Biodiversity's Big Wet Secret: The Global Distribution of Marine Biological Records Reveals Chronic Under-Exploration of the Deep Pelagic Ocean

Background

Understanding the distribution of marine biodiversity is a crucial first step towards the effective and sustainable management of marine ecosystems. Recent efforts to collate location records from marine surveys enable us to assemble a global picture of recorded marine biodiversity. They also effectively highlight gaps in our knowledge of particular marine regions. In particular, the deep pelagic ocean – the largest biome on Earth – is chronically under-represented in global databases of marine biodiversity.

Methodology/Principal Findings

We use data from the Ocean Biogeographic Information System to plot the position in the water column of ca 7 million records of marine species occurrences. Records from relatively shallow waters dominate this global picture of recorded marine biodiversity. In addition, standardising the number of records from regions of the ocean differing in depth reveals that regardless of ocean depth, most records come either from surface waters or the sea bed. Midwater biodiversity is drastically under-represented.

Conclusions/Significance

The deep pelagic ocean is the largest habitat by volume on Earth, yet it remains biodiversity''s big wet secret, as it is hugely under-represented in global databases of marine biological records. Given both its value in the provision of a range of ecosystem services, and its vulnerability to threats including overfishing and climate change, there is a pressing need to increase our knowledge of Earth''s largest ecosystem.     

Acoustic Observation of Living Organisms Reveals the Upper Limit of the Oxygen Minimum Zone

Background

Oxygen minimum zones (OMZs) are expanding in the World Ocean as a result of climate change and direct anthropogenic influence. OMZ expansion greatly affects biogeochemical processes and marine life, especially by constraining the vertical habitat of most marine organisms. Currently, monitoring the variability of the upper limit of the OMZs relies on time intensive sampling protocols, causing poor spatial resolution.

Methodology/Principal Findings

Using routine underwater acoustic observations of the vertical distribution of marine organisms, we propose a new method that allows determination of the upper limit of the OMZ with a high precision. Applied in the eastern South-Pacific, this original sampling technique provides high-resolution information on the depth of the upper OMZ allowing documentation of mesoscale and submesoscale features (e.g., eddies and filaments) that structure the upper ocean and the marine ecosystems. We also use this information to estimate the habitable volume for the world''s most exploited fish, the Peruvian anchovy (Engraulis ringens).

Conclusions/Significance

This opportunistic method could be implemented on any vessel geared with multi-frequency echosounders to perform comprehensive high-resolution monitoring of the upper limit of the OMZ. Our approach is a novel way of studying the impact of physical processes on marine life and extracting valid information about the pelagic habitat and its spatial structure, a crucial aspect of Ecosystem-based Fisheries Management in the current context of climate change.     

Shearwater Foraging in the Southern Ocean: The Roles of Prey Availability and Winds

Background

Sooty (Puffinus griseus) and short-tailed (P. tenuirostris) shearwaters are abundant seabirds that range widely across global oceans. Understanding the foraging ecology of these species in the Southern Ocean is important for monitoring and ecosystem conservation and management.

Methodology/Principal Findings

Tracking data from sooty and short-tailed shearwaters from three regions of New Zealand and Australia were combined with at-sea observations of shearwaters in the Southern Ocean, physical oceanography, near-surface copepod distributions, pelagic trawl data, and synoptic near-surface winds. Shearwaters from all three regions foraged in the Polar Front zone, and showed particular overlap in the region around 140°E. Short-tailed shearwaters from South Australia also foraged in Antarctic waters south of the Polar Front. The spatial distribution of shearwater foraging effort in the Polar Front zone was matched by patterns in large-scale upwelling, primary production, and abundances of copepods and myctophid fish. Oceanic winds were found to be broad determinants of foraging distribution, and of the flight paths taken by the birds on long foraging trips to Antarctic waters.

Conclusions/Significance

The shearwaters displayed foraging site fidelity and overlap of foraging habitat between species and populations that may enhance their utility as indicators of Southern Ocean ecosystems. The results highlight the importance of upwellings due to interactions of the Antarctic Circumpolar Current with large-scale bottom topography, and the corresponding localised increases in the productivity of the Polar Front ecosystem.     

