Canyon conditions impact carbon flows in food webs of three sections of the Nazaré canyon

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Canyon conditions impact carbon flows in food webs of three sections of the Nazaré canyon

Dick van Oevelen1,*, Karline Soetaert1, Rosa García Novoa2,3, Henko de Stigter4, Marina da Cunha5, Antonio Pusceddu6, Roberto Danovaro6

1 Centre for Estuarine and Marine Ecology, Netherlands Institute of Ecology (NIOO-KNAW), POB 140, 4400 AC Yerseke, The Netherlands

2 Jacobs University Bremen, Campus Ring 1, 28759 Bremen, Germany

3 Department of Global Change Research, IMEDEA (CSIC-UIB) Instituto Mediterráneo de Estudios Avanzados, Miquel Marqués 21, 07190 Esporles, Spain

4 Royal Netherlands Institute for Sea Research (NIOZ), POB 59, 1790 AB Den Burg - Texel, The Netherlands

5 Centro de Estudos do Ambiente e do Mar (CESAM) & Departamento de Biologia, Universidade de Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal

6 Department of Marine Science, Polytechnic University of Marche, Via Brecce Bianche, 60131 Ancona, Italy

* corresponding author:


Submarine canyons directly transport large amounts of sediment and organic matter (OM) from the continental shelf to the abyssal plain. Three carbon-based food web models were constructed for the upper (300 – 750 m water depth), middle (2700 – 3500 m) and lower section (4000 – 5000 m) of the Nazaré canyon (eastern Atlantic Ocean) using linear inverse modeling to examine how the food web is influenced by the characteristics of the respective canyon section. The models were based on an empirical dataset consisting of biomass and carbon processing data, and general physiological data constraints from the literature. Environmental conditions, most notably organic matter (OM) input and hydrodynamic activity, differed between the canyon sections and strongly affected the benthic food web structure. Despite the large difference in depth, the OM inputs into the food webs of the upper and middle sections were of similar magnitude (7.98±0.84 and 9.30±0.71 mmol C m-2 d-1, respectively). OM input to the lower section was however almost 6-7 times lower (1.26±0.03 mmol C m-2 d-1). Canyon conditions greatly influenced OM processing within the food web. Carbon processing in the upper section was dominated by prokaryotes (70% of total respiration), though there was a significant meiofaunal (21%) and smaller macrofaunal (9%) contribution. The high total faunal contribution to carbon processing resembles that found in shallower continental shelves and upper slopes, although the meiofaunal contribution is surprisingly high and suggest that high current speeds and sediment resuspension in the upper canyon favor the role of the meiofauna. The high OC input and conditions in the accreting sediments of the middle canyon section were more beneficial for megafauna (holothurians), than for the other food web compartments. The high megafaunal biomass (516 mmol C m-2), their large contribution to respiration (56% of total respiration) and secondary production (0.08 mmol C m-2 d-1) shows that these accreting sediments in canyons are megafaunal hotspots in the deep-sea. Conversely, carbon cycling in the lower canyon section was strongly dominated by prokaryotes (86% of respiration) and the food web structure therefore resembled that of lower slope and abyssal plain sediments. This study shows that elevated OM input in canyons may favor the faunal contribution to carbon processing and create hotspots of faunal biomass and carbon processing along the continental shelf.


Submarine canyons are incisions of the continental margin and directly link the continental shelf with deep-sea plains by transporting large amounts of sediment (Canals et al., 2006; de Stigter et al., 2007) and OM (Epping et al., 2002; Vetter and Dayton, 1999). The comparatively rapid transport in active canyons results in the sedimentary OM being also of higher quality as compared to slope sediments at similar water depth (Garcia et al., 2007; Pusceddu et al., 2010; Vetter and Dayton, 1999). The high quantity and quality of the OM in canyon sediments results in carbon oxidation rates (Epping et al., 2002; Rabouille et al., 2009) and benthic standing stocks of nematodes (Ingels et al., 2009) and deposit feeding holothurians (Amaro et al., 2009; De Leo et al., 2010; Vetter and Dayton, 1999) that are higher as compared to adjacent open slopes and indicate extensive carbon cycling in the benthic food web.

