The fundamental niche of blood oxygen binding in the pelagic ocean

Marine species ranging in size from microscopic zooplankton to large predatory fish move vertically in the ocean water column to forage for food and avoid predators. Oxygen and temperature decrease, often rapidly, from shallow to deeper depths, restricting the ability of species to use the vertical habitat. One physiological trait that determines the tolerance of organisms to low oxygen is the oxygen affinity of oxygen carrier proteins, hemoglobin and hemocyanin, in the blood. To quantify the range of oxygen affinities for marine organisms, we surveyed the literature for measurements of oxygen binding to blood at multiple temperatures to account for its temperature sensitivity. Oxygen affinity is mapped within the ocean environment using the depth at which oxygen pressure decreases to the point at which the blood is 50% oxygenated (P₅₀ depth) as organisms move from the surface to depth in the ocean water column. We find that vertical gradients in both temperature and oxygen impact the vertical position and areal extent of P₅₀ depths. Shifts in P₅₀ due to temperature cause physiological types with the same P₅₀ in the surface ocean to have different P₅₀ depths and physiological types with different P₅₀'s in the surface ocean to have the same P₅₀ depth. The vertical distances between P₅₀ depths are spatially variable, which may determine the frequency of ecological interactions, such as competition and predation. In summary, P₅₀ depth, which represents a key physiological transition point between dexoxygenated and oxygenated blood, provides mechanistic insight into organism function within the water column of the global ocean.     

Large but uneven reduction in fish size across species in relation to changing sea temperatures

Ectotherms often attain smaller body sizes when they develop at higher temperatures. This phenomenon, known as the temperature–size rule, has important consequences for global fisheries, whereby ocean warming is predicted to result in smaller fish and reduced biomass. However, the generality of this phenomenon and the mechanisms that drive it in natural populations remain unresolved. In this study, we document the maximal size of 74 fish species along a steep temperature gradient in the Mediterranean Sea and find strong support for the temperature–size rule. Importantly, we additionally find that size reduction in active fish species is dramatically larger than for more sedentary species. As the temperature dependence of oxygen consumption depends on activity levels, these findings are consistent with the hypothesis that oxygen is a limiting factor shaping the temperature–size rule in fishes. These results suggest that ocean warming will result in a sharp, but uneven, reduction in fish size that will cause major shifts in size‐dependent interactions. Moreover, warming will have major implications for fisheries as the main species targeted for harvesting will show the most substantial declines in biomass.     

Ecological change in dynamic environments: Accounting for temporal environmental variability in studies of ocean change biology

The environmental conditions in the ocean have long been considered relatively more stable through time compared to the conditions on land. Advances in sensing technologies, however, are increasingly revealing substantial fluctuations in abiotic factors over ecologically and evolutionarily relevant timescales in the ocean, leading to a growing recognition of the dynamism of the marine environment as well as new questions about how this dynamism may influence species' vulnerability to global environmental change. In some instances, the diurnal or seasonal variability in major environmental change drivers, such as temperature, pH and seawater carbonate chemistry, and dissolved oxygen, can exceed the changes expected with continued anthropogenic global change. While ocean global change biologists have begun to experimentally test how variability in environmental conditions mediates species' responses to changes in the mean, the extensive literature on species' adaptations to temporal variability in their environment and the implications of this variability for their evolutionary responses has not been well integrated into the field. Here, we review the physiological mechanisms underlying species' responses to changes in temperature, pCO₂/pH (and other carbonate parameters), and dissolved oxygen, and discuss what is known about behavioral, plastic, and evolutionary strategies for dealing with variable environments. In addition, we discuss how exposure to variability may influence species' responses to changes in the mean conditions and highlight key research needs for ocean global change biology.     

