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Effects of macroalgae and sea urchin grazing pressure on zoantharians growth under laboratory conditions

May 2024
Marine Environmental Research 198(3):106534

May 2024
198(3):106534

DOI:10.1016/j.marenvres.2024.106534

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CC BY-NC 4.0

Authors:

María Elisa Lambre

Universidad de La Laguna

Cataixa López

University of Hawaiʻi at Mānoa

Sabrina Clemente

Universidad de La Laguna

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Content may be subject to copyright.

Marine Environmental Research 198 (2024) 106534

Available online 3 May 2024

nc/4.0/).

Effects of macroalgae and sea urchin grazing pressure on zoantharians

growth under laboratory conditions

María Elisa Lambre

, Cataixa L´

opez

, Bel´

en Acha-Araico , Sabrina Clemente

Departamento de Biología Animal, Edafología y Geología, Facultad de Ciencias, Universidad de La Laguna, San Crist´

obal de La Laguna, Spain

ARTICLE INFO

Keywords:

Palythoa caribaeorum

Zoanthus pulchellus

Diadema africanum

Paracentrotus lividus

Lobophora

Crustose coralline algae

Competitions

Benthic ecology

Coastal zone

ABSTRACT

In the context of ocean warming, thermophilic organisms such as zoantharians are expanding and altering

shallow benthic habitats. Here, a four-month laboratory experiment was performed to examine the inuence of

three types of macroalgae morphotypes common in the Canary Islands (turf algae, Lobophora spp., and crustose

coralline algae) on the growth of two zoantharian species, Palythoa caribaeorum and Zoanthus pulchellus. Addi-

tionally, the grazing effects of echinoids Diadema africanum and Paracentrotus lividus were assessed as facilitators

of substrate colonization by means of controlling macroalgae cover. Colony and algal coverages were measured

at the beginning, middle and end of the experiment, and increments were calculated. Results indicated a general

decrease in zoantharian colony sizes in contact with different algal types in the absence of sea urchins. However,

P. caribaeorum colonies showed signicant growth in the presence of D. africanum, highlighting the ecological

importance of sea urchins in zoantharian population proliferation and subsequent community modication. This

study represents the rst investigation into zoantharian-macroalgae interactions under controlled conditions.

1. Introduction

The ongoing increase in atmospheric CO

due to anthropic activities

has led to an elevation in sea surface temperatures (SST) at a rate close to

0.1 ◦C per decade, with projections foreseeing an increase of 0.6–2.0 ◦C

within the upper 100 m layer by the end of the 21st century (IPCC,

2013). Temperature is a natural barrier for species distribution that is

now becoming distorted, facilitating the latitudinal migration of ther-

mophilic species towards polar regions, and inducing a tropicalization

on a global scale (Hyndes et al., 2016; Osland et al., 2021; Raitsos et al.,

2010; Verg´

es et al., 2014, 2016). Simultaneously, native species with

tropical and subtropical afnities are increasing their populations in

response to rising temperatures, a phenomenon known as meridionali-

zation that can cause ecological effects at regional and local scales (Brito

et al., 2014; Coco et al., 2022; Sangil et al., 2012; Yapici, 2016). These

alterations bring numerous consequences that disrupt the equilibrium of

coastal marine ecosystems, triggering rapid shifts in the distribution

ranges of species and reshaping local communities (Cheung et al., 2009;

Fogarty et al., 2017).

In many temperate and subtropical regions, the consequences of the

ongoing tropicalization of the marine biota are already evident. Many

studies have focused on how native species are competing or sharing

ecological niches with newly arrived tropical competitors (Bennett et al.,

2021; Santana-Garcon et al., 2023; Smith et al., 2021), accelerating the

degradation of native habitats (Hughes et al., 2013). However, less

studied are those ecological alterations due to the proliferation of

thermophilic native species that are thriving under the current warming

conditions. For instance, new zoanthid-dominated areas are arising in

several parts of the world, both in tropical environments typically

dominated by scleractinian corals and in temperate or subtropical re-

gions dominated by macroalgae (Reimer et al., 2021). These shifts have

been attributed to the thermophilic nature and absence of a calcareous

skeleton in zoantharians, which makes them more resilient to uctua-

tions in temperature and pH (Reimer et al., 2008). Other anthropogenic

stressors beyond warming waters have been appointed to exacerbate the

impacts on marine communities (Barnosky et al., 2012; Harley et al.,

2006), and recent studies have reported a positive correlation between

anthropogenic disturbances and zoantharian phase shifts (Belford and

Phillip, 2012; Cruz et al., 2014, 2015, 2016; Rogers et al., 2014). Given

the current anthropogenic coastal degradation worldwide, along with

* Corresponding author.

E-mail address: malambre@ull.edu.es (M.E. Lambre).

Present address: Hawai’i Institute of Marine Biology, School of Ocean & Earth Sciences & Technology, University of Hawai’i at M¯

anoa, Moku o Lo’e, K¯

ane’ohe,

HI, United States.

Contents lists available at ScienceDirect

Marine Environmental Research

journal homepage: www.elsevier.com/locate/marenvrev

https://doi.org/10.1016/j.marenvres.2024.106534

Received 20 March 2024; Received in revised form 25 April 2024; Accepted 29 April 2024

Marine Environmental Research 198 (2024) 106534

the effects of ongoing climate change processes, zoanthid-dominated

habitats are expected to be more frequent in the near future scenario

(L´

opez et al., 2019; Reimer et al., 2021).

The Canary Islands archipelago is especially vulnerable to seawater

warming, due to its subtropical localization that enables the coexistence

of biota of both tropical and temperate origins. Clear indicators of tro-

picalization of marine systems are already evident, as many tropical

species have recently arrived and settled populations on the islands, e.g.

sh such as Uraspis secunda (Falc´

on et al., 2018), Parablennius goreensis

(Falc´

on et al., 2015) and Cantherines macrocerus (Brito et al., 2017), and

cnidarian species like Millepora sp. (Clemente et al., 2011). Similarly,

meridionalization processes are becoming more frequent in the archi-

pelago (Clemente et al., 2011; Sangil et al., 2011). For example, the

native benthic zoantharians Palythoa caribaeorum and Zoanthus pulchel-

lus are increasing their population abundances, especially in the

warmest coasts of the islands (Clemente et al., 2022; L´

opez et al., 2020).

In fact, it is known that some Zoanthus and Palythoa species have been

able to cover large areas of hundreds of square meters in intertidal and

subtidal locations worldwide (Reimer et al., 2021), altering the local

biota composition due to their mat-forming growth and substrate

dominance (Durante et al., 2018; Gonz´

alez-Delgado et al., 2018; Mor-

eno-Borges et al., 2022; Reimer et al., 2021). This has been related to

their powerful palytoxins that avoid predators, their rapid growth rates

due to the lack of carbonates in their skeleton and their high resilience to

environmental stressors (Reimer et al., 2021).

In shallow and illuminated benthic environments of the Canary

Islands, macroalgae hold major ecological importance (Afonso-Carrillo

et al., 2001; Barquín-Diez et al., 2005; Sangil et al., 2007). As marine

ecosystem engineers, they provide essential habitat for numerous spe-

cies and thus play a fundamental role in the maintenance of local

biodiversity (Sangil, 2011). In the Archipelago, the most abundant

macroalgal taxa consist of crustose coralline algae (CCA) and Dictyo-

tales, specically species of the genus Lobophora, representing alto-

gether nearly 88% of total substrate coverages (Sangil, 2011; Sangil

et al., 2012, 2018). However, in the last few decades some locations that

used to be covered by macroalgae beds are now dominated by extensive

colonies of Zoanthus pulchellus and Palythoa caribaeorum (L´

opez et al.,

2020; Moreno-Borges et al., 2022). The proliferation of such colonies

establishes a direct competition with macroalgae for substrate and light

availability, being able to create new ecosystems that have already

altered local invertebrate and sh communities (Clemente et al., 2022;

Gonz´

alez-Delgado et al., 2018; Moreno-Borges et al., 2022; 2024).