These latter studies focus on individual components of the benthic food web and suggest that different benthic components may benefit from the enhanced influx of OM into canyons. These comparisons are, however, based on single biomass-to-biomass or process-by-process comparisons. It is unclear how the structure of the whole food web and carbon partitioning within the food web is affected by canyon conditions. Moreover, it is unclear whether and how emerging properties at the whole food web level are impacted by canyon conditions. Network analysis has been developed to condense information contained in complex networks, such as food webs, into interpretable indices (Fath and Patten, 1999; Ulanowicz, 2004). The index total system throughput () sums carbon flows in the food web to obtain a measure of total food web activity. The Finn cycling index summarizes the fraction of total carbon cycling that is generated by recycling processes (Allesina and Ulanowicz, 2004). Another index that is claimed to be related to food web maturity is average mutual information (AMI), that gauges how orderly and coherently flows are inter-connected (Ulanowicz, 2004 and references therein). It is claimed that AMI is indicative of the developmental status of an ecosystem and that while a food web develops specialization results in higher values of AMI.

The Nazaré canyon intersects the Portuguese continental shelf and extends from a water depth of 50 m near the coast down to 5000 m at the abyssal plain and presents an interesting case study because of the varying conditions within the canyon. The upper canyon section (50 – 2700 m water depth) is characterized by a V-shaped valley that is deeply incised in the continental shelf. The middle canyon (2700 – 4000 m) is a broad meandering valley with terraced slopes that may experience high rates of particle and organic matter sedimentation (Masson et al., this issue). The upper and middle canyon sections capture suspended particulate matter from the adjacent shelf and are affected by internal tide circulation of water with high bottom current speeds, thereby imposing physical disturbance on the sedimentary environment (de Stigter et al., 2007). Finally, the lower canyon is a kilometers-wide flat-floored valley that gently descends from 4000 to 5000 m depth (de Stigter et al., 2007; Masson et al., this issue).

The physical disturbance of sediments is especially strong in the narrow V-shaped valley of the upper canyon section and this may impose constraints on the development of the food web. Especially large and longer-lived components of the food web may be affected and carbon cycling may be shifted towards microbes as compared to sediments with similar OM input that are less frequently disturbed (Aller and Aller, 2004). Carbon recycling, quantified with the Finn cycling index, may therefore be lower because fewer food web components give rise to more limited recycling in the food web. Also food web maturity, as measured with the network index AMI, is expected to be lower as compared to the middle and lower canyon sections.

The terraced slopes of the middle canyon section experience high rates of sedimentation and associated organic matter input. Transport of (semi)-labile OM to these greater depths in the canyon may imply a deviation from the archetypical relation between water depth and sediment oxygen consumption (SOC). The SOC and the network index “total system throughput” is expected to be comparatively elevated in the middle section of the canyon due to the enhanced OM input as compared to open slope sediments at similar water depth. The enhanced input OM may not be partitioned equally among the food web compartments and may be influenced by the environmental conditions in the respective canyon. De Leo et al. (2010) for example, reported extremely high biomass levels of particularly deposit-feeding holothurians in a low relief muddy sediment at 900 – 1100 m in the Kaikoura Canyon (New Zealand). The conditions in the Kaikoura canyon are reported to be similar to the middle section of the Nazaré canyon and indeed high holothurian abundances are found there too (Amaro et al., 2009). With a whole food web approach as followed here it will be possible to study quantitatively whether different food web compartments take proportional advantage of the enhanced OM input in this section of the Nazaré canyon.

The deeper canyon section is where the canyon widens into a kilometres-broad channel in the abyssal plain (de Stigter et al., 2007). This deep canyon section, which only intermittently receives material derived from up-canyon sections via sediment gravity flows, better resembles regular abyssal plain conditions with an associated lower OM input. Under these lower OM inputs, lower faunal contributions to carbon cycling are expected and the more steady conditions may imply a higher food web maturity and higher recycling within the food web.

Verifying how specific conditions in the three canyon sections impose on the benthic food web requires an analysis of the trophic structure of the complete benthic food web. The quantification of complete food webs is however a data-demanding effort and canyon data sets are typically incomplete and limited in scope. To overcome these limitations and maximize the amount of information gained from the available data, so-called linear inverse models (LIM) have been developed. LIM allow quantifying biological interactions in a complex food web from an incomplete and uncertain data set such as encountered in the deep-sea (Soetaert and Van Oevelen, 2009). For example, Van Oevelen et al. (2009) using linear inverse modeling to quantify the interactions in the complex food web of a cold-water coral community at Rockall Bank and provided evidence that coral communities are hot-spots of biomass and carbon cycling along continental margins.

Here we develop linear inverse models (LIM) to quantify carbon flows in the complex food webs characterizing upper, middle and lower sections of the Nazaré canyon. The observed food web structures and selected network indices are examined as a function of the characteristics of the respective canyon section.

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