Journal of the Marine Spatio-temporal variation in rate of carbonate
Biological Association of the
United Kingdom
cambridge.org/mbi
Original Article
Cite this article: Alvarado-Rodríguez JF, Nava
H, Carballo JL (2019). Spatio-temporal
variation in rate of carbonate deposition by
encrusting organisms in different reef
microhabitats from Eastern Pacific coral reefs.
Journal of the Marine Biological Association of
the United Kingdom 1–11. https://doi.org/
10.1017/S0025315419000638
Received: 22 March 2018
Revised: 6 May 2019
Accepted: 21 June 2019
Key words:
Carbonate deposition; calcification accretion
units; encrusting calcifiers; microhabitat
Author for correspondence:
H. Nava, E-mail: hnava@umich.mx
© Marine Biological Association of the United
Kingdom 2019
Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
deposition by encrusting organisms in different
reef microhabitats from Eastern Pacific
coral reefs
J. F. Alvarado-Rodríguez , H. Nava and J. L. Carballo
Laboratorio de Biodiversidad Marina, Departamento de Zoología, Instituto de Investigaciones sobre los Recursos
Naturales, Universidad Michoacana de San Nicolás de Hidalgo, C.P. 58337, Morelia, Michoacán, México
Abstract
Reef encrusting calcifiers (non-scleractinian species) constitute assemblages that participate in
the carbon cycle at coral reefs. Despite their apparent secondary role in building the reef
framework, they contribute to the reef consolidation binding sediments and inducing larval
recruitment from other epilithic invertebrates. The contribution of encrusting calcifiers on
reef accretion was examined by the assessment of their rate of carbonate deposition on
four different simulated reef microhabitats using calcification accretion units (CAUs) during
12 months at Playa Las Gatas and Islote Zacatoso, two coral communities from the coast of
the Mexican Pacific. Encrusting calcifiers from Playa Las Gatas, the most impacted site,
showed a rate of carbonate deposition (mean ± SD) four times higher than at
Islote Zacatoso (10.02 ± 3.22 g CaCO3 m−2 d−1 vs 2.48 ± 1.01 g CaCO3 m−2 d−1). Overall,
the rate of carbonate deposition on surfaces protected from sedimentation and light was up
to 1.8 times higher than on exposed ones (11.40 ± 4.35 g CaCO3 m−2 d−1 vs 6.18 ±
3.13 g CaCO3 m−2 d−1). Carbonate deposition by calcareous algae was higher on the well-lit
exposed surfaces while filter-feeding invertebrates showed the major contribution on the
shaded cryptic surfaces. Although rate of carbonate deposition by encrusting calcifiers
seems to be lower than hermatypic corals, it seems to be relevant on coral reefs affected by
anthropogenic impacts where coral calcification is low. Under global demise of coral reefs
by environmental degradation and climate change, encrusting calcifiers may become relevant
for the process of carbonate deposition.
Introduction
Encrusting calcifiers on coral reefs are comprised of diverse assemblages of bryozoans, calcar-
eous algae, foraminiferans, polychaetes, barnacles and gastropod species that inhabit cryptic
and exposed surfaces of reef structures (Garrett et al., 1971; Martindale, 1976; Stearn et al.,
1977). Morphologically they are of low profile, with their basal surface cemented to the reef
substrate (Mallela, 2007). These organisms play major roles on coral reefs: they stabilize
coral fragments in the reef framework, enhance topographic complexity and contribute to
CaCO3 deposition (Scoffin, 1992; Gherardi & Bosence, 1999; Rasser & Riegl, 2002).
Although the important role of these organisms is well documented, few estimates of carbon-
ate deposition by assemblages of encrusting calcifiers are available globally, with no data avail-
able for the Mexican Pacific.
On coral reefs, the level of environmental exposure seems to be important for carbonate
deposition by assemblages of encrusting calcifiers. At the level of microhabitat, for example,
higher deposition of CaCO3 by encrusting calcifiers was documented in exposed habitats
than in cryptic ones (Mallela & Perry, 2007; Mallela, 2013). Level of exposure seems to be
related to light intensity (Steneck & Adey, 1976; Martindale, 1992; Björk et al., 1995), sediment
deposition (Fabricius & De’ath, 2001; Maughan, 2001; Azevedo et al., 2006), water temperature
(Vásquez-Elizondo & Enriquez, 2016) and pH (Price et al., 2012; Vargas et al., 2015). In the
Caribbean for example, coral reefs affected by terrestrial runoff show low levels of carbonate
deposition (Mallela, 2007). In the Pacific Ocean, high daily variation of pH was related to
low levels of carbonate deposition in coral reefs (Price et al., 2012). In this region, it is esti-
mated that encrusting calcifiers produce between 1.24 and 5.51 g CaCO3 m−2 d−1 (Price
et al., 2012; Morgan & Kench, 2014; Vargas et al., 2015) while in the Caribbean it is estimated
that carbonate deposition ranges between 0.20 and 2.85 g CaCO3 m−2 d−1 (Mallela, 2007,
2013; Kuffner et al., 2013; Hepburn et al., 2014).
Environmental degradation and climate change are related to coral reef decline around the
world (Bryant et al., 1998; Gardner et al., 2003; De’ath et al., 2012). Extensive mass coral
bleaching and coral mortality events have been documented in the Mexican Pacific as a result
of the El Niño phenomenon (Reyes-Bonilla, 1993; Carriquiry et al., 2001; Reyes-Bonilla et al.,
2002). In addition, excessive suspended sediments and organic pollution may enhance over-
growing and bioerosion of corals by sponges (Rützler, 2002). Due to the decline of corals
on a global scale, the relative contribution of assemblages of encrusting calcifiers to the
 2 J. F. Alvarado-Rodríguez et al.
gross carbonate production of coral reefs is likely to increase
(Morgan & Kench, 2014). Moreover, different approaches
reported variation in carbonate deposition rates on artificial sub-
strata emulating several microhabitats present in coral reefs (Price
et al., 2012; Hepburn et al., 2014). The present study deals with
the characterization of encrusting calcifiers settled on artificial
surfaces and documents their contribution to carbonate depos-
ition in four different microhabitats from coral reefs from
Zihuatanejo, Guerrero, Mexico.
Materials and methods
Study area
Our study was performed at Zihuatanejo, Guerrero, Mexico along
the coast of the southern Mexican Pacific (Figure 1A,
Seaturtle.Org Maptool, 2002). A seasonal change in winds and
currents occurs at this region: south-east winds and the
Equatorial Counter Current prevail between May and August
and south-east winds and the California Current influence this
region between November and April. Monthly average tempera-
ture ranges between 18 and 32°C and the rainy season occurs
from June to September (Semar-Digaohm, 2015). Coral reefs
are located at two sites with different levels of anthropogenic
impact. Playa Las Gatas (17°37′ 19.7′′ N 101°33′ 10.5′′ W), consid-
ered the most impacted coral community, is situated within the
Zihuatanejo Bay, a tourist destination whose anthropogenic
impact includes sewage outlets, urban development, anchoring,
fishing and recreational snorkelling. This site harbours a less
developed reef structure, with numerous coral colonies of
Pocillopora verrucosa, P. capitata and P. damicornis that spread
over a rocky substratum between 2 and 6 m depth and cover
nearly 8% of the substratum. Several patches of dead coral matrix
(15.1%) and coral rubble (9.3%) are another feature of this site.
Islote Zacatoso (17°39′ 14.5′′ N 101°37′ 18.7′′ W) is considered well
conserved because no obvious signs of extensive physical damage
have been observed there. It is located outside the bay and has a
well-developed reef structure, only visited by scuba divers and
several fishermen. This locality harbours a well-developed reef
framework between 1 and 10 m depth comprised mainly of
P. damicornis and P. verrucosa that cover almost 66.6% of the
substratum (Nava et al., 2014).
Environmental characterization
To obtain a reference of the water quality at both sites, several crit-
ical environmental variables for coral survival were recorded
(mean ± SD) in January, June and December 2015. Water trans-
parency (m) was recorded on three consecutive days during
each sampling period using standard Secchi disk depth measure-