Normal giants? Temporal and latitudinal shifts of Palaeozoic marine invertebrate gigantism and global change

During and after the Cambrian explosion, very large marine invertebrate species have evolved in several groups. Gigantism in Carboniferous land invertebrates has been explained by a peak in atmospheric oxygen concentrations, but Palaeozoic marine invertebrate gigantism has not been studied empirically and explained comprehensively. By quantifying the spatiotemporal distribution of the largest representatives of some of the major marine invertebrate clades (orthoconic cephalopods, ammonoids, trilobites, marine eurypterids), we assessed possible links between environmental parameters (atmospheric or oceanic oxygen concentrations, ocean water temperature or sea level) and maximum body size, but we could not find a straightforward relationship between both. Nevertheless, marine invertebrate gigantism within these groups was temporally concentrated within intervals of high taxonomic diversity (Ordovician, Devonian) and spatially correlated with latitudes of high occurrence frequency. Regardless of whether temporal and spatial variation in sampled diversity and occurrence frequency reflect true biological patterns or sampling controls, we find no evidence that the occurrences of giants in these groups were controlled by optimal conditions other than those that controlled the group as a whole; if these conditions shift latitudinally, occurrences of giants will shift as well. It is tempting to attribute these shifts to contemporary changes in temperature, oxygen concentrations in the atmosphere and the oceans as well as global palaeogeography over time, but further collection‐based studies are necessary on finer stratigraphic and phylogenetic resolution to corroborate such hypotheses and rule out sampling or collection biases.     

The influence of the biological pump on ocean chemistry: implications for long‐term trends in marine redox chemistry,the global carbon cycle,and marine animal ecosystems

The net export of organic matter from the surface ocean and its respiration at depth create vertical gradients in nutrient and oxygen availability that play a primary role in structuring marine ecosystems. Changes in the properties of this ‘biological pump’ have been hypothesized to account for important shifts in marine ecosystem structure, including the Cambrian explosion. However, the influence of variation in the behavior of the biological pump on ocean biogeochemistry remains poorly quantified, preventing any detailed exploration of how changes in the biological pump over geological time may have shaped long‐term shifts in ocean chemistry, biogeochemical cycling, and ecosystem structure. Here, we use a 3‐dimensional Earth system model of intermediate complexity to quantitatively explore the effects of the biological pump on marine chemistry. We find that when respiration of sinking organic matter is efficient, due to slower sinking or higher respiration rates, anoxia tends to be more prevalent and to occur in shallower waters. Consequently, the Phanerozoic trend toward less bottom‐water anoxia in continental shelf settings can potentially be explained by a change in the spatial dynamics of nutrient cycling rather than by any change in the ocean phosphate inventory. The model results further suggest that the Phanerozoic decline in the prevalence ocean anoxia is, in part, a consequence of the evolution of larger phytoplankton, many of which produce mineralized tests. We hypothesize that the Phanerozoic trend toward greater animal abundance and metabolic demand was driven more by increased oxygen concentrations in shelf environments than by greater food (nutrient) availability. In fact, a lower‐than‐modern ocean phosphate inventory in our closed system model is unable to account for the Paleozoic prevalence of bottom‐water anoxia. Overall, these model simulations suggest that the changing spatial distribution of photosynthesis and respiration in the oceans has exerted a first‐order control on Earth system evolution across Phanerozoic time.     

Human-induced salinity changes impact marine organisms and ecosystems

Climate change is fundamentally altering marine and coastal ecosystems on a global scale. While the effects of ocean warming and acidification on ecology and ecosystem functions and services are being comprehensively researched, less attention is directed toward understanding the impacts of human-driven ocean salinity changes. The global water cycle operates through water fluxes expressed as precipitation, evaporation, and freshwater runoff from land. Changes to these in turn modulate ocean salinity and shape the marine and coastal environment by affecting ocean currents, stratification, oxygen saturation, and sea level rise. Besides the direct impact on ocean physical processes, salinity changes impact ocean biological functions with the ecophysiological consequences are being poorly understood. This is surprising as salinity changes may impact diversity, ecosystem and habitat structure loss, and community shifts including trophic cascades. Climate model future projections (of end of the century salinity changes) indicate magnitudes that lead to modification of open ocean plankton community structure and habitat suitability of coral reef communities. Such salinity changes are also capable of affecting the diversity and metabolic capacity of coastal microorganisms and impairing the photosynthetic capacity of (coastal and open ocean) phytoplankton, macroalgae, and seagrass, with downstream ramifications on global biogeochemical cycling. The scarcity of comprehensive salinity data in dynamic coastal regions warrants additional attention. Such datasets are crucial to quantify salinity-based ecosystem function relationships and project such changes that ultimately link into carbon sequestration and freshwater as well as food availability to human populations around the globe. It is critical to integrate vigorous high-quality salinity data with interacting key environmental parameters (e.g., temperature, nutrients, oxygen) for a comprehensive understanding of anthropogenically induced marine changes and its impact on human health and the global economy.     

