The Mexican Central Pacific is located in a zone of oceanographic transition between two biogeographic provinces with particular conditions that affect the associated fauna. The objective of this study was to evaluate the variation of hermatypic coral assemblages in this region and to determine their relationship with the heterogeneity of the benthonic habitat and spatial variables. A total of 156 transects were carried out at 41 sites in the years 2010 and 2011. The sampling effort returned 96.7% of the coral richness expected for the area, with a total of 15 species recorded. The results showed that richness, diversity and cover of corals varied only at the site and state scales. However, the composition and coverage of all coral species, as well as the benthonic habitat structure, differed significantly across the study scales (i.e. sites, zones and states). Canonical redundancy analysis showed that variation in the richness, diversity and assemblages of corals was explained by the cover of live corals, articulated calcareous algae, sandy substrate, sponges and fleshy macroalgae. This study suggests that local scale (i.e. site) variation in the coral assemblages of the Mexican Central Pacific is the result of the heterogeneity of the benthonic habitat, while geomorphological and oceanographic characteristics play a greater role at regional scale.
El Pacífico Central Mexicano se localiza en una zona de transición oceanográfica entre dos provincias biogeográficas con condiciones ambientales particulares que afectan la fauna asociada. El objetivo del estudio fue evaluar la variación de las comunidades de coral hermatípico de esta región y determinar su relación con la heterogeneidad del hábitat bentónico y variables espaciales. Se realizaron 156 transectos en 41 sitios en los años 2010 y 2011. El esfuerzo de muestreo representó el 96.7% de la riqueza de coral esperada para el área, con un total de 15 especies registradas. Los resultados mostraron que la riqueza, diversidad y cobertura de corales variaron sólo en las escalas de sitio y de estado. En cambio, la composición y cobertura de todas las especies de coral, así como la estructura del hábitat bentónico, fueron significativamente diferentes en todas las escalas estudiadas (i.e. sitio, zona y estado). Los análisis de redundancia canónica mostraron que la variación de la riqueza, la diversidad y las comunidades de corales eran explicadas por la cobertura de coral vivo, algas calcáreas articuladas, sustrato arenoso, esponjas y macroalgas carnosas. Este trabajo sugiere que la variación de las comunidades de coral en el Pacífico Central Mexicano a escala local (i.e. sitio) se debe a la heterogeneidad del hábitat bentónico, mientras que a escala regional, las características geomorfológicas y oceanográficas desempeñan un papel más importante.
The coral ecosystems of the Mexican Pacific are currently considered among the most important of the Tropical Eastern Pacific, since they comprise more than 30 coral species (
In the Mexican Pacific, the highest richness and coverage of corals is found in the Mexican Central Pacific (
Recently, the condition and conservation status of the Mexican Pacific coral ecosystems were evaluated (
Detailed evaluations of the coral ecosystems of the Mexican Central Pacific are required in order to further our understanding of the relationship between the coral assemblages and habitat heterogeneity at different spatial scales, considering biogeographic position, status of protection and particular local characteristics. The objective of this study was therefore to evaluate the spatial variation of the Mexican Central Pacific coral assemblages and explore their relationship with structural elements of the habitat and other regional (i.e. geomorphological, oceanographic and biogeographic) processes at different spatial scales. This knowledge is important in order to propose new marine protected areas (MPAs) in the region of study, particularly on the coasts of southern Jalisco and Colima, where the coral ecosystems are currently unprotected.
