Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

Demographic and population response of the threatened coral

Acropora cervicornis (Scleractinia, Acroporidae) to fireworm corallivory

Paola Santiago-Padua1; https://orcid.org/0000-0002-1942-7480

Jeremy Velázquez-Alvarado1,2; https://orcid.org/0000-0003-0778-7339

Arelys Del Mar López-Pérez1; https://orcid.org/0000-0002-1942-7480

Julimar Nevárez-Mélendez1; https://orcid.org/0000-0002-1221-3383

Lemuel E. Díaz-Druet1; https://orcid.org/0000-0002-3002-6530

Samuel E. Suleimán-Ramos1; https://orcid.org/0000-0002-3953-964X

Alex E. Mercado-Molina1,2 *; https://orcid.org/0000-0002-1162-5474

1. Sociedad Ambiente Marino, Calle 3 #1130, Urbanización Villa Nevárez, San Juan, Puerto Rico, 00927;

paolasantiago@sampr.org, jeremyvelazquez@sampr.org, arelys.lopez2@upr.edu, julimarnevarez@sampr.org,

lemueldiaz@sampr.org, samuelsuleiman@sampr.org, alexmercado@sampr.org (*Correspondence)

2. Universidad Ana G. Méndez-Recinto de Gurabo, PO Box 3030, Gurabo, Puerto Rico, 00778.

Received 26-IX-2022. Corrected 27-I-2023. Accepted 17-II-2023.

ABSTRACT

Introduction: The fireworm Hermodice carunculata is a widespread polychaete that can prey upon many coral

species. However, few studies have examined the effect of fireworm predation on coral demographics during

non-outbreak periods.

Objective: To determine whether predation by H. carunculata compromised the growth, survival, and popula-

tion performance of the threatened coral Acropora cervicornis.

Methods: Nursery-reared coral fragments (n = 99) were fixed to the bottom of Punta Melones reef in the Island

Municipality of Culebra, Puerto Rico. Predation activity and its demographic consequences on coral outplants

were assessed from December 2020 to August 2022. Susceptibility to predation was compared between colo-

nies collected directly from the reef and those originating from outside sources (e.g., coral nurseries). With the

demographic data, simple size-based population matrix models were developed to 1) examine whether fireworm

predation led to a significant decline in population growth rate (λ), 2) determine the demographic transition(s)

that contribute the most to λ, and 3) determining the demographic transition(s) that accounted for differences

in λ when comparing scenarios that considered either only predated colonies or both predated and non-predated

outplants.

Results: Predation increased over time, being more frequently observed in the area with the highest topographic

relief and on colonies foreign to the study site. Outplants that were partially consumed grew significantly slower

than non-predated colonies; however, predation did not threaten their survival. The likelihood of being attacked

by the fireworm increased with branching complexity. The estimated λ for a scenario considering only predated

colonies was 0.99, whereas, for a scenario where both predated and non-predated colonies were considered, λ

was 0.91. Population growth, under the two scenarios, was mainly influenced by the probability of a large colony

surviving and remaining at the largest size.

Conclusions: Although predation can negatively impact coral growth, the relatively high survival rate of pre-

dated colonies compensates for the adverse effect. Since survival is the demographic transition that contributes

most to population growth, it could be concluded that under a non-outbreak scenario, fireworm predation may

not be the primary cause of A. cervicornis population decline.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54912

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

The fireworm Hermodice carunculata

(Pallas, 1766) is a widespread polychaete

found in tropical and temperate marine eco-

systems (Righi et al., 2020; Wolf et al., 2014).

It can prey on many benthic species, including

corals, octocorals, and hydrozoans (Vreeland &

Lasker, 1989; Witman, 1988). In the Caribbean,

H. carunculata can prey heavily on the reef-

forming coral Acropora cervicornis (Lamarck,

1816) (Fig. 1, Knowlton et al., 1990; Miller

et al., 2014). The fireworm does not neces-

sarily consume the entire colony; however, it

can adversely affect coral demography (Miller

et al., 2014). For instance, the survival and

growth of A. cervicornis can be compromised

if tissue consumption exceeds 20 % of the total

colony size (see Mercado-Molina et al., 2018).