Global patterns of bacterial beta-diversity in seafloor and seawater ecosystems

Background

Marine microbial communities have been essential contributors to global biomass, nutrient cycling, and biodiversity since the early history of Earth, but so far their community distribution patterns remain unknown in most marine ecosystems.

Methodology/Principal Findings

The synthesis of 9.6 million bacterial V6-rRNA amplicons for 509 samples that span the global ocean''s surface to the deep-sea floor shows that pelagic and benthic communities greatly differ, at all taxonomic levels, and share <10% bacterial types defined at 3% sequence similarity level. Surface and deep water, coastal and open ocean, and anoxic and oxic ecosystems host distinct communities that reflect productivity, land influences and other environmental constraints such as oxygen availability. The high variability of bacterial community composition specific to vent and coastal ecosystems reflects the heterogeneity and dynamic nature of these habitats. Both pelagic and benthic bacterial community distributions correlate with surface water productivity, reflecting the coupling between both realms by particle export. Also, differences in physical mixing may play a fundamental role in the distribution patterns of marine bacteria, as benthic communities showed a higher dissimilarity with increasing distance than pelagic communities.

Conclusions/Significance

This first synthesis of global bacterial distribution across different ecosystems of the World''s oceans shows remarkable horizontal and vertical large-scale patterns in bacterial communities. This opens interesting perspectives for the definition of biogeographical biomes for bacteria of ocean waters and the seabed.     

Wasp-waist interactions in the North Sea ecosystem

Background

In a “wasp-waist” ecosystem, an intermediate trophic level is expected to control the abundance of predators through a bottom-up interaction and the abundance of prey through a top-down interaction. Previous studies suggest that the North Sea is mainly governed by bottom-up interactions driven by climate perturbations. However, few studies have investigated the importance of the intermediate trophic level occupied by small pelagic fishes.

Methodology/Principal Findings

We investigated the numeric interactions among 10 species of seabirds, two species of pelagic fish and four groups of zooplankton in the North Sea using decadal-scale databases. Linear models were used to relate the time series of zooplankton and seabirds to the time series of pelagic fish. Seabirds were positively related to herring (Clupea harengus), suggesting a bottom-up interaction. Two groups of zooplankton; Calanus helgolandicus and krill were negatively related to sprat (Sprattus sprattus) and herring respectively, suggesting top-down interactions. In addition, we found positive relationships among the zooplankton groups. Para/pseudocalanus was positively related to C. helgolandicus and C. finmarchicus was positively related to krill.

Conclusion/Significance

Our results indicate that herring was important in regulating the abundance of seabirds through a bottom-up interaction and that herring and sprat were important in regulating zooplankton through top-down interactions. We suggest that the positive relationships among zooplankton groups were due to selective foraging and switching in the two clupeid fishes. Our results suggest that “wasp-waist” interactions might be more important in the North Sea than previously anticipated. Fluctuations in the populations of pelagic fish due to harvesting and depletion of their predators might accordingly have profound consequences for ecosystem dynamics through trophic cascades.     

Trophic interactions and community structure in the upwelling system off Central Chile (33-39°S)