The study area includes ~600 km of the Mexican Central Pacific coastline including four states: Nayarit to the north, Jalisco and Colima in the centre, and Michoacán to the south (
The sampling strategy comprised a nested hierarchical design including states (>105 km), zones (1.5-10 km) and sites (<0.1 km). The state scale is affected by the geomorphological, oceanographic and biogeographic processes of the region, while local effects (e.g. those of habitat structure) operate at the site scale. At the zone scale, a synergy exists between regional and local effects. A total of 41 sites were sampled throughout the study area: 1) in Nayarit, nine sites in Isla Isabel and six in Islas Marietas; 2) in Jalisco, six in Bahía Chamela and five in Bahía Cuastecomate-Punta Melaque; 3) in Colima, three in Bahía Ceníceros and three in Bahía Santiago; 4) and in Michoacán, five in Faro de Bucerías and four in Caleta de Campos (
Surveys were performed in 2010 and 2011 during the same climatic season (summer from June to September). In 2010, we sampled the sites belonging to the states of Jalisco, Colima and Michoacán, while those of Nayarit were sampled in 2011. However, this study only considered the spatial variation, since some states were sampled in different years. At each site, coral coverage was recorded in situ using five transects of length 25 m placed parallel to the coastline at depths of between 4 and 12 m. Sampling strategy corrresponded to quadrats nested in line transects. Five quadrats (1 m2) were sampled per transect and these were evenly spaced at a distance of 5 m. Likewise, in each quadrat, coverage of the different morphofunctional benthonic groups was estimated: soft corals, hydrocorals, turf, articulated and crustose calcareous algae, fleshy macroalgae, sponges, barnacles, rubble, rock, sand and dead coral. All quadrats were considered pseudoreplicates, such that total coral richness and the coverages of coral species and morphofunctional benthonic groups were estimated as mean values per transect. The sampling effort was unbalanced at the site scale, with a total of 156 transects in the study area.
Sampling effort was evaluated with observed and expected species accumulation curves and the estimators Chao 1, Chao 2 and Jackknife 2 at the scale of state and Mexican Central Pacific, using 10000 randomizations without replacement in Estimates V9.1 (
Y = µ + STi + ZNj(STi) + SIk(ZNj(STi)) + εijk |
(1) |
where Y is the variable under analysis (i.e. S, LCC and H′), µ is the mean of the analysed variable, and ε is the accumulated error of the factors ST, ZN and SI. The factor ST considered the biogeographic eco-regions following the criteria of
The spatial variation of the hermatypic coral assemblages (composition and abundance) and the structure of the benthonic habitat were analysed with permutational multivariate analysis of variance (PERMANOVA), following the previously described ANOVA design. This analysis was conducted with Bray-Curtis similarity matrices using square root–transformed data in order to reduce the contribution of the abundant species and increase that of the species of lower abundance (
The relationship between the coral assemblages and spatio-environmental variables was evaluated with additive partitions based on canonical redundancy analysis (RDA), with the relationship assumed to be linear. The biological variables corresponded to Y vectors constructed with species richness (S) or Shannon diversity (H′), as well as a Y matrix with the composition and cover of the coral species. The X matrices were constructed with environmental variables relating to variation in the corals, such as the cover values of live coral, soft corals, hydrocorals, turf, articulated and crustose calcareous algae, fleshy macroalgae, sponges, coral rubble, rock, sand and dead coral. The W matrix corresponded to the spatial variables obtained with a trend-surface analysis, based on geographic coordinates (latitude=x, longitude=y) transformed into UTM units and represented as a third-order polynomial (x, y, x2, y2, x3, y3, xy, x2y, xy2) (
A total of 15 species of hermatypic corals were recorded in the Mexican Central Pacific, belonging to four genera and four families. A total of 12 species were identified in the northern state of Nayarit, 9 and 11 in the central states of Jalisco and Colima, respectively, and 5 in the southern state of Michoacán (Supplementary Material, Table S1). Species richness, estimated with Chao 2 and Jackknife 2, showed a representativity of the observed species richness of 100% for Nayarit and Jalisco (
Across the entire study area, the highest total species richness of corals was found at the sites of the central zone of the region (i.e. Jalisco and Colima), where Carrizales had 11 species and Cuastecomatito, Las Monjas 1 and Las Monjas 2 had 7 species each. The northern sites (i.e. Nayarit) Punta Rocosa, Las Monas Interno, Bahía Rabijuncos, Ensenada Pescadores each had 7 species. In contrast, the southern sites (i.e. Michoacán) Barco Hundido, Isla Pájaros Oeste, Isla Pájaros, Manto Carrizo, El Faro and El Relis, only had 1 species each. The zones with the highest total species richness were Isla Isabel (12) in the northern part, followed by Bahía Ceníceros (11) and Bahía Chamela (8) in the central zone. The lowest richness was recorded in Faro de Bucerías and Caleta de Campos in the southern zone, with 4 species (Supplementary Material, Fig. S1, Table S1).
