Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Towards reef restoration in Zihuatanejo, Guerrero,

México: lessons learned

Héctor Nava 1*; https://orcid.org/0000-0003-0419-6840

Antonio González-Rodríguez 2; https://orcid.org/0000-0002-6196-7288

Nemer E. Narchi 3; https://orcid.org/0000-0002-3508-3913

Ana Crisol Méndez-Medina 3; https://orcid.org/0000-0002-0761-5791

Yurixhi Maldonado-López 4; https://orcid.org/0000-0003-0161-1789

María Angeles Cárdenas-Alvarado2; https://orcid.org/0000-0002-0121-4508

Antonieta Gina Figueroa-Camacho 1; https://orcid.org/0000-0002-9459-6161

Huran Tonalli Drouet-Cruz 5; https://orcid.org/0000-0003-2080-5132

Néstor Corona-Morales 3; https://orcid.org/0000-0001-5511-2518

1. Instituto de Investigaciones sobre los Recursos Naturales, Universidad Michoacana de San Nicolás de Hidalgo,

Morelia, Michoacán, México; hector.nava@umich.mx (*Correspondence), a.ginafigueroa@gmail.com

2. Instituto de Investigaciones en Ecosistemas y Sustentabilidad, Universidad Nacional Autónoma de México, Morelia,

Michoacán, México; agrodrig@cieco.unam.mx, mcardenas@cieco.unam.mx

3. Centro de Estudios en Geografía Humana, El Colegio de Michoacán, La Piedad de Cabadas, Michoacán, México;

narchi@colmich.edu.mx, crisolmm@gmail.com, corona@ecolmich.edu.mx

4. Consejo Nacional de Ciencia y Tecnología-Instituto de Investigaciones sobre los Recursos Naturales, Universidad

Michoacana de San Nicolás de Hidalgo, Morelia, Michoacán, México; yurixhimaldonado@gmail.com

5. Systems Ecology and Resource Management Research Unit, Université Libre de Bruxelles; htdrouet.cruz@gmail.com

Received 05-IX-2022. Corrected 07-I-2023. Accepted 19-I-2023.

ABSTRACT

Introduction: Coral reef structures in Zihuatanejo, Guerrero are well-preserved. The coverage of living corals,

near 60 % at several locations, makes them comparable to other coral reefs in the states of Oaxaca, Jalisco, and

Nayarit and with high potential to promote their conservation.

Objective: To present the outcome of 12 years of research in coral communities from Zihuatanejo, Guerrero, as

a justifying argument for the current conservation efforts in the area.

Methods: We developed a baseline on the conservation status of the reef structures, bioerosion processes and the

source of major natural and anthropogenic impacts. We assessed the genetic diversity of the coral zooxanthellae

symbionts, the outcome of a technique of coral transplantation to recover the coverage of living corals and the

local ecological knowledge to involve local inhabitants to promote conservation.

Results: At least five coral reefs remain exposed to a medium-low level of impact by bioerosion and anthropiza-

tion. Coral transplantation experiments made in the area showed records of transplant survival nearing 90 %.

Although the warming of the sea surface temperature that occurred during the El Niño of 2015-2016 caused

coral bleaching and mortality in several coral populations in this area, there were no affectations attributed to this

phenomenon in other locations. This response was not related to the level of exposure to anthropogenic impacts,

and the presence of thermal resistant zooxanthellae was assessed using molecular tools, confirming the existence

of zooxanthellae of the genus Durusdinium. The analysis of local ecological knowledge of the inhabitants of

Zihuatanejo showed that they keep elaborate knowledge on the ecology of coral reefs. This is complemented with

scientific knowledge that will encourage community participation in conservation strategies.

https://doi.org/10.15517/rev.biol.trop..v71iS1.54792

SUPPLEMENT

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

INTRODUCTION

The eastern tropical Pacific has subopti-

mal oceanographic conditions for coral com-

munity development (Glynn & Ault, 2000).

The Mexican Pacific coast is a region with high

primary productivity enhanced by the nutrient

enrichment coming from riverine discharge,

upwelling currents, and a high seasonal tem-

perature variability jointed with high turbidity

of the water column that difficult coral survival

(Reyes-Bonilla, 2003). The development of

human settlements near coral communities

also has exerted negative impact through the

discharge of sewage, solid waste, and land

transformation, causing coastal erosion and

enhancing the sedimentation rate at some sites

harboring corals (Nava & Ramírez-Herrera,

2012). Added to these anthropized conditions

is the impact of the El Niño phenomenon,

which in the last decades has decimated entire

populations of reef corals at some localities in

this region (Nava et al., 2019). Some of these

impacts, chronic and silent, exceptional or dev-

astating, have occurred without being recorded

in detail. This is not the case with the coral

communities from Zihuatanejo, which remain

among the most conserved on the Mexican

Conclusions: A long-term multidisciplinary strategy is required for coral reef conservation that encompasses: 1)

assessing the role of the overall holobiont in the thermal resistance of corals from this area and 2) establishing

restoration strategies of coral reefs that include the local knowledge about marine ecology, for the establishment

of coral reef protection and management schemes put in place by local inhabitants.

Key words: Pocillopora; restoration; Mexican Pacific; citizen science; coral reefs.

RESUMEN

Hacia la restauración arrecifal en Zihuatanejo Guerrero, México: lecciones aprendidas.

Introducción: Los arrecifes coralinos de Zihuatanejo Guerrero están bien conservados. La cobertura de corales

vivos, cerca del 60 %, los hace comparables a otras comunidades coralinas presentes en Oaxaca, Jalisco y Nayarit

y con un alto potencial para promover su conservación.

Objetivo: Presentar los resultados de 12 años de investigación en las comunidades coralinas de Zihuatanejo,

Guerrero, como un argumento que justifica los esfuerzos actuales de conservación en el área.

Métodos: Desarrollamos una línea base del estado de conservación de la estructura arrecifal, los procesos de

bioerosión y las fuentes principales de impactos naturales y antropogénicos. Evaluamos la diversidad genética de

los simbiontes zooxantelados de los corales, el resultado de una técnica de trasplante de corales para recuperar

la cobertura de corales vivos y el conocimiento ecológico local para desarrollar estrategias de conservación con

participación local.

Resultados: Cinco de esas comunidades coralinas permanecen expuestas a un nivel de impacto medio a bajo por

bioerosión y antropización. Los experimentos de trasplante de corales en el área mostraron una supervivencia

cercana al 90 %. Aunque el calentamiento de la temperatura superficial del mar ocurrido durante el evento El

Niño 2015-16 causó blanqueamiento y mortalidad coralina en algunas poblaciones de corales del área, no hubo

afectaciones atribuidas a este fenómeno en otras. Esta respuesta no se relacionó con el nivel de exposición a

impactos antropogénicos y la presencia de poblaciones de zooxantelas fue examinada usando herramientas

moleculares, confirmando la existencia de una población del género Durusdinium. El análisis del conocimiento

ecológico local de los habitantes de Zihuatanejo mostró que estos resguardan conocimientos complejos sobre

la ecología de las comunidades coralinas. Este conocimiento es complementario al conocimiento científico y

servirá para promover estrategias de participación ciudadana en la conservación de las comunidades coralinas.

Conclusiones: Se requiere una estrategia multidisciplinaria de largo plazo para la conservación de las comu-

nidades coralinas que incluya: 1) examinar el papel del holobionte completo en la resistencia térmica de los

corales de esta área y 2) establecer estrategias de restauración en arrecifes coralinos que incluyan el conocimiento

ecológico local para el establecimiento de esquemas de protección y manejo de los arrecifes coralinos a cargo

de los habitantes locales.