ments. The Secchi disk was tied to a nylon string and submerged
to the maximum depth at which the disk was visible (Edinger
et al., 1998). The depth was then recorded in a log, this procedure
was repeated three times and data averaged per day and site. At
the end of each sampling period, we get at least three averaged
measures of water transparency per site. Water temperature (°C)
and light intensity (lux) at 5 m depth above the bottom were
recorded using a Hobo® temperature/light (waterproof) pendant
data logger at each site. These devices were programmed to meas-
ure both parameters every 5 min during 72 h during each survey
period. At the end of each survey all devices were collected and
their temperature/light data recorded. All data collected of water
temperature were averaged and data of light intensity were aver-
aged from records made between 9:00 am and 3:00 pm.
Sedimentation rate (kg m−2 d−1) was recorded using sediment
traps. Traps consisted of 1-l plastic bottles (2.4 ratio of height
Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
to diameter, Carballo et al., 1996). Six replicate traps were
deployed 1 m above the substrate at a depth of 5 m at each site.
Sediment traps were attached in pairs to three vertical PVC
pipes (each 1 m long) anchored above the bottom of the reef.
Sediments were collected over a period of 3–4 days and rinsed
with fresh water at the laboratory prior to oven-drying and weigh-
ing (Cortés & Risk, 1985). To obtain the sedimentation rate, we
used the following formula:
DW
Sedimentation (kg · m−2 · d−1 ) =
(A · d)
where DW = the dry weight of the sediments, A = the sediment
catchment area (m2) of the traps, and d = the period (days) of
sediment traps deployment.
Carbonate deposition by encrusting calcifiers
To record carbonate deposition on artificial surfaces (mean ± SD)
we used Calcification/Accretion Units (CAUs, Figure 1B). Each
CAU consisted of four PVC 100 cm2 surfaces (10 × 10 cm) stacked
1 cm apart in pairs and fixed to the reef framework (10 cm above
the substrate and >1.0 m apart) with steel rods and marine epoxy
plaster (N = 10 per site). Each CAU simplified four different micro-
habitats found in reef structures: exposed upper surfaces (EUS),
facing up and fully exposed to light and sediment deposition; cryp-
tic upper surfaces (CUS), facing down and protected from direct
light and sediment deposition; cryptic bottom surfaces (CBS),
facing up and protected from direct irradiance but exposed to sedi-
ment deposition and exposed underside surfaces (EDS), facing
down and protected from direct light and sedimentation. Similar
artificial surfaces have been successfully tested in experimental
studies dealing with recruitment and carbonate deposition of
encrusting calcifiers at the Central Pacific (Price et al., 2012;
Vargas et al., 2015) and the South Atlantic (Reis et al., 2016).
All CAUs were deployed at 5 m depth over the bottom at each
site in January 2015. After 6 and 12 months (June and December
2015), a set of five CAUs were collected and each surface was
stored in a plastic bag and frozen until processing in a laboratory.
Afterwards, each surface was submerged for 24 h in a solution of
4% chloride to eliminate organic matter and to clean calcareous
structures. All surfaces were washed with distilled water and
oven dried (70°C for 48 h). Encrusting calcifiers attached to sur-
faces were observed and identified with a stereoscopic microscope.
All organisms were separated within five major groups: (Ca)
calcareous algae, (Br) bryozoans, (Mo) molluscs (bivalves and
gastropods), (Ba) barnacles and (Po) serpulid polychaetes.
Carbonate deposited by each taxonomic group was scraped
from each PVC surface and weighed with an analytical balance
(± 0.001 g). The weight of this material was divided by both the
area of the PVC surface and the number of days of deployment
of CAUs, to calculate the rate of carbonate deposition
(g CaCO3 m−2 d−1) per taxonomic group at each microhabitat
and site. Carbonate material deposited by all taxonomic groups
together on each surface we also used to calculate the overall
rate of carbonate deposition per microhabitat and site.
w
Carbonate deposition (gCaCO3 m−2 d−1 ) =
a·t
Where w = dry weight of carbonate (g), a = area of CAU surface
(m2), t = time of deployment of CAUs (days).
Data analysis
Data were analysed with R software version 3.3.2 (R Core Team,
2016). Environmental data did not meet the assumptions of
 Journal of the Marine Biological Association of the United Kingdom
Fig. 1. (A) Location of the study area: (PG) Playa Las Gatas and (IZ) Islote Zacatoso; (B) CAU (Calcification/Accretion Unit) after installation. The four surfaces
exposed to the settlement of encrusting calcifiers are shown: (EUS) exposed upper surface, (CUS) cryptic upper surface, (CBS) cryptic bottom surface and
(EDS) exposed underside surface.
normality and homoscedasticity (Kolmogorov–Smirnov test,
Sokal & Rohlf, 1981) and were analysed using a series of non-
parametric Kruskal–Wallis tests with Dunn’s post-hoc compari-
sons to determine statistical differences among sampling periods
and sites. Carbonate deposition rate was ln-transformed and
thereafter a series of ANOVA and Student–Newman–Keuls
post-hoc tests (Zar, 1984) was performed to determine significant
differences between sites, sampling periods, microhabitat and
taxonomic groups. To evaluate the contribution of all taxonomic
groups to carbonate deposition in all experimental surfaces, a tri-
dimensional nMDS ordination and cluster classification analysis
were developed constructing a Bray–Curtis similarity matrix
(Bray & Curtis, 1957) based on the data of carbonate deposited
per taxonomic group, which were square root-transformed and
standardized beforehand (Warwick & Clarke, 1991). Similarity
percentages (SIMPER) analysis was performed to detect which
taxonomic groups were responsible for these observed clusters
(Warwick et al., 1990; Clarke & Ainsworth, 1993).
Results
Environmental characterization
Environment data showed significant differences at each site with
time (Figure 2). At Playa Las Gatas, for example, significant differ-
ences existed between sampling periods for water transparency
(H = 11.37, P < 0.01). Post-hoc test confirmed that the highest
transparency (mean ± SD) was recorded during January and the
lowest during December (7.96 ± 0.78 m and 5.67 ± 0.78 m,
Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
3
respectively, P < 0.01). Similarly, at Islote Zacatoso significant dif-
ferences were also observed between sampling periods (H = 19.44,
P < 0.001). Post-hoc comparisons revealed that the highest record
(mean ± SD) was made during December and the lowest during
June (12.29 ± 0.60 m and 7.10 ± 0.56 m, respectively, P < 0.001).
Water transparency also showed significant differences between
sites (H = 12.80, P < 0.001). Post-hoc test indicated that these
differences only occurred during December, when the highest
record occurred at Islote Zacatoso (P < 0.001, Figure 2A).
Sediment deposition showed temporal differences at both
sites (H = 13.255, P < 0.01 for Playa Las Gatas and H = 13.947,
P < 0.001 for Islote Zacatoso). Post-hoc tests indicated that sediment
deposition (mean ± SD) was significantly higher in June than in
December at both sites (Playa Las Gatas: 2.07 ± 0.29 kg m−2 d−1
vs 0.13 ± 0.02 kg m−2 d−1, P < 0.001 and Islote Zacatoso:
1.19 ± 0.28 kg m−2 d−1 vs 0.17 ± 0.06 kg m−2 d−1, P < 0.001). Only
during June were there significant differences in sediment depos-
ition between both sites (H = 6.708, P < 0.001), these being higher
at Playa Las Gatas than at Islote Zacatoso (P < 0.01, Figure 2B).
Water temperature showed significant differences during the
study at both sites: Playa Las Gatas (H = 152.55, P < 0.001) and
Islote Zacatoso (H = 128.58, P < 0.001). The highest records
(mean ± SD) were made during June (31.18 ± 0.20°C, P < 0.001
and 31.08 ± 0.29°C, P < 0.001 respectively) and the lowest during
January (27.81 ± 0.23°C, P < 0.001 and 27.75 ± 0.15°C, P < 0.001
respectively). Significant differences between sites were found
only during December, when water temperature was higher at
Playa Las Gatas than at Islote Zacatoso (H = 27.96, P < 0.001,
Figure 2C). Light intensity showed temporal differences at both
 4 J. F. Alvarado-Rodríguez et al.

