Marine Ecology. ISSN 0173-9565
ORIGINAL ARTICLE
Spatial distribution of surgeonfish and parrotfish in the
north sector of the Mesoamerican Barrier Reef System
ndez-Landa1, Gilberto Acosta-Gonza
lez1, Enrique Nu
~ ez-Lara2 &
n
Roberto C. Herna
1
lez
s E Arias-Gonza
Jesu
n y Estudios Avanzados del I.P.N-Unidad, Me
rida, Yucat
1 Centro de Investigacio
an, M
exico
noma del Carmen, Ciudad del Carmen, Campeche, M
2 Facultad de Ciencias Naturales, Universidad Auto
exico
Keywords
Coral; distribution patterns; herbivorous fish
assemblage; Mesoamerican Reef System; reef
habitat; rugosity.
Correspondence
s
Roberto Carlos Hern
andez-Landa and Jesu
Ernesto Arias-Gonz
alez, Centro de
n y Estudios Avanzados del I.P.NInvestigacio
erida Antigua Carretera a Progreso
Unidad. M
km 6, M
erida, Yucat
an C.P. 97310, Mexico.
E-mail: rhlanda73@hotmail.com; earias@mda.
cinvestav.mx
Accepted: 28 January 2014
doi: 10.1111/maec.12152
Abstract
Surgeonfish and parrotfish play an important role in structuring the benthic
communities of coral reefs. However, despite their importance, little is known
about their distribution patterns in the north sector of the Mesoamerican Reef
System. This study evaluated the distribution of these fish in 34 sites in four
habitats (lagoon, front, slopes and terrace) along a depth gradient (c 0.5–20 m).
These herbivorous fish were assessed by visual censuses. Species dominance was
evaluated for each habitat using SIMPER analysis. Habitat characteristics data
were collected to determine the relationship between habitat conditions and spatial variations in herbivorous fish (using abundance and biomass as a proxy) via
redundancy analysis. The herbivorous fish assemblage had a low density (fish
per 100 m2) and biomass (g100 m 2) in comparison with assemblages in similar studies. In contrast, species richness was high compared with other studies in
the Caribbean. Spatial variation of the abundance, biomass and size of herbivorous fish was strongly related to coral and seagrass cover, as well as to depth and
rugosity. These four variables were critical in controlling the distribution patterns of the herbivorous fish assemblages. No associations were found between
fish and macroalgae or any other benthic group. The present study indicates that
the species richness of surgeonfish and parrotfish was not regionally affected by
the dominance of macroalgae in the habitats studied. Seagrass beds and the coral
reef matrix need to be preserved for the herbivorous fish assemblages to remain
healthy and capable of controlling excess macroalgae growth.
Introduction
Understanding the distribution patterns of herbivorous
coral reef fish is of practical importance to the management
and conservation of coral reefs (Mumby 2006; Hughes
et al. 2007). Two of the most dominant herbivorous taxa
in the Western Atlantic are the acanthurids and scarine
labrids (surgeonfish and parrotfish). The ecological significance of this group of fish on coral reefs has been associated with ecosystem function, playing an important role in
structuring the benthic communities of coral reefs (Hughes
1994; Belliveau & Paul 2002; Hoey & Bellwood 2008).
Surgeonfish and parrotfish are commonly distributed on
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
fore-reef habitats at depths of 1–30 m and are important in
terms of abundance and biomass (Lewis & Wainwright
1985). The biological structure of these fish varies over a
wide range of spatial scales, associated with their feeding
and shelter requirements (Hoey & Bellwood 2008; Nemeth
& Appeldoorn 2009; Adam et al. 2011; Kopp et al. 2012).
For example, they can vary among adjacent zones within
reefs (e.g. lagoon, crest and slope) as well as with location
on the continental shelf or with differences in environmental parameters at a regional level (Williams & Hatcher
1983; Russ 1984a,b; Gust et al. 2001; Hoey & Bellwood
2008; Nemeth & Appeldoorn 2009; Kopp et al. 2012).
However, despite their importance, little is known about
1
Surgeonfish and parrotfish in the nsMARS
their abundance and distribution patterns over spatial and
temporal gradients in the north sector of the Mesoamerican Barrier Reef System (nsMBRS).
The distributions of surgeonfish and parrotfish can
provide insights into their environmental preferences and
restrictions to potential areas that the fish can occupy
(Johansen et al. 2008). Some species with low abundance
or those with restricted distributions and limited environmental tolerances may be the most susceptible to changes
in habitat characteristics (Cheal et al. 2010). Previous
studies have highlighted the importance of rugosity (Risk
1972; Luckhurst & Luckhurst 1978; Chabanet et al. 1997;
Hoey & Bellwood 2009) and percentage live cover,
including coral (Vincent et al. 2011) and seagrass (Edgar
& Shaw 1995; Hemminga & Duarte 2000), as well as predation, herbivore social behaviour (e.g. herding), depth,
water movement and management practices (Coughenour
1991; Nemeth & Appeldoorn 2009; Kopp et al. 2012).
The reefs of the nsMBRS possess discrete habitats distributed along a depth gradient, which start in a shallow
reef lagoon (c 1.5 m depth) and extend to the deepest
~ez-Lara & Ariashabitat of the reef terrace (c 20 m) (N
un
~ez-Lara et al. 2005). This is useful for
Gonzalez 1998; N
un
describing distribution patterns of abundance, size and
functional characteristics in order to relate these to habitat geomorphology. These habitats are affected by the
recurrent impact of natural disturbances (e.g. hurricanes)
(Almada-Villela et al. 2003) and human activities (e.g.
fishing, tourism and coastal development), which have
~ez-Lara
increased substantially in the last decade (N
un
et al. 2005; Arias-Gonzalez et al. 2008; Arias-Gonzalez
et al. 2011). Consequently, these habitats tend to be dominated by macroalgae and relatively low coral cover
(Bozec et al. 2008; Acosta-Gonzalez et al. 2013).
A number of studies have assessed the status of benthic
communities and fish assemblages (mainly those of com~ez-Lara & Arias-Gonzalez 1998;
mercial importance) (N
un
Anderson et al. 2008; Rodrıguez-Zaragoza & AriasGonzalez 2008; ECO-AUDIT 2011; Acosta-Gonzalez et al.