However, mechanisms behind these phase-shifts from

macroalgae-dominated areas to zoantharian-dominated areas are still

unknown and therefore, it is imperative to understand the factors

driving zoantharian success over macroalgae, for establishing proper

management measurements that ensure ecosystems services and func-

tion (Soares et al., 2022).

Macroalgae employ different mechanisms to directly compete

against other benthic organisms and proliferate in rocky substrates.

Some species use mechanical abrasion (Chadwick, 1988; Hughes, 1989;

Tanner, 1995) while others like Lobophora spp. (Smith et al., 2006;

Vieira et al., 2016) and some turf algae (Cetz-Navarro et al., 2015; Pratte

et al., 2018) secrete substances that affect coral-associated microbial

communities and can cause mortality. Meanwhile, palytoxins are highly

potent toxins that, together with other biological traits of zoanthids,

might be enhancing the spread of zoantharians colonies. However, many

other indirect factors might be shaping the composition of benthic

communities of the Canary Islands, including environmental factors

such as hydrodynamics or sedimentation, and biotic factors such as

herbivore activity. In fact, the grazing pressure of sea urchins on mac-

roalgal communities has been extensively studied in the Canarian ar-

chipelago. As sea urchin densities increase, it leads to a simplication of

algal communities, reducing richness and diversity (Hern´

andez et al.,

2008a; Sangil et al., 2010; Tuya et al., 2004a, 2004b), ultimately

resulting in the formation of sea urchin barrens (Brito, 2008; Clemente

et al., 2007). Specically, the sea urchins Diadema africanum in the

subtidal and Paracentrotus lividus in the intertidal and shallow subtidal

play an important ecological role in the Canary Islands ecosystems by

mediating the transition between macroalgal beds and sea urchin bar-

rens (Hern´

andez et al., 2008a). Therefore, populations of these two

intense herbivorous species could be enhancing the increase in zoan-

tharian abundances by leaving free space for them to grow.

In this study, we aimed to investigate the mechanisms behind the

processes of zoantharian-macroalgae competition for substrate in the

Canary Islands. To do so, we conducted laboratory experiments to

investigate changes in growth rates of Palythoa caribaeorum and Zoan-

thus pulchellus when interacting in close proximity with the most

dominant morpho-functional groups of algae found sharing natural

habitats: Lobophora spp., mixed turf macroalgae, and CCA. Furthermore,

we evaluated the role of sea urchins in zoanthid colony growth and their

potential contribution to substrate colonization by controlling macro-

algal cover.

2. Material and methods

2.1. Sample collection and acclimatization to laboratory conditions

Specimens of Zoanthus pulchellus, Palythoa caribaeorum and their

main cohabiting types of macroalgae (Lobophora spp., turf algae and

CCA) were collected in December 2020 at two different locations off

Tenerife Island, where populations of these zoantharians dominated the

rocky habitat. The subtidal zone of Tajao (28◦9

′

59.77

″

N, 16◦25

′

41.06

″

W) was selected to collect samples of P. caribaeorum and the

different macroalgae by means of scuba diving at 3–7 m depth. The

intertidal zone of Punta del Hidalgo (28◦34

′

″

N, 16◦19

′

″

W) was

chosen for the collection of samples of Z. pulchellus and macroalgae that

were obtained from tidepools. Approximately 40 colonies of

P. caribaeorum (7.75 ±3.81 cm

; 26.13 ±8.46 polyps) and 40 fragments

of Z. pulchellus (5.74 ±2.21 cm

; 39.06 ±17.27 polyps) were collected

with the aid of a knife. Small rocks (39.86 cm

±13.86) covered by the

target macroalgae were also gathered. By collecting macroalgae in the

same areas at subtidal and intertidal habitats respectively, we sought to

recreate zoantharian-algae interactions in their natural environment. In

order to evaluate whether sea urchins grazing facilitates zoantharians

colony growth by creating available substrate, we collected the most

abundant sea urchin species at each sampling location. Six Diadema

africanum (34.58 ±5.28 mm in test diameter), and seven Paracentrotus

lividus (29.52 ±2.42 mm in test diameter) were used for experiments

with P. caribaeorum and Z. pulchellus, respectively. Samples were

immediately transported under humid and dark conditions to the lab-

oratory and placed in tanks with running seawater at 12-h light/12-h

dark cycle using LED lights (Coral Led Blue Screens from ICA S.A.).

2.2. Experimental design and data acquisition

Two experiments were carried out for each zoanthid species in the

laboratory. To assess the potential effects of macroalgae on zoantharian

colonies growth, we put in contact fragments of both Z. pulchellus and

P. caribaeorum with each of the three morphotypes of macroalgae

dominating the intertidal and subtidal habitats of the study locations,

respectively (Fig. 1). Therefore, experimental units consisted in rocks

with the different algae treatments (Lobophora spp., turf algae and CCA),

in which a colony of the corresponding zoantharian species was attached

using SOUDAL-CYANOFIX 84 A adhesive (following the methodology

described by L´

opez et al., 2021). Previously to adding the zoantharian

colony, rocks were carefully scraped using metal brushes and scouring

pads to open a free substrate space for the colony, while trying to avoid

any harm to the algae. Only the experimental units in which both

zoantharian and macroalgae looked in healthy conditions after an

acclimatization period of 30 days were used for further experiments,

resulting in an uneven allocation of replicates among treatments.

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

Therefore, the experiment nally consisted of 21 colonies of Zoanthus

pulchellus (7 replicates with Lobophora spp., 7 replicates with intertidal

turf algae, and 7 replicates with CCA) and 26 colonies of Palythoa car-

ibaeorum (9 replicates with Lobophora spp., 9 replicates with subtidal

turf algae, and 8 replicates with CCA) (Fig. 1A–F).

A second laboratory experiment consisted of evaluating the role of

sea urchins as facilitators of zoanthid colony growth in areas covered by

CCA, since this macroalgae morphotype dominates sea urchin barrens of

the Canary Islands. For this purpose, two treatments were assessed: one

exposing zoantharian colonies on a rocky substrate with CCA to one sea

urchin and the other without sea urchin, considering sea urchin species

naturally inhabiting intertidal and subtidal habitats. Thus, this experi-

ment consisted of 15 colonies of Z. pulchellus attached to rocks with CCA

collected in the intertidal habitat, following the same procedures as

explained above: 7 replicates with the presence of the sea urchin Para-

centrotus lividus and 7 replicates in the absence of the sea urchins. In the

case of the experiment with P. caribaeorum, 14 colonies glued to rocks

with CCA collected in the subtidal habitat were used: 6 replicates

exposed to a sea urchin Diadema africanum and 8 replicates without sea

urchins (Fig. 1G and H).

For both experiments, each experimental unit was placed in a 2 L

transparent cylindrical container, randomly distributed across three sea

water running tanks, with a 300 L capacity, resulting in 20 samples per

tank. The containers received a constant ltered water ow through a

thin hose xed to their bottoms, ensuring independent conditions for

each replicate. Excess water at each container owed by gravity into the

upper compartment of the tank that circulated into a lower reservoir

passing through 50

m and 10

m polyamide lters before recirculating

back to containers. Seawater temperature was kept constant using

aquarium coolers (HAILEA HC-500 A) and heaters (EHEIM JAGER 150

W) placed within each tank. This setup ensured that each independent

containers positioned in the upper part of the tank was immersed in a

water bath, effectively regulating the water temperature throughout

(See supplementary material, Fig. S1).