Estuary–ocean connectivity: fast physics,slow biology

Estuaries are connected to both land and ocean so their physical, chemical, and biological dynamics are influenced by climate patterns over watersheds and ocean basins. We explored climate‐driven oceanic variability as a source of estuarine variability by comparing monthly time series of temperature and chlorophyll‐a inside San Francisco Bay with those in adjacent shelf waters of the California Current System (CCS) that are strongly responsive to wind‐driven upwelling. Monthly temperature fluctuations inside and outside the Bay were synchronous, but their correlations weakened with distance from the ocean. These results illustrate how variability of coastal water temperature (and associated properties such as nitrate and oxygen) propagates into estuaries through fast water exchanges that dissipate along the estuary. Unexpectedly, there was no correlation between monthly chlorophyll‐a variability inside and outside the Bay. However, at the annual scale Bay chlorophyll‐a was significantly correlated with the Spring Transition Index (STI) that sets biological production supporting fish recruitment in the CCS. Wind forcing of the CCS shifted in the late 1990s when the STI advanced 40 days. This shift was followed, with lags of 1–3 years, by 3‐ to 19‐fold increased abundances of five ocean‐produced demersal fish and crustaceans and 2.5‐fold increase of summer chlorophyll‐a in the Bay. These changes reflect a slow biological process of estuary–ocean connectivity operating through the immigration of fish and crustaceans that prey on bivalves, reduce their grazing pressure, and allow phytoplankton biomass to build. We identified clear signals of climate‐mediated oceanic variability in this estuary and discovered that the response patterns vary with the process of connectivity and the timescale of ocean variability. This result has important implications for managing nutrient inputs to estuaries connected to upwelling systems, and for assessing their responses to changing patterns of upwelling timing and intensity as the planet continues to warm.     

Microbial ecology of expanding oxygen minimum zones

Dissolved oxygen concentration is a crucial organizing principle in marine ecosystems. As oxygen levels decline, energy is increasingly diverted away from higher trophic levels into microbial metabolism, leading to loss of fixed nitrogen and to production of greenhouse gases, including nitrous oxide and methane. In this Review, we describe current efforts to explore the fundamental factors that control the ecological and microbial biodiversity in oxygen-starved regions of the ocean, termed oxygen minimum zones. We also discuss how recent advances in microbial ecology have provided information about the potential interactions in distributed co-occurrence and metabolic networks in oxygen minimum zones, and we provide new insights into coupled biogeochemical processes in the ocean.     

Oxygen: a fundamental property regulating pelagic ecosystem structure in the coastal southeastern tropical Pacific

Background

In the southeastern tropical Pacific anchovy (Engraulis ringens) and sardine (Sardinops sagax) abundance have recently fluctuated on multidecadal scales and food and temperature have been proposed as the key parameters explaining these changes. However, ecological and paleoecological studies, and the fact that anchovies and sardines are favored differently in other regions, raise questions about the role of temperature. Here we investigate the role of oxygen in structuring fish populations in the Peruvian upwelling ecosystem that has evolved over anoxic conditions and is one of the world''s most productive ecosystems in terms of forage fish. This study is particularly relevant given that the distribution of oxygen in the ocean is changing with uncertain consequences.

Methodology/Principal Findings

A comprehensive data set is used to show how oxygen concentration and oxycline depth affect the abundance and distribution of pelagic fish. We show that the effects of oxygen on anchovy and sardine are opposite. Anchovy flourishes under relatively low oxygen conditions while sardine avoid periods/areas with low oxygen concentration and restricted habitat. Oxygen consumption, trophic structure and habitat compression play a fundamental role in fish dynamics in this important ecosystem.

Conclusions/Significance

For the ocean off Peru we suggest that a key process, the need to breathe, has been neglected previously. Inclusion of this missing piece allows the development of a comprehensive conceptual model of pelagic fish populations and change in an ocean ecosystem impacted by low oxygen. Should current trends in oxygen in the ocean continue similar effects may be evident in other coastal upwelling ecosystems.     