Fig. 2. Environment variables recorded in Playa Las Gatas (black

columns) and Islote Zacatoso (white columns) during (Jan)
January 2015, (Jun) June 2015 and (Dec) December 2015. (A)
Water transparency, (B) sediment deposition, (C) water tempera-
ture and (D) light intensity. The bars in the columns represent
the standard deviation.

Fig. 3. Averaged rate of carbonate deposition at both reefs during (J) June 2015 and (D) December 2015 for: (A) per site, (B) per surface and (C) per taxonomic
group. (EUS) exposed upper surface, (CUS) cryptic upper surface, (CBS) cryptic bottom surface and (EDS) exposed underside surface. Groups: (CA) calcareous algae,
(Br) bryozoans, (Mo) molluscs, (Po) serpulid polychaetes, (Ba) barnacles. The bars in the columns represent the standard deviation.

sites (H = 120.72, P < 0.001 for Playa Las Gatas and H = 81.362, P <
0.001 for Islote Zacatoso), with the highest records (mean ± SD)
made during June (12,159.7 ± 2842.2 lux, P < 0.001 and 12,324.6
± 2809.6 lux, P < 0.001 respectively) and with the lowest records
made during December (7060.1 ± 2690.4 lux, P < 0.001 and
6172.9 ± 2676.6 lux, P < 0.001 respectively). No significant differ-
ences were detected between sites during the study (Figure 2D).
Carbonate deposition rate by encrusting calcifiers
Significant differences in carbonate deposition rate by encrusting
calcifiers (mean ± SD) were found between sites. The rate was
higher at Playa Las Gatas than at Islote Zacatoso during June
(10.79 ± 3.84 g CaCO3 m−2 d−1 vs 2.95 ± 0.75 g CaCO3 m−2 d−1,
F = 29.05, P < 0.001) and December (9.24 ± 2.59 g
CaCO3 m−2 d−1 vs 2.01 ± 1.27 g CaCO3 m−2 d−1, F = 31.26, P <
0.001) (Figure 3A). At Playa Las Gatas, carbonate deposition
rate among microhabitats also presented significant differences
during June (F = 29.045, P < 0.001) and December (F = 31.26,
P < 0.001). EDS showed the highest rate of carbonate deposition
rate through this study and CBS the lowest. At Islote Zacatoso,
only during June were there significant differences (F = 5.868,
P < 0.01). The highest rate of carbonate deposition was recorded
at CBS and the lowest at EUS (Figure 3B). The rate of carbonate
deposition recorded per taxonomic group at Playa Las
Gatas showed significant differences. During June (F = 41.35,

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 Journal of the Marine Biological Association of the United Kingdom 5

Table 1. Average carbonate deposition rate (g CaCO3 m−2 d−1) of major encrusting calcifiers in groups A, B and C of Playa Las Gatas and contribution (i) to the
average similarity within of each group (A = 85.83, B = 83.38, C = 83.00)

i SD(i) i/SD(i) i% ∑i%

Group A
Barnacles 15.34 47.90 4.11 11.66 55.80 55.80
Polychaetes 3.73 18.53 7.21 2.57 21.58 77.39
Molluscs 1.01 8.92 4.23 2.11 10.39 87.78
Bryozoans 0.45 6.31 2.95 2.14 7.35 95.13
Group B
Polychaetes 3.68 34.36 6.09 5.64 41.21 41.21
Molluscs 1.51 19.53 4.36 4.47 23.42 64.63
Barnacles 1.22 15.23 6.59 2.31 18.26 82.89
Calcareous algae 0.35 9.94 2.83 3.51 11.92 94.82
Group C
Molluscs 4.01 34.51 5.04 6.85 41.59 41.59
Barnacles 2.34 20.52 7.25 2.83 24.73 66.31
Polychaetes 0.71 10.92 4.11 2.66 13.16 79.47
Calcareous algae 0.38 9.48 2.38 3.98 11.42 90.89

