Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Nursery-reared coral outplanting success in

an upwelling-influenced area in Costa Rica

Sònia Fabregat-Malé1*; https://orcid.org/0000-0001-6764-0502

Sebastián Mena2; https://orcid.org/0000-0002-1403-5533

Juan José Alvarado3,4,5; https://orcid.org/0000-0002-2620-9115

1. Posgrado en Biología, Sistema de Estudios de Posgrado, Universidad de Costa Rica, San Pedro, San José 11501-2060,

Costa Rica; sonia.fabregat@ucr.ac.cr (*Correspondence)

2. Posgrado en Gestión Integrada de Áreas Costeras Tropicales, Universidad de Costa Rica, San Pedro, San José 11501-

2060, Costa Rica; sebas.menago@gmail.com

3. Escuela de Biología, Universidad de Costa Rica, San Pedro, San José 11501-2060, Costa Rica;

juan.alvarado@ucr.ac.cr

4. Centro de Investigación en Biodiversidad y Ecología Tropical (CIBET) (previously Museo de Zoología), Escuela de

Biología, Universidad de Costa Rica, San Pedro, San José 11501-2060, Costa Rica.

5. Centro de Investigación en Ciencias del Mar y Limnología (CIMAR), Universidad de Costa Rica, San Pedro, San José

11501-2060, Costa Rica.

Received 27-VIII-2022. Corrected 09-II-2023. Accepted 14-II-2023.

ABSTRACT

Introduction: Environmental and intrinsic factors such as seawater temperature, salinity, nutrient concentration,

upwelling, species, and life history can influence coral outplant survival and growth, and in consequence, the

effectiveness of restoration. Thus, it is key to understand how these factors can shape coral outplant performance

to ensure the long-term success of a restoration program.

Objective: To establish the survival and growth rate of outplanted coral nursery-reared colonies of branching

Pocillopora spp. and massive corals Pavona gigantea, Pavona clavus, and Porites lobata in Bahía Culebra,

North Pacific of Costa Rica, and to determine whether the site of origin of the coral fragment and the presence

of seasonal upwelling affected the growth of Pocillopora outplants.

Methods: From September 2020 to September 2021, we monitored the survival, health, and growth of 30

Pocillopora spp. colonies from six donor sites, and 31 fragments of massive species (P. gigantea [n = 18], P.

clavus [n = 8], P. lobata [n = 5]) that were outplanted to a degraded reef. We recorded in situ seawater tempera-

ture, salinity, and nutrient concentration.

Results: By the end of the year, 100 % of the Pocillopora spp. outplants survived. Survival was 71.4 % for P.

clavus, 47.5 % for P. gigantea, and 20 % for P. lobata. Coral tissue loss and predation marks were observed at

least once in 71 % of massive outplants. Pocillopora spp. colonies increased their initial area in 333.1 %, at a rate

of 9.98 ± 1.69 cm yr-1. The site of origin of the outplant influenced growth rate, but not the presence of seasonal

upwelling. Massive species fragments grew at a rate of 1.35 ± 0.24 cm yr-1 for P. clavus, 1.48 ± 0.21 cm yr-1 for

P. gigantea, and 0.61 cm yr-1 for P. lobata, with no differences among them.

Conclusions: Environmental conditions at site level allow for high survival and growth of Pocillopora spp.

outplants, previously considered as sensitive to stressors, and point towards acclimation to seasonal upwelling.

Although survival of massive species was lower, developing a multi-species approach is key to enhance restora-

tion success.

Key words: Bahía Culebra; coral reef; coral gardening; Eastern Tropical Pacific; ecological restoration;

growth rate.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54879

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

As coral reefs worldwide are declining,

active solutions have been developed over the

last few decades in order to reverse this alarm-

ing trend and restore the function of these

ecosystems (Hughes et al., 2019; Lirman &

Schopmeyer, 2016; Unsworth et al., 2020).

Coral gardening is a popular technique to

reestablish coral populations and increase coral

cover (Ladd et al., 2018; Rinkevich, 1995);

this strategy uses fragments from wild donor

colonies and grows them in nurseries, followed

by their outplanting to a degraded reef (Rinkev-

ich, 2014). Even though the nursery stage of

coral restoration and propagation methodolo-

gies are well-established, outplanting success

can vary, with an average survival of 66 % of

the outplanted corals (Boström-Einarsson et

al., 2020), but with some projects reporting

a higher survival of up to 89 % (Ware et al.,

2020). However, the time frame considered

to monitor outplant survival is often short,

as most projects do so during a 12-month

period (Boström-Einarsson et al., 2020). Coral

outplants can undergo rapid mortality due to

several stressors, both abiotic and biotic, such

as temperature, disease, predation, and pres-

ence of competitor species (Cano et al., 2021;

Foo & Asner, 2020; Hughes et al., 2017; Koval

et al., 2020; Miller et al., 2014; van Woesik et

al., 2017; Ware et al., 2020). Hence, there is

increasing interest in developing techniques

that could improve the efficiency and long-

term success of such efforts (Lohr et al., 2020).

RESUMEN

Éxito de trasplante de colonias de coral cultivadas en vivero en un área influenciada

por afloramiento en Costa Rica.

Introducción: Factores ambientales e intrínsecos como la temperatura del agua, salinidad, concentración de

nutrientes, afloramiento, especies e historia de vida pueden influir en la supervivencia y crecimiento de los

trasplantes de coral y, en consecuencia, en la eficacia de la restauración. Por ello, entender cómo estos factores

pueden moldear el desempeño de los trasplantes es clave para asegurar el éxito de un programa de restauración

a largo plazo.

Objetivo: Establecer la supervivencia y tasa de crecimiento de los trasplantes de colonias de coral previamente

cultivadas en viveros del coral ramificado Pocillopora spp. y las especies de crecimiento masivo Pavona gigan-

tea, Pavona clavus y Porites lobata en Bahía Culebra, Pacífico Norte de Costa Rica, y determinar si el sitio

donante de origen del fragmento de coral y la presencia de afloramiento estacional afectó el crecimiento de los

trasplantes de Pocillopora.

Métodos: De setiembre 2020 a setiembre 2021, se monitoreó la supervivencia, salud y crecimiento de 30 colo-

nias de Pocillopora spp. de seis sitios donantes diferentes y 31 fragmentos de especies masivas (P. gigantea [n =

18], P. clavus [n = 8], P. lobata [n = 5]) que se trasplantaron a un arrecife degradado. Se registró la temperatura

del agua, la salinidad y concentración de nutrientes in situ.

Resultados: Al final del año, el 100 % de los trasplantes de Pocillopora spp. sobrevivieron. La supervivencia

fue de 71.4 % para P. clavus, 47.5 % para P. gigantea y 20 % para P. lobata. Se observaron pérdidas de tejido y

marcas de depredación al menos una vez en un 71 % de los trasplantes masivos. Las colonias de Pocillopora spp.

aumentaron su área inicial en un 333.1 %, a una tasa de 9.98 ± 1.69 cm año-1. El sitio de origen del trasplante tuvo

efecto sobre la tasa de crecimiento, pero no la presencia de afloramiento estacional. Los fragmentos de especies

masivas crecieron a tasas de 1.35 ± 0.24 cm año-1 (P. clavus), 1.48 ± cm año-1 (P. gigantea) y 0.61 cm año (P.

lobata), sin diferencias entre ellas.

Conclusiones: Las condiciones del sitio permiten una alta supervivencia y crecimiento de trasplantes de

Pocillopora spp., que previamente habían sido considerados sensibles a factores estresantes, e indican aclimata-

ción a las condiciones locales de afloramiento estacional. Pese a que la supervivencia de las especies masivas fue

menor, es esencial desarrollar un enfoque multi-especie para aumentar el éxito de la restauración.