Palabras clave: Pocillopora; restauración; Pacífico mexicano; ciencia ciudadana; arrecifes coralinos.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

central Pacific coast. These communities vary

in their extension and structural characteristics,

but all have provided relevant life support sys-

tems to the inhabitants of the municipality of

Zihuatanejo de Azueta for 400 years (Sánchez-

Briones, 2010). Since that time, the activity of

traditional fishing has been part of the identity

of the inhabitants of this municipality and the

region (Reyes-García, 2012). Since the decade

of 1980, Playa las Gatas has been an important

tourist destination in Zihuatanejo, allowing

the establishment of several service providers

offering lodging, food, and recreational ser-

vices. The first studies of the conservation state

of five locations with coral communities in the

area began in 2009, which are Islote Zacatoso,

Playa las Gatas, Caleta de Chon, Playa Man-

zanillo, and Playa Riscalillo (Fig. 1). Such

studies provided relevant information about

the environmental conditions of each site,

suggesting that these communities are under

pressure of anthropogenic origin (Nava &

Ramírez-Herrera, 2012). Data on the coverage

of living corals and their ratio concerning dead

coral substrata have evidenced the presence of

locations with reef patches with an acceptable

conservation status (Nava & Ramírez-Herrera,

2012; Nava et al., 2019; Nava et al., 2021).

These data suggest such communities present a

high potential to develop restoration initiatives.

Assuming the process of sponge bioerosion as

an indicator of the conservation state of the

reef ecosystem, the survey of boring sponge

abundance in reefs from Zihuatanejo revealed

that bioerosion may weaken the reef framework

in locations with high cover of dead corals

(Nava et al., 2019). Previous tests of a reliable

and low-cost strategy for coral transplantation

on rocky substrata showed to be effective and

that it can be used by local inhabitants at sites

with reduced coral coverage. Nonetheless, the

impact of the event of the El Niño of 2015-16

showed that it is necessary to implement a mul-

tidisciplinary strategy to restore the coverage

with living corals resistant to thermal stress

(Cárdenas-Alvarado et al., 2021). The algal

Fig. 1. Detail of the study area and coral communities in Zihuatanejo, Guerrero. A. location of the sites in the study area,

B. coral reef in Islote Zacatoso, C. coral community of Playa las Gatas and D. coral bleaching of Playa Manzanillo during

the El Niño 2015-16. Images: Héctor Nava.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

symbionts of corals (Symbiodiniaceae) are

relevant since they provide corals with nutri-

ents and oxygen and allow them to increase

their calcification rate (Muller-Parker et al.,

2015). Since Cladocopium and Durusdinium

are the most tolerant genera to high seawater

temperatures (Baker et al., 2004; LaJeunesse

et al., 2018), we aimed to test if the identity

of algal symbionts may influence the response

of coral bleaching in Zihuatanejo and now are

attempting restoration emerging from a citizen

science approach. Recent research has demon-

strated that local inhabitants are owners of their

elaborated ecological knowledge that is used to

manage natural resources from coral communi-

ties (Drouet-Cruz, 2020). Current efforts aim at

integrating all available information to sustain

strategic alliances among academic, citizen,

and government agencies to develop restoration

initiatives based on the participation of local

inhabitants that promote coral communities

restoration with thermally resistant reef corals.

This contribution provides an analysis of the

outcome of this work in process and proposes

an approach to establish a long-term initiative

for the conservation of coral communities from

Zihuatanejo, Guerrero.

MATERIALS AND METHODS

Study area: The municipality of Zihua-

tanejo de Azueta is located at 17° 37’ - 17°

41’N and 101° 31’ - 101° 39’ W. Throughout

the coast, there are abrupt rocky formations

alternated with sandy beaches with variable

slopes. The most evident landforms are head-

lands, cliffs, coves, islets, estuaries, and a

coastal lagoon. The bottom substrate type var-

ies according to the geographic orientation and

it is divided into two main areas: the upper

northwest, where rocky outcrops dominate

with a cover approximately 70 %, and the lower

southeast, covered mainly by sandy bottoms,

reaching an 80 %. Along this area there are

distinct locations with relevant coral communi-

ties whose distribution varies from very shal-

low areas to more than 20 m in depth. Some

of these locations are Islote Zacatoso, Playa las

Gatas, Caleta de Chon, Playa Manzanillo, and

Playa Riscalillo (Fig. 1).

Islote Zacatoso (17° 39’ 13.2” N and

101°37’ 13.3” W) is an islet located 1 km

southwestward to the Ixtapa Zihuatanejo vil-

lage. There is a monospecific fringing reef,

located at the islet area protected from the

surge, that spreads out from 1 m to near 6 m

in depth. It is mainly composed by Pocillopora

damicornis, and P. verrucosa, although other

species, like P. capitata, Pavona gigantea and

Porites lobata are also present. This reef seems

to be well conserved. The access to this site is

only with boats and the use of the reef includes

low-impact artisanal fishing and non-intensive

recreational scuba diving (only few scuba agen-

cies bring a reduced amount of scuba divers to

visit the reef each week).

Playa las Gatas (17° 37’ 16.8” N and 101°

33’ 8.55” W) is inside the Zihuatanejo Bay. The

coral community in this area is mainly com-

posed by colonies of the genera Pocillopora,

Pavona, and Porites, growing over a substra-

tum composed by boulders that can reach 2

m in diameter and distributed between 3 and

6 m in depth. Since more than three decades

ago, these corals have been exposed to strong

anthropogenic pressure by locals and tourists

(mainly boat anchoring, touching corals and

domestic sewage discharge). Nowadays, this

coral community presents the lowest cover of

living corals.

Caleta de Chon (17° 36’ 52.8” N and

101° 33’ 16.3” W) harbors a fringing reef that

extends from 1 m to near 7 m in depth and is

composed of reef corals of the genera Pocil-

lopora and Pavona that build a reef framework

of more than 1 m in height. To date, this reef

presents one of the highest covers of living

corals in Zihuatanejo and spreads out parallel

to the shoreline at the head of the cove. This

impact comes from the construction of roads

and buildings near the cove that have caused

land erosion at least during the last 10 years.

The main access to this site is by boat, but the

opening of roads allows the access of visitors

by land.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Playa Manzanillo and Playa Riscalillo (17°

37’ 11.4” N, 101° 31’ 27.6” W and 17° 37’

0.7” N, 101° 31’ 3.5” W) are areas close to

each other, with monospecific fringing reefs

that spread out from the surface level to 6 m

in depth. Until the event of the El Niño of

2015-16, both reefs were the best preserved in

the area. To date, the reef of Playa Riscalillo

is highly damaged, although both reefs are far

from inhabited sites and access is mainly by

boat; the only human activities at the sites are

snorkeling, scuba diving, and artisanal fishing.

Baseline study of the conservation sta-

tus of coral reefs: The coverage of the major

components of the substrata was recorded by

the Marine Biodiversity Laboratory of the

Universidad Michoacana de San Nicolás de

Hidalgo. Coverage of live corals (LC), dead

coral framework (DC), algae, sand, and rocks

was quantified using 20m-long photo-transects

(five transects in 2010, three transects in 2015

and 2018) recording the proportion (%) cov-

ered by each category in ten photo-quadrants

of 1m2 per transect. Each image was analyzed

with CPCe (Coral Point Count with Excel

extensions) software developed by the National

Coral Reef Institute (FL, USA), using 100

random dots. To assess the conservation status

of each coral reef, the coral mortality index

(CMI) (Gómez et al., 1994) was used. This

index is based on the ratio between the cover-

age of living and dead corals, and values near

zero indicate a dominance of living corals (well

conserved coral reef) and values near 1 indi-

cate a dominance of dead corals (deteriorated

coral reef):

The environmental conditions were char-

acterized in each site recording the sedimenta-

tion rate using sediment collecting bottles (n

= 6) and the transparency of the water column

using the Secchi disk method (n = 3). The con-

centration of total suspended solids (mg·l-1, n

= 3) and chlorophyll in the water column were

measured in samples of 3l of seawater (mg·m3,

n = 3). The records of 𝛿15N and 𝛿13C in samples

of dried Amphiroa sp. (n = 5) because were

taken due both parameters are indicators of

terrestrial sources of nitrogen and carbon (see

Nava et al., 2014 for more details).