2013). However, none of these studies has focused particularly on analyzing herbivorous fish. We assume that surgeonfish and parrotfish on the nsMBRS are not randomly
distributed but that their distribution and community
structure is influenced by habitat characteristics such as
coral and seagrass cover, rugosity and depth and not by
the high homogenization of the reef bottom by macroalgae. Given the lack of knowledge on the spatial distribution of this group of fish on the nsMBRS, the aims of
this study were (i) determine the distribution patterns of
surgeonfish and parrotfish along a depth gradient and for
habitats of different structural complexity and (ii) quantify the morpho-functional benthic groups in order to
identify which environmental conditions underpin the
2
~ez-Lara & Arias-Gonz
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species assemblage. This baseline information is important for identifying the potential environmental factors
that influence surgeonfish and parrotfish distribution in
order to establish management criteria. These are essential for improving our understanding of herbivorous fish
abundance and distribution patterns in the nsMBRS.
Material and Methods
Study area
Ten reefs distributed along approximately 400 km of
Mexican Caribbean coast in the north sector of the Mesoamerican Barrier Reef System (nsMBRS) were studied as
part of a long-term study that began in 2000. We present
the information for this year because of the importance
of generating a historical baseline for herbivorous fish
assemblages in the nsMBRS. The reefs chosen form a
semi-continuous barrier that starts in Punta Nizuc in the
north and extends to Xcalak in the south (21°000 N,
86°460 W to 18°160 N, 87°490 W) (Fig. 1). From the coast
seawards, these reefs present five characteristic habitats: a
shallow reef lagoon (c 0.5 m depth), which extends to the
crest (the seawards transition to deeper habitats), front (c
~ez-Lara
6 m), slope (c 12 m) and terrace (c 20 m) (N
un
~ez-Lara et al. 2005).
& Arias-Gonzalez 1998; N
un
Sampling protocol
The reefs chosen were separated by 30–70 km. Thirtyfour sites were sampled within these reefs, corresponding
to 10 lagoons, 10 fronts, seven slopes and seven terraces
(Fig. 1). The reefs of Punta Nizuc, Puerto Morelos and
Punta Maroma only have two well defined habitats
(lagoon and front), whereas the other reefs also have a
slope and terrace (Fig. 1).
Herbivorous fish assemblages
Diurnal visual censuses (08.00–16.00 h) were performed
to quantify the surgeonfish and parrotfish. The species of
both families were included in this study because they are
believed to be particularly important in the prevention of
the uncontrolled growth of macroalgae in the Caribbean
(Mumby 2006). Twelve transects (50 m long 9 2 m
wide) were sampled at each site. These were positioned
parallel to the coast and separated from one another by
50 m. The depth (m) was recorded at the beginning of
each transect. The fish of both families observed along
the transects were counted, identified to species and their
total length (TL in cm) was estimated visually. Subsequently, the total length was converted into biomass
using the allometric function W = a Lb, where W is the
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
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Surgeonfish and parrotfish in the nsMARS
Fig. 1. (a) Study area: Ten reefs were chosen
along the Mexican Caribbean coast which
corresponds to the north sector of the
Mesoamerican Reef System (nsMARS). (b)
Sampling design: Reef and code name.
Asterisks show the habitats sampled per reef
along the depth gradient. (c) Reef profile:
Lagoon (0.5 m), front (6 m), slope (12 m) and
reef terrace (20 m).
mass of the fish (g), L represents total length (cm), and a
and b are specific constants (Froese & Pauly 2010).
Coral reef benthic communities
The benthic community was quantified by means of
video-transects (50 m in length 9 0.5 m wide) using an
underwater video-camera kept at 40 cm above the substrate (Aronson & Swanson 1997; Osborne & Oxley 1997).
The fish visual censuses were performed along the same
video-transects, following the protocol previously used by
Arias-González et al. (2011) and Acosta-Gonzalez et al.
(2013). The cover of the following morpho-functional
benthic groups recorded was considered as environmental
variables: seagrass (Thalassia sp.), coral, macroalgae
(including the following genera: Sargassum, Dictyota, Stypopodium, Padina and Lobophora), turf algae, crustose coralline algae, calcareous algae of the genus Halimedae,
hydrocoral, octocoral and sponge. The inert substrates
bare substrate, rubble and sand were also recorded.
Rugosity index (RI)
The rugosity index was obtained using the chain method,
which consisted of placing a chain 18 m in length over
the sea floor, following the bottom contour. The equation
for estimating the rugosity index (RI) was: 1 – (dm/Lt),
where dm is the distance covered by the chain along the
transect from start to finish, and Lt is the length of the
chain (Risk 1972). The mean of all transects in each habitat was calculated to generate a single rugosity index (RI)
value per habitat.
Data analysis
For each habitat studied, the fish were analyzed in the
following categories: (i) all herbivorous fish (surgeonfish
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
and parrotfish together), and by family (ii) surgeonfish
and (iii) parrotfish. Diversity was described based on species richness. Each category was analyzed in terms of density (individuals per 100 m2), biomass (g100 m 2) and
average size (cm), compared among habitats. The statistical assumption of a normal distribution was not met,
hence the above attributes were analyzed using multiple
non-parametric Kruskal–Wallis test comparisons (H test,
P > 0.05) (INFOSTAT version 2010, Di Rienzo et al.
2010). The percentage contribution of density and biomass of the fish assemblage in each habitat was assessed
by a SIMPER analysis using the PRIMER v6 program
(Anderson et al. 2008).
To identify associations between the total abundance
and biomass of the herbivorous fish and the cover of different benthic functional groups, a canonical redundancy
analysis (RDA) was performed (Rao 1964), using the CANOCO v4.5 program (ter Braak & Smilauer 2002). This
technique was used to relate the species abundance for a
response variables matrix (Y), to a correspondence
matrix of environmental or explanatory variables (X)
(Legendre & Legendre 1998). The first step consisted of
evaluating the gradient length, i.e. the unimodality of the
species data (in terms of abundance and biomass) along
an ordination axis, using detrended correspondence
analysis (DCA). If the resulting value is <4, it supports
the use of the redundancy analysis (RDA; ter Braak &
Smilauer 2002), as was the case in the present study.
