Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

Succession of the sessile benthic community

at a coral reef restoration site

Benjamin R. Chomitz1, 5 *; https://orcid.org/0000-0002-8878-5935

Joan Anne Kleypas2; https://orcid.org/0000-0003-4851-7124

Jorge Cortés3, 4; https://orcid.org/0000-0001-7004-8649

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

1. Posgrado en Biología, Universidad de Costa Rica, San Pedro, San José, Costa Rica; ben@chomitz.com

(* Correspondence)

2. Climate and Global Dynamics Lab, University Corporation for Atmospheric Research, Boulder, Colorado, United

States of America; kleypas@ucar.edu

3. Centro de Investigación en Ciencias del Mar y Limnología, Universidad de Costa Rica, San Pedro, San José, Costa

Rica; jorge.cortes@ucr.ac.cr

4. Escuela de Biología, Universidad de Costa Rica, San Pedro, San José, Costa Rica; juan.alvarado@ucr.ac.cr

5. Cooperative Institute for Marine and Atmospheric Studies, Atlantic Oceanic and Meteorological Laboratories, Miami,

Florida, United States of America.

Received 24-VIII-2022. Corrected 10-III-2023. Accepted 17-III-2023.

ABSTRACT

Introduction: Ecosystem restoration facilitates ecological succession. When a coral reef experiences a distur-

bance, the community of sessile benthic organisms can follow a successional trajectory that favors the domi-

nance of coral or a change of state to an ecosystem dominated by algae.

Objective: To better understand the impact of coral transplants on succession of the sessile benthic community.

Methods: To measure and monitor the coral cover (cm2) of Pocillopora spp., and the composition of the associ-

ated benthic community, experimental and control coral reef patches were established at the coral restoration

site in Golfo Dulce, South Pacific Costa Rica. Thirty Pocillopora spp. colonies were attached to nails on the

substrate in an experimental patch. The control coral patch contained nails with non-transplanted colonies. Both

treatments were photographed monthly during a period of eight months. Changes in the coverage of coral and

other sessile benthic organisms were measured from the images and compared over time between the experi-

mental and control patches.

Results: The coral transplants experienced bleaching events in August through September 2019 and January

through February 2020. The first bleaching event possibly due to sedimentation, and the second to high tem-

peratures. By the end of the experiment, 83 % of the colonies had survived. The live colonies grew significantly

following transplantation; > 67 % of their initial coverage area after eight months. In the experimental patch, the

areas of Pocillopora spp., coralline crustose algae (CCA), and cyanobacteria increased while the area of algal

turf decreased. The increase in coral coverage and CCA, and decrease in algal turf in the experimental patch

could be due to herbivores attracted to transplants. The increase in cyanobacteria in the experimental patch could

be the result of higher temperatures and may have been a factor in the death of colonies.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54881

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

Coral reefs are in decline globally due

to many factors including climate change,

pollution, inadequately planned coastal devel-

opment, mismanagement of fisheries, and

eutrophication (Sandin et al., 2008, Van Oppen

et al., 2017). In addition to the ecological

impact, this decline has an economic impact

on societies that depend on coral reefs for their

livelihood (Costanza et al., 2014). The marine

conditions responsible for this decline in reef

ecosystems can inhibit the recuperation of a

coral reef following a disturbance to the reef

environment (Anthony et al., 2020; Good &

Bahr, 2021; Rinkevich, 2005). Coral reef res-

toration is one form of human mediation that

aims to rebuild coral reef communities through

active propagation of coral in order to promote

the recovery of the ecosystems’ natural comple-

ment of diversity and ecological functionality

(Hancock et al., 2017; Horoszowski-Fridman et

al., 2015). The most common method of coral

reef restoration is through coral gardening and

transplantation (Bayraktarov et al., 2019).

Coral restoration is essentially a facilita-

tion of natural successional processes through

the reintroduction and management of key

species (Walker et al., 2007; Young, 2001).

Ecological succession is the process by which

Conclusions: The transplantation of Pocillopora spp. colonies in Golfo Dulce changed the early successional

trajectory of the sessile benthic community to favor the dominance of coral dominance in the experimental patch.

These results may be useful in informing expectations for future restoration efforts.

Key words: coral reef; reef phase change; coral-algae interaction; inhibition.

RESUMEN

Sucesión de la comunidad bentónica sésil en un sitio de restauración de arrecifes de coral.

Introducción: La restauración de ecosistemas facilita la sucesión ecológica. Cuando un arrecife de coral experi-

menta una perturbación, la comunidad de organismos sésiles bentónicos puede seguir una trayectoria de sucesión

que favorezca la dominancia del coral o un cambio de estado a un ecosistema dominado por algas.

Objetivo: Comprender mejor el impacto de los trasplantes de coral en la sucesión de la comunidad bentónica

sésil.

Métodos: Para medir y monitorear la cobertura de coral (cm2) de Pocillopora spp. y la composición de la comu-

nidad bentónica asociada se establecieron parches de arrecifes de coral experimentales y de control en el sitio

de restauración de coral en Golfo Dulce, Pacífico Sur de Costa Rica. Treinta colonias de Pocillopora spp., se

trasplantaron a los clavos en el sustrato en el parche experimental. El parche de coral de control contenía clavos

sin colonias trasplantadas. Ambos tratamientos fueron fotografiados mensualmente durante un periodo de ocho

meses. Los cambios en la cobertura de coral y otros organismos bentónicos sésiles se midieron a partir de las

imágenes y se compararon a lo largo del tiempo entre los parches experimentales y de control.