Palabras clave: Bahía Culebra; arrecife coralino; jardinería de coral; Pacífico Tropical Oriental; restauración

ecológica; tasa de crecimiento.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Several techniques exist for outplanting

coral colonies or fragments onto either suitable

natural reef substrate or artificial structures

(Ferse et al., 2021). Most restoration practitio-

ners use marine epoxy, cable ties, steel cables

or nails to attach corals onto the substrate

(Boström-Einarsson et al., 2020; Goergen &

Gilliam, 2018; Omori, 2019). Which technique

is the most appropriate is highly site-specific,

depending on the type of substrate, currents,

wave action, herbivore presence, and even

colony size and density (Goergen & Gilliam,

2018; van Woesik et al., 2017). Thus, these

considerations should be taken into account

for the outplanting design before scaling up

outplanting efforts.

Therefore, the success of the outplanting

stage will also be inevitably affected by the

appropriate selection of the outplanting site,

which must gather conditions that promote

coral survival and growth (see Kleypas et al.,

1999). These include environmental factors

such as seawater temperature (Coles & Jok-

iel, 1978; Foo & Asner, 2020), pH (Kleypas

& Yates, 2009), nutrients, salinity (D’Angelo

& Wiedenmann, 2014; Faxneld et al., 2010;

Wiedenmann et al., 2013), and light (Coles

& Jokiel, 1978; Foo & Asner, 2021); and bio-

logical factors like the presence of associated

organisms such as fish, invertebrates, and other

benthic groups (Cano et al., 2021; Rivas et al.,

2021). Furthermore, intrinsic factors such as

the coral species, life history, acclimation to

local conditions, and genotype have an equally

important role in shaping restoration outcomes

(Baums et al., 2019; Goergen & Gilliam, 2018;

Lirman et al., 2014).

Once transplanted, monitoring coral out-

plants is key for measuring outplanting suc-

cess and thus, evaluating restoration efforts

(Edwards, 2010; Foo & Asner, 2020). Despite

the lack of standardised monitoring guide-

lines, outplant survival and growth rate are

some of the most widely used assessments for

this purpose (Hein et al., 2017; Edmunds &

Putnam, 2020).

In the Eastern Tropical Pacific (ETP), coral

restoration experiences are limited compared

to other regions such as the Indo-Pacific and

Caribbean region (Bayraktarov et al., 2020).

In recent years, however, restoration initiatives

in the ETP are rapidly increasing, and most

of them focus on the branching coral genus

Pocillopora (Chomitz, 2021; Combillet et al.,

2022; Ishida-Castañeda et al., 2020; Liñán-

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

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

transplantation in the Central Mexican Pacific

showed a survival rate between 89–95.5 % over

270 days (Liñán-Cabello et al., 2011), which go

in concordance with results in Colombia, which

show 100 % survival after 5-months using

nursery-reared Pocillopora fragments (Ishida-

Castañeda et al. 2020), with higher growth

rates than direct transplants. Outplanting using

micro-fragmentation has only been implement-

ed once in the ETP (Tortolero-Langarica et

al., 2020), but never in Costa Rica, where only

two studies have focused on Pocillopora spp.

outplanting success; Guzmán (1991) reported

a 79-83 % survival in Caño Island, while Cho-

mitz (2021) reports 83 % survival and an aver-

age 68 % growth in area along eight months of

study in Golfo Dulce, both in the South Pacific

of the country. However, this data cannot

be extrapolated as environmental conditions

between areas of the Pacific coast of Costa

Rica are different, as are reef dynamics and the

main coral reef-building species, mainly due to

the presence of a seasonal upwelling and lower

precipitation in the North Pacific of the country

(Cortés et al., 2010).

This study represents the assessment of

the first restoration project in the area, in

order to evaluate the outplanting success of the

first nursery-reared corals outplanted onto a

degraded reef, therefore we aimed to (1) moni-

tor the health and survival of outplanted colony

fragments of the branching Pocillopora spp.

and massive Pavona gigantea (Verrill, 1869),

Pavona clavus (Dana, 1846) and Porites lobata

(Dana, 1846) corals in Bahía Culebra, North

Pacific of Costa Rica, (2) quantify the growth

rate of outplanted corals in terms of area and

diameter and (3) determine whether the origin

(donor colonies sites) of the coral fragment and

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

presence of upwelling have an effect on coral

growth for Pocillopora spp. colonies, one year

post-outplanting.

MATERIALS & METHODS

Study area: Bahía Culebra (10°37’N -

85°39’W) is a semi-enclosed bay in the Gulf

of Papagayo, North Pacific of Costa Rica (Fig.

1). The bay extends for more than 20 km2,

and reaches its maximum depth at about 42

m (Rodríguez-Sáenz & Rodríguez-Fonseca,

2004). It is influenced by seasonal upwelling

from December to April, causing a decrease

in seawater temperature up to 10 ºC from the

annual mean (27 ± 0.1 ºC) (Jiménez, 2001;

Jiménez et al., 2010), and bringing up more

acidic (pH 7.8) nutrient-rich waters (Rixen

et al., 2012; Sánchez-Noguera et al., 2018b;

Stuhldreier et al., 2015).

Bahía Culebra once harboured some of the

most extensive coral reefs on the Pacific coast

of the country, mainly built by the branching

coral Pocillopora, with high live coral cover

(44.0 ± 0.3 %) (Jiménez 2001; Cortés & Jimé-

nez, 2003). However, in the last two decades,

coral reefs in the bay experienced intense coral

bleaching and mass coral mortality (Sánchez-

Noguera, 2012) caused by El Niño South-

ern-Oscillations (ENSO) events, increase in

anthropic eutrophication and frequent harmful

algal blooms (Fernández, 2007; Jiménez, 2007;

Sánchez-Noguera, 2012), resulting in an abrupt

loss of coral cover. This situation favoured the

recruitment and proliferation of macroalgae

(Alvarado et al., 2018; Fernández-García et al.,

2012), and a cascading effect on high densi-

ties of the sea urchin Diadema mexicanum (A.

Agassiz, 1863). As a consequence of sea urchin

bioerosion, the coral framework weakened and

was undermined (Alvarado et al., 2012; Alvara-

do et al., 2016). In order to mitigate the dam-

age, a coral restoration project was initiated in

Bahía Culebra in September 2019, by using

Fig. 1. Location of Güiri-Güiri outplanting site (yellow square), Jícaro nursery site (red star), and donor colonies sites (blue

dot) in Bahía Culebra, North Pacific of Costa Rica.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

coral gardening techniques and a subsequent

transplant to nearby sites in the bay (Fabregat-

Malé et al., in prep.).

Experimental design: The species of cor-

als used in this study were the branching Pocil-

lopora genus, and the massive P. gigantea, P.

clavus, and P. lobata. Here, we worked with

Pocillopora damicornis (Linnaeus, 1758) and

Pocillopora elegans (Dana, 1846). To visually

distinguish these species based on their mor-

phology is equivocal (Pinzón et al., 2013); thus,

considering their functional and genetic simi-

larities (Pinzón & LaJeunesse, 2011; Pinzón

et al., 2013), they were grouped and further

referred as “Pocillopora spp.”. Coral fragments

had been previously obtained from donor colo-

nies on different reefs and coral communities

around Bahía Culebra (Fig. 1). Donor colonies

were randomly selected at depths between 2-7

m, growing at least 5 m from each other so as to

maximize chances of sampling distinct genets.

For Pocillopora spp., five fragments of about

2–5 cm were originally extracted from each

donor colony, while for massive species (P. cla-

vus, P. gigantea and P. lobata), microfragments

of around 1.5–2 cm2 were obtained, using a dia-

mond band saw (Model C-40, Gryphon, USA)

(Fabregat-Malé et al., in prep.).

Nursery-reared coral colonies were out-

planted in September 2020 to Güiri-Güiri reef

(10° 36’ 49.7” N, 85° 41’ 24.1” W), in Bahía

Culebra (Fig. 1), after a one-year cultivation in

the nurseries. The reef formation in Güiri-Güiri

is mainly built by dead Pavona framework,

and some sparse Pocillopora, P. gigantea and

P. clavus colonies (Jiménez, 1997; Jiménez,

2007). Coral colonies were outplanted at 5 m

depth and on dead coral substrate, comprising

an area of approximately 100 m2 on the back-

reef area.