Monte Carlo randomizations were used based on 999
iterations to determine the significance of the canonical
axes for the fish and environmental variables. The analysis was performed using a variance inflation factor (VIF)
below 20 to avoid severe multicollinearity. The following
benthic functional groups (biotic and abiotic) were considered as environmental variables: seagrass, coral, macroalgae, turf, crustose coralline algae, calcareous algae,
hydrocoral, octocoral, sponge, bare substrate, rubble,
3
Surgeonfish and parrotfish in the nsMARS
sand and rugosity index. Depth was considered as a supplementary variable in the analysis. In accordance with
Legendre & Gallagher (2001), the species abundance and
biomass matrixes were transformed a priori into Hellinger distances. Legendre & Legendre (1998)demonstrated
that this transformation makes species abundance or biomass data amenable to RDA. The significance (P < 0.05)
of the variables was tested using a forward automatic
selection analysis.
Results
Herbivorous fish assemblage structure
We recorded three species of surgeonfish and 12 of parrotfish. The absolute abundance of fish per habitat was
1058, 2077, 1433 and 1411 for the lagoons, fronts, slopes
and terraces, respectively. The most numerically important species was Acanthurus bahianus (Abah), followed by
Acanthurus coeruleus (Acoe) Sparisoma aurofrenatum
(Saur), Scarus iseri (Sise) and Sparisoma viride (Svir),
which constituted 66.8% of the total abundance. In
descending order, the remaining 33.2% consisted of
Acanthurus chirurgus (Achi), Scarus taeniopterus (Stae),
Sparisoma chrysopterum (Schy), Sparisoma rubripinne
(Srub), Sparisoma radians (Srad), Scarus vetula (Svet),
Sparisoma atomarium (Sato), Cryptotomus roseus (Cros),
Scarus coelestinus (Scoel) and Scarus coeruleus (Scoer). Following the depth gradient, the total species richness was
13, 12, 12 and 13, with an average number of species
(SE) per habitat of 8.6 2.0, 9.8 1.3, 11.5 0.9,
and 9.4 0.9, respectively, for the lagoon, front, slope
and terrace. Species richness varied significantly between
habitats as follows: fronts 6¼ lagoons 6¼ slopes 6¼ terraces
(Kruskal–Wallis, H = 11.9743, P = 0.007).
All herbivorous fish
The lagoon and the front showed the greatest densities of
herbivorous fish, which were different to the densities
registered for the slope and terrace. From the lagoon to
the terrace the general fish density decreased by 27.3%.
Biomass increased by 47.2% from the lagoon (where the
lowest values were recorded) to the front, and by 40.2%
from the lagoon to the terrace. The greatest biomass was
concentrated on the front. Similarly, the average fish size
increased significantly from the lagoon to the terrace by
40.6% (Fig. 2a, Table 1).
By family: surgeonfish and parrotfish
The lagoon was dominated (4.5 fish100 m 2) by small
surgeonfish (average 11.7 cm), contributing a relatively
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low biomass to the general assemblage of this habitat.
From the lagoon to the terrace the density of surgeonfish decreased significantly by 52.5%. An increase in
the size of the surgeonfish of 34.7% was found between
these two habitats, where the largest fish were found
(average 17.9 cm). The greatest biomass of surgeonfish
was concentrated on the front (537.8 g100 m 2), which
decreased by 38.8 and 35.1% towards the slope and the
terrace, respectively. The smallest parrotfish (average
12.8 cm) were recorded in the lagoon. The density of
parrotfish remained relatively constant across all habitats and no statistically significant differences were
found. The size of the fish increased significantly
(34%) on the terrace, where the largest fish were concentrated (average 19.5 cm). Maximum parrotfish biomass was estimated for the terrace and front (512.1
and 497.7 g100 m 2, respectively), and varied significantly with respect to the other habitats (Fig. 2b–d,
Table 1).
SIMPER analysis: abundance and biomass contribution
The five species that together contributed more than 75%
of the abundance and biomass of each habitat are shown
in Fig. 3. In terms of abundance (Fig. 3a, Table 2), Abah
contributed most to the lagoon and front, with 336 and
497 fish, representing 38.4% and 37.6% of the total abundance, respectively. On the slope, with 166 fish recorded,
Acoe represented the greatest contribution of abundance
for this assemblage at 17.7%. Abah, Acoe, Saur, Sise, Svir
were the dominant species on the front and slope,
although there was a greater homogeneity in the contribution percentages between the slope species. On the terrace, Sise contributed 24.8% of the abundance with 251
fish. In terms of biomass (Fig. 3b, Table 2), Acoe was represented by fish of an average size of 12.7 cm, which contributed 29.0% of the total biomass of the lagoon. On the
front, the average size of Abah was 13.3 cm, contributing
19.5% of the total biomass. This surgeonfish was followed
by two conspicuous parrotfish, Svir and Sru, the largest
reaching 20 cm. Finally, the importance of Svir on the
slope and terrace was highlighted by the presence of the
largest fish of approximately 22 cm. These contributed
32.6% and 41.5% of the total biomass of these habitats,
respectively. Other species, including Stae, showed a substantial increase in the number of fish counted, from 17
fish in the lagoon to 134 fish on the terrace, where it was
one of the most important species, contributing 11.7%
(Fig. 3a, Table 2). Sub was present from the lagoon to
the slope but was not recorded in the terrace assemblage.
Other species were recorded in a single habitat, as was
the case of Cros in the lagoon, and Scoer and Scoel on the
terrace (Table 2).
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Surgeonfish and parrotfish in the nsMARS
(a)
(b)
(c)
(d)
Fig. 2. Distribution patterns of the Density
(Fish/100 m2), Biomass (g/100 m2) and Size
(cm) for (a) “All herbivorous fish” and by
family (surgeonfish and parrotfish) in figures
(b), (c) and (d), respectively.
