fica la implementación de una intervención activa.

Objetivo: El presente estudio demuestra la implementación exitosa de una técnica de restauración de bajo impac-

to basada en la fragmentación natural (“fragmentos de oportunidad”) del coral ramificado Pocillopora spp., la

cual es la especie coralina más abundante y principal productora de carbonato del Pacífico Oriental Tropical.

Métodos: El programa de restauración se implementó en dos sitios lejos de la costa y un sitio cercano a la costa,

con comunidades coralinas degradadas. Las relaciones entre la temperatura del agua de mar y la supervivencia,

el crecimiento y la tasa de adhesión de los corales se evaluaron durante un año con 183 fragmentos monitoreados

cada mes.

Resultados: La tasa media de crecimiento coralino fue de 3.3 ± 0.1 mm mo-1, con tasas de crecimiento anual

en largo y ancho de 39.9 ± 14.2 y 36.5 ± 19.5 mm año-1, respectivamente. La eficiencia de la auto-adherencia

fue del 78 % y la tasa de supervivencia fue alta (84 %). La tasa de crecimiento difirió significativamente entre

los arrecifes.

Conclusiones: Al monitorear directamente los corales fragmentados durante un año, las tasas de crecimiento

se consideraron lo suficientemente altas como para merecer una restauración activa en la región. Sin embargo,

nuestros datos muestran que las diferencias estructurales y abióticas y la variabilidad estacional deben conside-

rarse en general en las iniciativas exitosas de restauración de comunidades de coral a largo plazo en la región

del Pacífico oriental.

Palabras clave: restauración de arrecifes de coral; Pacífico oriental tropical; fragmentos de oportunidad; tasa de

crecimiento; ecología marina; Pocillopora.

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outplants can acclimatize to what might be dis-

tinct conditions from where the source colonies

were obtained (Shackelford et al., 2013). Given

this, it is surprising that seasonal variation

has not been considered in the early stages of

restoration projects, especially given that coral

growth and survival may change over monthly

and annual timescales (Lough & Cooper, 2011;

Manzello et al., 2017; Romero-Torres et al.,

2020; Tortolero-Langarica et al., 2017).

Most coral restoration sites are located

in the Caribbean and Indo-Pacific regions

(Boström-Einarsoon et al., 2020), with few

efforts underway in the Eastern Tropical Pacif-

ic (ETP) despite the massive loss of coral cover

in the region that has occurred in recent years

(e.g., Carriquiry et al., 2001). Effective restora-

tion protocols recently implemented along the

ETP, though it is important to 1) select robust

corals and, 2) target the coral species that have

historically been distributed in the site to be

restored (Combilet et al., 2022; Ishida-Castañe-

da et al., 2020; Lizcano-Sandoval et al., 2018;

Nava & Figueroa-Camacho, 2017; Tortolero-

Langarica et al., 2014, Tortolero-Langarica et

al., 2019; Tortolero-Langarica et al., 2020).

Herein we used a low-impact approach to eval-

uate the growth of Pocillopora spp. outplants

over time in the Northeastern Tropical Pacific.

We hypothesized that seawater temperature

(SWT, i.e., season) and reef location (offshore

vs. inshore) could influence coral growth and

survival over the one-year monitoring period.

MATERIALS AND METHODS

The Central Mexican Pacific (CMP) har-

bors one of the most important coral communi-

ties in the ETP (Glynn & Ault, 2000). The coral

community of Islas Marietas National Park, an

Fig. 1. Study area. Offshore sites in Islas Marietas National Park (IMNP): Zona de Restauración (ZR) and Cueva del Muerto

(CM). Inshore reef: Punta de Mita (PM).

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offshore marine protected area (referred to as

simply “Islas Marietas” throughout the text)

located 7.9 km northeast (20.69 °N, 105.57

°W) to an inshore reef known as “Punta de

Mita” (PM, 20.76 °N, 105.54 °W). Both sites

(Fig. 1), used to maintain a coral cover of

nearly 40 % in the late 1990s, but mass coral

bleaching during the 1997-98 ENSO event led

to 90 % mortality (Carriquiry et al., 2001).