A total of 30 Pocillopora spp. colonies

were tagged and outplanted onto the dead

coral substrate using steel nails and cable ties

(Fig. 2A), with a minimum distance of 50 cm

from each other. Nursery-reared Pocillopora

spp. colonies originally came from six differ-

ent donor sites on the bay (Fig. 1): Matapalo

(n = 11), Sombrero (n = 7), Esmeralda (n =

4), Jícaro (n = 4), Güiri-Güiri (n = 3), Palmi-

tas (n = 1). For the massive coral species, an

underwater drill (Nemo V2, NemoPowerTools,

USA) was used to outplant 31 fragments (n =

18 P. gigantea fragments, n = 8 P. clavus, and

n = 5 P. lobata), which were then fixed to the

substrate using marine epoxy glue (Marine-

Tex, USA) (Fig. 2B). The small sample sizes

of massive species used during outplanting are

due to their low survival in the nursery stage

(Fabregat-Malé et al., in prep.). Massive frag-

ments from the same species and genotype

(i.e., donor colony) were outplanted together (2

cm apart) so as to promote fusion when grow-

ing (Forsman et al., 2015).

Fig. 2. A. Outplanting technique for nursery-reared Pocillopora spp. colonies and B. for massive species (Porites lobata,

Pavona gigantea and Pavona clavus) fragments, in Güiri-Güiri reef, Costa Rica.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Monitoring occurred monthly post-

outplanting for 12 months, from September

2020 to September 2021. The survival of each

individual colony and fragment (alive, pale/

bleached, dead or lost) was recorded, as well as

partial tissue mortality. Coral growth was also

recorded monthly, establishing a photoquadrat

around each colony using a polyvinyl chloride

(PVC) frame (30x30 cm) that held the camera

above the substrate and the coral colonies. Pho-

tographs were taken from the same angle and

direction, with a scaling object, using a Nikon

COOLPIX W300 underwater camera. Each

image was analysed using the photo-analysis

software PhotoQuad (Trygonis & Sini, 2012),

in order to calculate the area of outplanted

coral colonies (cm2) and colony diameter (cm),

evaluating lateral growth of colonies. Addition-

ally, sea urchin D. mexicanum density was

also censed, using belt-transects 10 x 2 m (20

m2) along the outplanting area, and used as an

indicator of bioerosion and potential population

controller of other groups (i.e., macroalgae and

turf) through herbivory (Alvarado et al., 2012).

To determine the environmental condi-

tions to which coral outplants were subject,

seawater temperature at site was recorded every

30 min using HOBO® data loggers. Six water

samples were collected in situ monthly to deter-

mine salinity (PSU) and nutrient concentration

(NO3-, NO2-, PO43-, NH4+, and SiO4), using

a plastic syringe with a 1 µm glass microfi-

ber filter, and were later processed using a

field refractometer (PCE-0100, PCE Instru-

ments, Germany) and a continuous flow auto-

analyzer (QuikChem 8500, Lachat Instruments,

USA), respectively.

Data analysis: Survival curves between

species were compared using a Kolmogorov-

Smirnov (KS) test. Lost fragments were con-

sidered as “dead” for calculating survival rates.

Differences in outplant size from initial to final

month were analysed using a Student’s t-test.

Growth rate of coral outplants was calculated

over the first year after transplantation; the

area (cm2) and diameter (cm) of each Pocil-

lopora spp. colony and massive fragment were

subtracted from the measurement of the follow-

ing month. Growth rate results from colonies

and fragments that had survived throughout

monitoring period. Pocillopora spp. growth

rates (cm mo-1) between upwelling and non-

upwelling season were compared using a Stu-

dent’s t-test. Differences in Pocillopora growth

rate (cm2 mo-1) between sites of origin of

Fig. 3. Cumulative survivorship (%) of massive coral fragments (Pavona clavus n = 8, in red; Pavona gigantea n = 18,

in yellow; and Porites lobata n = 5, in blue) in the outplanting site of Güiri-Güiri, Costa Rica, through monitoring period

(September 2020-September 2021).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

donor colonies were analyzed using a one-way

ANOVA, followed by Tukey HSD post-hoc

tests. Palmitas was excluded as a donor site

from this analysis as only one colony from

this site was outplanted. Growth rates between

massive species were also compared using a

non-parametric Kruskal-Wallis test. Data were

tested for normality and equality of variances

using the Shapiro-Wilk test and Bartlett test,

respectively, to ensure they met model assump-

tions. Statistical analyses were performed using

R (R Core Team, 2021).

RESULTS

Outplant survival: Exactly one year after

their transplantation to the Güiri-Güiri reef, 100

% of the Pocillopora spp. outplants survived,

none were lost, and no bleaching occurred.

When grouping massive species together, over-

all survival by the end of the first year was

48.4 % (P. clavus = 71.4 %, P. gigantea = 47.5

%, and P. lobata = 20.0 %) (Fig. 3). Decrease

in massive species survival was a result of the

loss of fragments during monitoring period,

not their death. This decline in survival in mas-

sive species was most pronounced in August

2021. Survival curves significantly differed

only between P. clavus and P. lobata (D =

0.727, P < 0.05). Partial mortality and preda-

tion marks were only observed in outplants of

massive species, with 22 fragments (71 %) hav-

ing experienced partial tissue loss at least once

during monitoring period (Fig. 4). Paleness in

P. lobata fragments was observed in December

2020, but fragments recovered their coloration

the following month.

Outplant growth: Pocillopora spp. colo-

nies were initially 63.24 ± 36.48 cm2 (8.66 ±

2.38 cm in diameter). One year after outplant-

ing, colonies significantly grew to 273.91 ±

105.81 cm2 and 18.64 ± 3.46 cm in diameter

(F1,58 = 106.3, P < 0.005) (Fig. 5). This repre-

sents a 333.1 % increase in area, and a 115.2

% increase in diameter from initial size. The

rate of change in area of the Pocillopora spp.

outplants was calculated to be 17.56 ± 6.28 cm2

mo-1 (9.98 ± 1.69 cm yr-1) (Table 1).

Despite the loss, massive species sig-

nificantly increased their area from initial size

in 157.3 % for P. gigantea fragments (R2 =

0.6421, F1,147 = 266.6, P < 0.005), 161.6 %

for P. clavus (R2 = 0.7496, F1,76 = 231.5, P <

0.005), and 70.4 % in P. lobata (R2 = 0.5452,

Fig. 4. Percentage (%) of outplanted fragments of massive species (Pavona clavus, in red; Pavona gigantea, in yellow; and

Porites lobata, in blue) exhibiting partial tissue loss through monitoring period (September 2020 to September 2021) in

Güiri-Güiri reef, Costa Rica.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

F1,25 = 32.17, P < 0.005). Growth rates for

massive species were 1.35 ± 0.24 cm yr-1 for

P. clavus, 1.48 ± 0.21 cm yr-1 for P. gigantea

and 0.61 cm yr-1 for P. lobata (Fig. 6, Table 1).

Growth rates between massive species did not

differ statistically (F2,220 = 2.934, P = 0.0553).

Monthly average growth rate of Pocil-

lopora spp. outplants showed statistical

differences through time, with a post-hoc Tukey

test revealing lower growth rates in October

2020 (P = 0.0941).

Outplant growth and environmental con-

ditions: Mean seawater temperature in the

outplanting site was 27.75 ± 1.90 ºC, with a

minimum of 19.08 ºC and a maximum of 30.52

ºC (Appendix 1). Significant differences in

Fig. 5. A. Increase of Pocillopora spp. colony area (cm2) from September 2020 to September 2021, B. and growth of the

same Pocillopora spp. outplant at the start of monitoring period (left), after six months (middle), and after one year (right),

in the outplanting site in Güiri-Güiri reef, Costa Rica.

TABLE 1

Initial and final sizes (mean area and diameter ± SD), and mean growth rate (± SD)

of outplanted species to Güiri-Güiri restoration site, Costa Rica.