Assessment of the sponge bioerosion in

the reef framework: The species richness and

abundance of boring sponges were recorded at

each coral reef collecting 9 cm3 coral fragments

of three types of substrata: living corals (n =

25), dead corals (n = 25), and coral rubble (n

= 25) developed by Pocillopora sp. along a 50

m long transect and replicating this sampling

in three transects. Each coral fragment was

broken into small pieces and revised with a

stereoscope to locate tissue of boring sponges

inside the fragment. Small samples of sponge

tissue were digested with sodium hypochlorite

and observed in an optic microscope to con-

firm the presence of boring species. The total

abundance was recorded as the proportion (%)

of all 75 fragments collected per transect and

containing boring sponges, averaged from the

tree replicates (mean ± standard deviation).

The abundance of boring sponge per substrate

type was recorded as the proportion (%) of

the 25 fragments collected per transect and

containing boring sponges, averaged from the

three replicates (mean ± standard deviation)

(Nava et al., 2014).

Experimental test of the transplanta-

tion technique of living coral fragments: The

experimental technique for transplanting living

corals was implemented in Playa las Gatas, a

site with low coverage of living corals (~ 4 %)

and abundant rocky boulders (57 %), as well as

high content of loose fragments growing on the

sand, considering these as an opportunity to be

used as transplants (Table 1, Fig. 1C). This study

assessed two treatments of transplantation of

living corals (Fig. 2): 1) using freshly dislodged

coral fragments 10 cm long, without signs of

healing in their fractured section (named coral

fragments) and 2) using loose coral fragments

of the same size that already healed the damage

suffered during the dislodgement (named loose

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

coral colonies). Such discrimination was taken

into account assuming that coral fragments will

show a faster fixation to the rocky substrata due

to their activated process of regeneration of the

fractured section. Likewise, we also evaluated

the possible effect of environmental seasonali-

ty, starting the first experiment at the beginning

of the rainy season and a second experiment

at the beginning of the dry season. All corals

from both treatments were transplanted onto

the surface of rocky boulders using steel grids

of 60 cm per side, with square division of 15

cm, which were tied with 12-gauge wire to five

boulders for each treatment. A total of 25 coral

transplants were established on the surface of

each boulder, immobilizing them below the

grid intersections and tying them with plastic

zip ties (Fig. 2). The mean proportion (%)

of these 25 transplants fixed on the rock was

recorded quarterly for 12 months. The growth

TABLE 1

Record of the coverage of major substrata components and coverage of living corals

in the coral communities of Zihuatanejo, Guerrero.

LC BC PC DC CR FA RO SN CMI

2010 (n = 5) Islote Zacatoso 65.85 0.00 0.00 12.04 6.92 5.10 13.76 4.86 0.16

16.86 0.00 0.00 5.33 3.28 3.46 7.30 5.04 0.09

Playa las Gatas 8.00 0.00 0.00 15.13 9.30 6.00 61.71 9.85 0.68

6.10 0.00 0.00 1.94 5.07 4.34 5.97 2.87 0.15

Caleta de Chon 61.11 0.00 0.00 13.87 8.95 6.78 16.64 8.23 0.19

12.74 0.00 0.00 8.58 1.54 5.30 6.76 9.88 0.12

Playa Manzanillo 54.95 0.00 0.00 29.49 11.36 19.06 7.56 6.03 0.35

14.34 0.00 0.00 11.62 4.83 12.90 5.33 3.06 0.15

Playa Riscalillo 77.23 1.01 0.00 8.27 2.60 5.64 11.48 1.79 0.10

15.68 2.26 0.00 6.41 1.10 4.26 9.94 1.13 0.09

2015 (n = 3) Islote Zacatoso 52.24 0.00 27.44 2.71 5.09 5.61 6.90 0.00 0.03

35.74 0.00 35.23 1.07 3.98 9.72 5.25 0.00 0.01

Playa las Gatas 0.37 31.89 1.97 0.74 5.91 0.08 49.64 9.40 0.02

0.65 20.98 2.93 0.58 2.15 0.14 15.13 7.20 0.01

Caleta de Chon 58.13 0.27 0.00 5.51 7.20 2.99 25.73 0.18 0.09

5.09 0.46 0.00 4.81 4.57 5.17 9.32 0.31 0.07

Playa Manzanillo 0.49 9.63 40.09 30.26 13.11 0.00 5.94 0.48 0.43

0.84 15.44 27.09 14.36 11.99 0.00 7.64 0.49 0.32

Playa Riscalillo 0.00 28.76 42.91 17.13 0.33 0.00 10.87 0.00 0.20

0.00 13.21 26.85 11.82 0.57 0.00 4.12 0.00 0.15

2018 (n = 3) Islote Zacatoso 79.93 0.00 0.00 3.82 3.33 1.42 12.92 0.00 0.05

12.46 0.00 0.00 2.48 3.25 2.45 7.42 0.00 0.03

Playa las Gatas 0.50 0.00 0.00 15.00 20.73 5.00 56.08 7.02 0.94

0.50 0.00 0.00 8.66 12.26 3.61 24.61 4.39 0.09

Caleta de Chon 82.33 0.00 0.00 0.73 2.00 0.00 13.18 1.75 0.01

8.19 0.00 0.00 1.27 2.00 0.00 8.09 2.22 0.01

Playa Manzanillo 62.65 0.00 0.00 22.75 2.42 10.25 11.43 1.00 0.33

10.03 0.00 0.00 12.76 1.46 9.50 7.81 1.00 0.02

Playa Riscalillo 24.42 0.00 0.00 59.17 0.50 25.17 16.08 0.33 0.67

23.07 0.00 0.00 36.11 0.87 18.11 13.13 0.58 0.35

LC = living corals, BC = bleached corals, PC = pale corals, DC = dead corals, CR = coral rubble, FA = filamentous algae,

RO = rocks, SN = sand, and CMI = coral mortality index. In bold: the mean proportion (%). In cursives: standard deviation.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

of transplants was also measured with a 30 cm

metal ruler as the increase of the maximum

diameter in the vertical (mean vertical growth)

and horizontal (mean horizontal growth) planes

considering their original size as 100 %. The

mean proportion of survival of transplants

(%) was recorded as the proportion of the 25

transplants that still remained alive during

each sampling.

Assessment of the genetic diversity of

algal symbionts (Symbiodiniaceae) in coral

populations of Zihuatanejo, Guerrero: The

Laboratory of Genetics for Conservation of

the Institute of Research in Ecosystems and

Sustainability of the National Autonomous

University of Mexico coordinates this line of

research. We evaluated the composition and

the genetic diversity of the populations of algal

symbionts in four coral communities in the

area (Islote Zacatoso, Playa Las Gatas, Caleta

de Chon, and Playa Riscalillo) after the event

of El Niño of 2015-2016. We obtained DNA of

102 coral fragments of Pocillopora verrucosa,

which were randomly sampled between 4 and

12 m in depth in each site during January and

June 2018. Total DNA was extracted using the

Invitrogen PureLink™ Genomic DNA Mini

Kit following the manufacturer’s instructions

with slight modifications (Cárdenas-Alvarado

et al., 2021). Afterwards, a fragment of the

28S ribosomal RNA gene and a fragment of

the Internal Transcribed Spacer 2 (ITS2) of

the ribosomal RNA genes were amplified with

the primer pairs designed by Tong et al. (2018)

and by Appril and Gates (2007), respectively.