Benthic community structure
The status of the environmental variables by habitat is
presented in Fig. 5a and b. Seagrass cover (29.1% 6.9)
was the dominant benthic component in the lagoons.
Coral cover increased gradually along the depth gradient,
with the greatest value recorded on the terrace
(25.0% 1.9). The algal assemblage was dominated by
macroalgae, with the greatest percentage recorded on the
front (47.0% 7.7). Turf algae showed generally low percentages (<1.0%), as did the hydrocorals, whereas the covers of crustose coralline algae and calcareous algae were
moderately important on the slope and the terrace
(5.4% 1.3 and 12.1% 0.8, respectively). The octocorals were well represented in all the habitats, with the
maximum cover recorded on the terrace (17.5% 1.6).
Regarding the inert substrates, bare substrate was relatively
important on the front (14.7% 6.3) and the greatest
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
rubble cover was recorded on the terrace (7.8% 2.5)
(Fig. 4a, Table 3). The RI varied significantly among habitats. The lagoon presented the lowest rugosity due to its
lack of coral formations. On the slope and front similar
rugosity values were recorded, reaching its highest value
on the terrace (RI = 0.5) (Fig. 4b & Table 3).
RDA: fish and benthic community associations
Along the first four axes the RDA showed a cumulative
percentage variance of 38.2 and 31.7% in the occurrence of
herbivorous fish species with regards to abundance and
biomass, respectively. A strong relationship was identified
for the environmental variables tested along the first and
second axis. The Monte Carlo permutation test indicated a
significant correlation between the canonical axes and the
environmental variables (P < 0.05, 999 permutations) of
R2 = 0.9 for abundance and R2 = 0.8 for biomass. Only
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Surgeonfish and parrotfish in the nsMARS
Table 1. Mean (SE) density (fish per 100 m2), biomass (g100 m 2) and size (cm) for the categories: ‘All herbivorous fish’, ‘surgeonfish’ and
‘parrotfish’ by habitat along a depth gradient.
all herbivorous fish
lagoon
front
slope
terrace
density (fish100 m 2) (SE)
H = 22.4, P < 0.05
biomass (g100 m 2) (SE)
H = 125.4, P < 0.05
size (cm) (SE)
H = 175.1, P < 0.05
7.3
6.9
5.7
5.3
272.3
514.7
358.1
455.8
11.3
17.4
16.4
19.0
(0.5),
(0.6),
(0.4),
(0.2),
A
A
B
A
H = 42.8, P < 0.05
surgeonfish
lagoon
front
slope
terrace
4.5
4.3
2.7
2.1
(0.3),
(0.4),
(0.1),
(0.1),
C
C
B
A
H = 1.6, P > 0.05
parrotfish
lagoon
front
slope
terrace
2.8
2.7
2.9
3.2
(0.2),
(0.1),
(0.2),
(0.3),
n.s.
n.s.
n.s.
n.s.
(36.9),
(56.1),
(24.8),
(34.5),
A
C
B
C
(0.4),
(0.3),
(0.3),
(0.4),
A
B
C
D
H = 26.6, P < 0.05
H = 68.8, P < 0.05
258.8
537.2
375.8
352.0
11.7
15.2
16.0
17.9
(36.9),C
(11.5), B
(30.8), A
(36.4), A
(0.5),
(0.3),
(0.3),
(0.4),
A
B
B
C
H = 55.9, P < 0.05
H = 74.1, P < 0.05
324.8
497.7
331.3
512.1
12.8
19.1
16.5
19.5
(66.0),
(45.2),
(33.4),
(49.2),
A
B
C
B
(0.6),
(0.7),
(0.4),
(0.5),
A
B
C
B
Letters represent significant differences provided by a Kruskal–Wallis multiple comparison (H-test, P < 0.05). n.s. = no significant differences.
(b) Biomass
(a) Abundance
Lagoon
8.0%
7.3%
29.0
16.3%
14.9%
11.7%
Saur
Achi
Acoe
Abah
Achi
Svir
38.4% 16.8% 12.0%
10
20
30
40
Abah
Acoe Srad
Front
10
20
30
40
Slope
10
20
30
40
9.8%
Srub
37.5%
17.8%
16.7%
8.1%
7.0%
19.5%
18.9%
18.4%
14.5%
8.7%
Abah
Acoe
Saur
Sise
Svir
Abah
Svir
Srub
Acoe
Saur
17.7%
15.1%
Acoe
Abah
15.0%
14.5%
Saur
13.4%
Sise
Svir
32.6%
13.5%
Svir
Srub
13.1%
Acoe
11.3%
Achi
7.9%
Abah
Terrace
10
20
30
40
24.8%
20.9%
15.0%
Sise
Saur
Acoe
13.6%
11.7%
Svir
Stae
500 600 700 900 1600
Distance to coast (m)
41.5%
Svir
11.5%
Acoe
11.4%
Saur
11.0%
7.2%
Sise
Achi
Fig. 3. SIMPER analysis. In decreasing order (left to right), the five main species which together contributed more than 75% of the (a)
Abundance and (b) Biomass, and contribution percentage of each one of these species. Reef profile: Fish illustrations modified from FAO 2002.
the first two canonical axes were used and included the
maximum variability expressed by the environmental variables. These axes explained 40.8 and 58.1% of the abundance and 31.8 and 55.2% of the biomass on the first and
second axis, according to the cumulative percentage variance in the species-environmental variables occurrence
6
relationship. The environmental variables that proved to be
significantly associated with the distribution patterns of
abundance were depth and the rugosity index (RI), seagrass
and coral cover (Fig. 5a). For biomass, the associated variables were seagrass and coral cover (Fig. 5b). In terms of
abundance, Srad, Achi and other species of lower numerical
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
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Surgeonfish and parrotfish in the nsMARS
Table 2. Habitats and depth gradient. Species composition for each habitat arranged in alphabetical order, code, total abundance, percentage
contribution (%) of abundance and biomass, and mean (SE), minimum and maximum size.
