Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Change in the composition of fauna associated with Pocillopora spp.

(Scleractinia, Pocilloporidae) following transplantation

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, juan.alvarado@ucr.ac.cr

4. Escuela de Biología, Universidad de Costa Rica, San Pedro, San José, Costa Rica.

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

Florida, United States of America.

Received 24-VIII-2022. Corrected 31-I-2023. Accepted 17-II-2023.

ABSTRACT

Introduction: Associated fauna comprises most of the diversity of a coral reef and performs ecological func-

tions essential to the reef’s survival. Since Pocillopora corals harbor an important associated fauna, reef restora-

tion efforts are underway in Golfo Dulce, Costa Rica, to preserve them.

Objective: To describe changes in cryptofauna and fish communities associated with Pocillopora colonies to

better understand the succession of associated fauna following transplantation.

Methods: An experimental patch of 30 nursery-grown Pocillopora colonies and a control patch containing

no colonies were monitored for 8 months following transplantation in Golfo Dulce. Cryptofauna within each

colony and fish within each patch were observed using SCUBA to quantify temporal changes in the abundance,

diversity, and community structure of the colonies.

Results: The abundance and diversity of cryptofauna increased throughout the experiment. Obligate symbiont

decapods were the most abundant. The composition of the community of cryptofauna differed between periods

with fish in the genus Scarus as the main contributor to any differences. The increase in abundance and diversity

of cryptofauna and fish may reflect coral growth and the corresponding availability of space and environmental

complexity in the experimental patch. The composition of the cryptofauna communities was generally consistent

with other studies. However, a high density of decapod symbionts could suggest that without other Pocillopora

colonies to move to, they may crowd together despite their aggressive tendencies.

Conclusions: Pocillopora colonies will experience an increase in symbionts that could positively contribute to

the health and survival of the coral following transplantation.

Key words: ecology; symbiosis; facultative; cryptic; seasonality.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54882

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

Coral reefs are the most diverse ecosys-

tems on Earth in terms of higher taxonomic

classification. Coral reefs harbor 32 of the

34 animal phyla, compared to 12 that live in

terrestrial environments (Reaka-Kudla, 1997;

Stella et al., 2011). The extraordinary biodi-

versity of coral reefs can be attributed to the

structural complexity of the corals and the

framework that they construct. This structural

complexity corresponds to a great diversifica-

tion and quantity of ecological niches that, in

turn, attract a large diversity of fauna (Stella

et al. 2011). The cryptofauna, the animals

that live in between the branches of the coral

and the reef structure, comprise the greatest

number of animal species on a reef but are

often overlooked when studying reef ecol-

ogy (Cortés et al., 2017; Glynn, 2013; Stella

et al. 2011). Corals host a variety of cryptic

organisms, many of which are symbionts that

live exclusively on particular species of corals

(Abele & Patton, 1976; Glynn, 1980; Glynn,

1983; Sin, 1999; Stella et al., 2010; Stella et al.

2011). The cryptofauna depend on the corals

for protection, food, and reproduction (Abele

& Patton, 1976; Castro, 1988; Stella et al.,

2011). In return, cryptofauna carry out critical

ecological processes within the reef ecosystem

such as protecting coral colonies and capturing

and recycling nutrients (Glynn, 2013; Glynn &

Enochs, 2011; Stella et al., 2011).

A great number of fish species also have an

ecological association with, or dependence on,

coral reefs for shelter, as direct or indirect food

sources, and as sites of reproduction (Froehlich

et al., 2021; Moeller et al., 2023). Some fish

live in closer association with the corals than

others, ranging from cryptic species living

within the branches to pelagic species that rely

on food sources derived from reefs (Reaka-

Kudla, 1997). The reef fish, in turn, provide

a variety of critical services to the reefs they

inhabit (Burkepile & Hay, 2010; Hixon, 1997;

Hixon & Bronstoff, 1996). Herbivore fish and

RESUMEN

Cambio en la composición de la fauna asociada a Pocillopora spp.

(Scleractinia, Pocilloporidae) después del trasplante.

Introducción: La fauna asociada comprende la mayor parte de la diversidad de un arrecife de coral y realiza

funciones ecológicas esenciales para la supervivencia del arrecife. Dado que los corales Pocillopora albergan

una importante fauna asociada, se están realizando esfuerzos de restauración de arrecifes en Golfo Dulce, Costa

Rica, para preservarlos.

Objetivo: Describir los cambios en la comunidad de criptofauna y peces asociados a las colonias de Pocillopora

para comprender mejor la sucesión de la fauna asociada después del trasplante.

Métodos: Un parche experimental de 30 colonias de Pocillopora cultivadas en vivero y un parche de control que

no contenía colonias fueron monitoreados durante 8 meses después del trasplante en Golfo Dulce. La criptofau-

na dentro de cada colonia y los peces dentro de cada parche se observaron usando SCUBA para cuantificar los

cambios temporales en la abundancia, diversidad y estructura de la comunidad de las colonias.

Resultados: La abundancia y diversidad de criptofauna aumentó a lo largo del experimento. Los decápodos

simbiontes obligados fueron los más abundantes. La composición de la comunidad de criptofauna difirió entre

períodos con peces del género Scarus como el principal contribuyente a cualquier diferencia. El aumento en la

abundancia y diversidad de criptofauna y peces puede reflejar el crecimiento de coral y la correspondiente dis-

ponibilidad de espacio y complejidad ambiental en el parche experimental. La composición de las comunidades

de criptofauna fue generalmente consistente con otros estudios. Sin embargo, una alta densidad de simbiontes

decápodos podría sugerir que, sin otras colonias de Pocillopora a las que trasladarse, pueden amontonarse a pesar

de sus tendencias agresivas.

Conclusiones: Las colonias de Pocillopora experimentarán un aumento de simbiontes que podrían contribuir

positivamente a la salud y supervivencia del coral después del trasplante.

Palabras claves: ecología; simbiosis; facultativo; críptico; estacionalidad.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

invertebrates graze on algae and reduce its cov-

erage so that the algae do not compete with cor-

als for space and resources (Burkepile & Hay,

2010; Hixon & Bronstoff, 1996; Hughes et al.,

2017; Humphries et al., 2014). Invertebrate-

eating fish protect the colonies from corallivo-

rous invertebrates, and predatory piscivorous

fish maintain healthy balances of reef species

by controlling the populations of coral preda-

tors and bio-eroding herbivores (Hixon, 1997).

One of the most important contributing

factors to supporting cryptofauna is the health

of the coral itself. Live corals have greater

diversity and abundance of fish than dead

corals (Bell & Galzin, 1984). Bleached cor-

als have less abundance and fewer species of

cryptic fauna than healthy corals (Tsuchiya,

1999). On dead coral, there is an initial increase

in biodiversity as boring invertebrates colo-

nize the exposed carbonate skeleton, which

is unprotected by the coral’s stinging polyps

(Enochs, 2012). This diversity is not sustained,

however, as eventually the skeleton is eroded,

and with it, the structural complexity sustains

the biodiversity of a living coral reef (Enochs

& Manzello, 2012a).

Coral restoration is essential to the facili-

tation and acceleration of natural successional

processes through the reintroduction and man-

agement of key species (Horoszowski-Fridman

& Rinkevich, 2017; Horoszowski-Fridman et

al., 2015; Walker, et al., 2007; Young, 2001).