In both acclimatization and experimental periods colonies were

maintained at the natural values of seawater salinity (36.7 ±1.0 UPS)

and temperature (20.00 ±1.00 ◦C) in the Canary Islands. Seawater

parameters were monitored twice daily in each experimental tank using

a WTW Cond 3110 device and 75% of seawater in each tank was

replaced once a week. Given the mixotrophic condition of zoantharians,

we added a light cycle of 12 h/12 h using ICA S.A Coral Led Blue Screens

and colonies were fed with a mixture of phytoplankton and zooplankton

(AF Phyto Mix from Aquaforest and Polyp-Lab reef roids) every two

days. For this, the water recirculation system was paused for a 4-h in-

terval to facilitate individual feeding of each colony within each

container.

Throughout the experiment, daily assessments were conducted to

monitor the overall condition of the colonies, specically looking for

signs of bleaching or deterioration. Photographs of each replicate were

taken at the beginning, midpoint (2 months), and at the end (4 months)

of the experiment, using a frame structure adjusted to t the camera

(Olympus TG6) and the size of the samples, ensuring consistent orien-

tation, position, and distance from samples for comparability. Further-

more, a metric scale was placed at the level of the zoanthid-macroalgae

interaction in each sample, serving as a reference for measuring the

growth and substrate cover of the zoanthid colony and macroalgae

through time (Fig. 1). Growth rates of the zoantharian colonies and

macroalgae were assessed by counting the number of polyps and by

calculating coverage areas in photographs using Image J v. 1.50 b

software. Additionally, we carefully evaluated boundaries of colonies

neighboring algae in all treatments to determine whether they advanced

on the substrate, remained stable, or retreated from the interface with

the algae.

2.3. Statistical analyses

To evaluate competition for space between zoantharians and mac-

roalgae, we analyzed growth rates as increments (Δ) in area and number

of polyps of Palythoa caribaeorum and Zoanthus pulchellus. In order to do

so, we separately constructed linear mixed effects models for the growth

variables of each zoantharian species as functions of the xed effects:

Algae treatment (3 levels; Lobophora spp., CCA and turf) and Period (2

levels; 2 and 4 months). The same design was performed to evaluate the

effect of the presence of sea urchins upon zoantharian growth, in this

case with two xed effects: Sea urchin (2 levels; presence/absence) and

Period (2 levels; 2 and 4 months under the experimental conditions). In

both cases, we included a varying-intercept random effect of replicate to

account for repeated measurements of replicates through time. The

growth rate model was tted following a Gaussian distribution by using

the lme4 package (Linear Mixed Effects version 4; Bates and Maechler,

Fig. 1. Experimental treatments of zoantharian-macroalgae interactions in experiments with Palythoa caribaeorum (rst row) and Zoanthus pulchellus (second row).

A)-F) Zoantharians cohabiting with different types of macroalgae: Lobophora spp. (A, B), turf algae (C, D), and crustose coralline algae (CCA) (E, F). G) P. caribaeorum

with CCA exposed to the sea urchin Diadema africanum. H) Z. pulchellus with CCA exposed to Paracentrotus lividus.

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

2010). Additionally, for the increment in the number of P. caribaeorum

polyps, we also tted a generalized linear mixed-effect model with a

Poisson distribution using the same explanatory variables. Model as-

sumptions were assessed using the DHARMa package (Hartig, 2022),

and pseudo-R

values were calculated for xed and random effects using

the jtools package (Long, 2022). The Akaike Information Criterion (AIC;

Akaike, 1974) was used to select the best-tting mixed-effects models

for our data. We compared different candidate models, including

different combinations of xed and random effects, and selected the

model with the lowest AIC as the nal model for each response variable.

All analyses were conducted in RStudio version 2023.6.1.524 (Posit

Team, 2023).

3. Results

During the experiment assessing the impacts of macroalgae over

zoantharian colonies, three replicate colonies of Zoanthus pulchellus in

the Lobophora spp. treatment, one in the turf algae treatment, and two in

the CCA treatment, were excluded from statistical analyses due to their

suboptimal health conditions. Thus, nal replicates for Z. pulchellus were

four, six, and ve for Lobophora spp., turf, and CCA treatments,

respectively. In contrast, all colonies of Palythoa caribaeorum remained

healthy throughout the four-month experiment, except for one replicate

from the turf algae treatment that was excluded because it detached

from the experimental substrate. In this case, nal replicates for

P. caribaeorum were nine, eight, and eight for Lobophora spp., turf, and

CCA treatments respectively.

In the second experiment evaluating the effects of sea urchin grazing

on zoantharian growth, ve colonies of Zoanthus pulchellus were

excluded from statistical assessments, including three replicates in CCA

with sea urchin treatment and two of CCA treatment without sea urchin.

Hence, the nal number of replicates in the experiment was four for the

former and ve for the latter treatments. Conversely, all colonies of

Palythoa caribaeorum survived in healthy condition during the whole

experiment.

3.1. Experiments of the effects of macroalgae on zoantharian colonies

3.1.1. Effects of macroalgae on P. caribaeorum growth

The increment in area of P. caribaeorum colonies showed no signi-

cant differences among macroalgae treatments nor between the two

time periods of the experiment (Table 1A). In general, the area of

P. caribaeorum colonies decreased along the whole experiment for the

three algae treatments (Fig. 2A). Colonies in the CCA treatments showed

no differences when compared with the other two algae treatments.

Colonies interacting with turf algae experienced a greater decrease than

the rest of the colonies during the rst part of the experiment (2

months), while the ones growing next to Lobophora spp. were more

affected after 4 months (Fig. 2A). Interestingly, although not signi-

cantly different, these same colonies at Lobophora spp. treatment were

the only ones that displayed a positive mean increment in area during

the rst period (Fig. 2A).

The increment in number of polyps of P. caribaeorum showed sig-

nicant differences between the two time periods while no differences

were found among macroalgae treatments (Table 1B). Regardless of the

algae cohabiting with the colonies, there was a general increase in the

number of polyps during the rst 2 months, followed by an overall

decrease in the last part of the experiment (Fig. 2B).

When analysing P. caribaeorum boundaries adjacent to the different

algae treatments (See supplementary material, Fig. S2A) during the rst

two months of experiment, 56% of the colonies exhibited stable inter-

acting boundaries at the interface with Lobophora spp., regardless of

overall colony growth or decline. In 22% of the replicates, interaction

borders extended towards the algae, while an additional 22% retreated

from the interface. During the subsequent period, only 11% of colonies

kept stable boundaries, while 56% retreated and 33% advanced on the

substrate. However, 75% of P. caribaeorum colonies interacting with turf

algae had borders that retreated in opposed direction to the algae during

the rst two months, and this trend continued during the second period,

with 63% of boundaries retreating. Additionally, colonies interacting

with CCA exhibited the highest prevalence of boundary advancement

compared to the other algae treatments, with 38% and 63% during the

rst and second experimental periods respectively (See supplementary

material, Fig. S2).

3.1.2. Effects of macroalgae on Z. pulchellus growth

The analysis of area growth by Zoanthus pulchellus colonies showed

no signicant differences between the three algae treatments (Table 2A),

and a general decrease in colony area was observed by the end of the

experiment. Like P. caribaeorum, although not statistically signicant,

colonies at Lobophora spp. treatment were the only ones that displayed a

mean positive increment in area during the rst period but experienced

the largest decrement during the second period (Fig. 3A).

