Canyon conditions impact carbon flows in food webs of three sections of the Nazaré canyon
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- 4.1 Upper canyon section
- 4.2 Middle canyon section
- 4.3 Lower canyon section
- 4.4 Comparison of canyon sections with network indices
DiscussionIn this paper, we present the first quantitative analysis of carbon flows within food webs of different sections of a submarine canyon. This provides a unique opportunity to study how different characteristics within a canyon influence food web structure and attributes such as total system throughput, recycling within the food web and food web maturity. The modeled food webs of the upper, mid and lower canyon sections are based on a large variety of site-specific biological and biogeochemical data and are combined with physiological constraints and empirical relations from the literature. Despite the large amount of data that are implemented, this is insufficient to uniquely quantify all carbon flows (Van Oevelen et al., 2010). This implies that a “solution space” exists, within which an infinite number of solutions are present that are consistent with the data (Soetaert and Van Oevelen, 2009). Conventional single-solution modeling approaches typically find a final solution at or close to boundaries of the solution space, making the final solution sensitive to the exact boundaries of the solution space ( Vézina et al., 2004; Kones et al., 2006; Van Oevelen et al., 2010). The multi-solution approach followed here, samples the solution space (Van den Meersche et al., 2009) such that the mean of this sampled set represents the best central flow value that is less sensitive to the boundaries of the solution space (Van Oevelen et al., 2010). Moreover, the standard deviation on each carbon flow indicates how the uncertainty in the data set propagates to an uncertainty on its value (Van Oevelen et al., 2010). The Coefficient of Variation (CoV) was smaller than 0.75 for 73 – 82% flows in the three sections (Web appendix), which indicates that the residual uncertainty on the flows is comparatively low and that the food web is well-constrained. The lowest CoVs are associated with the respiration flows of the biotic compartments, whereas highest CoVs are predominantly associated with carbon flows that exist between biotic compartments. This directly relates to the data availability. The carbon requirement of faunal compartments is constrained primarily by the available biomass data. There are however few data that constrain the origin of this carbon, such that the residual uncertainty on diet contributions and fates of secondary production are comparatively high. Perhaps even more important than the residual uncertainty on the flows, are the limitations and uncertainties with respect to the assumptions that were needed to setup the model. These sources of uncertainty mainly concern substrate heterogeneity and combining different data sets and will be discussed now. The seafloor in the Nazaré canyon is heterogeneous and consists of rocks, boulders, coarse gravel sediments, steep walls, a highly dynamic thalweg and terraces consisting of soft-sediments. The hard substrata may be draped with a thin soft muddy layer. Not surprisingly, also the associated fauna changes with substratum type and condition. Rocky surfaces for example are dominated by suspension feeders such as hard and soft corals, gorgonians, anemones, sea pens and crinoids (Tyler et al., 2009). In thalweg sediments, the biomass of nematodes (Garcia et al., 2007) is about one order of magnitude lower than in soft-sediment terraces (Ingels et al., 2009), which is attributed to repeated sediment disturbance of thalweg sediments that prevents the development of a mature nematode community (Garcia et al., 2007). In addition, megafauna and the giant epifaunal protozoans (xenophyophores) were not observed in the thalweg (Tyler et al., 2009) but are found outside the thalweg. Up to now, there are no quantitative data available on the biomass and activity of the filter-feeding community in the Nazaré canyon on rocky substrata. Moreover, quantitative data on the faunal community in the thalweg is only sparsely available and its food web structure is not representative for that of large sections of the canyon. Hence, in this study we restricted our analysis to the soft-sediments of the terraces adjacent to the thalweg and excluded other substrate types. This implies for example that we may miss the potentially high carbon processing activity associated with the canyon walls. In terms of areal coverage however, these soft-sediments with net mud deposition represent an appreciable ~70% of the total surface