Amílcar L. Cupul-Magaña

Host-symbiont recombination versus natural selection in the response of coral-dinoflagellate symbioses to environmental disturbance.

Mutualisms between reef-building corals and endosymbiotic dinoflagellates are particularly sensitive to environmental stress, yet the ecosystems they construct have endured major oscillations in global climate. During the winter of 2008, an extreme cold-water event occurred in the Gulf of California that bleached corals in the genus Pocillopora harbouring a thermally ‘sensitive’ symbiont, designated Symbiodinium C1b-c, while colonies possessing Symbiodinium D1 were mostly unaffected. Certain bleached colonies recovered quickly while others suffered partial or complete mortality. In most colonies, no appreciable change was observed in the identity of the original symbiont, indicating that these partnerships are stable. During the initial phases of recovery, a third species of symbiont B1Aiptasia, genetically identical to that harboured by the invasive anemone, Aiptasia sp., grew opportunistically and was visible as light-yellow patches on the branch tips of several colonies. However, this symbiont did not persist and was displaced in all cases by C1b-c several months later. Colonies with D1 were abundant at inshore habitats along the continental eastern Pacific, where seasonal turbidity is high relative to offshore islands. Environmental conditions of the central and southern coasts of Mexico were not sufficient to explain the exclusivity of D1 Pocillopora in these regions. It is possible that mass mortalities associated with major thermal disturbances during the 1997–1998 El Niño Southern Oscillation eliminated C1b-c holobionts from these locations. The differential loss of Pocillopora holobionts in response to thermal stress suggests that natural selection on existing variation can cause rapid and significant shifts in the frequency of particular coral–algal partnerships. However, coral populations may take decades to recover following episodes of severe selection, thereby raising considerable uncertainty about the long-term viability of these communities.

Effects of the El Niño-Southern Oscillation and the anti-El Niño event (1997–1999) on coral reefs of the western coast of México

The El Niño-Southern Oscillation (ENSO) is a natural phenomenon responsible for important damages to coral communities of the Pacific and Indian Oceans. The most intense recent events occurred in 1957–58, 1972– 73, 1982–83, and 1997–98 (Quinn et al. 1987; Wilkinson 2000), and their effects were especially catastrophic in the eastern tropical Pacific region (from Costa Rica to the Galápagos Islands, Ecuador) in 1982–83, when sea surface temperature was several degrees Centigrade above normal levels for an extended period of weeks and caused massive coral bleaching and mortality (Glynn 1990). To date, those reefs have not recovered and are in continuous deterioration because of an increase in corallivore and bioeroder activity (Glynn 1997), although they resisted well the increase in temperature triggered by the 1997–98 ENSO (Glynn et al. 2001; Guzmán and Cortés 2001; Vargas-Angel et al. 2001). The influence of the 1982–83 ENSO event on ocean productivity, plankton communities, and pelagic fish populations along the western coast of México has been well described (Lavaniegos-Espejo et al. 1989; Santamarı́a-del Angel et al. 1994). However, there are few data on the effects of that and other similar events on reef communities of that region. Reyes-Bonilla and Calderón-Aguilera (1994) indicated that the 1983 cohort of the coral Porites panamensis Verrill, 1866, from the Cabo Pulmo reef, Gulf of California (Fig. 1), was relatively smaller than in normal years, as evidenced by size and age structure of the population. Also, Glynn and Leyte-Morales (1997) showed that size distribution of Pavona gigantea Verrill, 1869, and the presence of large dead or eroded framework areas at La Entrega, in the Oaxaca reef tract (Fig. 1), may be indications of perturbations caused by ENSO events (possibly, in 1987). In contrast, Carriquiry and ReyesBonilla (1997) mentioned that reefs of north Banderas Bay (Fig. 1), studied in 1991, showed no evidence of ENSO-induced damage and suggested that their healthy state resulted from the low intensity of positive temperature anomalies historically recorded in that area of the Mexican Pacific. Direct observations of ENSO-caused perturbations to reef corals in western México were reported by Reyes-Bonilla (1993a), who estimated a 15% mortality of Pocillopora spp. at Cabo Pulmo reef in 1987, and Munguı́a-Vega and ReyesBonilla (1999), who quantified the loss of chlorophyll a in fully and partially bleached colonies of P. verrucosa (Ellis and Solander, 1786) from south La Paz Bay, in 1997. To improve on the scarcity of factual information about the effects of ENSO in México, the 1997–1998 event and the subsequent anti-El Niño (1998–1999) were studied in depth. The objective of this paper is to present new observations and to provide an overview, a chronological account, and an outline of the most important perturbations suffered by Mexican coral Coral Reefs (2002) 21: 368–372 DOI 10.1007/s00338-002-0255-4

Reclutamiento de Porites (Scleractinia) sobre sustrato artificial en arrecifes afectados por El Niño 1997-98 en Bahía de Banderas, Pacífico mexicano