Growth in terms of increment in number of polyps of Z. pulchellus

revealed a signicant effect across both time periods (Table 2B). Mean

increments in number of polyps remained negative for the three algae

treatments during the rst experimental period but became positive

during the last two months of the experiment (Fig. 3B). However, no

signicant effect of the type of macroalgae was detected (Table 2B)

(Fig. 3B).

When examining the boundaries of Z. pulchellus colonies interacting

with different algae treatments (See supplementary material, Fig. S3A),

Table 1

Results of the linear mixed effects models for growth variables of Palythoa caribaeorum colonies interacting with different macroalgae treatments (CCA, Lobophora spp.,

and turf algae). Model A) Results of the analysis for increment of P. caribaeorum coverages. Model B) Results of the analysis for increment in number of P. caribaeorum

polyps. p-values <0.05 were considered statistically signicant.

A) Dependent variable: Increment in P. caribaeorum coverage B) Dependent variable: Increment in P. caribaeorum polyps

Fixed effects Independent variable Estimate S.E t

value

Estimate S.E t

value

Intercept (Reference

=CCA)

−0.55 0.27 −2.03 43 0.049 0.87 0.38 2.27 29 0.031

Lobophora - CCA 0.59 0.38 1.58 43 0.122 −0.64 0.49 −1.30 22 0.206

CCA - Turf −0.31 0.39 −0.81 43 0.423 −0.25 0.50 −0.50 22 0.625

Period 0.07 0.36 0.20 22 0.845 −1.24 0.28 −4.45 24 0.000

Lobophora:Period −0.67 0.49 −1.37 22 0.184 (No interaction in the selected model)

Turf:Period 0.44 0.50 0.87 22 0.394

Random

effects

Independent variable Parameter Std. Deviation Parameter Std. Deviation

Replica (intercept) 0.31 (intercept) 0.73

Residual 0.71 0.98

Model Fit Pseudo R2 (Fixed

effects) =0.12

Model Fit Pseudo R2 (Fixed

effects) =0.24

Pseudo R2 (total) =0.25 Pseudo R2 (total) =0.61

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

we found that 75% of colonies remained stable at the interface with

Lobophora spp., regardless of colony growth or decline. Meanwhile, 25%

of colonies showed borders advancing towards the macroalgae, while

none retreated in the opposite direction. However, during the second

period, all colonies interacting with Lobophora spp. Maintained stable

interaction boundaries. In colonies interacting with turf algae, 50%

remained with stable borders at the interface, while 33% advanced to-

wards the algae, and 16% retreated within the rst 2 months. After 4

Fig. 2. Growth trends of Palythoa caribaeorum, both in terms of A) increment in colony coverage and B) increment in numbers of polyps, interacting with different

algae treatments (CCA, Lobophora spp., and turf algae) over two time periods at laboratory conditions.

Table 2

Results of the linear mixed effects models for growth variables of Zoanthus pulchellus colonies interacting with different algae treatments (CCA, Lobophora spp., and turf

algae). Model. A) Results of the analysis for increment of Z. pulchellus coverages. Model B) Results of the analysis for increment in number of Z. pulchellus polyps. p-

values <0.05 were considered statistically signicant.

A) Dependent variable: Increment in Z. pulchellus coverage B) Dependent variable: Increment in Z. pulchellus polyps

Fixed effects Independent variable Estimate S.E t value d.f p-value Estimate S.E t value d.f p-value

Intercept (Reference =CCA) −0.04 0.29 −0.13 26 0.901 −1.30 0.60 −2.16 26 0.040

Lobophora - CCA −0.18 0.38 −0.47 26 0.642 0.15 0.78 0.19 26 0.849

CCA - Turf −0.29 0.34 −0.84 26 0.410 −0.68 0.71 −0.97 26 0.341

Period −0.13 0.29 −0.43 26 0.668 1.80 0.60 2.99 26 0.006

(No interaction in the selected model) (No interaction in the selected model)

Random effects Independent variable Parameter Std. Deviation Parameter Std. Deviation

Replica (intercept) 0.00 (intercept) 0.00

Residual 0.80 1.65

Model Fit Pseudo R2 (Fixed effects) =0.03 Model Fit Pseudo R2 (Fixed effects) =0.27

Pseudo R2 (total) =0.03 Pseudo R2 (total) =0.27

Fig. 3. Growth trends of Zoanthus pulchellus, both in terms of A) increment in colony coverage and B) increment in numbers of polyps, interacting with different algae

treatments (CCA, Lobophora spp., and turf algae) over two time periods at laboratory conditions.

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

months, 67% of Z. pulchellus colonies retreated away from the turf, while

16% advanced, and another 16% mantained stable boundaries on the

substrate. In contrast, colonies in contact with CCA exhibited the highest

prevalence (40%) of boundaries advancement throughout the experi-

ment. During the rst two months, 60% of colonies had stable borders at

the interface, but this number dropped to 40% in the second period,

while 16% exhibited retreat (See supplementary material, Fig. S3).

3.2. Experiments assessing the effects of sea urchin grazing in zoantharian

growth

3.2. 1. Diadema africanum effect on P. caribaeorum growth

D. africanum specimens were consistently observed actively grazing

on the CCA and biolm covering the rocks in all replicates of the sea

urchin treatment. Results of the linear mixed effects model analyzing

P. caribaeorum growth showed signicant differences in terms of colony

area between the two sea urchin treatments, while no signicant effect

of time periods was observed (Table 3A). Colonies experienced a sig-

nicant growth in coverage when D. africanum was present, a trend that

remained consistent throughout the duration of the experiment

(Fig. 4A). In contrast, in the absence of the sea urchin, experimental

colonies experienced negative growths in terms of increment of

coverage areas of the colonies (Table 3A).

The increment of number of polyps did not show a signicant

response to the sea urchin treatment, but a signicant effect between

time periods was detected (Table 3B). Regardless of the presence or

absence of D. africanum, the increment in number of polyps was signif-

icantly higher during the rst period than during the second period of

the experiment (Fig. 4B). During the last 2 months, the number of polyps

in the colonies without sea urchin decreased and the ones in the treat-

ment with sea urchin remained constant (increment =0) (Fig. 4B).

P. caribaeorum replicates with sea urchin presence showed a higher

proportion of colonies with interacting boundaries advancing over the

CCA and bare rock compared to colonies adjacent to CCA without sea

urchins (See supplementary material, Fig. S2B). During the rst two

months percentages were 67% versus 38%, respectively, and increased

to 83% versus 63% during the second period. Furthermore, in treat-

ments with sea urchin, 17% of colony boundaries maintained their po-

sition at the front during the initial period while 17% retreated. In the

subsequent period, none remained stable, but 17% continued to retreat

in opposite direction to CCA. In contrast, in the absence of sea urchins, a

higher percentage of colonies retreated, with 38% during the rst period

and 25% during the second.

3.2. 2. Paracentrotus lividus effect on Z. pulchellus growth

Specimens of P. lividus were observed grazing on the CCA and biolm

within the sea urchin treatment replicates, and a decrease in algae

coverage over time was seen, despite they were generally more seden-

tary than D. africanum samples. The linear mixed effects analysis

revealed no signicant differences in the growth of colony area of

Z. pulchellus between treatments in presence or absence of the sea urchin

Paracentrotus lividus, nor between the time periods studied throughout

the experiment (Table 4A). Similarly, no signicant effects of the pres-

ence of the sea urchin or between time periods was observed upon the

increment in numbers of polyps of Z. pulchellus (Table 4B). Overall,

mean values for both growth variables remained negative throughout

the entire experiment, with one exception noted in the second period,

when the mean increment in area of Z. pulchellus exhibited a positive

trend in the absence of P. lividus (Fig. 5).

