Dimitri Gutiérrez

Revising the nitrogen cycle in the Peruvian oxygen minimum zone

The oxygen minimum zone (OMZ) of the Eastern Tropical South Pacific (ETSP) is 1 of the 3 major regions in the world where oceanic nitrogen is lost in the pelagic realm. The recent identification of anammox, instead of denitrification, as the likely prevalent pathway for nitrogen loss in this OMZ raises strong questions about our understanding of nitrogen cycling and organic matter remineralization in these waters. Without detectable denitrification, it is unclear how NH4+ is remineralized from organic matter and sustains anammox or how secondary NO2− maxima arise within the OMZ. Here we show that in the ETSP-OMZ, anammox obtains 67% or more of NO2− from nitrate reduction, and 33% or less from aerobic ammonia oxidation, based on stable-isotope pairing experiments corroborated by functional gene expression analyses. Dissimilatory nitrate reduction to ammonium was detected in an open-ocean setting. It occurred throughout the OMZ and could satisfy a substantial part of the NH4+ requirement for anammox. The remaining NH4+ came from remineralization via nitrate reduction and probably from microaerobic respiration. Altogether, deep-sea NO3− accounted for only ≈50% of the nitrogen loss in the ETSP, rather than 100% as commonly assumed. Because oceanic OMZs seem to be expanding because of global climate change, it is increasingly imperative to incorporate the correct nitrogen-loss pathways in global biogeochemical models to predict more accurately how the nitrogen cycle in our future ocean may respond.

Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997-98 El Nino

Oxygen minimum zones (OMZs) are widespread features in the most productive regions of the world ocean. A holistic view of benthic responses to OMZ conditions will improve our ability to predict ecosystem-level consequences of climatic trends that influence oxygen availability, such as global warming or ENSO-related events. Four stations off Callao, Peru (~12°S, Station A, 305 m; Station B, 562 m; Station C, 830 m and Station D, 1210 m) were sampled to examine the influence of the low bottom-water oxygen concentration and high organic-matter availability within the OMZ (O2 < 0.5 ml L−1) on sediments, benthic communities, and bioturbation. Sampling took place during early January 1998, an intense El Nino period associated with higher-than-normal levels of O2 on the shelf and upper slope. Peru slope sediments were highly heterogeneous. Sediment total organic carbon content exceeded 16%, lamination was present below 6 cm depth, and filamentous sulfur bacteria (Thioploca spp.) were present at Station A, (305 m, O2 < 0.02 ml L–1). Deeper sites contained phosphorite crusts or pellets and exhibited greater bottom-water oxygenation and lower content and quality of organic matter. X-radiographs and 210Pb and 234Th profiles suggested the dominance of lateral transport and bioturbation over pelagic sedimentation at the mid- and lower slope sites. Macrofauna, metazoan meiofauna and foraminifera exhibited coherence of density patterns across stations, with maximal densities (and for macrofauna, reduced diversity) at Station A, where bottom-water oxygen concentration was lowest and sediment labile organic matter content (LOC: sum of protein, carbohydrate and lipid carbon) was greatest. Metazoan and protozoan meiofaunal densities were positively correlated with sediment LOC. The taxa most tolerant of nearly anoxic, organic-rich conditions within the Peru OMZ were calcareous foraminifera, nematodes and gutless phallodrilinid (symbiont-bearing) oligochaetes. Agglutinated foraminifera, harpacticoid copepods, polychaetes and many other macrofaunal taxa increased in relative abundance below the OMZ. During the study (midpoint of the 1997–98 El Nino), the upper OMZ boundary exhibited a significant deepening (to 190 m) relative to ‘normal’, non-El Nino conditions (< 100 m), possibly causing a mild, transient oxygenation over the upper slope (200–300 m) and reduction of the organic particle flux to the seabed. Future sampling may determine whether the Peru margin system exhibits dynamic responses to changing ENSO-related conditions.