The most frequent species in the sites of the Mexican Central Pacific were
The results of the ANOVA showed that the average values of species richness (S) and Shannon diversity (H′), as well as live coral cover (LCC), mainly varied at the scales of site and state (
Source | Pseudo-F | P(perm) | Source | Pseudo-F | P(perm) | ||
---|---|---|---|---|---|---|---|
ANOVA | |||||||
Species richness (S) | ST | 6.0003 | 0.0038 | Shannon diversity (H′) | ST | 22.998 | 0.0001 |
ZN(ST) | 0.4917 | 0.7459 | ZN(ST) | 0.36071 | 0.8348 | ||
SI(ZN(ST)) | 2.3957 | 0.0017 | SI(ZN(ST)) | 2.997 | 0.0002 | ||
Live coral cover (LCC) | ST | 3.2391 | 0.0384 | ||||
ZN(ST) | 1.4057 | 0.2513 | |||||
SI(ZN(ST)) | 5.3919 | 0.0001 | |||||
PERMANOVA | |||||||
Coral assemblages | ST | 9.8113 | 0.0001 | Benthonic habitat structure | ST | 4.3896 | 0.0002 |
ZN(ST) | 5.3396 | 0.0001 | ZN(ST) | 1.9866 | 0.0224 | ||
SI(ZN(ST)) | 3.756 | 0.0001 | SI(ZN(ST)) | 6.7904 | 0.0001 |
The PERMANOVA showed significant spatial variation in the composition and abundance of corals at site, zone and state scales (
The PERMANOVA showed that habitat structure varied significantly at the site, zone and state scale (
Sponges showed a greater coverage at the northern site Platform
At the zone scale, the pairwise comparisons showed that the habitat stucture differed only between the central zones Bahía Chamela and Bahía Cuastecomate-Punta Melaque (Supplementary Material, Table S2). Bahía Cuastecomate-Punta Melaque and Bahía Ceníceros showed the highest live coral cover, while Bahía Santiago and Caleta de Campos showed the greatest cover of fleshy macroalgae. Turf was most abundant at Faro de Bucerías, Isla Isabel, Bahía Ceníceros and Islas Marietas. Rocky substrate had the greatest cover at Bahía Chamela and Islas Marietas, while sandy substrate dominated at Faro de Bucerías, Caleta de Campos, Isla Isabel and Islas Marietas. Crustose calcareous algae had the highest cover at Faro de Bucerías, Bahía Ceníceros and Caleta de Campos (
At the state scale, pairwise comparison showed that Nayarit has a habitat structure that differs from that of Jalisco and Colima, as well as from that of Michoacán (Supplementary Material, Table S2). Jalisco is characterized by the highest live coral cover of the Mexican Central Pacific and a high cover of rocky substrate. Nayarit showed the highest cover of rock and turf in the study area, as well as moderate cover of sandy substrate. In Michoacán, the lowest live coral cover was estimated, as well as a high cover of turf, sand and fleshy macroalgae. Finally, Colima had the highest cover of fleshy macroalgae and high live coral cover. Other benthonic elements with a cover of <10% are shown in
The results of the canonical additive partitions showed that total species richness (S) and Shannon diversity (H′), as well as the composition and abundance of corals, were primarily explained by pure environmental variation [a] and secondarily by spatially structured environmental variation [b] at the studied Mexican Central Pacific sites. Pure spatial variation [c] did not make a significant contribution. The total variation explained by the RDA models [a+b+c] ranged from 45.2% to 68.5%, with statistical significances of 0.0005<P<0.011 (