Trophic interactions and community structure in the upwelling system off Central Chile (USCCh) (33-39°S) are analyzed using biological and ecological data concerning the main trophic groups and the Ecopath with Ecosim software version 5.0 (EwE). The model encompasses the fisheries, cetaceans, sea lion, marine birds, cephalopods, large-sized pelagic fish (sword fish), medium-sized pelagic fish (horse mackerel, hoki), small-sized pelagic fish (anchovy, common sardine), demersal fish (e.g. Chilean hake, black conger-eel), benthic invertebrates (red squat lobster, yellow squat lobster) and other groups such as zooplankton, phytoplankton and detritus. Input data was gathered from published and unpublished reports and our own estimates. Trophic interactions, system indicators and food web attributes are calculated using network analysis routines included in EwE. Results indicate that trophic groups are aligned around four trophic levels (TL) with phytoplankton and detritus at the TL=1, while large-sized pelagic fish and cetaceans are top predators (TL>4.0). The fishery is located at an intermediate to low trophic level (TL=2.97), removing about 15% of the calculated system primary production. The pelagic realm dominates the system, with medium-sized pelagic fish as the main fish component in biomass, while small-sized pelagic fish dominate total landings. Chilean hake is by far the main demersal fish component in both, biomass and yield. Predators consume the greater part of the production of the most important fishery resources, particularly juvenile stages of Chilean hake. Consequently, mortality by predation is an important component of total mortality. However, fishery also removes a large fraction of common sardine, anchovy, horse mackerel, and Chilean hake. The analysis of direct and indirect trophic impacts reveals that Chilean hake is a highly cannibalistic species. Chilean hake is also an important predator on anchovy, common sardine, benthic invertebrates, and demersal fish. The fisheries heavily impact on Chilean hake, common sardine, anchovy, and horse mackerel. Total system biomass (B=476 t km⁻² year⁻¹) and throughput (T=89454 t km⁻² year⁻¹) estimated in the USCCh model are in accordance with models of comparable systems. Considering system attributes derived from network analysis, the USCCh can be characterized as an immature system, with short trophic chains and low trophic transfer efficiency. Finally, we suggest that trophic interactions should be considered in stock assessment and management programs in USCCh. In addition, future research programs should be carried out in order to understand the ecosystem effects of fishing and trophic control in this highly productive food web.     

Fishery-Independent Data Reveal Negative Effect of Human Population Density on Caribbean Predatory Fish Communities

Background

Understanding the current status of predatory fish communities, and the effects fishing has on them, is vitally important information for management. However, data are often insufficient at region-wide scales to assess the effects of extraction in coral reef ecosystems of developing nations.

Methodology/Principal Findings

Here, I overcome this difficulty by using a publicly accessible, fisheries-independent database to provide a broad scale, comprehensive analysis of human impacts on predatory reef fish communities across the greater Caribbean region. Specifically, this study analyzed presence and diversity of predatory reef fishes over a gradient of human population density. Across the region, as human population density increases, presence of large-bodied fishes declines, and fish communities become dominated by a few smaller-bodied species.

Conclusions/Significance

Complete disappearance of several large-bodied fishes indicates ecological and local extinctions have occurred in some densely populated areas. These findings fill a fundamentally important gap in our knowledge of the ecosystem effects of artisanal fisheries in developing nations, and provide support for multiple approaches to data collection where they are commonly unavailable.     

The making of a productivity hotspot in the coastal ocean

Background

Highly productive hotspots in the ocean often occur where complex physical forcing mechanisms lead to aggregation of primary and secondary producers. Understanding how hotspots persist, however, requires combining knowledge of the spatio-temporal linkages between geomorphology, physical forcing, and biological responses with the physiological requirements and movement of top predators.

Methodology/Principal Findings

Here we integrate remotely sensed oceanography, ship surveys, and satellite telemetry to show how local geomorphology interacts with physical forcing to create a region with locally enhanced upwelling and an adjacent upwelling shadow that promotes retentive circulation, enhanced year-round primary production, and prey aggregation. These conditions provide an area within the upwelling shadow where physiologically optimal water temperatures can be found adjacent to a region of enhanced prey availability, resulting in a foraging hotspot for loggerhead sea turtles (Caretta caretta) off the Baja California peninsula, Mexico.

Significance/Conclusions

We have identified the set of conditions that lead to a persistent top predator hotspot, which increases our understanding of how highly migratory species exploit productive regions of the ocean. These results will aid in the development of spatially and environmentally explicit management strategies for marine species of conservation concern.     

Geographically widespread swordfish barcode stock identification: a case study of its application

Background

The swordfish (Xiphias gladius) is a cosmopolitan large pelagic fish inhabiting tempered and tropical waters and it is a target species for fisheries all around the world. The present study investigated the ability of COI barcoding to reliably identify swordfish and particularly specific stocks of this commercially important species.

Methodology

We applied the classical DNA barcoding technology, upon a 682 bp segment of COI, and compared swordfish sequences from different geographical sources (Atlantic, Indian Oceans and Mediterranean Sea). The sequences of the 5′ hyper-variable fragment of the control region (5′dloop), were also used to validate the efficacy of COI as a stock-specific marker.

