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Lunulites are a polyphyletic group of marine bryozoans that have been a conspicuous element of marine shelf faunas since the Late Cretaceous into the present day. They are easily recognizable by their domed colony form and free-living mode of life on sea floor sediments. Here we explore the waxing and waning of the major lunulitiform groups and their unique morphology and mode of life from the Cretaceous to the present day. Because relatively few and simple modifications are needed to transition from an encrusting form into this highly specialized lifestyle, shared colonial features are rampant and we find examples of both convergent and iterative evolution across several unrelated clades, although detailed phylogenetic relationship remain largely unresolved. The early chapter of the ‘lunulite story’ is focused on the Late Cretaceous European Chalk Sea, which appears to have been a crucible for the evolution of ‘lunulites’. At least six, and likely more, cheilostome groups independently evolved the free-living mode of life in this tropical shelf area. To what extent any of these free-living clades gave rise to post-Cretaceous groups remains unclear. The Cenozoic chapter is more complex, comprising at least three independently evolved major clades, two of which are extant; (1) the Lunulitidae s. str., a North American/European cluster, comprising the classicLunulites, which became extinct in the late Neogene, (2) the Cupuladriidae, which reached circum-global tropical and sub-tropical distribution in the Miocene, and (3) the ‘Austral lunulite’ cluster, which is almost certainly polyphyletic and through most of its history confined to Australia and New Zealand, bar a comparatively brief colonization of the southern part of South America, with the earliest representatives from NW Western Australia.

While green turtles (Chelonia mydas) were once abundant throughout the Caribbean, overexploitation has dramatically reduced their numbers. We conducted a 168-day simulated grazing experiment to determine how loss of this once-abundant mega-herbivore could have affected the productivity and community composition of Thalassia testudinum-dominated seagrass beds in Bocas del Toro, Panama. Simulated grazing reduced both percent cover and productivity of T. testudinum. High runoff and local pollution from industrial farming may limit light availability and reduce seagrass photosynthetic performance to replace biomass lost to simulated grazing. Other seagrass species and algae failed to colonize space opened by reductions in T. testudinum percent cover. Many plots subjected to simulated grazing were also bioturbated by stingrays. Relevance of these findings to balancing sea turtle and seagrass conservation efforts are discussed.

International audience; Hotspots of tropical marine biodiversity are areas that harbour disproportionately large numbers of species compared to surrounding regions. The richness and location of these hotspots have changed throughout the Cenozoic. Here, we review the global dynamics of Cenozoic tropical marine biodiversity hotspots, including the four major hotspots of the Indo-Australian Archipelago (IAA), western Tethys (present Mediterranean), Arabian Sea and Caribbean Sea. Our review supports the ‘Hopping Hotspots’ model, which proposes that the locations of peak biodiversity are related to Tethyan faunal elements and track broad-scale shallow-marine habitats and high coastal complexity created by the collision of tectonic plates. A null hypothesis is the ‘Whack-A-Mole’ model, which proposes that hotspots occur in habitats suitable for high diversity regardless of taxonomic identity or faunal elements. Earlier ‘Centre-of’ theories (e.g. centres of origin with diversity decreasing with distance from supposed areas of exceptionally high rates of speciation, for which easy connection to adjacent regions to the east and west is important) were based on the analysis of recent biotas with no palaeontological foundation, and may better explain diversity dynamics within a hotspot rather than those between hotspots. More recently, however, human disturbance is massively disrupting these natural patterns.