Afterwards, coral cover in the region showed

a continued decline in response to more fre-

quent, intense and, unpredicted stress events

(e.g., ENSO; Santoso et al., 2017) and local-

ized anthropogenic pressures (e.g., tourism,

overfishing, and coastal development); never-

theless, a slow but steady recovery in specific

areas have been recorded (Cupul-Magaña &

Rodríguez-Troncoso, 2017; Martínez-Castillo

et al., 2022), acting as a possible refuge of coral

reef organisms as observed in other subtropical

reefs, as long as management and conservation

strategies are implemented (Beger et al., 2014).

At Islas Marietas, the mean SWT is

~ 27 °C, with an annual range of 18-30 °C

(Palacios-Hernández et al., 2010). The coral

community is characterized as a patchy reef,

located between 1-15 m, with the highest live

coral cover, with high abundance of branching

corals ≤ 8 m depth (Hernández-Zulueta et al.,

2017), as also the presence of bare rock and

few dead coral skeletons (Sotelo-Casas et al.,

2019). The area is a touristic hotspot due to the

high quality seascape for SCUBA and free-div-

ing, which in past years have caused physical

damage to the coral colonies, and in addition

to other local-scale impacts such as seawater

pollution, led to the implementation of a pro-

gram designed to restrict the number of visitors

(Cupul-Magaña & Rodríguez-Troncoso, 2017).

The PM reef experiences even higher

anthropogenic pressure due to rapid coastal

urbanization, the development of golf courses,

and luxury tourist development (ECOPLAMB,

2004), which have become the main local

stressors as inorganic nutrient levels and sedi-

mentation have increased from terrestrial run-

off (Martínez-Castillo et al., 2020). The SWT

in situ averages ~ 26 °C, ranging from 20.8 to

30.6 °C (Palacios-Hernández et al., 2010). The

area used to harbor a well-developed shallow

reef patch with a ≈ 35 % of live coral cover-

age (Martínez-Castillo et al., 2022), which was

lost during the mass mortality associated to the

intense 1997-98 ENSO event (Carriquiry et al.,

2001), leaving a full path of dead coral matrix

as available substrata to transplant coral frag-

ments. The coral coverage has shown a slow

natural recovery; however, due to its depth (1-3

m) and proximity to the coast, it is considered

a highly vulnerable site, but with the poten-

tial to be restored despite these sub-optimal

local conditions (Martínez-Castillo et al., 2020;

Martínez-Castillo et al., 2022).

The sites to restore were selected accord-

ing to the following characteristics: 1) histori-

cal high coverage (over 30 %) of Pocillopora

spp. colonies and 8-10 % of healthy coral

coverage, 2) stable dead coral matrix or rocks

with cavities upon which coral fragments could

attach, 3) healthy fragments of opportunity. The

coral fragments are referred to as “fragments

of opportunity”, i.e., those detached from par-

ent colonies through natural processes such as

currents, swells, or bioerosion (Monty et al.,

2006). The restoration protocol was imple-

mented at two offshore sites from Islas Mari-

etas, Zona de Restauración (ZR) and Cueva del

Muerto (CM), as well as the only coastal patch

reef PM. Fragments were arranged in a total

area of 200 m2 at ZR (~5-7 m depth), 75 m2 at

CM (~ 4-6 m), and 125 m2 at PM (~ 2-3 m).