Thus, the best sites for coral reef restoration are

those sites where corals previously flourished

but where they are unlikely to settle and grow

under the current conditions (Rinkevich, 2005).

Likewise, the best candidates for species to

be transplanted are those that might not colo-

nize the restoration area unassisted (Society

for Ecological Restoration International Sci-

ence & Policy Working Group [SER], 2004).

Pocillopora coral is a good candidate for reef

restoration in that their branched skeletons

create conditions that allow other organisms

to colonize an area where they previously

lacked habitat (Clark & Edwards, 1994; Dar-

ling et al., 2012).

Except for a survey of coral borers (Fon-

seca & Cortés, 1998), no published survey

information exists that describes the species

of cryptic fauna associated with Pocillopora

in Golfo Dulce. However, the coral-associ-

ated fauna expected to be present can be

predicted from surveys conducted in other

reefs in the Eastern Tropical Pacific (ETP)

including Bahía Culebra, Costa Rica (Alvarado

& Vargas-Castillo, 2012; Salas-Moya et al.,

2021), Uva Island in Panama (Abele & Pat-

ton, 1976; Glynn, 1980; Glynn, 2013; Gotelli

& Abele, 1983; Gotelli et al., 1985), and the

Pacific coast of Mexico (Hernández et al.,

2009; Hernández et al., 2013). The species

composition of ichthyofauna of Golfo Dulce

is similar to but statistically different from that

of the rest of the Pacific coast of Costa Rica

(Alvarado et al., 2014).

The timing of recruitment of the associated

fauna onto a coral colony appears to also be of

importance for the reef’s survival and health.

For example, it is known that some cryptic

fauna is recruited to corals quickly and begin to

reduce the effects of sedimentation and provide

protection from predation (Glynn, 2013; Stew-

art et al., 2006). This is particularly important

for juvenile corals compared to larger, more

mature corals (Toh et al., 2014). In laboratory

settings, juvenile host corals have higher sur-

vival rates when colonized with juvenile Trape-

zia crabs, which offer the host coral protection

from predation (Rouzé et al., 2014). However,

it is not known when and in what order cryptic

fauna are recruited in coral transplants.

Although non-coral animals such as fish

and invertebrates make up the majority of a

reef’s biomass and diversity (Cortés et al.,

2017; Stella et al., 2011), most studies address-

ing the success of a restoration effort focus on

the growth and survival of the corals them-

selves (Ladd et al., 2019; Stella et al., 2011).

While the corals are critical to forming the

basic structure of coral reefs that allows them

to harbor such great biodiversity, the effect of

reef restoration on the community structure of

coral-associated animals is relatively under-

studied by comparison. Most of the available

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

literature on the succession of fish following

restoration efforts focuses on non-living arti-

ficial reefs (Becker et al., 2017; Russell, 1975;

Santos et al., 2011). Similarly, studies concern-

ing the succession or community structure of

cryptic fauna on reefs have used non-coral

substrates (Breitburg, 1985) or the collec-

tion and destruction of coral colonies (Enochs

& Hockensmith, 2008; Enochs & Manzello,

2012b; Enochs et al., 2011).

Given the importance of reef-associated

animals to the health and survival of the coral,

the ecosystem services provided by the asso-

ciates, and the wide-ranging impacts of reef

communities on the ecology of the oceans,

more research on the effects of reef restoration

and rehabilitation on coral-associated animals

is essential. Ecological restoration and reha-

bilitation are considered to be successful when

they can regain the full complement of native

species and recuperate ecological processes

essential for the long-term persistence and self-

sustainability of the reef (SER, 2004; Walker

et al., 2007).

To understand the processes of the suc-

cession of the cryptofauna and fishes in a

coral reef of the ETP, this project aims to: 1)

Describe the community of cryptofauna living

in the coral transplants; 2) monitor changes in

the community of cryptofauna in Pocillopora

colonies in the 8 months following transplan-

tation; and 3) explore changes in the reef fish

community following transplantation.

MATERIALS AND METHODS

Golfo Dulce is a narrow-mouthed embay-

ment (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 approxi-

mate length of 50 km and width between 10

Fig. 1. Location of Golfo Dulce within Costa Rica: Punta Bejuco (transplantation site) is marked with a red star and Nicuesa

(coral nursery), is marked with a red asterisk. The red triangle in the top-right quadrant marks the meteorological station.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

and 15 km, and covers an area of 680 km2

with a maximum depth of 200 m. The average

yearly rainfall in Golfo Dulce is 4 000 to 5 000

mm and temperatures range from 18 ºC to 35

ºC with an average of approximately 26.5 ºC.

The dry season lasts from December to March

with an average rainfall of 100 to 160 mm per

month. The wet season peaks in October with

an average monthly rainfall of 800 mm (Cortés,

1990; Quesada-Alpízar & Cortés, 2006). For

this study, data collection months were grouped

by “seasons” that roughly correspond to sea-

sonal ranges in Golfo Dulce as described by

Cortés (1990). The “Wet” season includes Sep-

tember, October, November, & December, the

“Dry” season includes January, February, and

March, and the “Transition” season includes

April, May, June, July, & August. During the

period of this study (July 2019 – June 2020),

there was a total rainfall of 3 687 mm based on

meteorological data from the Fundación Neo-

trópica station of the Instituto Meteorológico

Nacional, near Golfo Dulce (08º 42’ 02.9” N,

83º 30’ 49.4” W, at 80 m above sea level) (Fig.

2). The area-averaged daytime sea surface tem-

peratures during the study period ranged from

29.3 ºC in October to 31.4 ºC in February based

on the NASA GIOVANNI satellite (Fig. 3).

Timeframe: The experiment took place

between July 2019 and February 2020. Twelve

months of data collection were planned, but

due to the COVID-19 global pandemic, field

trips were terminated in February 2020, result-

ing in eight months of data.

Geographically and ecologically, Golfo

Dulce is part of the ETP marine biologi-

cal province (Glynn et al., 2017). It is often

referred to as a tropical fjord due to its anoxic

deep waters and bathymetry (Cortés, 1990;

Hebbeln & Cortés, 2001; Wolff et al., 1996).

The anoxic waters prevent the energy contained

in detritus that sinks to the depth of the gulf to

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

2020. The timeframe of the experiment is shaded in gray. Data from the NASA GIOVANNI satellite.

Fig. 2. Rainfall (mm month-1) data from the Instituto

Meteorológico Nacional de Costa Rica, near Golfo Dulce

(08º42’03”N, 83º30’49”W, at 80 m above sea level). The

gray shaded area represents the timeframe of the study.

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

be recycled back into higher trophic levels of

the ecosystem (Wolff et al., 1996).

Experimental coral colonies: Thirty

Pocillopora damicornis (Linnaeus, 1758) and

Porites evermannii Vaughan, 1907 colonies

were selected at random from a crop of colonies

grown in the coral tree nurseries in Nicuesa,

Costa Rica (Fig. 1). These nurseries form part

of a restoration initiative that started in 2016

as a project of the non-governmental organiza-

tion Raising Coral Costa Rica and the Center

for Research in Marine Science and Limnol-

ogy (CIMAR) of the University of Costa Rica

(UCR) (Kleypas et al., 2021; Villalobos, 2019).

The two species were not distinguished for this

study and are referred to as “Pocillopora” for

the rest of this article.