Moreover, predation can result in population

decline if large colonies retrogress into smaller

sizes (Mercado-Molina, Ruiz-Diaz, Pérez, et

al., 2015). In fact, in Jamaica, H. carunculata

was linked to the extinction of an A. cervicornis

subpopulation (Knowlton et al., 1990).

Although H. carunculata corallivory may

negatively affect A. cervicornis, its feeding

dynamic is poorly understood. Furthermore,

Key words: coral demographics; coral outplants; elasticity analysis; Hermodice carunculata; population matrix

model; predation; restored population.

RESUMEN

Respuesta demográfica y poblacional del coral amenazado Acropora cervicornis

(Scleractinia, Acroporidae) a la coralivoria por gusano de fuego

Introducción: El gusano de fuego Hermodice carunculata es un poliqueto común que puede depredar muchas

especies de coral. Sin embargo, pocos estudios han examinado el efecto de la depredación del gusano de fuego

en la demografía de los corales durante periodos sin brotes poblacionales.

Objetivo: Este estudio tuvo como objetivo determinar si la depredación por H. carunculata compromete el cre-

cimiento, la supervivencia y el desempeño poblacional del coral amenazado Acropora cervicornis.

Métodos: Fragmentos de coral criados en vivero (n = 99) se fijaron al fondo del arrecife Punta Melones en la

Isla Municipio de Culebra, Puerto Rico. La actividad de depredación y sus consecuencias demográficas en los

trasplantes de coral se evaluaron desde diciembre de 2020 hasta agosto de 2022. Se comparó la susceptibilidad

a la depredación entre las colonias recolectadas directamente del arrecife y las que se originaron en fuentes

externas (p. ej., viveros de coral). Con los datos demográficos, se desarrollaron modelos matriciales simples de

población basados en el tamaño para 1) examinar si la depredación del gusano de fuego causa una disminución

significativa en la tasa de crecimiento de la población (λ), 2) determinar las transiciones demográficas que más

contribuyen a λ, y 3) determinar la(s) transición(es) demográfica(s) que explican las diferencias en λ al comparar

escenarios que consideraron solo colonias depredadas o la combinación de colonias depredadas y no depredadas.

Resultados: La depredación aumentó con el tiempo, observándose con mayor frecuencia en la zona de mayor

relieve topográfico y en colonias ajenas al sitio de estudio. Los trasplantes consumidos parcialmente crecieron

significativamente más lento que las colonias no depredadas; sin embargo, la depredación no amenazó su super-

vivencia. La probabilidad de ser atacado por el gusano de fuego aumentó con la complejidad morfológica de la

colonia. El λ estimado para un escenario que consideraba solo las colonias depredadas fue de 0.99, mientras que,

para un escenario en el que se consideraron tanto las colonias depredadas como las no depredadas, λ fue de 0.91.

El crecimiento de la población, en ambos escenarios, estuvo influenciado principalmente por la probabilidad de

que una colonia grande sobreviviera y permaneciera en el tamaño más grande.

Conclusiones: Aunque la depredación puede tener un impacto negativo en el crecimiento de los corales, una

tasa de supervivencia relativamente alta de las colonias depredadas compensa los efectos adversos. Dado que la

supervivencia es la transición demográfica que más contribuye al crecimiento de la población, se podría concluir

que, en un escenario sin brotes, la depredación por gusanos de fuego no debe ser la causa principal de la dismi-

nución de la población de A. cervicornis.

Palabras claves: análisis de elasticidad; demografía de coral; depredación; Hermodice carunculata; modelo de

matriz de población; población restaurada; trasplantes de coral.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

very few studies have attempted to understand

the effects of predation at the population level

(Goergen et al., 2019; Wolf et al., 2014; Miller

et al., 2014). The coral A. cervicornis is a

threatened species that plays an essential role

in maintaining the ecological functions and

services of coral reefs. It contributes to reef

accretion (Gilmore & Hall 1976; Tunnicliffe,

1981), promotes biodiversity (Agudo-Adriani

et al., 2016), and shapes biological interactions

(Weil et al., 2020). Due to its ecological impor-

tance, many restoration programs have been

established across the region (Bayraktarov et

al., 2020; Hernández-Delgado et al., 2014).