Meiofauna and sedimentary organic matter off Central Chile: response to changes caused by the 1997–1998 El Niño

Quantitative surveys of metazoan meiofauna were carried out in an upwelling region off Central Chile (36oS). During May 1997 and May 1998, coinciding with the onset and end of El Nino, five benthic stations (respectively 27, 34, 64, 88, and 120 m depth), from the middle of Concepcion Bay to the edge of the adjacent continental shelf, were sampled. The sedimentary organic matter biopolymeric fraction (proteins, carbohydrates and lipids) and chloroplastic pigments were also assessed. Total meiofauna abundance and biomass increased significantly between sampling dates at the mid-bay and inner shelf sites, from 1474 ± 354 to 5035 ± 291 individuals 10 cm–2 and from 2618 ± 332 to 5241 ± 903 individuals 10 cm–2, respectively. The relative importance of copepods in the top 2 cm increased at all sites (except in the bay mouth). During May 1998, meiofauna, especially nematodes, penetrated deeper in the bay, as well as in the inner and middle shelf sediments. Changes observed in meiobenthos structure among sites and periods were attributed to the higher oxygenation of bottom waters during the summer of 1998 (i.e. El Nino conditions). This was most evident at sites such as the mid bay, where during non-El Nino years, oxygen-deficient conditions prevail. A decrease of organic matter quantity and quality, related to low primary productivity conditions in 1998 (El Nino), apparently caused few changes in meiofauna structure. A positive correlation between Thioploca and the meiofauna biomass was observed in May 1997, whereas in May 1998 no relationship was found.

Declining oxygen in the global ocean and coastal waters

Beneath the waves, oxygen disappears As plastic waste pollutes the oceans and fish stocks decline, unseen below the surface another problem grows: deoxygenation. Breitburg et al. review the evidence for the downward trajectory of oxygen levels in increasing areas of the open ocean and coastal waters. Rising nutrient loads coupled with climate change—each resulting from human activities—are changing ocean biogeochemistry and increasing oxygen consumption. This results in destabilization of sediments and fundamental shifts in the availability of key nutrients. In the short term, some compensatory effects may result in improvements in local fisheries, such as in cases where stocks are squeezed between the surface and elevated oxygen minimum zones. In the longer term, these conditions are unsustainable and may result in ecosystem collapses, which ultimately will cause societal and economic harm. Science, this issue p. eaam7240 BACKGROUND Oxygen concentrations in both the open ocean and coastal waters have been declining since at least the middle of the 20th century. This oxygen loss, or deoxygenation, is one of the most important changes occurring in an ocean increasingly modified by human activities that have raised temperatures, CO2 levels, and nutrient inputs and have altered the abundances and distributions of marine species. Oxygen is fundamental to biological and biogeochemical processes in the ocean. Its decline can cause major changes in ocean productivity, biodiversity, and biogeochemical cycles. Analyses of direct measurements at sites around the world indicate that oxygen-minimum zones in the open ocean have expanded by several million square kilometers and that hundreds of coastal sites now have oxygen concentrations low enough to limit the distribution and abundance of animal populations and alter the cycling of important nutrients. ADVANCES In the open ocean, global warming, which is primarily caused by increased greenhouse gas emissions, is considered the primary cause of ongoing deoxygenation. Numerical models project further oxygen declines during the 21st century, even with ambitious emission reductions. Rising global temperatures decrease oxygen solubility in water, increase the rate of oxygen consumption via respiration, and are predicted to reduce the introduction of oxygen from the atmosphere and surface waters into the ocean interior by increasing stratification and weakening ocean overturning circulation. In estuaries and other coastal systems strongly influenced by their watershed, oxygen declines have been caused by increased loadings of nutrients (nitrogen and phosphorus) and organic matter, primarily from agriculture; sewage; and the combustion of fossil fuels. In many regions, further increases in nitrogen discharges to coastal waters are projected as human populations and agricultural production rise. Climate change exacerbates oxygen decline in coastal systems through similar mechanisms as those in the open ocean, as well as by increasing nutrient delivery from watersheds that will experience increased precipitation. Expansion of low-oxygen zones can increase production of N2O, a potent greenhouse gas; reduce eukaryote biodiversity; alter the structure of food webs; and negatively affect food security and livelihoods. Both acidification and increasing temperature are mechanistically linked with the process of deoxygenation and combine with low-oxygen conditions to affect biogeochemical, physiological, and ecological processes. However, an important paradox to consider in predicting large-scale effects of future deoxygenation is that high levels of productivity in nutrient-enriched coastal systems and upwelling areas associated with oxygen-minimum zones also support some of the world’s most prolific fisheries. OUTLOOK Major advances have been made toward understanding patterns, drivers, and consequences of ocean deoxygenation, but there is a need to improve predictions at large spatial and temporal scales important to ecosystem services provided by the ocean. Improved numerical models of oceanographic processes that control oxygen depletion and the large-scale influence of altered biogeochemical cycles are needed to better predict the magnitude and spatial patterns of deoxygenation in the open ocean, as well as feedbacks to climate. Developing and verifying the next generation of these models will require increased in situ observations and improved mechanistic understanding on a variety of scales. Models useful for managing nutrient loads can simulate oxygen loss in coastal waters with some skill, but their ability to project future oxygen loss is often hampered by insufficient data and climate model projections on drivers at appropriate temporal and spatial scales. Predicting deoxygenation-induced changes in ecosystem services and human welfare requires scaling effects that are measured on individual organisms to populations, food webs, and fisheries stocks; considering combined effects of deoxygenation and other ocean stressors; and placing an increased research emphasis on developing nations. Reducing the impacts of other stressors may provide some protection to species negatively affected by low-oxygen conditions. Ultimately, though, limiting deoxygenation and its negative effects will necessitate a substantial global decrease in greenhouse gas emissions, as well as reductions in nutrient discharges to coastal waters. Low and declining oxygen levels in the open ocean and coastal waters affect processes ranging from biogeochemistry to food security. The global map indicates coastal sites where anthropogenic nutrients have exacerbated or caused O2 declines to <2 mg liter−1 (<63 μmol liter−1) (red dots), as well as ocean oxygen-minimum zones at 300 m of depth (blue shaded regions). [Map created from data provided by R. Diaz, updated by members of the GO2NE network, and downloaded from the World Ocean Atlas 2009]. Oxygen is fundamental to life. Not only is it essential for the survival of individual animals, but it regulates global cycles of major nutrients and carbon. The oxygen content of the open ocean and coastal waters has been declining for at least the past half-century, largely because of human activities that have increased global temperatures and nutrients discharged to coastal waters. These changes have accelerated consumption of oxygen by microbial respiration, reduced solubility of oxygen in water, and reduced the rate of oxygen resupply from the atmosphere to the ocean interior, with a wide range of biological and ecological consequences. Further research is needed to understand and predict long-term, global- and regional-scale oxygen changes and their effects on marine and estuarine fisheries and ecosystems.

