Towards an understanding of resilience in isolated coral reefs

In 1998, seawater temperature anomalies led to unprecedented levels of coral bleaching on reefs worldwide. We studied the direct effects of this thermal event on benthic communities and its indirect effects on their associated coral reef fish communities at a group of remote reefs off NW Australia. Long‐term monitoring of benthic and fish assemblages on these reefs allowed us to compare the responses of these communities to coral bleaching using a data series that included 4 years before, and 6 years following, this bleaching event. While bleaching mortality was evident to >30 m depth, it was patchy among the shallower survey sites with decreases in live coral cover ranging from 30% to 90% across seven surveyed locations Within 2 years of the bleaching, hard coral recovery had begun at all sites and by 2003 reef‐wide coral cover had increased to ～39% of its preimpact levels. We exploited this pattern of differential survival of corals among sites, the associated changes in these benthic communities, and their patterns of recovery, to better understand links between benthic community dynamics and their associated fish communities. Temporal changes in the resident fish communities strongly reflected the differential shifts in the benthic communities, but were lagged by 12–18 months. Five years after the bleaching event, the fish communities on five of the seven surveyed locations showed evidence of recovery, however, none had regained their preimpact structures. Analyses of these communities by taxonomic family revealed a range of responses to the disturbance reflective of their life‐histories and trophic and habitat affiliations. The slow but recognizable recovery of this isolated reef system has parallels with other relatively isolated systems that displayed resilience to the 1998 bleaching event, e.g. the Chagos archipelago, but it also contrasts sharply with low levels of resilience documented in other isolated reef systems subject to the same disturbance, e.g. the Seychelles. In this context, our results highlight the significant knowledge gaps remaining in understanding the resilience of these ecosystems to disturbance.     

Extinct large colobines from the Plio-Pleistocene of Africa

Three genera and six species of extinct African Plio-Pleistocene Colobinae are discussed. One new genus, Rhinocolobus and three new species, R. turkanaensis, Cercopithecoides kimeui and Paracolobus mutiwa are named. These colobines show a diversity in postcranial and dental morphology not seen among extant species. Rhinocolobus was most similar to extant Colobus in postcranial morphology and had similar high-cusped shearing teeth. Cercopithecoides shows a number of postcranial skeletal features typical of terrestrial cercopithecid species and has lower cusped teeth. Paracolobus, while generally more similar to Rhinocolobus than to Cercopithecoides, is intermediate in some features of its postcranial morphology. The distribution of the various taxa among East and South African sites with different palaeoenvironments is generally consistent with the morphological interpretation. With the exception of Cercopithecoides kimeui, which persisted a little longer, these large colobines disappear from the fossil record about 1.8 million years ago. Their disappearance coincides with an interval of increasing aridity documented at Olduvai Gorge, the Omo Valley, and East Turkana.     

Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs

Around the globe, coral reefs and other marine ecosystems are increasingly overfished. Conventionally, studies of fishing impacts have focused on the population size and dynamics of targeted stocks rather than the broader ecosystem-wide effects of harvesting. Using parrotfishes as an example, we show how coral reef fish populations respond to escalating fishing pressure across the Indian and Pacific Oceans. Based on these fish abundance data, we infer the potential impact on four key functional roles performed by parrotfishes. Rates of bioerosion and coral predation are highly sensitive to human activity, whereas grazing and sediment removal are resilient to fishing. Our results offer new insights into the vulnerability and resilience of coral reefs to the ever-growing human footprint. The depletion of fishes causes differential decline of key ecosystem functions, radically changing the dynamics of coral reefs and setting the stage for future ecological surprises.     

Further hominids from the Plio-Pleistocene of Koobi Fora, Kenya

Fifty-eight new fossil hominids from Plio-Pleistocene sediments east of Lake Turkana, Kenya, are described. They include cranial, mandibular, dental, and postcranial parts. Some are illustrated.     

Century‐scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold

Coral bleaching, during which corals lose their symbiotic dinoflagellates, appears to be increasing in frequency and geographic extent, and is typically associated with abnormally high water temperatures and solar irradiance. A key question in coral reef ecology is whether local stressors reduce the coral thermal tolerance threshold, leading to increased bleaching incidence. Using tree‐ring techniques, we produced master chronologies of growth rates in the dominant reef builder, massive Montastraea faveolata corals, over the past 75–150 years from the Mesoamerican Reef. Our records indicate that the 1998 mass bleaching event was unprecedented in the past century, despite evidence that water temperatures and solar irradiance in the region were as high or higher mid‐century than in more recent decades. We tested the influence on coral extension rate from the interactive effects of human populations and thermal stress, calculated here with degree‐heating‐months (DHM). We find that when the effects of chronic local stressors, represented by human population, are taken into account, recent reductions in extension rate are better explained than when DHM is used as the sole predictor. Therefore, the occurrence of mass bleaching on the Mesoamerican reef in 1998 appears to stem from reduced thermal tolerance due to the synergistic impacts of chronic local stressors.     