P < 0.001) the highest contribution to carbonate deposition rate was
made by barnacles and molluscs and the lowest contribution was
made by calcareous algae and bryozoans. During December there
were also significant differences among taxa, but more groups
contributed to the highest rate of carbonate deposition. These
were barnacles, serpulid polychaetes and molluscs while the lowest
contribution was made by calcareous algae and bryozoans. At Islote
Zacatoso there were significant differences in the rate of carbonate
deposition among different taxa only during December (F = 5.93,
P < 0.01). The major contribution was made by calcareous algae
and serpulid polychaetes and less so by bryozoans (Figure 3C).
Variation in the contribution of calcifiers in time and space
Cluster, nMDS and SIMPER analyses helped to describe the con-
tribution of different taxa to carbonate deposition rate among
microhabitats (Table 1, Figure 4A).
At Playa Las Gatas, group A (similarity of 85.83%) was com-
prised mainly of EDS, where barnacles (55.80% of contribution
to the conformation of this group) maintained the highest rate
of carbonate deposition during June and December. Group B
(similarity of 83.38%) was comprised mainly of EUS and CUS
sampled during December, where serpulid polychaetes (41.21%
of contribution) showed the highest rate of carbonate deposition.
Finally, group C (similarity of 83.00%) was comprised of EUS,
CUS and CBS sampled during June, where molluscs (41.59% of
contribution) showed the highest rate of carbonate deposition.
Rate of carbonate deposition among groups at replicates of CBS
sampled during December were highly heterogeneous, although
both molluscs and serpulid polychaetes tended to be major calci-
fiers in this microhabitat.
At Islote Zacatoso, nMDS, cluster and SIMPER analysis
showed three major groups (Table 2, Figure 4B). Group A (simi-
larity of 75.36%) was comprised mainly of EUS sampled during
June and December, where calcareous algae (55.71% of contribu-
tion) maintained the highest rate of carbonate deposition. Group
B (similarity of 77.08%) was comprised of EDS sampled during
June where barnacles (36.36% of contribution) presented the
highest rate of carbonate deposition. Group C (similarity of
78%) was comprised of CUS and CBS sampled during June,
where serpulid polychaetes (contribution of 29.82%) presented
the highest rate of carbonate deposition.
The same analysis made with samples from both sites showed
four major groups during June (Table 3, Figure 5A). Group A
(similarity of 79.09%) was comprised of EUS from Islote
Zacatoso, where calcareous algae (81.91% of contribution) pre-
sented the highest rate of carbonate deposition. Group B (similar-
ity of 79.91%) was comprised mainly of CUS from Islote Zacatoso,
where serpulid polychaetes (contribution of 32.76%) showed the
highest rate of carbonate deposition. Group C (similarity of
84.07%) was comprised mainly of EDS sampled at both sites
and where barnacles (contribution of 52.93%) showed the highest
rate of carbonate deposition. Group D (similarity of 80.63%) was
comprised mainly of EUS and CBS from Playa las Gatas, where
molluscs and barnacles showed the highest rate of carbonate
deposition.
During December, such multivariate analyses also detected four
major clusters (Table 4, Figure 5B). Group A (similarity of 79.09%)
was comprised of EUS from Islote Zacatoso, where calcareous algae
presented the highest rate of carbonate deposition (contribution of
54.99%; Table 5). Group B (similarity of 87.41%) was comprised of
EDS from Playa Las Gatas, where barnacles (contribution of
54.89%; Table 5) presented the highest rate of carbonate deposition.
Group C (similarity of 85.02%) was comprised of EUS and CUS
from Playa Las Gatas, where serpulid polychaetes (contribution
of 44.00%; Table 5) presented the highest rate of carbonate depos-
ition. Group D (similarity of 81.89%) was comprised mainly of
CBS from both sites where molluscs showed the highest rate of
carbonate deposition (contribution of 34.19%; Table 5).
Discussion
Our study confirms the importance of encrusting calcifiers for
carbonate deposition on coral reefs from Mexican Pacific coast.
Previous records of carbonate deposition at other locations are
even lower than the lowest records of 2.01 g CaCO3 m−2 d−1
made at Zihuatanejo. Since some of these records have been
made at well-conserved reefs, it is important to be careful with
comparisons, since carbonate deposition by encrusting calcifiers
at both contrasting conditions (conserved vs degraded reefs)

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 6 J. F. Alvarado-Rodríguez et al.

Fig. 4. Dendrogram of carbonate deposition of encrusting calcifiers based on group-average clustering using Bray–Curtis similarity (right) and 3d nMDS ordination
(left) for (A) Playa Las Gatas and (B) Islote Zacatoso during (J) June 2015 and (D) December 2015. The y axis shows the similarity percentage (%). (EUS) exposed
upper surface, (CUS) cryptic upper surface, (CBS) cryptic bottom surface and (EDS) exposed underside surface.

Table 2. Average rate of carbonate deposition (g CaCO3 m−2 d−1) of major encrusting calcifiers in groups A, B and C of Islote Zacatoso and contribution (i) to the
average similarity within of each group (A = 75.36, B = 77.08, C = 78.43)

i SD(i) i/SD(i) i% ∑i%

Group A
Calcareous algae 1.02 41.99 10.88 3.86 55.71 55.71
Polychaetes 0.27 19.16 7.05 2.79 25.42 81.14
Bryozoans 0.04 6.59 4.74 1.39 8.74 89.88
Molluscs 0.04 4.66 3.28 1.42 6.19 96.07
Group B
Barnacles 2.43 28.02 15.07 1.86 36.36 36.36
Calcareous algae 0.39 14.36 2.18 6.59 18.63 54.99
Bryozoans 0.38 12.93 3.51 3.68 16.78 71.76
Molluscs 0.39 11.86 4.05 2.93 15.39 87.16
Group C
Polychaetes 1.07 23.39 6.52 3.59 29.82 29.82
Calcareous algae 0.38 16.04 2.51 6.38 20.46 50.28
Molluscs 0.72 14.40 9.66 1.49 18.35 68.63
Barnacles 0.47 13.55 6.24 2.17 17.28 85.91

seems to be occur on a different scale (Table 6). At well conserved
coral reefs, good water quality have been related to high levels of
carbonate deposition (Mallela, 2007, 2013). As an example, at Rio
Bueno, in the Caribbean, the highest rates of carbonate deposition
were recorded on ceramic tiles at sites with good water quality
(between 0.13 and 0.54 g CaCO3 m−2 d−1). Such records were
made where sedimentation rates were lower than 0.1 g m−2 d−1
and water transparency was higher than 18 m (Mallela, 2007).
Reis et al. (2016), on other hand, reported carbonate deposition
rates between 1.19 and 2.04 g CaCO3 m−2 d−1 on cryptic and
exposed surfaces of PVC CAUs at Bahia, Brasil in South
Atlantic. They also reported the highest records at sites with
low sedimentation rates. At the Eastern Pacific, Price et al.
(2012) and Vargas et al. (2015) reported records of carbonate
deposition between 5.32 and 5.51 g CaCO3 m−2 d−1, respectively
in CAUs similar to those used in our study at well conserved

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 Journal of the Marine Biological Association of the United Kingdom 7