Transplantation site: Punta Bejuco reef

(8° 43’ 39” N, 83° 24’ 30” W) (Fig. 1) was

selected as the transplantation site for the Pocil-

lopora colonies. Punta Bejuco consists of three

reefs with steeply sloping edges separated by

channels of sand. The reef substrates are mostly

made up of dead Pocillopora and Psammocora

rubble. The live coral species Porites lobata

Dana, 1846 and P. evermanni are predominant

in this site (Boulay et al., 2014; Cortés, 1990).

No live colonies of Pocillopora have pres-

ently been encountered in Punta Bejuco, but

the presence of live Pocillopora in the past can

be inferred from coral skeletons (Cortés, 1990).

Pocillopora corals have low rates of natural

recruitment in Golfo Dulce (Villalobos, 2019),

and small colonies are more likely to die as a

result of predation (Toh et al., 2014) and com-

petition with algae (Kuffner et al., 2006).

Out-planting of nursery-grown Pocil-

lopora colonies and experimental design:

The colonies were anchored with nylon zip-

ties to steel nails, and driven into the calcium

carbonate substrate in a six by five rectangular

arrangement of the colonies 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 affects

the fish and benthic invertebrate communities

and the sea floor cover, a control transect was

designated and monitored using the same meth-

ods as the transplantation site, e.g., with 30

steel nails but devoid of Pocillopora outplants

(Fig. 4). The control transect is located at Punta

Bejuco at the same depth as the transplant area

in a relatively flat region with a (visually) simi-

lar substrate composition.

Monitoring of cryptic fauna: In the

transplanted transect, the cryptofauna in each

colony were identified and counted by visual

census every month. The observer identified

and recorded all of the visible cryptofauna

occupying the space between the branches or

on the surface of each colony. The observer

positioned themselves about 3 to 10 cm from

each colony and viewed it from every angle

to ensure that they recorded all cryptofauna

therein before moving to the next colony. Most

methods used to investigate the cryptofauna

living between the branches of corals require

the corals to be removed from the study site

and destroyed (Abele & Patton, 1976; Alvarado

& Vargas-Castillo, 2012; Enochs & Hock-

ensmith, 2008; Enochs & Manzello, 2012a;

Enochs & Manzello, 2012b; Stella et al., 2010).

In situ visual identification provides a low-cost,

non-destructive method for the quantification

of the cryptic community over time, although

it is not as effective as a destructive collec-

tion in the identification of very small and

burrowing cryptic species (Alzate et al., 2014;

Caldwell et al., 2016) which were not the focus

of this study.

Monitoring of ichthyofauna communi-

ties in transplanted and control transects:

To identify and count the reef-associated fish

in either patch, each month a diver observed

ichthyofauna from a fixed position approxi-

mately 2 m away from the deepest border of the

out-planted transect and the control transect.

For 10 minutes on each experimental patch,

the observer identified and counted fish within

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

an imaginary rectangular prism extending the

length and width of each transect and 3 m

above the sea floor (Fig. 5). The icthyofauna

communities associated with the Pocillopora

outplants and control transect were summa-

rized by three measurements: Shannon-Weiner

diversity index (H’ = -Σpi * ln(pi)), total abun-

dance of fish, and the specific abundance of

each species.

Data analysis

Cryptofaunal community: The diver-

sity and abundance of cryptic organisms are

described in terms of operational taxonomic

units (OTUs) instead of species according

to Enochs & Manzello (2012b), to prevent

overestimation. The cryptic faunal community

associated with the Pocillopora outplants is

summarized in terms of the number of OTUs,

the total abundance of cryptic organisms, and

the specific abundance of each OTU in each

colony and within the experimental patch as

a whole. The diversity of the cryptofauna was

defined as the number of unique OTUs present

in each colony.

Generalized linear models (GLMs) in

Poisson distribution were used to identify

trends in both abundance and diversity over

time in the eight months following transplanta-

tion. To explore changes in the cryptofaunal

community living between the branches of the

transplanted Pocillopora colonies, the similar-

ity of community composition in terms of the

presence and abundance of cryptofauna OTUs

between and across months and seasons (dry,

transition, and rainy) was quantified with clus-

ter analysis performed in PRIMER 7 (Clarke

& Gorley, 2015). First, the average abundance

of each cryptic species each month was square

root transformed to enhance the impact of less

common OTUs and to diminish that of the

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 (left) or as controls (right). The circles represent Pocillopora colonies. The dotted

line represents the edge of the experimental and control patches. Each colony or nail position is given a procedural name

so that it can be easily located.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

most common OTUs. The transformed data

were then used to build a Bray-Curtis similarity

matrix (Clarke & Gorley, 2015). This similarity

matrix was used to represent the similarity of

the cryptic community each month in two (2)

dimensions using non-metric multidimensional

scaling (nMDS) (Clarke & Gorley, 2015) and

to build a dendrogram showing the similarity

of the cryptic community of the transplanted

colonies between sample months. Additionally,

the data were used to generate a heat plot that

displays the contribution of each OTU to the

cryptic community each month.

To test for significant differences in the

cryptic community between seasonal groupings

of months in terms of the average abundance of

OTUs, an analysis of similarity (ANOSIM)

was conducted using the Bray-Curtis similarity

matrix. To determine which OTUs contributed

most to any dissimilarity in the cryptofau-

nal community amongst groupings, similarity

percentage analysis (SIMPER) was conduct-

ed using the Bray-Curtis similarity matrix in

PRIMER 7 (Clarke & Gorley, 2015).

Ichthyofaunal community: Student’s

t-tests were performed in R to detect differenc-

es between the experimental and control tran-

sects in the abundance (number of individuals

per patch) and Shannon-Weiner diversity index

(H’) of the ichthyofauna over the eight months

of data collection. The ordination method of

nMDS was performed in PRIMER 7 (Clarke &

Gorley, 2015) to explore differences in the reef

fish community between the experimental and

control patches. The abundances of fish spe-

cies each month were square root transformed

to enhance the impact of less common species

and to diminish that of the most common spe-

cies. The transformed data were then used to

build a Bray-Curtis similarity matrix (Clarke

& Gorley, 2015). This similarity matrix was

used to represent the similarity of the fish com-

munity each month in two dimensions using

non-metric multidimensional scaling (nMDS)

(Clarke & Gorley, 2015). Differences in the

reef fish community between experimental and

control patches were explored with ANOSIM

and SIMPER tests in PRIMER 7(Clarke &

Gorley, 2015).

RESULTS

Description of the cryptofaunal commu-

nity: Over the eight months of the study, a total

of 17 OTUs of cryptofauna were identified

and counted (Table 1). These OTUs were split

into four categories based on their taxonomy

and ecological role in the reef ecosystem: (1)

Fig. 5. Method for counting coral-associated fish at the experimental and control sites.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

decapod crustaceans, (2) cryptic fish that per-

manently occupied the spaces between the

coral branches, (3) reef fish that are usually

encountered in the water column around corals,

and (4) encrusting animals attached to the coral

transplants. The decapod crustaceans included

Trapezia spp., Alpheus lottini, Harpiliopsis

depressa, Palaemonella holmesi, Palaemon rit-

teri, the family Paguridae, and the superfamily

Majoidea. All of the cryptic fish were within

the order Blenniiformes, and included Axo-

clinus lucilae, Acanthemblemaria exilispinus,

Elacatinus punticulatus, Plagiotremus azaleus,

and individuals that were not identified at the

species level within the family Tripterygiidae.