Resultados: Los trasplantes de coral experimentaron eventos de blanqueamiento de agosto a septiembre de 2019

y de enero a febrero de 2020. El primer evento de blanqueamiento puede haber sido el resultado de la sedimen-

tación y el segundo puede deberse a las altas temperaturas. Al final del experimento, el 83 % de las colonias

habían sobrevivido. Las colonias vivas crecieron significativamente después del trasplante; > 67 % de su área

de cobertura inicial después de ocho meses. En el parche experimental, las áreas de Pocillopora spp., algas

coralinas costrosas (ACC) y cianobacterias aumentaron mientras que el tapete de algas disminuyó. El aumento

en la cobertura de coral y ACC, y la disminución en tapetes de algas en el parche experimental podría deberse a

los herbívoros atraídos por los trasplantes. El aumento de cianobacterias en el parche experimental podría ser el

resultado de temperaturas más altas y puede haber sido un factor en la muerte de las colonias.

Conclusiones: El trasplante de las colonias de Pocillopora spp. en Golfo Dulce cambiaron la trayectoria de suce-

sión temprana de la comunidad bentónica sésil para favorecer la dominancia del coral en el parche experimental.

Estos resultados pueden ser útiles para informar las expectativas de futuros esfuerzos de restauración.

Palabras claves: arrecife de coral; cambio de fase de arrecifes; interacción coral-alga; inhibición.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

an ecosystem undergoes a predictable sequence

of the replacement of communities that reach

a stable climax and remains reasonably

unchanged over time until the next disturbance

(Odum, 1964). The early succession of a reef is

critical to the establishment, survival and resil-

ience of coral reef communities (Doropoulos

et al., 2016). For example, algal turf impedes

the settlement of coral larvae and the growth of

colonies (O’Brien & Schiebling, 2018; Smith

et al., 2010). Conversely, coralline crustose

algae promote the settlement and growth of

corals (Doropoulos et al., 2016).

Coral growth rate is one of the most widely

used assessments of coral reef health and res-

toration success (Edmunds & Putnam, 2020).

The growth of corals can be affected by envi-

ronmental factors including temperature (Jimé-

nez & Cortés, 2003; Manzello, 2010), seawater

pH (Guo et al., 2020; Manzello, 2010), nutri-

ents (Toh et al., 2014), light (Wellington,

1982), depth, and biological factors such as the

presence of certain fish, invertebrates (Glynn &

Enochs, 2010) and algae (Lirman, 2001). Coral

growth information is used to assess and pre-

dict the environmental conditions and locations

where corals can survive and thrive (Edmunds

& Putnam, 2020).

The succession of coral reefs occurs at

short time scales in the range of months and

geological time scales that occur over cen-

turies, millennia or even millions of years

(Grigg, 1983; Karlson, 1999). At short time

scales, succession is localized on small patches

of substrate and is dominated by fast-growing

organisms such as algae competing for light,

space, and other resources. This short time

scale succession is the most relevant to pro-

cesses of coral recruitment, competition, and

growth (Doropoulos et al., 2016). Coral reef

succession at geological time scales is charac-

terized by turnovers of species of hermatypic

corals and the physical structure of the reef as

long-term changes in the ecology, environment,

and frequency of disturbance favor the growth

of certain species and forms over others (Grigg,

1983). For example, fast-growing branching

corals such as pocilloporids and acroporids

tend to be early colonizers of a new reef that

are sensitive to environmental changes and are

replaced by slower growing, more tolerant,

massive species that build on the physical and

ecological foundations of the branching spe-

cies, eventually replacing them as the dominant

growth forms (Grigg, 1983).

Coral reefs are ecosystems characterized

by constant disturbance, including anthropo-

genic and natural factors. This constant dis-

turbance contributes to the high diversity of

life in coral reefs (Grigg, 1983) and also their

vulnerability to decline. Disturbances such as

high sediment loads, elevated temperatures

from El Niño Southern Oscillation (ENSO)

events stress corals and cause them to lose their

zooxanthellae symbionts a process known as

coral bleaching. If a disturbance is strong and

persistent, a coral reef ecosystem can settle

into alternate stable states dominated by dif-

ferent organisms depending on environmental

and ecological factors (Dudgeon et al., 2010;

Fung et al., 2011). Thus, as succession follows

a disturbance, its trajectory can be affected by

these environmental and ecological factors. For

example, under conditions of constant distur-

bance, climate change and other anthropogenic

factors tend to push recovering ecosystems

to favor the proliferation of macroalgae and

turfs instead of reef-forming corals. Algae-

dominated marine ecosystems often do not

naturally revert to coral-dominated ecosystems

without intervention (Smith et al., 2010). This

is because reef-forming corals tend to be out-

competed by algal turfs that often flourish in

ecosystems with high water nutrient concentra-

tions and fewer herbivores; a condition that can

occur in ecosystems degraded by eutrophica-

tion and poorly regulated fisheries (Smith et al.,

2010). However, processes such as herbivory

and coral expansion that encourage the eco-

logical trajectory towards a self-sustaining reef

ecosystem are also evident in the dynamics of

the community of benthic encrusting organ-

isms on the reef bottom (Ceccarelli et al., 2011;

Fong et al., 2016).

The benthic sessile community of a reef

is a complex and competitive arena. The main

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competitors are often simplified into the fol-

lowing categories: turf, an overarching term for

a multispecies, dense, often filamentous mat of

algae; crustose coralline algae (CCA) that can

promote the growth and recruitment of coral;

and scleractinian corals (Flower et al. 2017;

Smith et al., 2010; Steneck & Dethier, 1994).

Corals, especially highly branched species such

as Pocillopora, provide structural complexity

to a reef ecosystem that attracts diverse and

abundant populations of fish and other associ-

ated fauna (Stella et al., 2011). Herbivorous

coral associates control populations of turf and

macroalgae that inhibit the growth and settle-

ment of coral and thus encourage the expan-

sion of the reef (Burkepile & Hay, 2010; Hixon

& Bronstoff 1996; Humphries et al., 2014).

Seasonal shifts in the populations of species

associated fauna can influence the interactions

between algae and coral (Brown et al., 2019;

Doropoulos et al., 2016; Fong et al., 2016;

Muthukrishnan et al., 2016).