Case Report

This information was successfully applied to the discrimination of unknown samples from the market, detecting in some cases mislabeled seafood products.

Conclusions

The NJ distance-based phenogram (K2P model) obtained with COI sequences allowed us to correlate the swordfish haplotypes to the different geographical stocks. Similar results were obtained with 5′dloop. Our preliminary data in swordfish Xiphias gladius confirm that Cytochrome Oxidase I can be proposed as an efficient species-specific marker that has also the potential to assign geographical provenance. This information might speed the samples analysis in commercial application of barcoding.     

Multifarious anchovy and sardine regimes in the Humboldt Current System during the last 150 years

The Humboldt Current System (HCS) has the highest production of forage fish in the world, although it is highly variable and the future of the primary component, anchovy, is uncertain in the context of global warming. Paradigms based on late 20th century observations suggest that large‐scale forcing controls decadal‐scale fluctuations of anchovy and sardine across different boundary currents of the Pacific. We develop records of anchovy and sardine fluctuations since 1860 AD using fish scales from multiple sites containing laminated sediments and compare them with Pacific basin‐scale and regional indices of ocean climate variability. Our records reveal two main anchovy and sardine phases with a timescale that is not consistent with previously proposed periodicities. Rather, the regime shifts in the HCS are related to 3D habitat changes driven by changes in upwelling intensity from both regional and large‐scale forcing. Moreover, we show that a long‐term increase in coastal upwelling translates via a bottom‐up mechanism to top predators suggesting that the warming climate, at least up to the start of the 21st century, was favorable for fishery productivity in the HCS.     

Oldest Evidence of Toolmaking Hominins in a Grassland-Dominated Ecosystem

Background

Major biological and cultural innovations in late Pliocene hominin evolution are frequently linked to the spread or fluctuating presence of C₄ grass in African ecosystems. Whereas the deep sea record of global climatic change provides indirect evidence for an increase in C₄ vegetation with a shift towards a cooler, drier and more variable global climatic regime beginning approximately 3 million years ago (Ma), evidence for grassland-dominated ecosystems in continental Africa and hominin activities within such ecosystems have been lacking.

Methodology/Principal Findings

We report stable isotopic analyses of pedogenic carbonates and ungulate enamel, as well as faunal data from ∼2.0 Ma archeological occurrences at Kanjera South, Kenya. These document repeated hominin activities within a grassland-dominated ecosystem.

Conclusions/Significance

These data demonstrate what hitherto had been speculated based on indirect evidence: that grassland-dominated ecosystems did in fact exist during the Plio-Pleistocene, and that early Homo was active in open settings. Comparison with other Oldowan occurrences indicates that by 2.0 Ma hominins, almost certainly of the genus Homo, used a broad spectrum of habitats in East Africa, from open grassland to riparian forest. This strongly contrasts with the habitat usage of Australopithecus, and may signal an important shift in hominin landscape usage.     

Recruitment variability in North Atlantic cod and match-mismatch dynamics

Background

Fisheries exploitation, habitat destruction, and climate are important drivers of variability in recruitment success. Understanding variability in recruitment can reveal mechanisms behind widespread decline in the abundance of key species in marine and terrestrial ecosystems. For fish populations, the match-mismatch theory hypothesizes that successful recruitment is a function of the timing and duration of larval fish abundance and prey availability. However, the underlying mechanisms of match-mismatch dynamics and the factors driving spatial differences between high and low recruitment remain poorly understood.

Methodology/Principal Findings

We used empirical observations of larval fish abundance, a mechanistic individual-based model, and a reanalysis of ocean temperature data from 1960 to 2002 to estimate the survival of larval cod (Gadus morhua). From the model, we quantified how survival rates changed during the warmest and coldest years at four important cod spawning sites in the North Atlantic. The modeled difference in survival probability was not large for any given month between cold or warm years. However, the cumulative effect of higher growth rates and survival through the entire spawning season in warm years was substantial with 308%, 385%, 154%, and 175% increases in survival for Georges Bank, Iceland, North Sea, and Lofoten cod stocks, respectively. We also found that the importance of match-mismatch dynamics generally increased with latitude.