13 pages, 4 figures, supporting Information https://doi.org/10.1111/ecog.05606.-- Data availability statement: Data available from the Dryad Digital Repository: https://dx.doi.org/10.5061/dryad.zs7h44j8s (Figuerola et al. 2021), Coastal hypoxia has become an increasingly acknowledged threat to coral reefs that is potentially intensifying because of increased input of anthropogenic nutrients. Almirante Bay (Caribbean Panama) is a semi-enclosed system that experiences hypoxia in deeper waters which occasionally shoals onto shallow coral reefs, suffocating most aerobic benthic life. To explore the long-term history of reefs in the bay we extracted reef matrix cores from two reefs that today experience contrasting patterns of oxygenation. We constructed a 1800-year-long record of gastropod assemblages and isotope compositions from six U-Th chronologically-constrained reef matrix cores. We extracted two cores from each reef at 3 m water depth and two additional cores from a deeper part (4.8 m) of the hypoxia-exposed reef. Results show that the deeper part of the hypoxic reef slowed in growth and stopped accreting approximately 1500 years BP while the shallow part of the reef continued to accrete to the present day, in agreement with a model of expanding hypoxia at this time. Our proxy-based approach suggests that the patterns of increasing herbivores and decreasing carbon isotope values in the deeper part of the hypoxic reef may have been driven by an increase in hypoxia via eutrophication caused by either natural changes or human impacts. Similar patterns in these paleoindicators occurred in the shallow part of the hypoxic reef during the last few decades. This suggests that the deep water hypoxia may be expanding to depths as shallow as 3 m and that shallow reefs are at greater risk due to increased human activity, This project and the research visit of BF to Texas A&M Univ. were financially supported by the Secretaría Nacional de Ciencia y Tecnología e Innovación (SENACYT; 47-2017-4-FID16-239), Sistema Nacional de Investigación (SENACYT), the Scholarly Studies Program (Smithsonian Institution), Smithsonian Tropical Research Institute (STRI), Texas A&M University and donations from M. Selin and family, J. Bilyk, V. and B. Anders, J. and M. Bytnar and the Young Presidents Organization (Los Angeles Gold Chapter). BF was supported by a STRI postdoctoral fellowship and the postdoctoral fellowships programme Beatriu de Pinós funded by the Secretary of Universities and Research (Government of Catalonia) and by the Horizon 2020 programme of research and innovation of the European Union under the Marie Skłodowska-Curie grant agreement no. 801370 (Incorporation grant 2019 BP 00183) and the Juan de la Cierva programme funded by the Ministry of Science and Innovation (Incorporation grant IJCI-2017-31478). With the institutional support of the ‘Severo Ochoa Centre of Excellence' accreditation (CEX2019-000928-S)

Caribbean coral reefs started to deteriorate before systematic monitoring began and so questions remain about how reefs have changed since human impact and if they have transitioned into functionally ‘novel’ states. To explore these questions, we mapped and bulk-sampled several hectares of mid-Holocene reefs in Caribbean Panama and the Dominican Republic and compared the composition and ecological function of these pre-human impact reefs to nearby modern reefs. We quantified the remains of all major reef groups, but focus here on molluscs, corals, and fishes. Filter feeding molluscs are twice as abundant relative to other feeding modes on modern reefs, commensurate with eutrophication from land use changes. At the same time, large herbivorous gastropods declined significantly in size due to millennia of human selective harvesting. We observed the well-documented loss of Acroporid corals and a functional shift in coral communities towards weedier, slower growing, and brooding species. Some modern coral communities appear to retain some historical functions, and isolated Acropora refugia do persist, but the corals in them are less robust than those in the mid-Holocene, questioning their functional resilience to future change. Reef fish otolith assemblages suggest an 80% decline in non-harvested fish and a relative increase in planktotrophy—patterns best explained by the loss of coral structure and eutrophication. Counterintuitively, otolith sizes suggest that non-harvested fish are larger than they were in the past, a result that suggests lower mortality rates from reduced predation due to a loss of predators. This conclusion is supported by the estimated 71% decline in shark abundances and 400% increase in evidence of damselfish algal-gardening on modern reefs. These examples illustrate how both bottom-up and top-down processes have reshaped the structure, trophic interactions and ecosystem functions of Caribbean reefscapes.

Along the coastal Tropical Eastern Pacific (TEP), regions of strong seasonal upwelling bring cold, nutrient-rich waters, controlling ecological conditions and sustaining millions of people through large-scale fisheries. The TEP is also important for the regulation of global climate and is affected by large-scale environmental processes such as ENSO. How the nutrient dynamics of this region will respond to climate change and what the implications will be for coastal ecology remains unknown. Environmental records are needed that capture intra and inter-decadal variation and extend over millennia where these biotic and abiotic processes interact. Here, we develop a new sampling approach and construct two coral skeleton records (n = >600) from reef matrix cores that extend six millennia, from the upwelling Gulf of Panamá and the non-upwelling Gulf of Chiriquí. We ask what effects millennial-scale climate patterns have on upwelling in the region, and how the magnitude of upwelled nutrients influences ecological productivity and even human habitation. We combined multiple proxies using climatic (carbonate δ18O), nutrient (skeletal-organic matrix δ15N), diagenetic (taphonomic scoring), ecological (benthic community composition), and temporal (U-Th dates) data. Using Generalised Additive Models to assess variability, we find strong divergences in the nutrient (δ15N; range >5 ‰) records between Gulfs, while δ18O (range ~2‰) is more stable. The greatest variation in δ15N values occurs during times of high reef accretion whereas δ18O is constant, suggesting that nutrients, not temperature, are driving reef productivity. Taphonomic, taxonomic, and age data reveal periodic shifts and collapses of coral communities that differ between Gulfs. We end by drawing connections between these ecological shifts to the episodic human habitation documented during the late-Holocene and hypothesize what this may mean for ecosystem resilience and environmental management under future climate.

