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Gayana (Concepción)

versión impresa ISSN 0717-652Xversión On-line ISSN 0717-6538

Gayana (Concepc.) v.70  supl.1 Concepción oct. 2006

http://dx.doi.org/10.4067/S0717-65382006000300008 

Suplemento Gayana 70: 29-36, 2006


Oxygen deficiency and benthic communities in the peruvian upper continental margin



Deficiencia de oxigeno y comunidades bentónicas en el margen continental superior de Perú

 

Dimitri Gutiérrez, Luis Quipúzcoa, Edgardo Enríquez

Oceanographic Research Directorate, Institute of the Sea of Perú (IMARPE), P.O. Box 22, Callao, Perú, dgutierrez@imarpe.gob.pe


ABSTRACT

The oxygen minimum zone (OMZ) off the Peruvian coast, though shallower and more intense than other OMZs, exhibits a spatial distribution that varies with latitude, depth and distance to the coast. The spatial variability in oxygen content imposes latitudinal and bathymetric zonations of the benthic communities. Nevertheless the spatial patterns of the benthic communities are also modulated by the bottom topography and the sedimentary environments, which in turn are controlled to a large extent by the poleward undercurrent. While the bathymetric patterns of the macro- and meiobenthos have been previously described, latitudinal changes have received less attention. We found that, in parallel with opposed latitudinal gradients of oxygen and fresh organic matter load in the sediments, there is a latitudinal sequence in the distribution of macrofaunal biomass, diversity and density, as described by the Pearson and Rosenberg model (1978) for the macrobenthic response under organic enrichment. This latitudinal pattern is complemented by the maximum development of the giant sulphur nitrate vacuolated bacteria Thioploca spp. under more extreme oxygen deficiency (but not anoxia) and organic load than the macrofauna is able to cope with. Temporal variability in the OMZ also results in significant responses of the benthic communities, but there are differences in the sign and intensity according to the sedimentary environment. In the organic-rich sediments off the central Peruvian shelf, different benthic states, involving the macrobiotic components (infauna and Thioploca) and the meiofauna, are triggered by the varying subsurface oxygen regime.

Keywords: OMZ, Peru, benthos, Thioploca, Pearson and Rosenberg model.


RESUMEN

La zona de mínimo de oxígeno (ZMO) frente a la costa peruana, si bien más somera e intensa que otras ZMOs, exhibe una distribución tridimensional que varía con la latitud, profundidad y distancia de la costa. La variación espacial del contenido de oxígeno disuelto impone una zonación batimétrica y una zonación latitudinal a las comunidades bentónicas. Sin embargo, estos patrones espaciales del bentos son también modulados por la topografía del fondo y los ambientes sedimentarios, que son controlados a su vez en gran medida por la contracorriente subsuperficial. Aunque la variación batimétrica del macro- y meiobentos ha sido estudiada anteriormente, los cambios latitudinales han recibido menos atención. En este trabajo describimos que, en paralelo con gradientes latitudinales opuestos de oxígeno y sedimentación de materia orgánica fresca, existe una secuencia latitudinal en la distribución de la biomasa, diversidad y densidad de la macrofauna, parecida a la respuesta macrobentónica al enriquecimiento orgánico del modelo de Pearson y Rosenberg. Este patrón latitudinal es complementado por el desarrollo óptimo de las bacterias gigantes Thioploca spp en condiciones más extremas de deficiencia de oxígeno (pero sin anoxia) y de sedimentación orgánica que la macrofauna pueda tolerar. La variabilidad temporal de la ZMO también se refleja en respuestas significativas de las comunidades bentónicas, aunque con diferencias en signo e intensidad de acuerdo al ambiente sedimentario. En los sedimentos ricos en materia orgánica de la plataforma central de Perú, el régimen variable del oxígeno gatilla diferentes estados del bentos, que involucran tanto los componentes de la macrobiota (infauna y Thioploca) como de la meiofauna.

Palabras Claves: OMZ, Perú, bentos, Thioploca, modelo de Pearson y Rosenberg.