Conclusions/Significance

Our analyses indicate that a key factor for enhancing survival is the duration of the overlap between larval and prey abundance and not the actual timing of the peak abundance. During warm years, the duration of the overlap between larval fish and their prey is prolonged due to an early onset of the spring bloom. This prolonged season enhances cumulative growth and survival, leading to a greater number of large individuals with enhanced potential for survival to recruitment.     

Real-time ichthyoplankton drift in Northeast Arctic cod and Norwegian spring-spawning herring

Background

Individual-based biophysical larval models, initialized and parameterized by observations, enable numerical investigations of various factors regulating survival of young fish until they recruit into the adult population. Exponentially decreasing numbers in Northeast Arctic cod and Norwegian Spring Spawning herring early changes emphasizes the importance of early life history, when ichthyoplankton exhibit pelagic free drift. However, while most studies are concerned with past recruitment variability it is also important to establish real-time predictions of ichthyoplankton distributions due to the increasing human activity in fish habitats and the need for distribution predictions that could potentially improve field coverage of ichthyoplankton.

Methodology/Principal Findings

A system has been developed for operational simulation of ichthyoplankton distributions. We have coupled a two-day ocean forecasts from the Norwegian Meteorological Institute with an individual-based ichthyoplankton model for Northeast Arctic cod and Norwegian Spring Spawning herring producing daily updated maps of ichthyoplankton distributions. Recent years observed spawning distribution and intensity have been used as input to the model system. The system has been running in an operational mode since 2008. Surveys are expensive and distributions of early stages are therefore only covered once or twice a year. Comparison between model and observations are therefore limited in time. However, the observed and simulated distributions of juvenile fish tend to agree well during early fall. Area-overlap between modeled and observed juveniles September 1^st range from 61 to 73%, and 61 to 71% when weighted by concentrations.

Conclusions/Significance

The model system may be used to evaluate the design of ongoing surveys, to quantify the overlap with harmful substances in the ocean after accidental spills, as well as management planning of particular risky operations at sea. The modeled distributions are already utilized during research surveys to estimate coverage success of sampled biota and immediately after spills from ships at sea.     

Deposit-Feeding Sea Cucumbers Enhance Mineralization and Nutrient Cycling in Organically-Enriched Coastal Sediments

Background

Bioturbators affect multiple biogeochemical interactions and have been suggested as suitable candidates to mitigate organic matter loading in marine sediments. However, predicting the effects of bioturbators at an ecosystem level can be difficult due to their complex positive and negative interactions with the microbial community.

Methodology/Principal Findings

We quantified the effects of deposit-feeding sea cucumbers on benthic algal biomass (microphytobenthos, MPB), bacterial abundance, and the sediment–seawater exchange of dissolved oxygen and nutrients. The sea cucumbers increased the efflux of inorganic nitrogen (ammonium, NH₄ ⁺) from organically enriched sediments, which stimulated algal productivity. Grazing by the sea cucumbers on MPB (evidenced by pheopigments), however, caused a net negative effect on primary producer biomass and total oxygen production. Further, there was an increased abundance of bacteria in sediment with sea cucumbers, suggesting facilitation. The sea cucumbers increased the ratio of oxygen consumption to production in surface sediment by shifting the microbial balance from producers to decomposers. This shift explains the increased efflux of inorganic nitrogen and concordant reduction in organic matter content in sediment with bioturbators.

Conclusions/Significance

Our study demonstrates the functional role and potential of sea cucumbers to ameliorate some of the adverse effects of organic matter enrichment in coastal ecosystems.     

Spatio-temporal history of the disjunct family Tecophilaeaceae: a tale involving the colonization of three Mediterranean-type ecosystems

Background and Aims

Tecophilaeaceae (27 species distributed in eight genera) have a disjunct distribution in California, Chile and southern and tropical mainland Africa. Moreover, although the family mainly occurs in arid ecosystems, it has colonized three Mediterranean-type ecosystems. In this study, the spatio-temporal history of the family is examined using DNA sequence data from six plastid regions.