However, the lack of information about the

predatory behavior of fireworms limits prac-

titioners’ ability to develop restoration plans

that can counteract the aggressive behavior of

the fireworms. By understanding the predation

dynamics of H. carunculata, coral outplanting

can, for instance, be timed and located based

on where and when the species is more active.

Such information can be used to predict future

trends of restored populations under different

predation scenarios.

This study aims to describe the predation

dynamics of H. carunculata on a restored pop-

ulation of the threatened coral A. cervicornis

in Puerto Rico. The following questions were

answered: 1) Do predation rates vary in space

and time? 2) Are introduced colonies more

susceptible to predation than local colonies?

3) Is there a relationship between colony com-

plexity and predation susceptibility? 4) Does

predation by H. carunculata put the viability

of the restored population at risk? The answer

to these questions will contribute to a better

understanding of the processes that can hinder

the success of coral reef restoration and help

improve recovery plans for A. cervicornis.

MATERIALS AND METHODS

Study site: The study was conducted in

the Island Municipality of Culebra, approxi-

mately 30 km east of the mainland of Puerto

Rico (Fig. 2). In 2014, the USA National

Oceanographic and Atmospheric Administra-

tion designed Culebra as part of the Northeast-

ern Reserves System Habitat Focus Area due

to its representative biodiversity of Caribbean

marine ecosystems and its socio-economic

value. The study was carried out specifically at

Punta Melones reef (PMEL), where Sociedad

Ambiente Marino (SAM) is mitigating the

effects of reef degradation by increasing the

density of A. cervicornis. PMEL, located on the

western coast of Culebra, has a maximum depth

of five meters and is dominated by macroalgae

assemblages (e.g., algae turfs and Ramicrusta

sp.). The macroalgal community also includes

Dictyota spp., but their abundance varies con-

siderably throughout the year (unpublished

Fig. 1. Left: The white tips of an A. cervicornis colony show signs of recent tissue consumption by Hermodice carunculata.

Right: Hermodice carunculata engulfing a colony outplant of the threatened coral Acropora cervicornis at Punta Melones

reef in Culebra, Puerto Rico.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

data). The sea fan Gorgonia ventalina (Linnae-

us, 1758) is the predominant octocoral species,

being particularly abundant in the shallower

zones of the reef (e.g., reef crest). Approxi-

mately 5 % of the reef is covered by corals,

mostly Porites astreoides (Lamarck, 1816) and

Porites porites (Pallas, 1766). Before the start

of the restoration program, A. cervicornis was

absent from the study site. Information about

the abundance and distribution of H. carun-

culata in PMEL is lacking. However, we have

observed the fireworms across the whole reef,

including reef flats, sandy areas, and areas of

high topographic relief.

Restored populations: At the beginning

of the study in December 2020, three 60 m2

(30 m x 2 m; Fig. 3) permanent belt transects,

separated by 5 m each, were established paral-

lel to the coast. In each transect, 150 fragments

of A. cervicornis (median colony size = 17.40

cm) were fixed to the reef substrate using

concrete nails and plastic cable ties. Coral

fragments were harvested from in-situ coral

nurseries operated by SAM. The physical struc-

ture of the reef framework differed between

the transects. Transect A, the southernmost,

was a reef flat dominated by small dead coral

boulders and flat consolidated substrate, being

the less complex (Rugosity Index = 1.17) of

Fig. 2. The study was conducted at Punta Melones reef, located in the Island Municipality of Culebra, Puerto Rico.

Fig. 3. Schematic representation of transects positioning

along the coastline of Punta Melones reef.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

the three transects established. Transect B was

laid across a moderately complex reef slope

(Rugosity Index = 1.19) with a consolidated

bottom. Transect C, the northernmost, was

characterized by pinnacles and ridges up to 3

m in height, visually dominated by holes and

crevices. In this sense, Transect C was the most

complex (Rugosity Index = 1.24) of the three

reef areas studied. Topographic relief was esti-

mated using the chain method to calculate its

rugosity index (Mercado-Molina, Montañez-

Acuña, et al., 2015; Nemeth & Appeldoorn,

2009). A 10 m long chain was superimposed

along the contour of the reef substrate, and

the rugosity index was calculated as the ratio

between the length of the chain and the dis-

tance it covered along the contour of the reef

substrate (Nemeth & Appeldoorn, 2009).