When evaluating the boundaries of Z. pulchellus colonies in the

presence or absence of P. lividus (See supplementary material, Fig. S3B),

a higher percentage of colony borders (50%) was observed advancing

towards CCA in the presence of sea urchin compared to treatments

without sea urchin (40%) during the rst period. However, this trend

reversed during the second period, with a higher proportion of colonies

showing advancing boundaries in the absence of P. lividus (40%

compared to 25% in the presence os sea urchin). Additionally, the per-

centage of colonies that retreated from the interface was higher in the

presence of sea urchins, with 25% in both periods. In the absence of

P. lividus, no colonies retreated during the rst period, but they

increased to 20% during the second period.

4. Discussion

Results of this study revealed that Palythoa caribaeorum and Zoanthus

pulchellus nd difculties displacing the main functional groups of

macroalgae found in the Canary Islands at rocky substrates. In general,

colonies of both zoantharians experienced a decrease in growth, indi-

cating no clear competitive advantage for either species among the

studied macroalgae. In general, Z. pulchellus exhibited more tolerance to

algae, maintaining a higher proportion of stable colony boundaries

directly interacting with macroalgae compared to P. caribaeorum

throughout the experiment, supporting previous studies that found

higher macroalgae coverages in habitats dominated by this zoantharian

species (Clemente et al., 2022; Moreno-Borges et al., 2022). Moreover,

despite the presence of Paracentrotus lividus having no effect on the

expansion of Z. pulchellus colonies, the grazing activity of the sea urchin

Diadema africanum over CCA facilitated P. caribaeorum growth. Our re-

sults provided evidence of a positive feedback between this sea urchin

species and the spread of zoantharian colonies. This is particularly

relevant considering D. africanum and P. caribaeorum tropical afnities

and the current context of ocean warming scenarios.

In general, colonies displayed active polyps and maintained healthy

appearance after the acclimatization and experimental periods.

P. caribaeorum exhibited a remarkable 100% survival rate throughout

the 4-month experiment, while Z. pulchellus, though slightly lower, also

presented a high survival rate (71,43%). Our results revealed signicant

differences in colony growth for both zoantharian species over time,

specically in terms of polyp numbers, and a clear trend of decreasing

zoanthid cover throughout the experiment. These uctuations in colony

Table 3

Results of the linear mixed effects models for growth variables of Palythoa caribaeorum at experiments assessing the effects of the presence of the sea urchin Didema

africanum. Model A) Results of the analysis for increments of P. caribaeorum coverages. Model B) Results of the analysis for increments in number of P. caribaeorum

polyps. p-values <0.05 were considered statistically signicant.

A) Dependent variable: Increment in P. caribaeorum coverage B) Dependent variable: Increment in P. caribaeorum polyps

Fixed effects Independent variable Estimate S.E t value d.f p-value Estimate S.E t value p-value

Intercept −0.72 0.34 −2.16 16 0.046 1.13 0.18 6.1 0.000

Sea Urchin 1.24 0.47 2.64 12 0.022 0.32 0.23 1.35 0.178

Period 0.41 0.27 1.54 13 0.148 −0.78 0.25 −3.08 0.002

(No interaction in the selected model) (No interaction in the selected model)

Random effects Independent variable Parameter Std. Deviation Parameter Std. Deviation

Replica (intercept) 0.72 (intercept) 0.00

Residual 0.70

Model Fit Pseudo R2 (Fixed effects) =0.30 Model Fit Pseudo R2 (Fixed effects) =0.36

Pseudo R2 (total) =0.66 Pseudo R2 (total) =0.36

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

growth might be attributed to the inherent variability in size and weight

experienced by soft-bodied organisms due to their physiological state or

in response to environmental disruptions (Fabricius, 1995; Hellstr¨

and Benzie, 2011).

No overall differences were found in colony growth of both zoan-

tharian species between algae treatments, but colonies decreased in area

and polyp numbers in all treatments. These ndings suggest adverse

algae effects on colony growth. Kuffner et al. (2006) emphasized that

Fig. 4. Growth trends of P. caribaeorum, both in terms of A) increment in colony coverage and B) increment in numbers of polyps, over two time periods in laboratory

experimental conditions of presence or absence of the sea urchin Diadema africanum.

Table 4

Results of the linear mixed effects models for growth variables of Zoanthus pulchellus at experiments assessing the effects of the presence of the sea urchin Paracentrotus

lividus. Model A) Results of the analysis for increment of Z. pulchellus coverages. Model B) Results of the analysis for increments in number of Z. pulchellus polyps. p-

values <0.05 were considered statistically signicant.

A) Dependent variable: Increment in Z. pulchellus coverage B) Dependent variable: Increment in Z. pulchellus polyps

Fixed effects Independent variable Estimate S.E t value d.f p-value Estimate S.E t value d.f p-value

Intercept −0.07 0.32 −0.23 13 0.824 −0.96 0.59 −1.62 13 0.129

Sea Urchin −0.32 0.41 −0.76 13 0.460 −0.43 0.76 −0.57 13 0.578

Period −0.05 0.40 −0.13 13 0.896 1.12 0.74 1.53 13 0.150

(No interaction in the selected model) (No interaction in the selected model)

Random effects Independent variable Parameter Std. Deviation Parameter Std. Deviation

Replica (intercept) 0.00 (intercept) 0.00

Residual 0.80 1.47

Model Fit Pseudo R2 (Fixed effects) =0.04 Model Fit Pseudo R2 (Fixed effects) =0.15

Pseudo R2 (total) =0.04 Pseudo R2 (total) =0.15

Fig. 5. Growth trends of Z. pulchellus, both in terms of A) increment in colony coverage and B) increment in numbers of polyps, over two time periods in laboratory

experimental conditions of presence or absence of the sea urchin Paracentrotus lividus.

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

coral-algae interactions can be metabolically expensive for some species

of corals. While zoantharians are recognized for their success due to fast

growth rates and toxins production (Moore and Scheuer, 1971), several

macroalgae exhibit a wide variety of competitive strategies to ensure

their survival as well. Lobophora spp. Are able to compete for substrate

by producing bioactive compounds (Vieira et al., 2016) that can alter

coralline bacterial communities (Morrow et al., 2012; Morrow et al.,

2013; Smith et al., 2006; Vieira, 2020), or by mechanical defences such

as suffocation or impeding polyp movement (Coyer et al., 1993; Tanner,

1995). However, the potential adverse effects of the erect canopy

forming Lobophora spp. on zoanthid colonies were not evident.

Throughout the experiment neither species was able to overgrow the

other, unlike some cases observed by other authors between corals and

Lobophora spp. (Vieira, 2020). Despite not signicant, both zoantharian

species interacting with Lobophora spp. showed a slight positive mean

increment in coverage during the rst period but a marked decrease

during the second period. These results suggest that zoantharian col-

onies may have exhibited greater resistance during the initial phase of

interaction with Lobophora spp. compared to longer-term exposure.

These ndings are consistent with observations on colony boundaries of

P. caribaeorum interacting with algae, which revealed that most colonies

initially maintained their position in the substrate when in contact with

Lobophora spp.. However, this stability weakened considerably in the

second experimental period, with the majority of P. caribaeorum borders

retreating, indicating a clear decline in competitiveness against the

algae. Alternatively, it is plausible that the absence of herbivory,

resulting in the proliferation of biolm and caespitose algae, posed

additional challenges for the zoantharians to thrive. According to Eich

et al. (2019), the presence of epiphytic algae on Lobophora spp. was

correlated with notably heightened algal competitiveness against corals.

