Evolution and environment of Caribbean coastal ecosystems.

Isolation of the Caribbean Sea from the tropical Eastern Pacific by uplift of the Isthmus of Panama in the late Pliocene was associated with major, taxonomically variable, shifts in Caribbean biotic composition, and extinction, but inferred causes of these biological changes have remained elusive. We addressed this through falsifiable hypotheses about how independently determined historical changes in oceanographic conditions may have been responsible. The most striking environmental change was a sharp decline in upwelling intensity as measured from decreases in intra-annual fluctuations in temperature and consequently in planktonic productivity. We then hypothesized three general categories of biological response based upon observed differences in natural history between the oceans today. These include changes in feeding ecology, life histories, and habitats. As expected, suspension feeders and predators became rarer as upwelling declined. However, predicted increases in benthic productivity by reef corals, and benthic algae were drawn out over more than 1 Myr as seagrass and coral reef habitats proliferated; a shift that was itself driven by declining upwelling. Similar time lags occurred for predicted shifts in reproductive life history characteristics of bivalves, gastropods, and bryozoans. Examination of the spatial variability of biotic change helps to understand the time lags. Many older species characteristic of times before environmental conditions had changed tended to hang on in progressively smaller proportions of locations until they became extinct as expected from metapopulation theory and the concept of extinction debt. Faunal turnover may not occur until a million or more years after the environmental changes ultimately responsible.

Coral reefs in the Anthropocene.

Coral reefs support immense biodiversity and provide important ecosystem services to many millions of people. Yet reefs are degrading rapidly in response to numerous anthropogenic drivers. In the coming centuries, reefs will run the gauntlet of climate change, and rising temperatures will transform them into new configurations, unlike anything observed previously by humans. Returning reefs to past configurations is no longer an option. Instead, the global challenge is to steer reefs through the Anthropocene era in a way that maintains their biological functions. Successful navigation of this transition will require radical changes in the science, management and governance of coral reefs.

Evolutionary Determinants of Morphological Polymorphism in Colonial Animals.

Colonial animals commonly exhibit morphologically polymorphic modular units that are phenotypically distinct and specialize in specific functional tasks. But how and why these polymorphic modules have evolved is poorly understood. Across colonial invertebrates, there is wide variation in the degree of polymorphism, from none in colonial ascidians to extreme polymorphism in siphonophores, such as the Portuguese man-of-war. Bryozoa are a phylum of exclusively colonial invertebrates that uniquely exhibit almost the entire range of polymorphism, from monomorphic species to others that rival siphonophores in their polymorphic complexity. Previous approaches to understanding the evolution of polymorphism have been based on analyses of (1) the functional role of polymorphs or (2) presumed evolutionary costs and benefits based on evolutionary theory that postulates polymorphism should be evolutionarily sustainable only in more stable environments because polymorphism commonly leads to the loss of feeding and sexual competence. Here we use bryozoans from opposite shores of the Isthmus of Panama to revisit the environmental hypothesis by comparison of faunas from distinct oceanographic provinces that differ greatly in environmental variability, and we then examine the correlations between the extent of polymorphism in relation to patterns of ecological succession and variation in life histories. We find no support for the environmental hypothesis. Distributions of the incidence of polymorphism in the oceanographically unstable Eastern Pacific are indistinguishable from those in the more stable Caribbean. In contrast, the temporal position of species in a successional sequence is collinear with the degree of polymorphism because species with fewer types of polymorphs are competitively replaced by species with higher numbers of polymorphs on the same substrata. Competitively dominant species also exhibit patterns of growth that increase their competitive ability. The association between degrees of polymorphism and variations in life histories is fundamental to understanding of the macroevolution of polymorphism.

Anthropogenic mortality on coral reefs in Caribbean Panama predates coral disease and bleaching.

Caribbean reef corals have declined precipitously since the 1980s due to regional episodes of bleaching, disease and algal overgrowth, but the extent of earlier degradation due to localised historical disturbances such as land clearing and overfishing remains unresolved. We analysed coral and molluscan fossil assemblages from reefs near Bocas del Toro, Panama to construct a timeline of ecological change from the 19th century-present. We report large changes before 1960 in coastal lagoons coincident with extensive deforestation, and after 1960 on offshore reefs. Striking changes include the demise of previously dominant staghorn coral Acropora cervicornis and oyster Dendrostrea frons that lives attached to gorgonians and staghorn corals. Reductions in bivalve size and simplification of gastropod trophic structure further implicate increasing environmental stress on reefs. Our paleoecological data strongly support the hypothesis, from extensive qualitative data, that Caribbean reef degradation predates coral bleaching and disease outbreaks linked to anthropogenic climate change.

Bryozoan revelations.

Bryozoans, simple invertebrates living on the sea floor, are emerging as a model system for understanding ecological and evolutionary processes on macroevolutionary scales.

Colloquium paper: ecological extinction and evolution in the brave new ocean.