Favorable sites for coral reef restoration

are areas where corals previously flourished

and are unlikely to settle and grow at a new site

under current marine conditions (Rinkevich,

2005). Likewise, the most appropriate candi-

dates for species to be introduced are those

that might not colonize the restoration area

unassisted (Society for Ecological Restoration

International Science & Policy Working Group

[SER], 2004). In Golfo Dulce, an ecologically

unique tropical fjord-like embayment on the

southern Pacific coast of Costa Rica, histori-

cally abundant branching corals in the genus

Pocillopora have practically disappeared. The

initial loss of Pocillopora was due the change

in the path of rivers that brought fresh water

and sediments into the Gulf (Cortés, 1991;

Cortés & Reyes-Bonilla, 2017). In more recent

history, coastal development and deforesta-

tion around the rivers liberated sediment and

resulted in the further destruction of the gulf’s

reefs and a near complete loss of Pocillopora

corals (Cortés, 1991). With so few colonies

remaining, the population of Pocillopora in the

gulf could have experienced the Allee effect,

a condition of a community where there is not

enough population density to sustain sexual

reproduction (Allee, 1938; Gascoigne & Lip-

cius, 2004). A small number of Pocillopora

colonies in Golfo Dulce that have demonstrated

particular resilience to sedimentation and ther-

mal stress (J. Kleypas, pers. comm., 2020) have

become the basis of a coral reef restoration

effort to preserve and propagate the genus in

the Gulf.

Monitoring the health and growth of trans-

planted corals and changes to the ecosystem

around them provides insight into whether

those colonies are functioning ecologically as

“ecosystem engineers,” and thus can inform

future reef restoration efforts. This exploratory

study aimed 1) to monitor the health and survi-

vorship of a cohort of transplanted Pocillopora

spp. colonies in Golfo Dulce, South Pacific

Costa Rica, 2) calculate the growth rate of the

corals in terms of area, and 3) to describe the

effect of the transplantation of the colonies

on a short time scale succession of the sessile

benthic community. This information will aid

reef restoration scientists in understanding how

the reef community changes following coral

colony transplantation.

MATERIALS & METHODS

Study area: Golfo Dulce is a narrow-

mouthed embayment (8° 27’ – 8° 45’ N, 83° 07’

– 83° 30’ W) oriented northwest to southeast

between the Osa peninsula and the southern

Pacific coast of Costa Rica (Fig. 1). The Gulf

has an approximate length of 50 km and width

between 10 and 15 km and covers an area of

680 km2 with a maximum depth of 200 m. The

dry season lasts from December to March with

an average rainfall of 100 to 160 mm per month

(Fig. 2). The wet season peaks in October with

an average rainfall of 800 mm (Cortés, 1990).

The monthly seawater temperature ranging

from 18 º to 35 ºC with annual average of

approximately 26.5 ºC (Fig. 3).

Geographically and ecologically, Golfo

Dulce is part of the Eastern Tropical Pacific

(ETP) marine biological province (Glynn et

al., 2017; Guzmán & Cortés, 1993). It is often

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

referred to as a tropical fjord due to its anoxic

deep waters and bathymetry (Cortés, 1990;

Wolff et al., 1996). The anoxic waters prevent

the energy contained in detritus that sinks to

the depths of the gulf from being recycled back

into the higher trophic levels of the ecosystem

(Wolff et al., 1996). These unique conditions

result in a community structure of fish and

invertebrates that differs significantly from

other marine ecosystems of the Pacific coast of

Costa Rica (Alvarado et al., 2014).

Coral Nurseries: The experiment was

performed between July 2019 and February

2020. The coral colonies used in this study were

cultivated in in situ nurseries at Playa Nicuesa

(Fig.1) as part of the restoration initiative of the

NGO Raising Coral Costa Rica and the Center

of Marine Science and Limnology (CIMAR) of

the University of Costa Rica (UCR). The coral

nurseries are tree-shaped structures with central

PVC “trunk” and radiating fiberglass “branch-

es” to which the Pocillopora spp. colonies

Fig. 1. A. The location of Golfo Dulce within Costa Rica. B. The transplantation site at Punta Bejuco is marked with a red

star and Nicuesa site is marked with a red asterisk and the red triangle marks where the meteorological data were collected.

C. The location of the transplantation and control sites near Punta Bejuco marked with a red star.

Fig. 2. Rainfall (mm month-1) data from January 2019

through August 2020 from the Instituto Meteorológico

Nacional de Costa Rica station, near Golfo Dulce (08º

42’ 03” N, 83º 30’ 49” W, at 80 m above sea level). Gray

shading indicates the timeframe of the experiment.

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area attached with nylon monofilament lariats.

These colonies are derived from wild Pocil-

lopora spp. from various reefs in Golfo Dulce.

The colonies are fragmented by breaking off

the tips of the branches either manually or

using a diamond band saw to multiply the num-

ber of individual colonies through reproduction

assisted fragmentation (Horoszowski-Fridman

et al., 2015; Rinkevich, 2005). The nurseries

are located between 3 and 5 m of depth below

the water surface and anchored to the sea floor

with rope and kept vertical with a floating

buoy. The colonies in the nurseries are cleaned

of algae each month and their health monitored

(T. Villalobos, pers. comm., 2019). The experi-

mental colonies were chosen at random from

the coral nurseries before being transplanted at

Punta Bejuco.

Study organisms: Pocillopora is a fast-

growing genus (Darling et al., 2012) of branch-

ing scleractinian coral and an important reef

builder in the ETP (Guzmán & Cortés, 1993).