To determine the identity of zooxanthellae, we

constructed two phylogenetic trees with the

Fig. 2. Detail of coral transplant experiments in Playa las Gatas. A. loose coral colonies at the beginning of the experiment,

B. after 13 months, C. coral fragments at the beginning of the experiment and D. after 13 months.

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

sequences of the 28S and ITS2 regions from

this study and the different genera of Symbio-

diniaceae from GenBank. The genetic diversity

of zooxanthellae for each reef was calculated

with haplotype diversity (h) and nucleotide

diversity (π).

Record of the local ecological knowl-

edge: Understanding local knowledge and per-

ception is especially relevant when promoting

citizen participation in conservation efforts as

local ideas of ecosystem functioning are valu-

able sources of useful long-duration data points

that serve as the blueprints for participatory

conservation plans. For this reason, this project

stands on methodologies recording the local

knowledge rigorously and systematically and

the CoLaboratories of Social Oceanography

of the El Colegio de Michoacán is working

towards this goal. Qualitative social data used

to record and analyze local ecological knowl-

edge of corals and coral reefs were obtained

through a mixed methods approach. Firstly,

to assess the collective perception about the

composition and diversity of the coral com-

munity we used free listing. This technique is a

simple and easy way to obtain and systematize

empirical data (Quinlan, 2005) and is gener-

ally used to identify elements of a cultural

domain (e.g., fish species) (Smith et al., 1995).

A second component of our mixed methods

was an ethnographic approach based on col-

loquial conversations and unstructured inter-

views. This approach allowed interaction with

more than eighteen individuals representing

the fishing, tourism, and governmental sectors

in Zihuatanejo. The interactions were recorded

as notes and these, in turn, were transformed

into a field log (Bernard, 1995). The starting

point, Drouet-Cruz’s work (2020), is now mov-

ing forward by fostering characterization of

the sociopolitical context. By accounting the

connections among different actors and power-

ful groups that have access to the coral reef,

we look to foster new collaborative strategies

to protect coral communities and manage their

diversity. Understanding the social, political,

and economic context will allow for designing

strategies of citizen participation that can be

strengthened and appropriated by the people

of the Azueta municipality. The strategies that

this project considers 1) to include a diversity

of local actors and deep knowledge about the

biology and ecology of corals, 2) to incentiv-

ize dialogue and exchange among local and

scientific knowledge, to generate a common

language that facilitates collaboration, 3) to

make available to local stakeholders the techni-

cal information, that allows them to participate

in tasks destined to restore and monitor the

coral communities, 4) to encourage the creation

of collaborative networks among all actors, to

implement actions that preserve these coral

communities, and 5) to incentivize the proposal

of new local initiatives for this purpose. In this

way, we expect that this initiative can endure.

Data analysis: Both environmental and

biological data were tested for normality

and homogeneity of variances (Kolmogorov

Smirnov test). In the case of data not normally

distributed, they were square-root transformed.

A series of separate one-way analyses of vari-

ance (ANOVA) were conducted on the environ-

mental and biological parameters to determine

significant differences in the coverage of sub-

strata and abundance of boring sponges. The

effectiveness between transplantation tech-

niques were determined with two-way analysis

of variance (ANOVA) with repeated measures,

in which the replication factor was the sam-

pling periods and the independent factor was

each parameter measured (proportion of trans-

plant fixation, growth, and survival among

either seasons, locations and treatments).

RESULTS

The conservation state of the coral reefs

from Zihuatanejo: The data provided from

this study in 2010 confirmed the existence of

locations with a relevant coverage of living cor-

als, being high in almost all locations (between

54.95 ± 14.34 % and 77.23 ± 15.68 %) with the

exception of Playa las Gatas, where the cover

of living corals was the lowest (8.00 ± 6.10 %)

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

(F = 15.619, P < 0.001). The cover of dead

corals was low at almost all locations (between

8.27 ± 6.41 % and 15.13 ± 1.94 %) with excep-

tion of Playa Manzanillo (29.49 ± 11.62 %) (F

= 5.817, P < 0.005). The lowest record of CMI

(0.10 ± 0.09) was made at the most preserved

sites and the highest record of CMI was found

in Playa las Gatas, the closest site to the human

settlements (0.68 ± 0.15) (F = 17.862, P <

0.001, Table 1). Some of the symptoms of envi-

ronmental degradation during 2010 were high

rates of sedimentation in Playa Riscalillo (1.57

± 0.27 kg·m-2 d-1) and high levels of d15N and

low water transparency in Islote Zacatoso (9.49

± 0.43 and 7.46 ± 1.99 m, respectively) as well

as high levels of d13C and a high chlorophyll

concentration for Playa las Gatas (up to -13.25

± 0.67 and 1.82 ± 0.86 mg m-2 d-1) (Table 2).

Boring sponge abundance: A total of

12 species of boring sponges belonging to the

genera Cliona, Pione, Siphonodictyon, and

Thoosa were recorded at the study area. Among

all sites, Caleta de Chon (59.9 ± 11.2 %) was

the most affected site by sponge bioerosion

and Playa Manzanillo (23.2 ± 4.9 %) showed

the lowest abundance of boring sponges (F

= 12.170, P < 0.001). The dead corals were

the most invaded substrata by boring sponges

(63.72 ± 25.165) and living corals were the less

affected (25.12 ± 12.69 %) (F = 34.982, P <

0.001), with the highest records in Playa Risca-

lillo and Caleta de Chon (up to 86 ± 19.8 %)

(F = 4.567, P < 0.01). The substrata composed

by living corals showed the highest invasion by

boring sponges in Caleta de Chon (up to 32.8

± 7.2 %) in comparison to Playa las Gatas and

Playa Manzanillo (up to 12.8 ± 7.6 %) (F =

4.359, P < 0.01, Fig. 3).

TABLE 2

Averaged record (mean ± standard deviation) of sedimentation rate (Sed), water transparency (Trans), total suspended solids

(TSS), chlorophyll concentration (Cla), levels of d15N, and d13C recorded at Islote Zacatoso (IZ), Playa las Gatas (PG),

Caleta de Chon (CC), Playa Manzanillo (PM), and Playa Riscalillo in 2010*

Sed

(kg m-2 d-1) n = 6

Trans

(m) n = 3

Cla

(mg · m-3) n = 3

TSS

(mg · l-1) n = 3

d15N

n = 5

d13C

n = 5

IZ 1.03 ± 0.49 7.46 ± 1.99 0.79 ± 0.11 23.69 ± 9.85 9.49 ± 0.43 -14.55 ± 0.63

PG 0.48 ± 0.19 3.71 ± 0.70 1.82 ± 0.86 18.74 ± 11.57 9.23 ± 0.50 -13.25 ± 0.67

CC 1.23 ± 0.27 5.45 ± 0.95 0.71 ± 0.43 34.75 ± 6.60 9.35 ± 0.47 -14.44 ± 0.70

PM 0.71 ± 0.14 5.97 ± 1.90 0.27 ± 0.11 32.35 ± 9.53 8.38 ± 0.53 -15.67 ± 0.97

PR 1.57 ± 0.27 6.13 ± 1.70 0.58 ± 0.07 27.43 ± 11.97 8.84 ± 0.34 -14.07 ± 1.06

* Modified from Nava et al., 2014.

Fig. 3. Average abundance of boring sponges per locality and by each type of coraline substrata. ZA = Islote Zacatoso, LG =

Playa las Gatas, CC = Caleta de Chon, PM = Playa Manzanillo, PR = Playa Riscalillo, LC = living corals, DC = dead corals,

and CR = coral rubble. Bars above the columns indicate the standard deviation.