[a] | [b] | [c] | [d] | Total Exp. Var. [a+b+c] | Env. Var. [a+b] | Spat. Var. [b+c] | |
---|---|---|---|---|---|---|---|
Species richness (S) | 36.4 | 27.8 | 0.0 | 35.8 | 64.2 | 64.2 | 27.8 |
P=0.0001 | P=0.0001 | P=0.0005 | |||||
Environmental variables: LCC, RSC, CCA, FMA and SS Spatial variables: x |
|||||||
Shannon diversity (H′) | 29.9 | 15.4 | 0.0 | 54.8 | 45.2 | 45.2 | 15.4 |
P=0.0010 | P=0.0010 | P=0.0109 | |||||
Environmental variables: LCC, RSC, CCA, FMA and SS Spatial variables: x |
|||||||
Coral assemblage (composition and cover) | 45.3 | 23.0 | 0.0 | 31.5 | 68.5 | 68.5 | 23.0 |
P=0.0001 | P=0.0001 | P=0.0005 | |||||
Environmental variables: LCC, RSC, CCA, FMA and SS Spatial variables: x and y |
Notes: Hermatypic coral spatial diversity was represented by Y vectors (i.e. species richness and Shannon diversity) and Y matrices (i.e. coral species composition and cover). Environmental variables (Env. Var.) were included in X matrices, where LCC is live coral cover; RSC is sponge; CCA is crustose calcareous algae; FMA is fleshy macroalgae; SS is sand. W matrices corresponded to spatial variables (Spat. Var.), where x, y, x2, y2, x3, y3, xy, x2y, xy2 were derived from third-order polynomial terms of geographic coordinates represented as distances in metres. The total explained variation (Total Exp. Var.) was represented by [a + b + c] fraction, where = [a + b + c] = Y vs. X and W; [a + b] = Y vs. X; [b + c] = Y vs. W; [a] = pure environmental variation; [b] = spatially structured environmental variation; [c] = pure spatial variation; and [d] = unexplained variation. Bold numbers correspond to a statistical significance p<0.05.
The hermatypic coral assemblage structure of the Mexican Central Pacific varied significantly among the different spatial scales studied. At the regional (i.e. state) scale, the species richness and composition recorded were similar to those reported at other locations of the Mexican Pacific (
Richness, diversity, live coral cover and composition of coral assemblages are also affected by anthropogenic activities. Coral ecosystems in the Mexican Central Pacific are distributed in zones that have different degrees of natural and human disturbance (
At the local scale, the coral assemblages varied significantly among sites, due probably to the fact that they have a discontinuous distribution and poor development generated, at least in part, by the following circumstances: (1) the continental platform of the Mexican Central Pacific is narrow and depths greater than 100 m are reached within short distances from the coast, affecting the temperature and illumination necessary for coral survival; and (2) the transparency of the water is seasonally very variable and occasionally low in the study area, which reduces the light and thus the photosynthetic activity of
The greatest total species richness of corals was recorded in Carrizales, Colima, where a true coral reef exists. This is one of the sites of greatest species richness in the Mexican Pacific, exceeding that of the largest and most developed reefs of southern Baja California (e.g. Cabo Pulmo,
The estimated Shannon diversity at the sites with coral reefs and coral communities of the Mexican Central Pacific is low because of the high dominance of certain species within the assemblages.