Shark populations have declined over the last half century, but the patterns of change vary across space. Long-term records of shark abundance are limited, making it challenging to determine how local environmental conditions influence pre-exploitation shark baselines and their susceptibility to human impacts. We use shark scales (dermal denticles) preserved in coral reef sediments to reconstruct shark communities during the mid-Holocene and today across the Isthmus of Panama. We interpret these data alongside records of primary productivity, habitat, and fish abundance to explore energy flow to higher trophic levels on each coast. The Tropical Eastern Pacific is a productive system driven by seasonal upwelling with a long history of shark exploitation. The Caribbean coast, on the other hand, is oligotrophic and environmentally stable, with lower rates of harvesting. We find that denticle accumulation rates, a proxy for shark abundance, are an order of magnitude greater in Pacific Panama (Gulf of Panama) than in Caribbean Panama (Bocas del Toro). Primary productivity and fish abundance are also higher in Pacific Panama, helping to support these large predator populations. Denticle accumulation rates declined by 71% since the mid-Holocene in Caribbean Panama, including a selective loss of pelagic sharks. In contrast, modern denticle accumulation rates in Pacific Panama are comparable to their range of variability during the mid-Holocene, and the composition of denticle assemblages remained similar through time—suggesting that sharks in the Gulf of Panama have persisted despite intensive fishing. We postulate that the region’s high productivity might underlie its high shark abundance and apparent resilience by increasing available resources for predators. Our findings shed light on the role of energy in shaping natural variability in shark baselines and recovery potential. They also highlight the importance of incorporating oceanographic context into shark management.

Avila-Cervantes et al. proposed that glacial-interglacial sea level changes played an important role in the evolutionary and demographic histories of the crocodile Crocodylus acutus on the Isthmus of Panama. However, the study used erroneous sea level proxy data that produced flawed paleogeographic reconstructions. We present new paleogeographic reconstructions and review the timing of, and proposed mechanisms behind, the demographic events estimated by Avila-Cervantes et al.. With the data currently available, we find little evidence to support the hypothesis that sea level changes drove population demographic events in crocodiles on the Isthmus. Alternative hypotheses, including changing climate and habitat suitability, are equally valid and should be considered along with well-supported sea level models.

Caribbean biota underwent major ecological and evolutionary transformation in the Pliocene–Pleistocene, but a lack of detailed paleoenvironmental reconstruction prevents thorough resolution of cause and effect. We quantify levels of upwelling and freshwater input into Caribbean coastal shelf ecosystems over the last ∼6 m.y. with >3300 stable isotope measurements from 74 fossil serially sampled gastropods by normalizing δ18O values to open-ocean δ18O from planktonic foraminifera. We find that the influence of Pacific-like upwelling in the southwestern Caribbean was low after 4.25 Ma but coastal ecosystems were heavily influenced by seasonal freshening until ca. 2.5 Ma, after which time low-freshwater conditions were established. The origination of modern oligotrophic coastal conditions was therefore a result of oceanographic change causing declining upwelling, and declining nutrients from terrestrial sources. We speculate that a southward shift of the Intertropical Convergence Zone, associated with Northern Hemisphere glaciation, reduced rainfall and terrestrial nutrient input and contributed to biotic turnover in the southwestern Caribbean, including the proliferation of modern reef communities.

Coastal hypoxia has become an increasingly acknowledged threat to coral reefs that is potentially intensifying because of increased input of anthropogenic nutrients. Almirante Bay (Caribbean Panama) is a semi-enclosed system that experiences hypoxia in deeper waters which occasionally expand into shallow coral reefs, suffocating most aerobic benthic life. To explore the long-term history of reefs in the bay we extracted reef matrix cores from two reefs that today experience contrasting patterns of oxygenation. We constructed a 1800-year-long record of gastropod assemblages and isotope compositions from six U-Th chronologically-constrained reef matrix cores. We extracted two cores from each reef at 3 m water depth and two additional cores from a deeper part (4.8 m) of the hypoxia-exposed reef. Results show that the deeper part of the hypoxic reef slowed in growth and stopped accreting approximately 1500 years BP while the shallow part of the reef continued to accrete to the present day, in agreement with a model of expanding hypoxia at this time. Our proxy-based approach suggests that differences among these palaeoindicators in the two reefs may have been driven by an increase in hypoxia via eutrophication caused by either natural changes or human impacts. Similar patterns of increasing herbivores and decreasing carbon isotope values occurred in the shallow part of the hypoxic reef during the last few decades. This suggests that hypoxia may be expanding to depths as shallow as 3 m and that shallow reefs are experiencing greater risk due to increased human activity.