Reef fish included Abudefduf troschelli, Scarus

spp., Stegastes acapulcoensis, and fish within

the family Chaetodontidae. The encrusting

metazoan group included polychaetes within

the family Sabellidae, ascidians, gastropods

within the family Vermetidae, and bivalves

within the genus Spondylus.

Patterns in the community of cryp-

tofauna in Pocillopora colonies following

transplantation: The dominant cryptofauna

throughout the experiment were symbiont

decapods in the OTUs Trapezia spp., Harpili-

opsis depressa, and Alpheus lottini. They com-

prised on average 81 % (43 %, 30 %, and 18

% respectively) of the fauna identified within

the 30 colonies over the eight months of moni-

toring (Table 1). The rest of the cryptofauna

identified within the colonies were cryptic

fish, transient fish, and encrusting metazoans,

accounting for 19 % of the associated fauna

found between the branches of the Pocillopora

transplants.

TABLE 1

Counts and percentages of cryptofauna OTUs identified within the transplanted corals each month following transplantation

at Punta Bejuco, Golfo Dulce.

Group O T U (symbol) Jul19 Aug19 Sep19 Oct19 Nov19 Dec19 Jan20 Feb20

n % n % n % n % n % n % n % n %

Decapod Trapezia spp.* (tra) 168 54.7 117 50.9 153 45.0 128 30.8 153 49.7 181 51.9 252 37.9 250 38.9

Decapod Harpiliopsis depressa* (hde) 103 33.6 73 31.7 83 24.4 183 44.0 79 25.6 50 14.3 238 35.8 157 24.4

Decapod Alpheus lottini * (alo) 24 7.8 38 16.5 90 26.5 89 21.4 46 14.9 102 29.2 119 17.9 91 14.2

Encruster Spondylus sp. (spo) 8 2.6

Decapod Palaemonella holmesi (pho) 4 1.3 46 7.2

Decapod Majoidea (maj) 2 0.9

Cryptic fish Blenniiformes (blenny) 4 1.2 4 1.0 18 2.7 2 0.3

Decapod Paguridae (pagu) 4 1.2 8 1.9 10 3.2 4 1.1 10 1.5 8 1.2

Encruster Vermetidae (verm) 2 0.6 2 0.5 10 3.2 4 1.1 2 0.3

Encruster Ascidea (asci) 2 0.5 2 0.6 6 1.7

Encruster Sabellidae (sab) 8 2.6 2 0.6

Reef fish Scarus spp. (scar) 24 3.6 27 4.2

Reef fish Stegastes acapulcoensis (sac) 4 0.6 8 1.2

Decapod Palemon ritteri (pri) 42 6.5

Reef fish Chaetodontidae (chaet) 8 1.2

Reef fish Abudefduf troschelli (atr) 2 0.3

TOTAL Abundance 307 100 230 100 340 100 416 100 308 100 349 100 665 100 643 100

Total OTUs 546777712

Symbols in parentheses are used in Fig. 8. Asterisks (*) indicate OTUs that are obligate symbionts of Pocillopora spp. OTUs

are arranged by order of first observ ation and percent contribution to the cryptofaunal community each month.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Abundance: In July 2019, the day fol-

lowing the transplantation of the colonies, an

average of 10 individual cryptic organisms

were observed per colony (ind colony-1). In

February 2020, an average of 21 ind colony-1

were observed. Based on the GLM analysis,

the abundance of cryptofauna living within the

transplanted coral colonies increased signifi-

cantly with time (P < 0.001, df = 7) over the

eight months following transplantation (Fig. 6).

Diversity: The diversity of cryptofauna

within the transplanted coral colonies increased

significantly with time (P < 0.01, df = 230)

in the eight months following transplantation

(Table 1). In the entire experimental patch, five

OTUs were present at the initial observation

and increased to 12 OTUs by the end of the

eight months of data collection (Table 2).

Monthly change in cryptofaunal com-

munity composition: Non-metric multidi-

mensional scaling (nMDS) (Fig. 7) and the

corresponding cluster analysis dendrogram

(Fig. 8) showed three distinct groupings of

average monthly cryptofauna community com-

positions (> 80 % similarity within groups)

corresponding to seasonal groupings “Wet”,

“Transitional”, and “Dry”. Analysis of simi-

larity (ANOSIM) was used to detect differ-

ences between these groups. The groups were

shown to be well separated (R statistic) but not

significantly different (p statistic) in composi-

tion (global R = 0.988, global P = 0.05; Dry

vs. Trans.: R = 1, P = 0.33; Dry vs. Wet: R

= 1, P = 0.07; Trans. vs. Wet: R = 0.96, P =

0.07). Results of similarity percentage analysis

(SIMPER) show that the three groups differ

more from each other than within each group

(Table 2).

Fig. 6. Number of individuals of cryptofauna living within the branches of each Pocillopora colony (ind colony-1) over the

eight months of data collection after transplantation. The blue line is a generalized linear model of the data based on Poisson

distribution. The gray area around the line represents the 95 % confidence interval.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Changes in the reef fish community fol-

lowing transplantation: Although there are

trends toward greater abundance and diversity

of reef fish in the experimental compared to

the control patch, these trends were not statisti-

cally significant: Abundance (Student’s t-test:

Df = 11.72, P > 0.05) (Fig. 9A) and Shannon

diversity (Student’s t-test: df = 13.03, P >

0.05) (Fig. 9B). Twenty-two and 17 species

were observed in the experimental and control

patches respectively. The average numbers

of individual fish observed each month were

44.9 and 33.1 in the experimental and control

patches, respectively (Table 3). The species

with the greatest number of observations was

Stegastes acapulcoensis. The ichthyofaunal

community did not differ significantly between

the control and experimental patches based on

the presence and abundance of fish species dur-

ing the monitoring time (ANOSIM R = 0.143,

P > 0.05) (Fig. 10).

DISCUSSION

Over the eight months following trans-

plantation to the restoration site, the crypto-

faunal community was dominated by obligate

decapod symbionts: Trapezia spp., Harpiliopsis

depressa, and Alpheus lottini. This is con-

sistent with the hypothesis that these species

only live within Pocillopora (Abele & Patton

1976; Castro, 1988; Glynn, 1980; Glynn, 1983;

TABLE 2

SIMPER table showing the similarity/dissimilarity within and between seasons and the percentage difference the most

significant OTUs contribute.

Season % Similarity/Dissimilarity OTU % Contribution

Dry 82.3 % Similar Scarus spp.37.9

Trapezia spp.22.2

Harpilliopsis depressa 17.6

Transition 85.3 % Similar Trapezia spp.45.8

Harpilliopsis depressa 36.2

Wet 84.3 % Similar Trapezia spp.35.4

Harpilliopsis depressa 25.1

Alpheus lottini 24.9

Dry & Transition 46.1 % Dissimilar Scarus spp.38.7

Trapezia spp.15.7

Harpilliopsis depressa 10.1

Palaemonella holmesi 4.7

Palemon ritteri 4.4

Dry & Wet 44.2 % Dissimilar Scarus spp.38.1

Trapezia spp.12.2

Alpheus lottini 10.4

Harpilliopsis depressa 7.4

Vermetidae 4.7

Transition & Wet 23.6 % Dissimilar Alpheus lottini 15.2

Paguridae 14.6

Vermetidae 11.8

Harpilliopsis depressa 11.6

Spondylus sp.8.7

Ascidea 7.6

Trapezia spp.7.1

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Fig. 7. Non-metric multidimensional scaling of the composition of cryptofauna within the transplanted Pocillopora colonies

in the experimental patch, Punta Bejuco, Golfo Dulce for each month. nMDS based on Bray-Curtis similarity matrices built

on square-root transformed monthly average abundances of cryptofauna OTUs and by the “season” as a factor.