Pocillopora spp. can be categorized as pioneer

species in the establishment of a coral reef

due to the rapid growth rate and highly com-

plex structure of corals in the genus (Clark &

Edwards, 1994). Thus, Pocillopora is a popular

genus for coral reef restoration (Boström-Ein-

arsson et al., 2018). This coral is highly impor-

tant to reef ecosystems due to its complex

structure that permits the coral to harbor the

greatest diversity of associated organisms of

all coral genera (Stella et al., 2011). Pocillo-

pora spp. in the ETP are particularly resilient

to thermal stress (Manzello, 2010), possibly

due to their propensity to harbor the more ther-

mally tolerant Durusdinium glynnii (formerly

“Clade D”) zooxanthellae symbionts (Wham et

al., 2017). Pocillopora may be thought of as a

pioneer species and is a good candidate in that

their branched skeletons create the conditions

that allow other organisms to colonize an area

where they previously would not be able (Clark

& Edwards, 1994; Darling et al., 2012).

The benthic organisms and abiotic com-

ponents of the sea floor in this study were

categorized in operational taxonomic units

(OTUs). These OTUs included: rubble, sand,

bare calcium carbonate (CaCO3), the corals

Pocillopora spp. and Porites spp., dead Pocil-

lopora spp. (Dead Coral), unclassified sponge,

the macroalga Caulerpa spp., Cyanobacteria

(Cyano.), articulated coralline algae (ACA),

crustose coralline algae (CCA), the bivalve

mollusk Pinna rugosa and algal turf (Turf).

Fig. 3. Area-averaged daytime sea surface temperatures from the northern tip of Golfo Dulce from July 2018 to July 2020,

as derived from the MODISA satellite data using the NASA GIOVANNI web application for the coordinate rectangle: - 83°

26’ 12”, 8° 42’ 3”, - 83° 24’ 38, 8° 43’ 14.88”. Gray shading indicates the timeframe of the experiment.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

Transplantation site: Punta Bejuco reef

(8° 43’ 39” N, 83° 24’ 29” W) (Fig. 1) was

selected as the transplantation site for the

Pocillopora spp. colonies that were cultivated

in underwater coral nurseries near Playa Nicue-

sa of Golfo Dulce. Punta Bejuco was chosen as

a site for transplantation because Pocillopora

colonies that had been transplanted there prior

to this study were healthy and growing (T. Vil-

lalobos, pers. comm., 2020). The species of

corals used in this study were P. damicornis

and P. elegans although they were not distin-

guished from one another in the experiment.

Pocillopora spp. currently has low rates

of natural recruitment in Golfo Dulce (T. Vil-

lalobos pers. comm., 2020). Small Pocillopora

colonies are more likely to die as a result of

predation (Toh et al., 2014) and out-compe-

tition by algae (Kuffner et al., 2006). Punta

Bejuco consists of three reef-built platforms

with steeply sloping edges separated by chan-

nels of sand. The reef substrates are mostly

made up of dead Pocillopora and Psammocora

rubble. The predominant live coral species are

Porites lobata (Cortés, 1990) and Porites ever-

manni (Boulay et al., 2014) that have an aver-

age coverage of 0.97 % of the sea floor (Cortés,

1990). Living colonies of Pocillopora that

were not cultivated in coral nurseries are cur-

rently absent from Punta Bejuco, but the his-

torical presence of Pocillopora can be inferred

from coral skeletons (Cortés, 1990).

Out-planting of nursery-grown Pocil-

lopora colonies and experimental design: A

total of 30 Pocillopora spp. colonies were trans-

planted to the restoration site in Punta Bejuco

in July 2019. The colonies were anchored with

nylon zip-ties to steel nails, driven into the cal-

cium carbonate substrate in a six by five colony

rectangular arrangement with a distance of 30

cm from neighboring colonies. The rectangular

transect extended 15 cm from the centroids of

the fringing nails to measure 1.5 by 1.8 m in

total (Fig. 4). To understand how the presence

of the transplanted coral effected the benthic

Fig. 4. The arrangement of experimental colonies and nails within transects on the sea floor. The black dots represent nails

used as attachment points for the colonies or as markers of transect area and quadrat centers. The white circles represent

Pocillopora spp. colonies. The dotted line represents the edge of the experimental and control transects. Each colony or nail

position is given a procedural name so that it can be easily located.

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community, a control transect, devoid of coral

transplants was designated and monitored

using the same methods as the transplantation

site. The control transect was located approxi-

mately 10m from the experimental patch at

Punta Bejuco in a relatively flat region with a

(visually) similar substrate composition. This

transect was prepared in the same layout of

30 steel nails as the experimental transplanted

transect, but contains no Pocillopora trans-

plants (Fig. 4). The control patch contained no

corals, living or dead over the course of the

experiment. Likewise, the experimental patch

never contained P. rugosa. Both the experimen-

tal and control patches contained negligible

areas of sponge and sand.

Data Collection and Processing: Data

from the 30 transplanted Pocillopora spp.

colonies were recorded monthly from July

2019 to February 2020 using photography

and observation.

Coral transplant survivorship and bleach-

ing: The bleaching and survival status of each

Pocillopora spp. colony was recorded each

month. Coral could be categorized as bleached

(and alive), dead or healthy (neither bleached

nor dead). If a transplanted coral colony was

visibly completely white yet free of macroal-

gae, cyanobacteria or loose tissues, the colony

was recorded as bleached, having lost its

symbiotic microalgae. If a colony had tissues

visibly separated from the skeleton and/or the

exposed skeleton was completely covered in

macroalgae or cyanobacteria, the colony was

recorded as dead as it no longer had any sig-

nificant living, growing coral tissue.

In situ photography: To monitor the

behavior of the community of sessile ben-

thic organisms, a quadrat around each coral

colony was photographed once each month

from above using an Olympus TG-5 camera in

a proprietary waterproof housing attached to a

polyvinyl chloride (PVC) armature that held

the camera 40 cm above the sea floor. The base

of the armature formed a frame measuring 30 x

30 cm and was situated so that each anchor nail

was positioned at the center of the base using

virtually marked center point on the camera’s

monitor. For each photograph, the camera was

set to “under-water wide mode” with a zoom of

1.1 and set to shoot in RAW and JPEG image

file formats. Each image was evaluated using

the purpose-made photo analysis software,

PhotoQuad (Trygonis & Sini, 2012) in order to

calculate the coverage area of the transplanted

coral colonies and benthic sessile organisms.