The great mass extinctions of the fossil record were a major creative force that provided entirely new kinds of opportunities for the subsequent explosive evolution and diversification of surviving clades. Today, the synergistic effects of human impacts are laying the groundwork for a comparably great Anthropocene mass extinction in the oceans with unknown ecological and evolutionary consequences. Synergistic effects of habitat destruction, overfishing, introduced species, warming, acidification, toxins, and massive runoff of nutrients are transforming once complex ecosystems like coral reefs and kelp forests into monotonous level bottoms, transforming clear and productive coastal seas into anoxic dead zones, and transforming complex food webs topped by big animals into simplified, microbially dominated ecosystems with boom and bust cycles of toxic dinoflagellate blooms, jellyfish, and disease. Rates of change are increasingly fast and nonlinear with sudden phase shifts to novel alternative community states. We can only guess at the kinds of organisms that will benefit from this mayhem that is radically altering the selective seascape far beyond the consequences of fishing or warming alone. The prospects are especially bleak for animals and plants compared with metabolically flexible microbes and algae. Halting and ultimately reversing these trends will require rapid and fundamental changes in fisheries, agricultural practice, and the emissions of greenhouse gases on a global scale.

Coral reef-associated bryozoans of Jamaica.

As part of a long-term ecological study of the cryptic comunity of Jamaican coral reefs carried out by Jeremy B.C. Jackson and associates during the 1970s and early 1980s, collections were made of reef bryozoans found at 14 sites around the island. Space occupied by bryozoans on undercoral surfaces is dominated by relatively few species. However, during scanning electrone microscopy study and monograph preparation a diverse assortment of relatively rare species was discovered. Of the 132 species found, 56%, 74 species (70 cheilostomes and 4 cyclostomes) are new, as are one family (Inversiscaphidae) and 5 genera (Planospinella, Caribaria, Spirocoleopora, Gemellitheca, and Palliocella).

The transformation of Caribbean coral communities since humans.

The mass die-off of Caribbean corals has transformed many of this region's reefs to macroalgal-dominated habitats since systematic monitoring began in the 1970s. Although attributed to a combination of local and global human stressors, the lack of long-term data on Caribbean reef coral communities has prevented a clear understanding of the causes and consequences of coral declines. We integrated paleoecological, historical, and modern survey data to track the occurrence of major coral species and life-history groups throughout the Caribbean from the prehuman period to the present. The regional loss of Acropora corals beginning by the 1960s from local human disturbances resulted in increases in the occurrence of formerly subdominant stress-tolerant and weedy scleractinian corals and the competitive hydrozoan Millepora beginning in the 1970s and 1980s. These transformations have resulted in the homogenization of coral communities within individual countries. However, increases in stress-tolerant and weedy corals have slowed or reversed since the 1980s and 1990s in tandem with intensified coral bleaching and disease. These patterns reveal the long history of increasingly stressful environmental conditions on Caribbean reefs that began with widespread local human disturbances and have recently culminated in the combined effects of local and global change.

How colonial animals evolve.

The evolution of modular colonial animals such as reef corals and bryozoans is enigmatic because of the ability for modules to proliferate asexually as whole colonies reproduce sexually. This reproductive duality creates an evolutionary tension between modules and colonies because selection operates at both levels. To understand how this evolutionary conflict is resolved, we compared the evolutionary potential of module- and colony-level traits in two species of the bryozoan Stylopoma, grown and bred in a common garden experiment. We find quantitatively distinct differences in the evolutionary potential of modular and colony traits. Contrary to solitary organisms, individual traits are not heritable from mother to daughter modules, but colony traits are strongly heritable from parent to offspring colonies. Colony-level evolution therefore dominates because no evolutionary change can accumulate among its modules.

Widespread loss of Caribbean acroporid corals was underway before coral bleaching and disease outbreaks.

The mass mortality of acroporid corals has transformed Caribbean reefs from coral- to macroalgal-dominated habitats since systematic monitoring began in the 1970s. Declines have been attributed to overfishing, pollution, sea urchin and coral disease, and climate change, but the mechanisms are unresolved due to the dearth of pre-1970s data. We used paleoecological, historical, and survey data to track Acropora presence and dominance throughout the Caribbean from the prehuman period to present. Declines in dominance from prehuman values first occurred in the 1950s for Acropora palmata and the 1960s for Acropora cervicornis, decades before outbreaks of acroporid disease or bleaching. We compared trends in Acropora dominance since 1950 to potential regional and local drivers. Human population negatively affected and consumption of fertilizer for agriculture positively affected A. palmata dominance, the latter likely due to lower human presence in agricultural areas. The earlier, local roots of Caribbean Acropora declines highlight the urgency of mitigating local human impacts.

Historical decline in coral reef growth after the Panama Canal.