Coral bleaching, reef fish community phase shifts and the resilience of coral reefs

The 1998 global coral bleaching event was the largest recorded historical disturbance of coral reefs and resulted in extensive habitat loss. Annual censuses of reef fish community structure over a 12-year period spanning the bleaching event revealed a marked phase shift from a prebleach to postbleach assemblage. Surprisingly, we found that the bleaching event had no detectable effect on the abundance, diversity or species richness of a local cryptobenthic reef fish community. Furthermore, there is no evidence of regeneration even after 5–35 generations of these short-lived species. These results have significant implications for our understanding of the response of coral reef ecosystems to global warming and highlight the importance of selecting appropriate criteria for evaluating reef resilience.     

Reconstructing past species assemblages reveals the changing patterns and drivers of extinction through time

Predicting future species extinctions from patterns of past extinctions or current threat status relies on the assumption that the taxonomic and biological selectivity of extinction is consistent through time. If the driving forces of extinction change through time, this assumption may be unrealistic. Testing the consistency of extinction patterns between the past and the present has been difficult, because the phylogenetically explicit methods used to model present-day extinction risk typically cannot be applied to the data from the fossil record. However, the detailed historical and fossil records of the New Zealand avifauna provide a unique opportunity to reconstruct a complete, large faunal assemblage for different periods in the past. Using the first complete phylogeny of all known native New Zealand bird species, both extant and extinct, we show how the taxonomic and phylogenetic selectivity of extinction, and biological correlates of extinction, change from the pre-human period through Polynesian and European occupation, to the present. These changes can be explained both by changes in primary threatening processes, and by the operation of extinction filter effects. The variable patterns of extinction through time may confound attempts to identify risk factors that apply across time periods, and to infer future species declines from past extinction patterns and current threat status.     

Molar tooth fragment BL5-0: the oldest human remain found in the Plio-Pleistocene of Orce (Granada province, Spain)

A molar tooth fragment from the Plio-Pleistocene Barranco León site 5 at Orce is shown to belong toHomo by analyses of its enamel in terms of the arrangement of the striae of Retzius and Hunter-Shreger bands, presence of perikymata, and of the thickness of the enamel, when compared with teeth of similarsized mammals of other taxa.     

Bears,pigs, and Plio-Pleistocene hominids: A case for the exploitation of belowground food resources

Belowground plant parts were important potential food resources in the habitats associated with Pliocene and early Pleistocene hominids. The food gathering and dental adaptations of three groups of modem mammals — bears, pigs, and humans — testify to the earlier convergence of these animals on this resource. Since belowground food reserves are relatively unaffected by the factors controlling aboveground food supply (fire, drought, and grazing stress), exploitation of this stable nutritional bank had distinct energetic and behavioral advantages for hominids.     

Habitat loss, resource specialization, and extinction on coral reefs

Coral reefs worldwide are being degraded because of global warming (coral bleaching) and coastal development (sedimentation and eutrophication). Predicting the risk of species extinctions from this type of habitat degradation is one of the most challenging and urgent tasks facing ecologists. Habitat specialists are thought to be more prone to extinction than generalists; however, specialists may be more susceptible to extinction because (1) they are specialists per se, (2) they are less abundant than generalists, or (3) both. Here, I show that declines in coral abundance lead to corresponding declines in the abundance of coral‐dwelling fishes, but with proportionally greater losses to specialists than generalists. In addition, specialists have smaller initial population sizes than generalists. Consequently, specialists face a dual risk of extinction because their already small populations decline more rapidly than those of generalists. Corresponding with this increased extinction risk, I describe the local extinction of one specialist species and the near‐global extinction of another species. I conclude that habitat specialists will be the first species lost from coral reefs because their small populations suffer the most from human‐induced disturbances.     