The reef restoration protocol was based on

the method described by Tortolero-Langarica

et al. (2014). Initially, fragments of opportunity

(50-100 mm in length), were collected near

the restoration area (no further than ≈ 50 m

away) and carefully inspected in situ to avoid

the use of no-healthy fragments with evidence

of bleaching, tissue damage, or bioeroding

sponges (e.g., Cliona spp.). Each healthy frag-

ment was fixed to the natural substrata using

plastic cable ties (sensu Edwards, 2010), either

in a horizontal or vertical orientation (depend-

ing on fragment morphology and substrate

geometry), to reach the best support (tightening

of the cable tie; Fig. 2A-D). During the first

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restoration effort, 183 fragments were tagged

and assessed monthly during a one-year period

(Fig. 2B) at ZR (n = 63), CM (n = 78), and PM

(n = 42). Individually, both length (maximum

linear distance from base to tip) and width

(maximum diameter perpendicular to the verti-

cal axis of the fragment) were measured using

plastic calipers (FOY 6”; precision = 0.05 mm;

Fig. 2C). Self-attachment was considered to

have occurred when evidence of calcification at

the base could be visualized and quantified as

a percent of fragments per month (% mo); the

survival rate was also recorded (%).

It is important to notice that the cable tie

was not removed as the fragment calcified

around it, and the removal could detach the

colony from the substrata; and it is a “visual

reference” to differentiate the natural recruited

from the transplanted colonies. In addition,

to continue with the restoration process after-

ward outplanting, 1 139 fragments were trans-

planted but not tagged across both inshore and

offshore sites.

In addition, sea water temperature (SWT)

was recorded in situ every 25 min with digital

loggers (HOBO® Pendant Onset) installed near

the fragments at each restoration site. Coral

growth was correlated with the season (Pala-

cios-Hernández et al., 2010), with a specific

emphasis on uncovering differences between

the temperate-dry season (January to May) and

the warm-rainy season (August to December).

Annual (mm yr-1) and monthly growth

(mm mo-1) rates were calculated, and all data

were tested for normality (P < 0.05) and

homogeneity of variance (P < 0.05) using

Fig. 2. Coral propagation technique. A) Coral vertically attached to rocky substrata (site: Cueva del Muerto). B) Example of

one-year coral colony after intervention; the cable tie stays within the colony for visual identification. C) Fragment measured

by using plastic calipers, D) Coral horizontally attached to dead stable coral matrix.

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Shapiro-Wilk and Levene’s tests, respectively.

Since data neither exhibited normal distribu-

tions nor homogeneous variances, non-para-

metric Kruskal-Wallis tests were instead used

to test for differences in coral growth over

time and across sites. Whenever results were

significant, post-hoc comparisons were calcu-

lated using Dunn’s tests (P < 0.05). Chi-squared

tests were used to compare attachment and

survivorship (rate and percentage, respectively)

Fig. 3. Coral fragment (%) survivorship and attachment. (A) Coral survivorship over one-year (2016-2017). (B) Coral

attachment efficiency, inshore reef: Punta de Mita (PM), offshore reefs: Zona de Restauración (ZR) and Cueva del

Muerto (CM).

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between sites and between seasons. A Mann-

Whitney test was used to compare coral growth

between Islas Marietas reefs (offshore) and

PM (inshore patch reef). All statistical analy-

ses were performed using SigmaPlot® ver. 11

(SPSS Inc., USA).for Windows, and an alpha

of 0.05 was set for all analyses.

RESULTS

At the end of the year, 84 % of the frag-

ments survived, and PM presented a survival

rate of ~ 75 % that was significantly higher

than the other two sites (X2 = 6.96, P < 0.05;

Fig. 3A). Also, differences in self-attachment

were observed between sites; at PM, fragments

attached after four months, with an overall

attachment rate of 83 % by the end of the year.

Meanwhile, ZR presented the lowest rates, as

the first fragments were attached after nine

months, and by the end of the year, only 36 %

were complete fixed to the substrata (Fig. 3B).

Seawater temperature was recorded for

both sites. Islas Marietas (offshore site) tem-

perature average was 27.07 ± 0.07 °C with the

minimum values during February (22.6 ± 0.02

°C) and a maximum in September (30.4 ± 0.01

°C). At PM (inshore site), the average SWT

was 27.6 ± 0.67 °C, and it ranged between

22.6-30.8 °C during the same months (Fig. 4).