Species Initial size Final size Growth rate (cm2 yr-1)

Area (cm2)Diameter (cm) Area (cm2)Diameter (cm)

Pocillopora spp. 63.24 ± 36.48 8.66 ± 2.38 273.91 ± 105.81 18.64 ± 3.46 210.67 ± 75.41

Pavona gigantea 5.29 ± 1.25 2.24 ± 0.28 13.61 ± 2.87 4.11 ± 0.35 8.18 ± 2.29

Pavona clavus 4.37 ± 0.91 2.37 ± 0.49 11.43 ± 1.43 3.80 ± 0.20 6.69 ± 1.63

Porites lobata 4.60 ± 1.25 2.40 ± 0.35 7.84 3.16 2.77

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

temperature between upwelling (26.47 ± 1.87

ºC) and non-upwelling season (29.00 ± 0.76

ºC) were detected (t11437 = 117.08, P < 0.0005).

Mean seawater salinity was 33.18 ± 1.05 PSU,

and was significantly higher during dry season

(33.72 ± 0.81 PSU) than during rainy season

(32.71 ± 0.72 PSU) (t369.47 = -12.906, P <

0.005) (Appendix 2). Nutrient concentration

was highly variable and did not show any pat-

tern (Appendix 3). Nitrate was the only nutrient

whose concentration differed between upwell-

ing and non-upwelling season, with higher

concentrations during the non-upwelling rainy

season (F1,11 = 6.667, P < 0.05, Table 2).

Despite the observed environmental differences

between upwelling and non-upwelling season,

Pocillopora spp. growth rate was not affected

(F1,358 = 2.955, P = 0.0865).

Finally, mean density of Diadema mexi-

canum in the outplanting area was 21.71 ±

1.48 ind m-2.

Influence of sites of origin on Pocillopora

spp. outplant growth: Growth rate of Pocil-

lopora spp. coral colonies differs by site of

origin (F5,354 = 10.13, P < 0.005) (Fig. 7A), as

Matapalo outplants presented a higher growth

rate (23.81 ± 17.56 cm2 mo-1, or 285.66 ± 69.82

cm2 yr-1) than the rest of the donor sites (overall

Fig. 6. Changes in area (cm2) of outplanted fragments of massive fragments (Pavona clavus, in red; Pavona gigantea,

in yellow; and Porites lobata, in blue) over monitoring period (September 2020-September 2021) in Güiri-Güiri reef,

Costa Rica.

TABLE 2

Nutrient concentration (µM) in outplanting site Güiri-Güiri, Costa Rica, from September 2020 to September 2021.

Nutrient Mean (± SD) Maximum Minimum Upwelling season

(mean ± SD)

Non-upwelling season

(mean ± SD)

Nitrate (NO3-)3.82 ± 2.06 7.23 1.30 2.51 ± 0.33* 4.95 ± 2.28*

Nitrite (NO2-)3.03 ± 0.38 3.79 2.48 2.85 ± 0.22 3.19 ± 0.43

Phosphate (PO43-)0.13 ± 0.13 0.34 UDL 0.16 ± 0.17 0.11 ± 0.09

Ammonium (NH4+)4.76 ± 1.17 6.71 2.93 5.18 ± 1.26 4.40 ± 1.04

Silicate (SiO4)1.97 ± 2.83 7.93 UDL 2.02 ± 3.34 1.93 ± 2.59

Upwelling season: November to April; Non-upwelling season: May to October. UDL = under detection limit (0.48 µM). *

= P < 0.05.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

mean = 13.94 ± 9.10 cm2 mo-1, or 167.25 ±

32.02 cm2 yr-1) (P < 0.05) (Fig. 7B).

DISCUSSION

Identifying the causes of low survivorship

in coral outplants is crucial to improve restora-

tion techniques and their long-term effective-

ness (Liñán-Cabello et al., 2011; Ware et al.,

2020). In order for coral outplants to become

a resource for other organisms, reproduce

through fragmentation or sexual mechanisms,

and contribute to reef complexity until no

further transplantation and/or individual moni-

toring of the colonies is needed, it is important

that they survive during the first year after

transplantation and keep growing (Goergen

& Gilliam, 2018). While all the outplanted

Pocillopora spp. colonies survived during the

first year after transplantation, over 50 % of

the massive outplants were lost and 67.7 % of

the remaining fragments experienced partial

mortality and tissue loss, which is common

for species with massive growth (Rivas et al.,

2021) Different factors could explain the low

survivorship in our results: (i) the process of

microfragmentation may damage healthy tis-

sue, in addition to their smaller sizes, which

increase their vulnerability to other stressors

(Arnold et al., 2010; Forsman et al., 2015),

and may result into partial tissue mortality.

Nonetheless, microfragments grow at a faster

rate than larger corals (Page et al., 2018) and

isogenic fusion of fragments may be used for

colonies to reach a larger size in a shorter

period of time (Forsman et al., 2015); and (ii)

the technique implemented, due to the ceramic

disk being mechanically dislodged by currents

or the interaction of other reef species (Shafir

& Rinkevich, 2013; van Woesik et al., 2017),

including the presence of herbivores or preda-

tors. Large and dense patches of the sea urchin

D. mexicanum (up to 28.5 ind m-2) were record-

ed during monitoring, covering the areas where

massive corals had been outplanted. Their bio-

erosive activity may have promoted partial tis-

sue mortality and interrupted the calcification

process, which is essential for coral attachment

to the natural substrate (Herrera-Escalante et

al., 2005; Omori, 2019). In addition, fragments

were damaged by fish bites. Predation by reef

fish is one of the main drivers of mortality for

small coral recruits or, in this case, outplants of

Fig. 7. Differences of mean annual growth rate (cm2 yr-1) of Pocillopora spp. outplants between different sites of origin of

donor colonies (A), and between outplants originally from Matapalo (in red) and the other sites (B) at Güiri-Güiri restoration

site, Costa Rica.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

sizes ≤ 5 cm2 (Ishida-Castañeda et al., 2020;

Page et al., 2018; Palacios et al., 2014; Rivas

et al., 2021), which decreases dramatically

when fragments reach ≥ 25 cm2 and attach to

the substrate by tissue spreading (Tortolero-

Langarica et al., 2020). Physical protection

against coral predators increases survival and

reduces predation effects (Hughes et al., 2007;

Rivas et al., 2021), therefore it can be a poten-

tial tool to decrease mortality during the first

growth phase, until outplants surpass a size that

makes them less susceptible to predation and so

increase their chances of long-term survival.

The lowest survivorship corresponds to P.

lobata, which presents low dominance in the

area, in contrast to coral reefs in the Central and

South Pacific of Costa Rica (Cortés & Jiménez,

2003; Cortés et al., 2010; Jiménez, 2001). This

might potentially indicate that local conditions

at the restoration site are non-optimal for this

species to prevail as a dominant reef-building

coral. This situation contrasts with the high sur-

vivorship of Pocillopora spp. outplants, which

used to be considered a highly sensitive genus

to natural stressors (Glynn & Ault, 2000).

However, they have recently proven to have the

ability to acclimate to extreme conditions, espe-

cially thermal anomalies (Cruz-García et al.,

2020; Romero-Torres et al., 2020) and upwell-

ing conditions (Combillet et al., 2022). Due

to their life history, it is expected that, in the

short-term, Pocillopora spp. outplant survival

will remain high, as colony size increases and

competition for space and resources with other

benthic fast-growing groups (e.g., macroalgae,

turf) is reduced (Kodera et al., 2020; Lizcano-

Sandoval et al., 2018; van Woesik et al., 2017).

Coral outplants in this study significantly

increased their size in one year after their trans-

plantation. Pocillopora spp. outplants experi-

enced a 4-fold increase from their initial area

in one year, while massive species showed a

much slower growth: P. clavus and P. gigantea

increased their initial area over 150 %, while

P. lobata fragments did not even double their

initial size. These differences between coral

species respond to differences in their growth

form, life history, local acclimatization, and

reproduction strategies (Lirman & Schopmey-

er, 2016; Page et al., 2018; Rinkevich, 2014).