contribution of
size (cm)
habitat
species name
code
total abundance
abundance (%)
biomass (%)
mean
(SE)
minimum
maximum
lagoon (0.5 m)
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Cryptotomus roseus
Scarus iseri
Scarus taeniopterus
Scarus vetula
Sparisoma atomarium
Sparisoma aurofrenatum
Sparisoma chrysopterum
Sparisoma radians
Sparisoma rubripinne
Sparisoma viride
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Scarus iseri
Scarus taeniopterus
Scarus vetula
Sparisoma atomarium
Sparisoma aurofrenatum
Sparisoma chrysopterum
Sparisoma radians
Sparisoma rubripinne
Sparisoma viride
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Scarus iseri
Scarus taeniopterus
Scarus vetula
Sparisoma atomarium
Sparisoma aurofrenatum
Sparisoma chrysopterum
Sparisoma radians
Sparisoma rubripinne
Sparisoma viride
Acanthurus bahianus
Acanthurus chirurgus
Acanthurus coeruleus
Scarus coelestinus
Scarus coeruleus
Scarus iseri
Scarus taeniopterus
Scarus vetula
Sparisoma atomarium
Sparisoma aurofrenatum
Sparisoma chrysopterum
Sparisoma radians
Sparisoma viride
Abah
Achi
Acoe
Cros
Sise
Stae
Svet
Sato
Saur
Schr
Srad
Srub
Svir
Abah
Achi
Acoe
Sise
Stae
Svet
Sato
Saur
Schr
Srad
Srub
Svir
Abah
Achi
Acoe
Sise
Stae
Svet
Sato
Saur
Schr
Srad
Srub
Svir
Abah
Achi
Acoe
Scoel
Scoer
Sise
Stae
Svet
Sato
Saur
Schr
Srad
Svir
336
98
161
2
79
17
6
4
99
25
76
55
100
497
124
390
173
74
13
3
247
45
8
96
162
143
65
166
177
62
13
12
166
85
12
50
151
101
46
145
2
1
251
134
6
6
226
37
2
124
38.4
7.3
16.8
0.04
4.8
0.7
0.03
0.2
8.0
2.4
12.0
2.7
6.7
37.6
3.4
17.8
8.1
2.7
0.4
0.1
16.7
1.8
0.2
4.3
7.0
15.1
4.7
17.7
14.5
6.3
0.9
0.4
15.0
6.7
1.0
4.3
13.4
7.9
3.0
15.0
0.0
0.0
24.8
11.7
0.2
0.1
20.9
2.8
0.0
13.6
16.2
14.9
29.0
0.01
1.8
0.2
0.3
0.1
8.6
5.4
2.0
9.8
11.7
19.5
8.5
14.5
3.8
1.6
1.9
0.10
8.7
4.4
0.0
18.4
18.9
7.9
11.3
13.1
5.3
1.7
6.4
0.0
5.1
3.1
0.1
13.5
32.6
4.0
7.2
13.6
0.0
0.0
11.0
6.0
0.5
0.0
11.4
4.8
0.0
41.5
10.8
12.3
12.7
6.0
9.2
13.1
25.5
8.5
13.3
18.3
6.7
21.7
13.9
13.3
20.3
15.5
12.6
14.9
26.8
6.0
16.1
26.7
6.0
27.5
22.7
14.1
19.6
15.6
13.5
11.1
29.8
6.0
14.0
14.9
7.8
26.9
22.1
15.5
23.0
17.1
59.0
46.0
15.2
17.8
30.8
6.0
16.0
21.5
6.0
26.7
0.8
1.5
0.8
0.0
1.2
2.9
10.5
2.5
1.1
2.8
0.4
1.6
2.2
0.4
0.8
0.4
0.7
0.7
3.4
0.0
0.6
1.5
0.0
1.2
1.1
0.5
0.9
0.4
0.7
0.8
2.8
0.0
0.6
0.8
1.2
1.3
1.1
0.4
1.1
0.5
0.0
0.0
0.6
0.9
3.0
0.0
0.6
2.0
0.0
1.4
5.0
1.5
5.0
6.0
6.0
6.0
15.0
6.0
6.0
6.0
6.0
6.0
6.0
5.0
16.0
6.0
6.0
6.0
16.0
6.0
6.0
6.0
6.0
11.0
6.0
5.0
6.0
6.0
6.0
6.0
16.0
6.0
1.0
6.0
6.0
16.0
5.0
6.0
15.0
11.0
59.0
46.0
6.0
6.0
25.0
6.0
6.0
3.0
6.0
6.0
24.0
34.0
26.0
6.0
16.0
26.0
36.0
16.0
26.0
36.0
16.0
36.0
52.0
21.0
26.0
26.0
21.0
21.0
43.5
6.0
26.0
36.0
6.0
44.0
36.0
26.0
26.0
26.0
26.0
16.0
51.0
6.0
26.0
26.0
16.0
36.0
36.0
26.0
36.0
36.0
59.0
46.0
26.0
37.0
36.0
6.0
26.0
36.0
6.0
52.0
front (6 m)
slope (12 m)
terrace (20 m)
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
7
~ez-Lara & Arias-Gonz
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andez-Landa, Acosta-Gonz
alez, Nu
alez
Surgeonfish and parrotfish in the nsMARS
(a)
(b)
Fig. 4. (a) Benthic community measurements, (b) Rugosity index
values (RI).
occurrence, such as Cros and Sato, were significantly associated with the seagrass vector. Schr, Saur and Svir were associated with rugosity for the slopes (Fig. 5a). On the terrace,
two of the most conspicuous parrotfish, Sise and Sate, were
associated with the depth and coral cover vectors. Sise was
predominant in this habitat (251 fish, with an average size
of 15.2 cm) (see Table 2), followed by Stae (134 fish and
average size of 17.5 cm). Scoer and Scoel were only
recorded on the terrace and were mainly associated with
coral cover (Fig. 4a, Table 2). In terms of biomass
(Fig. 5b) Srad was also strongly associated with seagrass.
Stae, Saur and Sise were strongly associated with coral
cover, as were the largest parrotfish, Scoel and Scoer, with
sizes of 56 and 60 cm, respectively.