These authors attributed this phenomenon to an augmented production

or concentration of defensive chemicals by both epiphytes and Lobo-

phora spp., thereby enhancing host competitiveness in coral–algal in-

teractions. In contrast, most Z. pulchellus colony boundaries exhibited

greater tolerance to the presence of Lobophora spp. remaining stable,

despite decrements in overall colony area occurring predominantly on

the opposite side of the colony. This disparity in response between

zoantharian species may be attributed to differences in body organiza-

tion. While P. caribaeorum exhibits embebed polyps, Z. pulchellus pos-

sesses a thinner coenenchyme and liberae polyps (L´

opez et al., 2019),

allowing for interspecies cohabitation (Clemente et al., 2022), leading to

a greater tolerance to macroalgae.

In the Canary Islands, ocean warming is facilitating the expansion of

thermophilic Lobophora species on rocky illuminated substrates

(Hern´

andez et al., 2018; Sangil et al., 2011), which could play a

fundamental role in preventing the expansion of zoanthids. However,

several studies have conrmed that grazing activity can substantially

restrict the distribution of Lobophora spp. (de Ruyter van Steveninck and

Breeman, 1987; Lewis, 1985; Van den Hoek et al., 1978), especially

since Diadema spp. have a strong preference for this algal genus

(Rodríguez et al., 2018; Tuya et al., 2001). Hence, excessive herbivory

may not only degrade macroalgae beds, as reported for the Canary

Islands (Sangil et al., 2014), but also create free substrates for the set-

tlement of other opportunistic organisms. Still, despite our ndings, the

impacts of Lobophora canopies on zoantharian growth performance

remain unclear. Further research addressing zoantharian-Lobophora spp.

interactions are imperative, as both species display warm water afn-

ities and could dominate the rocky substrate of the Canary Islands in an

ocean warming scenario.

Similar observations were noted in colonies of P. caribaeorum and

Z. pulchellus under the presence of macroalgae turf. While not signi-

cant, a general decline in both area and number of polyps occurred, with

the former exhibiting a continuous decrease throughout the entire

experiment. In line with these ndings, in most colonies of both zoan-

tharian species, colony borders tended to retreat when adjacent to turf

algae, although Z. pulchellus exhibited some initial resistance. Previous

studies showed that turf algae may allelopathically compete with corals

(Cetz-Navarro et al., 2015; Jompa and McCook, 2003; Pratte et al.,

2018; Roach et al., 2020; Vermeij et al., 2010). According to Barott et al.

(2009), coral surfaces in direct contact with turf algae frequently exhibit

hypoxic conditions. Pratte et al. (2018) even highlighted the capacity of

specic mixed turf algae to modulate coral microbiomes, emphasizing

their competitiveness. Yet, competitive potential varies signicantly

among algal taxa within a functional group. Some lamentous algae can

overgrow and damage corals (Jompa and McCook, 2003; Littler and

Littler 1997; Potts 1977), while others are displaced by coral growth

(McCook 2001), particularly encrusting coral species (Swierts and Ver-

meij, 2016). Given the intricate composition of turf algae, comprising

juvenile erect algae, lamentous algae, cyanobacteria (Afonso-Carrillo

et al., 2007; Hester et al., 2016; Sangil et al., 2007) and diverse bacteria

(Walter et al., 2016), it is possible that different components exhibit

varying interactions with zoanthids. Therefore, future studies should

undertake a more detailed examination of specic turf algae taxa in the

Canary Islands, disentangling composition of turfs cohabiting with each

zoanthid species, to elucidate both enhancers and constraints inu-

encing zoanthid colony growth.

Colonies of both zoantharian species in contact with CCA showed the

highest percentage of advancing boundaries across the substrate

compared to other algae treatments, suggesting that this algae mor-

photype offers less resistance to the spread of zoantharian colonies.

However, an overall decline in colony area and polyp number was also

noted in colonies, indicating, on the contrary, a negative effect of CCA

on colony health. Although some authors reported that CCA can be used

as controls because they have little to no negative effect on corals (Barott

et al., 2009; Vermeij et al., 2010), our experiment showed no signicant

differences compared to the other algae treatments, whose negative

effects on corals have already been stated (Morrow et al., 2013; Roach

et al., 2020; Vieira, 2020). These unexpected results could be attributed

to the defensive nature of the selected CCA species, since Jorissen et al.

(2020) reported that certain sub-cryptic CCA species act as inhibitors

rather than facilitators of coral survival and growth after settlement

(Arnold and Steneck 2011; Doropoulos et al., 2016; Harrington et al.,

2004). Yet, research on coral-algae interactions has primarily concen-

trated on scleractinian corals, but zoantharian-algae interactions may

yield different effects. Furthermore, the slight growth of biolm under

the absence of herbivore activity may have contributed to the impact

observed, since caespitose algae can stress corals even with barely

visible overgrowth (Vermeij et al., 2010). Thus, the second experimental

approach in which main herbivore sea urchins were added to CCA

treatments allowed us to overcome these potential effects.

Different results were observed depending on the zoanthid and sea

urchin species considered. In particular, the substrate facilitating effect

of the sea urchin Paracentrotus lividus on Zoanthus pulchellus growth

could not be demonstrated, as P. lividus did not exhibit a signicant

impact in this study. Probably the grazing effect of this sea urchin spe-

cies was not enough to signicantly alter crustose algae coverage and

render free substrate for colony growth. In fact, P. lividus is primarily

known to feed on eshy algae rather than CCA (Agnetta et al., 2013),

which is why rocky substrates with high densities of P. lividus are mainly

colonized by encrusting Corallinaceae (Bulleri et al., 1999). Alterna-

tively, the lack of increased growth in colonies in presence of the sea

urchin could be due to the behavior of experimental sea urchins that

pulled off some polyps of the colonies to shelter themselves, a covering

behavior known for this species in natural conditions to nd protection

against UV radiation (Verling et al., 2002) and predation (Amsler et al.,

1999). Future studies should include small rocks or shells in the exper-

imental units to provide additional cover for P. lividus.

A positive effect of the presence of Diadema africanum over the

growth of P. caribaeorum colonies was observed, consistent with previ-

ous studies highlighting positive interactions between sea urchins and

corals (Cano et al., 2021; Carpenter and Edmunds 2006; Foster, 1987;

Hughes et al., 1987; Idjadi et al., 2010; Soto-Santiago and Irizarry-Soto,

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

2013). The intense grazing activity of D. africanum specimens reduced

macroalgal cover and facilitated zoantharian growth, with colonies

increasing even up to 3.814 cm

and 7 polyps. Globally, population

dynamics of this sea urchin genus closely correlate with transitions from

coral-dominated ecosystems, prevalent when sea urchins are present, to

macroalgae-dominated habitats following Diadema spp. mass mortality

events (Carpenter, 1990; Hughes et al., 1987). However, while the

literature has extensively documented the facilitative role of sea urchins

in scleractinian coral recruitment and growth (Carpenter and Edmunds,

2006; Edmunds and Carpenter, 2001), contributing to the stability of

coral reef systems (Idjadi et al., 2010), limited attention has been given

to their inuence on the growth and expansion of photophilic zoan-

tharians. In this sense, our results evidenced that D. africanum pop-

ulations could facilitate transitions from macroalgal to zoanthid

communities in subtropical regions. Whether providing free space in the

substrate or releasing the CCA from other overgrowing algae, the posi-

tive effect of D. africanum over P. caribaeorum growth cannot be denied,

emphasizing the critical role that sea urchin populations may be playing

in the expansion of zoanthid populations.