Photo Preparation: The JPEG imag-

es from the camera were loaded into Adobe

Bridge where they were organized and renamed

according to the month and colony number or

position within the control transect. The images

were corrected for “fisheye” distortion from

the wide-angle settings of the camera and opti-

cal properties of water in the Adobe Camera

Raw image editor. To correct the distortion

effectively, the correction was set to the point

where the frame in the image was parallel with

the gridlines in Camera Raw. The distortion

correction was set to -31 for all of the images.

Quadrat assignment: Once loaded into the

PhotoQuad application, distances in the distor-

tion-corrected images of each coral were cali-

brated individually by selecting the “calibrate”

toggle and dragging the ends of the calibration

bar to the bottom inner edge of the T-joints on

the left and right of the PVC frame. The length

of the calibration bar was then set to 30cm, the

true distance between the supports of the PVC

frame (Trygonis & Sini, 2012).

Coral area measurement: The quadrat of

each image was assigned manually using the

“manual detection” toggle in the PhotoQuad

application. The quadrat was defined by drag-

ging the points supplied by the application to

the inner corners of PVC frame to draw straight

lines on the inner borders and around the joints

of the PVC frame. The area of the coral colo-

nies parallel to the substrate was measured with

the “region of interest” (ROI) method in Photo-

Quad (Trygonis & Sini, 2012). In this method,

the border of the living coral tissue (tissue that

was neither visibly separated from the skeleton

nor covered in macroalgae nor cyanobacte-

ria) was traced and assigned as Pocillopora

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damicornis. The data from PhotoQuad were

then exported as comma separated values for

analysis using R (R Core Team, 2013). The

“SPECIES Area Total cm2 (sic.)” PhotoQuad

output variable was used for analysis. This

value was defined by the following formula:

Where: Apix is the number of pixels enclosed

in the ROI; fclb is the calibration factor of the

image based on the distance between the inside

edges of the PVC frame in the image.

Benthic coverage measurement: The

benthic community of the experimental tran-

sects was defined as the area of each encrust-

ing organism or abiotic benthic component

(OTU) within the quadrat. The area of each

of the encrusting organisms was measured in

PhotoQuad using the grid method (Trygonis &

Sini, 2012). A grid was drawn over the quadrat

with the horizontal grid field set to 150 pixels,

equivalent to 2 250 pixels in each cell. Grid

cells were selected when positioned over an

encrusting organism. When the grid cells fell

over the borders of the encrusting organisms,

the fraction of the cell occupied by the encrust-

ing organism was estimated and added to other

occupied fractions of grid cells. When the

fractions added up to one (1), a grid cell was

selected. Selected grid cells were assigned to

the OTU they covered. The data consisted of

the area covered by the OTU in cm2, pixels,

and the proportion of the quadrat occupied by

that OTU. These data were imported into R for

analysis (R Core Team, 2013).

Outliers: Two coral colonies extended

beyond the PVC frame in the image. The data

from the quadrats that contained these two

colonies were excluded from the data set and

analysis, but left in situ for other experiments.

Data derived from in situ photography during

the month of August was not included in the

results because of malfunctions with the cam-

era case that negatively affected the quality of

the images.

Statistical analysis:

Growth rate: To estimate the rate of cover

growth (cm2) of the corals over the eight

months of the experiment, the average area

(cm2) of each Pocillopora spp. colony were

plotted each month with line-of-best-fit from

linear regression. The slope of the line-of-best-

fit was the areal growth rate of the colonies in

cm2 month-1.

Comparison of experimental and control:

Non-metric multidimensional scaling (nMDS)

from Bray-Curtis similarity matrices was used

to detect differences in the benthic community

composition in the initial (July 2019) and final

(February 2020) months in the experimental

and control patches. These similarity matrices

were built using the areas of each OTU in each

of the photo-quadrats. The area values of OTUs

in each patch were square root transformed to

ensure that OTUs that occupied small propor-

tions of each photoquadrat were would not

“drowned out” by the OTUs that occupied the

majority of the photoquadrat area and could be

compared on the same scale. These area values

excluded Pocillopora spp. colonies, dead coral

and artificial structures (anchor nails, tags

and zip ties) to ensure that any differences in

benthic community resulted from the presence

of transplanted coral rather than simply detect-

ing the growth of the transplants themselves.

ANOSIM was performed on the nMDS data

to quantify the separation and significance of

any difference between initial and final ben-

thic communities. SIMPER was performed to

identify which OTUs contributed most to any

differences that were detected. Construction,

visualization and analysis of nMDS were per-

formed in PRIMER 7 (Clarke & Gorley, 2015).

Temporal changes in sessile benthic

community: Changes in the area of OTUs

in each patch over time were estimated with

linear regression in R (R Core Team, 2013).

In the experimental patch, measurements from

quadrats where the coral colony had died were

analyzed separately from those that survived

the eight months of the experiment. The quad-

rats were separated in this manner to see if

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

temporal patterns in the abundance of benthic

organisms were different when the coral trans-

plant had died.

RESULTS

Coral Survivorship and bleaching: In

the eight months following transplantation

(July 2019 – February 2020), five of the 30 (17

%) colonies died; three (10 %) died in October

(four months from planting) and two more in

November (7 %) (Table 1). The colonies expe-

rienced two episodes of bleaching: the first, in

August and September 2019 (13 and 52 % of

the original 30 colonies, respectively) and the

second, in January and February 2020 (10 and

67 % of the original 30 colonies, respectively)

(Table 1). At the end of the experiment, 5 colo-

nies had died and of the remaining 25 living

colonies, 20 were bleached and 5 were healthy.