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Experiences in coral transplantation:

During the dry season, the fixation of coral

transplants was faster in coral fragments (98.00

± 4.0 % in 9 months) in comparison to the loose

coral colonies (86.43 ± 18.86 % in 12 months)

(F = 6.258 P < 0.05), putatively caused by the

environmental stability. The vertical and hori-

zontal growth of coral fragments were almost

twice as large (161.18 ± 68.87 % and 106.80

± 24.45 %, respectively) as in the loose coral

colonies (88.29 ± 32.12 % and 72.94 ± 7.58

%, respectively) (F = 8.035, P < 0.05 and F =

15.274, P < 0.05, Fig. 4). Survival at the end of

the experiment made during the dry season was

higher in coral fragments than in loose coral

colonies (90.98 ± 6.48 % vs. 62.80 ± 43.42 %)

(F = 3.061, P < 0.05). During the rainy season,

the maximum fixation occurred after 8 months

Fig. 4. Temporal variation of the fixation success, the vertical and horizontal growth, and survival of coral transplants

recorded in the treatment of coral fragments (black columns) and loose coral colonies (gray columns) throughout 13 months

and started during the rainy and dry seasons. Vertical lines represent the standard deviation. Taken from Nava & Figueroa-

Camacho (2017).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

in coral fragments (89.27 ± 7.18 %), contrast-

ing the record made in loose coral colonies,

whose maximum record was made only after

11 months (84.46 ± 13.09 %) (F = 20.489,

P < 0.05, Fig. 4). The vertical and horizontal

growth were higher in coral fragments (209.63

± 43.65 % and 107.26 ± 25.75 %) than in loose

coral colonies (124.33 ± 15.83 % and 99.98 ±

19.74 %) (F = 25.532, P < 0.05 and F = 32.135,

P < 0.05, respectively). At the end of the experi-

ment of the rainy season, survival diminished

in both treatments, but it was higher in coral

fragments in comparison with loose coral colo-

nies (62.95 ± 42.78 % vs. 45.65 ± 53.19 %) (F

= 5.272, P < 0.05, respectively, Fig. 4).

Impact of the El Niño 2015-16 event:

During the conclusion of the transplantation

experiments, we witnessed the development of

the El Niño event of 2015-16. This phenom-

enon reached a level of 2.9 on the Oceanic

El Niño Index (ONI) and a lethal level of 8.5

of stress by warming in corals throughout 12

weeks (DHW), causing one of the strongest

impacts of this phenomenon in the last decades

(Fig. 5). As a result, corals in Zihuatanejo,

Guerrero were exposed to thermal stress for

almost 13 months. In June 2015, we recorded

major changes in coral reefs as the presence

of pale corals in almost all sites (up to 27.44

± 35.23 %) with exception of Caleta de Chon.

The presence of bleached corals was moderate

at Playa Mazanillo, Playa Riscalillo and Playa

las Gatas (up to 31.89 ± 20.89 %) but almost

or totally absent at Islote Zacatoso and Caleta

de Chon (up to 0.27 ± 0.46 %), although their

coverage seemed to be similar among locations

(F = 3.246, P = 0.08 and F =1.547, P = 0.276,

respectively). In 2018, the cover of dead corals

increased almost sixfold in Playa Riscalillo

(59.17 ± 36.11 %) in comparison to its previ-

ous records (F = 6.666, P < 0.05, Table 2).

The coverage of living corals was also reduced

significatively through de time, especially in

comparison to 2010 (24.42 ± 23.07 % vs. 77.23

± 15.68 %) (F = 6.520, P < 0.05) and the sig-

nificant change in the CMI confirmed that the

conservation state at this locality in 2018 was

the most reduced since 2010 (0.67 ± 0.35 vs.

0.10 ± 0.09) (F = 7.762, P < 0.05).

Genetic diversity of zooxanthellae in

coral populations of Zihuatanejo Guerrero:

The results of the phylogenetic trees obtained

Fig. 5. Monthly variation of the Degree Heating Weeks (DHW) and the Oceanic El Niño Index (ONI) since January 2005 to

May 2021 recorded at the sublittoral area of Zihuatanejo, Guerrero (modified from Nava et al. 2021).

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

from the two DNA regions (28S and ITS2)

showed that 100 % of the samples correspond-

ed to the genus Durusdinium (Fig. 6) and were

closer to the subclades D1.1 and D1.2 (Fig. 7).

The 28S molecular marker showed three haplo-

types in each reef and the haplotype diversity

values were h = 0.11 for Playa Riscalillo and

Islote Zacatoso, h = 0.12 for Playa Las Gatas,

and h = 0.14 for Caleta de Chon. The nucleo-

tide diversity (π) varied between 0.00034 and

0.00044. The genetic diversity for the ITS2

molecular marker was higher than for the 28S

molecular marker. Playa Las Gatas recorded

three haplotypes and h = 0.16, Playa Riscalillo

five haplotypes and h = 0.34, Caleta de Chon

seven haplotypes and h = 0.29, and Islote Zaca-

toso 17 haplotypes and h = 0.61. Nucleotide

diversity varied between 0.00107 and 0.02784.

Using local ecological knowledge as the

starting point for the inclusion of citizen

involvement: Local ecological knowledge is

not limited to the recognition and identification

of species. Like the case of the fish ‘cocinero’

(Caranx caballus), which, even though it is

not a highly-priced species compared to other

fishes in the area, it is well known and val-

ued by locals inhabitants in Zihuatanejo for

its frequent use as homemade food (Table 3).

Drouet-Cruz (2020) explained that the knowl-

edge around local biological resources is as

rich as to determine and describe a) the species

abundance, b) life cycles, including reproduc-

tive seasonality, c) behavior or species etiology,

d) seasonal distribution, and finally, e) the way

in that species in Zihuatanejo interact. Along

with biological knowledge, local collaborators

possess complementary observations linking

coral ecology with physical and climatological

phenomena. They use available local knowl-

edge about ocean currents, the morphology of

sites, and weather patterns to plan their daily

activities and future scenarios, as well as to

prevent environmental and productive con-

tingencies. Specifically of knowledge about

reefs, the inhabitants of Zihuatanejo sort their

species into two main categories: a) corals and

b) ‘ripio’ (gravel). For these people, corals are

defined exclusively as those plants that ‘seem

like a black tree, with phosphorescent branches

(Drouet-Cruz, 2020: 66, our emphasis). In

other words, in Zihuatanejo, only arborescent

Fig. 6. Phylogenetic tree for the genus Durusdinium built with sequences of the molecular marker 28s obtained from

GenBank and of zooxanthellae of the coral communities of Zihuatanejo, Guerrero (Islote Zacatoso, Playa las Gatas, Caleta

de Chon, and Playa Riscalillo) during 2018 and 2019 (modified from Cárdenas-Alvarado et al. 2021).

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Fig. 7. Phylogenetic tree for the genus Durusdinium built with sequences of the molecular marker ITS2 obtained from GenBank and of zooxanthellae of the coral communities of

Zihuatanejo, Guerrero (Islote Zacatoso, Playa las Gatas, Caleta de Chon, and Playa Riscalillo) during 2018 and 2019 (modified from Cárdenas-Alvarado et al. 2021).

14 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

corals, such as those in the genus Antipathes,

are considered corals. Ripios or scleractinian

corals, are more abundant in shallow areas.

Also, they are extensive, with 20 or 30 m in

length and are not conceptualized as corals in

the minds of local fishers. In all cases, corals

and ripios harbor numerous and diverse gilds

of fishes; in the case of ripios, they are of great

importance for local fishermen communities

because many fishes of commercial impor-

tance spawn and refuge among them, including

‘huachinango’ and ‘pargo’ (belonging to the

Lutjanidae and Sparidae families, respectively,

Drouet-Cruz, 2020).