Discussion
Herbivorous fish assemblage
We found wide variations in the spatial distribution and
structure of the surgeonfish and parrotfish assemblage on
the nsMBRS. An important finding was the high total
species richness, particularly for parrotfish, compared
with that recorded in similar studies on the Caribbean
region. Lewis & Wainwright (1985) reported nine species
on reefs in Belize (three surgeonfish and six parrotfish).
Nemeth & Appeldoorn (2009) recorded 11 species (three
surgeonfish and eight parrotfish) on reefs in Puerto Rico.
Toller et al. (2010) (Saba Bank reef, Netherlands Antilles)
recorded nine species (three surgeonfish and six parrotfish). Kopp et al. (2012) reported between six and 10 species of both families on the reef flats and from six to
nine species on the reef slopes of Guadaloupe Island.
Based on the above, the nsMBRS surgeonfish and parrotfish assemblage may be considered relatively well structured in terms of species richness. Previous studies have
reported that a high diversity of herbivores on coral reefs
can be beneficial, increasing the effective removal of macroalgae and promoting coral settlement and growth (Burkepile & Hay 2008). The 15 species recorded in this study
corresponded to 88% of the species of both families
reported for the Caribbean, including Florida and the
Bahamas (McAfee & Morgan 1996; Mumby & Wabnitz
2002; Human & DeLoach 2006; Tzadik & Appeldoorn
2013). Although the species richness on nsMBRS was high,
other ecological attributes including density and biomass
were lower than the values reported in similar studies (Bouchon-Navaro & Harmelin-Vivien 1981; Lewis & Wainwright 1985; Bruggemann et al. 1994; van Rooij et al. 1998;
Lawson et al. 1999; Kramer 2003; Lang 2003; Nemeth &
Appeldoorn 2009; Toller et al. 2010; Kopp et al. 2012).
These ecological attributes of the herbivorous fish are
commonly affected by several processes, including stochastic phenomena such as hurricanes (Fenner 1991) or
fishing pressure (Hughes 1994; Jackson 1997; Pauly et al.
1998; Pandolfi et al. 2003); low fish recruitment may also
be important (Cowen et al. 2006; Adam et al. 2011).
However, we believe that fishing could be partially
Table 3. Cover of the benthic components for each habitat studied along a depth gradient.
mean of benthic cover (SE) and rugosity Index (RI) by habitat
lagoon
front
slope
terrace
lagoon
front
slope
terrace
8
seagrass
macrolgae
turf
29.1 (4.3)
0
0
0
26.0
62.4
47.0
22.0
0.1
0.2
0.6
1.0
(8.2)
(7.5)
(7.7)
(4.3)
(0.0)
(0.1)
(0.5)
(0.5)
c. coralline algae
calcareous algae
hydrocoral
0.2
1.5
5.4
0.4
0.4
0.1
0.1
12.1
0.1
0.2
0.1
0.2
(0.1)
(1.4)
(1.3)
(0.2)
octocoral
bare substrate
rubble
sand
4.8
11.6
11.9
17.5
6.0
14.3
11.4
7
4.1
0.3
2.1
7.8
22.3
0.8
1.7
2.1
(1.5)
(2.2)
(1.7)
(1.6)
(1.7)
(6.3)
(2.3)
(1.7)
(2.7)
(0.0)
(0.7)
(2.5)
(0.2)
(0.0)
(0.0)
(0.8)
(0.0)
(0.0)
(0.0)
(0.0)
rugosity index (RI)
(4.3)
(0.5)
(0.5)
(0.5)
0.16
0.35
0.34
0.5
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
~ez-Lara & Arias-Gonz
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andez-Landa, Acosta-Gonzalez, Nu
alez
Abundance
1.0
(a)
0.10 m
Scoer
Seagrass
Srad
Scoel Coral
Achi
Sato Acoe
Depth
Stae
Sise
Schr Rugosity
Cros
Abah
Svir Saur
Svet
–1.0
Srub
–1.0
1.0
Lagoon
Terrace
Biomass
0.8
(b)
Slope
Front
0.10 m
Scoer Coral
Scoel Sise
Stae
Acoe Achi
Srad
Seagrass
Saur
Sato
Schr
Abah
Cros
Svir
Svet
–0.8
Srub
–1.0
1.0
Fig. 5. Association biplot based on an RDA ordination of the
herbivorous fish species (surgeonfish and parrotfish) (a) Abundance
and (b) Biomass constrained by the environmental variables. Only the
environmental variables indicated by the automatic selection (P <
0.05) are presented. These variables were Depth, Seagrass and Coral
cover and Rugosity. A change in the fish assemblage between
habitats is shown with increasing depth. Lagoons (blue circles), fronts
(green polygons), slopes (purple triangles) and terraces (orange
squares). Fish illustrations modified from FAO 2002.
responsible for the low abundance and biomass of herbivorous fish recorded. Although information on fisheries
activities in the nsMBRS is scarce, and virtually non-existent for herbivorous fish, we empirically know that surgeonfish and parrotfish have not traditionally been
targeted by Mexican fishermen (Bozec et al. 2008). Nevertheless, local fishermen in the south of the study area
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
Surgeonfish and parrotfish in the nsMARS
(from Mahahual to Xcalak) (R.C. Hernandez-Landa, personal observation) indicated that the lack of important
commercial species (e.g. snappers and groupers) has
resulted in parrotfish becoming an important secondary
target group of spear-gun fishing. Despite not being the
primary target, this group is also caught by nets and marketed locally. This transition from non-commercial to
target species is a consequence of dramatic declines in
species of higher trophic levels due to overfishing (Callum 1995; Pauly et al. 1998; FAO 2006). We assume this
to be a result of increased coastal development along the
nsMBRS, beginning in 1970 with the Cancun–Tulum
tourism corridor (Quintana Roo State, Mexico). This
quickly extended to the Costa Maya region (south of our
study area), and has become an important activity since
the beginning of the year 2000 (Rodrıguez-Zaragoza &
Arias-Gonzalez, 2008; Acosta-Gonzalez et al. 2013). This
may be a possible explanation for the low herbivorous
fish density and biomass recorded, which we associate
with the increasing demand of the tourism industry (e.g.
increase in local restaurants). However species richness
did not seem to be regionally affected. This coincides
with a recent study at the level of the Caribbean that
found that fishing pressure is not important for structuring biodiversity distribution patterns (Francisco-Ramos &
Arias-Gonzalez 2013), although it may affect fish size and
abundance, including surgeonfish and parrotfish, in the
nsMBRS. Despite this, the low abundances and size structures found here appear to indicate that several environmental factors, not only fishing, are negatively influencing
the grazing fish assemblages. In principle our analysis (see
Discussion below) suggests that the potential loss of coral
cover and seagrass in nsMBRS may be important factors
structuring surgeonfish and parrotfish biomass and abundance, with severe consequences for the dynamics and
regeneration of coral reefs. It has been shown recently
how phase shift regimes from coral to macroalgae cover
may affect coral reef fish temporal biodiversity patterns
(Acosta-Gonzalez et al. 2013). This may also affect biomass and abundance structure of herbivorous fish.