Significant SWT differences were detected

between zones and seasons; the temperature’s

most noticeable difference was at ZR in the

warm-rainy season (H´ = 26.97 interaction

effect of season x site, P < 0.001).

The mean monthly coral growth rate was

of 3.3 ± 0.1 mm mo-1; the lowest growth rate

was recorded at ZR (2.3 ± 0.1 mm mo-1), and

the highest growth rate was recorded at PM

(4.3 ± 0.1 mm mo-1; Fig. 5A). Significant

differences were recorded among sites (H =

92.210, P < 0.001), with growth rates of corals

of ZR significantly lower. An overall difference

between the Islas Marietas sites and PM was

also observed (U-Mann = 22410, P < 0.001).

Finally, no variation in growth rate between

sites was observed (Fig. 5B).

After one-year intervention period, coral

growth ranged from 51.2 ± 1.7 to 82.4 ± 3.4

mm yr-1 in length and from 34.6 ± 2.0 to 66.1 ±

3.1 mm yr-1 in width (Fig. 6A). After one-year,

these corals presented an overall size increase

Fig. 4. Seawater temperature (mean ± SD) recorded in situ at Punta Mita inshore (PM = orange circles) and Islas Marietas

offshore (IM = yellow circles) restoration sites.

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of 63.7 % (pooled data), with higher growth

rates in PM (92 %) than in the colonies of

Islas Marietas (39 %). The annual accumulated

growth was 39.9 ± 11.5 mm yr-1 in length and

36.5 ± 19.5 mm yr-1 in width, with higher mean

values for PM (53.6 ± 12.7 mm yr-1) vs. the

two offshore reefs (31.8 ± 11.4 mm yr-1; H´ =

95.267, P < 0.001; Fig. 3), with no differences

between seasons (P > 0.05; Fig. 6B).

DISCUSSION

Asexual propagation is the method primar-

ily used in coral restoration programs (Boström-

Einarsson et al., 2020). Prior implementation is

important to clear out the motivation, variables,

and possible outcomes (Bayraktarov et al.,

2019; Suding et al., 2015). Both the method

of obtaining fragments (e.g., fragmentation of

Fig. 5. Growth (mm ± SE) of Pocillopora spp. fragments. A) mean monthly growth rate (mm mo-1 ± SE). B) mean annual

growth rate (mm yr-1 ± SE). Sites: Punta de Mita (PM), Zona de Restauración (ZR) and Cueva del Muerto (CM). Light color

bars = length, intense color bars = width. Asterisk (*) denote statistical differences between groups.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54850, abril 2023 (Publicado Abr. 30, 2023)

adult and healthy colonies), as well as the trans-

plantation, which usually includes the introduc-

tion of nurseries and, a posterior outplanting

phase, led to increasing the financial cost with

≥ 55 % of long-term survival rate (Bayraktarov

et al., 2016; Bayraktarov et al., 2019, Boström-

Einarsson et al., 2020). The ETP region’s

hydrodynamic conditions restrict the suitable

sites where nurseries or artificial reefs can be

installed (Combilet et al., 2022); therefore,

direct propagation has become one of the most

practical and standardized active restoration

strategies to rehabilitate coral communities

along the ETP (Lizcano-Sandoval et al., 2018;

Nava & Figueroa-Camacho, 2017; Tortolero-

Langarica et al., 2014; Tortolero-Langarica et

al., 2019). However, to increase the efficiency

before the propagation, fragments of opportu-

nity should be individually assessed to avoid

non-healthy fragments, use the in-site substrata

Fig. 6. Seasonal effects on coral growth (mean ± SE). A) inshore reef: Punta de Mita (PM), B) offshore reef: Zona de

Restauración (ZR) and Cueva del Muerto (CM). Colored bars = monthly growth, Closed red circles = seawater temperature.

Red asterisk (*) denote significant differences among seasons.