Pocillopora is a fast-growing genus, with

growth rates over 5 cm yr-1 (Tortolero-Langari-

ca et al., 2017), and its branching morphology

exponentially increases the three-dimension-

ality of the colony, which translates to a high

contribution to coral cover and reef complexity

(Kodera et al., 2020; Tortolero-Langarica et al.,

2019). In contrast, slow growth rates of massive

species result in a short-term low contribution

to coral cover and reef heterogeneity (Forsman

et al., 2015; Page et al., 2018; Rivas et al.,

2021). Pocillopora outplants showed a high

growth rate of 9.98 ± 1.69 cm yr-1, in contrast

to massive outplants, which not only showed

low growth rates (0.61-1.48 cm yr-1), but

also experienced partial tissue mortality dur-

ing monitoring period. The high effectiveness

observed using Pocillopora fragments has been

key for it to be the most widely used genus

for restoration efforts throughout the ETP

(Combillet et al., 2022; Ishida-Castañeda et

al., 2020; Liñán-Cabello et al., 2011; Lizcano-

Sandoval et al., 2018). Nonetheless, in order to

achieve ecological rehabilitation, it is important

to consider not only structural complexity but

the calcification rate and calcium carbonate

production, which is mostly provided by mas-

sive species (Tortolero-Langarica et al., 2022).

Therefore, efforts should be focused on new

approaches and protocols that would allow to

increase the survival of the so-far challenging

massive corals, and hence scale and maximize

restoration efforts.

Although the rapid growth of Pocillopora

is the result of its life history, and even more so

in the study area, where growth rates are natu-

rally higher than in other localities in the ETP

(Jiménez & Cortés, 2003), other factors that

promote the survival and success of this genus

should be considered. Coral growth is influ-

enced by local and site-specific conditions (Foo

& Asner, 2020; Foo & Asner, 2021; Kodera

et al., 2020). Bahía Culebra is influenced

by seasonal upwelling, with sudden drops in

seawater temperature down to 19 °C, which

may elicit coral bleaching (Cupul-Magaña &

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Calderón-Aguilera, 2008; Lirman et al., 2011),

and compromise growth and reproduction

due to lack of energy available, but generally

cause low mortality (Rodríguez-Troncoso et

al., 2014). The ability of corals to maintain

their costly physiological processes like growth

and reproduction under such conditions is

an acclimatization response (Gerstle, 2020;

Rodríguez-Troncoso et al., 2010; Rodríguez-

Troncoso et al., 2014; Rodríguez-Troncoso

et al., 2016), as is the differential effect of

abnormal high and low-temperature bleaching.

Heat-induced bleaching causes an expulsion of

the symbiont –its main energy supplier–, but

also damages the polyp, while in abnormally

low temperature conditions, bleaching results

from photoinhibition of the symbiont (Lough

& van Oppen, 2018; van Oppen & Blackall,

2019). However, the coral maintains its physi-

ological processes by obtaining heterotrophic

energy, and thus may help compensate its

diminished autotrophic capacities (Jiménez &

Cortés, 2003; Ziegler et al., 2014), which may

cause a decrease but not inhibition of growth.

Therefore, corals in Bahía Culebra must have

the ability to acclimate to intense and sudden

decreases in temperatures occurring during

upwelling season. Moreover, unlike for massive

corals, the presence of herbivores is beneficial,

as D. mexicanum acts as a biological controller

for the main coral competitors such as macroal-

gae and turf (Alvarado et al., 2012, Alvarado et

al., 2016), thus decreasing competition pres-

sure and also, generating space for possible

sexual recruits (Cano et al., 2021; Graham et

al., 2015; Roth et al., 2018).

The lower growth rate exhibited by Pocil-

lopora outplants in the first month after their

outplanting could be a result of what has

been previously described as “transplantation

shock”. During this period, outplants under-

go handling stress caused by the transplanta-

tion process (Precht, 2006), and acclimate to

the environmental conditions of the new site;

hence, their growth may be reduced (Afiq-Ros-

li et al., 2017; Forrester et al., 2012; Forrester

et al., 2014; Lirman et al., 2010).

Our results show an influence of site of the

donor colony on Pocillopora outplant growth.

Differences in growth can be attributed to dif-

ferent genotypes and life history, even when

outplanted to the same site (Drury et al., 2017;

Goergen & Gilliam, 2018; Lirman et al., 2014;

van Oppen et al., 2015). We do not possess

information on every individual Pocillopora

genotype outplanted to the reef; however, we

hypothesize that the site of the donor colony

could here be used as a proxy for different envi-

ronmental tolerances, as fragments were origi-

nally collected from small areas in each donor

site, and branching species reproduce mainly

through fragmentation in the ETP (Bezy, 2009;

Glynn et al., 2017; Sánchez-Noguera et al.;

2018b). Coral colonies from Matapalo site

exhibited higher growth rates. Interestingly,

this is the only site located outside the bay, is

the most distant site from all others, and has

relatively stable carbonate chemistry conditions

(Sánchez-Noguera, 2019). Hence, the detected

differences between donor sites when being

subject to the same environmental conditions

in the outplanting site could be a result of their

life history and acclimation to the conditions

of the donor site (Baums et al., 2019). Identify-

ing growth differences between colonies and

donor sites is relevant, even though trade-offs

between growth, survival, resistance to disease,

thermal tolerance and reproductive capacity

may exist (Ware et al., 2020). Therefore, it is

important to still outplant colonies with differ-

ent life histories and responses to stress to the

same restoration area, as this will maximize

chances of survival in the face of changing con-

ditions. Moreover, once outplants are sexually

mature and reproduce among themselves, their

offspring will likely receive considerable adap-

tive benefits (Baums et al., 2019), and hence

ensure long-term success of restoration efforts.

As coral restoration is becoming a common

strategy to recover and rehabilitate degraded

coral reefs, it is essential to determine the

best practices to ensure outplant survival and

growth. These practices and techniques need

to adapt to the local site-specific conditions

for each area and outplanting site. Our results

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

highlight the relevance of considering ecologi-

cal processes such as herbivory and predation

to maximize the success of restoration (Cano et

al., 2021; Dang et al., 2020; Schopmeyer & Lir-

man, 2015) and how corals with different mor-

phologies and life strategies may respond to the

same environmental conditions. While Pocillo-

pora spp. outplants had a positive response to

outplanting technique and site conditions, frag-

ments of massive species did experience partial

tissue loss and dislodgement. Nevertheless, it

is still important to restore coral reefs using a

multi-species approach, since different coral

species have different responses to disturbances

(Lirman et al., 2011; Lustic et al., 2020). In

the face of future changing conditions, pro-

moting species richness and thus ecosystem

resilience is key to ensure long-term recovery

of coral reefs. Moreover, although monitoring

individual outplants in the first year is vital to

evaluate the feasibility of transplantation, there

is a need to increase monitoring timeframes

and develop appropriate ecological indicators

in order to evaluate restoration effectiveness

(Hein et al., 2017). These results could inform

future practices and improve success of restora-

tion efforts in the ETP.

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 study would not have been

possible without the support of Centro de

Investigación en Ciencias del Mar y Lim-

nología (CIMAR), from Universidad de Costa

Rica. This project was funded by Vicerrectoría

de Investigación of Universidad de Costa Rica

through Project B9089, Península Papagayo

through their environmental sustainability

program, and the German Agency for Inter-

national Cooperation (GIZ). We are especial-

ly thankful to Carlos Marenco and the staff

of Marina Papagayo for their support during

fieldwork. We thank Camila Valverde for her

help processing photographs, and Alma Paola

Rodríguez-Troncoso and Sergio Madrigal-

Mora for their suggestions and review of

the manuscript.

Ver apéndice digital /

See digital appendix - a06v71s1-A1

REFERENCES

Afiq-Rosli, L., Taira, D., Loke, H.X., Toh, T.C., Toh, K.B.,

Ng, C.S.L., Cabaitan, P.C., Chou, L.M., & Song,

T. (2017). In situ nurseries enhance coral trans-

plant growth in sedimented waters. Marine Biology

Research, 13(8), 878–887.

Alvarado, J. J., Beita-Jiménez, A., Mena, S., Fernández-

García, C., Cortés, J., Sánchez-Noguera, C., Jiménez,

C., & Guzmán-Mora, A. G. (2018). Cuando la con-

servación no puede seguir el ritmo del desarrollo:

Estado de salud de los ecosistemas coralinos del

Pacífico Norte de Costa Rica. Revista de Biología

Tropical, 66(S1), 280–308.