Table 3. Average rate of carbonate deposition (g CaCO3 m−2 d−1) of major encrusting calcifiers in groups A, B, C and D formed at 6 months in Playa Las Gatas and
Islote Zacatoso and contribution (i) to the average similarity within of each group (A = 79.09, B = 79.91, C = 84.07, D = 80.63)

i SD(i) i/SD(i) i% ∑i%

Group A
Calcareous algae 1.22 64.78 8.42 7.69 81.91 81.91
Polychaetes 0.10 10.15 3.11 3.26 12.83 94.74
Group B
Polychaetes 1.06 26.18 3.95 6.62 32.76 32.76
Bryozoans 0.47 17.31 5.58 3.10 21.66 54.43
Calcareous algae 0.42 17.04 3.68 4.62 21.33 75.76
Group C
Barnacles 10.27 44.49 5.40 8.24 52.93 52.93
Polychaetes 1.48 11.63 5.43 2.14 13.83 66.76
Bryozoans 0.60 11.15 2.24 4.97 13.26 80.01
Group D
Molluscs 3.39 30.20 5.92 5.10 37.45 37.45
Barnacles 2.19 20.62 7.44 2.77 25.58 63.03
Polychaetes 0.69 10.79 4.44 2.43 13.39 76.42
Calcareous algae 0.39 10.17 3.27 3.11 12.62 89.04

Fig. 5. Dendrogram of carbonate deposition of encrusting calcifiers based on group-average clustering using Bray–Curtis similarity (right) and 3d nMDS ordination
(left) for (PG) Playa Las Gatas and (IZ) Islote Zacatoso during (A) June 2015 and (B) December 2015. The y axis shows the similarity percentage (%). (EUS) exposed
upper surface, (CUS) cryptic upper surface, (CBS) cryptic bottom surface and (EDS) exposed underside surface.

reefs from Jarvis Island, EUA. Nonetheless, carbonate deposition intense sediment deposition. While sites with high water quality
rates recorded at these well-conserved sites (including records often coincide with high levels of light intensity and carbonate
from Islote Zacatoso), tend to be lower than records made at deposition at exposed surfaces (Mallela, 2013), at sites with low
Playa Las Gatas, the site with low water transparency and more water quality (e.g. caused by high sedimentation, phytoplankton

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 8 J. F. Alvarado-Rodríguez et al.

Table 4. Average carbonate deposition rate (g CaCO3 m−2 d−1) of major encrusting calcifiers in groups A, B, C and D formed at 12 months in Playa Las Gatas and
Islote Zacatoso and contribution (i) to the average similarity within of each group (A = 79.77, B = 87.41, C = 85.02, D = 81.89)

i SD(i) i/SD(i) i% ∑i%

Group A
Calcareous algae 1.08 43.87 6.93 6.33 54.99 54.99
Polychaetes 0.25 22.13 3.44 4.42 27.74 82.73
Molluscs 0.06 6.24 3.90 1.60 7.82 90.55
Group B
Barnacles 14.42 47.98 1.43 33.66 54.89 54.89
Polychaetes 5.42 25.49 4.86 5.24 29.16 84.05
Molluscs 1.02 6.39 4.37 1.46 7.31 91.36
Group C
Polychaetes 3.76 37.41 2.93 12.79 44.00 44.00
Molluscs 1.24 16.37 5.19 3.15 19.25 63.25
Barnacles 1.12 16.27 7.18 2.27 19.14 82.40
Calcareous algae 0.30 9.80 2.57 3.82 11.53 93.93
Group D
Molluscs 1.78 28.00 5.46 5.13 34.19 34.19
Polychaetes 0.74 19.65 3.29 5.96 23.99 58.18
Barnacles 0.85 14.02 7.49 1.87 17.12 75.31
Calcareous algae 0.40 13.84 3.43 4.04 16.90 92.20

Table 5. Average rate ( ± SD) of carbonate deposition (g CaCO3 m−2 d−1) recorded on both reefs for all taxa of encrusting calcifiers at each microhabitat during June
2015 (J) and December 2015 (D). (EUS) exposed upper surface, (CUS) cryptic upper surface, (CBS) cryptic bottom surface and (EDS) exposed underside surface

Playa Las Gatas Islote Zacatoso

Group Time EUS CUS CBS EDS EUS CUS CBS EDS

Calcareous J 0.67 ± 0.29 0.17 ± 0.04 0.25 ± 0.11 0.16 ± 0.05 1.04 ± 0.42 0.26 ± 0.06 0.46 ± 0.11 0.39 ± 0.06
algae
D 0.58 ± 0.22 0.21 ± 0.08 0.21 ± 0.08 0.17 ± 0.09 1.58 ± 2.15 0.26 ± 0.10 0.42 ± 0.19 0.70 ± 0.46
Bryozoans J 0.18 ± 0.09 0.67 ± 0.17 0.44 ± 0.28 0.68 ± 0.21 0.08 ± 0.05 0.52 ± 0.37 0.43 ± 0.17 0.38 ± 0.20
D 0.02 ± 0.01 0.13 ± 0.07 0.15 ± 0.07 0.16 ± 0.11 0.01 ± 0.01 0.07 ± 0.03 0.06 ± 0.03 0.16 ± 0.20
Molluscs J 4.55 ± 2.86 2.73 ± 2.70 3.69 ± 2.47 1.00 ± 0.43 0.04 ± 0.05 0.12 ± 0.10 1.47 ± 1.03 0.39 ± 0.28
D 3.17 ± 0.90 0.47 ± 0.16 1.44 ± 0.86 1.86 ± 2.12 0.02 ± 0.01 0.32 ± 0.45 0.58 ± 0.44 0.28 ± 0.30
Serpulid J 0.41 ± 0.39 1.26 ± 1.65 0.40 ± 0.24 2.37 ± 1.67 0.24 ± 0.22 0.94 ± 0.78 1.33 ± 1.17 0.37 ± 0.29
polychaetes
D 4.84 ± 5.03 2.38 ± 0.79 1.31 ± 1.58 4.50 ± 3.28 0.31 ± 0.30 0.60 ± 0.65 0.47 ± 0.21 0.97 ± 0.96
Barnacles J 4.77 ± 1.40 1.43 ± 1.21 1.26 ± 1.36 16.08 ± 8.16 0.11 ± 0.10 0.25 ± 0.15 0.65 ± 0.35 2.43 ± 1.50
D 2.15 ± 1.15 0.79 ± 0.61 0.70 ± 0.28 11.72 ± 6.73 0.01 ± 0.02 0.24 ± 0.35 0.18 ± 0.16 0.84 ± 0.68

productivity, dissolved organic matter and nutrient concentra-
tions) a different situation seems to occur: highest rates are
recorded at cryptic microhabitats.
At Playa Las Gatas, calcareous algae and bryozoans showed the
lowest rates of carbonate deposition. This site is highly impacted
by spill-out of residual waste water from the north side of
Zihuatanejo Bay (Izurieta et al., 2014) and such conditions have
been related to low cover of reef corals, high cover of filamentous
algae and high phytoplankton concentrations. The exposure of
this site to continuous anthropogenic impact accounts for per-
manent low levels of water transparency, although these stressful
conditions are more pronounced during summer, when the rain-
fall generates more intense runoff that carries sediments from the
land (Nava et al., 2014). At this site, the highest rate of carbonate
deposition was exerted by barnacles and molluscs during the first
6 months at EDS. Both invertebrates are rapid colonizers. In the
case of barnacles, larvae settlement may take place after only sev-
eral minutes of collector deployment (Geraci et al., 2008).
Additionally, EDS, exposed to water currents but not to sedimen-
tation, may be an ideal microhabitat for rapid settlement of larvae
with passive filtering behaviour. After 12 months of CAUs
exposure, when sedimentation decreased and water transparency