Areal Growth: The average area of live

Pocillopora spp. colonies increased signifi-

cantly (linear regression: P < 0.05, R2 = 0.036)

from an average of 119.4 ± 72.6 cm2 in July

2019 to 175.9 ± 113.0 cm2 in February 2020, a

68 % growth in area on average from initial to

final months. The change in area of the Pocil-

lopora spp. transplants was calculated to be 8.1

cm2 month-1 based on linear regression (R2 =

0.036, P < 0.05) (Fig. 5).

Change in the benthic community com-

position: The composition of the benthic com-

munity differed significantly between July

2019 and February 2020 in the experimental

patch (ANOSIM; P < 0.01, R = 0.147) but not

in the control patch (ANOSIM; P > 0.05, R =

0.031) (Fig. 6). Based on SIMPER analysis,

the main contributors to the difference in the

benthic community in the experimental patch

after 8 months following coral transplantation

were turf, CCA and Cyano.; contributing to

34, 27, and 37 % of the difference respectively

(Table 2).

Change in area of the benthic commu-

nities: In the experimental patch, the areas of

turf, cyanobacteria, dead coral, Pocillopora

spp. and CCA changed significantly over time

(linear regression: P < 0.05) in the 24 quadrats

where the colonies remained alive throughout

the experiment. The coverage area of turf

decreased by an average of 12.1 cm2 per month

and the coverage of cyanobacteria, dead coral,

and CCA increased by an average of 4.2, 1.0,

TABLE 1

Total number of transplanted Pocillopora spp. colonies that were bleached, dead, or healthy (neither bleached nor dead) each

month in the experimental patch in Golfo Dulce.

Month Jul Aug Sep Oct Nov Dec Jan Feb

Total n30 24 29 30 30 30 29 30

Total Bleached 0 3 15 0 0 0 3 20

Total Dead 00035555

% Bleached 0 % 13 % 52 % 0 % 0 % 0 % 10 % 67 %

% Dead 0 % 0 % 0 % 10 % 17 % 17 % 17 % 17 %

% Healthy 100 % 87 % 48 % 90 % 83 % 83 % 73 % 16 %

The number of colonies reported (n) varied from month to month due observational challenges.

Fig. 5. Monthly average area (cm2) of transplanted

Pocillopora spp. colonies in the transplanted site in Golfo

Dulce. The plot includes standard deviation and line-of-

best-fit from linear regression (line-of-best-fit equation:

Area of colony = 110.2 + 8.1 (number of months following

transplantation)); the gray area represents 95 % confidence

intervals.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

and 3.1 cm2 per month respectively. In the

four quadrats where corals died, the areas of

Pocillopora spp., cyanobacteria, and dead coral

changed significantly over time (linear regres-

sion: P < 0.05). The area of living Pocillopora

spp. decreased by 26.3 cm2 per month and the

areas of cyanobacteria and dead coral increased

by 32.8 and 24.8 cm2 per month respectively

(Fig. 7). In the control patch, the areas of OTUs

remained constant and none changed signifi-

cantly over time from their initial values.

The OTU that decreased the most in cov-

erage was Pocillopora spp. in the “dead” coral

quadrats with a decrease from 23.55 to 2.52 %

TABLE 2

Similarity of assemblages of benthic organisms in the

experimental patch at Punta Bejuco, Golfo Dulce and

OTUs with the greatest contribution as the result of

SIMPER.

Group Average

Similarity OTU % Contribution

February 84.68 % Turf 90.42

July 81.03 % Turf 90.47

February vs. July 80.55 %

Turf 33.67

CCA 27.32

Cyano. 26.39

Fig. 6. Non-metric multidimensional scaling of the benthic communities in Punta Bejuco July 2019 versus February 2020. A.

Communities in quadrats around Pocillopora spp. transplants in the experimental patch. B. Communities in quadrats around

marking nails in the control patch.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

of the total coverage. In the “dead” quadrats,

the coverage of cyanobacteria and dead coral

increased substantially as well from 0 to 20.20

% and 0 to 15.20 % respectively, taking up

more of the quadrats than the initial coverage

of the Pocillopora spp. transplants by 11.85

%. The average coverage of live Pocillopora

spp. increased by 7.95 % from 16.89 to 24.84

% in “live” coral quadrats. In the control patch,

no OTU changed more than 1.5 % in average

coverage of the quadrats (Table 3). No sand or

sponge was present in the control, nor experi-

mental patches.

DISCUSSION

Coral health and survivorship: Over

the course of eight months of this exploratory

study, there were two bleaching events and

17 % of the transplanted colonies died. It is

unknown whether a similar proportion of colo-

nies died in the nurseries where the corals were

grown. The first event occurred in August and

September 2019. High rainfall in these two

months typically causes significant run-off and

sedimentation in the gulf as sediment is washed

in from the surrounding rivers that feed into

Golfo Dulce and the water was visibly turbid

during field operations. This sedimentation

was one of the primary causes for the loss of

Pocillopora spp. colonies in the Gulf in the

1960’s-80’s (Cortés, 1990). Sediment settles

on the coral colonies, blocking sunlight, and

stimulating the production of excess mucus,

causing stress and bleaching (Philipp & Fabri-

cius, 2005). Alternatively, bleaching could

have occurred as the result of the stress of the

transplantation process, an event observed in

other restoration efforts (Cunning et al., 2014;

Forrester et al., 2012).