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(e.g., rock or dead coral matrix), and assume

that physiological indicators, such as growth,

survival, and resistance, will differ between

sites (in this case offshore and inshore coral

communities) and possibly over the years, as a

response to local and regional pressures. There-

fore, direct relocation of corals may require

local modifications to the protocol, including

the selection of substrata, use of tie wraps,

epoxy glue, marine cement, etc., according to

the site characteristics.

Restoration programs should prioritize the

biological assemblages, species composition

and representation to promote conditions from

historical trends (Guest et al., 2011; Suding et

al., 2015). The ETP reef and coral communi-

ties are considered mono-specific as Pocil-

lopora spp. is the most abundant reef-builder,

which, despite the effect of massive bleaching

and mortality events, has shown recently to

have high resistance and resilience to non-

optimal conditions (Manzello et al., 2017;

Rodríguez-Troncoso et al., 2016; Romero-

Torres et al., 2020). Besides their coverage,

branching corals have higher growth rates and

provide more available shelter or substrata to

other organisms than other local genera, such

as massive Pavona spp. or encrusting Porites

spp. (Lizcano-Sandoval et al., 2018; Nava &

Figueroa-Camacho, 2017; Tortolero-Langarica

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

Tortolero-Langarica et al., 2020), increasing

the relevance of promoting active protocols to

increase their presence in the coral community.

The results showed differences in growth

rate at the micro-scale level, despite their prox-

imity; and also, unexpectedly, the growth rates

were lower than those previously recorded in

the central Mexican Pacific (Nava & Figueroa-

Camacho, 2017; Tortolero-Langarica et al.,

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

growth responds to regional conditions and

global phenomena (Manzello et al., 2017;

Tortolero-Langarica et al., 2019), promoting

similar effects along the region; however, local

conditions (e.g., depth, wave action, nutrient

concentration, and space competitors) also

determines the growth rate (Lough & Cooper,

2011). A seasonal increase of nutrients in the

region can be caused by seasonal upwellings

(Palacios-Hernández et al., 2010), but at Punta

Mita the constant run-offs cause abnormal

high concentrations of inorganic nutrients and

sediments (Martínez-Castillo et al., 2020) from

fertilizers of the gulf course or discharged

from the touristic development (ECOPLAMB,

2004). Corals from Punta Mita exhibited a

higher growth rate than Islas Marietas colonies,

which is surprising as PM has been described

as a less-optimal site for coral development,

but the high light regime due to the low depth

and high nutrients, are beneficial conditions

for the endosymbionts and consequently ener-

gy translocated for growth (Fabricius, 2005;

Martínez-Castillo et al., 2020). Furthermore,

both conditions also contribute to the cor-

als’ ability to feed by suspension (Anthony &

Fabricius, 2000); however, the long-term effect

on coral skeletal density has to be determined,

as it can result in less dense and more fragile

skeletons, which can increase the vulnerability

of the reef framework (Chazottes et al., 2002;

Fabricius, 2005).

Both, short- and long-survival rates are

indicators of success (Bayraktarov et al., 2016).

The results showed a ≥ 83 % of survival, and

specifically, Punta de Mita showed a higher

survival rate than the offshore sites and high

self-attachment to the substrata. For restoration

purposes, fragment survival and attachment

depends as previously mentioned, by fragment

health but also the stress caused to corals due to

manipulation, depth, bio-erosion, macro-algal

competition, the proximity of reefs to sources

of anthropogenic stress and fragment size, yet

these were no evaluated herein (Bowden-Kerby,

2001; Guest et al., 2011; Shaish et al., 2008).

In addition, despite coral fragments used in

this study were visibly healthy and showed no

signs of bleaching, algal cover, or sponge, ~ 50

% of Pocillopora spp. coral colonies along the

ETP are invaded by Cliona vermifera, the most

abundant coral-excavating sponge (Alvarado

et al., 2017; Bautista-Guerrero et al., 2014),

which may compromise the coral colony struc-

ture and negatively impacts coral attachment.