With regards to spatial distribution, the numerous
small surgeonfish in the shallower habitats (lagoon and
front), and larger parrotfish recorded on the reef terrace,
was also observed by Lewis & Wainwright (1985) on reefs
in Belize. These reefs are located to the south of our
study area and are part of the MARS. These reefs consist
of a coral spurs and grooves system perpendicular to the
coast that tends to increase in complexity with depth and
extends to c 1600 m from the coast seaward, reaching its
maximum development on the terrace (c 20 m depth)
~ez-Lara & Arias-Gonzalez 1998). The spatial distri(N
un
bution pattern of surgeonfish and parrotfish in relation
to habitat depth seems to be typical of the coastal reefs of
9
Surgeonfish and parrotfish in the nsMARS
the MARS. Differences in the distribution of families with
depth have been explained by the tendency of surgeonfish
to form large schools over shallow habitats (Lewis &
Wainwright 1985). The advantages of the formation of
schools have been demonstrated for a wide range of animals and indicate that in single- and mixed-species
groups, this technique may enhance foraging efficiency
and improve protection from predators (Pitcher 1986;
Wolf 1987; Johansson et al. 2010). In contrast, parrotfish
have a lower tendency to form groups. In accordance
with Nemeth & Appeldoorn (2009), we found larger parrotfish in the deepest habitat compared with surgeonfish.
Other studies on Caribbean reefs have evaluated reef sites
stratified into inner-shelf, mid-shelf and outer-shelf reefs
over a wide cross-shelf. On reefs of Puerto Rico, the biomass of both families was greater at 3 m depth than in
deeper habitats (Nemeth & Appeldoorn 2009). On the
Island of Guadeloupe (French West Indies), parrotfish
abundance did not differ between reef flat and reef slope
habitats, whereas surgeonfish presented higher densities
on reef slopes (Kopp et al. 2012). Many of these studies,
including ours, indicated that the great spatial variation
of herbivorous fish is mainly displayed among reef habitats (depth gradient), rather than between adjacent reefs
(latitudinal gradient) (Robertson et al. 1979; BouchonNavarro & Harmelin-Vivien 1981; Bouchon-Navarro
1983; Russ 1984a,b; Fox & Bellwood 2008; Hoey & Bellwood 2010).
Fish and environmental variables associations
Each species has its own space–habitat range from which
to choose the most favorable habitat characteristics for
their distribution. However, it is difficult to describe all
the possible interpretations associated with the distribution patterns. One possible approach is to describe the
main distribution tendencies of the fish and infer the
potential effect that the significant variables have on the
different species. Approximately 40% of species data variance (for abundance and biomass) was explained by environmental variables in the RDA. The variation not
explained by the analysis could be due to unevaluated
processes such as recruitment, predation, competition,
feeding preferences, and algal consumption rates (Hixon
1991; Jones 1991; Sale 1991; Williams 1991; Paddack &
Cowen 2006). In this study the RDA stressed the importance of depth in structuring the distribution and the
way that parrotfish and surgeonfish utilize reef habitats.
In addition to depth, our data indicated that seagrass
constituted the most important benthic structural element for the lagoons, providing shelter for many young
fish of a variety of species (Harborne et al. 2006). For
example, Srad preferentially feeds on the blades of
10
~ez-Lara & Arias-Gonz
n
Hern
andez-Landa, Acosta-Gonz
alez, Nu
alez
T. testudinum (Lobel & Ogden 1981; Allen et al. 2006)
and showed a spatial distribution restricted to the lagoon.
Proof of this was the substantial decrease in abundance
and biomass towards the deeper and more complex habitats, in addition to the low variation in fish size along the
depth gradient. A similar case was presented by Cros, a
small and rare parrotfish associated with several environments, including seagrass beds, macroalgae, rubble, gorgonians and coral rocks (Carvalho-Filho 1999). In our
study this species was spatially restricted to the lagoons
showing a preference for seagrass. Neither of these cases
demonstrated an ontogenetic habitat shift; instead they
highlight the importance for these species of shallow habitats rich in seagrass, providing protection and abundant
food in order to complete their life history. Regarding
Achi, this species does not seem to depend entirely on
the characteristics of the lagoon, as it was widely distributed along the entire depth gradient. This suggests a differential ontogenetic use of the habitat with increasing
fish size towards deeper habitats. Robertson (1988), Risk
(1998) and Lawson et al. (1999) also found similar results
for surgeonfish species. The high species richness and
high density of juvenile fish of both families supported
by the lagoons highlight the importance of this habitat,
particularly for those species with a high dependence on
seagrass or those that use this habitat during some stage
in their early life.
Coral cover and rugosity should be considered key
structural components for the spatial ordination of surgeonfish and parrotfish into discrete assemblages, differentiated according to the abundance and biomass of their
dominant species. Together, these components have been
positively correlated with increased abundance, biomass
and high grazing rates of herbivorous fish in different
locations (Bouchon-Navarro 1983; Bell & Galzin 1984;
McCook 1996; Friedlander & Parrish 1998; Cadoret et al.
1999; McClanahan et al. 1999; Mumby 2006; Nemeth &
Appeldoorn 2009; Verges et al. 2011; Kopp et al. 2012).