Additionally, an interesting observation regarding P. caribaeorum

growth in treatments exposed to herbivory was recorded. Colonies

experienced an increase in polyp quantity during the rst period of the

experiment but maintained a constant number of polyps during the last

period while exhibiting a higher increase in colony area than in the rst

period. These results suggest a growth strategy for this species, in which

an initial rise in polyp number was followed by an investment of energy

to enhance the size and thickness of the coenenchyma. These ndings

reveal that the two measures employed in this study (colony area and

number of polyps) are equally important and should both be considered

to assess colony growth in future studies. The fact that Z. pulchellus

colonies showed an increase in polyp number during the second period

of the rst experiment might be related to variations in growth rates

among zoanthid species and the duration of the experiment. Previous

studies by Bastidas and Bone (1996) and Rabelo (2007) found that under

disturbance, P. caribaeorum displays a faster initial growth rate than

Zoanthus sociatus, which exhibits a more consistent growth rate over

time. While these ndings could align with the delayed increase in

Z. pulchellus polyp number observed by the end of the experiment,

further research into the biology and growth rates of Z. pulchellus and

P. caribaeorum is needed to conrm growth patterns in both species.

In the current climate change scenario, algal communities confront a

spectrum of challenges worldwide. In the Canary Islands, a wide range

of studies have reported declining benthic macroalgae populations over

recent decades, attributing changes in benthic community structure to

ocean warming and other anthropogenic impacts (´

Alvarez-Canali et al.,

2019; Martín-García et al., 2022; Riera et al., 2014, 2015). Previous

investigations have shown the higher resilience of zoantharians to

anthropogenic stressors, allowing them to proliferate in areas where

sedimentation, turbidity, and wastewater runoff have limited the sur-

vival of scleractinian corals and macroalgae communities (Reimer et al.,

2021). In addition, the intense overexploitation of sh resources, have

contributed to the decline of sea urchin predatory shes and a subse-

quent proliferation of D. africanum barren grounds in the Canary Islands

(Clemente et al., 2009). Consequently, the new available substrate

generated by sea urchins, or even other key herbivores, could create an

environment conducive to the proliferation and stability of thermophilic

and opportunistic organisms like zoantharians. On this basis, the future

stability of macroalgal communities in the Canary Islands rises concern,

and shifts towards habitats dominated by zoantharians could be

increasingly frequent. These mat-forming anthozoan colonies, particu-

larly species such as P. caribaeorum and Z. pulchellus, can cover large

areas, homogenizing the rocky surfaces and inducing a subsequent

reduction in substrate diversity with effects in accompanying biota

(Clemente et al., 2022; Gonz´

alez-Delgado et al., 2018).

Zoanthid-dominated ecosystems in the Canary Island have so far

demonstrated stability for several years once established in dense

populations in the substrate (Clemente et al., 2022; L´

opez et al., 2020;

Moreno-Borges et al., 2022), and not even the recurrent mass mortality

episodes of D. africanum (Clemente et al., 2014; Girard et al., 2012;

Sangil and Hern´

andez, 2022) have reverted ecosystem state to

algal-dominated systems typical of these subtropical latitudes. Probably,

available substrate provided by herbivores is crucial for the initial

establishment of zoantharians, yet their persistence in dense populations

is maintained by positive feedback mechanisms driven by the species

competitive biological traits (Acosta et al., 2001; Cen-Pacheco et al.,

2014; Costa et al., 2011; Patocka et al., 2015).

This is the rst study to assess the effects of different zoantharian-

macroalgae interactions under controlled laboratory conditions. Over-

all, our ndings revealed a declining trend in colony growth in all algae

treatments without herbivory activity, which suggested that seabeds

with high coverages of macroalgae, either erect, turf of CCA, may serve

as impediments to the proliferation of zoanthids, currently favoured by

ocean warming conditions (L´

opez et al., 2020, 2021). This dynamic is

intricately linked to the inuence of herbivory, which could facilitate

zoantharians growth by leaving free substrate as it has been observed for

other anthozoan species (Coyer et al., 1993; Edmunds and Carpenter,

2001; Maci´

a et al., 2007; Smith et al., 2006), and particularly seen in

P. caribaeorum. In this sense, our results fortify the notion that

D. africanum catalyzes not only the transition from erect macroalgal

dominance to crustose coralline dominance, as reported for decades in

the Canary Islands (Clemente et al., 2007; Hern´

andez et al., 2008b; Tuya

et al., 2004a), but also triggers a new phase shift resulting in

P. caribaeorum monopolizing the substrate and thereby reshaping

shallow rocky ecosystems. Given the thermophilic afnity of the species

and the high resilience of zoantharians to anthropogenic stressors, our

results demonstrated that P. caribaeorum could become the dominant

species in the benthic ecosystems of the Canary Islands in an ocean

warming and intense overshing scenario. Resource managers and

policy makers should prioritize attention to areas where macroalgae

cover is declining signicantly, either due to reduced water quality or

high sea urchin abundance. Implementing proactive management stra-

tegies is crucial to mitigate potential outbreaks of zoantharian pop-

ulations and subsequent disruptions to local marine ecosystems.

Funding

This study was funded by the Spanish “Ministerio de Ciencia,

Innovaci´

on y Universidades” under the program “Proyectos de I +D +i

Retos Investigaci´

on 2018

″

, supporting the project entitled “Zoantharian

benthic dominated systems: Unexplored phase-shifts in subtropical

coastal habitats under climate change conditions (ZoanSystem)" (RTI

2018-093943-A-I00). The rst author, María Elisa Lambre, was nan-

cially supported by a predoctoral contract from the Spanish “Ministerio

de Ciencia, Innovaci´

on y Universidades”, Government of Spain.

CRediT authorship contribution statement

María Elisa Lambre: Writing – original draft, Visualization, Meth-

odology, Investigation, Formal analysis, Data curation, Conceptualiza-

tion. Cataixa L´

opez: Writing – review & editing, Visualization,

Resources, Project administration, Methodology, Conceptualization.

Bel´

en Acha-Araico: Visualization, Methodology, Investigation, Data

curation, Conceptualization. Sabrina Clemente: Writing – review &

editing, Visualization, Supervision, Project administration, Funding

acquisition, Conceptualization.

Declaration of competing interest

The authors declare that they have no known competing nancial

interests or personal relationships that could have appeared to inuence

the work reported in this paper.

M.E. Lambre et al.

Marine Environmental Research 198 (2024) 106534

Data availability

Data will be made available on request.

Acknowledgement

We would like to thank Eulalia Peraza Gonz´

alez, Nuba Zamora

Jord´

an, Sonia Fern´

andez Martín and Sergio Moreno Borges for their

invaluable support in the eld, experiment setup and the aquarium

water changes. We would also like to express our gratitude to the

personnel of the Maintenance Service of the University of La Laguna for

providing sea water containers weekly throughout the experiment. Last

but not least, we extend our sincere appreciation to the anonymous re-

viewers whose invaluable insights signicantly enhanced the quality of

this manuscript.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.

org/10.1016/j.marenvres.2024.106534.