area of the canyon (Masson et al., 2010), such that a significantly large part of the Nazaré canyon is addressed here. One compartment that is not included in the food web is Foraminifera, which are protozoans that are typically of meiofaunal size but can occur as giant epifauna (xenophyophores). Meiofaunal foraminifera (Koho et al., 2008) and epifaunal xenophyophores (Tyler et al., 2009) have a high abundance in especially the muddy terraces with stable redox conditions and low disturbance. Foraminifera have been shown to play an important role in the initial processing of fresh phytodetritus under deep-sea conditions (Moodley et al., 2002) although their contribution may also be more limited (Woulds et al., 2007). Moreover, their contribution to total respiration in continental shelf sediments was recently found to be limited to <3% (Geslin et al., 2010). Unfortunately, the available abundance data could not be converted to biomass with reasonable accuracy, and since biomass is essential to constrain their activity in the food web we therefore decided to omit this compartment in this analysis. The site-specific data that we include in this study were lumped into the three canyon sections (Table 1 and 2). However, since deep-sea research is time consuming, conducted over large spatial areas and depends on ship time availability and meteorological/sea conditions, the data were not collected synoptically. Inevitably, this data ‘lumping’ into canyon sections will introduce errors in the food web analysis linked to the spatial and temporal variability of the data collected. Nevertheless, the Nazaré canyon is comparatively well-studied and one of the strengths of linear inverse modeling is that datasets are merged and tested for internal consistency (Van Oevelen et al., 2010). Given the amount of data in the models (Table 1 and 2), the inverse model analysis at least showed that the different data sets are consistent. The only exception was that the minimum degradation rate of semi-labile detritus in the lower canyon section was higher than the maximum rates of carbon oxidation and total carbon deposition. The carbon oxidation and deposition data are site-specific data and were therefore maintained. Instead, the minimum bound on semi-labile degradation was reduced by multiplication with the temperature limitation factor, which allowed solving the food web model. Several explanations may apply here. First, water temperature in the deep canyon section is about 2.5°C and lowest of the three sections. This low temperature may cause degradation to proceed slower than in the higher sections of the canyon with comparatively higher water temperatures. Moreover, the quality of the semi-labile detritus may have decreased during transport through the canyon and this may also lower the degradation rates further. Despite this minor adaptation that was needed, the results from the present analysis serve as a significant first step in gaining insight in the food web structure of submarine canyons. 4.1 Upper canyon sectionThe dynamic upper canyon receives about 8±0.84 mmol C m-2 d-1, which is lower than the 15 – 23 mmol C m-2 d-1 that is predicted using an empirical relation for continental shelf sediments (i.e. summed burial and mineralization rates at 700 and 300 m, respectively, Middelburg et al., 1997). However, carbon inputs at the open slope sediments of the adjacent Iberian margin are substantially lower than predicted by the empirical relation by Middelburg et al. (1997) and are between 2.3 and 4.3 mmol C m-2 d-1 (Epping et al., 2002). Thus, carbon inputs to the upper canyon section is higher those of adjacent slopes, but not extremely high as compared to other slope sediments. Burial rates in the upper and middle canyon are substantial flows in the food web (Fig. 1A, B), but burial efficiencies are comparable to Iberian open slopes and relate to sediment accumulations rates (Epping et al., 2002). Hence, the efficiency with which the food web processes organic carbon is similar to open slope sediments. The model results allow detailed deciphering of the biotic compartments that are responsible for carbon processing within the canyon. Woulds et al. (2009) used the results of isotope tracer experiments from different slope sediments to define different categories of biological C-processing. In this categorization, the “active-faunal-uptake” category contains mostly shallow (<300 m) slope sediments and is characterized by 10 – 25% metazoan uptake. This category matches best with the upper canyon section that has a faunal contribution of ~40% and bacterial contribution of 60% to total carbon assimilation. The faunal contribution to total respiration