Although protocols exist for the recovery of ancient DNA from land snail and marine bivalve shells, marine conch shells have yet to be studied from a paleogenomic perspective. We first present reference assemblies for both a 623.7 Mbp nuclear genome and a 15.4 kbp mitochondrial genome for Strombus pugilis, the West Indian fighting conch. We next detail a method to extract and sequence DNA from conch shells and apply it to conch from Bocas del Toro, Panama across three time periods: recently-eaten and discarded (n = 3), Late Holocene (984-1258 before present [BP]) archaeological midden (n = 5), and mid-Holocene (5711-7187 BP) paleontological fossil coral reef (n = 5). These results are compared to control DNA extracted from live-caught tissue and fresh shells (n = 5). Using high-throughput sequencing, we were able to obtain S. pugilis nuclear sequence reads from shells across all age periods: up to 92.5 thousand filtered reads per sample in live-caught shell material, 4.57 thousand for modern discarded shells, 12.1 thousand reads for archaeological shells, and 114 reads in paleontological shells. We confirmed authenticity of the ancient DNA recovered from the archaeological and paleontological shells based on 5.7× higher average frequency of deamination-driven misincorporations and 15% shorter average read lengths compared to the modern shells. Reads also mapped to the S. pugilis mitochondrial genome for all but the paleontological shells, with consistent ratios of mitochondrial to nuclear mapped reads across sample types. Our methods can be applied to diverse archaeological sites to facilitate reconstructions of the long-term impacts of human behaviour on mollusc evolutionary biology.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions., This Essay argues that in order to truly understand how marine hosts benefit from the immense diversity of microbes, we need to expand towards long-term, multi-disciplinary research focussing on few areas of the world’s ocean that we refer to as “natural experiments,” where processes can be studied at scales that far exceed those captured in laboratory experiments.

Although protocols exist for the recovery of ancient DNA from land snail and marine bivalve shells, marine conch shells have yet to be studied from a paleogenomic perspective. We first present reference assemblies for both a 623.7 Mbp nuclear genome and a 15.4 kbp mitochondrial genome for Strombus pugilis, the West Indian fighting conch. We next detail a method to extract and sequence DNA from conch shells and apply it to conch from Bocas del Toro, Panama across three time periods: recently-eaten and discarded (n=3), Late Holocene (984-1258 BP) archaeological midden (n=5), and a mid-Holocene (5711-7187 BP) paleontological fossil coral reef (n=5). These results are compared to control DNA extracted from live-caught tissue and fresh shells (n=5). Using high-throughput sequencing, we were able to obtain S. pugilis nuclear sequence reads from shells across all age periods: up to 92.5 thousand filtered reads per sample in live-caught shell material, 4.57 thousand for modern discarded shells, 12.1 thousand reads for archaeological shells, and 114 reads in paleontological shells. We confirmed authenticity of the ancient DNA recovered from the archaeological and paleontological shells based on 5.7x higher average frequency of deamination-driven misincorporations and 15% shorter average read lengths compared to the modern shells. Reads also mapped to the S. pugilis mitochondrial genome for all but the paleontological shells, with consistent ratios of mitochondrial to nuclear mapped reads across sample types. Our methods can be applied to diverse archaeological sites to facilitate reconstructions of the long-term impacts of human behavior on mollusc evolutionary biology.

Esta guía presenta una clave para la identificación de los otolitos sagita de las seis especies de Cynoscion reportadas en las costas Panameñas del Océano Pacífico y que ocupan un lugar importante dentro de las pesquerías del país. Para la creación de la misma se realizaron descripciones morfológicas y morfométricas, las cuales se encuentran organizadas en una serie de fichas que siguen un orden alfabético. También cuenta con láminas ilustrativas que presentan de tres a cuatro otolitos para cada especie, mostrando la cara interna, la cara externa y la vista lateral de cada uno. Solamente fueron seleccionados otolitos derechos para mantener una posición y orientación consistente. Los otolitos en las láminas están organizados en orden alfabético y varían en tamaño (siguiendo un orden de menor a mayor). Las barras de escala representan 1 unidad de centímetro.