The Panama Canal is near its vessel size and tonnage handling capacity, and Panamanians have decided to expand it. The expansion of the Canal may consider the historical long-lasting impacts on marine coastal habitats particularly on sensitive coral reefs. These potential impacts were discussed during the national referendum as were other equally important issues, such as its effects on forests, watersheds, and water supply. Coral growth rates provide a direct measure of coral fitness and past environmental conditions comparable to analyses of tree rings. We examined stable isotopes, metal geochemical tracers, and growth rates on a century-long (1880-1989) chronology based on 77 cores of the dominant reef-building coral Siderastrea siderea collected near the Caribbean entrance to the canal. Our results showed a gradual decline in coral growth unrelated to changes in sea surface temperature but linked to runoff and sedimentation to coastal areas resulting from the construction and operation of the Panama Canal.

Differences in extinction rates drove modern biogeographic patterns of tropical marine biodiversity.

Marine biodiversity in the Coral Triangle is several times higher than anywhere else, but why this is true is unknown because of poor historical data. To address this, we compared the first available record of fossil cheilostome bryozoans from Indonesia with the previously sampled excellent record from the Caribbean. These two regions differ several-fold in species richness today, but cheilostome diversity was strikingly similar until the end of the Miocene 5.3 million years ago so that the modern disparity must have developed more recently. However, the Miocene faunas were ecologically very different, with a greater proportion of erect and free-living species in the Caribbean compared to the less well-known Coral Triangle. Our results support the hypothesis that modern differences in diversity arose primarily from differential extinction of Caribbean erect and free-living species concomitant with oceanographic changes due to the uplift of the Isthmus of Panama, rather than exceptional rates of diversification in the Indo-Pacific.

Ghost reefs: Nautical charts document large spatial scale of coral reef loss over 240 years.

Massive declines in population abundances of marine animals have been documented over century-long time scales. However, analogous loss of spatial extent of habitat-forming organisms is less well known because georeferenced data are rare over long time scales, particularly in subtidal, tropical marine regions. We use high-resolution historical nautical charts to quantify changes to benthic structure over 240 years in the Florida Keys, finding an overall loss of 52% (SE, 6.4%) of the area of the seafloor occupied by corals. We find a strong spatial dimension to this decline; the spatial extent of coral in Florida Bay and nearshore declined by 87.5% (SE, 7.2%) and 68.8% (SE, 7.5%), respectively, whereas that of offshore areas of coral remained largely intact. These estimates add to finer-scale loss in live coral cover exceeding 90% in some locations in recent decades. The near-complete elimination of the spatial coverage of nearshore coral represents an underappreciated spatial component of the shifting baseline syndrome, with important lessons for other species and ecosystems. That is, modern surveys are typically designed to assess change only within the species' known, extant range. For species ranging from corals to sea turtles, this approach may overlook spatial loss over longer time frames, resulting in both overly optimistic views of their current conservation status and underestimates of their restoration potential.

Ecological persistence interrupted in Caribbean coral reefs.

The recent mass mortality of Caribbean reef corals dramatically altered reef community structure and begs the question of the past stability and persistence of coral assemblages before human disturbance began. We report within habitat stability in coral community composition in the Pleistocene fossil record of Barbados for at least 95,000 years despite marked variability in global sea level and climate. Results were consistent for surveys of both common and rare taxa. Comparison of Pleistocene and modern community structure shows that Recent human impacts have changed coral community structure in ways not observed in the preceding 220,000 years.

Structure of Caribbean coral reef communities across a large gradient of fish biomass.

The collapse of Caribbean coral reefs has been attributed in part to historic overfishing, but whether fish assemblages can recover and how such recovery might affect the benthic reef community has not been tested across appropriate scales. We surveyed the biomass of reef communities across a range in fish abundance from 14 to 593 g m(-2), a gradient exceeding that of any previously reported for coral reefs. Increased fish biomass was correlated with an increased proportion of apex predators, which were abundant only inside large marine reserves. Increased herbivorous fish biomass was correlated with a decrease in fleshy algal biomass but corals have not yet recovered.

Formation of the Isthmus of Panama.

The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.

Molluscan subfossil assemblages reveal the long-term deterioration of coral reef environments in Caribbean Panama.

Caribbean reef corals have declined sharply since the 1980s, but the lack of prior baseline data has hindered identification of drivers of change. To assess anthropogenic change in reef environments over the past century, we tracked the composition of subfossil assemblages of bivalve and gastropod mollusks excavated from pits below lagoonal and offshore reefs in Bocas del Toro, Panama. The higher prevalence of (a) infaunal suspension-feeding bivalves and herbivorous and omnivorous gastropods in lagoons and (b) epifaunal and suspension-feeding bivalves and carnivorous and suspension-feeding gastropods offshore reflected the greater influence of land-based nutrients/sediments within lagoons. Temporal changes indicated deteriorating environmental conditions pre-1960 in lagoons and post-1960 offshore, with offshore communities becoming more similar to lagoonal ones since 1960. Relative abundances of dominant bivalve species tracked those of their coral hosts, revealing broader ecosystem effects of coral community change. The nature and timing of changes implicate land-based runoff in reef deterioration.