and carbon processing typically decreases with increasing water depth and associated decrease in carbon input (Heip et al., 2001; Rowe et al., 2008; Woulds et al., 2009). Henceforth, the high faunal contribution in the upper canyon section is probably related to the higher OM content and quality as compared to slope sediments at comparable water depth (Garcia et al., 2007; Garcia and Thomsen, 2008; Pusceddu et al., 2010). One striking difference however is that meiofauna dominated faunal processing and contributed around 33% of the total carbon assimilation in the upper canyon section, which is much higher than in open slopes sediments included in the overview of Woulds et al. (2009). This high contribution also translates into a much higher meiofaunal respiration at 21% of total respiration in the upper section of the Nazaré canyon as compared to other open slopes that vary from 4 – 8% (Piepenburg et al., 1995; Heip et al., 2001; Soetaert et al., 2009). Rowe et al. (2008) and Bagulay et al. (2008) report even substantially higher contributions ranging from ~20 up to 51% for the Northern Gulf of Mexico. Their estimates are based on biomass-specific respiration rates of 0.04 to 0.11 d-1 at a temperature of 4 – 5°C. Moodley et al. (2008) used a novel micro-respiration system and reported specific rates of 0.021 to 0.032 d-1 for intertidal (20°C) Nematoda, Ostracoda and Foraminifera over a biomass range of 0.7 to 5.2 μC ind-1. Nematodes from the Gulf of Mexico are smaller (~0.1μC ind-1, Baguley et al., 2008), but specific respiration rates are still fairly high as compared to these intertidal meiofauna. The high meiofaunal contribution to total community respiration is therefore probably also related to the comparatively high biomass-specific respiration rates that are estimated for the Gulf of Mexico. Clearly more experimental work for especially small nematodes at lower temperatures is needed to better constrain these respiration rates. The carbon sources that are consumed by meiofauna to fuel these respiration rates are detritus and prokaryotes (e.g., Rowe et al., 2008, this study). Stable isotope tracer experiments allow direct quantification of labile food assimilation rates of amongst others meiofauna. Intriguingly, these results typically show low biomass-specific assimilation rates of <0.01 and mostly <0.001 d-1 ( Moens et al., 2007; Franco et al., 2008; Ingels et al., 2011;), a limited (<5%) contribution to 13C uptake by metazoan meiofauna on open slope (Moodley et al., 2002) and abyssal plain (Witte et al., 2003) sediments and negligible bacterivory by nematodes in a slope sediment (Guilini et al., 2010). Irrespective of the labeled substrate or setting, meiofauna consistently show an uptake of labile 13C carbon that seems to be in imbalance with carbon requirements as estimated from biomass-specific respiration rates. This is not in contrast with the meiofaunal diet composition as inferred for the Nazaré canyon (Fig. 2), where semi-labile detritus (a carbon source not used in isotope tracer studies) is the dominant component. This dominance of semi-labile detritus in their diet would explain the low labeling of metazoan meiofauna (dominated by nematodes) in isotope tracer studies. It also agrees with Soetaert et al. (1997), who found a strong positive correlation between depth profiles of nematodes and organic N content and suggested that the concentration of lower quality food primarily determines nematode depth distribution. The elevated OM input in the upper canyon section combined with hydrodynamic conditions with current speeds of up to 30 – 40 cm s-1 appear to particularly favor meiofauna, whereas macro- and megafauna have a lower contribution to carbon processing as compared to open slope sediments. As a result, meiofaunal biomass in the upper canyon section rank among the highest reported in marine sediments (Rex et al., 2006), whereas macrofaunal biomass is comparatively low. Prokaryotes are responsible for the dominant part of carbon cycling and respiration in the upper canyon section (Fig. 1 and Table 5). An important pathway, also seen in the middle and lower canyon section, is deposition of semi-labile detritus, dissolution to dissolved organic carbon, to prokaryotic uptake of this DOC and subsequent prokaryote respiration. A dominance of prokaryotes in carbon cycling and respiration is commonly found in continental shelf sediments (Canfield et al., 1993; Piepenburg et al., 1995; Heip et al., 2001; Rowe et al., 2008). Hence, it appears that hydrodynamic conditions in the upper canyon act predominantly on carbon partitioning between faunal compartments rather than on the partitioning between pro- and eukaryotes.