Fig. 8. Average union dendrogram showing the similarity of the cryptofaunal community of the Pocillopora transplants

between months in the experimental patch, Punta Bejuco, Golfo Dulce. Months are arranged chronologically from left to

right and grouped by the factor season. Below the dendrogram is a heatplot showing the square-root transformed abundances

(ind colony -1) of cryptofauna each month. OTU symbols are assigned in Table 1.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Glynn, 2013; Glynn & Enochs, 2011; Stella

et al., 2011) and maintain a constant presence

independent of the season (Gotelli et al., 1985).

Likewise, the Pocillopora colonies require the

symbionts to survive and grow (Glynn, 1983;

Glynn, 2013; Stella et al., 2011). The abun-

dance of cryptofauna more than doubled over

the observational period, from an average of 10

individuals in each of the 30 transplanted cor-

als on the day after transplantation to 21 indi-

viduals eight months later. The diversity of the

experimental patch also increased significantly,

with five OTUs in the first month and 12 OTUs

in the final month.

The cryptofaunal community observed at

the study site reflects the known ecology of

reef fauna reported in the literature. Decapod

crustaceans are the most abundant and diverse

cryptic symbionts (Glynn, 2013; Reaka-Kudla

et al. 1997; Stella et al. 2011). The brachyuran

crabs of the genus Trapezia and snapping

Fig. 9. A. Average abundance and B. average Shannon

diversity (H’= -Σpi * ln(pi)) of fish in experimental and

control patches throughout the experiment.

Fig. 10. Non-metric multidimensional scaling of the composition of the fish community within the experimental and control

patches at Punta Bejuco, Golfo Dulce each month based on Bray-Curtis similarity matrices built on square-root transformed

monthly averages of fish species abundances. The experimental and control patches are indicated with different symbols

and point colors.

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

shrimp of the genus Alpheus are common

decapod symbionts associated with the highly

branching coral Pocillopora. The decapods

defend their host coral from coralivorous inver-

tebrates like the sea star Acanthaster plancii

(Glynn, 1983; Glynn, 2013; Pratchett, 2001) or

the snail Drupella (McKeon & Moore, 2014;

Samsuri et al., 2018) by snapping at intrud-

ers. Symbiotic decapods reduce coral mortal-

ity due to sedimentation (Stewart et al., 2006;

Stier et al., 2012) and disease (Pollock et al.,

2013) by actively “kicking” and “shoveling”

unwanted particles from Pocillopora colonies,

thus reducing stress on the coral (Stewart et al.,

2006). The presence of Trapezia crabs induces

the Pocillopora host to produce nutrient-rich

mucus with fat globules to encourage the

mutualism between host coral and crab (Glynn,

1983; Stimson, 1990).

The change in the diversity of the fauna

living within Pocillopora colonies over time

appeared to represent different recruitment

periods of the ecological groups (Table 2). The

initial recruits were the obligate symbiont deca-

pods that were recruited to the colonies while

they grew in the coral nurseries located about

18 km from Punta Bejuco (personal observa-

tion) and remained present following transplan-

tation. The next recruits, first observed three

months post-transplantation (September 2019),

TABLE 3

Species observed and average monthly observations in the experimental and control patches following transplantation.

Species Ecological role Average observations per month

Experimental Control

Stegastes acapulcoensis Detritivore 10.6 14.0

Stegastes flavilatus Detritivore 1.5 0.1

Anisotremus taeniatus Invertebrate eater 0.0 0.1

Arothron hispidus Invertebrate eater 0.3 0.1

Bodianus diplotaenia Invertebrate eater 0.0 0.8

Canthigaster punctatissima Invertebrate eater 1.9 0.8

Gnathanodon speciosus Invertebrate eater 1.5 0.0

Haemulon steindachneri Invertebrate eater 1.8 0.0

Halichoeres dispilus Invertebrate eater 2.3 6.0

Halichoeres nicholsi Invertebrate eater 0.1 0.0

Johnrandallia nigrirostris Invertebrate eater 0.1 0.0

Pomacanthus zonipectus Invertebrate eater 0.1 0.1

Sphoeroides lobatus Invertebrate eater 0.8 0.8

Thalassoma lucasanum Invertebrate eater 2.9 1.8

Kyphosus elegans Macroalgae feeder 0.1 0.0

Scarus compressus Macroalgae feeder 0.3 0.8

Scarus ghobban Macroalgae feeder 6.6 3.0

Chaetodon humeralis Omnivore 0.1 0.0

Kyphosus ocyurus Omnivore 0.8 0.0

Cephalopholis panamensis Piscivore 1.9 0.3

Haemulon maculicauda Piscivore 3.4 2.9

Haemulon sexfasciatum Piscivore 0.1 0.0

Lutjanus argentiventris Piscivore 3.9 0.4

Lutjanus novemfasciatus Piscivore 0.0 0.5

Abudefduf troschelii Planktivore 4.0 0.9

Total 44.9 33.1

The gray shading highlights which species were observed in greater abundance in each patch.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

were blennies and other cryptic fish, followed

by encrusting animals. Others have observed

that as branching coral colonies grow, the tissue

on the bases of the branches begins to die and

sessile encrusting and boring animals can colo-

nize the exposed carbonate skeleton (Abele &

Patton, 1976; Enochs & Manzello, 2012a). The

final group of animals observed to be recruited

to the transplanted colonies were juveniles of

larger reef fish in January 2020.

The increase in abundance and diversity

of cryptofauna over time could be explained

by multiple processes. The first regards the

growth of the coral. As corals grow, more space

is available between their branches to harbor

symbionts, thus reducing competition for space

and allowing fauna abundance to increase

over time with the size of the coral colonies

(Abele & Patton, 1976). However, intense and

complex inter- and intraspecific aggressive

interactions in the common Pocillopora sym-

bionts Trapezia and Alpheus keep the diversity

of the obligate symbionts constant and prevent

other organisms from being recruited (Castro,

1996; Huber, 1987; Stier et al., 2012). This

could explain why for the experiment, obligate

symbionts in just three OTUs comprised 81 %

of the total number of individuals that occupied

the experimental coral transplants.

Other explanations could, as implied by

the seasonal differences in cryptofaunal com-

munity compositions, be the result of seasonal

changes in the environment. In the ETP, the

recruitment of associated fauna is greater in the

warmer months due to the increased metabolic

rate and reproduction of invertebrates (Rodrí-

guez-Troncoso et al., 2018). The environmental

factor that most distinguishes the seasons in

Golfo Dulce is precipitation (Cortés, 1990;

Quesada-Alpízar & Cortés, 2006), leading to

greater sedimentation in the gulf during the

rainy season. Sedimentation has physiological

consequences for the coral such as mucus pro-

duction and necrosis that could have effects on

the associated fauna (Fabricius, 2005).

Although not significantly different, the

results of the nMDS, cluster analysis, and

SIMPER (Fig. 10) suggest that the cryptic

communities were similar between months that

roughly correspond to commonly held ranges

of the three seasons in Costa Rica, as defined

by the amount of precipitation of that period of

the year (Table 1). Alvarado & Vargas-Castillo

(2012) found that the diversity of cryptofauna

in Pocillopora colonies in Bahia Culebra is

greater in the dry season than in the wet sea-

son. This trend was also observed in this study.