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Seasonality could also be considered as

a determining factor in the success of the

restoration program as seawater temperature

is one of the most important factors for coral

growth, reproduction and survival (Anthony &

Fabricius, 2000). In the central Mexican Pacific

SWT range from 19 °C during the temperate-

dry season to 31 °C during the warm-rainy sea-

son, with daily minimum-maximum ranges of

5 °C, which are attributed to seasonal upwell-

ing and internal waves (Palacios-Hernández

et al., 2010). Our surveys show a higher

growth rate during the warm-rainy period,

which can be considered a regular pattern

(Tortolero-Langarica et al., 2017), as long as

the temperature does not overcome the species’

thermal threshold.

Therefore, ENSO-driven temperature

anomalies and the historical local resistance of

the corals should also be considered. As previ-

ously described, the 1997-98 El Niño event

elicited bleaching and massive mortality in

the region (Carriquiry et al., 2001), with evi-

dence of low but constant recovery at specific

sites along the ETP (Rodríguez-Troncoso &

Cupul-Magaña, 2016; Rodríguez-Troncoso et

al., 2016; Romero-Torres et al., 2020) although

the influence of quasi-oscillatory positive and

negative thermal anomalies occurring in the

region in an average period of 2 years (Palacio-

Hernández et al., 2010; Santoso et al., 2017).

The transplantation coincided with the 2015-

2016 El Niño event, so far considered the most

extreme of the 21st century (Santoso et al.,

2017), with a dramatic impact on coral reefs

along the equatorial Pacific (e.g., Brainard et

al., 2018, Vargas-Ángel et al., 2019). However,

at the CMP, the thermal anomalies did not

cause massive bleaching or mortality but can

explain the lower growth rates. Still, the surviv-

al rate is higher than the one recorded in other

studies (Bayraktarov et al., 2016; Boström-

Einarsson et al., 2020), and more importantly,

a positive growth rate during adverse global

and local (urban development and touristic

activities) conditions.

The correct implementation of a well-

structured restoration initiative and long-term

assessment and monitoring stand to bring eco-

logical and societal benefits, particularly in

regions characterized by high urban and touris-

tic pressures. Any restoration protocol must be

replicable at a regional level and have the flexi-

bility to consider the local characteristics of the

site. Before starting a restoration program, it is

suggested to evaluate the area and consider: 1)

presence of fragments of opportunity or donor

colonies, 2) the availability of natural substrata,

3) Evidence of low density of internal bioerod-

ers, 4) determining those sites that may be

donors but are not optimal for intervention, 5)

seasonal temperature fluctuation and nutrients

and sedimentation rate, and 6) the resistance or

ability to recover from stress conditions (e.g.,

ENSO events). The success of any restoration

program depends to a large extent on establish-

ing them in sites that show in their recent his-

tory a capacity for acclimatization to stressful

conditions, and when implemented in the con-

tinuous monitoring, as the goal is to reach the

self-sustaining, where human intervention is

minimal and only passive restoration tools are

necessary, assisting the recovery of the coral

coverage and the associated organisms but to

reach the rehabilitation of the site (Boström-

Einarsson et al., 2020). The Mexican central

Pacific has proven to be a reef area that can

be considered a coralline refuge, where active

restoration protocol should be planned for the

long term to ensure the maintenance of these

high-value ecosystems.

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

The present work was supported by a

National Geographic Society grant (W405-15

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54850, abril 2023 (Publicado Abr. 30, 2023)

and NGS-55349R-19) to APRT and by the

National Commission of Natural Protected

Areas (CONANP) with the project CONANP-

PROCER/CCER/DROPC/09/2016 to ACM.

The authors thank the authorities of the Islas

Marietas National Park (CONANP) and Protec-

ción y Restauración de Islas y Zonas Naturales

(PROZONA A.C.) for their assistance with

field operations.

Author contributions: RPG, APRT,

ALCM conceived and designed the research;

RPG, APRT, ALCM JJATL performed the

fieldwork and obtained the data; RPG, APRT,

JJATL, LDKG analyzed the data; APRT, ALCM

contributed materials and field trips; RPG,

APRT, JJATL wrote and edited the manuscript.

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