With respect to the carbon partitioning within the food web, the middle canyon section seems to fall in the “metazoan-macrofaunal-uptake-dominated” category, a category that is typically found in shelf and upper slopes, with a comparatively high macrofaunal biomass (Woulds et al., 2009). An importanct discrepancy with the categorization by Woulds et al. is that faunal carbon processing in the middle canyon is not dominated by macrofauna, but by surface deposit-feeding and deposit-feeding megafauna (i.e. the holothurians Ypsilothuria bitentaculata and Molpadia musculus, respectively). The megafaunal importance is also apparent in community respiration (57%) and export of secondary production from the food web (79%). De Leo et al. (2010) reported recently for the Kaikoura Canyon (New Zealand) an extremely high biomass of 89±18 g C m-2 of megafauna (dominated by M. musculus) in low relief, muddy and accreting sediments at 900 – 1100 m of water depth. Megafaunal biomass in the middle section of the Nazaré canyon is about an order of magnitude lower (6.2 g C m-2), but still 2 – 3 orders of magnitude higher than found in open slopes at comparable depth (Rex et al., 2006). Amaro et al. (2010) conducted trophic studies on the holothurian M. musculus and estimated removal rates of 0.5 gC of semi-labile detritus m-2 d-1. Our food web analysis even suggests higher removal rates of 2.5 gC of semi-labile detritus m-2 d-1, showing that this holothurian can have an important impact on the sedimentary food web. Amaro et al. (2010) also inferred that prokaryotes delivered <0.1% of the assimilated proteins and it was concluded that holothurians do not appear to rely on microbes for direct nutrition. This is also supported by our diet reconstruction of deposit-feeding megafauna (i.e., M. musculus), where prokaryotes play only a marginal role (Fig. 2B). Carbon partitioning with the food web of the middle canyon section at 2700 – 4000 m is comparable to much shallower shelf and upper-slope sediments, where also an important faunal contribution is typically found. The large faunal contribution in the middle canyon section is due to the comparatively high input of OM, which is quantitatively comparable to the upper canyon section. It is however unclear why canyon-specific conditions in the middle section are particularly beneficial for (surface) deposit-feeding holothurians as compared to for example macrofaunal polychaetes. The deposit-feeding megafauna consist predominantly of the holothurian head-down feeder M. musculus and there was no evidence for a specialized prokaryotic community in the guts of M. musculus that may aid in the hydrolyzation of organic matter (Amaro et al., 2009). Other possible explanations for a strong proliferation of M. musculus in soft accreting sediments within canyons may involve a better adaptation to high sediment rates, enhanced trapping of the depositing organic matter in their feeding pits and negative feedbacks on macrofauna through, for example, predation or sediment disturbance.
Respiration in the lower canyon section is strongly dominated by protozoa (82% of total respiration) whereas the faunal compartments each respire <10%. These characteristics place the lower canyon section in the “respiration-dominated” category, in which most OM is respired by the prokaryotic community and the role of benthic fauna in carbon cycling is low (Woulds et al., 2009). Other sites that fall in this category are lower slope sediments and abyssal plains (Woulds et al., 2009), suggesting that the benthic food of the lower canyon section resembles others sites at similar depth . The lower canyon section seems to be less influenced by canyon conditions as compared to the upper and middle section of the canyon. 4.4 Comparison of canyon sections with network indicesThe lower carbon processing in the lower canyon is also evident in the index total system throughput (  ), in which carbon flows are summed to obtain a measure of total food web activity (Ulanowicz, 2004). Total system throughput does not differ significantly between the upper and middle sections (medians of 41.1 and 39.7 mmol C m-2 d-1, respectively), but is significantly lower in the lower canyon section (median of 6.7 mmol C m-2 d-1) (Table 6). Though community respiration and OM input is higher for the middle canyon section, total system throughput is slightly elevated (not significantly) in the upper canyon section. This reversal in activity measures is probably linked to the low recycling within the food web of the middle canyon as quantified with the Finn cycling index (Fig. 4B). This index summarizes the fraction of total carbon cycling that is generated by recycling processes (Allesina and Ulanowicz, 2004). Significant differences in recycling are found between the canyon sections, with the most notable difference being low recycling in the middle canyon section. One explanation relates to the viral shunt (Danovaro et al., 2008), in which viral infection cause lysis of prokaryotes and the subsequent release of dissolved organic matter that is again recycled by other heterotrophic prokaryotes (e.g., Van Oevelen et al., 2006a). Prokaryotes dominate carbon flows in the lower section, but this dominance is reduced in the upper and particularly the middle canyon section. If the viral-mediated shunt significantly influences the FCI, this would explain the decreasing FCI when going from the lower, upper to the middle canyon section. To examine the impact of the viral shunt on the FCI, the viral shunt was eliminated from the food web by only including the net flow from DOC to prokaryotes in the FCI calculations. Though differences in FCI remain, the FCI of the upper and lower sections drops to medians of 0.07 and 0.04, respectively, whereas the middle section is much less affected with a drop to 0.03. This exercise clearly shows that the viral shunt increases carbon recycling in benthic food webs rendering recycling to be higher in prokaryote-dominated food webs as compared to faunal-dominated food webs.