Fig. 7. Average areas (cm2) of benthic sessile organisms over time in the quadrats where corals in the experimental patch A.

survived for the length of the experiment or B. died before the end of the experiment and C. in the control patch at Punta

Bejuco, Golfo Dulce.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

The second bleaching event occurred in

January and February 2020. These months

correspond to the dry season when water tem-

peratures are typically elevated and sea surface

temperature at the study site averaged 31.2 °C

(Fig. 3) during this period of the experimental

timeframe. Although temperature tolerance can

vary significantly within corals of the same

species from different regions (Coles et al.,

1976), corals in the ETP have been reported to

bleach when sea surface temperatures exceed

30 ºC (Podestá & Glynn, 1997). In general,

corals often do not recover following severe

bleaching. The majority of the bleached cor-

als at the transplantation site regained some

of their original color and grew significantly

although none of the coral transplants regained

the color they had in the first month of the

experiment immediately following transplanta-

tion (personal observation).

Given that many of the colonies did not

survive in the timeframe of the experiment, a

different location and/or different environmen-

tal conditions should be considered for future

restoration efforts in Golfo Dulce. The rela-

tively shallow depth of the corals at 3 m may

have offered little protection for the corals from

higher temperatures near the water surface, or

higher light intensity; a problem encountered

in other coral transplantation efforts (Lohr

et al., 2016). Tides in Golfo Dulce can vary

between 2 m and 4 m in the inner part of the

gulf (Svendsen et al., 2006). The tidal activity

at Punta Bejuco was not recorded in this study

and it is possible that tides could have exacer-

bated the colonies’ exposure to solar radiation.

It is generally recommended to transplant cor-

als at the depth they are encountered naturally

in the area. In Golfo Dulce, Pocillopora spp. is

encountered from 3 to 5 m below the surface

(Cortés, 1990) although most of the native

colonies that provided fragments for the nurs-

ery were deeper, up to 8 m below the surface

(J. Kleypas, pers. comm., 2020.). As of October

2020, almost all of the nearby coral transplants

that were not part of the experiment and which

were positioned deeper at 5.6m survived the

TABLE 3

Average percent proportions (SD) of the quadrat area occupied by benthic organism OTUs in the initial (July) and final (February)

months of data collection at Punta Bejuco, Golfo Dulce.

Status nRubble ACA Bare CaCO3Pinna rugosa Pocillopora spp. Caulerpa spp. Porites spp. Turf Cyano. Dead Coral CCA

Live Jul Avg 23 0.0(0.0) 0.0(0.0) 0.1(0.5) 0.0(0.0) 16.9(10.6) 0.3(0.7) 0.5(2.4) 80.5(10.5) 0.18(0.9) 0.0(0.0) 1.6(3.1)

Live Feb Avg 17 0.0(0.0) 0.0(0.0) 0.0(0.0) 0.0(0.0) 24.8(13.2) 0.1(0.4) 0.8(3.3) 65.4(11.7) 3.6(4.2) 1.0(2.7) 4.2(3.8)

Dead Jul Avg 4 0.0(0.0) 0.0(0.0) 0.0(0.0) 0.0(0.0) 23.6(7.3) 0.0(0.0) 0.0(0.0) 73.5(6.0) 0.0(0.0) 0.0(0.0) 2.9(2.5)

Dead Feb Avg 4 0.0(0.0) 0.2(0.3) 0.0(0.0) 0.0(0.0) 2.5(2.9) 0.0(0.0) 0.0(0.0) 60.2(12.8) 20.2(9.4) 15.2(7.4) 1.7(1.5)

Cons Jul Avg 21 0.2(0.9) 0.0(0.0) 1.1(3.7) 0.1(0.3) 0.0(0.0) 0.0(0.2) 0.0(0.0) 97.1(6.2) 0.0(0.0) 0.0(0.0) 1.5(2.7)

Cons Feb Avg 29 0.0(0.0) 0.0(0.0) 0.2(0.9) 0.1(0.5) 0.0(0.0) 0.0(0.0) 0.0(0.0) 98.5(2.2) 0.0(0.1) 0.0(0.0) 0.9(1.6)

Averages are grouped by the patch and status of coral outplants as follows: Live – quadrats in the experimental patch where the coral survived the entire 8 months of the experiment;

Dead – quadrats in the experimental patch where the outplants died at some point over the course of the experiment; Control – quadrats (Cons) in the control patch.

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

bleaching event in January and February 2020

(T. Villalobos, pers. comm., 2020).

Coral growth: Despite the two bleach-

ing events and non-ideal transplantation site,

the average area of the corals grows signifi-

cantly over the course of the experiment. Other

research suggests that the average sizes of the

Pocillopora spp. colonies in the experimental

patch were in a range of sizes that are likely to

grow but less likely to survive over the course

of a year (Ishida-Castañeda et al., 2020; Kodera

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

This practical information could be very useful

for determining the size of coral transplants to

use for the purposes of restoration.

Temporal change in the sessile ben-

thic community following transplantation:

The increase in area of live coral, CCA and

Cyanobacteria and decrease in area of algal

turf in the experimental patch following the

transplantation of Pocillopora spp. colonies

suggests that the coral colonies affected the

succession of the sessile benthic community.

Corals, especially structurally complex, highly

branched forms such as Pocillopora, attract

associated fauna (Lewis, 1986, Smith et al.,

2010). Herbivorous coral associates contribute

to the health and resilience of coral reefs by

preventing algal succession from progressing

from a state dominated by early successional

CCA which do not compete with corals and

fleshy, leafy algae which impede growth of

corals (Burkepile & Hay, 2010; Hixon & Bron-

stoff, 1996; Humphries et al., 2014).

The lack of change in the coverage of

sessile benthic organisms in the control patch

further supports the conclusion that coral had

an effect on the trajectories of succession of

the benthic community. Differing trends in the

area of turf between experimental and control

patches may be the result of greater herbivory

in the experimental patch from herbivores

attracted to the structural complexity of the

transplanted coral (Lewis, 1986; Smith et al.,

2010). Conversely, the area of algal turf in

the control patch remained constant and high

because it is less structurally complex and thus

attracts fewer herbivores (Lewis, 1986).