Although, due to the timeframe of the study

which only included one dry and one wet

season, it is unclear whether the upward trend

would continue in the next seasonal cycle.

Ecological succession of species through

facilitation could be another explanation for

the increase in diversity and the sequential

appearance of different groupings of fauna fol-

lowing the transplantation of the Pocillopora

colonies. Although this study examines suc-

cession only insofar as to describe the order

of appearance of different species, the mecha-

nisms behind these patterns can be speculated.

The presence of cryptofauna, for example, may

attract larger species looking to feed on small

invertebrates living within the coral whom

themselves bring symbionts and nutrients to the

growing ecosystem.

As expected, greater diversity and abun-

dance of fish were observed in the experimen-

tal patch containing colonies rather than the

control patch without colonies although the dif-

ferences were not statistically significant. Fish

are attracted to structural complexity because it

provides numerous microhabitats that coincide

with a greater diversity of prey animals and

shelter whether it is a live reef (Bell & Galzin,

1984) or an artificial reef (Becker et al., 2017;

Russell, 1975; Santos et al., 2011). Herbivo-

rous fish control the population of leafy and

fleshy algae that can impede the settlement

and growth of corals (Burkepile & Hay, 2010;

Hixon & Bronstoff, 1996; Humphries et al.,

2014). There may be species-specific effects of

different herbivores on different types of algae,

meaning that fish diversity is important for the

health of reefs (Burkepile & Hay, 2010).

The cryptofaunal community in this study

behaved differently in some respects when

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

compared to descriptions in the literature. For

example, intraspecific competition normally

limits species in the genera Alpheus and Tra-

pezia to two individuals of the same species

per colony, a male and female reproductive

pair (Castro, 1996; Huber, 1987; Stier et al.,

2012). In this study, we observed an average

of 5.8 Trapezia individuals per colony, and 2.5

Alpheus individuals per colony. This could be

explained by the limited population of Pocil-

lopora in Golfo Dulce resulting in fewer places

for competing for decapod symbionts to move

(Castro, 1978).

The data collected for this project was used

to add to our understanding of the interrelation-

ships between associated fauna and corals, the

patterns of biodiversity, and ecological suc-

cession in Pocillopora transplants in the res-

toration project in Golfo Dulce, South Pacific,

Costa Rica. The results may be useful for help-

ing to plan future restoration projects and to

guide expectations regarding the magnitude of

the number and variety of cryptic organisms in

the immediate aftermath of coral transplanta-

tion and the expected timing of the recruitment

of associated fauna. Multiyear studies that

include extensive environmental monitoring

are required to tease out the relative contribu-

tion of the environment, interspecies interac-

tions, and the other multiple contributions to

the complex reef colony. This type of under-

standing of coral reef ecosystems is one of the

most critical ways to combat the ecological

crisis of coral decline (Bellwood et al., 2004).

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

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

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We acknowledge the Center for Research in

Marine Science and Limnology (CIMAR) and

the University of Costa Rica for their resources

and support. Additionally, we acknowledge the

field support, data collection, and advice from

Tatiana Villalobos, José Andrés Marín Moraga,

Celeste Sánchez, Adriana Arce, Beatriz Nara-

njo, Tatiana 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. Permission to conduct research

at the field site was approved by the Sistema

Nacional de Áreas de Conservación (Approval

Nº SINAC-ACOSA-DT-PI-R-011-19).

REFERENCES

Abele, L. G., & Patton, W. K. (1976). The size of coral

heads and the community biology of associated deca-

pod crustaceans. Journal of Biogeography, 3, 35–47.

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

García, C., & Guzmán-Mora, A. G. (2014). Ecosiste-

mas coralinos del Área de Conservación Osa, Costa

Rica: Estructura y necesidades de conservación.

Revista de Biología Tropical, 63 (Suppl. 1), 219–259.

Alvarado, J. J., & Vargas-Castillo, R. (2012). Invertebrados

asociados al coral constructor de arrecifes Pocillo-

pora damicornis en Playa Blanca, Bahía Culebra,

Costa Rica. Revista de Biología Tropical, 60 (Suppl.

2), 77–92.

Alzate, A., Zapata, F. A., & Giraldo, A. (2014). A com-

parison of visual and collection-based methods for

assessing community structure of coral reef fishes

in the Tropical Eastern Pacific. Revista de Biología

Tropical, 62, 359–369.

Becker, A., Taylor, M. D. & Lowry, M. B. (2017). Monito-

ring of reef associated and pelagic fish communities

on Australia’s first purpose built offshore artificial

reef. ICES Journal of Marine Science, 74, 277–285.

Bell, J. & Galzin, R. (1984). Influence of live coral cover

on coral-reef fish communities. Marine Ecology Pro-

gress Series, 15, 265–274.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

Bellwood, D. R., Hughes, T. P., Folke, C. & Nyström, M.

(2004). Confronting the coral reef crisis. Nature, 429,

827–833.

Boulay, J. N., Hellberg, M. E., Cortés, J., & Baums, I. B.

(2014). Unrecognized coral species diversity masks

differences in functional ecology. Proceedings of

the Royal Society of London. Series B: Biological

Sciences 281, 20131580. https://doi.org/10.1098/

rspb.2013.1580

Breitburg, D. L. (1985). Development of a subtidal epi-

benthic community: Factors affecting species compo-

sition and the mechanisms of succession. Oecologia,

65, 173–184.

Burkepile, D. E., & Hay, M. E. (2010). Impact of herbivore

identity on algal succession and coral growth on a

Caribbean reef. PLoS ONE, 5, e8963

Caldwell, Z. R., Zgliczynski, B. J., Williams, G. J., & San-

din, S. A. (2016). Reef fish survey techniques: Asses-

sing the potential for standardizing methodologies.

PloS ONE, 11(4), e0153066. https://doi.org/10.1371/

journal.pone.0153066

Castro, P. (1978). Movements between coral colonies

in Trapezia ferruginea (Crustacea: Brachyura), an

obligate symbiont of scleractinian corals. Marine

Biology, 46, 237–245

Castro, P. (1988). Animal symbioses in coral-reef commu-

nities - a review. Symbiosis, 5, 161–184.

Castro, P. (1996). Eastern Pacific species of Trapezia

(Crustacea, Brachyura: Trapeziidae), sibling species

symbiotic with reef corals. Bulletin of Marine Scien-

ces, 58, 531–554.

Clark, S., & Edwards, A. J. (1994). Use of artificial reef

structures to rehabilitate reef flats degraded by coral

mining in the Maldives. Bulletin of Marine Sciences,

55, 724–744.

Clarke, K. R., & Gorley, R. N. (2015). PRIMER v7: User

manual. PRIMER-E Ltd. http://updates.primer-e.

com/primer7/manuals/User_manual_v7a.pdf

Cortés, J. (1990). The coral reefs of Golfo Dulce, Costa

Rica: Distribution and community structure. Atoll

Research Bulletin, 344, 1–37.

Cortés, J., Enochs, I. C., Sibaja-Cordero, J., Hernán-

dez, L., Alvarado, J. J., Breedy, O., Cruz-Barraza,

J. A., Esquivel-Garrote, O., Fernández-García, C.,

Hermosillo, A., Kaiser, K. L., Medina-Rosas, P.,

Morales-Ramírez, Á., Pacheco, C., Pérez-Matus,

A., Reyes-Bonilla, H., Riosmena-Rodríguez, R.,

Sánchez-Noguera, C., Wieters, E., & Zapata, F.