INTRODUCTION

The upper Peruvian continental margin (50_600 m depth) is intersected by an intense oxygen minimum zone (OMZ; O2 <0.5 ml L-1) that results from large scale circulation patterns and the high regional primary productivity in near-surface waters. The OMZ undergoes significant interannual variability driven by the ENSO cycle and its upper boundary may deepen to 250 m during very strong EN events (Sánchez et al. 2000, Arntz et al. 1991, 2006). Oxygen deficiency plays a major role on the community structure and dynamics in the continental shelf and upper slope, resulting in a strong bathymetric zonation of the benthic communities (Rosenberg et al. 1983, Levin et al. 2002, Arntz et al. 2006). Within the core of the OMZ the metazoan fauna is scarce and bioturbation is weak, enabling the preservation of sediment paleo-records. However, the steep morphology of the upper continental margin and the erosive influence of the Perú-Chile poleward undercurrent limit the presence of laminated sediments. In this work we will shortly review some key features of the OMZ off Peru and its effect on benthic communities (especially macrobenthos), taking into account the influence of the sedimentary environments. We also present and discuss some new findings on the latitudinal and temporal variability of the benthic communities in relation to gradients of oxygen and organic matter.

Background

The oxygen minimum zone off Peru. Compared with other OMZs, the OMZ associated with the Humboldt Current System (HCS) off Peru is more intense and shallow. The OMZ gets wider, is thickened and gains in intensity from the Northern to the Central Peruvian coast (Wooster & Gilmartin 1961, Codispoti & Packard 1980), since organic matter oxidation rates tend to surpass the oxygen advection rates associated with the poleward undercurrent and upwelling (Richmann & Smith 1981). Off 5° S the OMZ upper boundary is usually located beneath 150m depth, while off Callao (12º S), the upper boundary may reach up to 30-40m below the sea surface (Wooster & Gilmartin 1961, Zuta & Guillén 1970). During non EN years, the core of the OMZ (<0.2 mL L-1) reaches its maximum thickness (~100 to ~350 m) and extension (~300 _ 400 km) at 10 _ 16ºS (central Peru). The lower boundary of the OMZ is located around 600m on average, tending to be shallower poleward (Zuta & Guillén 1970, Helly & Levin 2004). In parallel with OMZ intensification and growth, increasing levels of nitrite are recorded in subsurface waters, reaching maximum concentrations when oxygen contents are <0.2 mL L-1 (Richmann & Smith 1981, Codispoti & Packard 1980). Among the main boundary current systems, the HCS is the one that is most subjected to interannual variability, due to ENSO and its warm and cold phases, El Niño (EN) and La Niña, respectively (Brainard & McLain 1987, Carr 2002). Disturbances in the pressure field of the Equatorial Pacific, which are associated with the weakening of reversal of trade winds, trigger the propagation of Kelvin waves to the eastern Pacific. Kelvin waves are tracked by an increase in sea level and deepening of the thermocline, oxycline and nutricline. Total primary production decreases during EN, because the upwelling, if still active, ceases to transport nutrient-rich waters to the surface (Barber & Chavez 1983). The southern branch of the Cromwell Undercurrent that supplies more oxygenated waters off Northern Peru (Wooster & Cromwell 1958) becomes more intense, reaching the Central Peruvian coast during the strongest El Niños. The decrease of primary production, the deepening of the thermocline and the transient enhancement of the undercurrent contribute to the deepening of the OMZ during EN, down to 200 and to 250 m in 1982/83 and in 1997/98, respectively (Guillén et al. 1985, Sánchez et al. 2000).

Sedimentary environments. The spatial distribution of sediment type and organic content on the continental shelf displays variability at several scales. Fine sediments and organic carbon content tend to increase from north to south. There are also observed several nuclei of high surface organic carbon content below upwelling centers in wide shelf areas (Delgado & Gomero 1988). Off central and southern Peru, coastal and shelf sediments are intensely reduced and microbial oxidation of organic matter is dominated by sulphate reduction (Rowe & Howarth 1985, Suits & Arthur 2000). Off the central coast (09-15° S), 210Pb-sedimentation rates vary from 0.05 cm y-1 y to >0.2 cm y-1 on the continental shelf, and from 0.04 to 0.15 cm y-1 on the continental slope (Reimers & Suess, 1983, Henrichs & Farrington 1984, Levin et al. 2002). Sediments of the Peru slope are highly heterogeneous; authigenic precipitation of phosphorites, erosive processes and lateral transport are dominant processes superceding effects of depth or bottom water oxygenation on sediment properties (Levin et al. 2002). According to Reinhardt et al. (2003), the poleward undercurrent largely determines the distribution of the sediments. Off the central coast, the combination of high productivity, near-anoxic conditions over the bottom and low dilution by terrigenous sediments result in the preservation of the upwelling signal in laminated sediments by geochemical and paleo-biological indicators, provided proper topographic conditions (Krissek & Scheidegger 1983, Suess et al. 1990). Upper-slope mud lenses with laminated sediments have been observed off Huacho and Callao (11-12ºS) (Reinhardt et al. 2003) and off Bahía Independencia (14ºS) (Gutiérrez et al. 2006a).