Prevalence and incidence of predation:

33 colonies were tagged within each of the

transects (total = 99) to monitor the preva-

lence and incidence of fireworm predation

events. Tagged colonies were visited seven

times between December 2020 and August

2022. Prevalence was defined as the percent-

age of colonies that showed signs of predation

during a given time, whereas incidence was the

number of new predation cases detected during

the same period. Log-linear analysis was per-

formed to determine whether the incidence and

prevalence of fireworms predation were inde-

pendent of time and location. Fate (F) was set

as the response variable (e.g., predated vs. non-

predated), whereas time (T) and location (L)

were considered the explanatory factors. Fol-

lowing Caswell (2001) and Fingleton (1984),

0.5 was added to each cell value within the

contingency tables to avoid estimation prob-

lems for values equal to 0. Log-linear analysis

was performed in R (R Core Team, 2017) using

the library MASS (Venables & Ripley, 2013).

Effect of predation on coral demogra-

phy: The growth and survival of the tagged

coral colonies were tracked seven times

between December 2022 and August 2022.

A coral colony was considered dead if no

apparent live tissue was evident. Following

Mercado-Molina, Ruiz-Diaz & Sabat (2015),

growth rates were estimated as the change in

daily linear extension (final length − initial

length / total number of days) and expressed

as cm/day. To estimate colony size, in-situ pho-

tographs (scale-by-side) of each colony were

taken from different perspectives to ensure that

all branches were captured. The initial and final

sizes of the colonies were then calculated by

adding up the linear lengths of the branches,

excluding partial mortality when appropri-

ate. Coral Point Count with Excel extensions

(CPCe; Kohler & Gill, 2006) software was

used for processing the photographs. Survivor-

ship patterns and coral growth were compared

between predated vs. non-predated colonies

using the Kaplan-Meier Survival analysis and

Mann-Whitney-U test, respectively. Survival

analysis was performed in R using the package

simsurv (Brilleman et al., 2021).

Demographic modeling: The restored

fragments (collected from in-situ coral nurser-

ies) were classified into two size classes, small

(overall size ≤ 25 cm) and large (overall size >

25 cm). A size-based matrix population model

was developed to estimate the growth rate of

the restored population under two scenarios: 1.

considering only predated colonies and 2. con-

sidering all colonies. The demographic model

followed Equation 1:

(Equation 1)

Where the number of small-sized colonies

[s] and large-sized colonies [l] at time t + 1 (one

year into the future) equals the current number

of colonies in each of the two size classes mul-

tiplied by a two-by-two matrix of the transition

probabilities among size classes. The diagonal

elements in the matrix represent the prob-

abilities of colonies surviving and remaining

in their current size class (stasis: Sss; Sll). The

Rsl element of the matrix represents the con-

tribution of large-sized colonies to the small-

size class by size regression due to fireworm

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

consumption of live tissue. Gls represents the

probability of a colony transitioning from

the smallest to the largest size class. The two

size classes were chosen to maintain a sample

greater than 25 colonies for each size category.

Two transition matrices were created, one

accounted for only coral colonies that suf-

fered H. carunculata predation, and the second

included both predated and non-predated colo-

nies. The dominant eigenvalue was calculated

for each matrix to obtain the finite popula-

tion rate of increase (λ). A life table response

experiment (LTRE) analysis was performed

to provide information on the magnitude of

variation in a particular life cycle transition that

contributed most to the observed difference in

λ between treatments (e.g., fireworm coral-

livory). Elasticity was also used as an analysis

to determine the transition rate that would

contribute the most to λ values. Demographic

analyses were performed in R (R Core Team,

2017) using the package popbio (Stubben &

Milligan, 2007).