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Assessing diets of marine fauna associated with emerging zoantharian habitats in the Canary Islands

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Apr 2024
MAR BIOL

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Jan 2023

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Sep 2022
MAR ENVIRON RES

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Apr 2022
MAR ENVIRON RES

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Feb 2022

Climate change affects the shift range distribution of species, especially among mobile species, and this phenomenon can alter ecosystems and impacts human activities. Fishing is an anthropic activity that undergoes the effect not only of the introduction and increase of non-native species but also of native thermophilic ones. Some of these species can become a commercially exploitable resource. However, this information is often obscured by the negative effects these species can cause to the environment. We investigated how the thermophilic species Caranx rhonchus, neglected in Italy, could become a relevant resource. We studied the nutritional profile and the presence of heavy metal contamination and compared these traits with those of a similar common Mediterranean species, namely Trachurus trachurus. The proximate composition was determined following the AOAC procedure, while the fatty acid profile was determined by GC/MS, and the mineral component was obtained by mass spectrometer (ICP-MS). Caranx rhonchus is a nutritionally good species, although it is little consumed and exploited. Increasing the market supply with new commercially exploitable emerging species would benefit local communities and the environment. Therefore, it is necessary to investigate how a shift of the range caused by climate change can provide benefits within the human dimension.

The flourishing and vulnerabilities of zoantharians on Southwestern Atlantic reefs

Article

Full-text available

Nov 2021
MAR ENVIRON RES

In the Southwestern Atlantic reefs (SWA), some species of massive scleractinians and zoantharians are adapted to turbid waters, periodic desiccation, and sediment resuspension events. Moreover, phase shifts in this region have mostly been characterized by the emergence of algae and, less typically, zoantharians. However, nutrient excess and organic pollution are key drivers of the hard coral habitat degradation and may, thus, favor the emergence of novel zoantharian-dominated habitats. Many zoantharian species, particularly those from the genera Palythoa and Zoanthus, have traits that could help them thrive under conditions detrimental to reef-building corals, including rapid growth, several asexual reproduction strategies, high morphological plasticity, and generalist nutrient acquisition strategies. Thus, in a near future, stress-tolerant zoantharians may thrive in nutrient-enriched subtidal SWA locations under low heat stress, such as, upwelling. Overall, coral-zoantharian phase shifts in the SWA may decrease the species richness of fish and benthic communities, ultimately influencing ecosystem functioning and services, such as the provision of nursery habitats, fish biomass production, and coastline protection. However, zoantharians will also be threatened at intertidal zones, which are expected to experience higher heat stress, solar radiation, and sea-level rise. Although zoantharians appear to cope well with some local stressors (e.g., decreasing water quality), they are vulnerable to climate change (e.g., heatwaves), invasive species (Tubastraea spp.), microplastics, diseases, and mostly restricted to a narrow depth range (0–15 m depth) in SWA reefs. This shallow zone is particularly affected by climate change, compressing the three-dimensional habitat and limiting depth refugia in deeper SWA reefs. As mesophotic ecosystems have been hypothesized as short-term refuges to disturbances for some species, the narrow depth limit of zoantharians seems to be a potential factor that might increase their vulnerability to growing climate change pressures in SWA shallow-water reefs. Together, these could lead to both range expansions in some locations and loss of suitable reef habitats in other sites. Additional research is needed to better understand the systemic responses of these novel SWA reefs to the concert of increasing and interactive local and global stressors, and their implications for ecosystem functioning and service provisions.

Recurrent large-scale sea urchin mass mortality and the establishment of a long-lasting alternative macroalgae-dominated community state

Article

Full-text available

Oct 2021

Relationships between sea urchins and non-crustose macroalgae are typically non-linear, and an abrupt phase shift from a barren to a macroalgae-dominated state and vice versa happens when the sea urchin abundance exceeds a critical threshold. Here we have used two mass mortality events as a natural experiment to study progressive changes and dynamics between these stable states. In 2009-2010 and 2018 two mass mortalities decimated the populations of the sea urchin Diadema africanum in the Canary Islands (Eastern Subtropical Atlantic). In these islands, this sea urchin is a key-herbivore controlling the growth of macroalgae, and sea urchin barrens have persisted for more 60 years. Mass mortality events differed in intensity both in space and time, and two phase shifts from sea urchin barrens to macroalgal beds were detected in both when sea urchin density declined below a critical threshold of 4 indv. · m-2. The first mass mortality was greater in La Palma Island, consequently in this island a long-lasting alternative state dominated by non-crustose macroalgae has been established. Subsequently a recurrent mass mortality also favoured the transition from the sea urchin barrens to non-crustose macroalgal beds in Tenerife Island. After mass mortalities D. africanum populations were reduced by 94-98% in both islands. No signs of recovery of these populations have been identified after phase shifts; ecosystem feedbacks may be the cause of the low population density of D. africanum.

Tropicalization of temperate ecosystems in North America: The northward range expansion of tropical organisms in response to warming winter temperatures

Article

Full-text available

Mar 2021

Tropicalization is a term used to describe the transformation of temperate ecosystems by poleward‐moving tropical organisms in response to warming temperatures. In North America, decreases in the frequency and intensity of extreme winter cold events are expected to allow the poleward range expansion of many cold‐sensitive tropical organisms, sometimes at the expense of temperate organisms. Although ecologists have long noted the critical ecological role of winter cold temperature extremes in tropical‐temperate transition zones, the ecological effects of extreme cold events have been understudied, and the influence of warming winter temperatures has too often been left out of climate change vulnerability assessments. Here, we examine the influence of extreme cold events on the northward range limits of a diverse group of tropical organisms, including terrestrial plants, coastal wetland plants, coastal fishes, sea turtles, terrestrial reptiles, amphibians, manatees, and insects. For these organisms, extreme cold events can lead to major physiological damage or landscape‐scale mass mortality. Conversely, the absence of extreme cold events can foster population growth, range expansion, and ecological regime shifts. We discuss the effects of warming winters on species and ecosystems in tropical‐temperate transition zones. In the twenty‐first century, climate change‐induced decreases in the frequency and intensity of extreme cold events are expected to facilitate the poleward range expansion of many tropical species. Our review highlights critical knowledge gaps for advancing understanding of the ecological implications of the tropicalization of temperate ecosystems in North America.

Climate‐driven impacts of exotic species on marine ecosystems

Article

Full-text available

Mar 2021
GLOBAL ECOL BIOGEOGR

Aim Temperature is fundamental to the physiological and ecological performance of marine organisms, but its role in modulating the magnitude of ecological impacts by exotic species remains unresolved. Here, we examine the relationship between thermal regimes in the range of origin of marine exotic species and sites of measured impact, after human‐induced introduction. We compare this relationship with the magnitude of impact exerted by exotic species on native ecosystems. Location Global. Time period 1977–2017 (meta‐analysis). Major taxa studied Marine exotic species. Methods Quantitative impacts of exotic species in marine ecosystems were obtained from a global database. The native range of origin of exotic species was used to estimate the realized thermal niche for each species and compared with the latitude and climatic conditions in recipient sites of recorded impact of exotic species. The difference in median temperatures between recipient sites and the thermal range of origin (i.e., thermal midpoint anomaly) was compared with the magnitude of effect sizes by exotic species on native species, communities and ecosystems. Results Recorded impacts occurred predominantly within the thermal niche of origin of exotic species, albeit with a tendency toward higher latitudes and slightly cooler conditions. The severity of impacts by exotic species on abundance of native taxa displayed a hump‐shaped relationship with temperature. Peak impacts were recorded in recipient sites that were 2.2°C cooler than the thermal midpoint of the range of origin of exotic species, and impacts decreased in magnitude toward higher and lower thermal anomalies. Main conclusions Our findings highlight how temperature and climatic context influence ecological impacts by exotic species in marine ecosystems and the implications for existing and novel species interactions under climate change.

Widespread Zoanthus and Palythoa Dominance, Barrens, and Phase Shifts in Shallow Water Subtropical and Tropical Marine Ecosystems

Chapter

Sep 2021

Effects of macroalgae and sea urchin grazing pressure on zoantharians growth under laboratory conditions

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