The index average mutual information (AMI) gauges the developmental status of an ecosystem in the sense that while food webs develop, trophic specialization will result in higher values for AMI (Ulanowicz, 2004). The AMI is that part of the flow diversity (i.e. the Shannon index applied to flow diversity, Ulanowicz, 2004) that quantifies how orderly and coherently carbon flows are inter-connected. Since the AMI is claimed to assess the developmental status of an ecosystems it is interesting to assess whether differences in the food web structures are also reflected in the AMI index. More specifically, we had expected the less-disturbed lower canyon section to have highest AMI values with decreasing values going up-canyon. Differences in AMI between the upper and middle canyon are non-significant (Table 6), though large differences exist in environmental conditions and food web structure. The AMI is significantly lower in the lower canyon section though this section is less impacted by canyon conditions as compared to the other two sections. Tobor-Kaplon et al. (2007) quantified the AMI of soil food webs that were exposed to different stress levels (i.e. pH and copper) and concluded that AMI appeared useful as an indicator of environmental stress at the ecosystem level. For the benthic food webs analyzed here however, there does not seem to be a straightforward relation between AMI and environmental stress. On the other hand, there is another important factor that influences food web structure when going down-canyon, namely the reduced OM input. To verify the usefulness of AMI as a stress indicator it is therefore necessary to compare the AMI of marine benthic food webs at similar levels of OM input, but different levels of environmental stress. In conclusion, benthic food web structures in the upper, middle and lower sections of the Nazaré canyon were shown to be influenced by the conditions in the particular canyon section. The OM input in the upper and middle canyon sections is elevated as compared to those of the surrounding open slope sediments and this resulted in a higher contribution of fauna in carbon processing as compared to open slope sites at similar water depth. The compartments that were responsible for the faunal processing were strongly influenced by conditions in the particular canyon section. In the upper canyon section, a dominance of meiofauna in faunal carbon processing was evident, whereas a high faunal contribution to carbon processing in open slope sediments is typically dominated by macrofauna. It is proposed that hydrodynamic disturbance and resulting sediment resuspension in the upper canyon shifts the balance towards the meiofauna. In contrast, the food web of the accreting sediments in the middle canyon showed a completely different pattern where carbon processing was dominated by the megafaunal holothurians. Our study confirms that accreting sediments in canyons can be hotspots of megafaunal biomass and production and megafauna can greatly influence carbon processing. The food web structure of the lower canyon section resembled that of lower slope and abyssal plain sediment, where carbon processing is dominated by prokaryotes. The influence of the canyon-specific processes seems to vanish in the deeper sections where the Nazaré canyon widens and enters the abyssal plain. In all canyon sections, a dominance of semi-labile detritus in the diet of (surface) deposit feeders is suggested. These results are supported by stable isotope tracer (for meiofauna) and gut transformation (holothurian M. musculus) studies. This study shows that elevated OM input in canyons may favor the faunal contribution to carbon processing and creating hotspots of faunal biomass and carbon processing along the continental shelf.
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