Biotic and Human Vulnerability to Projected Changes in Ocean Biogeochemistry over the 21st Century

Ongoing greenhouse gas emissions can modify climate processes and induce shifts in ocean temperature, pH, oxygen concentration, and productivity, which in turn could alter biological and social systems. Here, we provide a synoptic global assessment of the simultaneous changes in future ocean biogeochemical variables over marine biota and their broader implications for people. We analyzed modern Earth System Models forced by greenhouse gas concentration pathways until 2100 and showed that the entire world''s ocean surface will be simultaneously impacted by varying intensities of ocean warming, acidification, oxygen depletion, or shortfalls in productivity. In contrast, only a small fraction of the world''s ocean surface, mostly in polar regions, will experience increased oxygenation and productivity, while almost nowhere will there be ocean cooling or pH elevation. We compiled the global distribution of 32 marine habitats and biodiversity hotspots and found that they would all experience simultaneous exposure to changes in multiple biogeochemical variables. This superposition highlights the high risk for synergistic ecosystem responses, the suite of physiological adaptations needed to cope with future climate change, and the potential for reorganization of global biodiversity patterns. If co-occurring biogeochemical changes influence the delivery of ocean goods and services, then they could also have a considerable effect on human welfare. Approximately 470 to 870 million of the poorest people in the world rely heavily on the ocean for food, jobs, and revenues and live in countries that will be most affected by simultaneous changes in ocean biogeochemistry. These results highlight the high risk of degradation of marine ecosystems and associated human hardship expected in a future following current trends in anthropogenic greenhouse gas emissions.     

The impact of marine nutrient abundance on early eukaryotic ecosystems

The rise of eukaryotes to ecological prominence represents one of the most dramatic shifts in the history of Earth's biosphere. However, there is an enigmatic temporal lag between the emergence of eukaryotic organisms in the fossil record and their much later ecological expansion. In parallel, there is evidence for a secular increase in the availability of the key macronutrient phosphorus (P) in Earth's oceans. Here, we use an Earth system model equipped with a size‐structured marine ecosystem to explore relationships between plankton size, trophic complexity, and the availability of marine nutrients. We find a strong dependence of planktonic ecosystem structure on ocean nutrient abundance, with a larger ocean nutrient inventory leading to greater overall biomass, broader size spectra, and increasing abundance of large Zooplankton. If existing estimates of Proterozoic marine nutrient levels are correct, our results suggest that increases in the ecological impact of eukaryotic algae and trophic complexity in eukaryotic ecosystems were directly linked to restructuring of the global P cycle associated with the protracted rise of surface oxygen levels. Our results thus suggest an indirect but potentially important mechanism by which ocean oxygenation may have acted to shape marine ecological function during late Proterozoic time.     

Dry season distribution of land crabs, Gecarcinus quadratus (Crustacea: Gecarcinidae), in Corcovado National Park, Costa Rica

The land crab Gecarcinus quadratus is an engineering species that controls nutrient cycling in tropical forests. Factors regulating their coastal distribution are not fully understood. We quantified land crab distribution during the dry season at Sirena Field Station in Corcovado National Park, Costa Rica, and found that land crab burrow density decreases with increasing distance from the ocean. Leaf litter depth and tree seedling density are negatively correlated with land crab burrow density. Burrows are strongly associated with sand substrate and burrow density is comparatively low in clay substrate. Results suggest that G. quadratus is limited to a narrow coastal zone with sand substrate, and this distribution could have profound effects on plant community structure.     

Observing climate change trends in ocean biogeochemistry: when and where

Understanding the influence of anthropogenic forcing on the marine biosphere is a high priority. Climate change‐driven trends need to be accurately assessed and detected in a timely manner. As part of the effort towards detection of long‐term trends, a network of ocean observatories and time series stations provide high quality data for a number of key parameters, such as pH, oxygen concentration or primary production (PP). Here, we use an ensemble of global coupled climate models to assess the temporal and spatial scales over which observations of eight biogeochemically relevant variables must be made to robustly detect a long‐term trend. We find that, as a global average, continuous time series are required for between 14 (pH) and 32 (PP) years to distinguish a climate change trend from natural variability. Regional differences are extensive, with low latitudes and the Arctic generally needing shorter time series (<~30 years) to detect trends than other areas. In addition, we quantify the ‘footprint’ of existing and planned time series stations, that is the area over which a station is representative of a broader region. Footprints are generally largest for pH and sea surface temperature, but nevertheless the existing network of observatories only represents 9–15% of the global ocean surface. Our results present a quantitative framework for assessing the adequacy of current and future ocean observing networks for detection and monitoring of climate change‐driven responses in the marine ecosystem.     