Alvarado, J. J., Cortés, J., Guzmán, H., & Reyes-Bonilla,

H. (2016). Density, size, and biomass of Diadema

mexicanum (Echinoidea) in Eastern Tropical Pacific

coral reefs. Aquatic Biology, 24, 151–161.

Alvarado, J. J., Cortés, J., & Reyes-Bonilla, H. (2012).

Reconstruction of Diadema mexicanum bioerosion

impact on three Costa Rican Pacific coral reefs.

Revista de Biología Tropical, 60(S2), 121–132.

Arnold, S. N., Steneck, R. S., & Mumby, P. J. (2010). Run-

ning the gauntlet: inhibitory effects of algal turfs on

the processes of coral recruitment. Marine Ecology

Progress Series, 414, 91–105.

Baums, I. B., Baker, A. C., Davies, S. W., Grottoli, A. G.,

Kenkel, C. D., Kitchen, S. A., Kuffner, I. B., LaJeu-

nesse, T. D., Matz, M. V., Miller, M. W., Parkinson,

J. E., & Shantz, A. A. (2019). Considerations for

maximizing the adaptive potential of restored coral

populations in the western Atlantic. Ecological Appli-

cations, 29(8), e01978.

Bayraktarov, E., Banaszak, A. T., Montoya-Maya, P., Kle-

ypas, J., Arias-González, J. E., Blanco, M., Calle-

Triviño, J., Charuvi, N., Cortés-Useche, C., Galván,

V., García-Salgado, M. A., Gnecco, M., Guendulain-

García, S. D., Hernández-Delgado, E. A., Marín-

Moraga, J. A., Maya, M. F., Mendoza-Quiroz, S.,

Mercado-Cervantes, S., Morikawa, M., Nava, G. ...

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Frías-Torres, S. (2020). Coral reef restoration efforts

in Latin American countries and territories. PLoS

ONE, 15 (8), e0228477.

Bezy, M. B. (2009). Reproducción sexual y reclutamiento

del coral masivo Pavona clavus en Bahía Cule-

bra, Golfo de Papagayo, Costa Rica [Unpublished

master’s thesis]. Universidad de Costa Rica.

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

Ceccarelli, D., Cook, N., Ferse, S. C. A., 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.

Cano, I., Sellares-Blasco, R. I., Lefcheck, J. S., Villalpando,

M. F., & Croquer, A. (2021). Effects of herbivory by

the urchin Diadema antillarum on early restoration

success of the coral Acropora cervicornis in the

central Caribbean. Journal of Experimental Marine

Biology and Ecology, 539, 151541.

Chomitz, B. (2021). The coral-associated fauna and sessile

benthic reef community of Pocillopora coral colonies

following transplantation in Golfo Dulce, South

Pacific, Costa Rica: Composition, dynamics and suc-

cession [Unpublished master’s thesis]. Universidad

de Costa Rica.

Coles, S. L., & Jokiel, P. L. (1978). Synergistic effects

of temperature, salinity and light on the hermatypic

coral Montipora verrucosa. Marine Biology, 49,

187–195.

Combillet, L., Fabregat-Malé, S., Mena, S., Marín-Moraga,

J. A., Gutiérrez, M., & Alvarado, J. J. (2022). Poci-

llopora spp. growth analysis on restoration structures

in an Eastern Tropical Pacific upwelling area. PeerJ,

10, e13248.

Cortés, J., & Jiménez, C. (2003). Corals and coral reefs of

the Pacific of Costa Rica: history, research and status.

In J. Cortés (Ed.), Latin American Coral Reefs (pp.

361-367). Elsevier Science.

Cortés, J., Jiménez, C. E., Fonseca, A. C, & Alvarado, J.

J. (2010). Status and conservation of coral reefs in

Costa Rica. Revista de Biología Tropical, 58(S1),

33–50.

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

Zaragoza, F. A., Mayfield, C. 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. L., & Calderón-Aguilera, L. (2008).

Cold water bleaching at Islas Marietas National

Park, Nayarit, Mexico. XV Oceanography National

Meeting, Veracruz, Mexico.

D’Angelo, C., & Wiedenmann, J. (2014). Impacts of

nutrient enrichment on coral reefs: new perspectives

and implications for coastal management and reef

survival. Current Opinion in Environmental Sustai-

nability, 7, 82–93.

Dang, V. D. H., Cheung, P. Y., Fong, C. L., Mulla, A. J.,

Shiu, J. H., Lin, C. H., & Nozawa, Y. (2020) Sea

urchins play an increasingly important role for coral

resilience across reefs in Taiwan. Frontiers in Marine

Science, 7, 581945.

Drury, C., Manzello, D. P., & Lirman, D. (2017). Geno-

type and local environment dynamically influence

growth, disturbance response and survivorship in the

threatened coral, Acropora cervicornis. PLoS ONE,

12, e0174000.

Edmunds, P. J., & Putnam, H. M. (2020). Science-based

approach to using growth rate to assess coral perfor-

mance and restoration outcomes. Biology Letters, 1,

20200227.

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

reef targeted research & capacity building for Mana-

gement Program. St Lucia, Australia.

Faxneld, S., Jörgensen, T. L., & Tedengren, M. (2010).

Effects of elevated seawater temperature, reduced

salinity and nutrient enrichment on metabolism of the

coral Turbinaria mesenterina. Estuarine, Coastal and

Shelf Science, 88(4), 482–487.

Fernández, C. (2007). Propagación del alga Caulerpa ser-

tularioides (Chlorophyta) en Bahía Culebra, Golfo

de Papagayo, Pacífico norte de Costa Rica [Unpu-

blished master’s thesis]. Universidad de Costa Rica.

Fernández-García, C., Cortés, J., Alvarado, J. J., & Nívia-

Ruiz, J. (2012). Physical factors contributing to the

benthic dominance of the algae Caulerpa sertula-

rioides (Caulerpaceae, Clorophyta) in the upwelling

Bahía Culebra, North Pacific of Costa Rica. Revista

de Biología Tropical, 60, 93–107.

Ferse, S. C. A., Hein, M. Y., & Rölfer L. (2021). A survey

of current trends and suggested future directions in

coral transplantation for reef restoration. PLoS ONE,

16(5), e0249966.

Foo, S. A, & Asner, G. P. (2020). Sea surface temperature

in coral reef restoration outcomes. Environmental

Research Letters, 15, 074045.

Foo, S. A., & Asner, G. P. (2021). Impacts of remotely sen-

sed environmental drivers on coral outplant survival.

Restoration Ecology, 29(1), e13309.

Forrester, G. E., Ferguson, M. A., O’Connell-Rodwell,

C. E., & Jarecki, L. L. (2014). Long-term survival

and colony growth of Acropora palmata fragments

transplanted by volunteers for restoration. Aquatic

Conservation: Marine and Freshwater Ecosystems,

24, 81–91.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Forrester, G. E., Maynard, A., Schofield, S., & Taylor,

K. (2012). Evaluating causes of transplant stress

in fragments of Acropora palmata used for coral

reef restoration. Bulletin of Marine Science, 88(4),

1099–1113.

Forsman, Z. H., Page, C. A., Toonen, R. J., & Vaughan,

D. (2015). Growing coral larger and faster: micro-

colony-fusion as a strategy for accelerating coral

cover. PeerJ, 3, e1313.

Gerstle, L. (2020). Growth and transgenerational acclima-

tization of juvenile Pocillopora damicornis [Unpu-

blished doctoral dissertation]. University of Hawai’i.

Glynn, P., & Ault, J. (2000). A biogeographic analysis and

review of the far eastern Pacific coral reef region.

Coral Reefs, 19, 1–23.

Glynn, P. W., Colley, S. B., Carpizo-Ituarte, E., & Rich-

mond, R. H. (2017). Coral reproduction in the Eastern

Pacific. In P. W. Glynn, D. P. Manzello, I. C. Enochs

(Eds.), Coral Reefs of the Eastern Tropical Pacific

(Vol 8, pp. 435–476). Springer Science+Business

Media.