Colony susceptibility: The susceptibility

of local and introduced populations to preda-

tion was compared. To accomplish this, we

conducted a second outplanting event between

January and February 2022 in which colony

fragments were collected from the original

restored population (e.g., >1-year-old, local

population) as well as nurseries outside the

study site (e.g., introduced population). Fol-

lowing the same methodology described above,

colonies were outplanted along the permanent

transects in the same numbers (e.g., 33 colonies

per transect). Coral fragments were revisited in

April 2022 and July 2022. The Chi-square test

was used to determine whether the number of

colonies predated was associated with their ori-

gin (local vs. introduced). Chi-square analysis

was performed using R (R Core Team, 2017).

RESULTS

Incidence and prevalence of colony pre-

dation: Results of the log-linear analysis indi-

cate that predation rates of H. carunculata

varied in space and time (Table 1). However,

no significant interaction was found between

the location (transect) and time (Table 1). Pre-

dation on coral outplants was first detected in

February 2021 (Fig. 4). After the first sight,

predatory attacks spiked considerably over

time. April 2022 was the month with the highest

percentage of new colonies predated. In August

2022, the incidence of predation decreased,

probably because fewer colonies were at risk

of being predated since most had already been

predated. Prevalence of predation reflected

the increasing incidence trends, suggesting

that affected colonies could not regenerate the

lost tissue (Fig. 5). By the end of the study,

approximately 84 % of the colonies showed

signs of predation. Corals outplanted in the

northernmost location (Transect C) were more

prone to predation than colonies outplanted in

the southern part (Transect A and Transect B).

In Transect C, the mean incidence rate per sur-

vey time was 42 % (range: 27-67 %), whereas,

at Transect A and Transect B, the rate of new

detections per survey time was approximately

TABLE 1

Results of the log-linear analysis comparing the effect of location and time on colony fate (e.g., predated vs. no predated) of

the restored Acropora cervicornis population at Punta Melones reef, Culebra, Puerto Rico.

Effect Models Delta G Delta df P

Location TL, F vs. TL, FL 7.35 2 0.025

Time TL, F vs. TL, FT 70.96 6 < 0.0001

Location, given time TL, LF vs. TL, FT, FL 86.51 6 < 0.0001

Time, given location TL, TF vs. TL, FT, FL 22.90 2 < 0.0001

Location x Time x Fate TL, FT, FL vs. TLF 14.31 12 0.281

T= time; L = location (transect); F = fate (predated or not predated); df = Degree of freedom.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

21 % (range: 0–42 %). Of the 33 tagged colo-

nies monitored in Transect C, only one was not

predated (97 % predation) compared to seven

and eight at Transect A (79 % predation) and

Transect B (76 % predation), respectively. In

general, predation within Transect C accounted

for at least 44 % (range: 44-100 %) of new

sights detected during survey times and ~ 40 %

of the total colonies predated. Predated colo-

nies also presented a moderate vulnerability for

further predation events, with an average of 34

% probability of experiencing further attacks.

Outplants along Transect C were more likely

to be re-predated than outplants in the other

Fig. 4. Spatiotemporal pattern of predation incidence by the fireworm Hermodice carunculata on Acropora cervicornis

outplants.

Fig. 5. Spatiotemporal pattern of predation prevalence by the fireworm Hermodice carunculata on Acropora cervicornis

outplants.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

two transects (Fig. 6). It was also found that

fireworm predation events were significantly

more prevalent in introduced colonies than

in those collected from the local site (Chisq

=8.58, P = 0.003, Fig. 7). The observed spatial

pattern of predation could be a consequence of

the spatial variation in abundance of the fire-

worms (Fig. 8).

Effect of fireworm corallivory on out-

plants demographic performance: Results

of the Mann-Whitney-U-test indicate that pre-

dation significantly affected coral growth (W

= -942, P < 0.0001). Before being attacked,

coral outplants grew at 0.54 cm/day (± 1.03

SD; median = 0.47), decreasing to -0.24 cm/

day (± 0.50 SD; median = -0.32) after being

partially consumed by the fireworm (Fig. 9).