Identifying multiple coral reef regimes and their drivers across the Hawaiian archipelago

Loss of coral reef resilience can lead to dramatic changes in benthic structure, often called regime shifts, which significantly alter ecosystem processes and functioning. In the face of global change and increasing direct human impacts, there is an urgent need to anticipate and prevent undesirable regime shifts and, conversely, to reverse shifts in already degraded reef systems. Such challenges require a better understanding of the human and natural drivers that support or undermine different reef regimes. The Hawaiian archipelago extends across a wide gradient of natural and anthropogenic conditions and provides us a unique opportunity to investigate the relationships between multiple reef regimes, their dynamics and potential drivers. We applied a combination of exploratory ordination methods and inferential statistics to one of the most comprehensive coral reef datasets available in order to detect, visualize and define potential multiple ecosystem regimes. This study demonstrates the existence of three distinct reef regimes dominated by hard corals, turf algae or macroalgae. Results from boosted regression trees show nonlinear patterns among predictors that help to explain the occurrence of these regimes, and highlight herbivore biomass as the key driver in addition to effluent, latitude and depth.     

CO2 partial pressure controls the calcification rate of a coral community

Previous studies have demonstrated that coral and algal calcification is tightly regulated by the calcium carbonate saturation state of seawater. This parameter is likely to decrease in response to the increase of dissolved CO₂ resulting from the global increase of the partial pressure of atmospheric CO₂. We have investigated the response of a coral reef community dominated by scleractinian corals, but also including other calcifying organisms such as calcareous algae, crustaceans, gastropods and echinoderms, and kept in an open‐top mesocosm. Seawater pCO₂ was modified by manipulating the pCO₂ of air used to bubble the mesocosm. The aragonite saturation state (Ω_arag) of the seawater in the mesocosm varied between 1.3 and 5.4. Community calcification decreased as a function of increasing pCO₂ and decreasing Ω_arag. This result is in agreement with previous data collected on scleractinian corals, coralline algae and in a reef mesocosm, even though some of these studies did not manipulate CO₂ directly. Our data suggest that the rate of calcification during the last glacial maximum might have been 114% of the preindustrial rate. Moreover, using the average emission scenario (IS92a) of the Intergovernmental Panel on Climate Change, we predict that the calcification rate of scleractinian‐dominated communities may decrease by 21% between the pre‐industrial period (year 1880) and the time at which pCO₂ will double (year 2065).     

Integrating microbiological, microsensor, molecular, and physiologic techniques in the study of coral disease pathogenesis

The study of coral diseases requires an integrated approach that includes a combination of field and laboratory methods. By combining and building upon information available from multiple disciplines, within both field and laboratory applications, we have been successful in characterizing a number of coral diseases. To illustrate the utility of the integrative approach two very different coral diseases, black band disease and plague, are discussed in detail. Comparison of our ongoing characterization of each disease demonstrates that, within the integrative approach, different combinations of microbiological, microsensor, molecular, and physiologic techniques are required. The pathobiology of black band disease, which consists of a complicated, synergistic microbial consortium functioning around a dynamic sulfur cycle, is slowly being unraveled using a combination of methods. Our study of plague, on the other hand, has progressed in a very different manner that is controlled by the fact that this disease has, to date, emerged in three forms on reefs of the Florida Keys. The study of plague types I, II, and III will be detailed to illustrate the difficulty of characterizing a disease that rapidly evolves in the natural environment of the reef. Our ongoing study of additional (also very different) coral diseases will be summarized from the perspective of combined methodologies to illustrate the range and magnitude of questions that must be addressed and answered in order to understand coral disease pathogenesis and thus coral disease etiology.     

Species characteristics associated with extinction vulnerability and nestedness rankings of birds in tropical forest fragments

Following habitat fragmentation, species are predicted to go locally extinct from remnant patches in a predictable order due to differential extinction vulnerabilities. This selective species loss will result in nested distributions of species such that species found in depauperate patches will also tend to be found in larger, more speciose patches. Therefore, it should be possible to determine the relationship between species-specific characteristics and extinction vulnerability by comparing the order in which species are nested [i.e. nestedness ranking (NR)] with various natural history characteristics available from the literature and/or collected in the field. In this study, we investigate the relationship between the NRs of 41 resident forest-interior bird species inhabiting recently isolated landbridge islands in Lago Guri, Venezuela, with a large number of natural history characteristics collected from the literature (regional abundance, body length, habitat specificity, trophic guild, sensitivity to disturbance, range size) and from the field (local population density). In a comparison of the best regression models generated using just variables available through the literature (i.e. no local population density) with the best model generated using all possible variables, we found that the inclusion of field-based data significantly improved the amount of variation explained. The best overall model ( r ²=0.40, P <0.001) included body size, habitat specificity, zoogeographic distribution (a measure of range size) and local population density as predictors of NR. Understanding the factors that influence extinction vulnerability has important implications for conservation and could be used to help direct management efforts.     