Benthic communities. Most studies on Peruvian benthic communities across the OMZ have been focused on bathymetric variability, e.g., those by Frankenberg & Menzies (1968), Rowe (1971), Rosenberg et al. (1983) and the most recent one by Levin et al. (2002). Clearly the OMZ setting imposes strong bathymetric zonation on benthic communities. According to Arntz et al. (2006), the oxygen ecotones off the Peruvian coast can be classified into three zones beneath the oxygen-saturated `coastal strip' (0-10 m). These zones are: i) an intermediate zone (10 -50 m) that experiences temporal or event hypoxia and even anoxia, depending on latitude and coastal topography (Gutiérrez et al. 2006b); ii) the OMZ itself, where macrofaunal biomass is scarce, only some polychaete species survive and Thioploca mats can attain their maximum biomass. Also, Nematoda and foraminifers are abundant in this region; and iii) a zone below the OMZ, where as oxygen gradually increases, macrofaunal biomass and bioturbation increases as well, attaining large biomasses and higher diversity (Rowe 1971, Neira et al. 1971a, Levin et al. 2002).


MATERIALS AND METHODS

We employed a database of 1330 stations from 27 research cruises from 1976 to 2005, covering a study zone from 03º20' to 10º00' S and from 30 to 500 m depth (Fig. 1). For all the cruises the macrobenthic organisms were classified, counted and weighed. Biomass and abundance measurements were log-transformed for analyses. Covariance analyses were used to test for spatial changes of both biotic and biotic factors under varying latitude and depth. In addition, we analyzed a monthly benthic time-series (macrofauna, meiofauna and Thioploca biomass -sheaths and trichomes-) at 12º off Callao, central Peru, since 1994.




Figure 1. Map of benthic stations surveyed from 1976 to 2005.

 

RESULTS AND DISCUSSION

Our historical database illustrates the degree of latitudinal and temporal variability of abiotic factors and community parameters along the Peruvian coastline. Figure 2 shows the bathymetric variation of dissolved oxygen near the bottom at different latitudinal ranges, during EN and non EN years. At a given depth over the upper continental margin, the oxygen content near the bottom decreases with latitude from the northern to the central coast, and this pattern is opposed by an increasing load of fresh organic matter in the surface sediments (Fig. 3a).




Figure 2. Bathymetric variation of dissolved oxygen near the bottom, a) during non El Niño cruises; and b) during El Niño cruises, from the historical database of IMARPE. Each plot point represents an average from many stations and several cruises at a given latitude range and bathymetric range (26-50, 51-75, 76-100, 101-125, 126-150, 150-175, 176-200, 201-250, 251-300, 301-400, 401-500 and 501-750 m).

In turn, these patterns are translated into a latitudinal variation of the sublittoral and upper bathyal macrobenthic communities as well, that resembles the Pearson & Rosenberg (1978) model of benthic succession under organic enrichment. During non El Niño years, at a given depth, the macrofaunal species richness tend to peak at 5-6ºS, while the macrofaunal biomass peaks at 6-7ºS and the macrofaunal abundance at 7-8ºS (Fig. 3b), and all the parameters decrease southward after their respective peaks. The phyletic composition also decreases along the same latitudinal range, towards higher polychaete dominance (Quipúzcoa et al., submitted). The species composition south of 6ºS is dominated by the interface-feeder spionid polychaete Paraprionospio pinnata. The Pearson & Rosenberg model (1978) has been proven valid in other natural environments as the Equatorial Pacific OMZ (Levin et al. 1991), where, as in the HCS case, opposed gradients of oxygen and organic matter occur. However, a particularity of the sublittoral and upper bathyal macrobenthos subjected to the OMZ off the Perú-Chile coast is the presence of the giant sulphur nitrate-vacuolated bacteria Thioploca spp. (Gallardo 1977, Zafra et al. 1988). These bacteria mats tend to attain their highest biomass (e.g., more developed mats in the sediment surface) at lower oxygen and higher organic loads than the macrofauna, which is expressed in a biomass peak at 8-9ºS (Fig. 3b). Further south, the Thioploca biomass tends to decrease with an increasingly anoxic environment, which is consistent with known Thioploca fitness in suboxic sedimentary environments (Huettel et al. 1996, Jørgensen & Gallardo 1999).