Bioturbation by symbiont-bearing annelids in near-anoxic sediments: Implications for biofacies models and paleo-oxygen assessments

Anoxic or nearly anoxic conditions (<4 μM O2) have long been associated with the absence of bioturbation and animal traces. This premise has guided interpretation of paleoceanographic conditions from rocks and sediments. We recently observed a high-density, living assemblage of highly mobile, symbiont-bearing, burrowing, phallodrilinid oligochaetes within a nearly anoxic basin (<1 μM O2 [0.02–0.03 ml l−1]) on the Peru margin (305 m). These observations were made during the most intense part of the 1997–98 El Nino when there may have been slight oxygenation of an otherwise anoxic basin, but oligochaete presence prior to this event is likely. The occurrence of symbiont-bearing gutless oligochaetes mainly within the upper 5 cm of the sediment column coincided with a bioturbated zone overlying distinctly laminated sediments. Our observations redefine the lower oxygen limit of macrofaunal bioturbation to ≪2 μM, and indicate a need to modify currently accepted ideas about the relationship between bioturbation and paleo-oxygen concentration. These results also address an ongoing debate about the lifestyles of bioturbating organisms in oxygen-poor settings.

Climate Change and Small Pelagic Fish: Variability from scales in marine sediments and other historical records

1 TOCA Summary 00 2 TOCA Introduction 00 3 TOCA Historical observations 00 4 TOCA Archaeological records 00 5 TOCA Sedimentary records 00 6 TOCB Oceanographic settings for sedimentary records 00 7 TOCB Chronostratigraphies and fish Scale Deposition 8 Rates (SDRs) 00

Evaluating fish scale preservation in sediment records from the oxygen minimum zone off Peru

Abstract Fish scales accumulating in marine laminated sediments can provide a record of population variability of small pelagic fishes. Although some studies have noted signs of scale degradation that could affect estimates of population variability, there are presently no well-developed means to evaluate degradation. We developed several indices as indicators of fish scale preservation in two box-cores that we collected off Pisco (14°S), one at 301 m near the center of the oxygen minimum zone (OMZ), and the other at 201 m near the upper limit of the OMZ. These indices include (1) an index of fish scale integrity (estimate of scale wholeness relative to fragmentation), (2) the fungi-free area of fish scales and vertebrae, (3) the ratio of fish scales to vertebrae (as well as fish scales to vertebrae and bones), and (4) the ratio of whole scales to fragments. We address whether lower numbers of anchovy scales occurring in association with reduced total organic carbon fluxes and higher bottom-water oxygen concentrations are due entirely to lower abundances of anchovy or whether differential preservation of the fish scales in the sediments plays an important role in reduced scale abundances. Comparison of temporal sequences between the two cores provides the means to assess whether there are differences in the preservation of fish scales. The combined indices indicate that the lower numbers of fish scales in the earliest period have been affected by degradation, and to a greater degree in the box-core from 201 meters, which can be subject to higher oxygen concentrations. On the other hand, decadal-scale variations in fish scale abundance within the period of better preservation are unlikely to be caused by degradation. We discuss the utility and drawbacks of different indices of preservation for reconstructing past changes in fish population sizes with fluxes of fish debris and also briefly discuss the utility of these indices to other paleobiological systems.