Quantitative assessment of coral diseases in the Florida Keys: strategy and methodology

Natural incidences of disease among scleractinian corals are unknown, since most studies have been initiated in response to specific disease outbreaks. Our ability to distinguish elevated disease incidences influenced by anthropogenic and climatic factors is limited since current estimates are probably inflated for extrapolation to larger areas. In our study, we used quantitative assessment methods to characterize the distribution and frequency of scleractinian and gorgonian coral diseases in the south Florida region. This paper is the first in a series that will detail different aspects of our studies. In this paper, we examined the strategy and methodology developed over 2 years to optimize the experimental design of our study. Pilot surveys were conducted in 1997 to develop and test methods, select and determine suitability of sites, and obtain preliminary data to assess the variance and efficiency of the sampling design. Survey periods targeted late spring, the time when coral diseases are believed to emerge, and late summer, the time when coral diseases are believed to be most prevalent. Two strata were chosen to evaluate patterns of coral disease: the first, geographic area, consisted of reefs in the vicinity of Key West, New Grounds and the Dry Tortugas; and the second, reef type, consisted of back, fore and transitional reefs. Random radial arc transects (10 m diameter) were used to quantify 10 diseases affecting 18 species of stony corals and gorgonian sea fans over a large geographical region. During the pilot survey, we demonstrated that the outer 8–10 m segment (113 m²) was an adequate sampling area. The survey implemented important quality assurance measures for data quality control. Power analysis determined that future studies should adopt =0.10, =0.0383, and 1-=0.9617 in our experimental design. The highest prevalence of disease in our study was during the 1997 summer survey, with a mean percent coral disease (MPCD) of 28% occurring at Key West area reefs, or 55% of all back reef stations. Our results do not show a clear pattern of seasonality in coral diseases within either stratum, although differences in disease distribution between reef types and geographic areas were apparent in some of the spring and summer surveys.     

Longitudinal study of dental development in chimpanzees of known chronological age: Implications for understanding the age at death of Plio-Pleistocene hominids

Reconstruction of life history variables of fossil hominids on the basis of dental development requires understanding of and comparison with the pattern and timing of dental development among both living humans and pongids. Whether dental development among living apes or humans provides a better model for comparison with that of Plio-Pleistocene hominids of the genus Australopithecus remains a contentious point. This paper presents new data on chimpanzees documenting developmental differences in the dentitions of modern humans and apes and discusses their significance in light of recent controversies over the human or pongid nature of australopithecine dental development. Longitudinal analysis of 299 lateral head radiographs from 33 lab-reared chimpanzees (Pan troglodytes) of known chronological age allows estimation of means and standard deviations for the age at first appearance of 8 developmental stages in the mandibular molar dentition. Results are compared with published studies of dental development among apes and with published standards for humans. Chimpanzees are distinctly different from humans in two important aspects of dental development. Relative to humans, chimpanzees show advanced molar development vis a vis anterior tooth development, and chimpanzees are characterized by temporal overlap in the calcification of adjacent molar crowns, while humans show moderate to long temporal gaps between the calcification of adjacent molar crowns. In combination with recent work on enamel incremental markers and CAT scans of developing dentitions of Plio-Pleistocene hominids, this evidence supports an interpretation of a rapid, essentially “apelike” ontogeny among australopithecines. © 1996 Wiley-Liss, Inc.     

White-band disease and the changing face of Caribbean coral reefs

In recent decades, the cover of fleshy macroalgae has increased and coral cover has decreased on most Caribbean reefs. Coral mortality precipitated this transition, and the accumulation of macroalgal biomass has been enhanced by decreased herbivory and increased nutrient input. Populations of Acropora palmata (elkhorn coral) and A. cervicornis (staghorn coral), two of the most important framework-building species, have died throughout the Caribbean, substantially reducing coral cover and providing substratum for algal growth. Hurricanes have devastated local populations of Acropora spp. over the past 20–25 years, but white-band disease, a putative bacterial syndrome specific to the genus Acropora, has been a more significant source of mortality over large areas of the Caribbean region.Paleontological data suggest that the regional Acropora kill is without precedent in the late Holocene. In Belize, A. cervicornis was the primary ecological and geological constituent of reefs in the central shelf lagoon until the mid-1980s. After constructing reef framework for thousands of years, A. cervicornis was virtually eliminated from the area over a ten-year period. Evidence from other parts of the Caribbean supports the hypothesis of continuous Holocene accumulation and recent mass mortality of Acropora spp. Prospects are poor for the rapid recovery of A. cervicornis, because its reproductive strategy emphasizes asexual fragmentation at the expense of dispersive sexual reproduction. A. palmata also relies on fragmentation, but this species has a higher rate of sexual recruitment than A. cervicornis. If the Acropora spp. do not recover, macroalgae will continue to dominate Caribbean reefs, accompanied by increased abundances of brooding corals, particularly Agaricia spp. and Porites spp. The outbreak of white-band disease has been coincident with increased human activity, and the possibility of a causal connection should be further investigated.     