Goergen, E. A., & Gilliam, D. S. (2018). Outplanting

technique, host genotype, and site affect the initial

success of outplanted Acropora cervicornis. PeerJ,

6, e4433.

Graham, N. A. J., Jennings, S., MacNeil, M. A., Mouillot,

D., & Wilson, S. K. (2015). Predicting climate-driven

regime shifts versus rebound potential in coral reefs.

Nature, 518, 1–17.

Guzmán, H. (1991). Restoration of coral reefs in Pacific

Costa Rica. Conservation Biology, 5(2), 189–195.

Hein, M. Y., Willis, B. E., Beeden, R., & Birtles, A. (2017).

The need for broader ecological and socioeconomic

tools to evaluate the effectiveness of coral restoration

programs. Restoration Ecology, 25(6), 873–883.

Herrera-Escalante, T., López-Pérez, R. A., & Leyte-Mora-

les, G. E. (2005). Bioerosion caused by the sea urchin

Diadema mexicanum (Echinodermata: Echinoidea)

at Bahías de Huatulco, Western Mexico. Revista de

Biología Tropical, 53(S3), 263–273.

Hughes, T. P., Kerry, J., Álvarez-Noriega, M., Álvarez-

Romero, J. G., Anderson, K. D., Baird, A. H., Bab-

cock, R. C., Beger, M., Bellwood, D. R., Berkelmans,

R., Bridge, T. C., Butler, I. R., Byrne, M., Cantin,

N. E., Comeau, S., Connolly, S. R., Cumming, G.

S., Dalton, S. J., Diaz-Pulido, G., … Wilson, S. K.

(2017). Global warming and recurrent mass blea-

ching of corals. Nature, 543, 373–377.

Hughes, T. P., Kerry, J. T., Baird, A. H. Connolly, S. R.,

Chase, T. J., Dietzel, A., Hill, T., Hoey, A. S., Hoo-

genboom, M. O., Jacobson, M., Kerswell, A., Madin,

J. S., Mieog, A., Paley, A. S., Pratchett, M. S., Torda,

G., Woods, R. M. (2019). Global warming impairs

stock–recruitment dynamics of corals. Nature, 568,

387–390.

Hughes, T. P., Rodrigues, M. J., Bellwood, D. R., Ceccarelli,

D., Hoegh-Guldberg, O., McCook, L., Moltschaniws-

kyj, N., Pratchett, M. S., Steneck, R. S., & Willis, B.

(2007). Phase shifts, herbivory, and the resilience of

coral reefs to climate change. Current Biology, 17(4),

360–365.

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

Zapata, F. A. (2020). Coral reef restoration in the Eas-

tern Tropical Pacific: feasibility of the coral nursery

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

Jiménez, C. (1997). Corals and coral reefs of Culebra

Bay, Pacific coast of Costa Rica: anarchy in the reef

[Paper presentation]. In H.A. Lessios & I.A. Macin-

tyre (Eds.), Proceedings of the VIII International

Coral Reef Symposium [Symposium], VIII Interna-

tional Coral Reef Symposium, Panama.

Jiménez, C. (2001). Arrecifes y ambientes coralinos de

Bahía Culebra, Pacífico de Costa Rica: aspectos bio-

lógicos, económicos, recreativos y de manejo. Revista

de Biología Tropical, 49(S2), 215–231.

Jiménez, C. (2007). Arrecifes coralinos, ¿víctimas de los

cambios? Ambientico, 171, 5–7.

Jiménez, C., Bassey, G., Segura, Á., & Cortés, J. (2010).

Characterization of the coral communities and reefs

of two previously undescribed locations in the upwe-

lling region of Gulf of Papagayo (Costa Rica). Revista

Ciencias Marinas y Costeras, 2, 95–108.

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

of scleractinian corals in an upwelling environment of

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

Bulletin of Marine Science, 72, 187–198.

Kleypas, J. A., & Yates, K. K. (2009). Coral reefs and ocean

acidification. Oceanography, 22(4), 108–117.

Kleypas, J. A., McManus, J. W., & Meñez L. A. B. (1999).

Environmental limits to coral reef development:

Where do we draw the line? American Zoologist,

39(1), 146–159.

Kodera, S. M., Edwards, C. B., Petrovic, V., Pedersen, N.

E., Eynaud, Y., & Sandin, S. A. (2020). Quantifying

life history demographics of the scleractinian coral

genus Pocillopora at Palmyra Atoll. Coral Reefs, 39,

1091–1105.

Koval, G., Rivas, N., D’Alessandro, M., Hesley, D., Santos,

R., & Lirman, D. (2020). Fish predation hinders the

success of coral restoration efforts using fragmented

massive corals. PeerJ, 8, e9978.

Ladd, M. C., Miller, M. W., Hunt, J. H., Sharp, W. C., &

Burkpile, D. E. (2019). Harnessing ecological proces-

ses to facilitate coral restoration. Frontiers in Ecology

and the Environment, 16(4), 239–247.

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

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

doval, M. A., García-Mendoza, E., Soriano-Santiago,

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

Pocillopora spp. during a coral restoration program

in Carrizales Bay, Colima, Mexico. Marine and

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

Lirman, D., & Schopmeyer, S. (2016). Ecological solutions

to reef degradation: optimizing coral reef restoration

in the Caribbean and Western Atlantic. PeerJ, 4,

e2597.

Lirman, D., Schopmeyer, S., Galvan, V., Drury, C., Baker,

A. C., & Baums, I. B. (2014). Growth dynamics of

the threatened Caribbean staghorn coral Acropora

cervicornis: influence of host genotype, symbiont

identity, colony size, and environmental setting. PLoS

ONE, 9(9), e107253.

Lirman, D., Schopmeyer, S., Manzello, D., Gramer, L. J.,

Precht, W. F., Muller-Karger, F., Banks, K., Barnes,

B., Bartels, E., Bourque, A., Byrne, J., Donahue,

S., Duquesnel, J., Fisher, L., Gilliam, D., Hendee,

J., Johnson, M., Maxwell, K., McDevitt, E., Monty,

J., Rueda, D., Ruzicka, R., & Thanner, S. (2011).

Severe 2010 cold-water event caused unpreceden-

ted mortality to corals of the Florida reef tract and

reversed previous survivorship patterns. PLoS ONE,

6(8), e23047.

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

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

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

horn coral Acropora cervicornis: methods to minimi-

ze the impacts of fragment collection and maximize

production. Coral Reefs, 29, 729–735.

Lizcano-Sandoval, L. D., Londoño-Cruz, E., & Zapata,

F. A. (2018). Growth and survival of Pocillopora

damicornis (Scleractinia: Pocilloporidae) coral frag-

ments and their potential for reef restoration in the

Tropical Eastern Pacific. Marine Biology Research,

14, 887–897.

Lohr, K. E., Ripple, K., & Patterson, J. T. (2020). Diffe-

rential disturbance effects and phenotypic plasticity

among outplanted corals at patch and fore reef sites.

Journal for Nature Conservation, 55, 125827.

Lough, J. M., & van Oppen, M. J. H. (2018). Introduction:

coral bleaching-patterns, processes, causes and con-

sequences. In M. J. H. van Oppen, & J. M. Lough

(Eds.), Coral Bleaching, Patterns, processes, causes,

and consequences (pp. 1–8). Springer.

Lustic, C., Maxwell, K., Bartels, E., Reckenbeil, B., Utset,

E., Schopmeyer, S., Zink, I., & Lirman, D. (2020).

The impacts of competitive interactions on coral

colonies after transplantation: A multispecies experi-

ment from the Florida Keys, US. Bulletin of Marine

Science, 96(4), 805–818.

Miller, M. W., Lohr, K. E., Cameron, C. M., Williams,

D. E., & Peters, E. C. (2014). Disease dynamics

and potential mitigation among restored and wild

staghorn coral, Acropora cervicornis. PeerJ, 2, e541.

Omori, M. (2019). Coral restoration research and technical

developments: what we have learned so far. Marine

Biology Research, 15(7), 377–409.

Page, C. A., Muller, E. M., & Vaughan, D. E. (2018).