A. (2017). Marine biodiversity of Eastern Tropical

Pacific coral reefs. In P. W. Glynn, D. Manzello, & I.

C. Enochs (Eds.), Coral reefs of the Eastern Pacific:

Persistence and loss in a dynamic environment. Coral

reefs of the World 8 (pp. 203–250). Springer. https://

doi.org/10.1007/978-94-017-7499-4_7

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. 361–385). Elsevier Science B.V. https://doi.

org/10.1016/b978-044451388-5/50017-5

Darling, E. S., Alvarez-Filip, L., Oliver, T. A., McCla-

nahan, T. R., & Côté, I. M. (2012). Evaluating

life-history strategies of reef corals from species

traits. Ecology Letters, 15(12), 1378–1386. https://

doi.org/10.1111/j.1461-0248.2012.01861.x.

Enochs, I. C. (2012). Motile cryptofauna associated with

live and dead coral substrates: implications for coral

mortality and framework erosion. Marine Biology,

159, 709–722.

Enochs, I. C., & Hockensmith, G. (2008). Effects of coral

mortality on the community composition of cryptic

metazoans associated with Pocillopora damicornis.

Proceedings of the 11th International Coral Reef

Symposium, 26, 1368–1372.

Enochs, I. C., & Manzello, D. P. (2012a). Responses of

cryptofaunal species richness and trophic potential to

coral reef habitat degradation. Diversity, 4, 94–104.

Enochs, I. C., & Manzello, D. P. (2012b). Species richness

of motile cryptofauna across a gradient of reef fra-

mework erosion. Coral Reefs, 31, 653–661.

Enochs, I. C., Toth, L. T., Brandtneris, V. W., Afflerbach,

J. C., & Manzello, D. P. (2011). Environmental deter-

minants of motile cryptofauna on an eastern Pacific

coral reef. Marine Ecological Progress Series, 438,

105–118 https://doi.org/10.3354/meps09259

Fabricius, K. E. (2005). Effects of terrestrial runoff on

the ecology of corals and coral reefs: review and

synthesis. Marine Pollution Bulletin, 50(2), 125–146.

https://doi.org/10.1016/j.marpolbul.2004.11.028

Fonseca, A. C., & Cortés, J. (1998). Coral borers of the

Eastern Pacific: Aspidosiphon (A.) elegans (Sipun-

cula: Aspidosiphonidae) and Pomatogebia rugo-

sa (Crustacea: Upogebiidae). Pacific Science, 52,

170–175.

Froehlich, C. Y. M., Klanten, O. S., Hing, M. L., Dowton,

M. & Wong, M. Y. L. (2021). Uneven declines bet-

ween corals and cryptobenthic fish symbionts from

multiple disturbances. Scientific Reports, 11, 16420.

https://doi.org/10.1038/s41598-021-95778-x

Glynn, P. W. (1980). Increased survivorship in corals har-

boring crustacean symbionts. Marine Biology Letters,

4, 105–111.

Glynn, P. W. (1983). Crustacean symbionts and the defense

of corals: Coevolution on the reef? In M. H. Nitecki

18 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

(Ed.), Coevolution (pp. 111–178). University of Chi-

cago Press,

Glynn, P. W. (2013). Fine-scale interspecific interactions

on coral reefs: functional roles of small and cryptic

metazoans. Smithsonian Contributions to the Marine

Sciences, 39, 229–248

Glynn, P. W., Alvarado, J. J., Banks, S., Cortés, J., Fein-

gold, J. S., Jiménez, C., Maragos, J. E., Martínez, P.,

Maté, J. L., Moanga, D. A., Navarrete, S., Reyes-

Bonilla, H., Riegl, B., Rivera, F., Vargas-Ángel, B.,

Wieters, E. A. & Zapata, F. A. (2017). Eastern Pacific

coral reef provinces, coral community structure, and

composition: An overview. In P. W. Glynn, D. Manze-

llo, & I. C. Enochs (Eds.), Coral reefs of the Eastern

Pacific: Persistence and loss in a dynamic environ-

ment. Coral reefs of the World 8 (pp. 107–176). Sprin-

ger. https://doi.org/10.1007/978-94-017-7499-4_5e

Glynn, P. W., & Enochs, I. C. (2011). Invertebrates and

their roles in coral reef ecosystems. In Z. Dubinsky,

& N. Stambler (Eds.), Coral reefs: An ecosystem

in transition (pp. 273–326). Springer. https://doi.

org/10.1007/978-94 -007-0114-4_18

Gotelli, N. J. & Abele, L. G. (1983). Community patterns

of coral-associated decapods. Marine Ecology Pro-

gress Series, 13, 131–139.

Gotelli, N. J., Gilchrist, S. L. & Abele, L. G. (1985). Popu-

lation biology of Trapezia spp. and other coral-asso-

ciated decapods. Marine Ecology Progress Series,

21, 89–98.

Hebbeln, D., & Cortés, J. (2001). Sedimentation in a tro-

pical fjord: Golfo Dulce, Costa Rica. Geo-Marine

Letters, 20, 142–148.

Hernández, L., Balart, E. F., & Reyes-Bonilla, H. (2009).

Checklist of reef decapod crustaceans (Crustacea:

Decapoda) in the southern Gulf of California, Méxi-

co. Zootaxa, 2119, 39–50.

Hernández, L., Ortiz, G. R. & Reyes-Bonilla, H. (2013).

Coral-associated decapods (Crustacea) from the

Mexican Tropical Pacific coast. Zootaxa, 3609(5),

451–464.

Hixon, M. A. (1997). Effects of reef fishes on corals and

algae. In C. Birkeland (Ed.), Life and death of coral

reefs (pp. 230–248). Chapman & Hall.

Hixon, M. A., & Brostoff, W. N. (1996). Succession and

herbivory: effects of differential fish grazing on

Hawaiian coral-reef algae. Ecological Monograph,

66, 67–90.

Horoszowski-Fridman, Y. B, Brêthes, J., Rahmani, N.,

Rinkevich, B. (2015). Marine silviculture: Incorpo-

rating ecosystem engineering properties into reef res-

toration acts. Ecological Engineering, 82, 201–213.

Horoszowski-Fridman, Y. B., Rinkevich, B. (2017).

Restoration of the animal forests: Harnessing sil-

viculture biodiversity concepts for coral trans-

plantation. In S. Rossi et al. (Eds.), Marine

Animal Forests (pp. 1–23). Springer. https://doi.

org/10.1007/978-3-319-21012-4_36

Huber, M. E. (1987). Aggressive behavior of Trapezia

intermedia Miers and T. digitalis Latreille (Brachyu-

ra: Xanthidae). Journal of Crustacean Biology, 7,

238–248.

Hughes, T. P., Barnes, M. L., Bellwood, D. R., Cinner, J.

E., Cumming, G. S., Jackson, J. B. C., Kleypas, J.

A, van de Leemput, I. A., Lough, J. M, Morrison,

T. H., Palumbi, S. R., van Nes, E. H., & Scheffer,

M. (2017). Coral reefs in the Anthropocene. Nature,

546, 82–90.

Humphries, A. T., McClanahan, T. R., & McQuaid, C. D.

(2014). Differential impacts of coral reef herbivores

on algal succession in Kenya. Marine Ecology Pro-

gress Series, 504, 119–132.