Colonies outplanted in Transect A (W = 77, P

= 0.013) and B (W = 136, P < 0.0001) showed

the largest decrease in growth rates, declining

Fig. 6. Spatial comparison of the probability of a coral

outplant to be re-predated by the fireworm Hermodice

carunculta along the three transects established at Punta

Melones reef, Culebra, Puerto Rico.

Fig. 7. Comparison of predation rates between colonies

originating from Punta Melones (PMEL), referred as local,

and colonies collected from outside nurseries (Introduced).

Fig. 8. Spatial variation in the abundance of the fireworm Hermodice carunculta in Punta Melones reef, Culebra, Puerto Rico.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

17 % and 21 % faster than colonies in Transect

C (Fig. 9). Growth rates before and after the

predation event did not vary statistically among

colonies growing in Transect C (W = 60, P =

0.40). The log-rank test based on the Kaplan-

Meier survival curve (Fig. 10) indicates that

fireworm predation did not significantly affect

the survival of colonies (Chisq = 3.1, P = 0.08).

Survival between predated and non-predated

coral colonies differed only by 10 % towards

the end of the study.

Effect of initial size and the number

of branches on predation rates: Results of

the logistic regression analysis indicate that

the vulnerability of a colony to be predated

increases with the number of colony branch-

es (i.e., branching complexity, z = 3.997,

P < 0.0001) but not with colony size (z = -1.337,

P = 0.181, Fig. 11). However, McFadens’s R2

value of 0.03, a vif value higher than 5, and a

ROC value of 0.53 indicate the models were

Fig. 9. Effect of predation by the fireworm Hermodice carunculata on Acropora cervicornis growth.

Fig. 10. Kaplan-Meier comparing survival pattern between

predated and non-predated outplanted colonies of Acropora

cervicornis.

Fig. 11. Relationship between the probability of predation

and colony size (A) and colony branching (B).

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

not necessarily a good fit for the data; there-

fore, results should be interpreted carefully.

Population response to fireworm preda-

tion: The estimated population growth rate for

the scenario considering only predated colonies

was 0.99 compared to 0.91 when considering

both predated and no-predated colonies (Fig.

12). Under the two scenarios, the demographic

transition that contributes the most to the esti-

mated λ was stasis of large colonies (Fig. 13).

LTRE analyses indicate that the difference in

λ could be attributed to a reduction in the sta-

sis of large-sized colonies under the scenario

considering both predated and non-predated

outplants (Fig. 14).

DISCUSSION

The observed rate of predation by H.

carunculata on A. cervicornis outplants was

84 %, which is ~1.5 times greater than what

was reported in the Florida Keys (Miller et

al., 2014). Biotic and abiotic factors specific

to the localities, such as fireworm abundance

and substrate complexity, may account for the

contrasting results between our study and that

of Miller et al. (2014). However, there is also

the possibility that different methodological

approaches could explain the higher preda-

tion rate we observed. For instance, Miller

et al. (2014) assessed colony predation in

restored populations two years old, whereas

we followed predation on newly fixed coral

Fig. 12. Estimated population growth rates for two

scenarios of predatory activity considering both predated

and non-predated (ALL) and considering only predated

colonies. Values below 1 indicate that the population

growth rate is negative (i.e., declining).

Fig. 13. Contribution of demographic transitions to the estimated population growth under two scenarios of predatory

activities. Considering both predated and non-predated (ALL) and considering only predated colonies. S = stasis, G =

growth, R = retrogression; s = small, l = large.

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outplants. Coral outplanting can be stressful

either because of the pruning and handling or

because coral fragments are placed in a new

environment. Colonies not yet recovered from

the collection event or acclimated to their new

environment may be under higher stress than

healed colonies already experiencing prevail-

ing environmental conditions, making them

more prone to be attacked by H. carunculata.

Therefore, we could have quantified preda-

tion during a period when coral fragments

were more susceptible to being predated. It

could also be possible that after two years in

the reefs, coral outplants developed a degree

of resistance or deterrence toward fireworm

predation. Indeed, Miller et al. (2014) found

that predation rates by H. carunculata on A.

cervicornis in both wild and restored popula-

tions were similar.