Mexican Pacific coral reefs were severely damaged by the sea surface warming observed during the 1997–98 El Niño. In Banderas Bay, massive coral mortality was as high as 97%, and the surviving colonies were exposed to sublethal temperatures and thermal stress. In this coral recruitment study we attempted to estimate the recovery and potential repopulation of corals in the Mexican Pacific. After the El Niño event, we used terracotta tiles to monitor the settlement of coral larval propagules at nine reefs in the region. The recruitment study took place from December 1998 to July 1999. Settlements of nine specimens of Porites were recorded at two localities. This is the first settlement record for this coral genus in the eastern tropical Pacific and the one with the largest number of specimens recruited during a study involving artificial substrate. The results indicate that these reefs do not totally depend on the arrival of allocthonous coral propagules from other regions of the tropical Pacific to maintain their development. This study also shows that corals maintain their reproductive activity despite the environmental disturbances. Therefore, sexual reproduction of reef corals of this region provides an effective alternative for the recovery of Mexican Pacific coral reefs.

Testing the genetic predictions of a biogeographical model in a dominant endemic Eastern Pacific coral (Porites panamensis) using a genetic seascape approach

The coral fauna of the Eastern Tropical Pacific (ETP) is depauperate and peripheral; hence, it has drawn attention to the factors allowing its survival. Here, we use a genetic seascape approach and ecological niche modeling to unravel the environmental factors correlating with the genetic variation of Porites panamensis, a hermatypic coral endemic to the ETP. Specifically, we test if levels of diversity and connectivity are higher among abundant than among depauperate populations, as expected by a geographically relaxed version of the Abundant Center Hypothesis (rel-ACH). Unlike the original ACH, referring to a geographical center of distribution of maximal abundance, the rel-ACH refers only to a center of maximum abundance, irrespective of its geographic position. The patterns of relative abundance of P. panamensis in the Mexican Pacific revealed that northern populations from Baja California represent its center of abundance; and southern depauperate populations along the continental margin are peripheral relative to it. Genetic patterns of diversity and structure of nuclear DNA sequences (ribosomal DNA and a single copy open reading frame) and five alloenzymatic loci partially agreed with rel-ACH predictions. We found higher diversity levels in peninsular populations and significant differentiation between peninsular and continental colonies. In addition, continental populations showed higher levels of differentiation and lower connectivity than peninsular populations in the absence of isolation by distance in each region. Some discrepancies with model expectations may relate to the influence of significant habitat discontinuities in the face of limited dispersal potential. Environmental data analyses and niche modeling allowed us to identify temperature, water clarity, and substrate availability as the main factors correlating with patterns of abundance, genetic diversity, and structure, which may hold the key to the survival of P. panamensis in the face of widespread environmental degradation.

Additive partitioning of reef fish diversity variation: a promising marine biodiversity management tool

Additive partitioning was applied to variation in reef fish spatial diversity at Isla Isabel National Park, Nayarit state, Mexico, and to identify the environmental and spatial variables that best explains it. Analyses included expected and observed species curves, rare species analysis, additive partitioning of alpha- and beta-diversity, and canonical redundancy analysis. A total of 10,517 individuals were recorded from 75 species and 33 reef fish families, representing 85% of expected richness. Species richness beta-diversity was dependent on the site scale, while the alpha-diversity of the Shannon diversity was most significant at the transect scale. Canonical partitioning showed species richness and Shannon diversity was explained by spatially-structured environmental components. Variation in species composition and abundance was explained by a purely environmental component. Therefore, elements of habitat structure (especially corals), topographic complexity, and refuge availability determine fish species diversity. Our results suggest that greater emphasis is required to conserve sites that promote β-diversity, increasing fish spatial diversity. In Isla Isabel, these sites would be mostly those located at eastern and southern of protected sides, where coral reef patches are well represented. The results of this multi-scale analysis are valuable and useful as an addition and complement to the holistic management strategies implemented at Isla Isabel.

Conservation and Sustainability of Mexican Caribbean Coral Reefs and the Threats of a Human-Induced Phase-Shift

Natural ecosystems around the world are continually changing, but in recent decades it has become increasingly evident that terrestrial and marine environments are degrading. It is considered that the main cause is the rapid human population growth and increas‐ ing demand of resources for our survival. In particular for coral reef ecosystems, they are experiencing a significant change as reflected in the decline of coral cover and diver‐ sity of species [1, 2].