Kleypas, J. A., Villalobos-Cubero, T., Marin-Moraga, J.

A., Cortés, J., Alvarado, J. J. (2021). Reef restoration

in the eastern tropical Pacific, a case study in Golfo

Dulce, Costa Rica. In D. Vaughan (Ed.), Active Coral

Reef Restoration: Techniques for a Changing Planet

(pp. 417-430). J. Ross Publishing.

Kuffner, I., Walters, L., Becerro, M., Paul, V., Ritson-

Williams, R., & Beach, K. (2006). Inhibition of coral

recruitment by macroalgae and cyanobacteria. Mari-

ne Ecology Progress Series, 323, 107–117.

Ladd, M. C., Burkepile, D. E., & Shantz, A. A. (2019).

Near-term impacts of coral restoration on target spe-

cies, coral reef community structure, and ecological

processes. Restoration Ecology, 27(5), 1166–1176.

McKeon, C. S., & Moore, J. M. (2014). Species and size

diversity in protective services offered by coral

guard-crabs. PeerJ, 2, e574. https://doi.org/10.7717/

peerj.574.

Moeller, H. V., Nisbet, R. M., & Stier, A. C. (2023).

Cascading benefits of mutualists’ predators on

foundation species: a model inspired by coral reef

ecosystems. Ecosphere, 14(1), e4382. https://doi.

org/10.1002/ecs2.4382

Pollock, F. J., Katz, S. M., Bourne, D. G., & Willis, B. L.

(2013). Cymo melanodactylus crabs slow progression

of white syndrome lesions on corals. Coral Reefs,

32, 43–48.

Pratchett, M. S. (2001). Influence of coral symbionts

on feeding preferences of crown-of-thorns starfish

Acanthaster planci in the western Pacific. Marine

Ecology Progress Series, 214, 111–119.

Quesada-Alpízar, M. A., & Cortés, J. (2006). Los ecosis-

temas marinos del Pacífico sur de Costa Rica: estado

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54882, abril 2023 (Publicado Abr. 30, 2023)

del conocimiento y perspectivas del manejo. Revista

de Biología Tropical, 54 (Suppl. 1), 101–145.

Reaka-Kudla, M. L. (1997). The global biodiversity of

coral reefs: a comparison with rain forest. In M. L.

Reaka-Kudla, D. E. Wilson, & E. O. Wilson (Eds.)

Biodiversity II (pp. 83–108). Joseph Henry Press.

Rinkevich, B. (2005). Conservation of coral reefs through

active restoration Measures: Recent approaches and

last decade progress. Environmental Science & Tech-

nology, 39, 4333–4342.

Rodríguez-Troncoso, A., Rodríguez-Zaragoza, F.,

Mayfield, A., & Cupul-Magaña, A. (2018). Temporal

variation in invertebrate recruitment on an Eastern

Pacific coral reef. Journal of Sea Research, 145,

8–15.

Rouzé, H., Lecellier, G., Mills, S. C., Planes, S., Berteaux-

Lecellier, V., & Stewart, H. (2014). Juvenile Trapezia

spp. crabs can increase juvenile host coral survival by

protection from predation. Marine Ecology Progress

Series, 515, 151–159.

Russell, B. C. (1975). The development and dynamics of

a small artificial reef community. Helgoländer Wis-

senschaftliche Meeresuntersuchungen, 27, 298–312.

Salas-Moya, C., Vargas-Castillo, R., Alvarado-Barrientos,

J. J., Azofeifa-Solano, J. C., & Cortés, J. (2021).

Decapod crustaceans associated with macroin-

vertebrates in Pacific Costa Rica. Marine Biodi-

versity Records, 14(1), 6. https://doi.org/10.1186/

s41200-020-00199-w

Samsuri, A. N., Kikuzawa, Y. P., Taira, D., Sam, S. Q., Sim,

W. T., Lionel Ng, C. S., Afiq-Rosli, L., Delon Wee,

T. W., Ng, N. K., Toh, T. C., & Chou, L. M. (2018).

The effectiveness of Trapezia cymodoce in defending

its host coral Pocillopora acuta against corallivorous

Drupella. Marine Biology, 165(4), 70. https://doi.

org/10.1007/s00227-018-3330-2.

Santos, L. N., García-Berthou, E., Agostinho, A.A., &

Latini, J. D. (2011). Fish colonization of artificial

reefs in a large Neotropical reservoir: Material type

and successional changes. Ecological Applications,

21, 251–262.

Society for Ecological Restoration International Science

& Policy Working Group. (2004). The SER Interna-

tional Primer on Ecological Restoration. Society for

Ecological Restoration International.

Sin, T. M. (1999). Distribution and host specialization in

Tetralia crabs (Crustacea: Brachyura) symbiotic with

corals in the Great Barrier Reef, Australia. Bulletin of

Marine Science, 65, 839–850.

Stella, J. S., Jones, G. P., & Pratchett, M. S. (2010). Varia-

tion in the structure of epifaunal invertebrate assem-

blages among coral hosts. Coral Reefs, 29, 957–973.

Stella, J. S., Pratchett, M., Hutchings, P., & Jones, G.

(2011). Coral-associated invertebrates: diversity,

importance, and vulnerability to disturbance. Ocea-

nography and Marine Biology, 49, 43–104.

Stewart, H. L., Holbrook, S. J., Schmitt, R. J., & Brooks, A.

J. (2006). Symbiotic crabs maintain coral health by

clearing sediments. Coral Reefs, 25, 609–615.

Stier, A. C., Gil, M. A., Mckeon, C. S., Lemer, S., Leray,

M., Mills, S. C., & Osenberg. C. W. (2012). House-

keeping mutualisms: Do more symbionts facilitate

host performance? PLoS ONE, 7(4), e32079. https://

doi.org/10.1371/journal.pone.0032079

Stimson, J. (1990). Stimulation of fat-body production in

the polyps of the coral Pocillopora damicornis by the

presence of mutualistic crabs of the genus Trapezia.

Marine Biology, 106, 211–218.

Toh, T. C., Ng, C. S. L., Peh, J. W. K., Toh, K. B., &

Chou, L. M. (2014). Augmenting the post-trans-

plantation growth and survivorship of juvenile scle-

ractinian corals via nutritional enhancement. PLoS

ONE, 9(6), e98529. https://doi.org/10.1371/journal.

pone.0098529

Tsuchiya, M. (1999). Effect of mass coral bleaching on the

community structure of small animals associated with

the hermatypic coral Pocillopora damicornis. Journal

of the Japanese Coral Reef Society, 1999, 65–72.

Villalobos, T. (2019). Integrated management and coral

restoration in Golfo Dulce reefs, South Pacific, Costa

Rica. [Unpublished master’s thesis]. University of

Costa Rica.

Walker, L. R., Walker, J., & Hobbs, R. J. (2007). Forging

a new alliance between succession and restoration,

In L. R. Walker, J. Walker, & J. R. Hobbs (Eds.),

Linking restoration and ecological succession (pp.

1–18). Springer.

Wolff, M., Hartmann, H. J., & Koch, V. (1996). A pilot tro-

phic model for Golfo Dulce, a fjord-like embayment,

Costa Rica. Revista de Biología Tropical, 44(Suppl.

3), 215–231.

Young, T. P., Chase, J. M., & Huddleston, R. T. (2001). Com-

munity Succession and Assembly. Ecological Resto-

ration, 19(1), 5–18. https://doi.org/10.3368/er.19.1.5.