DISCUSSION

The baseline study confirmed the relevance

of several sites such as Playa Manzanillo, Playa

Riscalillo and Islote Zacatoso because they har-

bored coral communities with a moderate-high

conservation status, confirming their potential

for conservation. The relative position to the

coast of these sites also favors the dilution of

the sewage contamination from Ixtapa and

Zihuatanejo Bay. Moreover, the lack of access

to Islote Zacatoso by land excludes some users,

which means a less intensive activity impact-

ing the site. In contrast, results evidenced that

locations with coral communities inside the bay

of Zihuatanejo (Playa las Gatas) or nearby to

places subjected to land transformation (Caleta

de Chon), were exposed to relevant anthropo-

genic pressure, visible as high concentration

of chlorophyll or high sedimentation rates,

attributed to the land transformation (Nava &

Ramírez-Herrera, 2012). Nonetheless, all reefs

support a high diversity of actors that have

access to the resources. Playa Manzanillo and

Playa las Gatas, more accessible by land and

closer to the bay, are places with a diversity of

types of fishing (e.g. recreational on boat, rec-

reational on-shore, commercial, and commer-

cial diving) and touristic activities coexisting.

The boring sponge assemblages present

in the coral reefs were comparable to other

assemblages distributed throughout the Mexi-

can Pacific in terms of abundance and diver-

sity (Carballo et al., 2019). The concentration

of chlorophyll and stable isotopes of nitrogen

and carbon (𝛿15N and 𝛿13C) coincided with the

development of boring sponge assemblages

in the reefs near the bay. Likewise, the results

showed that the skeleton of living coral colo-

nies was the least affected and confirmed that

the calcareous substratum formed by dead

corals was more vulnerable to bioerosion by

boring sponges. Although the weakening and

TABLE 3

Frequency (F), average rank (AR), and salience (S) of most salient commercially important species in Zihuatanejo according

to a free listing exercise among fishers.

Phylum Family Scientific name Common

local name F AR S

Chordata Lutjanidae Lutjanus campechanus - Poey, 1860 Huachinango 84.4 3.56 0.684

Carangidae Carax caballus - Günther, 1896 Cocinero 72.9 5.63 0.482

Haemulidae Hameulon spp. - Gill, 1862 Ronco 64.6 4.95 0.452

Lutjanidae Lutjanus aratus - Günter, 1864 Pargo 68.8 5.92 0.411

Scombridae Thunnus obesus - Lowe 1839 Atún 47.9 8.57 0.275

Carangidae Selar crumenophtalmus - Bloch y Schneider, 1801 Ojotón 49 7.72 0.254

Coryphaenidae Coryphaena hippurus - Linnaeus, 1758 Dorado 43.8 7.93 0.253

Istiophoridae Istiompax indica - Cuvier, 1832 Marlin 42.7 9.39 0.204

Mollusca Ostreidae Crassostrea spp. Ostión 16.7 5.69 0.132

Octopodidae Octopus spp. Pulpo 16.7 7.13 0.123

Haliotidae Haliotis spp. Abulón 5.2 17.6 0.03

Arthropoda Palinuridae Panulirus spp. Langosta 15.6 4.13 0.128

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

detaching of the reef framework free new spac-

es for colonization, it can cause a progressive

degradation of the coral reef if bioerosion sur-

passes the reef’s capability of recovery (Marlow

et al., 2019; Nava et al., 2019). Because boring

sponges are filter-feeding organisms, it has

been suggested that the water enrichment with

dissolved and particulate organic matter and

nutrients can enhance sponge abundance and

its bioerosion activity (Alvarado et al., 2017).

The increase of dead coral coverage attrib-

uted to environmental degradation and climate

change have been considered as a cause of the

rise in boring sponge abundance and bioerosion

rate during the last decades (Schönberg et al.,

2017), highlighting the importance of promot-

ing a high cover of living corals in the reef to

prevent the reef deterioration. For this purpose,

the implementation of coral reef restoration

strategies are useful (Nava et al., 2014) and we

found that coral fragments were an excellent

choice as coral transplants because they reach

the fixation more quickly, and reach the high-

est survival and growth over the loose coral

colonies. This could be explained by the initial

stimulation of healing after breakage, which

may favors the calcium carbonate deposition

(Rempel et al., 2020).

Seasonality was a relevant factor during

the implementation of our restoration plan,

because the strike of storms and hurricanes

could be prevented during the dry season,

reducing transplant detaching and mortality. It

is also important to highlight the relevance of

the immobilization of coral transplants and the

kind of substrate where they were transplanted

(Casey et al., 2015; Oviedo, 2011). We learned

that transplants should be attached to the natu-

ral substrate from the beginning, where they

contribute permanently to the coverage of liv-

ing corals in the reef framework. Several resto-

ration initiatives that have reported low survival

of coral transplants used artificial substrata

that never will be part of the reef framework

and natural materials that disintegrate or suf-

fer deterioration very quickly (Cabaitan et al.,

2015; Suzuki et al., 2011; Toh et al., 2017). The

use of pita fiber ropes as a holding material and

wood stakes as substrata (García et al., 1995)

for example, resulted in a final survival of 0

%. On the other hand, when the same treatment

is carried out with plastic ties, the percent-

age of survival was close to 67 %, increasing

up to 80-95 % when adherent solutions are

used (García et al., 1995; Ruiz et al., 2013;

Tortolero-Langarica et al., 2014). Procedures

that provide stability long enough to promote

the integration of transplants in the reef frame-

work, seem to be a key factor to the success of

the restoration (Edwards & Gomez, 2007).

The approach tested in Playa las Gatas

showed a high potential due to its low cost

and the possibility to be implemented by non-

specialized people. The steel grids were a reli-

able material to transplant corals in a damaged

coral community because they endured the

impact of the waves and currents until the fixa-

tion of coral transplants occurred. After several

months, this material disintegrated, leaving the

coral transplants fixed to the substratum. None-

theless, as many experimental approaches, the

experiment presented here requires the par-

ticipation of the local communities to reach a

significant outcome of coral reef restoration.

As we observed during the end of the experi-

ment, it is also important to prevent the future

impacts of natural phenomena, such as the El

Niño, that has the potential to revert the natu-

ral recovery of coral reefs or even the positive

outcome of restoration initiatives (Nava et al.,

2021). During the El Niño event of 2015, Islote

Zacatoso and Caleta de Chon endured the

thermal stress that caused bleaching and coral

mortality at the other localities.

After the examination of the symbiotic

relationship of corals with their algae symbi-

onts, which can confer them thermal resistance

(LaJeunesse et al., 2010; Wang et al., 2021),

we found that the current presence of only one

genus of Symbiodiniaceae in Zihuatanejo may

be the resulting selection made by previous El

Niño events in the region, that could promote

the acquisition of resistant symbiotic algae to

endure thermal stress (Baker et al., 2004; Stat

et al., 2009; Van Oppen et al., 2005; Wang et

al., 2021). The genetic diversity also could

16 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

be related to the resistance to thermal stress,

because sites such as Playa las Gatas and Playa

Riscalillo, with the lowest genetic diversity,

showed the highest records of coral bleaching

and mortality during the El Niño event of 2015-

16, being the opposite with Islote Zacatoso

and Caleta de Chon (Cárdenas-Alvarado et al.,

2021). In addition, the haplotypes with more

mutational steps from the common haplotype

corresponded to symbiotic algae from Islote

Zacatoso which showed the highest genetic

differentiation. This suggests that different hap-

lotypes of Islote Zacatoso could be conserved

and their genetic diversity contributed to the

resistance to bleaching by thermal stress. It

is important to assess the thermal resistance

of corals under more controlled conditions

focused on the entire coral holobiont (zooxan-

thellae and other associated microorganisms,

such as bacteria, fungi, viruses, etc.) (Brener-

Raffalli et al., 2022; Li et al., 2021; Van de

Water et al., 2022).