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Direct observations of marine ecosystems are inherently limited in their temporal scope. Yet, ongoing global anthropogenic change urgently requires improved understanding of long-term baselines, greater insight into the relationship between climate and biodiversity, and knowledge of the evolutionary consequences of our actions. Sediment cores can provide this understanding by linking data on the responses of marine biota to reconstructions of past environmental and climatic change. Given continuous sedimentation and robust age control, studies of sediment cores have the potential to constrain the state and dynamics of past climates and ecosystems on timescales of centuries to millions of years. Here, we review the development and recent advances in “ocean drilling paleobiology”—a synthetic science with potential to illumi-nate the interplay and relative importance of ecological and evolutionary factors during times of global change. Climate, specifically temperature, appears to control Cenozoic marine ecosystems on million-year, millennial, centennial, and anthropogenic time-scales. Although certainly not the only factor controlling biodiversity dynamics, the effect size of temperature is large for both pelagic and deep-sea ecosystems.

Seasonality is a dominant factor in the Earth’s climate system, but proxy reconstructions on this time scale are sparse. Corals provide an excellent archive to reconstruct environmental conditions on seasonal time scale using geochemical proxies. Here, we use subfossil (~6.2-7.1 ka BP) Siderastrea siderea and Pseudodiploria labyrinthiformis corals from a pristine Mid-Holocene reef, located in Panamá, southwestern Caribbean. Mid-Holocene insolation seasonality in the Northern Hemisphere was stronger than at present. We investigate the resulting changes in SST and hydrological seasonality using coral Sr/Ca, δ18O and δ13C. To evaluate, if the coral heads can be utilised for geochemical analyses, they have been screened for diagenetic alteration (2D-XRD, thin section analysis). Obtained modern coral Sr/Ca-SST based annual cycle corresponds well with in situ measured SST. Fossil coral Sr/Ca-SST based cycles exceed the modern one by up to 50%. Fossil coral δ18O seasonal amplitudes are higher than the modern one by up to 30% and show a reduction in the mean gradient between wet and dry period, attributable to the northward shift of the Intertropical Convergence Zone. Increased SST and δ18O seasonality are consistent with model simulated SSTs (Kiel Climate Model) and model-based calculated pseudocoral δ18O, but the model underestimates the seasonality increase in the Mid-Holocene.

Many Caribbean coral reefs are heavily degraded, yet their pre-human, natural states are often assumed or estimated using space-for-time substitution approaches. Here we use an 11-hectare suite of fossilised mid-Holocene (7.2–5.6 ka) fringing reefs in Caribbean Panama to define natural variation in hard coral community structure before human-impact to provide context to the states of the same reefs today. We collected bulk samples from four trenches dug into the mid-Holocene fossil reef and surficial bulk samples from 2–10 m depths on five adjacent modern reefs extending over 5 km. Analysis of the abundances of coral taxa in fossil bulk samples define the Historical Range of Variation (HRV) in community structure of the reefs. When compared to the community structure of adjacent modern reefs, we find that most coral communities today fall outside the HRV, identifying them as novel ecosystems and corroborating the well-documented transition from acroporid-dominated Caribbean reefs to reefs dominated by stress-tolerant taxa (Porites and Agaricia). We find one modern reef, however, whose community composition remains within the HRV showing that it has not transitioned to a novel state. Reef-matrix cores extracted from this reef reveal that the coral community has remained in this state for over 800 years, suggesting long-term stability and resistance to the region-wide shift to novel states. Without these data to provide historical context, this potentially robust and stable reef would be overlooked since it does not fulfil expectations of what a Caribbean coral reef should look like in the absence of humans. This example illustrates how defining past variation using the fossil record can improve our understanding of modern degradation and guide conservation.

Large tropical river dam projects are expected to accelerate over the forthcoming decades to satisfy growing demand for energy, irrigation and flood control. When tropical rivers are dammed the immediate impacts are relatively well studied, but the long-term (decades-centuries) consequences of impoundment remain poorly known. We combined historical records of water quality, river flow and climate with a multi-proxy (macrofossils, diatoms, biomarkers and trace elements) palaeoecological approach to reconstruct the limnological evolution of a shallow basin in Gatun Lake (Panama Canal, Panama) and assess the effects of multiple linked factors (river damming, forest flooding, deforestation, invasive species, pollution and hydro-climate) on the study area. Results show that a century after dam construction, species invasion, deforestation and salt intrusions have forced a gradual change in the study basin from a swamp-type environment towards a more saline lake-governed system of benthic-littoral production likely associated with the expansion of macrophyte stands. Hydrology still remains the most important long-term (decades) structural factor stimulating salinity intrusions, primary productivity, deposition of minerals, and reduction of water transparency during wet periods. During dry periods, physical-chemical conditions are in turn linked to clear water and aerobic conditions while nutrients shift to available forms for the aquatic biota in the detrital-rich reductive sediments. Our study suggests that to preserve the natural riverine system functioning of this area of the Panama Canal, management activities must address long-term ecosystem structural drivers such as river flow, runoff patterns and physical-chemical conditions.