Fluctuating deposition of ocean water drives plant function on coastal sand dunes

Sea‐level rise will alter the hydrology of terrestrial coastal ecosystems. As such, it becomes increasingly important to decipher the present role of ocean water in coastal ecosystems in order to assess the coming effects of sea‐level rise scenarios. Sand dunes occur at the interface of land and sea. Traditionally, they are conceived as freshwater environments with rain and ground water as the only water sources available to vegetation. This study investigates the possibility of ocean water influx to dune soils and its effect on the physiology of sand dune vegetation. Stable isotopes are used to trace the path of ocean water from the soil to the vegetation. Soil salinity, water content and δ¹⁸O values are measured concurrently with stem water and leaf tissue of eight species during the wet and dry season and from areas proximal and distal to the ocean. Our results indicate the dune ecosystem is a mixed freshwater and marine water system characterized by oceanic influence on dune hydrology that is spatially heterogeneous and fluctuates temporally. Ocean water influx to soil occurs via salt spray in areas 5–12 m from the ocean during dry season. Accordingly, vegetation nearest to the sea demonstrate a plastic response to ocean water deposition including elevated integrated water use efficiency (δ¹³C_leaf) and uptake of ocean water that comprised up to 52% of xylem water. We suggest physiological plasticity in response to periodic ocean water influx may be a functional characteristic common to species on the leading edge of diverse coastal habitats and an important feature that should be included in modeling coastal ecosystems. Rising sea level would likely cause a repercussive landward shift of dune species in response to encroaching maritime influences. However, human development would restrict this process, potentially causing the demise of dune systems and the protection from land erosion they provide.     

Biomineralization by photosynthetic organisms: Evidence of coevolution of the organisms and their environment?

Biomineralization is widespread among photosynthetic organisms in the ocean, in inland waters and on land. The most quantitatively important biogeochemical role of land plants today in biomineralization is silica deposition in vascular plants, especially grasses. Terrestrial plants also increase the rate of weathering, providing the soluble substrates for biomineralization on land and in water bodies, a role that has had global biogeochemical impacts since the Devonian. The dominant photosynthetic biomineralizers in today's ocean are diatoms and radiolarians depositing silica and coccolithophores and foraminifera depositing calcium carbonate. Abiotic precipitation of silica from supersaturated seawater in the Precambrian preceded intracellular silicification dominated by sponges, then radiolarians and finally diatoms, with successive declines in the silicic acid concentration in the surface ocean, resulting in some decreases in the extent of silicification and, probably, increases in the silicic acid affinity of the active influx mechanisms. Calcium and bicarbonate concentrations in the surface ocean have generally been supersaturating with respect to the three common calcium carbonate biominerals through geological time, allowing external calcification as well as calcification in compartments within cells or organisms. The forms of calcium carbonate in biominerals, and presumably the evolution of the organisms that produce them, have been influenced by abiotic variations in calcium and magnesium concentrations in seawater, and calcium carbonate deposition has probably also been influenced by carbon dioxide concentration whose variations are in part biologically determined. Overall, there has been less biological feedback on the availability of substrates for calcification than is the case for silicification.     

Monitoring austral and cyclonic swells in the “Iles Eparses” (Mozambique channel) from microseismic noise

We deployed five broadband three-components seismic stations in the Iles Eparses in the south-west Indian Ocean and on Mayotte Island, between April 2011 and January 2014. These small and remote oceanic islands suffer the effects of strong ocean swells that affect their coastal environments but most islands are not instrumented by wave gauges to characterize the swells. However, wave action on the coast causes high levels of ground vibrations in the solid earth, so-called microseismic noise. We use this link between the solid earth and ocean wave activity to quantify the swells locally. Spectral analyses of the continuous seismic data show clear peaks in the 0.05–0.10 Hz frequency band (periods between 10 and 20 s), corresponding to the ocean wave periods of the local swells. We analyze an example of austral swell occurring in August 2013 and a cyclonic event (Felleng) that developed in January 2013, and quantify the ground motion at each station induced by these events. In both cases, we find a linear polarization in the horizontal plane with microseismic amplitude directly correlated to the swell height (as predicted by the global swell model WaveWatchIII), and a direction of polarization close to the predicted swell propagation direction. Although this analysis has not been performed in real time, it demonstrates that terrestrial seismic stations can be efficiently used as wave gauges, and are particularly well suited for quantifying extreme swell events. This approach may therefore provide useful and cheaper alternatives to wave buoys for monitoring swells and the related environmental processes such as beach erosion or coral reef damages.     