Figure 3. Retrospective analyses of latitudinal patterns based on benthic and oceanographic surveys from 1976 to 2005. a) ANCOVA of dissolved oxygen and sedimentary chlorophyll-a among 1-degree latitudinal areas, with depth as covariable (mean depth: 160 m); b) ANCOVA of macrofaunal density, biomass and species richness, and of Thioploca biomass (trichomes + sheaths), with depth as covariable (mean depth: 147 m). Error bars are 95% confidence limits.


During El Niño, the bathymetric `intermediate zone' is transiently oxygenated and thickened down to 250 m (Arntz et al. 2006; see also Fig. 2). However, the benthic response varies with latitude and according to the local topographic conditions. In food-limited areas, such as sandy sediments where erosive processes are predominant, macrofaunal biomass tend to decrease during EN, probably due to a reduction of the flux of fresh organic matter from the near-surface waters (Gutiérrez et al. 2006b). In other areas, such as the organic-rich shelf sediments off Callao (12ºS), macrofaunal biomass, diversity and bioturbation potential may augment significantly during strong ENs (Gutiérrez et al. 2002).

Recently we analyzed the temporal variation of the benthic shelf communities off Callao (Gutiérrez et al. submitted). The benthic time-series exhibited an interannual variability triggered by changes in the subsurface oxygen regime. Three distinct benthic states could be characterized according to changes in the macrobiotic biomass: i) macrofaunal dominance, such as during the oxygenated 1997-98 EN; ii) Thioploca dominance, such as during the weakly oxygenated 2002-2003 period; iii) poor macrobiotic biomass, explained by both defaunation and nearly absence of Thioploca, such as during the strongly oxygen deficient periods 1998_2000 and 2004-2005. It appears that these states are also recognizable in terms of the meiofaunal community, which exhibited a higher phyletic diversity, lower nematode dominance and lower overall density in the Thioploca-dominated state, and viceversa under the poor macrobiotic biomass period (Fig. 4). These observations question the sulfide detoxifying activity of Thioploca as a driving role for the macrofaunal or meiofaunal biomass (Neira et al. 2001b, Arntz et al. 2006) since macrofaunal biomass is still scarce during the Thioploca period and the parallel higher phyletic diversity of meiofauna and biomass of Thioploca during 2002-2003 could also be attributed to the less hypoxic conditions that favour both the development of the bacterial mats and the development of meiofaunal populations that are less tolerant to anoxia.





Figure 4. Major phyletic meiofaunal composition (percent abundance) at 94m depth, 12ºS (Callao), during the warmer and more oxygenated period 2002-2003 (O2: 0.1-0.6 mL L-1), and during the cooler and strongly hypoxic period 2004-2005 (O2: 0.0-3 mL L-1). Percent of Nematoda is not shown but is the difference at each case.


ACKNOWLEDGEMENTS

The authors acknowledge the valuable comments of Dr. David Field that improved this manuscript . This study was funded by the IMARPE research project Interacción de la Zona de Mínima de Oxígeno con la Sedimentación de Carbono Orgánico y Procesos bentónicos. We deeply acknowledge the contribution of researchers and colleagues as W. Arntz and H. Salzwedel (German-Peruvian project PROCOPA), L.A. Flores, E. Chuman de Flores, A. Zafra and R. Marquina (IMARPE), among many others, who pioneered in some cases or still contribute with the Peruvian OMZ benthic studies. This study was supported by the IMARPE-IRD cooperation and the ATI project "Humboldt Current System", and by the EU-project CENSOR (Climate variability and El Niño Southern Oscillation).


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