To date, specialized experiments are being

made in the laboratory under different levels of

seawater temperature testing thermal resistance

of corals from Islote Zacatoso, Caleta de Chon,

and Playa Riscalillo. The identification of coral

populations resistant to thermal stress is a key

goal in this conservation effort in Zihuatanejo,

Guerrero, 1) to detect coral reefs with high

potential as source of transplants for coral com-

munities impacted by El Niño events, and 2) to

increase the possibilities of success of future

initiatives of coral reef conservation in front of

climate change. An additional lesson learned

is the importance of the evolving of local

inhabitants in coral reef restoration. Marine

ethnobiological knowledge is the empirical

understanding that coastal populations have

acquired on the ecological properties (structure

and function) of coastal and marine ecosystems

that provide them with resources and aesthetic,

cultural, and spiritual assets (Narchi et al.,

2014). In Zihuatanejo, only a few efforts have

accounted for this knowledge. One such effort

conducted by Drouet-Cruz (2020), registered

and analyzed the local ecological knowledge

held by different groups of actors regarding

their economic activity and closeness with

the coral communities and associated species.

A clear example is the capability that local

inhabitants have for recognition and naming

marine species. Through free-listing Drouet-

Cruz (2020, and references therein) identifies

23 species belonging to five phyla (Table 3);

four of them were animals a) Chordata, b) Mol-

lusca, c) Arthropoda, d) Echinodermata and e)

Chlorophyta (macroalgae).

As reported in other realms of ethnobiol-

ogy (Berlin, 2014), as the management of spe-

cies increases, different groups of actors tend

to correctly identify these species with greater

ease as the salience in Table 3 suggests. Con-

versely, as the management decreases, fewer

people will be able to identify and relate to

specific species. The easiness of species recog-

nition is closely related to their overall impor-

tance, and not only to the commercial relevance

of a species. At the same, time the complex

and diverse constellation of actors conven-

ing in Zihuatanejo has allowed us to realize

how different conceptualizations of resources

and the expectations about the rights of use

can hinder conservation efforts. For example,

people making a living from recreational tour-

ism, in collaboration with municipal govern-

ment agencies intended to define conservation

polygons. Various groups of local fishers have

not taken those initiatives very well, because

they felt their historical rights of use hadn’t

been included in these initiatives, and they also

felt excluded from the circles where important

decision-making is being taken. Therefore,

these previous initiatives hadn’t been success-

fully implemented since they have not had the

citizen support that is required in projects of

this nature. Zihuatanejo is an area with several

groups of users with different motivations, and

after a year of working with various stake-

holder groups, we have realized that the citizen

participation strategy requires deep grassroots

work. It requires a great effort in environmen-

tal education. While some users have deep

ecological knowledge about species diversity

and abundances (Douet-Cruz, 2020), this does

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

not exactly translate into direct empowerment

while promoting conservation.

Coral reefs of Zihuatanejo are relevant

ecosystems with a high potential for coral reef

restoration, although the anthropogenic and

natural sources of impact must be attended to in

order to meet a significant level of restoration.

The transplant of coral fragments is a reliable

approach to recover coverage of living corals.

To confront the increase in the use of coral

reefs and the impact of climate change, we rec-

ommended the use of thermal resistant corals

and to scale the restoration efforts, extending

the projects to local stakeholders, joining the

formal and local ecological knowledge.

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 acknowledgments

section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

This work was financed by the follow-

ing founding sources: FORDECYT-PRONAC-

ES/58533/2020, Consejo Nacional de Ciencia

y Tecnología-Secretaría de Eduación Pública

No. CB-2012-01-177537 and the Research

Council of Scientific Research of the Univer-

sidad Michoacana de San Nicolás de Hidalgo.

We also thank the Climate Prediction Center

supported by the National Oceanographic and

Atmospheric Administration’s National Weath-

er Service for the production of the Oceanic El

Niño Index and the National Aeronautics and

Space Administration Goddard Space Flight

Center for the production of the sea surface

temperature and the degree heating weeks data.

We would like to thank Thierry Durand and

Capitán ‘Chilolo’ for the logistical support pro-

vided during the sampling.

REFERENCES

Alvarado, J. J., Grassian, B., Cantera-Kintz, J. R., Carballo,

J. L., & Londoño-Cruz, E. (2017). Coral reef bioero-

sion in the Eastern Tropical Pacific in P. W. Glynn,

D. P. Manzello & I. C. Enochs (Eds.), Coral reefs of

the eastern tropical Pacific (pp. 369–403). Springer.

Appril, A., & Gates, R. (2007). Recognizing diversity in

coral symbiotic dinoflagellate communities. Molecu-

lar Ecology, 16(6), 1127–1134.

Baker, A. C., Starger, C., McClanahan, T. R., & Glynn, P.

W. (2004). Corals’ adaptive response to climate chan-

ge. Nature, 430(7001), 741–741.

Berlin, B. (2014). Ethnobiological classification: prin-

ciples of categorization of plants and animals in

traditional societies (Vol. 185). Princeton University

Press.

Bernard, H. R. (1995). Research methods in anthropology:

qualitative and quantitative approaches. Rowman &

Littlefield.

Brener-Raffalli, K., Vidal-Dupiol, J., Adjeroud, M., Rey,

O., Romans, P., Bonhomme, F., Pratlong, M., Hague-

nauer, A., Pillot, R., Feuillassier, L., Claereboudt,

M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D.,

Mita, G., & Toulza, E. (2022). Gene expression plas-

ticity and frontloading promote thermotolerance in

Pocillopora corals. Peer Community Journal, 2, e13.

Cabaitan, P. C., Yap, H.T., & Gomez, E. D. (2015). Per-

formance of single versus mixed coral species for

transplantation to restore degraded reefs. Restoration

Ecology, 23(4), 349–356.

Carballo, J. L., Cruz-Barraza, J. A., Vega, C., Nava, H., &

Chávez-Fuentes, M. D. C. (2019). Sponge diversity in

Eastern Tropical Pacific coral reefs: an interoceanic

comparison. Scientific Reports, 9(1), 1–15.

Cárdenas-Alvarado, M. A., Nava, H., González-Rodríguez,

A., Maldonado-López, Y., & Rodríguez-Lanetty, M.

(2021). Higher population genetic diversity within the

algal symbiont Durusdinium in Pocillopora verruco-

sa from Mexican Pacific reefs correlates with higher

resistance to bleaching after the El Niño 2015–16

event. Marine Ecology, 42(4), e12667.

Casey, J. M., Connolly, S. R., & Ainsworth, T. D. (2015).

Coral transplantation triggers shift in microbiome

and promotion of coral disease associated potential

pathogens. Scientific Reports, 5(1), 1–11.

Drouet-Cruz, H. T. (2020). El pescador y la mar: una

mirada etnoecológica a la pesca y arrecifes de coral

en Zihuatanejo de Azueta, Guerrero [Unpublished

Bachelor’s thesis]. Universidad Nacional Autónoma

de México, México.

18 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Edwards, A. J., & Gomez, E. D. (2007). Reef restoration

concepts and guidelines: making sensible manage-

ment choices in the face of uncertainty. Capacity

Building for Management Programme. Coral Reef

Targeted Research, Australia.

García, R. P., Alvarado, E. M. & Acosta, A. (1995). Rege-

neración de colonias y trasplante de fragmentos

de Acropora Palmata (Cnidaria:Scleractinia) en el

Parque Nacional Natural Corales del Rosario, Caribe

Colombiano. Anales del Instituto de Investigaciones

Marinas de Punta Betín, 24(1), 5–21.

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

and review of the far eastern Pacific coral reef region.

Coral Reefs 19(1), 1–23.

Gómez E. D., Aliño P. M., Yap H. T., Licuanan W. Y. (1994).

A review of the status of Philippine reefs. Marine

Pollution Bulletin, 29(1-3), 62–68.

LaJeunesse, T. C, Parkinson, J. E., Gabrielson, P. W., Jeong,

H. J., Reimer, J. D., Voolstra, C. R., & Santos, S.

R. (2018). Systematic revision of Symbiodiniaceae

highlights the antiquity and diversity of coral endos-

ymbionts. Current Biology, 28(16), 1–11.