Over the entire experimental patch and

particularly in quadrats where corals had died,

there was a strong increase in the coverage

of cyanobacteria. In quadrats where the coral

transplants had died, the area of cyanobacteria,

along with dead coral tissue had almost entirely

replaced live coral by the end of the experi-

ment. Cyanobacteria flourish in high tempera-

tures and could have contributed to the ultimate

death of the coral colonies following bleaching

by smothering the weakened coral and ben-

thos (Ford et al., 2018; Kuffner et al., 2006).

Cyanobacteria may produce toxins that could

deter herbivores that would otherwise control

macroalgal populations (Ford et al., 2018; Leão

et al., 2012). It is important to understand the

characteristics and processes that occur when

coral colonies die because it can provide clues

and warnings when monitoring the health of

reefs and implementing management responses

(Goatley et al., 2016). This could be a problem

for future coral transplantation in the zone as

the environmental conditions in the shallow

reefs of Golfo Dulce could favor the growth

of Cyanobacteria.

The decrease in algal turf in the experi-

mental patch from ~80 to ~65 % is comparable

in magnitude to the decrease in turf coverage

at the coral reefs of Coco Island following 20

years of reef recovery after the 1982-83 ENSO

event (Guzmán & Cortés, 2007). Coral cover-

age recovered from an average of 2.99 ± 0.25

% to 14.87 ± 6.78 % (average ± SE) % at Coco

Island, a similar magnitude to this study with

the experimental patch containing a negligible

coverage of coral before transplantation and

upwards of 24.8 % coverage eight months fol-

lowing transplantation. Although the study at

Coco Island was conducted at a much larger

spatial and temporal scales, and under much

higher conservation standards than in Golfo

Dulce, similar processes may account for the

decrease in turf coverage albeit over a much

shorter time period in this study. Restora-

tion, together with other coastal management

actions, could increase the survivorship of the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

corals and the recovery of the reef and their

ecological functions.

Although one of the shortest times report-

ed for succession to reach a climax in a coral

reef ecosystem is approximately ten months

(Matsuda, 1988), the process of succession on

coral reefs generally takes much longer than the

timeframe of this experiment (Karlson, 1999).

Over a longer timeframe, further evidence of

succession and its associated ecological pro-

cesses could be detected. Also, following the

ultimate bleaching and death of the coral trans-

plants, a longer experiment could explore how

succession of the sessile benthic community

changes following the death of corals, a process

that was beginning to occur with the increase

in cyanobacteria. Coral-algae interactions also

vary seasonally due to the complex interplay

between encrusting organisms, grazing ani-

mals, eroding animals, and the environmental

variables that effect their health, populations

and behaviors (Brown et al., 2019; Doropoulos

et al., 2016; Fong et al., 2016; Muthukrishnan

et al., 2016). As this experiment lasted less than

a year, a longer experiment where seasonal

cycles repeat could help discern what changes

in the benthic community are due to seasonal

shifts versus succession.

Photo-quadrats were positioned directly

over the transplanted coral colonies in the

experimental patch, resulting in a bias toward

greater coral coverage. An experiment using

larger quadrats could capture the dynamics

of the sessile benthic community at the scale

of a reef rather than a colony. The differ-

ences observed in the dynamics of the benthic

communities in the experimental and control

patches may be the result of methodological

artifacts. The observed decrease in turf area

may be the result of the coral transplants tak-

ing up more area of the photoquadrats as their

branches grow up and over the sea floor. The

branches could be covering turf in the image

that may still be present around the bases of the

colonies and thus, reduce their apparent area.

Ecological succession is intrinsically

important to restoration efforts. Environmen-

tal and ecological conditions can direct the

succession of a reef towards alternate stable

states (Smith et al., 2010). Under current envi-

ronmental conditions, many coral reefs tend

to follow a successional trajectory that favors

the dominance of algae and other organisms

that inhibit the recruitment and growth of cor-

als (Pandolfi et al., 2005; Rinkevich, 2005).

Coral restoration through transplantation is an

increasingly common intervention that is used

to accelerate the process of succession to favor

the growth and persistence of coral reefs.

The transplantation of Pocillopora spp.

colonies influenced the succession of a ses-

sile benthic community of a restoration site

in Golfo Dulce, as evidenced by the growth

of organisms that promote coral growth and

the decline of those that compete for space

and resources with corals. Additionally, fol-

lowing transplantation, these shifts in the sea

floor composition favored a successional tra-

jectory that promotes the growth of coral and

may improve the reefs’ resilience to future

disturbance and the acceleration of ecosystem

recuperation. Transplantation and growth of

Pocillopora spp. colonies corals modified the

local ecosystem around the colonies to promote

further coral reef growth and development.

These results suggest that the transplantation of

Pocillopora spp. could improve the outcomes

of coral restoration efforts by changing the

trajectory of succession. However, this must

be carried out in conjunction with watershed

management to reduce sedimentation in the

area and associated stress to the corals. A simi-

lar experiment conducted over longer temporal

and larger spatial scales may reveal if succes-

sional trends continue or change.

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.

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54881, abril 2023 (Publicado Abr. 30, 2023)

ACKNOWLEDGMENTS

We acknowledge the Center for Research

in Marine Science and Limnology (CIMAR),

the University of Costa Rica, and Raising Coral

Costa Rica for their resources and support.

Additionally, we acknowledge the field sup-

port, data collection and advice from Tatiana

Villalobos, José Andrés Marín Moraga, Celeste

Sánchez, Adriana Arce, Beatriz Naranjo, Tati-

ana Araya, Fabio Quesada, Sebastián Mena,

Andrea Arriaga, José Cascante, Carolina Salas-

Moya, Cindy Fernández, Sergio Madrigal,

Sònia Fabregat, Mario Espinoza, Davis Morera,

Eleazar Ruiz, Jon Chomitz, Virginia Rall Cho-

mitz and especially Juan Carlos Azofeifa who

was instrumental to every trip to the field. This

study could not have been carried out without

their generous contributions of time, resources

and creativity.

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