Microfragmenting for the successful restoration of

slow growing massive corals. Ecological Enginee-

ring, 123, 86–94.

Palacios, M. M., Muñoz, C. G., & Zapata, F. A. (2014).

Fish corallivory on a pocilloporid reef and experi-

mental coral responses to predation. Coral Reefs, 33,

625–636.

Pinzón, J. H., & LaJeunesse, T. C. (2011). Species delimita-

tion of common reef corals in the genus Pocillopora

using nucleotide sequence phylogenies, population

genetics and symbiosis ecology. Molecular Ecology,

20(2), 311–325.

Pinzón, J. H., Sampayo, E., Cox, E., Chauka, L. J., Chen,

C. A., Voolstra, C. R., & LaJeunesse, T. C. (2013).

Blind to morphology: genetics identifies several

widespread ecologically common species and few

endemics among Indo-Pacific cauliflower corals

(Pocillopora, Scleractinia). Journal of Biogeography,

40(8), 1595–1608.

Precht, W. F. (2006). Coral reef restoration handbook:

the rehabilitation of an ecosystem under siege. CRC

Press.

R Core Team (2021). R: A language and environment

for statistical computing [Computer software]. R

Foundation for Statistical Computing. http://www.r-

project.org/index.html

Rinkevich, B. (1995). Restoration strategies for coral reefs

damaged by recreational activities: The use of sexual

and asexual recruits. Restoration Ecology, 3(4),

241–251.

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

reef restoration lead to sustainable reefs? Current

Opinion in Environmental Sustainability, 7, 28–36.

Rivas, N., Hesley, D., Kaufman, M., Unsworth, J.,

D’Alessandro, M., & Lirman, D. (2021). Developing

best practices for the restoration of massive corals

and the mitigation of predation impacts: influences

of physical protection, colony size, and genotype on

outplant mortality. Coral Reefs, 40, 1227–1241.

Rixen, T., Jiménez, C., & Cortés, C. (2012). Impact of

upwelling events on the sea water carbonate chemis-

try and dissolved oxygen concentration in the Gulf

of Papagayo (Culebra Bay), Costa Rica: Implications

for coral reefs. Revista de Biología Tropical, 60(S2),

187–195.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

Rodríguez-Sáenz, K., & Rodríguez-Fonseca, J. (2004).

Avistamientos del delfín manchado, Stenella attenua-

ta (Cetacea: Delphinidae) en Bahía Culebra, Costa

Rica, 1999-2000. Revista de Biología Tropical, 49(2),

189–193.

Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., & Cupul-

Magaña, A. L. (2010). Differential response to cold

and warm water conditions in Pocillopora colonies

from the Central Mexican Pacific. Journal of Expe-

rimental Marine Biology and Ecology, 391(1–2),

57–64.

Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., & Cupul-

Magaña, A. L. (2016). Physiological response to

high temperature in the Tropical Eastern Pacific

coral Pocillopora verrucosa. Marine Ecology, 37(5),

1168–1175.

Rodríguez-Troncoso, A. P., Carpizo-Ituarte, E., Pettay, D.

T., Warner, M. E., & Cupul-Magaña, A. L. (2014).

The effects of an abnormal decrease in temperature

on the Eastern Pacific reef-building coral Pocillopora

verrucosa. Marine Biology, 161, 131–139.

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.

Roth, F., Saalmann, F., Thomson, T., Coker, D. J., Villalo-

bos, R., Jones, B. H., Wild, C., & Carvalho, S. (2018).

Coral reef degradation affects the potential for reef

recovery after disturbance. Marine Environmental

Research, 142, 48–58.

Sánchez-Noguera, C. (2012). Cambios socioeconómicos y

ambientales en Bahía Culebra, Guanacaste, Costa

Rica: implicaciones para su gestión [Unpublished

master’s tesis]. Universidad de Costa Rica.

Sánchez-Noguera, C. (2019). Carbonate chemistry and

coral reefs in the Pacific coast of Costa Rica [Unpu-

blished doctoral dissertation]. Universität Hamburg.

Sánchez-Noguera, C., Jiménez, C., & Cortés, J. (2018a).

Desarrollo costero y ambientes marino-costeros en

Bahía Culebra, Guanacaste, Costa Rica. Revista de

Biología Tropical, 66(S1), 309–327.

Sánchez-Noguera, C., Stuhldreier, I., Cortés, J., Jiménez,

C., Morales, Á., Wild, C., & Rixen, T. (2018b). Natu-

ral ocean acidification at Papagayo upwelling system

(north Pacific Costa Rica): implications for reef deve-

lopment. Biogeosciences, 15, 2349–2360.

Schopmeyer, S. A., & Lirman, D. (2015). Occupation dyna-

mics and impacts of damselfish territoriality on reco-

vering populations of the threatened staghorn coral,

Acropora cervicornis. PLoS ONE, 10(11), e0141302.

Shafir, S., & Rinkevich, B. (2013). Mariculture of coral

colonies for the public aquarium sector. In R. J.

Leewis, & M. Janse (Eds.), Advances in coral hus-

bandry in public aquariums (Vol 2, pp. 315–318).

Burgers’ Zoo.

Stuhldreier, I., Sánchez-Noguera, C., Roth, C., Cortés, J.,

Rixen, T., & Wild, C. (2015). Upwelling increases

net primary production of corals and reef-wide gross

primary production along the Pacific coast of Costa

Rica. Frontiers in Marine Science, 2, 113.

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

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

degraded coral reef using a natural remediation pro-

cess: 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.,

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. J. A., Rodríguez-Troncoso, A. P.,

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

tiago-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., & Rinkevich, B. (2020).

Micro-fragmentation as an effective and applied tool

to restore remote reefs in the Eastern Tropical Pacific.

International Journal of Environmental Research and

Public Health, 17, 6574.

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

Cupul-Magaña, A. L., Morales-de-Anda, D. E., Case-

lle, J. E., & Carricart-Ganivet, J. P. (2022). Coral

calcification and carbonate production in the eastern

tropical Pacific: The role of branching and massive

corals in the reef maintenance. Geobiology, 20(4),

533–545.

Trygonis, V., & Sini, M. (2012). PhotoQuad: A dedicated

seabed image processing software, and a comparative

error analysis of four photoquadrat methods. Jour-

nal of Experimental Marine Biology and Ecology,

424–425, 99–108.

Unsworth, J. D., Hesley, D., D’Alessandro, M., & Lirman,

D. (2020). Outplanting optimized: Developing a more

efficient coral attachment technique using Portland

cement. Restoration Ecology, 29(1), e13299.

van Oppen, M. J. H., & Blackall, L. L. (2019). Coral micro-

biome dynamics, functions and design in a changing

world. Nature Reviews Microbiology, 17, 557–567.

van Oppen, M. J. H., Oliver, J. K., Putnam, H. M., & Gates,

R. D. (2015). Building coral reef resilience through

18 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54879, abril 2023 (Publicado Abr. 30, 2023)

assisted evolution. Proceedings of the National Aca-

demy of Sciences, 112, 2307–2313.

van Woesik, R., Ripple, K., & Miller, S. L. (2017).

Macroalgae reduces survival of nursery-reared Acro-

pora corals in the Florida reef tract. Restoration

Ecology, 26(3), 563–569.

Ware, M., Garfield, E. N., Nedimyer, K., Levy, J., Kauf-

man, L., Precht, W., Winters, R. S., & Miller, S. L.

(2020). Survivorship and growth in staghorn coral

(Acropora cervicornis) outplanting projects in the

Florida Keys National Marine Sanctuary. PLos ONE,

15(5), e0231817.

Wiedenmann, J., D’Angelo, C., Smith, E.G., Hunt, A.

N., Legiret, F. E., Postle, A. D., & Achterberg, E. P.

(2013). Nutrient enrichment can increase the suscep-

tibility of reef corals to bleaching. Nature Climate

Change, 3, 160–164.

Ziegler, M., Roder, C. M., Büchel, C., & Voolstra, C. R.

(2014). Limits to physiological plasticity of the coral

Pocillopora verrucosa from the central Red Sea.

Coral Reefs, 33, 1115–1129.