Benthic Foraminiferal Communities and Microhabitat Selection on the Continental Shelf Off Central Peru

The ecology of the benthic foraminiferal community (62–150 and >150 μm) was studied in the continental shelf off Callao (12oS) during April 2009. Five sediment stations were sampled along a cross-shelf transect. All the sites were subjected to dysoxic conditions in the bottom water, but differed in its sedimentary biogeochemical conditions. The inner-shelf, characterized by high contents of labile organic matter in the sediment surface and sulfidic conditions in the pore water, presented a community dominated by Bolivina costata, followed by Virgulinella fragilis, a spherical allogromiid morphotype, and Nonionella auris. The outer-shelf, more permanently subjected to the oxygen minimum zone, and characterized by sedimentary suboxic conditions and lower contents of labile organic matter, was inhabited by a community dominated by Bolivina humilis and Buliminella tenuata. Vertical distributions of V. fragilis, N. auris, and the spherical allogromiid morphotype likely reflect physiological and symbiotic adaptations to anoxia. We conclude that under this oxygen-deficient setting, the labile organic matter content and the sedimentary redox conditions govern the community parameters.

Density dependence, prey accessibility and prey depletion by fisheries drive Peruvian seabird population dynamics

In marine ecosystems top predator populations are shaped by environmental factors affecting their prey abundance. Coupling top predators’ population studies with independent records of prey abundance suggests that prey fluctuations affect fecundity parameters and abundance of their predators. However, prey may be abundant but inaccessible to their predators and a major challenge is to determine the relative importance of prey accessibility in shaping seabird populations. In addition, disentangling the effects of prey abundance and accessibility from the effects of prey removal by fisheries, while accounting for density dependence, remains challenging for marine top predators. Here, we investigate how climate, population density, and the accessibility and removal of prey (the Peruvian anchovy Engraulis ringens) by fisheries influence the population dynamics of the largest sedentary seabird community (≈ 4 million individuals belonging to guanay cormorant Phalacrocorax bougainvillii, Peruvian booby Sula variegata and Peruvian pelican Pelecanus thagus) of the northern Humboldt Current System over the past half-century. Using Gompertz state–space models we found strong evidence for density dependence in abundance for the three seabird species. After accounting for density dependence, sea surface temperature, prey accessibility (defined by the depth of the upper limit of the subsurface oxygen minimum zone) and prey removal by fisheries were retained as the best predictors of annual population size across species. These factors affected seabird abundance the current year and with year lags, suggesting effects on several demographic parameters including breeding propensity and adult survival. These findings highlight the effects of prey accessibility and fishery removals on seabird populations in marine ecosystems. This will help refine management objectives of marine ecosystems in order to ensure sufficient biomass of forage fish to avoid constraining seabird population dynamics, while taking into account of the effects of environmental variability.

Hydrological controls on the biogeochemical dynamics in a Peruvian mangrove forest

A tropical mangrove forest in Northern Peru was studied to determine if physical and biogeochemical characteristics of creek water and subtidal sediments are related to the seasonal hydrological regimes. The results showed that during the dry season, there were greater reducing conditions (Eh) and greater fine particle content (silt and clay) in the subtidal sediments. In contrast, the wet season showed greater dissolved oxygen concentrations in creek water as well as lower total organic matter and chlorophyll-a contents in the subtidal sediments. Carbohydrate and protein concentrations indicated remobilization and degradation of sedimentary organic matter, which were higher during the dry season than in the wet season. The results presented here indicate that changes in the hydrological regime affect the biogeochemical dynamics of mangroves, modulating the sediment redistribution as well as the organic matter deposition and degradation. This research provides insight to the biogeochemical dynamics in Peruvian mangrove sediments which are sensitive to extreme El Niño-Southern Oscillation events and the potential effects of climate change.