Fireworms were less likely to consume

coral fragments originating from PMEL than

from off-site nurseries. This finding suggests

that exposure to a new environment rather

than pruning or handling makes corals more

vulnerable to predation. As a species that typi-

cally reproduces by branch fragmentation, A.

cervicornis may be more able to deal with frag-

mentation-related damage than with changes in

environmental conditions.

There was a significant decline in growth

rates once the colony was partially consumed

by the fireworm, providing further evidence

of predation’s demographic cost. Decreased

growth rates after being predated could result

from the coral diverting energy toward reduc-

ing mortality risk (i.e., Anthony et al., 2009).

Predated colonies developed a calcified bulge

(or neoplasia, Bak, 1983) at the interface

between the live tissue and the exposed skel-

eton. The bulge, considered a physical barrier

for repelling the spread of the algae coloniz-

ing dead portions of the colony, is energeti-

cally costly and may contribute to the observed

decrease in coral growth while increasing sur-

vival probability (Bak, 1983; Mercado-Molina

et al., 2018). Indeed, no significant difference

in survival was observed between predated

and non-predated outplants, as none of the

affected colonies were consumed entirely or

were infected by fireworm-borne diseases (see

Miller et al., 2014). The low mortality of pre-

dated coral outplants opposes previous reports,

Fig. 14. Results of life table experiment analysis showing the contribution of each life cycle transition to the population

growth rate of Acropora cervicornis outplants accounting for the effect of predation. G = growth; S = stasis; R =

retrogression; s = small, l = large.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

such as the extirpation of colonies in Jamaica

partly due to a fireworm outbreak (Knowlton

et al., 1990). However, our finding agrees with

that of Goergen et al. (2019), who observed

minimal mortality in A. cervicornis wild popu-

lations during a non-outbreak period. Thus, it

could be argued that H. carunculata may not

lead to considerable colony loss if its popula-

tion is relatively low.

As demonstrated in previous demographic

studies on A. cervicornis (Mercado-Molina,

Ruiz-Diaz, Pérez, et al., 2015; Mercado-Molina

et al., 2020), the stasis of large colonies was

the most important transition rate for popula-

tion growth in PMEL. Large colonies are better

able than smaller ones to withstand the nega-

tive demographic effects of partial mortality

(Hernández-Delgado et al., 2018; Mercado-

Molina, Ruiz-Diaz, Pérez, et al., 2015; Mer-

cado-Molina et al., 2018) explaining, in part,

the importance of large colonies for population

viability. For instance, when a small colony

of A. cervicornis loses more than 20 % of its

living tissue, its survival is ~ 33 % lower than

when a large colony loses the same amount of

tissue (Mercado-Molina et al., 2018). Thus,

the preference for H. carunculata predating

on large colonies (see below) may contribute

to the relatively low impact of predation at the

population level.

Surprisingly it was found that the esti-

mated λ for the demographic scenario consid-

ering only the colonies that were attacked by

the fireworms was higher than when predated

and non-predated colonies were combined.

LTRE analysis indicates that such a result

was due to the difference in the probability

of large colonies surviving and remaining in

the largest size class. Under the predated-only

scenario, the stasis of large colonies was ~ 97

%, compared to 88 % when considering all

colonies. This suggests that fireworm predation

does not necessarily force corals into a smaller

class size or lead to the death of the colony. It

also implies that another source of tissue loss

(or death) affects the demographic transitions

of large colonies not predated by the fire-

worm. We witnessed some colonies predated

by the corallivorous snail Coralliophila abbre-

viata; however, the population-level effect of

snail predation may be limited because very

few colonies were affected. It is known that

A. cervicornis could be very susceptible to

minor or moderate local variations in environ-

mental parameters (Mercado-Molina, Ruiz-

Diaz, Pérez, et al., 2015); thus, it is possible

that changes in environmental conditions not

perceptible to us (e.g., light incidence, tem-

perature) led to the mortality of colonies not

predated by H. carunculata.

Goergen et al. (2019) and Miller et al.