The significance of symbioses between eukaryotic hosts and microbes extends from the organismal to the ecosystem level and underpins the health of Earth’s most threatened marine ecosystems. Despite rapid growth in research on host-associated microbes, from individual microbial symbionts to host-associated consortia of significantly relevant taxa, little is known about their interactions with the vast majority of marine host species. We outline research priorities to strengthen our current knowledge of host–microbiome interactions and how they shape marine ecosystems. We argue that such advances in research will help predict responses of species, communities, and ecosystems to stressors driven by human activity and inform future management strategies., The significance of symbioses between eukaryotic hosts and microbes extends from the organismal to the ecosystem level and underpins the health of Earth’s most threatened marine ecosystems. This Perspective article outlines research priorities to strengthen our current knowledge of host-microbiome interactions, to help predict responses to anthropogenic stressors and to inform future management strategies.

Urchins are the last abundant grazers of macroalgae on most Caribbean reefs following the historical overexploitation of herbivorous fishes. The long-spined urchin Diadema antillarum was particularly effective at controlling macroalgae and facilitating coral dominance on Caribbean reefs until its ecological extinction from a catastrophic disease epidemic in the early 1980s. Despite their important role in the structure and functioning of Caribbean reef ecosystems, the natural dynamics of Caribbean reef urchin communities are poorly known due to the paucity of ecological survey data prior to large-scale human disturbances and the Diadema dieoff. To help resolve the baseline abundances and ecological roles of common urchin taxa, we track changes in urchin abundance and composition over the past 3000 yr from analysis of subfossil urchin spines preserved in reef matrix cores collected in Caribbean Panama. Echinometra consistently dominated the subfossil spine assemblage, while Diadema was consistently rare in the subfossil record in this region. Rather than increasing during a period of heightened human exploitation of their fish competitors and predators, Diadema began declining over a millennium ago. Convergent cross mapping (CCM) causality analyses reveal that Diadema abundance is causally related to coral community composition. Diadema is negatively affected by Acropora cervicornis dominance, likely due to the tight association between this coral and the threespot damselfish, an effective Diadema competitor. Conversely, Diadema positively affects the abundance of the coral Madracis mirabilis, possibly via its control of macroalgae. Causal relationships were not detected among abundances of individual urchin taxa, indicating that inter-specific echinoid competition is not a factor limiting Diadema recovery. Our detailed record of prehistorical and historical urchin community dynamics suggests that the failure of Diadema to recover over 30 yr after its mass mortality event may be due in part to the prey release of damselfish following the long-term overfishing of piscivorous fishes.

We use time-series δ18O and δ13C data from seawater and live-collected Conus shells from Panama's Pacific coast to test the fidelity of the gastropod's δ13C values as a proxy for the δ13C of marine dissolved inorganic carbon (DIC), and the potential of δ18O-δ13C correlations in shell profiles for resolving relative magnitudes of seasonal upwelling and freshening. Water samples were collected from March 2011 to August 2012 from Naos Island Marine Laboratory, and Conus specimens were collected from nearby Veracruz Beach in July 2013. In general, patterns corresponded with seasonal changes in rainfall and upwelling on the Pacific coast of Panama. During the long rainy season, the upwelling signal is absent and seawater salinity, δ18O, and δ13CDIC all decline. During the dry season, the upwelling signal increases and runoff declines increasing salinity, δ18O, and δ13CDIC values. Shell δ13C values strongly correlate with measured δ13CDIC values, but are lower than expected equilibrium for aragonite by approximately + 2‰ reflecting the incorporation of light metabolic C. The co-dependences of δ18O and δ13C provide reliable indicators of upwelling (negative correlation) and freshening (positive correlation) for nearshore environments, allowing for the study of historical climate change and upwelling based on beach-collected museum specimens.

Caribbean coral reefs have transformed into algal-dominated habitats over recent decades, but the mechanisms of change are unresolved due to a lack of quantitative ecological data before large-scale human impacts. To understand the role of reduced herbivory in recent coral declines, we produce a high-resolution 3,000 year record of reef accretion rate and herbivore (parrotfish and urchin) abundance from the analysis of sediments and fish, coral and urchin subfossils within cores from Caribbean Panama. At each site, declines in accretion rates and parrotfish abundance were initiated in the prehistorical or historical period. Statistical tests of direct cause and effect relationships using convergent cross mapping reveal that accretion rates are driven by parrotfish abundance (but not vice versa) but are not affected by total urchin abundance. These results confirm the critical role of parrotfish in maintaining coral-dominated reef habitat and the urgent need for restoration of parrotfish populations to enable reef persistence., Fishing of keystone herbivores such as parrotfish is thought to negatively impact corals. Here, Cramer and colleagues analyse the sedimentary record for the last 3,000 years from three coral reef sites in the Caribbean and show that indeed coral declines are linked to parrotfish declines.