In the studied sites of the Mexican Central Pacific, four sites showed high values of live coral cover (>47%), caused by the presence of abundant substrate (i.e. rocky substrate and coral reef matrix) for colonization by corals and stability of reef structures as well as a relative “stability” in oceanic temperature conditions. The live coral cover values estimated at Tenacatita, Carrizales, La Pajarera and Cuastecomatito, located in the central states (i.e. Jalisco and Colima), are considered among the highest in the Mexican Pacific, following the massive coral mortality event caused by the 1997-1998 ENSO (
In general, the coral assemblages of the Mexican Central Pacific showed higher values of species richness and live coral cover than those of Central and South American coral reefs (e.g. El Salvador, Nicaragua, Costa Rica, Panama, Colombia and Ecuador,
The coral species with the highest occurrence at the sampled sites of the Mexican Central Pacific were
The central states of Jalisco and Colima show the most similar coral assemblages. This similarity stems from the fact that both assemblages share geomorphological characteristics and a similar habitat structure. Furthermore, they show patches of coral with moderate live coral cover and fleshy macroalgae, as well as a low sandy substrate cover related to a greater contribution of
The composition and cover of hermatypic coral species and of the structural elements of the habitat varied at the scales of site, zone and state. Variation at site and state scales may be a product of the local factors and regional processes described previously that influence the richness, diversity and cover of these species. Variation at zone scale may be the product of a combination of local effects (e.g. structural heterogeneity of the benthonic habitat in each site) and regional processes (biogeographic, oceanographic and coastal geomorphological) that act at the state scale. The canonical additive partitions showed that the fractions that explained the richness, diversity, cover and structure of the hermatypic coral assemblages of the Mexican Central Pacific were the pure environmental fraction [a] and the spatially structured environmental fraction [b]. This finding shows that the coral assemblages are related to the elements of the benthonic habitat (i.e. fraction [a]) or covary with the spatial structure (i.e. fraction [b]) of the Mexican Central Pacific at the zone and state scales. This covariance at both scales could occur because of the influence of geomorphology, oceanographic patterns and the confluence of the biogeographic provinces of Corteziana and Mexicana. In general, the results of the canonical RDA showed that the live coral cover and crustose calcareous algae correlated best with the sites of greatest richness, diversity and cover of coral species. In contrast, high cover of sandy substrate, sponges and fleshy macroalgae is related to sites with a lower diversity and development of coral (
The live coral cover allows the growth and recruitment of coral colonies (
MPAs are currently recognized as a good management strategy that has proved useful for maintaining and promoting increased biodiversity (
We are indebted and grateful to all our colleagues in the “Arrecifes del Pacífico” group (www.mexlter.org.mx), who have worked assiduously over many years collecting most of the data presented here. This work was partially funded by the Universidad de Guadalajara (P3E2010 and P3E2011 to F.A. Rodríguez-Zaragoza), PROMEP (103.5/08/2919 and 103.5/10/927 to F.A. Rodríguez-Zaragoza), CONABIO (HJ026 to L.E. Calderón-Aguilera), (PIFI-2010-14MSU0010Z-10 to A.L. Cupul-Magaña) and the authorities from Isla Isabel and Islas Marietas National Park. We also thank two anonymous reviewers for their comments and suggestions, wqhich increased the quality of this work. Finally, J. Hernández-Zulueta acknowledges the doctoral fellowship from CONACYT (0262538).
The following material is available through the online version of this article and at the following link:
Figure S1. − Latitude of the different zones of the Mexican Central Pacific with their coral species richness.
Table S1. − Richness and coverages (%) of hermatypic corals species in the different sampling sites of the Mexican Central Pacific.
Table S2. − Results of the ANOVA and PERMANOVA pairwise test.
Table S3. − Results of the similarity percentage analysis (SIMPER) and coverages (%) of coral species by state. For SIMPER, only those species contributing 90% of the average dissimilarity (Ave. Dis.) of coral species between states of the Mexican Central Pacific are presented.
Table S4. − Results of the similarity percentage analysis (SIMPER) and coverages (%) of coral species per zone. For SIMPER, only those species contributing 90% of the average dissimilarity (Ave. Dis.) of coral species between zones of the Mexican Central Pacific are presented.
Table S5. − Results of the similarity percentage analysis (SIMPER) and coverages (%) of coral species per site. For SIMPER, only those species contributing 90% of the average dissimilarity (Ave. Dis.) of coral species between sampling sites of the Mexican Central Pacific are presented.
Table S6. − Coverages (%) of the morphofunctional groups per site.