Methods

Modern methods in divergence time estimation (BEAST), diversification (LTT and GeoSSE) and biogeography (LAGRANGE) are applied to infer the evolutionary history of Tecophilaeaceae. To take into account dating and phylogenetic uncertainty, the biogeographical inferences were run over a set of dated Bayesian trees and the analyses were constrained according to palaeogeographical evidence.

Key Results

The analyses showed that the current distribution and diversification of the family were influenced primarily by the break up of Gondwana, separating the family into two main clades, and the establishment of a Mediterranean climate in Chile, coinciding with the radiation of Conanthera. Finally, unlike many other groups, no shifts in diversification rates were observed associated with the dispersals in the Cape region of South Africa.

Conclusions

Although modest in size, Tecophilaeaceae have a complex spatio-temporal history. The family is now most diverse in arid ecosystems in southern Africa, but is expected to have originated in sub-tropical Africa. It has subsequently colonized Mediterranean-type ecosystems in both the Northern and Southern Hemispheres, but well before the onset of the Mediterranean climate in these regions. Only one lineage, genus Conanthera, has apparently diversified to any extent under the impetus of a Mediterranean climate.     

Rapid global expansion of invertebrate fisheries: trends, drivers, and ecosystem effects

Background

Worldwide, finfish fisheries are receiving increasing assessment and regulation, slowly leading to more sustainable exploitation and rebuilding. In their wake, invertebrate fisheries are rapidly expanding with little scientific scrutiny despite increasing socio-economic importance.

Methods and Findings

We provide the first global evaluation of the trends, drivers, and population and ecosystem consequences of invertebrate fisheries based on a global catch database in combination with taxa-specific reviews. We also develop new methodologies to quantify temporal and spatial trends in resource status and fishery development. Since 1950, global invertebrate catches have increased 6-fold with 1.5 times more countries fishing and double the taxa reported. By 2004, 34% of invertebrate fisheries were over-exploited, collapsed, or closed. New fisheries have developed increasingly rapidly, with a decrease of 6 years (3 years) in time to peak from the 1950s to 1990s. Moreover, some fisheries have expanded further and further away from their driving market, encompassing a global fishery by the 1990s. 71% of taxa (53% of catches) are harvested with habitat-destructive gear, and many provide important ecosystem functions including habitat, filtration, and grazing.

Conclusions

Our findings suggest that invertebrate species, which form an important component of the basis of marine food webs, are increasingly exploited with limited stock and ecosystem-impact assessments, and enhanced management attention is needed to avoid negative consequences for ocean ecosystems and human well-being.     

Pervasive growth reduction in Norway spruce forests following wind disturbance

Background

In recent decades the frequency and severity of natural disturbances by e.g., strong winds and insect outbreaks has increased considerably in many forest ecosystems around the world. Future climate change is expected to further intensify disturbance regimes, which makes addressing disturbances in ecosystem management a top priority. As a prerequisite a broader understanding of disturbance impacts and ecosystem responses is needed. With regard to the effects of strong winds – the most detrimental disturbance agent in Europe – monitoring and management has focused on structural damage, i.e., tree mortality from uprooting and stem breakage. Effects on the functioning of trees surviving the storm (e.g., their productivity and allocation) have been rarely accounted for to date.

Methodology/Principal Findings

Here we show that growth reduction was significant and pervasive in a 6.79·million hectare forest landscape in southern Sweden following the storm Gudrun (January 2005). Wind-related growth reduction in Norway spruce (Picea abies (L.) Karst.) forests surviving the storm exceeded 10% in the worst hit regions, and was closely related to maximum gust wind speed (R² = 0.849) and structural wind damage (R² = 0.782). At the landscape scale, wind-related growth reduction amounted to 3.0 million m³ in the three years following Gudrun. It thus exceeds secondary damage from bark beetles after Gudrun as well as the long-term average storm damage from uprooting and stem breakage in Sweden.

Conclusions/Significance

We conclude that the impact of strong winds on forest ecosystems is not limited to the immediately visible area of structural damage, and call for a broader consideration of disturbance effects on ecosystem structure and functioning in the context of forest management and climate change mitigation.