Large tropical river dam projects are set to accelerate over the forthcoming decades to satisfy growing demand for energy, irrigation and flood control. When tropical rivers are dammed, the immediate impacts are well studied, but the long-term (decades-centuries) consequences of impoundment remain poorly known. Here, we gather historical and paleoecological data from Gatun Lake, formed by the building of the Gatun Dam (Panama Canal, Panamá) over 100 years ago, to reconstruct the limnological evolution of the system in response to individual and linked stressors (river damming, forest flooding, deforestation, invasive species, pollution and hydro-climate). We found that after a century of dam construction parallels associated with the natural hydrological functioning of river floodplains persist. Hence, hydrology remains the most important temporal structural factor positively stimulating primary productivity, deposition of new minerals, and reduction of water transparency during wet periods. During dry periods, clear water and aerobic conditions prevail and nutrients transform into available forms in the detrital-rich reductive sediments. We highlight the importance of climate change as an ultimate rather than proximate anthropogenic factor for sustainable management options of tropical dams.

The significance of mutualisms between eukaryotic hosts and microbes extends from the organismal to the ecosystem level, and mutualistic symbioses underpin the health of Earth’s most threatened marine ecosystems. Despite rapid growth in research on host-associated microbes (microbiomes), very little is known about their interactions for the vast majority of marine host species. We outline research priorities to broaden our current knowledge of host-microbiome interactions and how they shape marine ecosystems. We argue that this research frontier will allow us to predict responses of species, communities, and ecosystems to stressors driven by human activity, and inform future management and mitigation.

AimTo quantify the effect of Pleistocene climate fluctuations on habitat connectivity across páramos in the Northern Andes.LocationNorthern Andes.MethodsThe unique páramos habitat underwent dynamic shifts in elevation in response to changing climate conditions during the Pleistocene. The lower boundary of the páramos is defined by the upper forest line, which is known to be highly responsive to temperature. Here, we reconstruct the extent and connectivity of páramos over the last 1 million years (Myr) by reconstructing the upper forest line from the long fossil pollen record of Funza09, Colombia, and applying it to spatial mapping on modern topographies across the Northern Andes for 752 time slices. Data provide an estimate of how often and for how long different elevations were occupied by páramos and estimate their connectivity to provide insights into the role of topography in biogeographical patterns of páramos.ResultsOur findings show that connectivity amongst páramos of the Northern Andes was highly dynamic, both within and across mountain ranges. Connectivity amongst páramos peaked during extreme glacial periods but intermediate cool stadials and mild interstadials dominated the climate system. These variable degrees of connectivity through time result in what we term the ‘flickering connectivity system’. We provide a visualization (video) to showcase this phenomenon. Patterns of connectivity in the Northern Andes contradict patterns observed in other mountain ranges of differing topographies.Main conclusionsPleistocene climate change was the driver of significant elevational and spatial shifts in páramos causing dynamic changes in habitat connectivity across and within all mountain ranges. Some generalities emerge, including the fact that connectivity was greatest during the most ephemeral of times. However, the timing, duration and degree of connectivity varied substantially among mountain ranges depending on their topographical configuration. The flickering connectivity system of the páramos uncovers the dynamic settings in which evolutionary radiations shaped the most diverse alpine biome on Earth.

Little is known about long-term changes in coral reef fish communities. Here we present a new technique that leverages fish otoliths in reef sediments to reconstruct coral reef fish communities. We found over 5,400 otoliths in 169 modern and mid-Holocene bulk samples from Caribbean Panama and Dominican Republic mid-Holocene and modern reefs, demonstrating otoliths are abundant in reef sediments. With a specially-built reference collection, we were able to assign over 4,400 otoliths to one of 56 taxa (35 families) though mostly at genus and family level. Many otoliths were from juvenile fishes for which identification is challenging. Richness (by rarefaction) of otolith assemblages was slightly higher in modern than mid-Holocene reefs, but further analyses are required to elucidate the underlying causes. We compared the living fish communities, sampled using icthyocide, with the sediment otolith assemblages on four reefs finding the otolith assemblages faithfully capture the general composition of the living fish communities. Radiocarbon dating performed directly on the otoliths suggests that relatively little mixing of sediment layers particularly on actively accreting branching coral reefs. All otolith assemblages were strongly dominated by small, fast-turnover fish taxa and juvenile individuals, and our exploration on taxonomy, functional ecology and taphonomy lead us to the conclusion that intense predation is likely the most important process for otolith accumulation in reef sediments. We conclude that otolith assemblages in modern and fossil reef sediments can provide a powerful tool to explore ecological changes in reef fish communities over time and space.