LaJeunesse, T. C., Pettay, D. T., Sampayo, E. M., Phong-

suwan, N., Brown, B., Obura, D., Hoegh-Guldberg,

O., & Fitt, W. K. (2010). Longstanding environ-

mental conditions, geographic isolation and host

symbiont specificity influence the relative ecologi-

cal dominance and genetic diversification of coral

endosymbionts in the genus Symbiodinium. Jour-

nal of Biogeography, 37(5), 785–800. https://doi.

org/10.1111/j.1365-2699.2010.02273.x

Li, J., Long, L., Zou, Y., & Zhang, S. (2021). Microbial

community and transcriptional responses to increased

temperatures in coral Pocillopora damicornis holo-

biont. Environmental microbiology, 23(2), 826–843.

Marlow, J., Schönberg, C. H., Davy, S. K., Haris, A.,

Jompa, J., & Bell, J. J. (2019). Bioeroding sponge

assemblages: the importance of substrate availabi-

lity and sediment. Journal of the Marine Biological

Association of the United Kingdom, 99(2), 343–358.

Muller-Parker, G., D’Elia, C. F., & Cook, C. B. (2015).

Interactions between corals and their symbiotic algae.

In C. Bikerland (Ed.), Coral Reefs in the Anthropoce-

ne (pp. 99–116). Springer.

Narchi, N. E., Cornier, S., Canu, D. M., Aguilar-Rosas, L.

E., Bender, M. G., Jacquelin, C., Thiba, M., Moura,

G. G. M., & De Wit, R. (2014). Marine ethnobiology

a rather neglected area, which can provide an impor-

tant contribution to ocean and coastal management.

Ocean & Coastal Management, 89, 117–126.

Nava, H., & Figueroa-Camacho, A. G. (2017). Rehabilita-

tion of damaged reefs: outcome of the use of recently

broken coral fragments and healed coral fragments of

pocilloporid corals on rocky boulders. Marine Ecolo-

gy, 38(5), e12456.

Nava, H., García-Madrigal, C. A. E., & Carballo, J. L.

(2019). Relationships between boring sponge assem-

blages and the availability of dead coral substrate on

Mexican Pacific coral reefs. Journal of the Marine

Biological Association of the United Kingdom, 99(4),

795–805.

Nava, H., & Ramírez-Herrera, M. T. (2012). Land use

changes and impact on coral communities along the

central Pacific coast of Mexico. Environmental Earth

Sciences, 65(4), 1095–1104.

Nava, H., López, N., Ramírez-García, P., & Garibay-Valla-

dolid, E. (2021). Contrasting effects of the El Niño

2015–16 event on coral reefs from the central pacific

coast of Mexico. Marine Ecology, 42(2), e12630.

Nava, H., Ramírez-Herrera, M. T., Figueroa-Camacho,

A. G., & Villegas-Sanchez, B. M. (2014). Habitat

characteristics and environmental factors related to

boring sponge assemblages on coral reefs near popu-

lated coastal areas on the Mexican Eastern Pacific

coast. Marine Biodiversity, 44(1), 45–54.

Oviedo, M. E. (2011). Viabilidad de trasplantes de coral

Cuerno de Alce Acropora palmata (Lamarck, 1816)

en el Parque Nacional Natural Tayrona, Caribe

colombiano. Centro de Estudios de Ciencias del Mar,

Universidad Nacional de Colombia, Colombia.

Quinlan, M. (2005). Considerations for Collecting Freelists

in the Field: Examples from Eth-nobotany, Field

Methods, 17(3), 219–234.

Rempel, H. S., Bodwin, K. N., & Ruttenberg, B. I. (2020).

Impacts of parrotfish predation on a major reef-buil-

ding coral: quantifying healing rates and thresholds of

coral recovery. Coral Reefs, 39(5), 1441–1452.

Reyes-Bonilla, H. (2003). Biogeografía y ecología de los

corales hermatípicos del Pacífico. In S. Salazar-

Vallejo, & N. E. González (Eds.), Biodiversidad

marina y costera de México (pp. 207–222). Comisión

Nacional para el Conocimiento y Uso de la Biodiver-

sidad (CONABIO) & Centro de Investigaciones de

Quintana Roo (CIQRO).

Reyes-García, L. A. (2012). Control colonial en el siglo

XVII. Geografía e Historia de Zihuatanejo de Azueta,

Guerrero [Unpublished Bachelor’s thesis]. Universi-

dad Nacional Autónoma de México, México.

Ruiz, H. J., Ortiz, A. L., Nemeth, M. I., Scherer M. T., &

Griffin, S. (2013). Casos de estudio en la restau-

ración de arrecifes de coral de Puerto Rico [Paper

presentation]. In L. M. Niño Martínez & M. C. Prada

Triana (Eds.), Primer Simposio Internacional de la

Administración Sostenible de los Archipiélagos Isla

del Rosario y San Bernardo [Symposium]. Cartagena,

Colombia.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71 (S1): e54792, abril 2023 (Publicado Abr. 30, 2023)

Sánchez-Briones, A. G. (2010). Geografía e Historia del

honorable municipio de Zihuatanejo de Azueta, Gue-

rrero [Unpublished Bachelor’s thesis]. Universidad

Nacional Autónoma de México, México.

Schönberg, C. H., Fang, J. K. H., & Carballo, J. L. (2017).

Bioeroding sponges and the future of coral reefs. In J.

L. Carballo & J. Bell (Eds.), Climate change, ocean

acidification and sponges (pp. 179–372). Springer.

Smith, J. J., Furbee, L., Maynard, K., Quick, S., & Ross, L.

(1995). Saliency counts: A domain analysis of english

color terms. Journal of Linguistic Anthropology, 5(2),

203–216.

Stat, M., Loh, W. K. W., LaJeunesse, T. C., Hoegh-Guld-

berg, O., & Carter, D. A. (2009). Stability of coral-

endosymbiont association during and after a thermal

stress event in the southern Great Barrier Reef. Coral

Reefs, 28(3), 703–713.

Suzuki, G., Kai, S., Yamashita, H., Suzuki, K., Iehisa,

Y., & Hayashibara, T. (2011). Narrower grid struc-

ture of artificial reef enhances initial survival of in

situ settled coral. Marine Pollution Bulletin, 62(12),

2803–2812.

Toh, T. C., Ng, C. S. L., Loke, H. X., Taira, D., Toh, K.

B., Afiq-Rosli, L., Poquita-Du, R. C., Cabaitan, P.,

Sam, S. Q., Kikuzawa, Y. P., Chou, L. M., & Song,

T. (2017). A cost-effective approach to enhance

scleractinian diversity on artificial shorelines. Ecolo-

gical Engineering, 99, 349–357.

Tong, F., Zhang, L., Mao Chen, P., & Cheng, J. (2018).

Molecular taxonomy and diversity of Symbiodinium

spp. based on 28S r DNA sequences within 15 coral

species in Daao Bay, Shenzhen. Conference Series:

Materials Science and Engineering, 392, 1–9.

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

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

degraded coral reef using a natural remediation pro-

cess: A case study from a Central Mexican Pacific

National Park. Ocean & Coastal Management, 96,

12–19.

Van Oppen, M. J. H., Mahiny, A. J., & Done, T. J. (2005).

Geographic distribution of zooxanthellae types in

three coral species on the Great Barrier Reef sampled

after the 2002 bleaching event. Coral Reefs, 24(3),

482–487.

Van de Water, J. A. J. M., Tignat-Perrier, R., Allemand, D, &

Ferrier-Pagés, C. (2022). Coral holobionts and biote-

chnology: from Blue Economy to coral reef conserva-

tion. Current Opinion in Biotechnology, 74, 110–121.

Wang, X., Wu, Z., Wu, Y., An, M., Zhou, Z., & Lin, S.

(2021). Differential affinities of a Pocillopora dami-

cornis galectin to five genera of Symbiodiniaceae at

different temperatures. Frontiers in Marine Science,

8, 754808.