The variety of growth forms of the corals is an indication
of different types of microhabitat. A greater variety of
these would offer a larger number of important resources
for the fish, including different food types, camouflage,
shelter, breeding sites or cleaning stations (Gratwicke &
Speight 2005; Alvarez-Filip et al. 2011). In the nsMBRS,
much of the structural complexity of the habitats (except
the lagoon) is supported by massive corals, including
Montastrea cavernosa and Orbicella annularis complex,
Undaria agaricies, Agaricia sp., Porites astreoides and Diploria sp. (Roff et al. 2011; Acosta-Gonzalez et al. 2013).
The structural heterogeneity of these reef habitats has
been well documented to control the distribution of fish
~ez-Lara & Arias-Gonzalez 1998; Ruızassemblages (N
un
~ez-Lara et al. 2005;
Zarate & Arias-Gonzalez 2004; N
un
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
~ez-Lara & Arias-Gonzalez
n
Hern
andez-Landa, Acosta-Gonzalez, Nu
Anderson et al. 2008; Rodrıguez-Zaragoza & AriasGonzalez 2008). This was also evident for the group of
herbivorous fish in the present study. For example, larger
parrotfish and a greater biomass were recorded for habitats with high rugosity and coral cover, as presented by
the terraces. These types of habitats with high rugosity
and coral cover provide shelter for the larger parrotfish as
well as protection against predators during inactivity at
night, when they sleep in mucus cocoons (Shephard
1994). In the study by Tzadik & Appeldoorn (2013),
three of four parrotfish species (Svir, Sise and Saur) were
positively correlated with reef structure (e.g. coral cover
and rugosity), with the exception of Sta. Our results were
consistent in terms of the positive relationship between
the aforementioned species, including Schr and Svet
found on the slope, and Stae, Scoer and Scoel found on
the terrace. The increase in size of these species towards
the deeper habitats has also been observed by different
authors in parrotfish and damselfish (Lirman 1994; McAfee & Morgan 1996; Cerveny 2006; Pittman et al. 2010;
Tzadik & Appeldoorn 2013). This highlights the importance of coral cover and rugosity as crucial indicators for
the distribution patterns of most parrotfish species in the
nsMBRS.
Several studies have indicated a strong negative relationship between herbivorous biomass and macroalgal
cover (Williams & Polunin 2001; Friedlander et al. 2007).
However, the high macroalgae on all habitats in this
study did not significantly affect the abundance and biomass of herbivorous fish as suggested by the RDA. Similar results have been found in other studies (Wellington
& Victor 1985; Williams 1986; Chabanet & Letourneur
1995; Carassou et al. 2013). For example, Abah was dominant on the fronts, where despite the overwhelming
dominance of macroalgae, it did not significantly influence the abundance and biomass distribution of this or
any other species. In our case, the reef front also seems
to show the greatest degree of degradation, where low
coral cover (7.0% 1.4) and the greatest percentage of
macroalgae were recorded (62.4% 7.5). This potentially
indicates that the fish avoid algae-dominated environments or that the composition of herbivorous fish species
is unable to control the excessive growth of macroalgae.
The terraces were in better condition than the other habitats. This is suggested by the following characteristics:
high rugosity (IR = 0.5), higher coral cover and lower
macroalgae cover (25.0% versus 22.0%, respectively), and
high species richness (13 species) and biomass, mainly
large parrotfish (512.1 g100 m 2).
Findings from the present study may provide an insight
into the environmental factors that underlie the diversity
and biological distribution patterns of surgeonfish and
parrotfish in the nsMBRS. Results suggest that low values
Marine Ecology (2014) 1–15 ª 2014 Blackwell Verlag GmbH
Surgeonfish and parrotfish in the nsMARS
of abundance, biomass and size obtained in our study
may be related to the health of coral reefs in the area. Our
results showed indications of a clear degradation of coral
reefs from the start of this study, particularly those located
in the northern sector of our study area, which coincides
with Bozec et al. (2008). Mass tourism in the study area is
producing important changes in water quality (Baker
et al. 2013) and sedimentation rates (ECO-AUDIT 2011),
which may be the primary cause of the coral-to-algal transition along the nsMBRS coast. The resulting loss in seagrass and coral cover, rugosity and general health of the
reef is likely to be one of the causes of the low biomass
and abundance of surgeonfish and parrotfish in our study.
Another important factor that cannot be neglected is global climate change, primarily temperature, as it affects
coral reef structure via bleaching events or by directly
affecting the distribution of fish species via metabolic rate
changes (Carpenter 1986; Floeter et al. 2005). Therefore,
the impacts of coastal development and associated fishing
pressure, and global climate change on coral reef ecosystem structure are perhaps the most important causes of
low abundance, biomass and size structure of surgeonfish
and parrotfish assemblages in the nsMBRS.
Conclusions
This study contributes information on the structure and
spatial distribution of surgeonfish and parrotfish on the
reef habitats of the nsMBRS. We have demonstrated that
the amount of live coral and other structural components
including seagrass and rugosity are important habitat
characteristics for herbivorous fish spatial distribution.
These results are critical for the nsMBRS. A major reduction in either of the significant benthic components
obtained in this study would therefore be expected to
decrease the species richness of the herbivorous fish community. The associations discussed here between the herbivorous fish species and the benthic components for the
different habitats may be vital for management and conservation strategies for the nsMBRS. These results can be
directly compared to other studies in the Caribbean
region. Future studies should be repeated over medium
and long-term spatial and temporal scenarios, as the
composition and distribution of herbivorous fish can vary
between locations, particularly in the nsMBRS, where at
present the information on this group of fish is still local
and regionally scarce.
Acknowledgements
The first author acknowledges the PhD scholarship
awarded on behalf of CONACyT (num. 100874). We
would like to thank MSc. G. Franklin, Dr. R. Rioja-Nieto,
11
Surgeonfish and parrotfish in the nsMARS
Dr. L. Arellano-Mendez and the journal reviewers for
their help with improving the text of this paper and for
providing useful comments. We thank Dr. M.A. RuizZarate, Dr. C. Gonzalez-Salas, and all volunteers for their
invaluable field support.
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