基于TM的渤海海岸带1988～2000年生态环境变化

海岸带作为海陆之间的过渡地带,是全球生态环境最为复杂和特殊之处。研究海岸带土地利用变化对于了解该区域生态环境演变具有重要意义。利用1988和2000年的Landsat-TM数据,在GIS技术支持下,通过一系列空间分析,得到渤海海岸带土地利用/土地覆盖变化,结合社会经济统计资料分析该区域生态环境的动态变化情况及其驱动因素。结果表明,1988~2000年,由于渤海海岸带社会经济的快速发展,海岸带土地利用格局发生了巨大的变化。耕地大面积减少,城乡工矿用地、养殖池塘、盐田急剧扩张;林地、湿地等具有重要生态价值的土地类型面积显著下降。表明强烈的人类活动已经使自然生态系统受到破坏,渤海海岸带生态环境质量总体上呈现下降趋势。     

Revisiting coral reef connectivity

A large river plume generated by anomalous precipitation and oceanic circulation associated with Hurricane Mitch was detected off Honduras in October 1998 using SeaWiFS ocean color images. This event provides the background for analyzing connectivity between coral reefs and land in the Meso-American reef system. We discuss the potential implications of such short-term events for disease propagation and nutrification, and their potential significance in evolutionary processes.     

Future fire emissions associated with projected land use change in Sumatra

Indonesia has experienced rapid land use change over the last few decades as forests and peatswamps have been cleared for more intensively managed land uses, including oil palm and timber plantations. Fires are the predominant method of clearing and managing land for more intensive uses, and the related emissions affect public health by contributing to regional particulate matter and ozone concentrations and adding to global atmospheric carbon dioxide concentrations. Here, we examine emissions from fires associated with land use clearing and land management on the Indonesian island of Sumatra and the sensitivity of this fire activity to interannual meteorological variability. We find ~80% of 2005–2009 Sumatra emissions are associated with degradation or land use maintenance instead of immediate land use conversion, especially in dry years. We estimate Sumatra fire emissions from land use change and maintenance for the next two decades with five scenarios of land use change, the Global Fire Emissions Database Version 3, detailed 1‐km² land use change maps, and MODIS fire radiative power observations. Despite comprising only 16% of the original study area, we predict that 37–48% of future Sumatra emissions from land use change will occur in fuel‐rich peatswamps unless this land cover type is protected effectively. This result means that the impact of fires on future air quality and climate in Equatorial Asia will be decided in part by the conservation status given to the remaining peatswamps on Sumatra. Results from this article will be implemented in an atmospheric transport model to quantify the public health impacts from the transport of fire emissions associated with future land use scenarios in Sumatra.     

Reed frog diversification in the Gulf of Guinea: Overseas dispersal,the progression rule,and in situ speciation

Oceanic islands accumulate endemic species when new colonists diverge from source populations or by in situ diversification of resident island endemics. The relative importance of dispersal versus in situ speciation in generating diversity on islands varies with a number of archipelago characteristics including island size, age, and remoteness. Here, we characterize interisland dispersal and in situ speciation in frogs endemic to the Gulf of Guinea islands. Using mitochondrial sequence and genome‐wide single‐nucleotide polymorphism data, we demonstrate that dispersal proceeded from the younger island (São Tomé) to the older island (Príncipe) indicating that for organisms that disperse overseas on rafts, dispersal between islands may be determined by ocean currents and not island age. We find that dispersal between the islands is not ongoing, resulting in genotypically distinct but phenotypically similar lineages on the two islands. Finally, we demonstrate that in situ diversification on São Tomé Island likely proceeded in allopatry due to the geographic separation of breeding sites, resulting in phenotypically distinct species. We find evidence of hybridization between the species where their ranges are sympatric and the hybrid zone coincides with a transition from agricultural land to primary forest, indicating that anthropogenic development may have facilitated secondary contact between previously allopatric species.