Migration is an integral feature of modern mysticete whale ecology, and the demands of migration may have played a key role in shaping mysticete evolutionary history. Constraining when migration became established and assessing how it has changed through time may yield valuable insight into the evolution of mysticete whales and the oceans in which they lived. However, there are currently few data which directly assess prehistoric mysticete migrations. Here we show that calcite δ(18)O profiles of two species of modern whale barnacles (coronulids) accurately reflect the known migration routes of their host whales. We then analyze well-preserved fossil coronulids from three different locations along the eastern Pacific coast, finding that δ(18)O profiles from these fossils exhibit trends and ranges similar to modern specimens. Our results demonstrate that migration is an ancient behavior within the humpback and gray whale lineages and that multiple Pleistocene populations were undertaking migrations of an extent similar to those of the present day.

The distribution of mid-Holocene, tropical benthic foraminiferal assemblages, including species' proportions, diversity, dominance and wall type, were analyzed for their correspondence to marine habitats and invertebrate facies. Benthic foraminifera are useful for paleoenvironmental reconstructions because the modern ecology of many species found as Quaternary fossils is known. Samples were collected from trenches in ~30,000 m2 of an excavated Acropora cervicornis-dominated, mid-Holocene reef with an age of ~6 kyr on Isla Colon (Colon island), bordering Almirante Bay in Bocas del Toro, Caribbean Panama. Bulk sediment samples were collected from a maximum depth of ~7 m below modern mean sea level and classified in the field into five invertebrate biofacies: 1) A. cervicornis-dominated reef, 2) molluscan mud, 3) Porites-Agaricia reef, 4) mixed coral, and 5) Lobatus-dominated seagrass. Sediment carbon and grain size analyses, a cluster analysis performed on the relative abundance of species per sample, and the Fisher's alpha diversity index were used to compare sample similarity and environmental variables to determine habitat relationships. Most samples contained high total inorganic carbon and poorly sorted, medium-coarse sediments. Principle component analysis of sediment grain size and carbon values did not show a clear correspondence among samples, habitat type or location of trenches. Foraminiferal assemblages in A. cervicornis and other reefal samples (categories 1, 3 and 4, above) had the greatest diversity and did not distinguish between the three reefal types, suggesting similar, normal marine conditions and/or mixing of coral fragments. Molluscan mud samples with high total organic carbon content were least diverse with dominant Ammonia and Elphidium taxa, though foraminifera in other molluscan mud samples showed a transition to proximal reef corals. Seagrass samples were differentiated from molluscan mud samples and had similar diversities and species assemblages to the Porites-Agaricia samples, and taxa known to be temporary grazers and living temporarily attached to seagrass blades are present in relatively greater amounts in these samples. Based on the distribution of foraminiferal species across this mid-Holocene coral reef, we conclude that it was a patch reef that included high-organic and seagrass facies similar to those of modern Almirante Bay. Results from this study can be compared to modern foraminiferal studies to investigate whether the modern habitats of BDT are significantly different from the pristine reefs of the mid-Holocene.

The breadth of habitat occupied by a species, and the rate at which a species can expand into new habitats has important ecological and evolutionary consequences. Here we explore when extant species of free-living cupuladriid bryozoans expanded into new benthic Caribbean habitats that emerged during the final stages of formation of the Isthmus of Panama. Habitat breadth was estimated using the abundances of over 90,000 colonies in ten cupuladriid species, along with the ecological and sedimentary characteristics of the samples in which they occurred. Data reveal that all species expanded their habitat breadths during the last 6 Myr, but did so at a different tempo. ‘Young’ species - those that originated after 5 Ma - expanded relatively quickly, whereas ‘old’ species - those that originated before 9 Ma - took a further 2 Myr to achieve a comparable level of expansion. We propose that, like invasive species, young species are less restrained when expanding their habitat breadths compared to older well-established species. Understanding the mechanism causing this restraint requires further research

Recognizing the threat of additive risk Humans are accelerating the extinction rates of species in both terrestrial and marine environments. However, species extinctions have occurred across time for a variety of other reasons. Finnegan et al. looked at the extinction rates across marine genera (groups of species) over the past 23 million years to determine intrinsic extinction rates and what traits or regions correspond to the highest rates. Combining patterns of intrinsic extinction with regions of high anthropogenic threat revealed taxa and areas, particularly in the tropics, where the risk of extinction will be especially high. Science , this issue p. 567