(2014) found that colony attacks by H. carun-

culata did not follow a consistent temporal

pattern. In contrast, we found that the incidence

and prevalence of predation showed an increas-

ing trend over time. The discrepancy between

studies could be associated with the capacity

of corals to heal after predation. In the case of

Miller et al. (2014), some colonies regained

the lost tissue, which we did not observe dur-

ing our study. A low capacity to regenerate the

tissue that has been lost is not uncommon in

A. cervicornis (Miller et al., 2014; Mercado-

Molina et al., 2018). However, it is unclear

why some colonies can heal while others do

not. Determining the effects of predation on the

immune system of the coral can provide valu-

able insights into how injured colonies recover

(Ruiz-Diaz et al., 2016); thus, comparative

studies between predated and non-predated

colonies are recommended.

The positive relationship between colony

complexity and the probability of being pre-

dated could also explain the temporal incre-

ment in predation incidence and prevalence.

In A. cervicornis, branch formation tends to

increase with colony size (Mercado-Molina et

al., 2016); consequently, as a colony grows, it

becomes more complex. Morphological com-

plex corals could provide a higher surface

area of nearby tissue for consumption while

allowing the fireworm to spend little energy

foraging. In fact, most of the predated colonies

had multiple branches consumed. Feeding on

large and more complex colonies could also

result from the fireworm preferring colonies in

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54912, abril 2023 (Publicado Abr. 30, 2023)

a compromised energetic state. For instance, as

A. cervicornis grows, it devotes more energy to

growth than maintenance and defense (Darling

et al., 2012; Mercado-Molina, Ruiz-Diaz &

Sabat, 2015; Mercado-Molina et al., 2016),

possibly limiting its ability to counteract fire-

worm aggression.

Although coral outplants across the three

transects (Transect A through Transect C)

showed a progressive increase in fireworm

predation over time, the area where corals were

located proved to be critical, as suggested by

Goergen et al. (2019) and Miller et al. (2014).

Predation rates were greater along Transect C,

probably because the fireworm was more abun-

dant along this transect. Transect C was the

most complex of the three reef areas studied.

For a cryptic species, such as H. carunculata,

a substrate characterized by many crevices and

holes can provide protection and may increase

abundance, as was the case in our study. Nev-

ertheless, Wolf et al. (2014) found the high-

est abundance of H. carunculata in areas of

low rugosity. Therefore, it is possible that the

spatial distribution of the fireworm across our

study site could be related to other factors not

necessarily associated with the structure of

the reef substrate (e.g., sediment composition,

Wolf et al., 2014).

In conclusion, this study confirms that H.

carunculata can predate heavily on A. cervi-

cornis outplants (Calle-Triviño et al., 2017;

Miller et al., 2014), negatively affecting coral

growth. Nevertheless, outplant survival was not

compromised. Such a demographic response

to predation assures a minimal effect at the

population level. Being large and complex is

a buffer against predation because even when

outplants are partially consumed, their sur-

vival tends to be high. Thus, outplanting large

and complex colonies could be a strategy to

improve the success of coral reef restoration

(Goergen & Gilliman, 2018; Mercado-Moli-

na, Ruiz-Diaz, & Sabat, 2015; Pérez-Pagán

& Mercado-Molina, 2018), especially when

introducing colonies from external sources.

Reduced growth rate, however, can be prejudi-

cial in the long term by, for example, delaying

the time a coral outplant can reach a refuge size

and its reproductive potential. H. caranculata

could also be a vector of coral diseases (Miller

& Williams, 2007; Miller et al., 2014; Sussman

et al., 2003). Thus, it is recommended to keep

fireworm populations as small as possible.

When designing a restoration program, atten-

tion to the area (e.g., small-scale topographic

relief) where corals will be outplanted must be

considered. However, it is not clear yet what

features of the reef’s substrate better explain

changes in the abundance of H. carunculata.

Studies in this direction are urgently needed.

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

This study was funded by the NOAA Fish-

eries Habitat Conservation Program. Award #

NA20NMF4630303; under the permit 0-VS-

PVS15-SJ-01188-1203-2021 granted by the

Puerto Rico Department of Natural and Envi-

ronmental Resources to Sociedad Ambiente

Marino (SAM). Thanks to the members of

SAM for their logistics and field support.

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