Calcification and growth rate recovery of the reef-building Pocillopora species in the northeast tropical Pacific following an ENSO disturbance

Pocilloporids are one of the major reef-building corals in the eastern tropical Pacific (ETP) and also the most affected by thermal stress events, mainly those associated with El Niño/Southern Oscillation (ENSO) periods. To date, coral growth parameters have been poorly reported in Pocillopora species in the northeastern region of the tropical Pacific. Monthly and annual growth rates of the three most abundant morphospecies (P. cf. verrucosa, P. cf. capitata, and P. cf. damicornis) were evaluated during two annual periods at a site on the Pacific coast of Mexico. The first annual period, 2010–2011 was considered a strong ENSO/La Niña period with cool sea surface temperatures, then followed by a non-ENSO period in 2012–2013. The linear extension rate, skeletal density, and calcification rate averaged (±SD) were 2.31 ± 0.11 cm yr−1, 1.65 ± 0.18 g cm−3, 5.03 ± 0.84 g cm−2 yr-1 respectively, during the strong ENSO event. In contrast, the respective non-ENSO values were 3.50 ± 0.64 cm yr−1, 1.70 ± 0.18 g cm−3, and 6.02 ± 1.36 g cm−2 yr−1. This corresponds to 52% and 20% faster linear extension and calcification rates, respectively, during non-ENSO period. The evidence suggests that Pocillopora branching species responded positively with faster growth rates following thermal anomalies, which allow them to maintain coral communities in the region.

The functional trophic role of whale shark (Rhincodon typus) in the northern Mexican Caribbean: network analysis and ecosystem development

The whale shark (Rhincodon typus) has a high value to tourism, fishing, and pharmaceutical industry, but this species is considered as vulnerable and with potential extinction. The largest aggregation of whale sharks occurs in an upwelling system (Holbox) at northeastern Mexican Caribbean, where we analyzed the trophic role of whale shark. A mass-balanced trophic model was built to: (1) analyze the ecosystem emergent or macroscopic properties; (2) estimate the system recovery time (resilience); (3) assess the fishery effects on different target species; and (4) evaluate the whale shark systemic role in this system. The results showed that the macroscopic properties of the Holbox ecosystem were similar to other upwelling systems with high rates of primary productivity and accumulated biomass in lower trophic levels. Even so, the food web was more like the structure of coral reefs. On the other hand, Holbox system had a lower maturity and development level than coral reefs, suggesting an increased resistance to disturbances. The mixed trophic impacts and short-term dynamic simulation showed that species like snook, sharks, groupers, benthic autotrophs, small benthic epifauna, and phytoplankton had the largest direct and indirect effects. The most significant systemic role of whale sharks is to provide the resilience of the system.

Abundance of three species of Isopoda (Peracarida, Isopoda) associated with a coral reef environment in Pacific Mexico

Fragments of dead coral belonging to Pocillopora Lamarck, 1816 were used during a 1-year period as artificial micro-habitats and positioned at a coral reef community at Islas Marietas, Bahia Banderas, on the west coast of Mexico, to attract and capture isopods. Three species of isopods, totaling 961 specimens were collected. The dominant species was Joeropsis dubia (Menzies, 1951) (Joeropsididae) (83.03% of the total number of specimens), followed by Califanthura squamosissima (Menzies, 1951) (Paranthuridae) (9.78%), and Paracerceis sculpta (Holmes, 1904) (Sphaeromatidae) (7.18%). The average density of isopods was of 12.0 × 10−2 ind. ⋅ cm−2. A positive relationship between water temperature and total density of individuals during the sampling period was found. Annual water temperature changes influenced the abundance of each species in a similar way, with the higher abundances associated to the lower temperatures, which is also related to an increase in primary productivity and the presence of upwellings in the area.

Influence of the coral reef assemblages on the spatial distribution of echinoderms in a gradient of human impacts along the tropical Mexican Pacific

Fourteen species of echinoderms and their relationships to the benthic structure of the coral reefs were assessed at 27 sites—with different levels of human disturbances—along the coast of the Mexican Central Pacific. Diadema mexicanum and Phataria unifascialis were the most abundant species. The spatial variation of the echinoderm assemblages showed that D. mexicanum, Eucidaris thouarsii, P. unifascialis, Centrostephanus coronatus, Toxopneustes roseus, Holothuria fuscocinerea, Cucumaria flamma, and Echinometra vanbrunti accounted for the dissimilarities among the sites. The spatial variation among the sites was mainly explained by the cover of the hard corals (Porites, Pocillopora, Pavona, Psammocora), different macroalgae species (turf, encrusting calcareous algae, articulated calcareous algae, fleshy macroalgae), sponges, bryozoans, rocky, coral rubble, sand, soft corals (hydrocorals and octocorals), Tubastrea coccinea coral, Balanus spp., and water depth. The coverage of Porites, Pavona, and Pocillopora corals, soft coral, rock, and Balanos shows a positive relationship with the sampling sites included within the natural protected area with low human disturbances. Contrary, fleshy macroalgae, sponges, and soft coral show a positive relationship with higher disturbance sites. The results presented here show the importance of protecting the structural heterogeneity of coral reef habitats because it is a significant factor for the distribution of echinoderm species and can contribute to the design of conservation programs for the coral reef ecosystem.