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 Journal of the Marine Biological Association of the United Kingdom 9

Table 6. Summary of carbonate deposition rates (g CaCO3 m−2 d−1) by encrusting calcifiers recorded on different experimental surfaces throughout the world.
Method: CAU (Calcification/Accretion Unit), PMS (Plastic Microscopic Slides). ‘All’ includes calcareous algae, bryozoans, molluscs, serpulid polychaetes and
barnacles

Deph Months of Encrusting Carbonate deposition

Region Site Method Habitat (m) exposure calcifiers (g CaCO3 m−2 d1) Reference

South Pacific Tikehau, French Porites – 1–2 24 Calcareous 3.10 ± 1.48 Pari et al.
Polynesia blocks algae (1998)
Takapoto, French Porites – 1–2 60 Calcareous 0.63 ± 0.06 Pari et al.
Polynesia blocks algae (2002)
Caribbean Rio bueno, Jamaica Ceramic Cryptic 10 12 All 0.19 ± 0.02 Mallela (2007)
tiles
Rio bueno, Jamaica Ceramic Exposed 10 12 All 0.44 ± 0.06 Mallela (2007)
tiles
Central Pacific Jarvis Island, USA CAU Cryptic & 5–10 6 All 5.32 Price et al.
exposed (2012)
Caribbean Florida, USA Plastic Vertical 4–6 24 Calcareous 1.30 Kuffner et al.
tiles algae (2013)
Caribbean Various sites, Ceramic Cryptic 10 12 All 1.70 ± 0.59 Mallela (2013)
Tobago tiles
Various sites, Ceramic Exposed 10 12 Calcareous 2.85 ± 0.82 Mallela (2013)
Tobago tiles algae
Various sites, Ceramic Vertical 10 12 All 1.68 ± 0.60 Mallela (2013)
Tobago tiles
Various sites, Ceramic Cryptic 10 12 Calcareous 1.1 0.02 Mallela (2013)
Tobago tiles algae
Various sites, Ceramic Exposed 10 12 Calcareous 0.29 ± 0.19 Mallela (2013)
Tobago tiles algae
Various sites, Ceramic Vertical 10 12 Calcareous 0.15 ± 0.02 Mallela (2013)
Tobago tiles algae
Various sites, Ceramic Cryptic 10 12 Bryozoans 0.06 ± 0.07 Mallela (2013)
Tobago tiles
Various sites, Ceramic Cryptic 10 12 Barnacles 0.01 ± 0.01 Mallela (2013)
Tobago tiles
Indo-Pacific Vabbinfaru, PVC pipes Vertical 1.5 12 All 1.28 ± 0.65 Morgan &
Maldives, Tobago Kench (2014)
Vabbinfaru, PVC pipes Vertical 1.5 12 Calcareous 1.24 ± 0.52 Morgan &
Maldives algae Kench (2014)
Mexican Puerto Morelos, Ceramic Exposed 2–4 24 All 0.20 Hepburn et al.
Caribbean Mexico tiles (2014)
Puerto Morelos, Ceramic Partially 2–4 24 All 1.31 Hepburn et al.
Mexico tiles cryptic (2014)
Pacific centre Jarvis Island, USA CAU Cryptic & 14–15 24 All 5.51 ± 0.90 Vargas et al.
and south exposed (2015)
Red Sea Saudi Arabia PMS Vertical 7.5–9 3 Calcareous 1.37 ± 0.25 Roik et al.
algae (2016)
South Atlantic Bahia, Brazil CAU Cryptic & 5 12 All 2.04 ± 0.07 Reis et al.
exposed (2016)
Bahia, Brazil CAU Cryptic & 3 12 All 1.44 ± 0.01 Reis et al.
exposed (2016)
Mexican Pacific Zihuatanejo, Mexico CAU Cryptic & ∼5 6 All 10.79 ± 3.84 This study
exposed
Zihuatanejo, Mexico CAU Cryptic & ∼5 6 Bryozoans 0.49 ± 0.17 This study
exposed
Zihuatanejo, Mexico CAU Cryptic & ∼5 6 Molluscs 2.99 ± 1.88 This study
exposed
Zihuatanejo, Mexico CAU Cryptic & ∼5 6 Barnacles 5.88 ± 2.66 This study
exposed
Zihuatanejo, Mexico CAU Cryptic & ∼5 12 Serpulid 3.26 ± 1.81 This study
exposed polychaetes
Zihuatanejo, Mexico CAU Cryptic & ∼5 12 Calcareous 0.74 ± 0.53 This study
exposed algae

Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
 10
rose, carbonate deposition increased at EUS and CUS by the same
taxa, with serpulid polychaetes arriving as late colonizers. Marine
invertebrates with filter feeding behaviour could benefit from a
high supply of suspended material (e.g. phytoplankton) that
results in individuals of higher size than others from less product-
ive areas (Sanford & Menge, 2001). Such environmental settings
are expected to influence the development of encrusting calcifiers
that consume dissolved nutrients and particulate organic matter
from the water column and hinder the development of photosyn-
thetic organisms that would have benefited from a more clear
water column (Fischer et al., 1995; Courtenay et al., 2005). In
fact, at sites with a high load of organic matter and nutrients, bar-
nacles may contribute almost 6 kg m−2 of calcareous material
after only 44 days of growth (Geraci et al., 2008).
In the opposite situation, CAUs from Islote Zacatoso showed
that calcareous algae and serpulid polychaetes were major contri-
butors of deposited carbonate at EUS throughout 12 months. Sites
with high water quality often coincide with high levels of light
irradiance and with dominance of calcareous algae at exposed
surfaces (Mallela, 2007). At this site, early colonizers that depos-
ited more carbonate at cryptic surfaces during June 2015 were
barnacles and serpulid polychaetes. Both cryptic taxa may be pro-
tected from clogging and sediment burial by growing in cryptic
habitats whose orientation prevents the settlement of sediment.
In serpulid polychaetes, it is known that their preferred habitats
are the more cryptic surfaces (Hepburn et al., 2014). Such taxa
exert a very important role on under-surfaces of coral reefs,
where their filtering activity may concentrate high amounts of
organic matter from the water column that may be liberated as
organic enriched pseudo faeces that can be horizontally trans-
ported by water currents (Brock & Smith, 1983). As was reported
by Mallela (2013) in the Caribbean, calcareous algae showed the
highest contribution at well-illuminated exposed surfaces and
both serpulid polychaetes and bivalves showed the highest contri-
bution at cryptic surfaces. Besides, Hepburn et al. (2014) noted
that carbonate production of serpulid worms recorded on ceramic
tiles was also negatively correlated to sediment exposure and
seemed to prosper at sites with high energy and low sediment
conditions. Thus, our results agree in that the conservation
state of reefs influences the composition of the structure of the
encrusting community.
The present study also reaffirms that the contribution to car-
bonate deposition by encrusting calcifiers is different across dis-
tinct levels of environmental exposure (e.g. cryptic and exposed
microhabitats) and that such contribution also is highly influ-
enced by water quality. As with pocilloporid corals, whose contri-
bution to carbonate deposition is near 143 g CaCO3 m−2 d−1 at
well-conserved reefs (Medellín-Maldonado et al., 2016), the con-
tribution of encrusting calcifiers seems to be comparatively low
again, according our data and previous studies (Table 6).
Nonetheless, assemblages of calcifying invertebrates seem to be
highly relevant in degraded reefs, where coral coverage is usually
low. Such results indicate that carbonate sequestration continues
even at coral degraded reefs where corals have been decimated.
Under the present scenario of global marine ecosystems degrad-
ation, this assumption must be considered during the analysis
of the balance of reef accretion.
Acknowledgements. We would like to thank Thierry Durand and Capitan
‘Chilolo’ for the logistical support provided during the sampling. Roberto
Dominguez ‘Bob’ helped in correcting the English text.
Financial support. This work was supported by the following sources of fund-
ing: CONACYT-SEP No.CB-2012-01-177537 and the Scientific Research
Coordination of the Universidad Michoacana de San Nicolás de Hidalgo.
Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
J. F. Alvarado-Rodríguez et al.
References
Azevedo FBB, Carloni GG and Carvalheira LV (2006) Colonization of ben-
thic organisms on different artificial substratum in Ilha Grande Bay, Rio de
Janeiro, Brazil. Brazilian Archives of Biology and Technology 49, 263–275.
Björk M, Mohammed SM, Bjorklund M and Semesi A (1995) Coralline
algae, important coral reef builders threatened by pollution. Ambio 24,
502–505.
Bray RJ and Curtis JL (1957) An ordination of the upland forest communities
of southern Wisconsin. Ecological Monographs 27, 325–349.
Brock RE and Smith SV (1983) Response of coral reef cryptofaunal commu-
nities to food and space. Coral Reefs 1, 179–183.
Bryant DG, Burke L, McManus J and Spalding M (1998) Reefs at Risk: A
Map-Based Indicator of Threats to the World’s Coral Reefs. Washington,
DC: World Resources Institute.
Carballo JL, Naranjo SA and García-Gómez JC (1996) The use of marine
sponges as stress indicators in marine ecosystems at Algeciras Bay
(Southern Iberian Peninsula). Marine Ecology Progress Series 135, 109–122.
Carriquiry JD, Cupul-Magaña AL, Rodríguez-Zaragoza F and Medina-
Rosas P (2001) Coral bleaching and mortality in the Mexican Pacific during
the 1997–98 El Niño and prediction from a remote sensing approach.
Bulletin of Marine Science 69, 237–249.
Clarke KR and Ainsworth M (1993) A method of linking multivariate com-
munity structure to environmental variables. Marine Ecology Progress Series
92, 205–219.
Cortés J and Risk MJ (1985) A reef under siltation stress: Cahuita, Costa Rica.
Bulletin of Marine Science 36, 339–356.
Courtenay G, Gladstone W and Schreider M (2005) Assessing the response
of estuarine intertidal assemblages to urbanised catchment discharge.
Environmental Monitoring Assessment 107, 375–398.
De’ath G, Fabricius KE, Swetman H and Puotinen M (2012) The 27-years
decline of coral cover on the Great Barrier Reef and its causes.
Proceedings of the National Academy of Sciences USA 109, 17995–17999.
Edinger EN, Jompa J, Limmon GV, Widjatmoko W and Risk MJ (1998)
Reef degradation and coral biodiversity in Indonesia: effects of land-based
pollution, destructive fishing practices and changes over time. Marine
Pollution Bulletin 36, 617–630.
Fabricius K and De’ath G (2001) Environmental factors associated with the
spatial distribution of crustose coralline algae on the Great Barrier Reef.
Coral Reefs 19, 303–309.
Fischer W, Krupp F, Scheider W, Sommer C, Carpenter KE and Niem VH
(1995) Guía FAO para la identificación de especies para los fines de la pesca.
Pacifico centro-oriental, vol. I. Plantas e Invertebrados. Rome: FAO.
Gardner TA, Côté IM, Gill JA, Grant A and Watkinson AR (2003)
Long-term región-wide declines in Caribbean corals. Science 301, 958–960.
Garrett P, Smith DL, Wilson AO and Patriquin D (1971) Physiography,
ecology, and sediments of two Bermuda patch reefs. Journal of Geology
79, 647–668.