The impact of reduced pH on the microbial community of the coral Acropora eurystoma

Rising concentrations of atmospheric carbon dioxide are acidifying the world''s oceans. Surface seawater pH is 0.1 units lower than pre-industrial values and is predicted to decrease by up to 0.4 units by the end of the century. This change in pH may result in changes in the physiology of ocean organisms, in particular, organisms that build their skeletons/shells from calcium carbonate, such as corals. This physiological change may also affect other members of the coral holobiont, for example, the microbial communities associated with the coral, which in turn may affect the coral physiology and health. In the present study, we examined changes in bacterial communities in the coral mucus, tissue and skeleton following exposure of the coral Acropora eurystoma to two different pH conditions: 7.3 and 8.2 (ambient seawater). The microbial community was different at the two pH values, as determined by denaturing gradient gel electrophoresis and 16S rRNA gene sequence analysis. Further analysis of the community in the corals maintained at the lower pH revealed an increase in bacteria associated with diseased and stressed corals, such as Vibrionaceae and Alteromonadaceae. In addition, an increase in the number of potential antibacterial activity was recorded among the bacteria isolated from the coral maintained at pH 7.3. Taken together, our findings highlight the impact that changes in the pH may have on the coral-associated bacterial community and their potential contribution to the coral host.     

Escaping the heat: range shifts of reef coral taxa in coastal Western Australia

One of the most critical challenges facing ecologists today is to understand the changing geographic distribution of species in response to current and predicted global warming. Coastal Western Australia is a natural laboratory in which to assess the effect of climate change on reef coral communities over a temporal scale unavailable to studies conducted solely on modern communities. Reef corals composing Late Pleistocene reef assemblages exposed at five distinct localities along the west Australian coast were censused and the results compared with coral occurrence data published for the modern reefs offshore of each locality. The resulting comparative data set comprises modern and Late Pleistocene reef coral communities occurring over approximately 12° of latitude. For the modern reefs this gradient includes the zone of overlap between the Dampierian and Flindersian Provinces. Modern reef coral communities show a pronounced gradient in coral composition over the latitudinal range encompassed by the study, while the gradient in community composition is not as strong for Pleistocene communities. Tropical‐adapted taxa contracted their ranges north since Late Pleistocene time, emplacing two biogeographic provinces in a region in which a single province had existed previously. Beta diversity values for adjacent communities also reflect this change. Modern reefs show a distinct peak in beta diversity in the middle of the region; the peak is not matched by Pleistocene reefs. Beta diversity is correlated with distance only for comparisons between modern reefs in the north and the fossil assemblages, further supporting change in distribution of the biogeographic provinces in the study area. Coral taxa present in modern communities clearly expanded and contracted their geographic ranges in response to climate change. Those taxa that distinguish Pleistocene from modern reefs are predicted to migrate south in response to future climate change, and potentially persist in ‘temperature refugia’ as tropical reef communities farther north decline.     

The future of evolutionary diversity in reef corals

One-third of the world''s reef-building corals are facing heightened extinction risk from climate change and other anthropogenic impacts. Previous studies have shown that such threats are not distributed randomly across the coral tree of life, and future extinctions have the potential to disproportionately reduce the phylogenetic diversity of this group on a global scale. However, the impact of such losses on a regional scale remains poorly known. In this study, we use phylogenetic metrics in conjunction with geographical distributions of living reef coral species to model how extinctions are likely to affect evolutionary diversity across different ecoregions. Based on two measures—phylogenetic diversity and phylogenetic species variability—we highlight regions with the largest losses of evolutionary diversity and hence of potential conservation interest. Notably, the projected loss of evolutionary diversity is relatively low in the most species-rich areas such as the Coral Triangle, while many regions with fewer species stand to lose much larger shares of their diversity. We also suggest that for complex ecosystems like coral reefs it is important to consider changes in phylogenetic species variability; areas with disproportionate declines in this measure should be of concern even if phylogenetic diversity is not as impacted. These findings underscore the importance of integrating evolutionary history into conservation planning for safeguarding the future diversity of coral reefs.