Geraci JB, Amrhein C and Goodson CC (2008) Barnacle growth rate on arti-
ficial substrate in the Salton Sea, California. Hydrobiologia 604, 77–84.
Gherardi DFM and Bosence DWJ (1999) Modeling of the ecological succes-
sion of encrusting organisms in recent coralline-algal frameworks from Atol
das Rocas, Brazil. PALAIOS 14, 145–158.
Hepburn LJ, Blanchon P, Murphy G, Cousins L and Perry CT (2014)
Community structure and palaeoecological implications of calcareous
encrusters on artificial substrates across a Mexican Caribbean reef. Coral
Reefs 34, 189–200.
Izurieta DJ, Saldaña FP, Inclan BL, Sánchez CJ, Ordoñez FA, Ruiz LA,
Mijangos CM, Cortes MJ, Morales PR, Pérez LJ, Vélez MH,
Ramírez AI and Mejía TA (2014) Contaminación en la bahía de
Zihuatanejo. In Botello AV, Páez-Osuna F, Mendez-Rodríguez L,
Betancourt-Lozano M, Álvares-Borrego S, Lara-Lara R (eds), Pacífico
Mexicano. Contaminación e impácto ambiental: Diagnóstico y tendencias.
San Francisco de Campeche, CA: UAN, UNAM-ICMyL, CIAD-Mazatlán,
CIBNOR, CICESE, pp. 751–788.
Kuffner IB, Hickey TD and Morrison JM (2013) Calcification rates of the
massive coral Siderastrea siderea and crustose coralline algae along the
Florida Keys (USA) outer reef tract. Coral Reefs 32, 987–997.
Mallela J (2007) Coral reef encruster communities and carbonate production
in cryptic and exposed coral reef habitats along a gradient of terrestrial dis-
turbance. Coral Reefs 26, 775–785.
 Journal of the Marine Biological Association of the United Kingdom
Mallela J (2013) Calcification by reef-building sclerobionts. PLoS ONE 8, e60010.
Mallela J and Perry CT (2007) Calcium carbonate budgets for two coral reefs
affected by different terrestrial runoff regimes, Rio Bueno, Jamaica. Coral
Reefs 26, 53–68.
Martindale W (1976) Calcareous encrusting organisms of the recent and
Pleistocene reefs of Barbados, West Indies (PhD thesis). University of
Edinburgh, Scotland.
Martindale W (1992) Calcified epibionts as palaeoecological tools: examples
from the recent and Pleistocene reefs of Barbados. Coral Reefs 11, 167–177.
Maughan BC (2001) The effects of sedimentation and light on recruitment
and development of a temperate, subtidal, epifaunal community. Journal
of Experimental Marine Biology and Ecology 256, 59–71.
Medellín-Maldonado F, Cabral-Tena RA, López-Pérez A, Calderón-Aguilera LE,
Norzagaray-López CO, Chapa-Balcorta C and Zepeta-Vilchis RC (2016)
Calcificación de las principales especies de corales constructoras de arrecifes
en la costa del Pacífico del sur de México. Ciencias Marinas 42, 209–225.
Morgan KM and Kench PS (2014) Carbonate production rates of encruster
communities on a lagoonal patch reef: Vabbinfaru reef platform,
Maldives. Marine and Freshwater Research 65, 720–726.
Nava H, Ramírez-Herrera MT, Figueroa-Camacho AG and Villegas-
Sanchez BM (2014) Habitat characteristics and environmental factors
related to boring sponge assemblages on coral reefs near populated coastal
areas on the Mexican Eastern Pacific coast. Marine Biodiversity 44, 45–54.
Pari N, Peyrot-Clausade M, Campion-Alsumard TL, Hutchings P,
Chazottes V, Golubic S, Campion JL and Fontaine MF (1998)
Bioerosion of experimental substrates on high islands and on atoll lagoons
(French Polynesia) after two years of exposure. Marine Ecology Progress
Series 166, 119–130.
Pari N, Peyrot-Clausade M and Hutchings PA (2002) Bioerosion of experi-
mental substrates on high islands and atoll lagoons (French Polynesia) dur-
ing 5 years of exposure. Journal of Experimental Marine Biology and Ecology
276, 109–127.
Price NN, Martz TR, Brainard RE and Smith JE (2012) Diel variability in
seawater pH relates to calcification and benthic community structure on
coral reefs. PLoS ONE 7, e43843.
Rasser MW and Riegl B (2002) Holocene coral reef rubble and its binding
agents. Coral Reefs 21, 57–72.
R Core Team (2016) R: A Language and Environment for Statistical
Computing. Vienna: R Foundation for Statistical Computing. Available at
http://www.R-project.org/.
Reis VMD, Karez CS, Mariath R, de Moraes FC, de Carvalho RT,
Brasileiro PS, da Gama-Bahia R, da Cruz-Lotufo TM, Vieira-
Ramalho L, de Moura RL, Franchini-Filho RB, Pereira-Filho GH,
Lopes-Thompson F, Cardoso-Bastos A, Tavares-Salgado L and
Downloaded from https://www.cambridge.org/core. Columbia University Libraries, on 07 Aug 2019 at 18:42:01, subject to the Cambridge Core terms of use, available at
https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0025315419000638
11
Amado-Filho GM (2016) Carbonate production by benthic communities
on shallow coralgal reefs of Abrolhos Bank, Brazil. PLoS ONE 11, e0154417.
Reyes-Bonilla H (1993) 1987 coral reef bleaching at Cabo Pulmo reef, Gulf of
California, Mexico. Bulletin of Marine Science 52, 832–837.
Reyes-Bonilla H, Carriquiry JD, Leyte-Morales GE and Cupul-Magana AL
(2002) Effects of the El Niño–Southern Oscillation and the Anti-El Niño
event (1997–1999) on coral reefs of the western coast of Mexico. Coral
Reefs 21, 368–372.
Roik A, Roder C, Röthig T and Voolstra CR (2016) Spatial and seasonal reef
calcification in corals and calcareous crusts in the central Red Sea. Coral
Reefs 35, 681–693.
Rützler K (2002) Impacts of crustose clionid sponges on Caribbean reef corals.
Acta Geologica Hispanica 37, 61–72.
Sanford E and Menge BA (2001) Spatial and temporal variation in barnacle
growth in a coastal upwelling system. Marine Ecology Progress Series 209,
143–157.
Seaturtle.Org (2002) Seaturtle.Org Maptool Available at http://www.seaturtle.
org/maptool. (Accessed July 2016).
Semar-Digaohm (2015) Available at http://digaohm.semar.gob.mx/ (Accessed
July 2015).
Scoffin TP (1992) Taphonomy of coral reefs: a review. Coral Reefs 11, 57–77.
Sokal RR and Rohlf FJ (1981) Biometry: The Principles and Practice of
Statistics in Biological Research, 2nd Edn. San Francisco, CA: W.H.
Freeman.
Stearn CW, Scoffin TP and Martindale W (1977) Calcium carbonate budget
of a fringing reef on the West coast of Barbados. Bulletin of Marine Science
27, 479–510.
Steneck RS and Adey WH (1976) The role of environment in control of
morphology in Lithophyllum congestum, a Caribbean algal ridge builder.
Botanica Marina 19, 197–2015.
Vargas-Ángel B, Richards CL, Vroom PS, Price NN, Schils T, Young CW,
Smith J, Johnson MD and Brainard RE (2015) Baseline assessment of net
calcium carbonate accretion rates on U.S. Pacific reefs. PLoS ONE 10,
e0142196.
Vásquez-Elizondo RM and Enríquez S (2016) Coralline algal physiology is
more adversely affected by elevated temperature than reduced pH.
Scientific Reports 5, 19030.
Warwick RM and Clarke KR (1991) A comparison of some methods for ana-
lysing changes in benthic community structure. Journal of the Marine
Biological Association of the United Kingdom 71, 225–244.
Warwick RM, Clarke KR and Suharsono (1990) A statistical analysis of coral
community responses to the 1982–83 El Niño in the Thousand Islands,
Indonesia. Coral Reefs 8, 171–179.
Zar JH (1984) Biostatistical Analysis. Upper Saddle River, NJ: Prentice-Hall.